close

Вход

Забыли?

вход по аккаунту

?

Interlobular excretory ducts of mammalian salivary glandsStructural and histochemical review.

код для вставкиСкачать
THE ANATOMICAL RECORD PART A 288A:498 –526 (2006)
Interlobular Excretory Ducts of
Mammalian Salivary Glands:
Structural and Histochemical Review
BERNARD TANDLER,1* CARLIN A. PINKSTAFF,2 AND
CARLETON J. PHILLIPS3
1
Department of Biological Sciences, School of Dental Medicine, Case Western
Reserve University, Cleveland, Ohio
2
Department of Anatomy, West Virginia University, Morgantown, West Virginia
3
Department of Biological Sciences, Texas Tech University, Lubbock, Texas
ABSTRACT
In the major salivary glands of mammals, excretory ducts (EDs) succeed
striated ducts. They are for the most part interlobular in position, although
their proximal portions sometimes are on the periphery of a lobule, where they
occasionally retain some of the structural features of striated ducts. Based on
a survey of a broad range of mammalian species and glands, the predominant
tissue type that composes EDs is pseudostratified epithelium. In some species,
there is a progression of epithelial types: the proximal EDs are composed of
simple cuboidal or columnar epithelium that, in the excurrent direction, usually gives way to the pseudostratified variety. Secretory granules are visible in
the apical cytoplasm of the principal cells of the EDs of only a few species, but
histochemistry has shown the presence of a variety of glycoproteins in these
cells in a spectrum of species. Moreover, the latter methodology has revealed
the presence of a variety of oxidative, acid hydrolytic, and transport enzymes in
the EDs, showing that, rather than simply acting as a conduit for saliva, these
ducts play a metabolically active role in gland function. It is difficult to describe
a “typical” mammalian ED because it can vary along its length and interspecific variation does not follow a phylogenetic pattern. Moreover, in contrast to intercalated and striated ducts, ED cellular features do not exhibit
a relationship to diet. Anat Rec Part A 288A:498 –526, 2006.
©
2006 Wiley-Liss, Inc.
Key words: submandibular gland; parotid gland; sublingual
gland; excretory ducts; interlobular ducts; glycoproteins; histochemistry
The present review of interlobular excretory ducts (EDs)
in mammalian salivary glands is the third in a series that
includes reviews of intercalated ducts (Tandler et al.,
1998c) and secretion by striated ducts (Tandler et al.,
2001). Our approach in each has been to summarize the
literature (which sometimes is abundant) on the subject,
present a substantial amount of previously unpublished
comparative information from 250 or more species of
mammals, and use evolutionary, systematic, and ecological information to interpret the comparative data set. In
some instances, it has been possible to posit new, testable
hypotheses about the function of salivary gland ducts
(Phillips, 1996).
Over the past decade, it has become increasingly clear
that salivary glands have played a vital role in mamma©
2006 WILEY-LISS, INC.
lian evolution and adaptive radiation (Phillips, 1996; Phillips and Tandler., 1996). To some extent, this role involves
diet and the ability of particular species to access specific
nutrient resources (Phillips et al., 1998; Tandler and Phil-
*Correspondence to: Bernard Tandler, Department of Biological Sciences, School of Dental Medicine, Case Western Reserve
University, 10900 Euclid Avenue, Cleveland, OH 44106. Fax:
216-368-3204. E-mail: bernard.tandler@case.edu
Received 8 June 2005; Accepted 29 December 2005
DOI 10.1002/ar.a.20319
Published online 12 April 2006 in Wiley InterScience
(www.interscience.wiley.com).
EXCRETORY DUCTS OF SALIVARY GLANDS
Fig. 1. Sublingual: human being (Homo sapiens). Light micrograph of
a paraffin-embedded ED. Note the thick covering of fibrous connective
tissue (CT), a part of an interlobular septum. Masson’s trichrome. Magnification ⫽ 200⫻.
lips, 1998). In a broader context, however, salivary gland
functions encompass a truly remarkable range of actions.
Among these, salivary pheromones are significant because
they can include proteins that enable kin recognition,
affect mate selection (premating reproductive isolation),
and have a fundamental role in speciation (Wickliffe et al.,
2002). With all these factors in mind, the importance of
comparative morphological and ultrastructural data is obvious.
Although some of the information reported here comes
from animals prepared under laboratory conditions (B.T.),
much more originates from specimens collected in the wild
by one of the authors (C.J.P.), field-fixed according to
previously described procedures (Phillips, 1985; Tandler
et al., 1998c) and deposited as vouchers in one of three
established research collections (Natural Science Research Laboratory of the Texas Tech Museum, Division of
Mammals of the Carnegie Museum of Natural History,
and the Nebraska State Museum of the University of
Nebraska-Lincoln). These vouchers serve as a permanent
foundation for species identification and other relevant
information about specimens from which our salivary
gland data were obtained. Species data from the literature
are reported here as provided by the original authors; in a
number of instances, we have only common names (species unknown or unverifiable). Much of the published data
is based on tissue samples for which there are no voucher
specimens. Thus, those workers who use the data collected
here (other than the bulk of those presented in Table 6)
must keep in mind that species identification cannot always be verified.
The excurrent duct system of parotid and submandibular salivary glands consists of intercalated duct (ID), stri-
499
Fig. 2. Parotid: Hart’s little fruit bat (Enchisthenes hartii). Survey
electron micrograph of a transitional duct. Although this duct actually is
situated within an interlobular septum, it is positioned at the edge of a
lobule and superficially still possesses the appearance of a striated duct.
In many species and glands, proximal EDs are structurally indistinguishable from striated ducts. Magnification ⫽ 1600⫻.
ated duct (SD), excretory duct, and main excretory duct
(MED) (Tandler, 1993a); in many species of rodents, a
further duct segment, the granular convoluted tubule
(granular duct), is interposed between intercalated and
striated ducts (Gresik, 1994). In the sublingual gland of
many mammals, the intercalated ducts shade into ducts
that probably are EDs, but which may include patches of
striated cells in their walls (Riva et al., 1988); in certain
species such as the ferret, sublingual secretory endpieces
drain directly into EDs without intervening intercalated
or striated ducts (Jacob and Poddar, 1989). In the cat
sublingual gland, endpieces often are in direct continuity
with the MED (Tandler and Poulsen, 1977), so that this
gland lacks intralobular and interlobular ducts altogether. Most published ultrastructural studies of entire
parotid and submandibular glands include descriptions of
IDs and SDs, but more often than not omit any description
of the intraglandular EDs. In contrast, many detailed
descriptions of the MED have appeared. This morphological neglect of the EDs is surprising because the physiology of these ducts may be of some importance in salivary
homeostasis. In this review, we describe the structure of
EDs in a variety of mammalian species. Despite their
deceptively simple histology in human beings and in common laboratory animals, these ducts show a degree of
variation across the spectrum of mammalian orders.
Although in most mammals, EDs lack distinctive structural features (such as the basal striations of SDs), they
are readily identified in both paraffin sections and in epoxy semithin sections by their extralobular (interlobular)
500
TANDLER ET AL.
Fig. 3. Submandibular: African yellow bat (Scotophilus dingani). An ED that consists of pseudostratified
epithelium, but the principal cells are low cuboidal. Magnification ⫽ 2,000⫻.
Fig. 4. Parotid: gray “four-eyed” opossum (Philander opossum). A portion of an ED immediately distal to
the striated duct at the left. The ED here consists of simple columnar epithelium. Magnification ⫽ 3,200⫻.
position and their relatively thick mantle of fibrous connective tissue (Fig. 1). It needs to be emphasized, however,
that in many small-sized species of mammals, the major
salivary glands are tightly compacted so that interlobular
ducts are difficult to locate. In certain species, especially
among bats, we have noted that an entire major salivary
gland (usually the parotid gland) consists of just a single
lobule, so that such organs perforce lack interlobular
ducts. If the most proximal portion of an MED in a monolobular gland is fortuitously included in a given section,
we considered it to be functionally analogous to bona fide
EDs and included it in our study (Fig. 2).
In recent textbooks of human histology, smaller EDs are
described as consisting of pseudostratified epithelium
that, as the ducts increase in caliber, become stratified
columnar epithelium. Actually, at any given level of human EDs (and in many other species as well), they are
composed of a melange of epithelial types, including simple cuboidal, simple columnar, pseudostratified, stratified
cuboidal, and stratified columnar (Figs. 3–5), in no particular pattern (Tandler and Riva, 1986; Tandler, 1988),
although a given ED can consist wholly of just one type or
one epithelial type may predominate. In this review, we
use the conventionally described histological organization
of human EDs as the exemplar of these ducts and detail
deviations from this arbitrary (nonphylogenetic) standard.
The transition between striated ducts and EDs is not
necessarily abrupt. Sometimes there are ducts of intermediate morphology, usually at the edge of a given lobule,
and continuing between lobules. Such intermediates usually display a modicum of basal striations, although some
proximal EDs sometimes exhibit all of the structural trappings of striated ducts (Fig. 6). These transitional ducts
are not dealt with in detail in this review. However, we do
take into account bona fide EDs that resemble striated
ducts, at least in their proximal portions.
In many species, the morphogenesis of the major salivary glands is incomplete at the time of birth (Young and
van Lennep, 1978). For example, in the neonatal mouse,
the parotid gland consists of a canalized branching duct
system and terminal buds. Sialographic studies have
shown that in this species, the organization of the peripheral duct system is developed by 3 weeks postnatally, and
that there are strain-specific differences in the ductular
patterns (Domon and Kurabayashi, 1987).
In the submandibular gland of the adult mouse, EDs
account for ⬃ 1.7% of total gland volume (Pardini and
Taga, 1996) and in the rat for ⬃ 1%. EDs constitute 2.8%
of the volume of the rat parotid gland (Ježek et al., 1996).
EXCRETORY DUCTS OF SALIVARY GLANDS
501
Fig. 5. Submandibular: Geoffroy’s long-nosed bat (Anoura geoffroyi). An ED that consists of stratified
columnar epithelium. Magnification ⫽ 12,100⫻.
In the submandibular gland of the South American sea
lion (Otaria byronia), EDs represent 1.3% of the fractional
volume, whereas in the parotid gland of the same animal
they represent just 0.6% (Fava-de-Moraes et al., 1966); the
same percentages apply respectively to the submandibular and parotid glands in the Southern fur seal, Arctocephalus australis (Fava-de-Moraes et al., 1966). The fractional volume of EDs in the human submandibular gland
is not fixed, but increases with age, ranging from ⬃ 0.5%
during years 16 –25 to ⬃ 1.0% during years 86 –95 (calculated from Scott, 1977).
In the rat submandibular gland (and probably in major
salivary glands of other species as well), the ducts are at
their largest at the gland hilus and, as they undergo
several orders of branching, they become smaller in diameter (Lorber, 1991). These ducts and their covering of
collagen are considered by Lorber (1991) to constitute a
structural framework for the fluctuant parenchyma that
helps to maintain the patency of endpiece, ductular, and
vascular structures in the face of cervical and mandibular
movements that potentially could occlude them. The presence of abundant circumferential elastic fibers in the connective tissue that surrounds the EDs (Phang and Rannie,
1982; Lorber, 1992) might be important in the mechanical
interplay between ducts and their connective tissue milieu
(Lorber, 1992).
In an ultrastructural study of EDs in human parotid
and submandibular glands, Lantini et al. (1990) describe
the walls of these ducts as consisting of tall principal cells
and widely scattered basal cells (and thus could properly
be described as consisting of pseudostratified epithelium).
The principal cells lack basal striations, but their lateral
surfaces are highly plicated and interlocked. The irregularity of these lateral cell surfaces is amply confirmed by
scanning electron microscope (SEM) studies of EDs that
have been divested of their basement membranes and that
have been fractured to reveal their entire profile (Riva et
al., 1990, 1993; Riva, 1992) (Fig. 7). It is the abundant
slender ridges on these external surfaces that are responsible for the lateral interfoliation of the principal cells. The
502
TANDLER ET AL.
Fig. 6. Submandibular: minipig (Sus scrofa). The basal portion of a
proximal ED that still retains the basal configuration of a striated duct.
Magnification ⫽ 15,800⫻.
lateral folds house the transport enzyme, K⫹-pNPPase
(Lantini et al., 1990). The luminal surfaces of the principal
cells frequently protrude into the duct lumen—these protrusions are different from the apical blebs that are often
observed in SDs and that in most cases represent fixation
artifacts (Tandler et al., 2001)—and that contain cytoplasm indistinguishable from that in lower reaches of the
cells. SEM reveals that these ED protrusions are covered
by stubby microvilli (Lantini et al., 1990).
Although the principal cells contain many mitochondria, these organelles show no preferential location within
the cytoplasm (Lantini et al., 1990). Despite their irregular distribution, the mitochondria are metabolically active, as shown by histochemical demonstration of dehydrogenase (Table 1) and oxidase (Table 2) activities.
Typically, the principal cells include scattered cisternae
of rough endoplasmic reticulum (RER) as well as some
smooth endoplasmic reticulum (SER). In the principal
cells of EDs in the accessory submandibular gland of the
long-winged bat, Miniopterus magnater, there are many
membranous crystalloids that appear to be localized specializations of the SER (Fig. 8) (Tandler et al., 1997a). We
Fig. 7. Submandibular: human (Homo sapiens). A portion of the wall
of an ED viewed in profile by SEM. Note the vertically oriented lateral
folds on the principal cells, as well as the numerous short microvilli on
the luminal surface of these cells. Magnification ⫽ 5,000⫻. Micrograph
courtesy of Alessandro Riva.
have hypothesized that these organelles might be involved
in steroid metabolism and conceivably could be involved in
reproductive behavior in this species.
Prominent lipofuscin deposits frequently are present in
the supranuclear cytoplasm of ED cells; these undoubtedly represent lysosomal structures. Acid phosphatase,
the marker enzyme for lysosomes, has been cytochemically identified in the ED cells of many mammals (Table
3). Other acid hydrolases also have been identified in ED
cells (Table 4). The apical protrusions include numerous
empty-appearing vesicles, but in some cells these vesicles
have a moderate density.
Cytokeratins, components of the cytoskeleton, are a
prominent feature of the apical cytoplasm of EDs in many
different species. These are intermediate filament proteins that have been classified into at least 20 subtypes
according to their molecular weights and isoelectric
points. Both monoclonal and polyclonal antibodies have
been used to identify cytokeratins in salivary glands; in
fact, more than 60 different antibodies have been used in
salivary gland studies. Table 5 is a compendium of species
503
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 1.
Enzyme
Dehydrogenases of ED cells
Common Name
Gland
References
P,SL,SM
P
SL
SM
SM
P
P,SM
SL
P,SL,SM
P,SL,SM
P,SL,SM
P
SL
Succinic dehydrogenase
cat
dog
Syrian hamster
SL,SM
Harrison, 1974
Kawakatsu et al., 1959b, 1962
Kawakatsu et al., 1959b
Kawakatsu et al., 1959b, Arvy, 1963
Triantafyllou et al., 1999
Kawakatsu et al., 1959b, 1962
Kawakatsu et al., 1959b, 1962
Kawakatsu and Mori, 1962
Kawakatsu et al., 1959b
Smith, 1969
Kawakatsu et al., 1959b
Ferguson, 1967
Kawakatsu et al., 1959b; Ferguson, 1967; Vetter, 1969;
Shiba et al., 1972
Hill and Bourne, 1954; Kawakatsu et al., 1959b; Arvy,
1963; Shklar and Chauncey, 1963; Ferguson, 1967;
Vetter, 1969; Mira et al, 1971; Shiba et al., 1972;
Tomich and Eversole, 1972; Chomette et al., 1981
Shapiro, 1967
rat
P
SL
SM
Ferguson, 1967
Ferguson, 1967; Chomette et al., 1981
Ferguson, 1967; Mira et al., 1971; Chomette et al., 1981
rat
P,SL,SM
Ferguson, 1967
rat
P,SL
SM
Ferguson, 1967
Ferguson, 1967; Chomette et al., 1981
rat
mouse
black-eared
tufted
marmoset
white-eared
tufted
marmoset
Philippine tarsier
human being
SM
SM
P
Mira et al., 1971; Tomich and Eversole, 1972
Tajima et al., 1979
Miraglia et al., 1974
P
Miraglia et al., 1974
P,SL,SM
P,SM
Smith, 1969
Sirigu et al., 1982b
black-eared
tufted
marmoset
white-eared
tufted
marmoset
human being
P
Miraglia et al., 1974
P
Miraglia et al., 1974
P,SM
Sirigu et al., 1982b
pig
SM
Booth and Polge, 1976
pig
SM
Flood, 1973
pig
SM
Flood, 1973
pig
SM
Flood, 1973
rat
P
SM
Ferguson, 1967
ferret
guinea pig
human being
mouse
Philippine tarsier
rabbit
rat
SM
Isocitrate dehydrogenase
␣-Ketoglutarate
dehydrogenase
Malate dehydrogenase
Glucose-6-phosphate
dehydrogenase
6-Phosphogluconate
dehydrogenase
3␤-Hydroxy-5-enesteroid dehydrogenase
5␤-3␤-Hydroxysteroid
dehydrogenase
D5-3␤-Hydroxysteroid
dehydrogenase
5␤-3␣-Hydroxysteroid
dehydrogenase
11␤-Hydroxysteroid
dehydrogenase
504
TANDLER ET AL.
TABLE 1. Dehydrogenases of ED cells (continued)
Enzyme
Common Name
Gland
References
17␤- Hydroxysteroid
dehydrogenase
human being
P,SM
Sirigu et al., 1982b
rat
P,SL
SM
Ferguson, 1967
Ferguson, 1967; Høyer and Møller, 1977
black-eared
tufted
marmoset
white-eared
tufted
marmoset
rat
P
Miraglia et al., 1974
P
Miraglia et al., 1974
SM
Mira et al., 1971; Tomich and Eversole, 1972
ferret
rat
SM
SM
Triantafyllou et al., 1999
Mira et al., 1971; Tomich and Eversole, 1972; Chomette
et al., 1981
cat
ferret
rat
P,SL,SM
SM
P
SM
Syrian hamster
SL,SM
Harrison, 1974
Triantafyllou et al., 1999
Peagler and Redman, 1999
Mira et al., 1971; Tomich and Eversole, 1972; Høyer
and Møller, 1977
Shapiro, 1967
black-eared
tufted
marmoset
white-eared
tufted
marmoset
cat
dog
ferret
Syrian hamster
rat
P
Miraglia et al., 1974
P
Miraglia et al., 1974
P,SL,SM
P
SM
SL,SM
SM
Harrison, 1974b
Kawakatsu et al., 1962
Triantafyllou et al., 1999
Shapiro, 1967
Mira et al., 1971; Høyer and Møller, 1977; Chomette et
al., 1981
Alcohol dehydrogenase
Glycerol-3-phosphate
dehydrogenase
Lactate dehydrogenase
NADH dehydrogenase
NADPH dehydrogenase
P, parotid; SL,sublingual; SM, submandibular.
and glands in which cytokeratin filaments have been identified in the principal cells of EDs by cytochemical and
immunocytochemical means. Some of the cited studies
include the identification of cytokeratins in a variety of
salivary gland tumors.
The ED basal cells are irregularly cuboidal as seen by
transmission electron microscopy (Lantini et al., 1990),
but as viewed by SEM they are cup-shaped, with their
concave surface facing the overlying principal cells (Riva
et al., 1992). This concave surface possesses slender folds
that are interlocked with those on the principal cells, with
occasional desmosomes binding the two disparate cell
types together. Their basal surface often forms irregular
projections into the duct surroundings that are quite evident with SEM (Brocco and Tamarin, 1979). Hemidesmosomes on these projections bind the basal cells, hence the
ED in toto, to the basement membrane. Sato and Miyoshi
(1999) have devised a method for isolating the intact duct
system of the rat submandibular gland, a technique that
in the future might facilitate the examination of EDs by
SEM.
Variations on this basic structure, some minor, some
major, are common in various species. Pinkstaff (1980)
has reviewed ED epithelial types in a variety of mammals,
a compendium based for the most part on paraffin-embedded material. The histological structure of EDs, based
largely on light microscopic observations of semithin sections stained with toluidine blue (indicated by an asterisk)
in many species, is given in Table 6; where electron microscopic observations are available, these are included.
EDs in the parotid gland of the olive baboon for the most
part resemble those in human parotid gland, but their
lateral walls show less interplication (Tandler and Erlandson, 1976). In the little brown bat, Myotis lucifugus,
the basal portion of the principal cells closely resembles
that of SD cells in that they have basal striations consisting of highly folded plasma membranes and vertically
oriented mitochondria (Fig. 9) (Tandler and Cohan, 1984).
The tall columnar light cells (terminology of Tamarin and
Sreebny, 1965) of laboratory rat submandibular glands
show interleafing of their basal portions of a complexity
greater than that seen in the SDs of the same gland; the
basal cells are similar to those in human beings.
Secretory granules are present in the apical cytoplasm
of EDs in various salivary glands of certain species (Fig.
10, Table 6). In the little brown bat, for example, cells with
505
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 2. Oxidases in ED cells
Enzyme
Common Name
Gland
References
Cytochrome oxidase
cat
dog
ferret
mouse
guinea pig
Philippine tarsier
human being
rabbit
rat
P,SM
SL
P
SL
SM
SM
P,SL,SM
P,SL,SM
P,SL,SM
P
SL
SM
P,SM
P
SL
SM
Harrison, 1974b; Kawakatsu et al., 1964b; Mori and
Mizushima, 1965
Harrison, 1974
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Mori and Mizushima, 1965
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Triantafyllou et al., 1999
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Smith, 1969
Kawakatsu et al., 1964b
Mori and Mizushima, 1965
Kawakatsu et al., 1964a, 1964b; Mori and Mizushima, 1965
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Kawakatsu et al., 1964b; Mori and Mizushima, 1965
Burstone, 1959; Kawakatsu et al., 1964b; Mori and
Mizushima, 1965
Kawakatsu et al., 1964b; Mori and Mizushima, 1965;
Tomich and Eversole, 1972
Monoamine oxidase
dog
rat
guinea pig
P,SL,SM
SL,SM
P,SM
Fujiwara et al, 1966
Almgren et al., 1966
Kawakatsu et al., 1961
P, parotid; SL, sublingual; SM, submandibular.
Fig. 8. Accessory submandibular: long-winged bat (Miniopterus
magnater). A crystalloid in a principal cell of an ED. These structures
appear to be local specializations of the SER. Magnification ⫽ 14,400⫻.
granules alternate with cells that lack these secretory
products (Fig. 11) (Tandler and Cohan, 1984). The controversial hormone, parotin, has been shown by immunocytochemistry to be localized in the supranuclear cytoplasm
of ED cells in the bovine parotid gland (Takano and Suzuki, 1971); presumably this factor is sequestered in secretory granules. Because ED granules have never been
isolated and biochemically analyzed, knowledge of their
composition, especially of their glucoconjugates, is based
almost entirely on histochemistry. Periodic acid-Schiff
(PAS)-positive glycoconjugates that may be either neutral
or sialoglycoconjugates have been shown in EDs of several
species: the sublingual gland of the vampire bat, Desmodus rotundus (DiSanto, 1960); buccal and submandibular
glands of the giant anteater, Myrmecophaga tridactyla
(Meyer et al., 1993); the parotid and submandibular
glands of the lesser anteater (genus Tamandua, species
not cited); the parotid gland of the giant anteater (Quintarelli and Dellovo, 1969); the submandibular glands of
the buffalo, Bubalus bubalis (Pal and Chandra, 1979); the
parotid gland of the little brown bat, Myotis lucifugus
(Pinkstaff et al., 1982); and the lingual serous glands and
lingual mucous glands of the ferret (Poddar and Jacob,
1979).
Acidic glycoconjugates have been localized in the ED
cells of several mammalian species. For example, alcian
blue (pH 2.5)-positive glycoconjugates occur in the ED
cells of the giant anteater (Meyer et al., 1993) and in the
lingual mucous glands of the ferret (Poddar and Jacob,
1979); these acidic glycoconjugates apparently are sialoglycoconjugates. Sulfated glycoconjugates are found in ED
cells of the vampire bat sublingual gland (DiSanto, 1960),
in the buccal glands of the giant anteater (Meyer et al.,
1993), and in the zygomatic glands of the ferret (Jacob and
Poddar, 1978). Acid glycoconjugates that stain metachromatically with toluidine blue have been reported as occurring in ED cells of the vampire bat sublingual gland (DiSanto, 1960).
The use of monoclonal antibodies to study glycoconjugates, primarily glycoproteins, has facilitated the localization of specific glycoconjugates in ED cells. Both H type 1
and H type 2 antigens of ABO blood group glycoproteins
have been localized in the ED cells of the human subman-
506
TANDLER ET AL.
TABLE 3. Acid phosphatase in ED cells
Common Name
Gland
References
cat
dog
cow
rabbit
human being
SM
P,SM
P,SM
P,SM
P
SM
P
P
SM
P
SM
Harrison, 1974
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1959
Chauncey and Quintarelli, 1959; Kawakatsu and Mori, 1962
Miraglia et al., 1974
Miraglia et al., 1974
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961; Shklar and Chauncey, 1963;
Arvy, 1963; Bogart, 1970; Tomich and Eversole, 1972;
Chomette et al., 1981; Isaacson, 1986
black-eared tufted marmoset
white-eared tufted marmoset
sheep
rat
P, parotid; SL, sublingual; SM, submandibular.
TABLE 4. Acid hydrolases in ED cells
Enzyme
␤-Galactosidase
␤-Glucosidase
␤-Glucuronidase
Common name
Gland
References
dog
sheep
pig
rabbit
human being
P,SM
SM
SM
P,SM
P
rat
guinea pig
SM
SM
SM
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1961
Chauncey and Quintarelli, 1959; Kawakatsu and
Mori, 1962
Rutenberg et al., 1958; Shklar and Chauncey, 1963
Kawakatsu et al., 1960
human being
SM
Kawakatsu and Mori, 1962
human being
rat
mouse
SM
SM
SM
Kawakatsu and Mori, 1962
Chomette et al., 1981;
Kawakatsu et al., 1960
rat
SM
Tomich and Eversole, 1972
rabbit
rat
SL,SM
SM
Vitaioli et al., 1983
Vitaioli et al., 1981
N-acetyl-␤-glucosaminidase
Arylsulphatase
P, parotid; SL, sublingual; SM, submandibular.
dibular gland (Liu et al., 1998). Class I and class II major
histocompatibility complex (MHC) antigens have been localized in ED cells of rat parotid, sublingual, and submandibular glands (Matthews et al., 1992). Polymorphic epithelial mucin has been localized by monoclonal antibodies
against MAM-3 and MAM-6 antigens in the columnar and
basal cells of the EDs of the human parotid and submandibular glands; columnar cells are labeled by antibody
against MAM-6, whereas basal cells are labeled by antibodies against MAM-3 (Yamada et al., 1989b, 1991; Mori
et al., 1992b). E-cadherin, a transmembrane glycoprotein
that is involved in cellular adhesion, has been identified in
human parotid and submandibular glands in the membranes of ED columnar cells and is strongly expressed in
the basal cells (Yamada et al., 1996, 1999). E-cadherin is
linked to actin molecules by ␤-catenin, which is a cytoplasmic protein that has been localized in the basal cells of the
human parotid and submandibular gland EDs (Yamada et
al., 1999). Variant isoforms of another transmembrane
glycoprotein, CD44, have been identified in basal cells of
EDs of human parotid glands (Terpe et al., 1994); no
function for CD44 in salivary glands has been advanced.
Human epithelial-related antigen (hERA), another transmembrane glycoprotein, has been identified in the columnar cells of the EDs of human parotid and submandibular
glands, whereas it is basal cells in the sublingual and
minor salivary mucous glands that are strongly labeled for
this factor (Yamada et al., 1997). Human lung and gastric
cancer antigen that closely resembles sialylated Lewis
antigen has been localized in the basal cells of EDs of
human submandibular (Tsuzi et al., 1989) and parotid
glands (Shinohara et al., 1996). Using a monoclonal antibody (JSE3), Durban et al. (1994) have localized a glycoprotein in the ED cells of mouse parotid, sublingual, and
submandibular glands. Therkildsen et al. (1994) have
used monoclonal antibodies to study the simple mucintype carbohydrate antigens Tn, sialosyl-Tn, T, sialosyl-T,
T, H, and A in human salivary glands. They found inconsistent staining for Tn, T, and sialosyl-T, H, and A antigens in the ED cells of human parotid, sublingual, sub-
507
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 5. Microfilaments and Intermediate Filaments in EDs
Cytokeratins
Common Name
Gland
Human being
P
SG
Golden hamster
Syrian hamster
Rabbit
Dog
Horse
Pig
Cow
Goat
Japanese macaque
Rat
Mouse
Guinea pig
Cat
SM
SG
SM
SM
SM
SG
SG
SG
SG
SG
SG
SG
SG
SM
SG
References
Caselitz et al., 1981a, 1981b, 1986; Burns et al., 1988; Dardick
et al., 1988
Mori et al., 1985b, 1989; Hosaka et al., 1985; Born et al., 1987;
Geiger et al., 1987; Takai et al., 1988; Gustafsson et al.,
1988; Lee et al., 1990; Mori, 1991; Hamakawa et al., 1999
Nakai et al., 1985; Marshak and Leitner, 1987
Takai et al., 1985a; Mori et al., 1985a; Mori, 1991
Hamakawa et al., 1999
Ogawa et al., 2001
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a; Mori, 1991
Takai et al., 1985a,b; Hamakawa et al., 1999
Takai et al., 1985a,b; Hamakawa et al., 1999
Takai et al., 1985a; Mori et al., 1985b; Mori, 1991
Marshak et al., 1987; Hamakawa et al., 1999
Mori 1991
P, parotid; SG, unidentified salivary gland; SM, submandibular.
mandibular, and labial salivary glands, and strong
staining of basal cells in all gland types for T and sialosyl-T antigens, but no staining of duct cells in any gland
type with antibody against sialosyl-Tn antigen.
In addition to glycoconjugates, several peptide growth
factors have been histochemically identified in ED cells in
salivary glands of a variety of mammals. For example,
basic fibroblast growth factor has been immunohistochemically localized in the ED cells of the rat parotid,
sublingual, and submandibular glands (Amano et al.,
1993). Nerve growth factor (NGF) and its mRNA have
been found in scattered cells in the EDs of the mouse
sublingual gland (Ayer-Le Lievre et al., 1989). Scattered
epidermal growth factor (EGF)-immunoreactive cells have
been reported in the EDs of rat submandibular glands
(Sakabe et al., 1988). EGF has been demonstrated in ED
cells of the human submandibular gland using ultrastructural staining methods (Cossu et al., 2000) and EGF receptors occur in the ED cells of human salivary glands
(Yamada et al., 1989a). Transforming growth factor ␤1
(TGF-␤1) has been localized in the ED cells of the rat
parotid, sublingual, and submandibular glands (Amano et
al., 1991), but no TGF-␤1 mRNA was found in the ED
cells, suggesting that the ducts take up TGF-␤1 rather
than synthesize it. Activin A belongs to the TGF-␤ superfamily; weak immunoreactivity for this growth factor has
been localized in the ED cells of the rat parotid, sublingual, and submandibular glands (Bläuer et al., 1996).
Transforming growth factor ␣ (TGF-␣) immunoreactivity
has been found in the ED cells of the submandibular
glands of mice, hamsters, guinea pigs, rabbits, Yucatan
pigs, dogs, and rhesus monkeys (Ikematsu et al., 1997)
and in human parotid, sublingual, and submandibular
glands (Ogbureke et al., 1995). TGF-␣ has been localized
in the ED cells of the rat parotid, sublingual, and submandibular glands; this peptide is not present in duct cells 4
weeks postnatally, but is present by 9 weeks (Wu et al.,
1993). Because both NGF and EGF are found in secretory
granules in the granular convoluted tubules of mice and
other rodents (Gresik, 1994), it is likely that all of the
aforementioned ED growth factors similarly are housed in
secretory granules.
The protease, glandular kallikrein, has been immunocytochemically identified in secretory granules in the striated ducts of certain salivary glands (reviewed by Tandler
et al., 2001). In salivary glands, this enzyme may be involved in control of electrolyte and water transport, salivary duct secretion, and regulation of blood flow in these
organs. Kallikrein has been localized in ED cells by histochemical means (Table 7); it always is located in the subluminal cytoplasm of the duct cells, suggesting that, as in
striated ducts, it is sequestered in secretory granules. This
appears to be the case in the submandibular EDs of the
pig where the apical granules are reported to contain
kallikrein (Dietl et al., 1978). Other esteroproteases have
been localized in EDs (Table 8).
EDs of both the parotid and submandibular glands of
the slow loris, Nyctecebus coucang, are heavily granulated
(Tandler et al., 1996). These granules show a spectrum of
sizes ranging from 0.2 ␮m to ⬎ 12 ␮m in diameter. Giant
granules also are present in the SDs of these glands.
Bundles of cytofilaments (presumably actin) are connected
to the limiting membranes of the giant granules in whatever kind of duct and presumably are involved in hauling
these outsized granules to the luminal membrane for exocytosis.
Large cytoplasmic inclusions are present in the ED cells
of the parotid gland of the African mole rat, Tackyoryctes
splendens (Fig. 12) (Tandler et al., 1998b). The inclusions
consist of low-density cytosol in which are embedded myriad short filaments; all membranous organelles are excluded from each inclusion (Fig. 13). It is not known at
present if these inclusions are in some way correlated with
either the ecology or behavior of this fossorial species.
Crystalloids are present in the taller ED cells in the sublingual gland of the African multimammate rodent, Praomys natalensis (Toyoshima and Tandler, 1991), and in the
508
TANDLER ET AL.
TABLE 6. Structural characteristics of EDs in mammalian salivary glands
Classification†
METATHERIA
(marsupials)
Philander opossum
EUTHERIA
Order Insectivora
Suncus murinus
Order Scandentia
Dasypus novemcinctus
Order Chiroptera
(Suborder
Megachiroptera)
Cynopterus sphinx
Epomophorus wahlbergi
Gland
Type of
Epithelium
P
Coa & Ps
SM
Psa
Shrewb,c
SM
Co
House shrew
P
SM
Co
Coa
Unpublished
Unpublished
Nine-banded armadillo
SM
SCub
Shackleford, 1963a
Short-nosed fruit bat
P
SM
Wahlberg’s epauletted fruit
bat
AP
Ps
Cu3Co &
Psa
Psa
PP
SM
AP
PP
SM
Ps
Psa
Ps
Ps
Psa
PP
Psa
AP
PP
SM
Psa
Psa
Psa
PP
Ps
P
Ps
PP
AP
PP
SM
PP
SM
C
Psa
Co & Ps
Ps & Coa
Coa
Co & Psa
ASM
P
PSM
ASM
P
PSM
P
Co3Cu
Cu & Ps
Co & Psa
Cu
Co
Co
Cu3Co &
Psa
Co & Psa
Psa
Cu3Co &
Psa
Psa
Cua
Coa
Cu3Psa
Cu3Psa
Coa
Coa
Common Name§
Grey ’four-eyed’ opossum
Megaerops ecaudatus
Temminck’s tailless fruit bat
Myonycteris relicta
East African little collared
fruit bat
Rousettus amplexicaudatus
Rousettus (Lissonycteris)
angolensis
Rousettus (Stenonycteris)
lanosus
Rousettus leschenaulti
Eonycteris spelaea
Angolan rousette
Macroglossus sobrinus
Hill’s long-tongued fruit bat
(Suborder Microchiroptera)
Cardioderma cor
Megaderma lyra
Heart-nosed bat
Greater false vampire bat
Megaderma spasma
Malayan false vampire bat
Leschenault’s rousette
Long-tongued dawn fruit bat
Rhinolophus acuminatus
SM
P
SM
Rhinolophus affinis
Rhinolophus coelophyllus
Rhinolophus fumigatus
Rhinolophus lepidus
Rüppell’s horseshoe bat
Rhinolophus pumilio
Hipposideros armiger
Horseshoe bat
Himalayan roundleaf bat
Hipposideros diadema
Diadem roundleaf bat
SM
P
P
SM
SM
P
SM
P
SM
Cu & Co &
Psa
Co & Psa
Unusual
features
Prox. basal
striations
References
Unpublished
Unpublished
Some basal
striations
Goblet cells
Unpublished
Unpublished
Unpublished
Unpublished
Goblet cells
Goblet cells
Some goblet
cells
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Some goblet
cells
Basal striations
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Basal striations
Long microvilli
Basal striations
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Some basal
striations
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
509
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 6. Structural characteristics of EDs in mammalian salivary glands (continued)
Classification†
Common Name§
Hipposideros gentilis
Saccopteryx bilineata
Greater sac-winged bat
Gland
Type of
Epithelium
a
P
SM
SM
P
SM
Ps
Psa
Psa
Co*
Co*
Noctilio leporinus
Mormoops blainevilli
Pteronotus parnellii
Greater bulldog bat
Blaineville’s leaf-chinned bat
Parnell’s mustached bat
SM
PSM
P
Cu
Psa
Psa
Macrotus waterhousi
California leaf-nosed bat
SM
P
SM
Psa
Cu3Coa
Cu & Co &
Psa
SM
SM
P
SM
Co prox
Psa
Psa
Psa
SM
P
SM
Psa
Psa
Psa prox.
P
Psa
Phyllostomus aphylla
Phyllostomus discolor
Phyllostomus elongatus
Phyllostomus hastatus
Phyllostomus latifolius
Tonatia bidens
Pale spear-nosed bat
Lesser spear-nosed bat
Pallas’s spear-nosed bat
Guianan spear-nosed bat
Greater round-eared bat
Unusual
features
a
SM
SM
Ps
Basal
striations
Alternating
light & dark
cells
Basal
striations
Basal
striations
Sparse
granules
Basal
striations;
nerve
terminals
Occasional
dense
granules
Tonatia silvicola
D’Orbigny’s round-eared bat
P
Psa
Trachops cirrhosus
Fringe-lipped bat
SM
P
SM
Erophylla sezekorni
Anoura geoffroyi
Buffy flower bat
Geoffroy’s long-nosed bat
SM
P
SL
SM
Glossophaga soricina
Long-tongued nectar bat
P
Leptonycteris nivalis
Saussure’s long-nosed bat
SM
SM
Cu3Co3Psa
Psa
Ps
Bundles of
nerve
terminals
Co & Ps
Ps*
Ps*
Psb* &
Some basal
SCo
striations
Cu prox &
Psa
Psa
Psa
Microvilli
Monophyllus redmani
Leach’s single leaf bat
Carollia perspicillata
Short-tailed leaf-nosed bat
P
SM
P
Coa
Coa
Ps
Ametrida centurio
Ariteus flavescens
White-shouldered bat
Jamaican fig-eating bat
SM
SM
P
SM
Psa
Psa
Cu3Coa
Cua
Some basal
striations;
numerous
hypolemmal
nerve
terminals
Prominent
microvilli
References
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Tandler et al.,
1999
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Phillips et al.,
1977;
Unpublished
Unpublished
Unpublished
Tandler et al.,
1988
Unpublished
Unpublished
Unpublished
Unpublished
510
TANDLER ET AL.
TABLE 6. Structural characteristics of EDs in mammalian salivary glands (continued)
Classification†
Common Name§
Gland
Type of
Epithelium
Unusual
features
Artibeus cinereus
Gervais’s fruit bat
P
Ps
Artibeus jamaicensis
Jamaican fruit bat
SM
P
Artibeus lituratus
Chiroderma villosum
Enchisthenes hartii
Big fruit bat
Sturnira lilium
Yellow epauletted bat
P
SM
Uroderma bilobatus
Tent-building bat
Desmodus rotundus
Common vampire bat
P
SM
ASM
Cu3Co3Psa
Cu & Psa
Resembles SD;
branching
dark cells
Cu*
Co & Psa
Cua
Ps
Prox: like SD
Dist:
numerous
mitochondria
a
Co3Ps
Cua prox
& Psa
Co3Cu
Cua
Microvilli
Co & Ps
PSM
Psa
Brush border
Ps
Cu
Cu
Coa
Brush border
Hart’s little fruit bat
SM
SM
SM
P
Diaemus youngi
Natalus strameus
White-winged vampire bat
Mexican funnel-eared bat
Chalinolobus argentatus
Silvered bat
P
SL
SM
P
Brazilian brown bat
SL
SM
SM
P
Coa
Cua
Cu & Psa
Co
P
P
SL
Psa
Psa
Psa
SM
Co & Psa
ASM
P
Coa
Ps
ASM
P
PSM
P
P
SM
Coa
Psa
Coa
Psa
Coa
Coa & Psa
P
Coa
Chalinolobus humeralis
Eptesicus brasiliensis
Eptesicus lynni
Hesperoptenus blanfordi
Myotis annectans
Myotis lucifugus
Lynn’s brown bat
Little brown bat
Myotis montivagus
Myotis muricula
Pipistrellus mimus
Pipistrellus pulveratus
Pipistrellus coromandra
Indian pipistrelle
Pipistrellus kuhli
Scotophilus dingani
Tylonycteris pachypus
a
European pipistrelle
P
SM
P
Ps
Psa
Ps
African yellow bat
Club-footed bat
SM
ASM
Ps?Cu
Cu
P
SM
Co & Psa
Psa
Many
mitochondria
Numerous
mitochondria
Mitochondrion:
desmosome
complexes;
basal
striations
Prox. basal
striations
Basal
striations
Alternating
non-granular
& granular
cells; basal
folds
Basal
striations
Some basal
striations
Small dense
granules
References
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Tandler et al.,
1990a
Tandler et al.,
1990a
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Tandler and
Cohan, 1984
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Azzali et al., 1986
Unpublished
Tandler et al.,
1995
Unpublished
Unpublished
511
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 6. Structural characteristics of EDs in mammalian salivary glands (continued)
Classification†
Tylonycteris pachypus
Common Name§
Club-footed bat
Harpiocephalus harpia
Hairy-winged tube-nosed bat
Murina cyclotis
Tube-nosed bat
Murina leucogaster
Miniopterus inflatus
Gland
Type of
Epithelium
ASM
Cu
a
Tube-nosed bat
Greater long-fingered bat
P
SM
P
SM
SM
ASM
Co & Ps
Psa
Ps
Co
Co & Ps
Ps
Miniopterus magnater
Western long-fingered bat
ASM
Ps
Miniopterus schreibersi
Schreiber’s long-fingered bat
ASM
Ps
Molossus molossus
Velvety free-tailed bat
P
PSM
P
Cu proxa
Cu & Co
Ps
Tadarida thersites
Free-tailed bat
AP
Ps
SM
SCoa
P
Ps
SM
Ps
Order Primates
Nycticebus coucang
Slow loris
Saguinas fuscicollis
Ateles paniscus
Tamarin
Spider monkey
P
P
Cu
PS
Macaca mulatta
Rhesus monkey
SM
Psb
Papio cynocephalus
Baboon
SM
Psb
Homo sapiens
Order Carnivora
Felis catus
Mustela putorius
Mustela siberica
Human being
Domestic cat
Ferret
Siberian weasel
Unusual
features
Hypolemmal
nerve
terminals
SER
crystalloids;
hypolemmal
nerve
terminals
Hypolemmal
nerve
terminals
A few
granulated
cells
Single row of
apical
granules
Some basal
striations
Many goblet
cells
P
SM
SCo
PS SCo
P
C
SM
Psa
P
Cu?Cob
SL
SCub
SM
Cu?Cob
P
Cu
SL
C
Tandler et al.,
1995
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Tandler et al.,
1998
Unpublished
Many
granules;
some giant
Many
granules;
some giant
b
References
Many goblet
cells
Vesiculated
tall cells
Goblet cells
Paracrystalloid
granules
Small secretory
granules
Tandler et al.,
1996
Tandler et al.,
1996
Unpublished
Leeson, 1969
Pinkstaff, 1980;
Boshell and
WiIlborn, 1983
Boshell and
Willborn, 1983
Scott, 1977
Paz Ossorio et
al.,1975;
Tandler and
Riva, 1986;
Riva et al.,
1990 Tandler,
1978
Menghi et al.,
1989
Tandler , 1993b,
Tandler and
Poulsen, 1976
Poddar and
Jacob, 1977
Poddar and
Jacob, 1977
Poddar and
Jacob, 1977
Matsunaga, 1992
Matsunaga, 1992
512
TANDLER ET AL.
TABLE 6. Structural characteristics of EDs in mammalian salivary glands (continued)
Gland
Type of
Epithelium
Pig
P
P
C
Ps
Glycogen
Minipig
SM
Co
One-humped camel
P
NA
Basal
striations;
numerous
granules
Goblet cellsb
P
Classification†
Order Artiodactyla
Sus scrofa
Camelus dromedarius
Common Name§
Bos indicus
Zebu
P
SCu &
SCob
SCu &
SCob
NA
Bos taurus
Cow
SM
Psb
Ovis aries
Order Lagomorpha
Lepus europaeus
Sheep
P
NA
European hare
P
Ps
Oryctolagus cuniculus
Rabbit
SM
Co3Ps
SM
Z
Order Rodentiac
Puget Sound deer mouse
Chipmunk
Desert rat
Sagebrush deer mouse
Western flying squirrel
Beechey ground squirrel
Grey squirrel
P
SL
SM
P
Psb
Psb
Psb
Psb
SL
Psb
SM
Psb
P
SL
SM
SL
SM
P
Cub
Cob
Cob
Psb
Psb
Cu & Co &
Psb
Cob
Psb
Cob
Cob
Cob
SL
SM
P
SL
SM
b
P
Ps
Psb
Co & Psb
Co & Psb
Coa
Psa
Acomys percivali
Cricetomys gambianus
Spiny mouse
Giant pouched rat
SM
P
SM
SM
P
Tachyoryctes splendens
African mole-rat
SM
P
Psa
Co
SM
Co
Lined squirrel
Unusual
features
Many goblet
cellsb
Many goblet
cells
Goblet cellsb
Light cells &
vacuolated
cells
Blebs on tall
cells
Granular cells
Some basal
striations
Many dark
cells
Some basal
striations
References
Imai et al., 1978
Boshell and
Wilborn, 1978
Unpublished
Nawar and ElKhaligi, 1975
Mansouri and
Atri, 1994
Mansouri and
Atri, 1994
Vignoli and
Nogueira, 1981
Shackleford and
Klapper, 1962
Quintarelli, 1963
Suzuki et al.,
1985
Toyoshima and
Tandler, 1986
Gargiulo et al.,
1996
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Some basal
striations
Cuboidal
principal
cells
Basal
striations
Large,
filamentous
inclusions
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Unpublished
Tandler et al.,
1998b
Unpublished
513
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 6. Structural characteristics of EDs in mammalian salivary glands (continued)
Classification†
Common Name§
Gland
Type of
Epithelium
Ps
Ps
Ps
Ps
Coa
Tatera nigricauda
Ondatra zibethicus
Castor canadensis
Naked soled gerbil
Muskrat
North American beaver
Marmota monax
Ground hog
SM
SM
P
SM
SL
Proechimys cuvieri
Apodemus agrarius
Cuvier’s spiny rat
Striped field mouse
SM
SM
Coa
Coa
Lophuromys sikapusi
Harsh-furred mouse
P
Ps
Praomys natalensis
African multi-mammate
rodent
Laboratory rat
SL
Co
P
Co
SL
variable
SM
Ps
Rattus norvegicus
Mus musculus
Laboratory mouse
SM
Ps
Zelotomys hildegardeae
Tachoryctes splendens
Broad-headed mouse
African mole-rat
SL
P
Ps
Ps
Zygodontomys reigi
Cane mouse
SM
Co
Myocastor coypus
Nutria
P
NA
Unusual
features
Basally
branched
dark cells
Basal
striations
Some globular
leukocytes
Cytoplasmic
crystalloids
Tall dark
vesiculated
cells
Catalasepositive rods
Luminal
membranes
positive for
carbonic
anhydrase I
&2
Filamentous
inclusions
Basal
striations
Many goblet
cellsb
References
Unpublished
Unpublished
Unpublished
Unpublished
Pinkstaff, 1980
Unpublished
Unpublished
Unpublished
Toyoshima and
Tandler, 1991
Jeẑek et al., 1996;
Unpublished
Garrett and
Anderson, 1991
Tamarin and
Sreebny, 1965
Hanker et al.,
1977
Ogawa et al.,
1992
Gutierrez Marin
et al. 1990
Unpublished
Tandler et al.,
1998
Unpublished
Dix, 1969
†
Generic and specific names are based on Wilson and Reeder (1993). In a few instances, we have corrected or updated generic
or specific names from the original published nomenclature. In published work other than our own, we are unable to confirm
the identifications.
§
Where there is no generally accepted common name, this designation is omitted. AP, accessory parotid; ASM, accessory
submandibular; P, parotid; PSM, principal submandibular; SL, sublingual; SM, submandibular; VB, ventral buccal; Z,
zygomatic; Co, simple columnar epithelium; Cu, simple cuboidal epithelium; Ps, pseudostratified epithelium; SCo, stratified
columnar epithelium; SCu, stratified cuboidal epithelium; NA, not available; SD, striated duct; ? , proceeding in a distal
direction; dist, distal; prox, proximal; a Based on semithin epoxy sections; b Based on paraffin sections; cInsectivore and rodent
data without genus and species identification are based on slides from the collection of the late Arnold Tamarin (no voucher
specimens were available for species identification).
EDs of the accessory submandibular glands of the longwinged bat, Miniopterus magnater (Tandler et al., 1997a).
EDs in the parotid glands of seven species of fruit bats
in the genus Artibeus resemble SDs in the same gland, but
occasionally include one or several dark cells in a given
sectioned duct (Fig. 14) (Tandler et al., 1997c). Dark cells
constitute 4.7% of the cells in the wall of the proximal EDs
in the rat submandibular gland and 7.2% of the cells in the
more distal EDs (Sato and Miyoshi, 1998). The nature of
dark cells is unclear. They conceivably may be fixation
artifacts; they also might represent a distinct phase in the
cell life cycle or physiological activity. In some glands,
dark cells might represent a unique cell type. This especially appears to be the case in the EDs of sublingual
glands of the woodchuck, where dark cells with branched
bases alternate with light cells of more typical morphology
(Pinkstaff, 1980). The subject of dark cells is more fully
dealt with elsewhere in the context of the striated duct
(Tandler et al., 2001).
In the sublingual glands of various mammals, endpieces
either empty into IDs, which lead into EDs without the
intervention of SDs, or empty directly into EDs. In the
retrolingual (equivalent to the sublingual) gland of the
European hedgehog, intercalated ducts gradually become
EDs, changing from simple cuboidal to simple columnar
epithelium in the process (Tandler, 1986). In this gland,
most of the principal cells of the ED display a subluminal
zone that contains an abundance of moderately dense
514
TANDLER ET AL.
granules, which measure ⬃ 0.2 ␮m in diameter. Intermingled with these granulated cells are a few rare cells that
lack granules. At a point at which the ED becomes
pseudostratified are occasional mitochondrial aggregates,
wherein adjacent organelles are joined by periodic crossbridges.
The ductular picture that emerges in minor salivary
glands is not unlike that occurring in the sublingual
glands. Endpieces can join intercalated ducts that
progress into EDs without an obvious line of demarcation
(Tandler et al., 1970; Takeda et al., 1978) or that may be
directly connected with EDs (Nagato et al., 1998). EDs in
human palatal glands run a twisted helical course (Maximuk and Shertyuk, 1990). In von Ebner’s glands of the
rabbit (Toyoshima and Tandler, 1986), the most proximal
duct cells contain dense serous-type granules that exhibit
a lacuna of lower density. Granules in the more distal
ducts of these glands differ from their predecessors, having a compound structure consisting of a dense portion
and a portion of lesser density. Cells of the latter type
occasionally include a dilated cistern of RER with a moderately dense content. Some ciliated cells are present in
the most distal EDs of human von Ebner’s glands (Azzali
et al., 1989). In certain minor glands, e.g., Weber’s glands
of the rat tongue (Nagato et al., 1997) and the midlingual
glands of the vampire bat (Tandler et al., 1997d), EDs may
lead directly onto an oral surface, in a sense acting as the
MED of such organs. In the latter glands, some of the duct
cells are fitted with cilia with typical 9⫹2 structure (Tandler et al., 1997d).
Human anterior lingual glands (glands of Blandin and
Nuhn) have EDs (Tandler et al., 1954) that resemble those
Fig. 9. Submandibular: laboratory rat (Rattus norvegicus). An ED
consisting of tall simple columnar epithelial cells. Note the highly folded
cell base. These folds are too slender to accommodate mitochondria,
hence the cells lack obvious basal striations. Magnification ⫽ 2,300⫻.
Fig. 11. Parotid: little brown bat (Myotis lucifugus). A principal cell in
an ED that is devoid of granules, but that contains an abundance of
smooth-surfaced vesicles and tubules. This cell is flanked by cells that
have an abundance of small dense granules. Magnification ⫽ 24,500⫻.
Fig. 10. Submandibular: minipig (Sus scrofa). The subluminal cytoplasm of several ED cells contains
many small dense secretory granules. Magnification ⫽ 12,700⫻.
515
EXCRETORY DUCTS OF SALIVARY GLANDS
TABLE 7. Kallikrein in ED cells
Common name
cat
rat
mouse
guinea pig
pig
sheep
crab-eating macaque
Japanese macaque
rhesus monkey
grivet
human being
Gland
References
P
SM
P
SL
SM
SM
SM
SM
SM
P,SL,SM
P,SL,SM
P,SL,SM
P,SL,SM
P
SM
Maranda et al., 1978
Maranda et al., 1978; Garrett et al., 1985
Arnold, 1985
Ørstavik et al., 1975; Arnold, 1985
Ørstavik et al., 1975; Gutkowska et al., 1983; Arnold, 1985
Penschow and Coghlan, 1993
Schachter et al., 1978
Dietl et al., 1978
Trahair and Ryan, 1989
Arnold, 1984, 1985
Yahiro and Miyoshi, 1996
Arnold, 1984
Arnold, 1984
Ørstavik et al., 1980; Kimura and Moriya, 1984, 1986
Ørstavik et al., 1980
P, parotid; SL, sublingual; SM, submandibular.
TABLE 8. Esteroproteases in ED cells
Common Name
mouse
rat
Phillipine tarsier
crab-eating macaque
Gland
References
SL
SM
P,SL
P,SM
P,SL,SM
Gresik and Barka, 1983
Lexow et al., 1979
Arnold, 1985
Smith, 1969
Arnold, 1985
P, parotid; SL, sublingual; SM, submandibular.
in the human parotid and submandibular glands (Lantini
et al., 1990), with a few structural deviations. The EDs in
these lingual glands [and in human labial glands as well
(Tandler et al., 1970)] often include patches of SDs that
are indistinguishable from those in human major glands
(Tandler, 1993b). The pyramidal basal cells often exhibit a
primary (solitary) cilium, a structural feature more often
associated with basal cells in the rodent MED (Higashi
and Sasa, 1985; Higashi et al., 1994).
Compared to principal cells, basal cells show relatively
little variation among mammalian species. Their precise
nature has aroused some controversy. Based on their
stainability with antibodies to S100b protein and to various keratins (Palmer et al., 1985; Caselitz et al., 1986;
Palmer, 1986; Born et al., 1987; Dardick et al., 1987, 1988;
Geiger et al., 1987; Gustafsson et al., 1988; Shinohara et
al., 1989) that stain endpiece myoepithelial cells (Dairkee
et al., 1985), at least some of the basal cells have been
labeled as myoepithelium or as “modified myoepithelium”
by some authors (Mori et al., 1992a). Other authors have
relied simply on the morphology of basal cells to justify
their identification as myoepithelial cells (Chaudhry et al.,
1987). Because myoepithelial cells are involved in the
histogenesis of a variety of salivary gland tumors (Batsakis et al., 1983; Dardick and van Nostrand, 1985; Nikai
et al., 1986; Gustafsson et al., 1989), it is of some importance to determine whether the ductular basal cells are in
fact of myoepithelial origin.
In a more recent report, Dardick et al. (1991) state that
S100 protein antibodies stain nerve fibers that are closely
applied to salivary parenchyma, rather than myoepithelium. Other workers have pointed out the unreliability of
S100 protein as a marker of myoepithelium (Gillett et al.,
1990; Möller and Hellmén, 1994). The use of antikeratin
antibodies to identify myoepithelial cells probably is similarly flawed, because various antibodies of this type label
basal cells of stratified epithelia, irrespective of the source
of this tissue (Pallesen et al., 1987; Maeda and Sueishi,
1989); the labeling of basal cells in tissues such as stratified squamous epithelium that clearly lack myoepithelial
components makes evident the unreliability of keratin
staining as a label for myoepithelium. When all is said and
done, the best marker for myoepithelial cells remains actin (Archer and Kao, 1968; Drenckhahn et al., 1977; Yoshihara et al., 1988; Norberg et al., 1992). Using an antiactin antibody, Nilsen and Donath (1981) found a few
positive cuboidal cells in the “larger” ducts of the human
submandibular and parotid glands, but Gugliotta et al.
(1988) failed to stain basal cells in EDs of several different
human salivary glands with a similar antibody, although
myoepithelial cells associated with endpieces and intercalated ducts were positive. Thus, it appears that basal cells
of EDs probably are not related to myoepithelial cells. The
absence from basal cells of the cytoplasmic machinery
normally associated with secretion or electrolyte transport
(although their histochemistry reveals the presence of
various transport enzymes) suggests that a major function
of these cells in the parotid and submandibular glands is
to bind the ductular epithelium to the basement membrane through the agency of their hemidesmosomes.
In some species, other cell types are intermingled with
the principal cells of the EDs. These include the aforementioned dark cells, and vesiculated, brush, and goblet cells
as well. Tall dark vesiculated cells characterized by a
dense cytosol and numerous small empty-appearing vesicles are present in the EDs of the rat submandibular gland
(Tamarin and Sreebny, 1965). These cells have basal striations that match those in their more conventional neighbors. Tuft cells have a unique structure that allows their
ready identification: they have many thick blunt microvilli
with very long rootlets, among which are numerous electron-lucent vesicles as well as microtubules (Sato and
Miyoshi, 1997). The function of these cells is unknown but
they might act as chemoreceptors (Höfer et al., 1996).
Scattered goblet cells are present in the EDs of both
parotid and submandibular glands primarily of primates
and of megachiropteran bats, but also occur in certain
516
TANDLER ET AL.
Fig. 13. Parotid: African mole rat (Tachyoryctes splendens). A cytoplasmic inclusion at higher magnification. It consists of a zone of moderate- to low-density cytosol in which short filaments and occasional
vesicles are embedded. All conventional cytoplasmic organelles are
excluded, even though the inclusion lacks a circumscribing membrane.
Magnification ⫽ 34,800⫻.
Fig. 12. Parotid: African mole rat (Tachyoryctes splendens). Top:
Photomicrograph of an ED in semithin section in which many constituent
cells contain a large lucent cytoplasmic inclusion. Toluidine blue. Magnification ⫽ 300⫻. Bottom: Low-magnification electron micrograph of a
portion of the wall of an ED showing the size and extent of the cytoplasmic inclusions. Magnification ⫽ 2,500⫻.
ungulates (Shackleford, 1963b), as well as in a variety of
other species. In some glands, the EDs occasionally include clusters of goblet cells within their walls (Fig. 15).
All ductular goblet cells are of typical morphology and are
reported to be PAS-positive. This is the case in oxen and
pig parotid glands (Munhoz, 1971), in buffalo submandibular glands (Pal and Chandra, 1979), in tapir submandibular glands (Quintarelli and Dellovo, 1969), in rhesus
monkey (Macaca mulatta) parotid and submandibular
glands (Boshell and Wilborn, 1983; Stephens et al., 1986),
in cow, guinea pig, and rhesus monkey parotid glands, in
cow and pig sublingual glands (Shackleford and Klapper,
1962), and in the submandibular gland of the miniature
pig (Pinkstaff, 1972). These PAS-positive glycoconjugates
may be either neutral or sialoglycoconjugates, or both.
Alcian blue (pH 2.5)-positive glycoconjugates in goblet
cells of EDs are believed to be sialoglycoconjugates and
have been reported to occur in the parotid glands of oxen
and pigs (Munhoz, 1971), in buffalo submandibular glands
(Pal and Chandra, 1979), in lingual serous glands and
lingual mucous glands of the ferret (Poddar and Jacob,
1979), and in the parotid and submandibular glands of the
rhesus monkey (Stephens et al., 1986). Sulfated glycoconjugates have been reported in the goblet cells of EDs in
oxen and pig parotid glands (Munhoz, 1971), in buffalo
submandibular glands (Pal and Chandra, 1979), and in
lingual serous and lingual mucous glands of the ferret
(Poddar and Jacob, 1979). It is obvious that goblet cells in
EDs add a mucus component to the saliva, even in ostensibly pure serous glands.
Oncocytes occasionally are present in the EDs of human
salivary glands (Riva et al., 1988; Lantini et al., 1990).
These cells characteristically contain a plethora of structurally modified mitochondria to the virtual exclusion of
the other cytoplasmic organelles (Tandler, 1966; Riva and
Tandler, 2000; Tandler and Hoppel, 2004). Little is known
of the physiology of oncocytes arising in normal salivary
glands.
Like other parenchymal components of salivary glands,
EDs are subject to invasion by mononuclear wandering
cells, usually lymphocytes (Takeda and Fujimura, 1985),
but sometimes neutrophils (Fig. 16); the duct walls in the
parotid gland of the harsh-furred mouse, Lophuromys
EXCRETORY DUCTS OF SALIVARY GLANDS
517
Fig. 14. Parotid: Jamaican fruit bat (Artibeus jamaicencis). An ED with many irregular dark cells. Magnification ⫽ 2,900⫻. Micrograph courtesy of Toshikazu Nagato.
sikapusi, occasionally include globular leukocytes (Fig.
17), which have also been observed in the parotid gland of
the cow (Gurusinghe and Birtles, 1985). Intruding wandering cells can be identified by their high nucleus-tocytoplasm ratio and by their total lack of desmosomal
connections to surrounding epithelial cells. In the rhesus
monkey, Macaca fascicularis, labial salivary glands are
subject to invasion by bacteria (Nair and Schroeder, 1985).
In this event, ducts are surrounded by lymphoid tissue
and are heavily infiltrated by lymphocytes and blast-forming T-cells, in some cases to a point where the duct epithelium is partially or wholly supplanted by lymphoid
cells. The nuclei in the ducts of human labial glands have
immunohistochemically detectable human ␤-defensin1
(hBD-1), an antimicrobial peptide (Sahasrabudhe et al.,
2000); this agent also coats the luminal surface of the duct
cells.
In contrast to the minor glands that evince inflammatory responses, the numerous bacteria that occupy the
lumina (including those of EDs) of the entire parenchymal
tree of the accessory submandibular gland of the clubfooted bat, Tylonycteris pachypus, fail to elicit an immunological response; mononuclear cells are absent from the
duct walls and lumina and are present in the surrounding
connective tissue in only modest numbers (Tandler et al.,
1995). In this instance, the bacteria may be acting as
symbionts.
In a few rare cases, EDs in human parotid glands form
cysts that contain large crystalloids (Kurashima, 1983;
Takeda and Ishikawa, 1983). These crystalloids are rich in
sulfur (Takeda and Ishikawa, 1983). Solid, homogeneously dense, usually eosinophilic deposits sometimes
are present in EDs of both major and minor human salivary glands (Scott, 1978, 1987).
Sebaceous differentiation frequently occurs in salivary
glands; this metaplasia often involves the EDs (Gnepp,
1983; Van Esch et al., 1986; Martinez-Madrigal and
Micheau, 1989). In such metaplastic ducts, a part of or the
entire duct wall may be replaced by sebaceous cells. In
human beings, such metaplastic foci are of importance
because they can give rise (although very rarely) to sebaceous neoplasms (Gnepp, 1983). In vitamin A-deficient
rats, EDs in the submandibular gland undergo squamous
metaplasia (Trowbridge, 1969). A similar process can occur in human salivary glands (Martinez-Madrigal and
Micheau, 1989) during inflammation, especially if the latter condition is associated with calculi (Isacsson and
Lundquist, 1982).
In connection with neoplasia, the basal cells of EDs are
considered by some authors (Regezi and Batsakis, 1977;
Batsakis, 1980) to constitute a population of semipleuripotential reserve cells that are the histogenic precursors
of such salivary gland tumors as mucoepidermoid and
squamous carcinomas (reviewed by Dardick et al., 1990).
Dardick (1998) presents evidence that militates against
this concept. It appears that every cell type that makes up
salivary parenchyma is capable of self-replication. Not
only basal cells of EDs, but principal cells as well, are
capable of division (Komiya and Fukushima, 1991; Redman, 1995) and thus are potential progenitors of neoplastic cells.
It is extremely difficult to arrive at a conclusion concerning innervation of EDs because most studies that deal
with salivary gland innervation simply lump all extraacinar parenchymal elements together under the rubric
“ducts.” Only rarely are EDs specified in such studies.
According to Garrett (1976), cholinergic nerves form a
loose association with extralobular ducts, i.e., EDs, but
adrenergic nerves have not been observed in such a relationship. The cholinergic innervation of EDs can vary even
in related species (Rossoni et al., 1981). In rat salivary
glands, both calcitonin gene-related peptide (CGRP) (Soinila et al., 1989) and met5-enkephalin-arg6-gly7-leu8
(MEAGL) (Soinila et al., 1991) immunoreactive nerve fibers are present in close relation to interlobular ducts.
Gland segments proximal to the EDs are directly inner-
518
TANDLER ET AL.
Fig. 16. Sublingual: broad-headed mouse (Zelotomys hildegardae). A
neutrophil has invaded the wall of an ED. The duct lumen is filled with
dense material, which may have attracted the neutrophil. Magnification ⫽ 7,500⫻.
Fig. 15. Parotid: tailless fruit bat (Megaerops ecaudatus). Two goblet
cells at the junction of a striated duct (left) with an ED (right). Magnification ⫽ 6,200⫻.
vated by hypolemmal nerve terminals (discussed by Garrett and Kidd, 1993). Such terminals previously have not
been reported in EDs of any salivary gland. In our comparative studies, we have encountered two species that
exhibit profuse hypolemmal innervation of their EDs. In
the short-tailed leaf-nosed bat (Carollia perspicillata),
bundles of naked axons and terminals are ubiquitous
throughout the ED wall (Fig. 18). As in several other bat
species (Tandler and Phillips, 1995), these hypolemmal
terminals are shrouded by mitochondria in the adjacent
duct cells. In the fringe-lipped bat, Trachops cirrhosis, the
accessory submandibular gland has a peculiar architecture (Tandler et al., 1997b). The secretory endpieces,
which have a follicular structure, empty into ducts consisting of simple cuboidal epithelium that probably represent intercalated ducts; the epithelium gradually increases in height to form what we interpret to be EDs.
Ensconced in the walls of these presumptive EDs are
bundles of hypolemmal nerve terminals. Unlike those in
Carollia, these show no special relationship to mitochondria in surrounding cells. The significance of ED innerva-
tion is unknown, but sodium and potassium transport in
the MED is under sympathetic control (Schneyer, 1976);
such a function probably can safely be extrapolated to
EDs.
Knowledge of the function of EDs is confined wholly to
experimental animals and is based almost entirely on
micropuncture and microperfusion studies (Schneyer et
al., 1972) and on histochemistry (Pinkstaff, 1980, 1993).
The production of saliva in major salivary glands is a
two-step process: the endpiece-intercalated duct complex
elaborates saliva that has plasma-like concentrations of
electrolytes, then electrolytes are resorbed from this primary saliva as it passes through the ductal tree to render
the final saliva hypotonic (Thaysen, 1960; reviewed by
Young, 1979). Early micropuncture studies involved collection of primary saliva from the endpiece-intercalated
duct complex and from distal parts, i.e., the MED, of the
duct system (e.g., Martinez et al., 1966). By comparing the
two samples, it is apparent that there is a net resorption
of electrolytes as the saliva passes through the duct system. The presence of Na⫹,K⫹-ATPase at the base of ED
cells in human, feline, and rodent salivary glands provides
the enzymatic basis for such activity (Winston et al., 1988,
1990; Peagler and Redman, 1999). The physiological
events involved in this process have been reviewed in
detail by Schneyer et al. (1972), Martinez (1987), and
Young et al. (1987). It needs to be pointed out that as-
EXCRETORY DUCTS OF SALIVARY GLANDS
Fig. 17. Parotid: harsh-furred mouse (Lophuromys sikapusi). A globular leukocyte is ensconced in the wall of an ED. Magnification ⫽
5,900⫻.
sumed transport functions of EDs are based on extrapolations from studies on the MED (Young et al., 1987). In
minor salivary glands that lack ductular segments other
than EDs, the final saliva usually is isotonic, suggesting
that in these small glands the EDs do not play a regulatory role in salivary composition.
Pinkstaff (1980, 1993) has reviewed the histochemical
and cytochemical literature on ED enzymes. Such studies
belie the general impression that EDs merely are passive
conduits for saliva. ED cells in various species evince
substantial enzymatic activity, as determined histochemically (Tables 1, 2, 3, 4, 8, and 9). For example, ED cells
exhibit carbonic anhydrase (CA) activity (Table 9); this
enzyme is involved in several physiological processes, including bicarbonate ion production, providing H⫹ and bicarbonate for other ions in transmembrane transport and
in the secretion of macromolecules. This enzyme may be
demonstrated by metal capture methods or by immunohistochemical methods; using immunohistochemical
methods, it has been possible to identify at least four
isozymes of carbonic anhydrase: CA-i, CA-II, CA-III, and
CA-VI (Table 9). Interestingly, there are significant species differences in the localization of the various carbonic
anhydrase isozymes. One species may be entirely devoid of
staining for an isozyme while other species may exhibit
staining for it. There are differences between staining
reactions in the different glands of the same species, and
519
Fig. 18. Submandibular: short-tailed leaf-nosed bat (Carollia perspicillata). A bundle of hypolemmal nerve terminals within the wall of an ED.
The varicosities contain both small clear synaptic vesicles and larger
dense-cored ones. The axons contain obvious neurotubules. Note the
relationship between the nerve bundle and the mitochondria in the
abutting cells. Magnification ⫽ 11,900⫻.
it is also of interest to note that in the EDs of some species
the columnar cells of stratified columnar or pseudostratified epithelia may be unstained but the basal cells will be
intensely stained, or both columnar cells and basal cells
are stained. For example, in the submandibular gland of
the guinea pig, the basal cells of the EDs are strongly
stained, whereas the columnar cells are negative to only
very faintly positive. In the horse parotid, sublingual, and
submandibular glands, intense activity of carbonic anhydrase III is seen in basal cells of EDs, but basal cells are
unstained for either carbonic anhydrase I or II. The possibility exists that basal cells function entirely differently
from columnar cells in terms of ionic transport.
Further evidence that EDs are involved in transport
phenomena is provided by immunohistochemical and histochemical examination of these duct segments for phosphatases. The most intensely studied phosphatase in ED
cells of salivary glands has been Na⫹,K⫹-adenosine
triphosphatase (Na⫹,K⫹-ATPase). This is a component of
the sodium pump and has been localized in sites of fluid
and ion transport. Na⫹,K⫹-ATPase activity has been localized in the basolateral plasma membranes of ED cells
in the cat parotid and sublingual glands (Winston et al.,
1990) and in the cat submandibular gland (Winston et al.,
520
TANDLER ET AL.
TABLE 9. Carbonic anhydrases (CA) in ED cells
Enzyme
Common name
Gland
References
Syrian hamster
guinea pig
human beings
horse
mouse
SM
SM
P,SM
P,SL,SM
SL
SM
P
SL
SM
Noda et al., 1986b
Noda et al., 1986b
Noda et al., 1986a, 1986c
Asari et al., 1991a
Hennigar et al., 1983
Hennigar et al., 1983; Noda et al., 1986b
Peagler et al., 1998; Asari et al., 1991b
Hennigar et al., 1983; Redman et al., 2000
Hennigar et al., 1983; Noda et al., 1986b; Ogawa et al., 1992;
Redman et al., 2000
P,SL,SM
P,SL
SM
SL,SM
SM
SL
SM
P
SM
Noda et al., 1986a, 1986b
Spicer et al., 1990
Noda et al., 1986b; Spicer et al., 1990
Asari et al., 1991a
Asari et al., 1989
Hennigar et al., 1983; Spicer et al., 1990
Hennigar et al., 1983; Noda et al., 1986b
Peagler et al., 1998
Noda et al., 1986b
P
SM
SL,SM
Asari et al., 1991b
Nishita et al., 1989
Spicer et al., 1990
SM
P,SL,SM
Asari et al., 1989, 1993
Asari et al., 1991a
P
SL,SM
Peagler et al., 1998
Redman et al., 2000
CA-I
rat
CA-II
human beings
guinea pig
horse
cow
mouse
rat
CA-III
rat
mouse
guinea pig
cow
horse
CA-VI
rat
P, parotid; SL, sublingual; SM, submandibular.
1990; Garrett et al., 1992), in human parotid, sublingual,
and submandibular glands (Winston et al., 1988), in
mouse parotid and sublingual glands (Winston et al.,
1988), in mouse submandibular glands (Sims-Sampson et
al., 1984; Winston et al., 1988; Kurihara et al., 1996), and
in the rat parotid, sublingual, and submandibular glands
(Winston et al., 1988). Na⫹,K⫹-ATPase has been studied
in the ED cells of the postnatally developing rat parotid
gland (Peagler and Redman, 1999). Another ATPase has
been localized primarily on the microvilli of ED cells of the
rat parotid and submandibular glands; this is an ectoATPase and may be identical to a membrane glycoprotein
called C-CAM 105 (Murphy et al., 1994). Two other phosphatases in ED cells are nucleoside diphosphatase, which
is found in what appears to be the area of the Golgi
complex in the cat parotid and submandibular glands, and
thiamine pyrophosphatase that is also localized in the
area of the Golgi complex in the cat submandibular gland
ED cells (Harrison, 1974). Clearly, Pinkstaff’s (1980) suggestion that “EDs do contribute in some way to the final
product of salivary gland secretion” is well founded.
In the broad view, the mammalian ED is variable in
terms of histology, histochemistry, and ultrastructure. Indeed, for this reason, it is impossible to describe a “typical”
ED. This circumstance is noteworthy because it raises an
evolutionary issue: is the absence of a conserved pattern
indicative of the adaptive importance of the ED, or is it
due to its relatively low functional importance?
We tested its potential adaptive importance by mapping
ED data on a phylogenetic tree. In this exercise, we did not
find patterns associated with diet, ecology, or evolutionary
lineage. Our interpretation is that species variation with
regard to EDs does not reflect “adaptive” responses involving this duct. Therefore, it seems possible that the variation in EDs is a reflection of the relative lack of evolutionary constraints or of selection pressures.
It is apparent that the ED differs from both SDs and
IDs. The latter two salivary gland ducts reflect evolutionary history and diet (Tandler et al., 1998c, 2001). For
instance, the ID in some bats varies according to hardbodied (chitinous) versus soft-bodied insects that constitute their diets (Tandler and Phillips, 1998). The ED data
for the same species do not exhibit any discernible patterns or differences associated with diet.
ACKNOWLEDGMENTS
The authors appreciate the professional assistance of
several colleagues who participated in fieldwork, confirmed species identification of voucher specimens, or
both. In particular, they thank Duane A. Schlitter, Stephen Williams, and Hugh H. Genoways. Toshikazu Nagato and Kuniaki Toyoshima participated in some of the
studies on which this review is based. Carol Ayala and
Thomas J. Slabe provided technical assistance for some
aspects of this work, which was supported in part by a
grant from the National Institute of Dental Research (to
B.T. and C.J.P.) and Hofstra University HCLAS grants (to
C.J.P.), as well as by financial support from the Texas
Tech University and Illinois State University Departments of Biological Sciences (to C.J.P.) and the Texas Tech
EXCRETORY DUCTS OF SALIVARY GLANDS
Institute of Environmental and Human Health (to B.T.).
This work is dedicated to the memory of Arnold Tamarin,
a pioneer in ultrastructural research on salivary glands
and a true friend.
LITERATURE CITED
Almgren O, Anden N-E, Jonason J, Norberg K-A, Olson L. 1966.
Cellular localization of monoamine oxidase in rat salivary glands.
Acta Physiol Scand 67:21–26.
Amano O, Tsuji T, Nakamura T, Iseki S. 1991. Expression of transforming growth factor ␤1 in the submandibular gland of the rat.
J Histochem Cytochem 39:1707–1711.
Amano O, Yoshitake Y, Nishikawa K, Iseki S. 1993. Basic fibroblast
growth factor in rat salivary glands. Cell Tissue Res 273:467– 474.
Archer FL, Kao VCY. 1968. Immunohistochemical identification of
actomyosin in myoepithelium of human tissues. Lab Invest 18:669 –
674.
Arnold WH. 1984. Comparative studies on the localization of esteroproteases and kallikrein-like activity in primate organs. Histochem
J 16:755–769.
Arnold WH. 1985. Vergleichende histochemische Untersuchungen zur
Lokalisation von Esteroproteasen und Enzymen mit kallikreinähnlicher Aktivität in Speicheldrüsen von Ratten und Affen. Acta Histochem 31(Suppl):211–219.
Arvy L 1963. Comparative histoenzymology of the salivary glands.
Ann NY Acad Sci 106:472– 492.
Asari M, Sasaki K, Kano Y, Nishita T. 1989. Immunohistochemical
localization of carbonic anhydrase isozymes I, II and III in the
bovine salivary glands and stomach. Acta Histol Cytol 52:337–344.
Asari M, Sasaki K, Kano Y, Nishita T. 1991a. Immunohistolocalization of the carbonic anhydrase isozymes I, II and III in equine
salivary glands. Okajimas Folia Anat Jpn 67:467– 472.
Asari M, Igarashi S-I, Sasaki K, Amasaki T, Nishita T, Amasaki H.
1991b. Immunocytochemical localisation of the carbonic anhydrase
III in the rat parotid gland. J Anat 179:9 –14.
Asari M, Sasaki K, Igarashi S, Amasaki T, Wakui S, Kano Y, Nishita
T. 1993. Distribution of carbonic anhydrase isozyme III (CA-III)positive cells in duct segments of the bovine submandibular gland.
Acta Histochem 94:67–72.
Ayer-Le Lievre C, Ebendal T, Olson L, Seiger Å, Persson H. 1989.
Detection of nerve growth factor and its mRNA by separate and
combined immunohistochemistry and in situ hybridization in
mouse salivary glands. Histochem J 21:1–7.
Azzali G, Romita G, Gatti R. 1986. Fine struttura ed aspetti stagionali
della ghiandola parotide. Arch Ital Anat Embriol 91:257–300.
Azzali G, Bucci G, Gatti R, Orlandini G, Ferrari G. 1989. Fine structure of the excretory system of the deep posterior (Ebner’s) salivary
glands of the human tongue. Acta Anat 136:257–268.
Batsakis JG. 1980. Salivary gland neoplasia: an outcome of modified
morphogenesis and cytodifferentiation. Oral Surg Oral Med Oral
Pathol 49:229 –232.
Batsakis JG, Kraemer B, Sciubba J. 1983. The pathology of head and
neck tumors: the myoepithelial cell and its participation in salivary
gland neoplasia, part 17. Head Neck Surg 5:222–233.
Bläuer M, Wichmann L, Punnonen R, Tuohimaa P. 1996. Measurement of activin B in human saliva and localization of activin subunits in rat salivary glands. Biochem Biophys Res Commmun 222:
230 –235.
Bogart BI. 1970. The effect of aging on the rat submandibular gland:
an ultrastructural, cytochemical and biochemical study. J Morphol
130:337–351.
Booth WD, Polge C. 1976. The occurrence of C19 steroids in testicular
tissue and submaxillary glands of intersex pigs in relation to morphological characteristics. J Reprod Fert 46:115–121.
Born IA, Schwechheimer K, Maier H, Otto HF. 1987. Cytokeratin
expression in normal salivary glands and in cystadenolymphomas
demonstrated by monoclonal antibodies against selective cytokeratin polypeptides. Virch Arch A 411:583–589.
Boshell JL, Wilborn WH. 1983. Differences in the ultrastructure of
the submandibular glands of baboon and Rhesus monkey revealed
by the use of different fixatives. Cell Tissue Res 231:655– 661.
521
Brocco SL, Tamarin A. 1979. The topography of rat submandibular
gland parenchyma as observed with S.E.M. Anat Rec 194:445– 460.
Burns BF, Dardick I, Parks WR. 1988. Intermediate filament expression in normal parotid glands and pleomorphic adenomas. Virch
Arch A Pathol Anat Histopathol 413:103–112.
Burstone MS. 1959. New histochemical techniques for the demonstration of tissue oxidase (cytochrome oxidase). J Histochem Cytochem
7:112–122.
Caselitz J, Osborn M, Seifert G, Weber K. 1981a. Intermediate-sized
filament proteins (prekeratin, vimentin, desmin) in the normal
parotid gland and parotid gland tumours: immunofluorescence
study. Virch Arch Pathol Anat 393:273–286.
Caselitz J, Löning T, Staquet MJ, Seifert G, Thivolet J. 1981b. Immunocytochemical demonstration of filamentous structures in the
parotid gland: occurrence of keratin and actin in normal and tumoral parotid gland with special respect to the myoepithelial cells.
J Cancer Res Clin Oncol 100:59 – 68.
Caselitz J, Walther B, Wustrow J, Seifert G, Weber K, Osborn M.
1986. A monoclonal antibody that detects myoepithelial cells in
exocrine glands, basal cells in other epithelia and basal and suprabasal cells in certain hyperplastic tissues. Virch Arch (Pathol Anat)
409:725–738.
Chaudhry AP, Cutler LS, Yamane GM, Labay GR, Sunderraj M,
Manak JR Jr. 1987. Ultrastructure of normal human parotid gland
with special emphasis on myoepithelial distribution. J Anat 152:1–
11.
Chauncey HH, Quintarelli G. 1959. Histochemical localization of hydrolytic enzymes in human salivary glands. J Dent Res 38:961–968.
Chauncey HH, Quintarelli G. 1961. Localization of acid phosphatase,
nonspecific esterases and ␤-D-galactosidase in parotid and submaxillary glands of domestic and laboratory animals. Am J Anat 108:
263–293.
Chomette G, Auriol M, Vaillant JM, Bertrand JC, Chenal C. 1981.
Effects of irradiation on the submandibular gland of the rat: an
enzyme histochemical and ultrastructural study. Virch Arch Pathol
Anat 391:291–299.
Cossu M, Perra MT, Piludu M, Lantini MS. 2000. Subcellular localization of epidermal growth factor in human submandibular gland.
Histochem J 32:291–294.
Dairkee SH, Blayney C, Smith HS, Hackett A. 1985. Monoclonal
antibody that defines human myoepithelium. Proc Natl Acad Sci
USA 82:7409 –7413.
Dardick I, van Nostrand AW. 1985. Myoepitheliual cells in salivary
gland tumors: revisited. Head Neck Surg 7:395– 408.
Dardick I, Rippstein P, Skimming L, Boivin M, Dairkee SH. 1987.
Immunohistochemistry and ultrastructure of myoepithelium and
modified myoepithelium of the ducts of human major salivary
glands: histogenetic implications for salivary gland tumors. Oral
Surg Oral Med Oral Pathol 64:703–715.
Dardick I, Parks WR, Little J, Brown DL. 1988. Characterization of
cytoskeletal proteins in basal cells of human parotid salivary gland
ducts. Virch Arch A 412:525–532.
Dardick I, Byard RW, Carnegie JA. 1990. A review of the proliferative
capacity of major salivary glands and the relationship to current
concepts of neoplasia in salivary glands. Oral Surg Oral Med Oral
Pathol 69:53– 67.
Dardick I, Stratis M, Parks WR, DeNardi FG, Kahn HJ. 1991. S-100
protein antibodies do not label normal salivary gland myoepithelium. Am J Pathol 138:619 – 628.
Dardick I. 1998. Mounting evidence against current histogenic concepts for salivary gland tumorigenesis. Eur J Morphol 36(Suppl):
257–261.
Dietl T, Kruck J, Fritz H. 1978. Localization of kallikrein in porcine
pancreas and submandibular gland as revealed by the indirect
immunofluorescence technique. Hoppe-Seyler’s Z Physiol Chem
359:499 –505.
DiSanto PE. 1960. Anatomy and histochemistry of the salivary glands
of the vampire bat, Desmodus rotundus. J Morphol 106:301–336.
Dix V. 1969. Histologische und histochemische Untersuchungen an
der grosse Speicheldrüsen von Lepus europaeus Pallas, Oryctolagus
cuniculus (L.), Myocastor coypus (Molina) und Cavia cobaya (Maregr.). Z Wissenschaft Zool 178:316 –347.
522
TANDLER ET AL.
Domon M, Kurabayashi T. 1987. Postnatal development of the duct
system in the mouse parotid gland. Anat Rec 217:391–394.
Drenckhahn P, Groschel-Stewart U, Unsicker K. 1977. Immunofluorescence-microscopic demonstration of myosin and actin in salivary
glands and exocrine pancreas of the cat. Cell Tissue Res 183:273–
279.
Durban EM, Barreto PD, Hilgers J, Sonnenberg A. 1994. Cell phenotypes and differentiative transitions in mouse submandibular salivary gland defined with monoclonalantibodies to mammary epithelial cells. J Histochem Cytochem 42:185–196.
Fava-de-Moraes F, Ximinez I, Radtke B, Junqueira LCU. 1966. Morphological and chemical studies on the salivary glands and pancreas of two species of Pinnipedia. Ann Histochim 11:199 –212.
Ferguson MM. 1967. Utilization of 11␤-hydroxysteroids by the salivary gland ducts. Histochemie 9:269 –274.
Flood PF. 1973. Histochemical localization of hydroxysteroid dehydrogenases in the maxillary glands of pigs. J Reprod Fert 32:125–127.
Fujiwara M, Tanaka C, Hikosaka H, Okegawa T. 1966. Cytological
localization of noradrenaline, monoamine oxidase and acetylcholinesterase in salivary glands of dog. J Histochem Cytochem 14:
483– 490.
Gargiulo AM, Ceccarelli P, Pedini V. 1996. The presence of granular
excretory ducts in the rabbit zygomatic gland. Anat Histol Embryol
25:175–176.
Garrett JR. 1976. Structure and innervation of salivary glands. In:
Cohen B, Kramer IRH, editors. Scientic foundations of dentistry.
London: Heineman. p 499 –516.
Garrett JR, Kidd A, Kyriacou K, Smith RE. 1985. Use of different
derivatives of D-Val-Leu-Arg for studying kallikrein activities in cat
submandibular glands and saliva. Histochem J 17:805– 818.
Garrett JR, Anderson LC. 1991. Rat sublingual salivary glands: secretory changes on parasympathetic or sympathetic nerve stimulation and a reappraisal of the adrenergic innervation of striated
ducts. Arch Oral Biol 36:675– 683.
Garrett JR, Winston DC, Proctor GB, Schulte BA. 1992. Na,K-ATPase
in resting and stimulated submandibular salivary glands in cats,
studied by means of ouabain-sensitive K⫹-dependent p-nitrophenylphosphatase activity. Arch Oral Biol 37:711–716.
Garrett JR, Kidd A. 1993. The innervation of salivary glands as
revealed by morphological methods. Microscopy Res Tech 26:75–91.
Geiger S, Geiger B, Leitner O, Marshak G. 1987. Cytokeratin polypeptides expression in different epithelial elements of human salivary
glands. Virch Arch A 410:403– 414.
Gillett CE, Bobrow LG, Millis RR. 1990. S100 protein in human
mammary tissue: immunoreactivity in breast carcinoma, including
Paget’s disease of the nipple, and value as a marker of myoepithelial cells. J Pathol 160:19 –24.
Gnepp DR. 1983. Sebaceous neoplasms of salivary gland origin: a
review. Pathol Annu 18:71–102.
Gresik EW, Barka T. 1983. Epidermal growth factor, renin, and
protease in hormonally responsive duct cells of the mouse sublingual gland. Anat Rec 206:169 –175.
Gresik EW. 1994. The granular convoluted tubule (GCT) cell of rodent
submandibular glands. Microscopy Res Tech 27:1–24.
Gugliotta P, Sapino A, Macrı́ L, Salli O, Gabbiani G, Bussolati G.
1988. Specific demonstration of myoepithelial cells by anti-alpha
smooth muscle actin antibody. J Histochem Cytochem 36:659 – 663.
Gurusinghe CJ, Birtles MJ. 1985. Light microscopic observations of
an intraepithelial granular cell type in the bovine parotid gland.
Acta Anat 124:122–126.
Gustafsson H, Kjörell U, Eriksson A, Virtanen I, Thornell L-E. 1988.
Distribution of intermediate filament proteins in developing and
adult salivary glands in man. Anat Embryol 178:243–251.
Gustafsson H, Bergman F, Virtanen I, Thornell L-E. 1989. Myoepithelial cells in salivary gland neoplasms. Acta Phathol Microbiol
Immunol Scand 97:49 –55.
Gutierrez Marin MS, Galera H, Bullón P. 1990. Effects of treatment
with noradrenaline and isoproterenol on the excretory portion of the
submaxillary gland in the rat: an ultrastructural study. Acta Anat
137:324 –330.
Gutkowska J, Thibault G, Cantin M, Garcia R, Genest J. 1983. Kallikrein concentration in submandibular glands of rats chronically
treated with isoproterenol. Can J Physiol Pharmacol 61:449 – 456.
Hamakawa H, Sumida T, Bao Y, Tanioka H, Sogawa K, Yamada T.
1999. Species specificity of cytokeratin polypeptide expression in
the submandibular gland. Cell Mol Biol 45:265–276.
Hanker JS, Preece JW, Burkes EJ Jr, Romanovicz. 1977. Catalase in
salivary gland striated and excretory duct cells. I. The distribution
of cytoplasmic and particulate catalase and the presence of catalase-positive rods. Histochem J 9:711–728.
Harrison JD. 1974. Salivary glands of the cat: a histochemical study.
Histochem J 6:649 – 664.
Hennigar RA, Schulte BA, Spicer SS. 1983. Immunolocalization of
carbonic anhydrase isozymes in rat and mouse salivary and exorbital lacrimal glands. Anat Rec 207:605– 614.
Higashi K, Sasa S. 1985. Fine structure of primary cilia in the basal
cells of main excretory ducts of rat submandibular glands. Jpn
J Oral Biol 27:842– 850.
Higashi K, Akimoto K, Sasa S. 1994. Fine structure of primary cilia in
the basal cells of main excretory ducts of hamster submandibular
glands. Jpn J Oral Biol 36:299 –305.
Hill CR, Bourne GH. 1954. The histochemistry and cytology of the
salivary gland duct cells. Acta Anat 20:116 –128.
Höfer D, Püschel B, Drenkhahn D. 1996. Taste receptor-like cells in
the gut identified by expression of ␣-gustducin. Proc Nat Acad Sci
USA 93:6631– 6634.
Hosaka M, Tatemoto Y, Yamagami T, Hikosaka N, Mori M. 1985.
Immunohistochemical evaluation of different filament proteins in
human salivary glands. Acta Histochem Cytochem 18:505–514.
Høyer PE, Møller M. 1977. Histochemistry of 11␤-hydroxysteroid
dehydrogenase in rat submandibular gland: effect of cortisol stimulation. Histochem J 9:599 – 618.
Ikematsu Y, Pour PM, Kazakoff K. 1997. Species differences in the
expression of transforming growth factor-alpha (TGF-␣) in the submandibular gland and pancreas. Int J Pancreatol 22:111–119.
Imai M, Mineda T, Oikawa M, Okano T. 1978. Investigation on
glycogen in the salivary glands of man and many kinds of animals.
Aichi-Gakuin J Dent Sci 16:37–131.
Isacsson G, Lundquist PG. 1982. Salivary calculi as an aetological
factor in chronic sialadenitis of the submandibular gland. Clin
Otolaryngol 7:231–236.
Jacob S, Poddar S. 1989. Ultrastructure of the ferret sublingual gland.
Acta Anat 135:344 –346.
Ježek D, Banek L, Banek T. 1996. Effects of orchiechtomy on the rat
parotid gland: an ultrastructural and stereological study. Acta Anat
155:172–183.
Kawakatsu K, Mori M, Fujita K, Fukuda M, Kawagoe T. 1959a.
Histochemical studies of normal salivary glands: II, distribution
and localization of esterase in the salivary glands of experimental
animals. J Osaka Univ Dent Soc 4:439 – 454.
Kawakatsu K, Mori M, Fukuda M, Fujita K, Hoshi N. 1959b. Histochemical studies of normal salivary glands: I, distribution and
localization of succinic dehydrogenase in human salivary gland and
experimental animals. J Osaka Univ Dent Soc 4:421– 438.
Kawakatsu K, Mori M, Fujita K, Fukuda M, Deguchi S. 1960. Histochemical studies of salivary glands: VI, histochemical demonstration of ␤-glucuronidase, ␤-galactosidase and ␤-glucosidase in normal salivary glands. Arch Histol Jpn 19:533–546.
Kawakatsu K, Mizushima T, Ohmachi K. 1961. Histochemical studies
of normal salivary glands: VIII, histochemical localization of monoamine oxidase activity. J Osaka Univ Dent Sch 1:9 –14.
Kawakatsu K, Mori M. 1962. Histochemical study of enzyme patterns
in the human submaxillary gland. Histochemie 2:393– 401.
Kawakatsu K, Mori M, Mizushima T, Koizumi H. 1962. Histochemical
studies of normal salivary glands: IX, histochemical localization of
succinic dehydrogenase and triphosphopyridine nucleotide diaphorase activity. Z Zellforsch 56:641– 648.
Kawakatsu K, Mori M, Mizushima T, Makino H. 1964a. Histochemical demonstration of oxidative enzymes in human salivary glands.
Arch Histol Jpn 24:247–256.
EXCRETORY DUCTS OF SALIVARY GLANDS
Kawakatsu K, Mori M, Mizushima T, Makino H. 1964b. Histochemical localization of cytochrome oxidase in salivary glands. Arch
Histol Jpn 24:427– 433.
Kimura K, Moriya H. 1984. Enzyme- and immuno-histochemical localization of kallikrein: I, the human parotid gland. Histochemistry
80:367–372.
Kimura K, Moriya H. 1986. Localization of kallikrein in the human
parotid gland and in the human kidney: a comparative study of
immunohistochemistry and enzyme histochemistry. Adv Exp Med
Biol 198A:27–34.
Komiya T, Fukushima M. 1991. Postnatal growth and differentiation
of the salivary gland. Acta Med Biol 39:129 –140.
Kurashima C. 1983. Histopathological studies on crystalloids in ducts
of human parotid glands. Kokyubo Gakkai Zasshi 50:212–225.
Kurihara K, Maruyama S, Hosoi K, Sato S, Ueha T, Gresik EW. 1996.
Regulation of Na⫹,K⫹-ATPase in submandibular glands of hypophysectomized male mice by steroid and thyroid hormones. J Histochem Cytochem 44:703–711.
Lantini MS, Proto E, Puxeddu P, Riva A, Testa Riva F. 1990. Fine
structure of excretory ducts of human salivary glands. J Submicrosc
Cytol Pathol 22:465– 475.
Lee S-K, Lim CY, Chi JG, Yamada K, Hashimura K, Kunikata M,
Mori M. 1990. Prenatal development of human major salivary
glands and immunohistochemical detection of keratins using monoclonal antibodies. Acta Histochem 89:213–235.
Leeson CR. 1969. The fine structure of the parotid gland of the spider
monkey (Ateles paniscus). Acta Anat 72:133–147.
Lexow U, Grossarth C, von Deimling O. 1979. Histochemical demonstration of mouse submandibular esteroproteases with a new chromogenic substrate. Histochemistry 60:327–334.
Liu Y-H, Fujitani N, Koda Y, Kimura H. 1998. Distribution of H type
1 and H type 2 antigens of ABO blood group in different cells of
human submandibular gland. J Histochem Cytochem 46:69 –76.
Lorber M. 1991. Branchings and course of the larger ducts and accompanying structures within the rat submandibular salivary
gland. Am J Anat 190:133–156.
Lorber M. 1992. Elastic fibers in the duct system of the rat submandibular salivary gland. Anat Rec 234:335–337.
Maeda K, Sueishi K. 1989. A monoclonal antibody that defines basal
cells of stratified epithelia in various human and rabbit tissues.
Histochemistry 92:319 –324.
Mansouri SH, Atri A. 1994. Ultrastructure of parotid and mandibular
glands of camel (Camelus dromedarius). J Appl Anim Res 6:131–
141.
Maranda B, Rodrigues JAA, Schachter M, Shnitka TK, Weinberg J.
1978. Studies on kallikrein in the duct system of the salivary glands
of the cat. J Physiol 276:321–328.
Marshak G, Leitner O. 1987. Cytokeratin polypeptides in normal and
metaplastic human salivary gland epithelia. J Oral Pathol 16:442–
449.
Marshak G, Leitner O, Geiger B. 1987. Cytokeratin polypeptide expression during the histogenesis of guinea pig submandibular salivary gland. Development 100:699 –711.
Martinez JR, Holzgreve H, Frick A. 1966. Micropuncture study of
submaxillary glands of adult rats. Pflügers Arch 290:124 –133.
Martinez JR. 1987. Ion transport and water movement. J Dent Res
66:638 – 647.
Martinez-Madrigal F, Micheau C. 1989. Histology of the major salivary glands. Am J Surg Pathol 13:879 – 899.
Matsunaga S. 1992. Light and electron microscopic and histochemical
studies on the major salivary glands of the Siberian weasel (Carnivora). Aichi-Gakuin J Dent Sci 30:241–272.
Matthews JB, Mason GI, Lawrence GM. 1992. Epithelial expression
of major histocompatibility complex (MHC) antigens in normal rat
salivary and lacrimal glands. Arch Oral Biol 37:93–97.
Maximuk YA, Shertyuk OA. 1990. Structural-spatial organization of
epithelial components in the palatal glands of newborns and persons of mature age. Arkh Anat Gistol Embriol 99:92–96.
Menghi G, Bondi AM, Accili D, Fumagalli L. 1989. Ultrastructure and
complex carbohydrate ultracytochemistry of the cat parotid gland.
Biol Struct Morphogen 2:149 –158.
523
Meyer W, Beyer C, Wissdorf H. 1993. Lectin histochemistry of salivary glands in the giant ant-eater (Myrmecophaga tridactyla). Histol Histopathol 8:305–316.
Mira E, Gerzeli G, De Piceis Polver P, Vidi I. 1971. Histofunctional
changes in isoproterenol enlarged submaxillary glands of adult
male rats. Acta Anat 80:235–249.
Miraglia T, Santana Moura C, Batista Neves H. 1974. Histochemical
data on the parotid glands of the marmosets, Callithrix jacchus and
Callithrix penicillata. Acta Anat 87:334 –344.
Möller AC, Hellmén E. 1994. S100 protein is not specific for myoepithelial cells in the canine mammary gland. J Comp Pathol 110:49 –
55.
Mori M, Mizushima T. 1965. Histochemical localization of cytochrome
oxidase in salivary glands. J Dent Res 44:825.
Mori M, Takai Y, Hosaka M, Hikosaka N. 1985a. Vimentin characteristically exists in granular convoluted tubules of hamster submandibular glands: immunohistochemical studies on comparative
localization of filament proteins in salivary gland ducts. Acta Histochem Cytochem 18:147–155.
Mori M, Murase N, Hyun KH, Sumitomo S, Kawamura K. 1985b.
Immunohistochemical studies of keratin distribution in salivary
gland tumors. Acta Histochem Cytochem 18:21–32.
Mori M, Ninomiya T, Okada Y, Tsukitani K. 1989. Myoepitheliomas
and myoepithelial adenomas of salivary gland origin: immunohistochemical evaluation of filament proteins, S-100 ␣. and ␤, glial
fibrillary acidic proteins, neuron-specific enolase, and lactoferrin.
Pathol Res Pract 184:168 –178.
Mori M. 1991. Histochemistry of the salivary glands. Boca Raton, LA:
CRC Press. p 1– 67.
Mori M, Takai Y, Sumitomo S. 1992a. Salivary gland tumors: a
possible origin of modified myoepithelial cells is ductal basal cells.
Cancer J 5:316 –320.
Mori M, Huang JW, Yamada K, Isono K, Shinohara M, Harada T, Oka
K, Tsubura A, Morii S, Hilgers J. 1992b. Immunohistochemical
characteristics of polymorphic epithelial mucin in mucoepidermoid
carcinoma of salivary glands using MAM-3 and MAM-6 antigens.
Acta Histochem Cytochem 25:473– 482.
Munhoz COG. 1971. Histochemical classification of acini and ducts of
parotid glands from Artiodactyles, Carnivores and Rodents. Acta
Histochem 39:302–317.
Murphy HC, Hand AR, Dowd FJ. 1994. Localization of an ectoATPase/cell-CAM 105 (C-CAM) in the rat parotid and submandibular glands. J Histochem Cytochem 42:561–568.
Nagato, T, Ren X-Z, Toh H, Tandler B. 1997. Ultrastructure of Weber’s salivary glands of the root of the tongue in the rat. Anat Rec
249:435– 440.
Nagato T, Tandler B, Phillips CJ. 1998. An unusual parotid gland in
the tent-building bat, Uroderma bilobatum: possible correlation of
interspecific ultrastructural differences with differences in salivary
pH and buffering capacity. Anat Rec 252:290 –300.
Nair PNR, Schroeder HE. 1985. Architecture of associations of minor
salivary gland ducts and lymphoid follicles in Macaca fascicularis:
an ultrastructural study. Cell Tissue Res 240:223–232.
Nakai M, Tsukitani K, Tatemoto Y, Hikosaka N, Mori M. 1985.
Histochemical studies of obstructive adenitis in human submandibular salivary glands: II, lectin binding and keratin distribution in
the lesions. J Oral Pathol 14:671– 679.
Nawar SM, El-Khaligi GE. 1975. Morphological micromorphological
and histochemical studies on the parotid salivary glands of the
one-humped camel (Camelus dromedaries), Gegenbauers Morphol
Jahr 121:430 – 449.
Nikai H, El-Bardaie AM, Takata T, Ogawa I, Ijuhin N. 1986. Histological evaluation of myoepithelial participation in salivary gland
tumors. Int J Oral Maxillofac Surg 15:597– 605.
Nilsen R, Donath K. 1981. Actin containing cells in normal human
salivary glands: an immunohistochemical study. Virch Arch Pathol
Anat 391:315–322.
Nishita T, Oshige H, Matsushita H, Kano Y, Asari M. 1989. The
immunohistolocalization of carbonic anhydrase III in the submandibular gland of rats and hamsters. Histochem J 21:8 –14.
Noda Y, Sumitomo S, Hikosaka N, Mori M. 1986a. Immunohistochemical observations on carbonic anhydrase I and II in human salivary
524
TANDLER ET AL.
glands and submandibular obstructive adenitis. J Oral Pathol 15:
187–190.
Noda Y, Sumitomo S, Orito T, Mori M. 1986b. Immunohistochemical
localization of carbonic anhydrase I and II in submandibular salivary glands of the mouse, rat, hamster and guinea pig. Arch Oral
Biol 31:795– 800.
Noda Y, Takai Y, Iwa Y, Meenaghan MA, Mori M. 1986c. Immunohistochemical study of carbonic anhydrase in mixed tumours from
major salivary glands and skin. Virch Arch (Pathol Anat) 408:449 –
459.
Norberg L, Dardick I, Leung R, Burford-Mason AP, Rippstein P. 1992.
Immunogold localization of actin and cytokeratin filaments in myoepithelium of human parotid salivary gland. Ultrastruct Pathol
16:555–568.
Ogawa Y, Chang C-K, Kuwahara H, Hong S-S, Toyosawa S, Yagi T.
1992. Immunoelectron microscopy of carbonic anhydrase isozyme
VI in rat submandibular gland: comparison with isozymes I and II.
J Histochem Cytochem 40:807– 817.
Ogawa C, Iwatsuki H, Sasaki K, Kumano I. 2001. Keratin filaments in
epithelial cells of the excretory ducts of rabbit submandibular
glands: an immunohistochemical and ultraimmunohistochemical
study. Kaibogaku Zasshi 76:389 –398.
Ogbureke KUE, MacDaniel RK, Jacob RS, Durban EM. 1995. Distribution of immunoreactive transforming growth factor-alpha in nonneoplastic human salivary glands. Histol Histopathol 10:691– 696.
Ørstavik TB, Brandtzaeg P, Nustad K, Halvorsen KM. 1975. Cellular
localization of kallikreins in rat submandibular and sublingual
salivary glands. Acta Histochem 54:183–192.
Ørstavik TB, Brandtzaeg P, Nustad K, Pierce JV. 1980. Immunohistochemical localization of kallikrein in human pancreas and salivary glands. J Histochem Cytochem 28:557–562.
Pal C, Chandra G. 1979. Histochemistry of mucins in the submaxillary salivary gland of buffalo (Bubalus bubalis). Acta Anat 103:
336 –343.
Pallesen G, Nielsen S, Celis JE. 1987. Characterization of a monoclonal antibody (BG3C8) that reacts with basal cells of stratified epithelia. Histopathology 11:591– 601.
Palmer RM, Lucas RB, Knight J, Gusterson B. 1985. Immunocytochemical identification of cell types in pleomorphic adenoma, with
particular reference to myoepithelial cells. J Pathol 146:213–220.
Palmer RM. 1986. The identification of myoepithelial cells in human
salivary glands: a review and comparison of light microscopical
methods. J Oral Pathol 15:221–229.
Pardini LC, Taga R. 1996. Stereological study of the sexual dimorphism in mouse submandibular glands. Okajimas Fol Anat Jpn
73:119 –124.
Paz Ossorio R, Gonzalez Gonzalez G, Peyro A. 1975. Observaciones
sobre la ultraestructura de la glandula submandibular en la especie
humana. An Esp Odontestomatol 34:457– 480.
Peagler FD, Redman RS, McNutt RL, Kruse DH, Johansson I. 1998.
Enzyme histochemical and immunohistochemical localization of
carbonic anhydrase as a marker of ductal differentiation in the
developing rat parotid gland. Anat Rec 250:190 –198.
Peagler FD, Redman RS. 1999. Enzyme histochemical localization of
Na⫹,K⫹-ATPase and NADH-DE in the developing rat parotid
gland. Anat Rec 256:72–77.
Penschow JD, Coghlan JP. 1993. Secretion of glandular kallikrein and
renin from the basolateral pole of mouse submandibular duct cells:
an immunocytochemical study. J Histochem Cytochem 41:95–103.
Phang YC, Rannie I. 1982. Oxytalan and elastic fibres in human
salivary glands: a light microscopy study. Austral Dent J 27:288 –
290.
Phillips CJ, Grimes GW, Forman GL. 1977. Oral biology. In: Baker
RJ, Jones JK Jr, Carter DC, editors. Biology of bats of the New
World family Phyllostomatidae, part II. Lubbock, Texas Tech University Press, p 121–246.
Phillips CJ. 1985. Field fixation and storage of museum tissue collections suitable for electron microscopy. Acta Zool Fennica 170:87–90.
Phillips CJ. 1996. Cells, molecules, and adaptive radiation in mammals. In: Baker RJ, Genoways HH, editors. Contributions in
mammalogy: a memorial volume honoring Dr. J. Knox Jones, Jr.
Lubbock, TX: Museum of Texas Tech University. p 1–24.
Phillips CJ, Tandler B. 1996. Salivary glands, cellular evolution, and
adaptive radiation in mammals. Eur J Morphol 34:155–161.
Phillips CJ, Weiss A, Tandler B. 1998. Plasticity and patterns of
evolution in mammalian salivary glands: comparative immunohistochemistry of lysozyme in bats. Eur J Morphol 36(Suppl):123–127.
Pinkstaff CA. 1972. Sexual dimorphism of the miniature pig submandibular glands. Am J Anat 135:371–379.
Pinkstaff CA. 1980. The cytology of salivary glands. Int Rev Cytol
63:141–261.
Pinkstaff CA, Tandler B, Cohan RP. 1982. Histology and histochemistry of the parotid and the principal and accessory submandibular
glands of the little brown bat. J Morphol 172:271–285.
Pinkstaff CA. 1993. Cytology, histology, and histochemistry of salivary glands: an overview. In: Dobrosielski-Vergona K, editor. Biology of the salivary glands. Boca Raton, LA: CRC Press. p 15–38.
Poddar S, Jacob S. 1977. Gross and microscopic anatomy of the major
salivary glands of the ferret. Acta Anat 98:434 – 443.
Poddar S, Jacob S. 1978. Histology and mucosubstance histochemistry of mongoose salivary glands. Acta Anat 100:545–556.
Poddar S, Jacob S. 1979. Histology and mucosubstance histochemistry of ferret lingual glands. Acta Anat 105:65–74.
Quintarelli G. 1963. Histochemical identification of salivary mucins.
Ann NY Acad Sci 106:339 –363.
Quintarelli G, Dellovo MC. 1969. Studies on the exocrine secretions:
histochemical investigations on the major salivary glands of exotic
animals. Histochemie 19:199 –223.
Redman RS. 1995. Proliferative activity by cell type in the developing
rat parotid gland. Anat Rec 241:529 –540.
Redman RS, Peagler FD, Johansson I. 2000. Immunohistochemical
localization of carbonic anhydrases I, II, and VI in the developing
rat sublingual and submandibular glands. Anat Rec 258:269 –276.
Regezi JA, Batsakis JG. 1977. Histogenesis of salivary gland neoplasms. Otolaryngol Clin North Am 10:297–307.
Riva A, Tandler B, Testa Riva F. 1988. Ultrastructural observations
on the human sublingual gland. Am J Anat 181:385–392.
Riva A, Lantini MS, Testa Riva F. 1990. Normal human salivary
glands. In: Riva A, Motta PM, editors. Ultrastructure of the extraparietal glands of the digestive tract. Boston: Kluwer Academic.
p 53–74.
Riva A. 1992. Microstruttura delle ghiandole salivari dell’uomo. Atti
Soc Ital Anat 97(Suppl):13– 49.
Riva A, Serra GP, Proto E, Faa G, Puxeddu R, Testa Riva F. 1992. The
myoepithelial and basal cells of ducts of human major salivary
glands: a SEM study. Arch Histol Cytol 55(Suppl):115–124.
Riva A, Valentino L, Lantini MS, Floris A, Testa Riva F. 1993. 3Dstructure of cells of human salivary glands as seen by SEM. Microscopy Res Tech 26:5–20.
Riva A, Tandler B. 2000. Three-dimensional structure of oncocyte
mitochondria in human salivary glands: a scanning electron microscope study. Ultrastruct Pathol 24:145–150.
Rossoni RB, Machado CRS, Machado ABM. 1981. Autonomic innervation of salivary glands in the armadillo, anteater, and sloth
(Edentata). J Morphol 168:151–157.
Rutenburg AM, Rutenburg SH, Monis B, Teague R, Seligman AM.
1958. Histochemical demonstration of ␤-D-galactosidase in the rat.
J Histochem Cytochem 6:122–129.
Sahasrabudhe KS, Kimball JR, Morton TH, Weinberg A, Dale BA.
2000. Expression of the antimicrobial peptide, human ␤-defensin 1,
in duct cells of minor salivary glands and detection in saliva. J Dent
Res 79:1669 –1674.
Sakabe K, Seiki K, Fujii-Hanamoto H, Kawashima I. 1988. Progestin
and estrogen receptors: characterization and localization in rat
submandibular glands, with special reference to epidermal growth
factor. Endocrinol Jpn 35:709 –723.
Sato A, Miyoshi S. 1997. Fine structure of tuft cells of the main
excretory duct epithelium in the rat submandibular gland. Anat Rec
248:325–331.
Sato A, Miyoshi S. 1998. Topographical distribution of cells in the rat
submandibular gland duct system with special reference to dark
cells and tuft cells. Anat Rec 252:159 –164.
Sato A, Miyoshi S. 1999. Simple method to isolate the intact duct
system of the rat submandibular gland. Anat Rec 254:74 –75.
EXCRETORY DUCTS OF SALIVARY GLANDS
Schachter M, Maranda B, Moriwaki C. 1978. Localization of kallikrein in the coagulating and submandibular glands of the guinea
pig. J Histochem Cytochem 26:318 –321.
Schneyer LH, Young JA, Schneyer CA. 1972. Salivary secretion of
electrolytes. Physiol Rev 52:720 –777.
Schneyer LH. 1976. Sympathetic control of Na, K transport in perfused submaxillary main duct of rat. Am J Physiol 230:341–345.
Scott J. 1977. A morphometric study of age changes in the histology of
the ducts of human submandibular salivary glands. Arch Oral Biol
22:243–249.
Scott J. 1978. The prevalence of consolidated salivary deposits in the
small ducts of human submandibular glands. J Oral Pathol 7:221–
227.
Scott J. 1988. Structural age changes in salivary glands. In: Ferguson
DB, editor. Frontiers in oral physiology, vol. 6. Basel: Karger. p
40 – 62.
Shackleford JM, Klapper CE. 1962. Structure and carbohydrate histochemistry of mammalian salivary glands. Am J Anat 111:25– 48.
Shackleford JM. 1963a. The salivary glands and the salivary bladder
of the nine-banded armadillo. Anat Rec 145:513–520.
Shackleford JM. 1963b. Histochemical comparison of mucous secretions in rodent, carnivore, ungulate, and primate major salivary
glands. Ann NY Acad Sci 106:572–582.
Shapiro BL. 1967. A morphologic and histochemical study of three
oxidative enzymes in the hamster submandibular gland. Arch Oral
Biol 12:1053–1061.
Shiba R, Hamada T, Kawakatsu K. 1972. Histochemical and electron
microscopical studies on the effect of duct ligation of rat salivary
glands. Arch Oral Biol 17:299 –309.
Shinohara H, Yamada K, Tanaka T, Meenaghan MA, Takai Y, Mori
M. 1989. Monoclonal antibody to keratin K8.12 expression in ductal
basal cells of obstructive lesions and in outer tumor cells of salivary
pleomorphic adenomas. Acta Histochem Cytochem 22:375–384.
Shinohara M, Ikebe T, Nakamura S, Takenoshits Y, Oka M, Mori M.
1996. Multiple pleomorphic adenoma arising in the parotid and
submandibular lymph node. Br J Oral Maxillofac Surg 34:515–519.
Shklar G, Chauncey HH. 1963. Effects of hypophysectomy on the
enzyme histochemistry of the rat submaxillary gland. J Dent Res
42:71–77.
Sims-Sampson G, Gresik EW, Barka T. 1984. Histochemical localization of ouabain-sensitive, K⫹-dependent p-nitrophenylphosphatase
(Na⫹-K⫹-ATPase) activity in the submandibular gland of the
mouse: effect of androgen, thyroid hormone, or postnatal age. Anat
Rec 210:53– 60.
Sirigu P, Cossu M, Perra MT, Puxeddu P. 1982b. Histochemistry of
the 3␤-hydroxysteroid, 17␤-hydroxysteroid and 3␤-hydroxysteroid
dehydrogenases in human salivary glands. Arch Oral Biol 27:547–
551.
Smith AA. 1969. Major salivary glands of the Philippine tarsier. Fol
Primatol 10:113–130.
Soinila J, Salo A, Uusitalo H, Yanaihara N, Häppölä O. 1989. CGRPimmunoreactive sensory nerve fibers in the submandibular gland of
the rat. Histochemistry 91:455– 460.
Soinila J, Salo A, Uusitalo H, Yanaihara N, Häppölä O. 1991. Met5enkephalin-arg6-gly7-leu8-immunoreactive nerve fibers in the major
salivary glands of the rat: evidence for both sympathetic and parasympathetic origin. Cell Tissue Res 264:15–22.
Spicer SS, Ge Z-H, Tashian RE, Hazen-Martin DJ, Schulte BA. 1990.
Comparative distribution of carbonic anhydrase isozymes III and II
in rodent tissues. Am J Anat 187:55– 64.
Stephens LC, King GK, Aug KK, Schultheiss TE, Peters LJ. 1986.
Surgical and microscopic anatomy of parotid and submandibular
salivary glands of rhesus monkeys (Macaca mulatta). J Med Primatol 15:105–119.
Tajima Y, Utsumi N, Takuma T, Kumegawa M. 1979. Histochemical
study on the localization of glucose-6-phosphate dehydrogenase induced by androgen or thyroxine in the convoluted tubules of mouse
submandibular gland. Histochemistry 63:261–264.
Takai Y, Noda Y, Sumitomo S, Kawamura K, Mori M. 1985a. Immunohistochemical detection of keratin proteins in salivary gland
ducts of mammals. Arch Histochem Cytochem 18:353–361.
525
Takai Y, Sumitomo S, Noda Y, Hikosaka N, Mori M. 1985b. Comparison of effectiveness of different fixatives for keratin distribution in
ductal segments of salivary glands. Acta Histochem Cytochem 18:
139 –146.
Takai Y, Yamada K, Shinohara H, Orito T, Tsukitani K, Mori M.
1988. Monoclonal antibodies against keratins bind to intercalated
duct and ductal basal cells of normal salivary glands in paraffin
sections. Acta Histochem Cytochem 21:575–584.
Takano K, Suzuki T. 1971. Localization of parotin in bovine parotid
gland, demonstrated by the immunohistochemical method. Acta
Histochem Cytochem 4:1–10.
Takeda Y, Komori A, Ishikawa G. 1978. An electron microscopic study
of human labial salivary glands: II, duct system. J Jpn Stomatol Soc
27:280 –295.
Takeda Y, Ishikawa G. 1983. Crystalloids in salivary duct cysts of the
human parotid gland: scanning electron microscopical study with
electron probe X-ray microanalysis. Virch Arch (Pathol Anat) 399:
41– 48.
Takeda Y, Fujimura A. 1985. Interepithelial (sic) lymphocytes of the
rat submandibular gland. Jpn J Oral Biol 27:1197–1201.
Tamarin A, Sreebny LM. 1965. The rat submaxillary salivary gland:
a correlative study by light and electron microscopy. J Morphol
117:295–352.
Tandler B. 1966. Fine structure of oncocytes in human salivary
glands. Virch Arch Pathol Anat 341:317–326.
Tandler B, Denning CR, Mandel ID, Kutscher AH. 1970. Ultrastructure of human labial salivary glands: III, myoepithelium and ducts.
J Morphol 130:227–246.
Tandler B, Erlandson RA. 1976. Ultrastructure of baboon parotid
gland. Anat Rec 184:115–132.
Tandler B, Poulsen JH. 1976. Ultrastructure of the main excretory
duct of the cat submandibular gland. J Morphol 149:183–198.
Tandler B, Poulsen JH. 1977. Ultrastructure of the cat sublingual
gland. Anat Rec 187:153–172.
Tandler B. 1978. Salivary glands and the secretory process. In: Shaw
JH, Sweeney EA, Cappuccino CC, Meller SM, editors. A textbook of
oral biology. Philadelphia, PA: W.B. Saunders. p 547–592.
Tandler B, Cohan RP. 1984. Ultrastructure of the parotid gland in the
little brown bat. Anat Rec 210:491–502.
Tandler B. 1986. Ultrastructure of the retrolingual salivary gland in
the European hedgehog. J Submicrosc Cytol 18:249 –260.
Tandler B, Riva A. 1986. Salivary glands. In: Mjör IA, Fejerskov O,
editors. Human oral embryology and histology. Copenhagen:
Munksgaard International. p 243–284.
Tandler B. 1988. Structure of the human parotid and submandibular
glands. In: Sreebny LM, editor. The salivary system. Boca Raton,
LA: CRC Press. p 21– 41.
Tandler B, Phillips CJ, Nagato T, Toyoshima K. 1990a. Ultrastructural diversity in chiropteran salivary glands. In: Riva A, Motta P,
editors. Ultrastructure of the extraparietal glands of the alimentary
tract. Boston: Kluwer Academic. p 31–52.
Tandler B, Toyoshima K, Phillips CJ. 1990b. Ultrastructure of the
prinicipal and accessory submandibular glands of the common vampire bat. Am J Anat 189:303–315.
Tandler B. 1993a. Introduction to mammalian salivary glands. Microscopy Res Tech 23:1– 4.
Tandler B. 1993b. Structure of the duct system in mammalian major
salivary glands. Microscopy Res Tech 26:57–74.
Tandler B, Pinkstaff CA, Riva A. 1994. Ultrastructure and histochemistry of human anterior lingual salivary glands (glands of Blandin
and Nuhn). Anat Rec 240:167–177.
Tandler B, Phillips CJ. 1995. Special relationship between mitochondria and hypolemmal nerve terminals in salivary glands of some
bats. Anat Rec 243:312–317.
Tandler B, Toyoshima K, Phillips CJ. 1995. Symbiotic bacteria in the
accessory submandibular gland of the club-footed bat, Tylonycteris
pachypus. Ann Anat 177:111–117.
Tandler B, Pinkstaff CA, Nagato T, Phillips CJ. 1996. Giant secretory
granules in the ducts of the parotid and submandibular glands of
the slow loris. Tissue Cell 28:321–329.
526
TANDLER ET AL.
Tandler B, Nagato T, Phillips CJ. 1997a. Crystalloids in the excretory
ducts of the accessory submandibular gland of the long-winged bat,
Miniopterus magnator. Microscopy Res Tech 37:592–597.
Tandler B, Nagato T, Phillips CJ. 1997b. Ultrastructure of the unusual accessory submandibular gland in the fringe-lipped bat, Trachops cirrhosus. Anat Rec 248:164 –175.
Tandler B, Nagato T, Phillips CJ. 1997c. Ultrastructure of the parotid
gland in seven species of fruit bats in the genus Artibeus. Anat Rec
248:176 –188.
Tandler B, Toyoshima K, Seta Y, Phillips CJ. 1997d. Ultrastructure of
the salivary glands in the midtongue of the common vampire bat,
Desmodus rotundus. Anat Rec 249:196 –205.
Tandler B. Phillips CJ. 1998. Microstructure of salivary glands and its
relationship to diet. In: Garrett JR, Ekström J, Anderson LC, editors. Glandular mechanisms of salivary secretion, vol. 1. Basel:
Karger. p 21–35.
Tandler B, Nagato T, Phillips CJ. 1998a. Ultrastructure of the binary
parotid glands in the free-tailed bat, Tadarida thersites: II, accessory parotid gland. Anat Rec 251:122–135.
Tandler B, Nagato T, Phillips CJ. 1998b. Ultrastructure of major
intraglandular ducts of the parotid gland of the African mole-rat.
Eur J Morphol 36(Suppl):27–30.
Tandler B, Nagato T, Toyoshima K, Phillips CJ. 1998c. Comparative
ultrastructure of intercalated ducts in mammalian salivary glands:
a review. Anat Rec 252:64 –91.
Tandler B, Nagato T, Phillips CJ. 1999. Ultrastructure of the parotid
gland in two species of naked-backed bats. Anat Rec 255:105–115.
Tandler B, Gresik EW, Phillips CJ, Nagato T. 2001. Secretion by
striated ducts of mammalian major salivary glands: a review from
an ultrastructural, physiological, and evolutionary perspective.
Anat Rec 264:121–145.
Tandler B, Hoppel CL. 2004. Oncocytes. In: Lennarz WL, Lane MD,
editors. Encyclopedia of biological chemistry, vol. 3. Oxford:
Elsevier Science. p 165–167.
Terpe H-J, Stark H, Prehm P, Günthert U. 1994. CD44 variant
isoforms are preferentially expressed in basal epithelia of nonmalignant human fetal and adult tissues. Histochemistry 101:79 –
89.
Thaysen JH. 1960. Handling of alkali metals by exocrine glands other
than the kidney. In: Ussing HH, Kruhpffer P, Thaysen JH, Thorn
NA, editors. Handbuch der Experimentellen Pharmakologie, pt. 2,
vol. 13. Berlin: Springer-Verlag. p 424 –507.
Therkildsen MH, Mandel U, Thorn J, Christensen M, Dabelsteen E.
1994. Simple mucin-type carbohydrate antigens in major salivary
glands. J Histochem Cytochem 42:1251–1259.
Tomich CE, Eversole LR. 1972. The enzyme histochemistry of isoproterenol-induced salivary gland hyperplasia. Oral Surg Oral Med
Oral Pathol 33:857– 871.
Toyoshima K, Tandler B. 1986. Ultrastructure of the submandibular
gland in the rabbit. Am J Anat 176:469 – 481.
Toyoshima K, Tandler B. 1991. Ultrastructure of the sublingual gland
in the African multimammate rodent. Anat Rec 229:482– 488.
Trahair JF, Ryan GB. 1989. Co-localization of neuron-specific enolaselike and kallikrein-like immunoreactivity in ductal and tubular
epithelium of sheep salivary gland and kidney. J Histochem Cytochem 37:309 –314.
Triantafyllou A, Fletcher D, Scott J. 1999. Morphological phenotypes
and functional capabilities of submandibular parenchymal cells of
the ferret investigated by protein, mucosubstance and enzyme histochemistry. Histochem J 31:789 –796.
Trowbridge HO. 1969. Salivary gland changes in vitamin-A-deficient
rats. Arch Oral Biol 14:891–900.
Tsuzi T, Shinozaki F, Yamada K, Mori M. 1989. Immunohistochemical detection of human lung and gastric cancer antigen in human
salivary gland tumors. Anticancer Res 9:327–340.
Van Esch E, Dreef-van der Meulen HC, Feron VJ. 1986. Spontaneous
hyperplastic and metaplastic duct epithelium in the sublingual
salivary glands of Wistar rats. Lab Anim 20:127–131.
Vetter, H. 1969. Histochemie und Kapillarisierung der Gangsysteme
der drei grossen Speicheldrüsen und der Glandula lacrimalis exorbitalis der Ratte. Z Anat Entwickl-Gesch 128:141–162.
Vignoli W, Nogueira JC. 1981. Histology and mucosubstance histochemistry of the parotid gland in suckling, prepuberal and puberal
zebus (Bos indicus). Anat Histol Embryol 10:147–158.
Vitaioli L, Bondi AM, Menghi G, Materazzi G. 1981. Localization of
the activity of Arylsulphatases A and B in the rat salivary glands.
Acta Histochem 69:70 –76.
Vitaioli L, Bondi AM, Menghi G, Materazzi G. 1983. Soluble arylsulphatases in the rabbit salivary glands: a light and electron microscopic study. Acta Histochem 73:193–203.
Wickliffe JK, Lee VH, Smith E, Tandler B, Phillips CJ. 2002. Gene
expression, cell localization, and evolution of rodent submandibular
gland androgen-binding protein. Eur J Morphol 40:257–260.
Wilson DE, Reeder DM. 1993. Mammal species of the world: a taxonomic and geographic reference, 2nd ed. Washington, DC: Smithsonian Institution Press.
Winston DC, Hennigar RA, Spicer SS, Garrett JR, Schulte BA. 1988.
Immunohistochemical localization of Na⫹,K⫹-ATPase in rodent and
human salivary and lacrimal glands. J Histochem Cytochem 36:
1139 –1145.
Winston DC, Schulte BA, Garrett JR, Proctor GB. 1990. Na⫹,K⫹ATPase in cat salivary glands and changes induced by nerve
stimulation: an immunohistochemical study. J Histochem Cytochem 38:1187–1191.
Wu HH, Kawamata H, Wang DD, Oyasu R. 1993. Immunohistochemical localization of transforming growth factor ␣ in the major salivary glands of male and female rats. Histochem J 25:613– 618.
Yahiro J, Miyoshi S. 1996. Immunohistochemical localization of kallikrein in salivary glands of the Japanese monkey, Macaca fuscata.
Arch Oral Biol 41:225–228.
Yamada K, Iwai K, Okada Y, Mori M. 1989a. Immunohistochemical
expression of epidermal growth factor receptor in salivary gland
tumours. Virch Arch A 415:523–531.
Yamada K, Tanaka T, Mori M, Tsubura A, Morii S, Tsubone M, Ando
C, Hilgers J. 1989b. Immunohistochemical expression of MAM-3
and MAM-6 antigens in salivary gland tumours. Virch Arch A
415:509 –521.
Yamada K, Kunikata M, Mori M, Chomette G, Auriol M, Vaillant JM,
Tubura A, Mori S, Hilgers J. 1991. Immunohistochemical localization of MAM-3 and MAM-6 antigens in adenoid cystic carcinoma.
J Oral Pathol Med 20:57– 63.
Yamada K, Kudeken W, Sumitomo S, Muramatu Y, Shiba T, Takai Y,
Mori M, Speight PM. 1996. Immunohistochemical expression of
E-cadherin in salivary glands and their tumors. Acta Histochem
Cytochem 29:305–310.
Yamada K, Kudeken W, Muramatsu Y, Sumitomo S, Takai Y, Mori M.
1997. Human epithelial related antigen (hERA) in salivary glands
and their tumors: immunohistochemical observations. Acta Histochem Cytochem 30:477– 482.
Yamada K, Namba M, Kudeken W, Takai Y, Mori M, Tsukitani K, Yang
LJ, Speight PM. 1999. Comparative expression of E-cadherin, and ␤
catenin in salivary gland. Acta Histochem Cytochem 32:305–313.
Yoshihara T, Kanda T, Nagata H, Nomoto M, Kaneko T, Kato Y, Yaku
Y. 1988. Cytochemical demonstration of actin filaments in myoepithelial cells of the human parotid gland. Acta Anat 132:317–320.
Young JA, van Lennep EW. 1978. The morphology of salivary glands.
London: Academic Press.
Young JA. 1979. Salivary secretion of inorganic electrolytes. In: Crane
RK, editor. Gastrointestinal physiology III, vol. 19. Baltimore, MD:
University Park Press. p 1–58.
Young JA, Cook DI, van Lennep EW, Roberts M. 1987. Secretion by
the major salivary glands. In: Johnson LR, editor. Physiology of the
gastrointestinal tract, 2nd ed. New York: Raven Press. p 773– 815.
Документ
Категория
Без категории
Просмотров
2
Размер файла
1 337 Кб
Теги
mammalia, excretory, glandsstructural, salivary, interlobular, review, duct, histochemical
1/--страниц
Пожаловаться на содержимое документа