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THE ANATOMICAL RECORD 255:105–115 (1999)
Ultrastructure of the Parotid Gland in
Two Species of Naked-Backed Bats
BERNARD TANDLER,1 TOSHIKAZU NAGATO,2
AND CARLETON J. PHILLIPS3*
1Department of Biological Sciences and Institute of Environmental and Human
Health, Texas Tech University, Lubbock, Texas
2Second Department of Oral Anatomy, Fukuoka Dental College, Fukuoka, Japan
3Department of Biological Sciences, Texas Tech University, Lubbock, Texas
ABSTRACT
Naked-backed bats of the genus Pteronotus (family Mormoopidae) occur
in the Neotropics from Mexico through northern South America. These are
relatively small-sized insectivorous species that frequently roost in caves.
Eight specimens of naked-backed bats (Pteronotus parnellii) were livetrapped in Suriname and one in Cuba (P. quadridens). Their parotid glands
were fixed in an aldehyde mixture designed for field work and postfixed in
the laboratory with osmium tetroxide. Tissues were further prepared for
electron microscopy by conventional means. The parotid glands of the two
species of Pteronotusclosely resemble each other except for the substructure
of their serous secretory granules. Serous granules in P. parnellii are
bizonal, with a moderately dense inner matrix and an outer, denser corona
or crescent. The matrix is occupied by laminae, flakes, and filaments in
random array. In contrast, serous granules in P. quadridens consist of a
uniform matrix that contains dense, usually stacked toroids or tubules
either in random array or packed in bundles. A parotid gland from one
specimen of P. parnellii contained an endpiece that consisted of cells that
contained giant (up to 9 µm in diameter) serous granules. Serous cells in
both species contain aggregates of small, uniformly dense, rod-like, membrane-delimited organelles as well as occasional bundles of cytofilaments.
The endpieces are separated from intercalated ducts by a ring of granulated
cells that contain secretory granules that often have a bull’s-eye configuration. Intercalated and striated ducts are typical in appearance, except that
many of the cells in the latter contain small, dense secretory granules in
their apical cytoplasm. The parotid glands in the two species of naked-baked
bats differ slightly in terms of acinar secretory granule ultrastructure, but
otherwise are fairly conservative. It is thought that the glands in these
particular bats might represent the ‘‘basal’’ condition of the salivary glands
of insectivorous bats and thus can serve as a reference point for making
comparisons to the highly diversified (in terms of diet) phyllostomid bats.
Anat Rec 255:105–115, 1999. r 1999 Wiley-Liss, Inc.
Key words: salivary glands; secretory granules; bats; Pteronotus parnellii;
Pteronotus quadridens
It can be argued that salivary glands have played very
important—perhaps ‘‘keystone’’—roles in the adaptive radiation of mammals. There is mounting evidence that the
ultrastructure and function of these glands reflect a combination of evolutionary history (phylogeny), ecology, and
adaptation (Phillips, 1996). The salivary glands of bats
provide especially useful models for testing hypotheses
r 1999 WILEY-LISS, INC.
Grant sponsor: The National Institute of Dental Research (BT,
CJP); Grant sponsor: The Carnegie Museum of Natural History
(CJP); Grant sponsor: The United States Navy (CJP).
*Correspondence to: Dr. Carleton J. Phillips, Department of
Biological Sciences, Texas Tech University, Lubbock TX 79409–
3131.
Received 30 April 1998; Accepted 19 July 1998
106
TANDLER ET AL.
about the relationship between gland ultrastructure and
diet (Phillips et al., 1993; Tandler and Phillips, 1998)
because bats exhibit a remarkable diversity in diet.
The naked-backed bats (also called ‘‘mustache’’ bats) of
the genus Pteronotus are important in comparative studies
for two reasons. These bats (and their relatives in the
family Mormoopidae) are insectivorous, but as an evolutionary lineage they have been separate from other major
groups of insectivorous bats for ⬃50 million years (Simmons and Geisler, 1998). Thus, although insectivorousness
might be a shared ancestral diet, it has evolved along
independent lines for a long period of time. Additionally,
Pteronotus and its relatives share an ancestry with the
Neotropical phyllostomid bats. Pteronotus thus offers a
reference point (in systematic terms, a ‘‘sister’’ group) for
comparison with the phyllostomid bats, which in turn
exhibit the most diversified diets and salivary glands of
any bat species (Phillips and Tandler, 1987; Phillips et al.,
1993). In addition, one of the naked-backed bats, P. parnellii, has served as an important model for understanding
auditory capabilities and echolocation in insectivorous
bats (Pollak and Casseday, 1989). In terms of foraging
behavior and diet, bats of the genus are characterized by
enlarged fleshy lip pads and para-oral, bristle-like hairs
that might serve to direct the flow of air into the mouth as
the bat closes in on its prey (Nowak, 1991). Typically, bats
in this genus feed on small, soft-bodied flying insects such
as moths.
MATERIALS AND METHODS
Eight naked-backed bats (Pteronotus parnellii) were
live-trapped during field work in Suriname and one was
obtained in Cuba (P. quadridens). Voucher specimens are
in the research collections at the Carnegie Museum of
Natural History and Texas Tech University, Lubbock. Of
the South American bats, three were males and five were
females; the specimen of P. quadridens was a female. The
parotid glands were removed from the animals, which had
been anesthetized with T-61 euthanasia solution (no longer
marketed), and minced in fixative. Salivary glands from
the Suriname specimens were fixed in a modified triple
aldehyde-DMSO solution (Phillips, 1985) based on the
fixative of Kalt and Tandler (1971). The specimen of P.
quadridens was fixed in modified half-strength Karnovsky’s (1965) solution that contained DMSO and LiOH.
After the initial fixation in aldehydes, all specimens were
stored in 3% glutaraldehyde until refrigeration became
available (Phillips, 1985). After thorough washing in buffered sucrose, the specimens were postfixed in phosphatebuffered 2% osmium tetroxide (Millonig, 1961a) and washed
in distilled water. An overnight soak in acidified 0.25%
uranyl acetate (Tandler, 1990) was followed by a second
round of washing in distilled water. After dehydration in
ascending concentrations of ethanol, the tissue blocks
were embedded in Epon:Maraglas (Tandler and Walter,
1977). Thin sections were consecutively stained with acidified methanolic uranyl acetate (Tandler, 1990), then with
either lead tartrate (Millonig, 1961b) or lead citrate (Venable and Coggeshall, 1965), and examined with either a
JEOL 1200 EX (Tokyo, Japan) or a Siemens 101 or 1a
Elmiskop (Berlin, Germany) electron microscope. Semithin sections were stained with methylene blue-azure II
(Laczkó and Lévai, 1975), and examined with an Olympus
Vanox.
RESULTS
In their general histology, the parotid glands of P.
parnellii and P. quadridens are quite typical. Most of the
serous secretory endpieces form acini, but some are tubuloalveolar. The intercalated ducts are short and difficult to
detect, but the striated ducts are of usual length and
prominence (Fig. 1).The apical surfaces of the serous cells
face the endpiece lumen, and a typical system of microvillus-lined intercellular canaliculi courses down the lateral
surfaces of these cells. The cell base is characterized by
numerous slender basal folds; the intercellular space
between these folds is occupied by a homogeneous dense
material, which apparently is deposited in this location by
exocytosis of coatamer vesicles. We have elsewhere described in detail this unusual basal apparatus (Nagato et
al., 1998).
In both species, the serous cells contain a full complement of secretory granules (Fig. 2). In a few cells in P.
parnellii, these granules consist wholly of a structureless
dense matrix. In most cells, however, the granules, the
largest of which measure ⬃0.9 µm in diameter, have a
well-defined, bizonal substructure (Figs. 3, 4). The matrix
in such granules consists of a moderately dense core, and a
marginally denser halo or crescent underlying the granule
membrane. The inner core contains a variable number of
apparently linear densities, but the true three-dimensional structure of these densities is difficult to decipher
(Fig. 4). Certain of the densities probably have the form of
flat, elliptical laminae or irregular flakes, whereas others
are corrugated. In some granules, dot-like structures are
visible. Some of these dots probably represent transversely
sectioned rods, which would appear as laminae in longitudinal section. Other dots have a much smaller diameter
than the thickness of the laminar densities or putative
rods, and may represent cross-sectioned thin filaments. In
a few cells, the granules may have only a partial outer
halo, or may be lacking this component altogether. In this
case, the core material fills the entire granule.
The parotid serous granules of P. quadridens are quite
different from those of its congeneric species. They tend to
be larger (⬃1.3 µm in diameter) and their matrix lacks a
bizonal appearance; it is homogeneous and of moderate
density. At lower magnifications, the matrix is seen to
contain many small densities, some of which are round,
some of which are oblong (Fig. 5). At high magnification, it
becomes evident that many of these densities actually
consist of concentric, stacked, quite dense tori (Fig. 6). The
outermost torus of each matrical inclusion is fitted with a
series of short spinules (actually ribs) ⬃19–28 nm long. In
other granules, the matrix includes an array of cylindrical
structures measuring ⬃47 nm in diameter and with dense
walls. These tend to be arranged in parallel in bundles, but
the bundles are randomly disposed, so that these aggregates are sectioned in a variety of planes in the same
granule (Figs. 7, 8). In transverse section, the cylinders are
seen to be in a square packing arrangement (Fig. 8).
In a very small portion of a single lobule from one of the
eight specimens of P. parnellii in our sample, we encountered a few serous secretory cells that contained one or
several giant secretory granules in addition to their complement of typical ones (Fig. 9). These outsized granules
measure 7–9 µm in diameter; in addition to a giant one, a
few cells had intermediate-sized granules. The matrix in
the large granules is of the same general density as in
PAROTID STRUCTURE IN NAKED-BACKED BATS
Fig. 1. P. parnellii. Survey electron micrograph of the parotid gland
showing the heavily granulated endpiece cells. Two segments of the
same intercalated duct are indicated by arrows. 800⫻.
Fig. 2. P. parnellii. An endpiece cell at higher magnification. It is
107
underlaid by a process of a myoepithelial cell (MC). A transversely
sectioned intercellular canaliculus (ICC) is present at the lateral border of
the cell. 10,100⫻.
108
TANDLER ET AL.
Fig. 3. P. parnellii. A cluster of serous granules in an endpiece cell.
Although these granules exhibit minor variation in substructure, they all
have the same basic morphology. 34,500⫻.
Fig. 4. P. parnellii. A serous granule at high magnification. It contains
two zones of marginally different density. The lighter zone contains what
appear to be profiles of short laminae. 80,500⫻.
PAROTID STRUCTURE IN NAKED-BACKED BATS
Fig. 5. P. quadridens. A cluster of serous granules in an endpiece cell.
The morphology of these granules clearly differs from that of P. parnellii.
39,500⫻.
109
Fig. 6. P. quadridens. A serous granule at high magnification. The
dense inclusions consist mainly of stacked toroids that exhibit an axial
periodicity. 70,500⫻.
110
TANDLER ET AL.
Fig. 7. P. quadridens. In this serous granule, the dense inclusions
consist of twisted, tubular forms. 66,000⫻.
Fig. 8. P. quadridens. In this serous granule, the dense tubules are in
a closely packed, parallel array. They are seen in both transverse and
longitudinal section. The lucent space at the bottom of the granule is due
to the artifactual separation of the granule from the embedding medium.
66,200⫻.
Fig. 9. P. parnellii. A serous endpiece in which several of the
constituent cells harbor giant secretory granules. Small and intermediate
size granules are also present in the same cells. 5,200⫻.
Fig. 10. P. parnellii. The edge of a giant granule showing some of the
faint inclusions in the granule matrix. 31,800⫻.
PAROTID STRUCTURE IN NAKED-BACKED BATS
111
Fig. 11. P. parnellii. The basal cytoplasm of a serous cell with a
collection of dense, membrane-delimited rods. 33,000⫻.
Fig. 12. P. parnellii. Two sheaves of cytofilaments in a serous cell.
64,000⫻.
Fig. 13. P. quadridens. A granular cell that separates the endpiece
from the intercalated duct proper. The substructure of the granules is
completely different from that of granules in the serous cells or in the
intercalated duct cells that follow. 15,600⫻.
normal-sized ones and tends to be homogeneous, but small
vesicles with lucent borders are randomly arrayed at the
periphery of the matrix of the enlarged granules (Fig. 10).
Because most serous cells in our specimens are replete
with secretory granules, both the rough endoplasmic reticulum (RER) and Golgi apparatus are relatively inconspicuous. The RER is manifested as some scattered cisternae;
free ribosomes are abundant. The Golgi apparatus consists
of three or four parallel saccules, several of which may be
moderately dilated. A few coated vesicles sometimes are
present near the Golgi saccules, but in the main condensing vacuoles are absent.
In both species, the serous cell cytoplasm contains
collections of loosely aggregated dense rods (Fig. 11). These
structures are delimited by a single membrane and contain a homogeneous dense material. They are up to 0.7 µm
long and 60 nm in diameter. These structures have no
obvious relationship to any cytoplasmic organelle. Some
serous cells in P. parnellii contain cytoplasmic bundles of
parallel cytofilaments; each filament measures ⬃10 nm in
thickness (Fig. 12).
Intervening between secretory endpieces and intercalated ducts are rings of intermediate granular cells. These
contain granules that frequently have a bull’s-eye configuration (Fig. 13). In some granules, the substructure is less
regular.
Intercalated ducts are simple affairs. They consist of a
single layer of cuboidal epithelium that lacks distinguish-
ing features and is underlaid by myoepithelial cells (Fig.
14). The duct cells have a relatively large nucleus and a
few scattered mitochondria. Except for several short microvilli, they lack surface modifications. A few secretory
granules are present in the duct cells of P. quadridens, but
are absent from the same site in P. parnellii. The granules
in the former bat are up to 0.9 µm in diameter and of low
matrix density; some contain a spherule (Fig. 15).
Striated ducts in the parotid glands of both kinds of
naked-backed bats in general are similar in structure to
those in a variety of bats (Tandler et al., 1989; Tandler,
1993) (Fig. 16). In addition to the usual basal array of
folded plasma membranes and vertically oriented mitochondria (Fig. 17), some of the duct cells feature a juxtaluminal band of small, dense, structureless granules (Fig.
17). This band of apical granules is more prominent in P.
parnellii than in P. quadridens, but the granules are more
distinct in the latter. The granular duct cells may alternate
with cells of similar overall morphology, but that lack
apical granules altogether (Fig. 18).
DISCUSSION
Compared to serous granules in the serous endpieces of
the parotid gland of many other species of bats (Phillips et
al., 1987; Tandler and Phillips, 1993), those in the parotid
of Pteronotus have a very unusual substructure. We previously attempted to explain granule substructure by postu-
112
TANDLER ET AL.
Fig. 14. P. quadridens. An intercalated duct sectioned in a slightly
oblique transverse plane. The cuboidal epithelial cells of the duct lack
secretory granules or cytoplasmic specializations. It may be inferred that
this section passes through an intermediate segment of the duct. 5,400⫻.
Fig. 15. P. quadridens. Secretory granules in a proximal cell of an
intercalated duct. They consist of a dense, ragged, eccentrically placed
spherule suspended in a relatively light matrix. 27,000⫻.
lating a self-assortment mechanism for the different molecules in the granule matrix, leading to the production of
patterning based on distribution of electron-dense components. This supposition is now backed by some experimental evidence (Takano et al., 1991, 1993). If such a mechanism is operative in the serous granules of the nakedbacked bat, it must be an extraordinarily complex one,
given the diversity of structural components in the mature
granules of P. parnellii, i.e., dense and less-dense zones,
flat and corrugated dense laminae, dense rods, and thin
filaments.
The serous granules of P. quadridens also have an
extremely unusual substructure. Spiny inclusions of somewhat similar type also have been noted in the submandibular serous cells of the little brown bat, Myotis lucifugus
(Tandler and Cohan, 1984), but as in P. quadridens, the
putative spines turned out to be ribs in three dimensions;
however, the inclusions in the granules of the former are
quite different in appearance from those in the granules of
P. quadridens.
Unfortunately, we were unable to trace the morphological concomitants of secretion of the complex granules in
either species of Pteronotus, because almost all endpiece
cells were crammed with stored mature granules; that is,
these cells were not actively secreting new granules.
Although the composition of the parotid secretory granules
in Pteronotus is unknown, their electron-density points to
the possibility of an enzyme-rich content (Junqueira et al.,
1973). In a previous study (Phillips et al., 1998), we
screened P. parnellii with a polyclonal antiserum to lysozyme; the parotid gland acinar and intercalated duct cells
were negative. This negative finding is interesting because
the parotid glands of some species of insectivorous bats
exhibit considerable lysozyme-like immunoreactivity. The
most likely difference is that species of Pteronotus feed on
insects that are soft-bodied (low in chitin).
The presence of giant secretory granules in a subset of
serous cells of a parotid gland in a single individual of P.
pteronotus is unprecedented in the annals of salivary
gland research. Although giant granules have been reported to occur in the striated and excretory ducts of the
parotid and submandibular glands of the slow loris (Tandler et al., 1996), practically every ductal cell in these
specific glands is involved in the elaboration of grossly
enlarged granules; this clearly is a manifestation of a
mechanism that regulates granule size in each and every
duct cell. Giant secretory granules up to 8 µm in diameter
sporadically occur in serous glands underlying the mucosa
of human nasal turbinates (R.A. Erlandson, personal
communication). Their occurrence in only a few cells in
just one specimen of P. parnellii and in some human nasal
glands is difficult to explain. The propinquity of the
affected serous cells suggests that they represent a clone of
endpiece cells. A recent study by Redman (1995) has shown
PAROTID STRUCTURE IN NAKED-BACKED BATS
Fig. 16. P. parnellii. A portion of a striated duct. The cells have both
basal mitochondria and apical, dense secretory granules. 8,400⫻.
Fig. 17. P. parnellii. The base of striated duct cells showing the
vertically oriented, rod-shaped mitochondria alternating with folded plasma
membranes. 15,600⫻.
113
Fig. 18. P. parnellii. The apices of two adjacent striated duct cells. The
cell on the right contains a panoply of secretory granules, whereas its
immediate neighbor on the left lacks these structures altogether. 20,000⫻.
114
TANDLER ET AL.
that salivary acinar cells are fully capable of selfreplication.
We posit the following scenario: A somatic mutation took
place during mitosis of a serous cell and was propagated
through several rounds of cell division, forming a clone.
This mutation, while not having immediate overt effects,
rendered the granule-elaborating cytological machinery
capable of producing huge granules. Mroz and Léchene
(1986) have shown that pancreatic zymogen granules can
differ markedly in protein composition and Schick et al.
(1984) have demonstrated that diet can affect the composition of pancreatic exocrine granules. If the naked-backed
bat in question consumed just the right combination of
nutrients, the production of megagranules might have
been triggered in the susceptible, mutated cells. If a
mutation of this type had occurred in the gametes before
fertilization or during embryonic development of the bat,
then the presence of giant granules would be a widespread
phenomenon, rather than being confined to a small group
of neighboring serous cells.
The precise mechanism whereby giant secretory granules are engendered is unknown. One obvious way might
be by fusion of smaller granules, a process that has been
documented in cells of the anterior pituitary gland (Senda
et al., 1998). Some simple computations are enough to
dispel this notion. A giant granule has a volume roughly
equal to a thousand normal-sized granules, but because of
surface area to volume ratios, a thousand normal granules
collectively have a surface area about 2.5 times greater
than a single megagranule. This means that if fusion
occurs, a huge amount of limiting membrane becomes
superfluous and must be eliminated. The relatively few
small vesicles within the matrix of the giant granules may
be the relics of such an elimination process, but these by
themselves cannot account for all of the unneeded membrane. Similar internal vesicles are present in the giant
ductular granules of the parotid and submandibular glands
of the slow loris (Tandler et al., 1996). However, inspection
of the serous cell cytoplasm fails to reveal either autophagic vacuoles or of pools of membrane, indicating that
granule fusion is not responsible for the production of
giant granules.
In normal exocrine cells, the terminal expansions of the
inner Golgi saccules become filled with secretory product
and, when a certain size range is reached, separate from
the Golgi to give rise to mature secretory granules. In the
affected cells in the parotid gland of P. parnellii, the
scission process might be compromised, so that the terminal dilatations continue to grow by acquisition of additional secretory product, until they reach huge proportions. Then a nascent giant granule might separate from
the Golgi apparatus by virtue of its mass, or the entire
Golgi saccule, having been filled to bursting with secretory
product, is cast out in toto into the cytoplasm.
In general, acinar secretory cells are similar within a
given salivary gland, giving the impression that all of
these cells represent but a single population. An earlier
ultrastructural study of the human submandibular gland
(Tandler and Erlandson, 1972) documented the presence
in the same gland of two serous cell phenotypes with
secretory granules that exhibited two widely differing
substructural patterns. Using histochemistry, we found
that only scattered individual acinar cells in the parotid
gland of the sac-winged bat, Saccopteryx bilineata, were
immunoreactive to antilysozyme antiserum (Phillips et
al., 1998). Although such data do not prove that some cells
are regulated independently from others, the results raise
the possibility that there can be more than one ‘‘class’’ of
acinar cells in a serous gland. In addition to being an
interesting issue in evolutionary terms, e.g., the possibility
of intragland diversification in secretory product, these
observations also call attention to the dynamics of gland
development. The possibility of secretory diversification
and subdivision of the parotid gland acinar cell population
has been discussed by Denny et al. (1993).
Granular cells positioned between secretory endpieces
and intercalated ducts have been observed in salivary
glands from five different mammalian orders. The only
chiropteran other than naked-backed bats whose salivary
glands are reported to contain such cells is the common
vampire bat, Desmodus rotundus, where they are present
in the principal submandibular glands (Tandler et al.,
1990). The precise status of these cells remains to be
established.
The striated ducts in the two Pteronotus species are
quite typical of bat salivary glands. Not only do they have
the usual basal array of mitochondria and folded plasmalemma, but they sporadically have an abundance of small,
apical secretory granules, in this respect paralleling the
situation in the excretory ducts of the parotid gland of the
little brown bat, in which organ granular cells alternate
with nongranular ones (Tandler and Cohan, 1984). These
ducts appear to be able to modify the initial saliva by
liberating significant amounts of organic secretion into it,
as well as by active transport of electrolytes.
ACKNOWLEDGMENTS
We appreciate the field participation of H.H. Genoways
(University of Nebraska) and R.J. Baker (Texas Tech
University).
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