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Serous Cells in the Parotid Glands of Two Species of TamarinsPolarized Secretory Granules.

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THE ANATOMICAL RECORD 291:1254–1261 (2008)
Serous Cells in the Parotid Glands of
Two Species of Tamarins: Polarized
Secretory Granules
BERNARD TANDLER*
Department of Biological Sciences, School of Dental Medicine,
Case Western Reserve University, Cleveland, Ohio
ABSTRACT
The parotid glands of two species of tamarins were examined by electron microscopy. Endpiece cells are typical in appearance, with an extensive rough endoplasmic reticulum, prominent Golgi apparatuses, and
numerous serous granules. In the saddleback tamarin, the secretory
granules contain a dense spherule pressed against the inner aspect of the
limiting membrane, leading to a surface bulge. During the course of merocrine secretion (a form of exocytosis), such morphologically polarized
granules approach the luminal plasma membranes with the bulge in the
vanguard. It is these protuberances that fuse with the plasmalemma. In
contrast, although serous granules in the cotton top tamarin contain a
spherule, they lack surface bulges and their docking on luminal membranes seems to be a random event with respect to their surface morphology. Moreover, certain other types of cells in a taxonomically wide spectrum of species have granules with a less obvious structural polarity, as
well as cells whose granules lack morphological polarity but have a functional polarity that comes into play during exocytosis of such secretory
granules. Anat Rec, 291:1254–1261, 2008. Ó 2008 Wiley-Liss, Inc.
Key words: merocrine secretion; exocytosis; salivary glands;
secretion; secretory granules; tamarins; monkeys
Since the original report by Palade (1959) on exocrine
pancreas secretory phenomena, the basic morphological
steps in the regulated liberation of exocrine protein
products from serous cells are well recognized. When a
secretory cell is signaled to secrete, mature storage
granules move to and dock onto a luminal plasma membrane to which they fuse, forming a pentalaminar barrier between the contents of the secretory granule and
the cell exterior (Palade, 1975). This barrier is reduced
to a trilaminar one [in salivary gland mucous cells, it is
reported that this reduction results from avulsion of the
plasma membrane (Tandler and Poulsen, 1976)], which
ultimately ruptures, allowing the outflow of the secretory product.
There is little argument over the reality of these steps,
but the mechanism of attachment of granule membrane
to plasma membrane still is controversial. In the parotid
gland of a particular species of tamarin, exocytosis of
serous granules involves a morphological modification of
the granules that has implications for regulated exocytosis of secretory products in general.
Ó 2008 WILEY-LISS, INC.
MATERIALS AND METHODS
This study is based on archival material. The animals
were obtained from a breeding colony at the University of
Texas Dental Science Institute at Houston, TX. Four adult
tamarins were used in this study: one male and one female
saddleback tamarin (Saguinus fuscicollis) and one male
and one female cotton top tamarin (Saguinus oedipus).
They had been housed in hanging wire mesh cages and
food and water were available ad libitum. The two saddleback tamarins, which were being used for other experimental purposes, were sacrificed by injection of an overdose of
*Correspondence to: Dr. Bernard Tandler, Department of
Biological Sciences, School of Dental Medicine, Case Western
Reserve University, Cleveland, OH 44106-4905.
E-mail: bernard.tandler@case.edu
Received 26 October 2007; Accepted 15 May 2008
DOI 10.1002/ar.20744
Published online in Wiley InterScience (www.interscience.wiley.
com).
AROTID GLANDS OF TAMARINS
Fig. 1. Saddleback tamarin: Survey electron micrograph of several
endpiece cells in the parotid gland. The cells include an extensive
RER and numerous serous granules. The latter contain a dense spherule that often causes a surface bulge. Scale bar 5 2 mm.
methoxyfluorane (‘‘Metofane,’’ Pitman-Moore, Indianapolis,
IN). Their parotid glands were fixed by immersion in phosphate-buffered half-strength Karnovsky’s (1965) fixative.
They were postfixed with 2% osmium tetroxide in the same
buffer, and then, after rinsing in saline, they were soaked
overnight in 0.5% uranyl acetate in saline. After another
saline rinse, they were dehydrated in ascending concentrations of ethanol. In the case of the two cotton top tamarins,
parotid glands were removed from monkeys anesthetized
with Metofane; both animals survived salivary gland ablation. Gland specimens were fixed by immersion in cacodylate-buffered 3% glutaraldehyde and then postfixed in 2%
osmium. After a rinse in buffer, they were soaked overnight
in acidified 0.25% uranyl acetate (Tandler, 1990), then
rinsed and dehydrated in ethanol. Irrespective of the mode
of fixation, all dehydrated specimens were passed through
propylene oxide and embedded in Maraglas:DER 732
(Erlandson, 1964). Thin sections were stained with acidified uranyl acetate (Tandler, 1990) followed by lead tartrate
(Millonig, 1961) or by bismuth subnitrate (Riva, 1974) and
then examined in a Siemens Elmiskop 1a electron microscope.
RESULTS
Histologically, parotid glands in both species of tamarin conform in structure to that exhibited by their
1255
Fig. 2. Saddleback tamarin: A localized specialization of the RER
that to a degree resembles the ‘‘coat-of-mail’’ configuration noted in
other cell types. Scale bar 5 0.5 mm.
namesakes in other primates. Their parenchyma consists of serous endpieces, short and inconspicuous intercalated ducts, prominent striated ducts, and occasional
excretory ducts. In semithin sections, the endpiece serous granules are heavily stained with toluidine blue. In
the saddleback tamarin, these granules tend to cluster
near the luminal border of the serous cells and frequently outline intercellular canaliculi.
At the ultrastructural level, the endpiece secretory
cells in both species have all of the morphological hallmarks of serous cells, namely, an extensive, regular
rough endoplasmic reticulum, a prominent supranuclear
Golgi apparatus, and numerous dense secretory granules
(Fig. 1) (Tandler and Phillips, 1993). In a few rare sites,
the endoplasmic reticulum is locally modified (Fig. 2) to
form a series of undulating, smooth-surfaced membranes
corresponding in appearance to the ‘‘coat-of-mail’’
described in other cell types (Franke and Scheer, 1971).
The Golgi apparatus consists of several slightly dilated,
imbricated saccules that often show terminal expansions, a scattering of small vesicles, and some vacuoles.
The vesicles and the expanded saccular termini often
contain a dense spherule that is retained in the condensing vacuoles, ultimately in the mature granules.
Fully mature serous granules in the saddleback tamarin parotid gland consist of a fairly dense matrix delimited by a single membrane. Many contain a dense spherule that usually is pressed against the granule mem-
1256
TANDLER
Fig. 3. Saddleback tamarin: Higher magnification of a cluster of
serous granules, each with a spherule-containing surface bulge. Scale
bar 5 1 mm.
brane, leading it to bulge outward to form a surface
bump (Fig. 3). Those granules that appear to lack spherules might in fact possess them, but because these inclusions are small and acentrically positioned, they are
often missed in thin sections. In a few granules, two
spherules are present. The majority of granules lying
near a lumen, whether endpiece or canalicular, are oriented in such manner that the surface bulge produced
by the spherule points toward the lining plasmalemma
(Figs. 4 and 5).
In contrast to the saddleback tamarin, the serous
granules of the cotton top tamarin are spherical in outline, without surface bulges, although they contain a
lenticular dense inclusion that adheres to the inner aspect of the membrane (Fig. 6). Although the specimens
of this species were fixed in a slightly different manner
from those originating from the saddleback tamarin,
Tandler and Phillips (1993) found that other primate
species similarly feature granules that always lack
bulges, even when fixed in precisely the same manner
as was the saddleback tamarin—in other words, the difference in granule morphology between the two tamarin
species in this study is not ascribable to a variation in
fixation. The granules in S. oedipus show no preferential
orientation with respect to the plasma membranes.
The lumina of the endpieces of the saddle-back tamarin, including those of the intercellular canaliculi, are
scalloped as a result of extensive exocytosis. In addition
to the expected X-shaped invaginations, there are deep,
tortuous secretion channels resulting from compound
(chain) exocytosis. A prominent feature of the lumina in
these tamarins is the presence of assemblages of dense
material, which consists in part of globules that resemble the spherules of the in situ serous granules in size,
Figs. 4 and 5. Saddleback tamarin: Both figures show the relationship of serous granules to the lumina of intercellular canaliculi. Note
that most of the granules are oriented with their surface bulges pointing
toward the plasma membrane. Both illustrations show evidence of a
recent exocytotic event. That the invaginations marked by an asterisk
are of exocytotic origin rather than being intrinsic components of the
luminal membrane is supported by their complete lack of microvilli, in
contrast to the connected lumina. An aggregate of lipid-like bodies is
present in the canaliculus shown in Fig. 5. Scale bars 5 1 mm.
AROTID GLANDS OF TAMARINS
1257
Fig. 7. Saddleback tamarin: A large aggregate of lipid-like bodies
in the lumen of an endpiece. The larger structures are similar to the
serous granule spherules in size and density; the absence from the
serous cell cytosol of obvious lipid droplets strongly bolsters the
notion that the luminal structures originate in the secretory granules.
Scale bar 5 1 mm.
Fig. 6. Cotton top tamarin: In this species, the serous granules
contain lenticular spherules, but lack surface bulges. The light granule
in the center is not quite mature. Scale bar 5 1 mm.
shape, and density (Figs. 4b, 7). The second component
of the luminal material consists of substantially smaller
and less dense particles. Both components frequently
are present in the channels formed by compound exocytosis, where at first glance they appear to be intracellular. In addition to particulate material, scattered oddments of membranes are present in the lumina. In the
cotton-topped tamarin, the endpiece lumina contain only
sparse spherule-sized dense globules.
DISCUSSION
The most interesting aspect of the tamarin parotid
glands concerns their serous granules. Superficially,
these granules resemble their counterparts in the parotid glands of most of the few studied primate species:
spider monkey (Leeson, 1969); squirrel monkey (Cowley
and Shackleford, 1970); human being (Riva and RivaTesta, 1973); olive baboon (Tandler and Erlandson,
1976); green monkey (Messelt, 1981); and the tufted capuchin monkey (Watanabe, 1990)—also see Figs. 8–13 in
Tandler and Phillips (1993) for a side-by-side comparison
of primate serous granules in both the parotid and submandibular glands. Irrespective of matrix substructure,
salivary serous granules in most primate species contain
a dense inclusion, dubbed the ‘‘spherule’’ by Tandler and
Erlandson (1972). Immunocytochemical tests of the serous granules in the submandibular glands of the longtailed macaque, Macaca fascicularis, that contain a
prominent spherule have shown that these spherules
consist at least in part of proline-rich proteins (PRP)
(Kousvelari et al., 1982), suggesting that the spherules
in the parotid granules in the two species of tamarins
examined in this study also contain PRP. It should be
noted, however, that in human parotid granules PRP is
not confined solely to the spherules, but is distributed
throughout the granule content; instead, it appears that
it is amylase that is localized predominantly in the
spherules (Takano et al., 1993). Although PRP is present
in parotid serous granules from other monkey species
that have prominent spherules (Williams and Keller,
1973; Arneberg et al., 1976), the precise intragranular
localization of these proteins has not been established.
In the saddleback tamarin, the spherules are associated with surface bulges that confer a structural polarity
on the granules. This bulge is intimately involved with
granule exocytosis, because most granules near to a
luminal membrane are oriented with the spherule-containing bulge toward the plasmalemma. A similar phenomenon occurs in the vervet monkey, Cercopithecus
aethiops, where parotid serous granules approach luminal membranes with their spherule-containing pole leading the way (Messelt, 1981). Nevertheless, in this species there is no bulge at the point where the spherule
1258
TANDLER
contacts the limiting membrane of the granule, thus no
surface indication of polarity. It seems unlikely that PRP
(or a related protein) in and of itself is responsible for
the adherence of spherules to the inner side of the granule membrane because this happens only in the saddleback tamarin and not in the cotton-top tamarin nor in
many other mammalian species that have salivary secretory granules that contain spherules, some of which
have been determined to consist in part of PRP. It nonetheless is true that, in many species, spherules, sometimes lenticular in form, adhere to the bounding membrane of their encompassing granule (Tandler and Phillips, 1993). In the rat mammary gland, spherules—here
called micelles—which consist of casein, are attached to
the inner aspect of the granule membrane by fine filaments of unknown nature (Franke et al., 1976).
Several mechanisms for spherule position-determined
exocytosis of secretory granules suggest themselves. One
is that in these two species (S. fuscicollis and C.
aethiops), the proximity of the spherule to the granule
membrane produces a localized charge on that membrane opposite to that of the plasma membrane, resulting in an electrostatic attraction between the two. The
molecular mechanisms involved in fusion of exocytotic
structures with the plasma membrane have been
reviewed by Watson (1999), Gerber and Sudhof (2002),
Wasle and Edwardson (2002), and Burgoyne and Morgan
(2003). The presence of the spherule adjacent to the
granule membrane might result in the selective adherence of a protein from the cytosol [such as ADP-ribosylation factor (Arf) (Dohke et al., 1998), VAMP-2 (FujitaYoshigaki et al., 1998), rap1 (D’Silva et al., 1997),
Rab3D (Ohnishi et al., 1996)] or Rab26 (Nashida et al.,
2006), which ordinarily appear to be disposed over the
entire granule surface and that could act as a docking
protein. Another candidate is synexin or a synexin-like
molecule, which has been proposed as a recognition protein that mediates fusion of chromaffin granules with
the plasma membrane of cells in the adrenal medulla
(Pollard et al., 1979). In sea urchin eggs, it has been
found that the proteins involved in the fusion step of
exocytosis are immobile within the granule membrane
(Wong et al., 2007), suggesting that in the saddleback
tamarin parotid gland the bulges are fixed in position on
individual granules.
In a sense, the surface bulges on the tamarin granules
might be analogous to the exocysts of yeast cells. Exocysts are complexes of proteins with some rod-like
domains consisting of helical bundles (Munson and
Novick, 2006) that are carried by secretory vesicles and
target them to plasmalemmal exocytotic sites (Guo
et al., 1999), which are marked by other units of the exocysts (Boyd et al., 2004).
An additional possibility is that actin filaments, which
are involved in the translocation of salivary serous granules to a secretory surface (Segawa and Riva, 1996;
Jerdeva et al., 2005), are attached only to the spherulecontaining pole and pull this pole toward the cell surface
so that it perforce becomes the forepart of the granule
about to be exocytosed. The absence of obvious actin filaments in our preparations might be due to the wellknown propensity of osmium tetroxide to cause the depolymerization of this molecule (Boyles et al., 1985).
The presence of an ostensibly polarized membrane on
the saddleback tamarin serous granules raises some in-
triguing questions. Freeze-fracture studies of rat parotid
serous granules in the process of exocytosis reveal that
at the zone of contact between granules and plasmalemma, there is a marked difference in the density of
intramembrane particles, with the granule membranes
having a low density and the plasma membrane having
a high density (De Camilli et al., 1976; Tanaka, 1980).
As a result, during release of the secretory product and
briefly thereafter, the luminal membrane has a mosaic
arrangement. After (and even during) exocytosis, the
excess luminal membranes are retrieved by endocytosis
(Amsterdam et al., 1969) by a calcium-dependent mechanism (Koike and Meldolesi, 1981); this reuptake is
highly specific for those patches originating from the
exocytosed granules (Meldolesi and Ceccarelli, 1981).
The fate of these recaptured membranes still is controversial. They clearly are recycled, but in what fashion?
Are they used exclusively to delimit nascent granules?
Do they become incorporated into the general membrane
complement of the cell? Are they degraded and their
components used in the de novo synthesis of the sundry
cellular membranes?
Because serous granules in the saddleback tamarin
parotids were not subjected to freeze-fracture analysis,
the status of intramembrane particles on the leader
bulge versus the remainder of the granule membrane is
unknown. Freeze-fracture studies of pancreatic islet cell
granules, which have no obvious polarity in thin sections, reveal a highly circumscribed aggregate of particles on their P-face (Berger et al. 1975); in other words,
the granule membranes in these cells do not have a homogeneous structure. If such aggregates overlie the
bulges in the tamarin granules, are they leader domains
and can they be distinguished from the plasmalemma
once fusion has been achieved? Are such patches selectively removed from the cell surface during recovery
from an exocytotic event? Once internalized, do they
have the same or a different fate from indifferent exocytotic membranes?
Comparative Considerations
Compelling examples of structurally polarized secretory granules are found in certain ciliated protozoa,
including Paramecium and Tetrahymena. In these protozoa, trichocysts, which are internally polarized elliptical
secretory structures (Bannister, 1972), become joined to
the plasmalemma only at their anterior, rounded end in
a junction that involves a particulate annulus on their
limiting membranes, and a little knob at the tip of the
trichocyst (Beisson et al., 1980). In Tetrahymena, when
an elliptical mucocyst approaches the plasma membrane, an annulus of particles forms at its leading end
(Satir et al., 1973). A similar phenomenon occurs in the
extrusosomes of the actinopod, Heterophrys marina
(Davidson, 1976).
In the lactating rat mammary gland, secretory granules are partially or completely coated with bristles
(Franke et al., 1976). Most of the granules in early
stages of exocytosis illustrated by these workers have a
partial bristle coat and it is this membrane zone that is
in contact with the plasmalemma, strongly suggesting
that these granules are in fact polarized. In the same
vein, a freeze-fracture study of bovine chromaffin granules revealed that in early stages of exocytosis there are
AROTID GLANDS OF TAMARINS
bridges, presumably proteinaceous, that connect the
granule membrane to the plasmalemma (Aunis et al.,
1979).
An example of secretory granules that may have physiological polarity in the absence of structural indications
in thin sections are pancreatic exocrine granules of the
rat. Using Helix pomatia lectin-gold, Kan and Bendayan
(1989) demonstrated immunocytochemically that the
lectin-binding glycoconjugates are unevenly distributed
on the granule surface and that the labeled surfaces are
the ones that join the plasmalemma during exocytosis.
Granule Pseudopodia
In a number of cell types, including parotid serous
cells of the rat (Schramm et al., 1972; Zellinger et al.,
1974) and olive baboon (Tandler and Erlandson, 1976),
secretory cells of the shell membrane-secreting gland of
the duck (Sandborn et al., 1975), neurosecretory cells in
the neurohypophysis of the mouse (Castel, 1977), and
peripolar cells in the kidney of the sheep (Ryan et al.,
1982), granules approaching luminal membranes often
form pseudopodia that become attached to the plasmalemma. All of the foregoing examples of granule pseudopodia were observed by conventional transmission
electron microscopy. Odajima and Nakane (1984) noted
the same phenomenon in quick-frozen rat submandibular acinar cells, as did Tanaka (1980) in freeze-fractured
pancreatic acinar cells. Granule contents are expelled
via these extensions, leaving behind invaginations of the
luminal membrane that are shaped like Florence flasks.
It is unclear as to whether these pseudopodia form only
in relation to specialized zones of the granule membrane
or can originate from any spot on the granule surface. If
they are restricted as to point of origin, pseudopodia
would be another indication of polarized secretory granules.
An example of structurally polarized granules whose
exocytosis remains conjectural is to be found in the
so-called rodlet cells, a peculiar cell type occurring in
relation to some, but not all, chemosensory cells of the
zebrafish (Dezfuli et al., 2007). The rodlet cells contain
cytoplasmic ‘‘inclusions’’ (original authors’ term), which
are implied to be secretory granules, albeit of unusual
shape. These inclusions consist of a major portion that
is ovate, and a single long, tubular projection that is
pointed toward the cell apex. A dense core runs the
length of the inclusion and may furnish the necessary
stiffness to maintain its asymmetric form. The authors
claim that the ends of these projections pierce the apical
membrane, implying that the contents of the inclusions
might eventually be exocytosed, but close inspection of
their published micrographs suggests that the putative
portions of the projections lying above the plasmalemma
actually are microvilli. The precise excretory status of
these polarized inclusions in the secretory cycle remains
to be established, but whatever it may turn out to be,
they are highly polarized and maintain a strict orientation vis-à-vis the apical plasma membrane.
Compound Exocytosis
In many species, e.g., the rat (Amsterdam et al.,
1969), parotid endpiece cells engage in compound (chain)
exocytosis where secretory granules fuse in turn to the
1259
granule membrane of their merocrine predecessor ultimately to form a channel of catenated empty granule
membranes that debouches into a lumen. In the tamarin, the spherule-laden bulge is what attaches to the
invaginated membranes. In this process, the membranes
surrounding the now empty granule remnants must
take on the characteristics of the plasmalemma so that
further granules recognize them as potential docking
sites. In the pancreatic acinar cell, it has been shown by
confocal immunofluorescence microscopy that protein
attachment protein acceptors, such as syntaxin 2, extend
from the plasmalemma into the membranes of fused
granules (Pickett et al., 2005).
In the rat parotid gland, secretory granules in unstimulated cells occasionally become closely apposed to
form pentalaminar membranous barriers between their
respective contents (Tanaka, 1982). In the saddleback
tamarin, no examples of the granule bulge were encountered that formed such focal appositions with neighboring granules, indicating that the bulges are programmed
to interact solely with surface membranes, whether of
primary or secondary origin.
Based on the many foregoing studies, it would appear
that ultrastructural cyto- and immunocytochemical studies of molecules that have been implicated in secretory
granule exocytosis where there is no obvious structural
polarity might reveal an unsuspected differentiation of
granule membranes.
Luminal Contents
Finally, the contents of the endpiece lumina in the
saddleback tamarins deserve comment. This globular
dense material is reminiscent of neutral lipids that have
been blackened by osmium tetroxide. The larger globules
precisely match in size and appearance the spherules of
the serous granules. On the basis of the fact that the
spherules in poorly fixed serous granules in human submandibular glands sometimes form myelin figures, Tandler and Erlandson (1972) suggested that these structures consist in part of phospholipids. A histochemical
study of the same gland failed to identify any lipid in
the secretory granules (Sirigu et al., 1976), but similar
studies of rat parotid gland revealed the presence of lipoidal material in serous granules (Simson et al., 1973).
Biochemical studies of human saliva have established
that lipids are present in small quantities in this fluid
(Mandel and Einstein, 1969; Rabinowitz and Shannon,
1975; Slomiany et al., 1985; Larsson et al., 1996). Small
amounts of phospholipids conceivably could be added to
saliva as the result of membrane shedding during exocytosis (Doljanski and Kapeller, 1976). In the saddleback
tamarin, the dense luminal globules in the endpieces
and proximal intercalated ducts are completely absent
from the striated and excretory ducts, indicating that
they have been disassembled.
Saddleback tamarin saliva contains twice as much
total lipid as does human saliva (Murty et al., 1984).
Specialized components in saliva might give certain species access to dietary components that otherwise would
be off-limits to them (Tandler and Phillips, 1998). Lipids
in saliva might serve such a function in tamarins.
1260
TANDLER
CONCLUSIONS
It is obvious that regulated exocytosis of secretory
granules involves a complex set of biochemical and physiological interactions between the two membranes, granular and plasmalemmal. From an ultrastructural standpoint, the morphology of secretory granules may participate in or modify these interactions in an as yet
unrecognized fashion.
ACKNOWLEDGMENTS
The author is indebted to Dr. Barnett L. Levy for providing the tissue specimens used in this study and to
Drs. Alan Tartakoff and Richard Jurevic for a critical
reading of the manuscript.
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