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Ultrastructural changes of secretory cells of salamander lingual salivary glands under varying conditions.

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THE ANATOMICAL RECORD 243:303-311 (1995)
Ultrastructural Changes of Secretory Cells of Salamander L
Salivary Glands Under Varying Conditions
Department of Histology, School of Dentistry, The Nippon Dental University, Chiyoda-ku,
Tokyo, Japan
Background: In general the ultrastructure of secretory
cells can be modified under secretory stimulated and non-stimulated conditions. The ultrastructure of the lingual salivary glands of hibernating
salamanders in the natural environment was examined and compared to
those of fasted and fed animals kept in the laboratory.
Methods: Hibernating salamanders of the species Hynobius tokyoensis
were collected from the natural environment during the winter breeding
season and sacrificed for this study. One group was sacrificed immediately,
another group was kept under fasted condition, and another group was
regularly fed; both of the latter groups were kept at room temperature for
1month and then sacrificed. The tongue was fixed for electron microscopy
and processed by conventional methods, and semithin sections were histochemically examined for glycoconjugates.
Results: The lingual salivary glands of this salamander species were composed of simple or often branched tubular glands opening onto the dorsal
surface of the tongue. The secretory cells which composed their terminal
portions were all columnar in morphology and histochemically mucous in
nature. Under hibernation or prolonged fasting at room temperature, the
mucous granules of these columnar secretory cells were decreased in number and the Golgi apparatus appeared inactive. A conspicuous structural
peculiarity was multiple fingerprint-like structures of the rough-surfaced
endoplasmic reticulum (RER). Most of these membranes were composed of
stacks of tightly packed cisternae. Under regular feeding, the mucous granules were closely packed in the cytoplasm of the secretory cells and the
basal nucleus was slightly enlarged. The Golgi apparatus showed progressive activation with distended saccules. The unique membranous arrangement of the RER which was observed in the fasting animals was completely
absent, and the cisternae were irregular in width with considerable variation of the intercisternal spaces.
Conclusions: The tongue of the salamander H. tokyoensis has numerous
tubular salivary glands which are mucous in nature. The architecture of
the organelles in the secretory cells is subject to modification in response to
the cellular metabolism. o 1995 Wiiey-Liss, Inc.
Key words: Whorls of rough-surfaced endoplasmic reticulum, Golgi apparatus, Lingual salivary glands, Ultrastructure, Hibernation,
Salamander, Amphibia
The putative alteration of the architecture of intracellular organelles according to cellular metabolism
has been documented in some endocrine and exocrine
secretory cells. Species inhabiting the temperate zone
have developed adaptive responses to the exposure to
seasonal variation. The metabolism of hibernators is
very low under fasting condition and at the low ambient temperatures that prevail during the hibernation
period. Therefore, they are suitable materials to look
into the reversible modifications of the secretory cells.
The pancreas tissues, for example, have been studied in
a few species of hibernators (Watari, 1968; Poort and
Geuze, 1969; Geuze, 1970). However, to our knowledge
there are no data available on the synthetic activity of
the salivary glands in hibernators during hibernation
or during the period of awakening after hibernation.
Received December 12, 1994; accepted July 7, 1995.
Address reprint requests to Shingo Kurabuchi, Department of Histology, School of Dentistry at Tokyo, The Nippon Dental University,
Chiyoda-ku, Fujimi 1-9-20, Tokyo 102, Japan.
Fig. 1. Light micrographs of lingual salivary glands of salamander
Hynobius tokyoensis. a: A cross-section of the tongue. Numerous tubular glands are closely packed, opening onto the dorsum of the
tongue. Hematoxylin and eosin. x 50. b: Goblet-cells scattered a t the
neck of the tubular glands. Arrows: opening ducts of tubular glands.
Alcian blue. X 160. c: Columnar secretory cells form a single layer
lining the terminal portion of several tubular glands. L, lumen. Alcian blue. x 160.
Fig. 2. Tubular terminal portions of lingual salivary glands in the animals in the hibernation group (a),
fasted group a t moderate temperature (b),and fed group (c).Heidenhain’s iron hematoxylin. x 450.
Only a few histological and histochemical studies have
been conducted in the lingual salivary glands of
urodele amphibia (Saegusa, 1943; Francis, 1961; Zylberberg, 1973, 1977; Fahrmann, 1974; Kurabuchi,
1986), and the ultrastructure of these glands has been
documented in only a few species (Fahrmann, 1974,
1975; Zylberberg, 1977). The present report describes
the ultrastructural features of the secretory cells of the
lingual salivary glands of the salamander Hynobius
tokyoensis during hibernation in the natural environment, and under feeding and fasted condition while
kept a t room temperature in our laboratory.
The Japanese salamander Hynobius tokyoensis was
used in this study. Adult males and females with a
total body length of about 9 cm were gathered near a
gentle flowing stream during the breeding season in
late winter and early spring. They had been exposed to
low temperature and prolonged fasting conditions, as
evidenced by the lack of gastric intestinal food content.
Immediately after collection, 10 salamanders were sacrificed for examination of the ultrastructure under the
hibernating condition. Next, to eliminate the effect of
recent exposure to low temperatures, the following two
groups of 10 salamanders each were cared for in our
laboratory: one group kept in an aquarium at room
temperature (18-24°C on a 12L/12Dphotocycle) without food for 1 month (the fasted group), and another
group also kept a t room temperature but regularly fed
tubifex for 1 month (the feeding group). Salamanders
in both these groups were sacrificed at 1 month.
The salamander was anesthetized with 0.5%MS 222
(Sandoz)and the upper jaw and tongue were dissected
and immersed for 6 hr in a cold Karnovsky solution
containing 2.5% glutaraldehyde and 2% paraformaldehyde in a cacodylate buffer at pH 7.4. The tongue was
then trimmed into several pieces and postfixed in 1%
cacodylate-bufferedosmium tetroxide solution for 1hr.
After being dehydrated in a graded series of ethanol
solutions, it was embedded in epoxy-resin, and sliced
into ultrathin sections that were stained with uranyl
acetate and lead citrate and then examined with a
transmission electron microscope (JEOL, JEM2000EXII).
The 2-pm-thick epoxy-resin embedded sections were
deresined (Imai et al., 1968) and routinely stained with
hematoxylin-eosin or Heidenhain’s iron hematoxylin,
while the adjacent sections were subjected to histochemical techniques. The periodic acid Schiff (PAS)
technique for neutral mucosubstances (MacManus,
1946) and Alcian blue 8 GX at pH 2.5 for acidic mucosubstances (Lison, 1954)were employed to examine the
histochemical nature of the lingual gland secretory
Light Microscopy
When viewed as semithin sections, the lingual salivary glands appeared composed of a series of numerous
simple non-branched or occasionally simple branched
tubular glands, all of which were closely packed and
opened onto the dorsal surface of the tongue (Fig. la).
The basal one-third of the tubular glands extended into
the tongue muscle. The secretory cells were scattered
on the dorsal epithelium of the tongue and around the
duct of every tubular gland and had expanded cupshaped rims of cytoplasm filled with mucous granules,
which were stained by the PAS reaction and Alcian
blue staining (Fig. lb). Thus, in terms of their shape
and staining pattern, the secretory cells were similar
to mammalian goblet cells. The terminal portion of every tubular gland examined consisted of columnar
secretory cells arranged in the form of simple columnar
epithelium. Their secretory granules exhibited reactions to Alcian blue (Fig. h)and weak reactions to PAS
but were entirely unstained by Heidenhain’s iron hematoxylin (Fig. 2), indicating that their secretory granules were mucous in nature and mainly contained acid
mucopolysaccharides. These columnar secretory cells
showed conspicuous structural variation according to
the conditions under which each group of animals was
kept. In the hibernating animals and the fasting animals kept at room temperature, almost all columnar
secretory cells in the tubular glands contained only a
few mucous granules adjacent to the lumen (Fig. 2a
and b). In the regularly fed animals, the supra-nuclear
cytoplasm of almost all of the secretory cells contained
numerous mucous granules (Fig. 2c). The nuclei and
secretory cells were somewhat larger in the glands of
the fed animals than those in the hibernating or fasted
animals, and the lumina of the tubular glands were
Electron Microscopy
In every group of animals, the secretory cells composing the terminal portion of every tubular gland in
the tongue had an ultrastructurally smooth base that
was attached to the basal lamina by hemidesmosomes,
lateral processes that engaged with similar processes
projecting from adjacent cells, and a free surface that
contained several microvilli. The roughly spherical nucleus located near the base of the cell, was surrounded
by an extensive rough-surfaced endoplasmic reticulum
(RER) and topped by a Golgi apparatus. The secretory
granules had an electron-lucent and structureless content, and were typically mucous in appearance. However, the state of preservation of the membrane-enveloped mucous was often poor, mainly to due artifactural
swelling of mucigen droplets during the fixation with
chemical reagents (see Ichikawa et al., 1987). The ultrastructural features of these columnar secretory cells
showed distinct modifications, described below, according to whether the animal had been in hibernation,
fasted at room temperature, or regularly fed.
In hibernation
In the lingual salivary glands of hibernating animals, as shown in Figure 3, each columnar secretory
cell contained only a few large (500-1,400 nm in diameter) mucous granules clustered and occasionally fused
to each other at the apical-most one-quarter to one-fifth
of the cell, and a roughly spherical nucleus near the
base. Rather small mucous granules, vacuoles, inclusion bodies, and a Golgi apparatus were coalesced in a
supra-nuclear group. The inclusion bodies were irregularly shaped but uniformly electron-dense, sometimes
containing vacuoles, which were larger in size and
more numerous than those in the columnar cells in the
feeding animals. The loci of the Golgi apparatus were
dispersed in a supra- and para-nuclear zone, and this
organelle was mingled with a group of small mucous
granules and other organelles. At higher magnification
(Fig. 4), the Golgi apparatus was seen to be composed of
about 5-6 mostly flattened saccules with moderately
dilated edges. The other portion of the cytoplasm was
occupied by RER. The RER cisternae showed uniformly
parallel arrangement in typical lamellar fashion, constructing concentric circles forming whorls or whorl
modifications in several areas of the cytoplasm, thus
resembling the pattern of a fingerprint (Fig. 5). The
distance between adjacent RER lamellae was fairly
uniform, as was the width of the intracisternal spaces.
However, the arrangement and density of the RER varied from cell to cell, and thus, the cytoplasmic electron
density of the secretory cells showed some variation.
Fenestration, as described in pancreatic acinar cells by
Orci et al. (1972), i.e., sites of pinching together of the
cisternal membranes of the RER, was seen at several
points. Some of the whorls were tightly rolled without
any entrapped cytoplasm, while others showed somewhat concentric rings of cytoplasm at the center and a
slightly deviated edge. In the center of the whorls were
seen mitochondria, smooth-surfaced vacuoles, and elec-
Figs. 3-5.
Fig. 6. Electron micrograph of columnar secretory cells of lingual
salivary glands in a salamander kept under fasting condition at moderate temperature. Mucous granules are relatively rich in these cells.
The supra- and para-nuclear regions are occupied by RER, in which
well-developed fingerprint-like architecture is seen. G, Golgi apparatus; I, electron-dense inclusions; L, lumen; N, nucleus. x 6,000.
tron-dense bodies, and occasionally large mucous granules and fat droplets.
Fed at room temperature
Fasted at room temperature
In the fasted animals, the ultrastructure of the columnar secretory cells of the lingual salivary glands
was essentially the same as that in the hibernating
animals. The Golgi complex had a compact structure
and the fingerprint-like architecture of the RER in the
columnar secretory cells was also prominent (Fig. 6).
Fig. 3-5. Electron micrographs of columnar secretory cells of lingual salivary glands in the animals in the hibernation group. Fig. 3.
Columnar secretory cells with fingerprint-like figures of RER. To apical quarter and supra-nuclear space are packed with secretory granules, the nucleus (N) is basally placed, and the other broad regions are
occupied by RER. BM, basement membrane; G, Golgi apparatus; I,
electron-dense inclusions; L, lumen. X 5,000. Fig. 4. The Golgi region
of a columnar secretory cell. Each cisterna of the Golgi apparatus (GI
shows deflation and mild dilation at the edge. M, mitochondria; N,
nucleus. x 23,000. Fig. 5. RER concentric whorl made up of closely
packed cisternae in a columnar secretory cell. Electron-dense inclusions (I), small mucous granules, and vacuoles (V) are seen at the
center of the whorl. Arrows indicate the interruptions of concentrically arranged RER. M, mitochondria. x 23,000. Inset: The spheroidal portion of a RER shows cisternae with reduced cavities.
x 120,000.
In the fed group, a large amount of mucous granules
was closely packed a t the apical two thirds of the columnar secretory cells, and the organelles were distributed mainly around a roughly spherical nucleus at the
base (Fig. 7). Fat droplets were not observed. Only a
few inclusion bodies were observed, but they were
smaller than those seen under the fasted or hibernating condition. The Golgi apparatus was larger than
that in either of the other two groups, and was easily
found even a t the supra- and para-nuclear position
(Fig. 8). As shown in Figure 9, the Golgi apparatus was
composed of 5 to 6 saccules, all of which were dilated
and had swollen margins. The RER was of the lamellar
type. However, their lamellae took a zig-zag form, the
membranes undulated, and the inter- and intra-cisternal spaces were somewhat irregular compared to the
RER arrangement observed in the fasted animals. Fenestrations as observed in the RER fingerprint-like architecture were rarely observed.
The tongues of the H. tokyoensis salamanders used in
this study were found to possess a large number of
tubular glands. The columnar secretory cells that composed the terminal portions of every tubular gland
Figs. 7-9.
were mucous in character, and the secretory granules
exhibited the typical histochemical reactions for acid
mucosubstances. In addition, their ultrastructural appearance is typical of that of mucous granules. The
discharge of secretions from the lumina of these salivary glands may have been caused by the contraction
of lingual muscle fibers within tubular glands since
every tubular terminal lacked myoepithelial cells. It
has been reported that the lingual salivary glands of
several species of salamanders and newts consist of tubular glands, although the newt’s tubular glands are
branched and intricate (Saegusa, 1943; Francis, 1961;
Zylberberg, 1973, 1977; Fahrmann, 1974, 1975;
Kurabuchi, 1986). Some of these glands, histochemically examined, are of a muco-serous nature (Zylberberg, 1973, 1977; Fahrmann, 1974, 1975; Kurabuchi,
1986), and, under electron microscopy, the secretory
granules appear as an lucent matrix, into which dense
material embedded (Fahrmann, 1974, 1975). Like the
salamander tongue, several species of lizards are also
known to have numerous tubular glands crowded in
the tongue (Gabe and Girons, 1969; Kochva, 1978;
Kurabuchi and Aiyama, 1987; Nagumo et al., 1988;
Rabinowitz and Tandler, 1991). As Rabinowitz and
Tandler (1991) pointed out in their report, secretion
from these salivary glands may be utilized in the capturing of prey and in swallowing. Moisture in the oral
cavity is maintained by goblet cells in the necks of
tubular glands and other oral mucosa. The present
study demonstrated that considerable ultrastructural
alterations occur in the columnar secretory cells of
these glands depending on whether the animals are
hibernating, fasted at moderate temperature, or fed. It
is well known that the variation in the appearance of
secretory cells reflects the degree of secretory activity
(Slot and Geuze, 1979; Godet et al., 1983). Therefore, it
is not surprising that, in these salamander lingual salivary glands, the feeding condition caused the columnar secretory cells to hypertrophy with considerable
increase in synthetic organelles, while hibernation
caused them to atrophy with decreased synthetic organelles. On the other hand, it has been indicated that
the number of zymogen granules in the pancreatic acinar cells increases during the late periods of amphibian hibernation, despite the fact that the animals are
hibernating (Poort and Geuze, 1969). This is probably
due to incidental temperature elevation. In the present
study, there were no ultrastructural differences between the group of animals in hibernation and in the
fasting group maintained at moderate temperature.
Therefore, the atrophic features of the columnar secre-
Fig. 7-9. Electron micrographs of columnar secretory cells of lingual salivary glands in salamanders kept under feeding condition.
Fig. 7. Columnar secretory cells contain a large amount of secretory
granules. The nucleus (N), RER, and other organelles are compressed
into the basal cytoplasm. BM, basement membrane; G; Golgi apparatus; I, electron-dense inclusions; L, lumen. X 4,300. Fig. 8. Basal area
of columnar secretory cells. Although the RER is of lamellar type,
RER are uniformly constituted of rather irregular cisternae. BM,
basement membrane; G , Golgi apparatus; N, nucleus. x 6,500. Fig. 9.
The Golgi region of a columnar secretory cell. The Golgi apparatus
(G), lying in the para-nuclear position, is composed of remarkably
dilated cisternae. M, mitochondria; N, nucleus. x 23,000.
tory cells were not caused by the prolonged fasting, but
by the low temperature during hibernation.
The degenerative modifications that were observed
in the columnar secretory cells of lingual salivary
glands in hibernating salamanders and those fasting
at moderate temperature but not observed in feeding
animals were reductions in the size of the nucleus and
Golgi apparatus, the unique arrangement of the RER,
and decrease of the number of mucous granules. Similar observations have been made in pancreatic acinar
cells of bats during artificial hibernation (Watari,
19681, lizards during seasonal starvation periods (Godet et al., 19831, starved frogs (Slot and Geuze, 1979),
hibernating frogs (Geuze, 19701, fasting mice (Nevalainen and Janigan, 1974) and rats placed on a protein-free diet (Weisblum et al., 19681, as well as in the
parotid salivary glands of rats on a diet of liquid Metrecal (Wilborn and Schneyer, 1970) or with actinomycin D administration (Han, 1967).However, in the current study, the columnar secretory cell size did not
significantly change under the varying conditions, although the acinar cells of rodent salivary glands have
been noted to be markedly enlarged according to the
state of hypertrophy (Hand and Ho, 1985) and undersized in the state of atrophy (Wilborn and Schneyer,
1970). Certain degenerative features of the secretory
cells suggest that the stages of the secretory process
(Jamieson and Palade, 1967, 1971; Palade, 1975) of
synthesis, intracellular transport, and release of secretory substances may have been inhibited.
The most obvious distinguishing feature in the secretory cells of the hibernating and fasted animals was
the fingerprint-like arrangement of RER, in which concentric whorls were formed. Membranous concentric
whorls of RER and smooth-surfaced ER (SER) have
been reported in several types of secretory cells and
their cytophysiological functions have been discussed.
It has been suggested that these whorls are centers for
the formation of new RER (Herman and Fitzgerald,
1962). However, in the atrophic pancreatic acinar cells
of starved and hibernating bats (Watari, 1968), lizards
(Godet et al., 1983), and fasting mice (Nevalainen and
Janigan, 1974), and of mice administered actinomycin
D (Rodriguez, 1967),it has been demonstrated that the
whorls of the RER membrane reflect reduced stimulation or atrophy of secretory cells. Taira (1981) noted the
temporary occurrence and disappearance of RER concentric whorls, demonstrating that in pancreatic acinar cells the whorls change reversibly according to the
fasting-refeeding conditions in newts and toads. The
same phenomenon was noted in the SER in adrenocortical cells of Mongolian gerbil adrenal glands not stimulated by ACTH, although the whorls disappeared
with ACTH administration (Nickerson and Curtis,
1969; Nickerson, 1970). That is, the most conceivable
scenario is that these membranous whorls of ER reflect
the atrophic state of secretory cells and that they act as
a membrane reservoir, disappearing when the production of secretory substances resumes. On the other
hand, irreversible changes in the RER concentric
whorls have been noted in the prostatic epithelial cells
of castrated rats when the whorls were enclosed by a
cellular membrane and later segregated as autophagic
vacuoles within the cells (Helminen and Ericsson,
1971). Irreversible changes were also seen in the RER
whorls of granular duct cells of suncus submandibular
glands, where the whorls were discharged into the lumen as apocrine-like processes (Mineda and Kasuga,
1985). Such irreversible features were not detected in
the present study of the columnar secretory cells of
salamander lingual salivary glands. However, some of
the smooth-surfaced vacuoles found in the center of the
whorl seem t o be derived from the RER, vesiculated
and devoid of ribosomes, as suggested in the whorls of
pancreatic acinar cells (Taira, 1981) and prostatic epithelial cells (Helminen and Ericsson, 1971). It cannot
be excluded, therefore, that a few irreversible changes
of the RER may occur in the center of the whorls found
in the secretory cells of the salamamnder lingual
The size and architecture of the Golgi apparatus reflect the degree of secretory activity (Han, 1967; Slot
and Geuze, 1979; Broadwell and Oliver, 1981; Hand
and Oliver, 1984; Hand and Ho, 1985; Clermont et al.,
1993; Diederen and Vullings, 1995). Generally, with
low secretion activity and atrophy, the Golgi apparatus
becomes shrunken and the total Golgi zone is undersized, whereas, when secretion is stimulated, the Golgi
saccules are dilated and elongated, expanding the
Golgi apparatus. Similar ultrastructural modifications
of the Golgi complex were observed in the present
study of lingual salivary glands. Other ultrastructural
characteristics observed in the fasted animals included
the appearance of a considerable number of inclusion
bodies. The large, dense inclusion bodies showed the
same morphology as those that appeared in the atrophied acinar cells of rat parotid glands (Wilborn and
Schneyer, 1970) and the pancreatic acinar cells of bats
(Watari, 1968) and frogs (Geuze, 1970). The inclusion
bodies seemed to originate in lysosome-like organelles
and probably were capable of digesting some degenerative and sequestered materials and organelles to socalled residual bodies, especially in atrophied cells.
However, noticeable changes typical of autophagic vacuoles were not observed in these lingual salivary
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ultrastructure, salamander, change, secretory, gland, linguam, salivary, varying, conditions, cells
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