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Ultrastructure of the cat sublingual gland.

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Ultrastructure of the Cat Sublingual Gland
D e p a r t m e n t of Oral Biology a n d M e d i c i n e , School of Dentzstry, Case W e s t e r n
Reserve U n i v e r s i t y , C l e v e l a n d , Ohio 441 0 6 , cind A n a t o m y D e p a r t m e n t C
a n d I n s t i t u t e of Medzcal Physioloqy A, U n i v e r s i t y of
C o p e n h n g e n , DK-2100 C o p e n h a g e n 0, D e n m a r k
The sublingual gland of the cat consists primarily of branched
secretory tubules that open into an abbreviated duct system. The simple epithelium that composes the secretory tubules consists of a n admixture of mucous
and serous cells, with the former predominating. Some secretory tubules are
capped by a serous demilune. Regardless of position, almost all serous cells have
prominent basal folds and border on at least one intercellular canaliculus as
well as on the tubule lumen. Serous cells possess a n extensive array of irregular,
distended cisternae of rough-surfaced endoplasmic reticulum that frequently
contain dense intracisternal granules. Serous granules are relatively few i n
number and rarely show evidence of substructure. Mucous cells, which lack
basal folds, contain a n apical mass of secretory material in the form of partially
fused droplets. The duct system is somewhat less ordered than in most major
salivary glands; secretory tubules empty into structures resembling intercalated
ducts or may be in direct continuity with ducts intermediate in morphology between intercalated and excretory ducts. The absence of striated ducts noted in
this study may be correlated with the high sodium content of cat sublingual
saliva. The main excretory duct of the sublingual gland closely resembles that
of the cat submandibular gland in terms of morphology, but exhibits little of the
transport functions reported in the latter duct.
Unlike other salivary glands in most species, the sublingual gland of the cat produces saliva that is isotonic, rather than
hypotonic (Lundberg, '57). The role in electrolyte and water transport of the various
histologic components of the cat sublingual
gland has recently been at least partially
determined by micropuncture studies (Kaladelfos and Young, '73). While the light
microscopic appearance ( J h i , '40) and
histochemistry (Shackleford and Mapper,
'62; Fava-de-Moraes, '65; Leppi et al., '68;
Tachi, '72; Harrison, '74) of this gland are
well established, its ultrastructure, with
the exception of a brief description of the
myoepithelial cells (Garrett and Harrison,
'70) and of the localization of alkaline phosphatase (Davies and Garrett, '72), has not
been reported. This article describes the
fine structure of the sublingual gland in
the cat, and relates its architecture to the
available physiological data.
Sublingual glands from 15 adult mongrel
cats, both male and female, were used in
this study. The glands were fixed in conANAT. REC., 187: 153-172.
tinuity with the submandibular glands, i.e.,
fixative introduced into the submandibular
gland via the lingual or carotid artery also
reached and fixed the sublingual gland.
The fixatives used and their manner of application were detailed in previous communications (Tandler and Poulsen, '76a,b).
To recapitulate briefly, the initial fixative used i n this study was primarily a mixture of 2% parafonnaldehyde, 3 % glutaraldehyde, 1% acrolein, and 2.5% DMSO
in a phosphate buffer (final osmolality =
1,350 mOs/kg HzO) (Kalt and Tandler, '71).
This mixture was warmed to 3 8 4 0 ° C before perfusion was initiated. After rinsing
in buffered sucrose, tissue specimens were
postfixed in 2% osmium tetroxide in a
phosphate buffer (363 mOs/kg HzO). After
osmication, the tissue blocks were rinsed,
soaked overnight in cold 0 . 5 % uranyl acetate, rinsed once again, dehydrated in
graded ethanol, and embedded in Epon
(Luft, '61). Thin sections were serially
stained with uranyl acetate (Stempak and
Ward, '64) and either lead citrate (ReynReceived June 10, ' 7 6 . Accepted Aug. 26, ' 7 6
Fig. 1 Survey photomicrograph showing the
arrangement of the secretory elements of the cat
sublingual gland. The gland consists of branched
secretory tubules that are predominantly mucous
i n nature. Toluidine blue. X 225.
olds, '63) or lead tartrate (Millonig, 'Sl),
or were stained solely with bismuth subnitrate (Riva, '74). Such sections were examined in either a Siemens Elmiskop l a
or Philips 300 electron microscope. Sections 1 wm thick were stained with toluidine blue and examined and photographed
in a Zeiss Ultraphot 11.
The sublingual gland of the cat consists
primarily of fairly long, branched secretory
tubules that are of greatest diameter a t
their blind (proximal) ends and that are
slightly tapered distally (fig. 1). The tubule
walls are composed of a simple epithelium
in which mucous cells predominate. The
tubules are usually capped by a serous
demilune. In many instances, demilune
cells may extend between mucous cells to
border directly on the lumen of the tubule
(figs. 2, 3). Some serous cells with no obvious relationship to demilunes may be scat-
Fig. 2 Photomicrograph demonstrating the
two cell types that make u p the secretory tubules.
Serous cells are identified by their dense, compact
secretory granules, while mucous cells contain
larger, lightly stained mucous droplets. An intercellular canaliculus, outlined i n longitudinal section by serous granules, is seen in the lower tubule
(double arrow), and two transversely-sectioned
canaliculi i n the upper tubule are similarly surrounded by granules (single arrows). Toluidine blue.
x 1.000
tered between mucous cells. Demilune cells
without access to the tubule lumen empty
their secretory products into a system of
microvillus-lined intercellular canaliculi,
which course between the mucous cells to
eventually debouch into the lumen (figs.
2, 5). Even those demilune cells that reach
the tubule lumen may also border on a
canaliculus. Some serous cells, whether or
not a part of a demilune, have prominent
basal folds similar to those described in
acinar cells of the human submandibular
gland (Tandler, '62) (fig. 4). As in the latter organ, the folds may be in close relation to the terminus of an intercellular
canaliculus (fig. 5). In contrast to serous
cells, all of the mucous cells lack basal
surface specialization. Myoepithelial cells
are present at the proximal ends of the
secretory tubules, where they are situated
between the basal lamina and the overlying secretory cells (fig. 3). Myoepithelial
cell processes extend distally over the basal
surfaces of demilune cells and tubule cells
alike, and are bound to these cells by occasional desmosomes. Some processes may
reach the most proximal duct cells.
The most obvious cytological feature of
the serous cells is their extensive roughsurfaced endoplasmic reticulum (RER)
(figs. 3, 6). Rather than consisting of parallel arrays of flattened infranuclear cisternae as in the serous cells of the human
submandibular gland (Tandler and Erlandson, '72), the RER of cat sublingual gland
serous cells is composed of irregular, highly distended cisternae that occupy not only
the bulk of the infranuclear cytoplasm, but
the lion's share of the apical cytoplasm as
well. The dilatation of the RER cisternae is
not a fixation artefact, since the RER in
nearby plasma cells is completely normal
in appearance (fig. 7). The cisternae in the
serous cells contain a homogeneous, finely
fibrillo-granular material of moderate density (fig. 6). In a few serous cells of some
of the glands examined, intracisternal inclusions are present (fig. 8). These are
fairly dense, have rather uneven edges, and
measure up to 1.2 pm in diameter. In the
basal cytoplasm, the cytosol between cisternae contains numerous free ribosomes
and a considerable number of rod-shaped
mitochondria with transverse cristae. Above
the nucleus is a Golgi complex. Some RER
cisternae in the vicinity of this organelle
show evidence of bud formation, and may
be considered to represent transitional elements. The supranuclear cytoplasm between RER cisternae contains some lysosome-like bodies and a variable number of
secretory granules (fig. 9). These serous
granules measure about 1 pm, and are
delimited by a single membrane. They are
of moderate density, and usually lack a n y
substructure. In granules of some cells,
however, a small dense spherule may be
present, while in other cells the granule
matrix may contain small areas of low electron-density (fig. 10).
The mucous cells vary in appearance
according to the amount of mucus they
contain. This mucus is in the fonn of droplets whose limiting membranes are preserved only with the greatest difficulty. In
mucous cells containing numerous mu-
cous droplets, these bodies show a strong
tendency to fuse, forming a continuous
mass of secretory material in which the
disrupted outlines of the original droplets
may still be identifiable (fig. 11). The contents of the droplets are finely reticulate
and of low density. In some cells, the mucous droplets may contain a relatively dense
inclusion that always seems to adhere to
the membrane (fig. 13).
The organelles of the mucous cells are
best seen in those cells that have relatively
few secretory droplets. In such cells, the
supranuclear Golgi complex is observed to
be quite extensive, consisting of stacked
saccules, vacuoles of various sizes, and
numerous vesicles, both coated and smooth
(fig. 12). The saccules, which are usually
more than seven in number, are flattened
and closely packed in the center of the
stack, but those on the surface may exhibit
some distention. In some Golgi complexes,
coated vesicles may be observed in direct
continuity with the edge of a saccule (fig.
12). All Golgi vacuoles, regardless of size.
contain material identical in appearance
to that in the mucous droplets, and undoubtedly represent nascent droplets. Transitional elements of the RER may be present near the entrance face of the Golgi.
In mucous cells at the beginning of their
secretory cycle, there is a substantial
amount of RER. The cisternae of these cells
are quite different from those in neighboring serous cells. In mucous cells, they tend
to have a round or oval profile, with none
of the irregularity of outline seen in the
serous cells. Furthermore, their content is
of a coarser texture in the mucous cells.
These differences in appearance of the
RER in the two cell types are shown to advantage in figure 14.
As the mucous cell fills with mucus, both
the Golgi complex and RER appear to involute, until the former is represented by
one or two small dictyosomes between the
nucleus and the secretory mass, and the
latter by a few scattered cisternae.
Some mucous cells in several of the specimens contained large lipid inclusions
(fig. 15). Instead of having an even texture,
as is usually the case. these lipid droplets
contain a variety of irregular membranelike formations or negative images of acicular material often covered by minute particles of high electron-density.
The duct system of the cat sublingual
gland is relatively inconspicuous. Some
secretory tubules empty into ducts that
have the general appearance of intercalated ducts, while others are directly confluent with ducts that have a morphological appearance intermediate between intercalated and excretory ducts. Still other
tubules are connected to the main excretory duct of the gland. In this study, no
striated ducts were observed.
The intercalated-type ducts consist of a
simple low cuboidal epithelium with occasional myoepithelial processes (fig. 16). The
duct cells lack microvilli and show few lateral interdigitations with their neighbors.
While the cytoplasm appears active, there
is little evidence of secretory granule formation. The intermediate ducts have a
larger lumen than the preceding ducts,
and are composed of pseudostratified epithelium consisting of cuboidal cells and
very flat basal cells. The cuboidal cells,
which display some lateral interlocking,
are cytologically unremarkable. Basal cells
are characterized by the large number of
hemidesmosomes on their basal surface.
The main excretory duct of the sublingual
gland is virtually identical in structure to
the same duct in the submandibular gland
of the same animal, the cat (Tandler and
Poulsen, '76b) (fig. 17). The basal cells of
the pseudostratified epithelium comprising
the wall of the main duct in the sublingual
gland are considerably paler than the adjacent tall cells, as well as being paler than
their counterparts in the cat submandibular gland (fig. 18).
suggest that the secretory potential in
acinar cells is related to permeability
changes that may occur at least at the
contraluminal membrane upon the initiation of stimulation. The system of basal
folds present in the serous cells of the cat
sublingual gland greatly increases their
basal surface area and would markedly
enhance diffusion based on altered permeability. Demilune cells in the cat submandibular gland have a morphology similar
to those in cat sublingual gland, albeit a
different type of secretory product. A recent autoradiographic study of these cells
in the cat submandibular gland has shown
that only they, and not the acinar cells,
have (Na+-K+)-ATPaseactivity on their
plasma membranes (Poulsen et al., '75).
This observation suggests that serous cells
in the cat sublingual gland may have similar membrane properties. Moreover, these
sublingual serous cells, even when they
reach the tubule lumen, are usually associated with intercellular canaliculi, structures which are necessary to set up the
standing gradient that is responsible for
the formation of an isotonic secretion (Diamond, '71 ; Kaladelfos and Young, '73).
Compared to serous-type cells in salivary
glands of many other mammals, the serous
cells of the cat sublingual gland have a
rather unusual appearance. They are characterized by abundant irregular RER cisternae greatly distended by their content
of moderately dense material. Furthermore,
these RER elements often contain intracisternal granules. While frequently observed
in cells of the exocrine pancreas, such
granules are extremely rare in salivary
glands, having been described only in the
Micropuncture studies of the cat sub- resting parotid of the baboon (Tandler and
lingual gland by Kaladelfos and Young Erlandson, '76) and in the electrically('73) have demonstrated that saliva is pro- stimulated parotid of the rabbit (Fujimoto
duced in this organ by a two-stage process. et al., '72). One can make the generalizaThe primary secretion, which has a plas- tion that in any exocrine cell the overall
ma-like electrolyte composition, is elabo- appearance of the protein-secreting apparated by acinar (tubular) cells. As this ratus depends on the relative rate of activsaliva passes through the abbreviated duct ity of each of its several components. Thus
system, i t is modified by the addition of C1 it would appear that in the cat sublingual
in exchange for HC03.
gland, transfer of protein from the RER to
Based on the present study, it seems condensing vacuoles does not keep pace
reasonable to conclude that it is the serous with synthesis of new protein. Because the
cells, both demilunar and tubular, that are packaging process is, relatively speaking,
responsible for production of initial saliva sluggish, protein accumulates within the
having electrolyte concentrations similar cisternae, where, when the concentration
to those of plasma. Schneyer et al. ('72) reaches some threshold level, i t precipitates
in the form of intracisternal granules. The
absence of highly dilated Golgi saccules or
of large accumulations of condensing vacuoles or secretory granules militates against
the bottleneck in the handling of protein
existing more distally along the secretory
The secretory granules of the serous
cells in cat sublingual gland are few in
number and show little evidence of substructure. In a histochemical investigation
(Tachi, ’72), it was found that these granules are PAS-positive, and probably contain neutral mucopolysaccharides, sialomucin, and sulfomucin. Harrison (‘74) reported on the histochemistry of cells in the
cat sublingual gland that contained discrete granules of “mucin” in contrast to
other cells whose luminal part was occupied by “diffuse mucin.” Based on our ultrastructural findings, we interpret the
former cells as being equivalent to serous
cells, while the latter represent mucous
cells. According to Harrison, the secretory
material in the serous cells contains acid
and neutral mucosubstances. In the present study, no serous granules were observed
discharging their contents into lumina,
but they probably do so by a typical merocrine process such as occurs in the serous
cells of the hypotonic-secreting sublingual
gland of the rat (Kim et al., ’72; Kim and
Han, ’75).
Although the mucous cells of the cat
sublingual gland are typical in appearance,
their secretory droplets have a different
substructure than that of mucous droplets
in both acinar and demilunar cells in the
submandibular gland of the same animal
(Shackleford and Wilborn, ’70; Tandler
and Poulsen, ’76a). This observation parallels that of Riva et al. (‘74) who found that
serous granules had distinctly different
morphologies in the three major human
salivary glands. According to Tachi (‘72),
the mucous cells of the cat sublingual
gland, like the serous cells, contain neutral
mucopolysaccharides, sialomucin, and sulfomucin, but the histochemical reactions
for these substances are more intense in
the former cell type. Harrison (‘74) reported
the presence of acid mucosubstance in the
mucous cells, and suggested that it contains a mixture of carboxyl and sulfate
groups different from that in other cat
salivary glands. Extending his studies to
enzyme histochemistry, Harrison found
both thiamine pyrophosphatase and nucleoside diphosphatase had a “Golgi-like” distribution in the mucous cells. This is in
keeping with our observation of an extensive Golgi complex in these cells, especially
those at the beginning of their secretory
cycle. The large amount of secretion product in the mucous cells was suggested by
Harrison to be related to the spontaneous
secretion by the cat sublingual gland, a
process that occurs without any secretory
Most major salivary glands possess a
complex system of excurrent ducts, including intercalated, striated, excretory, and
main excretory ducts. In those glands that
produce a hypotonic saliva, all ducts beyond the intercalated duct engage in reabsorption and secretion of electrolytes from
and into the saliva, with the striated ducts
being the most active in this regard
(Schneyer et al., ’72). This is certainly true
of rat sublingual glands, where micropuncture studies have shown saliva within striated ducts to be already hypotonic (Martin
and Young, ’71). Although striated duct
cells may occasionally be seen in the cat
sublingual gland by light microscopy (Harrison, ’74), none were observed in the present study, which was conducted primarily
at the ultrastructural level. It may be concluded that this relative paucity, if not outright absence, of striated ducts is responsible for the high Na content of cat sublingual saliva.
K+ concentration in the final sublingual
saliva of the cat is not greater than in the
primary fluid, a n unusual occurrence in
comparison to those exocrine glands so far
subjected to micropuncture analysis, where
high levels of K+ are the rule. Kaladelfos
and Young (‘73) conclude that the cat sublingual ducts lack transport mechanisms
for K+ as well as for Na+. Poulsen et al.
(‘75) have proposed that active transport
of monovalent cations in the duct system
of the cat submandibular gland is mediated
by (Na+-K+)-ATPase; the virtual absence
of this enzyme from ducts of the cat sublingual gland lends support to the conclusion reached by Kaladelfos and Young (‘73).
With respect to K+ in cat sublingual gland,
Schneyer et al. (’72) suggest that acinar
cells possess a transport mechanism for
this electrolyte that is responsible for the
concentration gradient of K+ between initial saliva and interstitial fluid in the unstimulated gland. This proposition is based
on acceptance of the notion that cat sublingual glands lack intercalated ducts.
While our observations show that these
glands do in fact have intercalated ducts,
their morphology is not indicative of a
transport function. It is for this reason,
coupled with the observed absence of (Na+K+)-ATPase from these ducts, that we are
in agreement with Schneyer et al. (‘72)
that the transport mechanism in question
resides in the acinar (probably serous) cells
of the cat sublingual gland.
The main excretory duct of the cat sublingual glands bears a remarkable morphological resemblance to the MED of the cat
submandibular gland (Tandler and Poulsen, ’76b). Functionally, however, these
two ducts are widely divergent. The submandibular MED probably engages in significant electrolyte transport, while the
sublingual MED either transports Na at
such a low level as to be undetectable or
eschews this activity altogether. These observations illustrate the pitfalls inherent
in attributing similar functions to structurally similar components in different
types of salivary glands, even if these organs are derived from the same animal.
We are grateful to Professor Harald Moe
for making the facilities of his department
available to us, and for his unfailing interest and encouragement. Mrs. Susan
Max-Jacobsen and Mrs. Lene Caroc provided expert technical assistance.
Supported in part by National Institutes
of Health Grant 5 SO7 HR 05335-15 and
by a grant from the Danish Medical Research Council.
A portion of this work was performed
while the senior author was o n sabbatical
leave a t the University of Copenhagen.
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BF, Basal folds
IC, Intercellular
LU, Lumen
MC, Mucous cell
MED, Main excretory duct
MYO, Myoepithelial cell
SC, Serous cell
Survey electron micrograph of the terminus of a secretory tubule showing the arrangement of mucous and serous cells. Note that the serous
cells on the left border directly o n the lumen of the secretory tubule. A
myoepithelial cell process extends across the base of both types of secretory cells. X 5,800.
Bernard Tandler a n d Jdrgen Kedemark Poulsen
The base of a serous cell showing the extensive system of basal folds,
which are devoid of organelles. X 16,700.
A montage of electron micrographs showing a microvillus-lined intercellular canaliculus extending from the tubule lumen to a position near
the base of two neighboring serous cells. Note the close relationship
between the canaliculus and the basal folds. X 10,800,
Bernard Tandler and Jdrgen Hedemark Poulsen
Dilated cisternae of rough-surfaced endoplasmic reticulum in a typical
serous cell. X 19,000.
The basal portion of a serous cell in close relation to an interstitial
plasma cell. Although the RER i n the serous cell is dilated, that within
the plasma cells shows no evidence of dilatation. Such contrasting configurations of RER in juxtaposed cells strongly supports the idea that
the observed irregularity of this organelle in serous cells is not an artefact. x 8,500.
Dense intracisternal granules i n the basal cytoplasm of a serous cell.
X 19,800.
Bernard Tandler and Jdrgen Hedemark Poulsen
The supranuclear cytoplasm of a serous cell bordering on a tubule
lumen. Cisternae of RER and serous granules are evident. X 19,000.
These serous granules, which are close to a tubule lumen (upper left
corner), show evidence of substructure. X 17,000.
The apical portion of a mucous cell showing a mass of partially fused
mucous droplets. X 12,800.
Bernard Tandler and J0rgen Hedemark Poulsen
The Golgi complex of a mucous cell early in the secretory cycle. Buds
arising from transitional elements of RER are indicated by arrows. A
coated vesicle in apparent continuity with a Golgi saccule is indicated
by the asterisk. X 45,000.
A mucous droplet with a dense peripheral inclusion. X 22,000.
A comparison of RER in a serous cell (lower left) with that in a mucous
cell (upper right). Note that this organelle differs in the two cell types
with regard to shape and content ofcisternae. X 19,500.
A lipid droplet in a mucous cell, exhibiting electron-lucent, possibly
crystalline material. X 8,500.
Bernard Tandler and J6rgen Hedenlark Poulsen
An intercalated-type duct. A fibroblast extends along the bottom of the
micrograph. X 6,500.
Photomicrograph of the connection between sublingual gland secretory
elements (right) and the main excretory duct of the gland. The duct
has a n irregular lumen and consists of pseudostratified epithelium.
Note the high degree of vascularization of the duct; the patency of the
surrounding small vessels is due to successful perfusion fixation. A ganglion is present at the lower border of the micrograph. Toluidine blue.
x 225.
Survey electron micrograph of a portion of the wall of a main excretory duct. The lighter basal cells have a n irregular basal surface with
numerous hemidesmosomes. X 3,100.
Bernard Tandler and Jbrgen Hedemark Poulsen
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ultrastructure, cat, sublingual, gland
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