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Histology and histochemistry of human eccrine sweat glands with special reference to their defense mechanisms.

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Histology a n d Histochemistry of Human Eccrine
Sweat Glands, with Special Reference to
their Defense Mechanisms
MARJORIE M. C. LEE
Department of Anatomy, University of H o n g K o n g , H o n g Kong
In their histochemical investigations of
the human eccrine sweat gland, Montagna
et al. (’53) demonstrated coarse Schiff-reactive saliva-resistant granuels in the distal
end of the “ d a r k cells of the secretory coil,
and reported that the granules showed a
metachromatic tinge with toluidin blue at
pH 5.0. However, the authors did not clearly distinguish these metachromatic granules from those composed of dense basophilic cytoplasmic RNA, also found in
these cells. Lobitz et al. (’54a, ’54b and
’55) have described a thin lining of Schiffpositive, non-glycogen fibrillar material
along the lumen of the sweat duct, which
sometimes stains metachromatically with
toluidin blue. Mucopolysaccharides apart,
the saliva-resistant Schiff-positive substances present in eccrine sweat glands
might also contain muco- or glycoprotein
or glycolipid groups. Wislocki (’47) considers that not all metachromasia is referable to mucopolysaccharides. One aim
of the experiments here reported was to
use Steedman’s (’50) Alcian blue 8GS to
investigate the acid mucopolysaccharides
in the human eccrine sweat gland. Steedman’s method is specific, easily applied and
gives clear and permanent results.
Certain morphological aspects of the eccrine sweat gland and duct are mentioned
in this paper. Although most of these have
been described previously, few attempts
have been made to explain their functional
significance. The purpose of this paper is
to correlate the histological structure of the
eccrine sweat glands and ducts with their
acid mucopolysaccharide content and to
suggest that their functions include a possible defense mechanism in the human
skin.
MATERIALS AND METHODS
Human skin specimens were obtained
from 33 Chinese bodies at autopsy, and
were selected from the following regions:
scalp, axilla, abdomen, palm and sole. The
specimens were removed and fixed less
than 24 hours after death, and most of the
bodies reached the refrigerator within the
first few hours. Skin from both male and
female cadavers was included. Ages
ranged from 6 to 68 with an average of
38.3 years. The skin samples chosen were
considered “healthy” by inspection. Six
additional specimens of abdominal skin,
surgically removed from living patients,
were also included in the series.
Skin specimens were fixed in Helly’s
fluid and chilled 85% alcohol. Paraffin
sections were cut at 6 LI and stained by
hematoxylin and eosin, Masson’s trichrome
and Heidenhain’s iron hematoxylin. The
mucopolysaccharide content of the eccrine
sweat glands and ducts were investigated
by McManus’ (PAS) technique. Any glycogen present was removed by incubating
the slides in saliva at 37°C for one hour
prior to staining, and the remaining salivaresistant PAS-positive material was tested
for acid mucopolysaccharides as follows :
1. Staining with 1% Alcian blue 8GS
for 20 seconds.
2. Metachromasia: revealed by staining
with 0.05% toluidin blue for 15 minutes.
The stain was adjusted to the following pH
values: 3.5, 4.5, 5.0, 6.0 and 7.0 by McIlvaine buffer. A few sections were treated
in 0.01% ribonuclease at 60°C for three
hours to remove RNA before being stained
with toluidin blue, the potency of the
ribonuclease being controlled by incubating sections in distilled water at the same
97
98
MARJORIE M . C. LEE
temperature and for an equal length of
time. Sections for metachromasia were all
examined in water.
Sample sections were also incubated for
18 hours at 37°C in a dilute solution of
testicular hyaluronidase (45 I.U. per milligram of normal saline) and then stained
with PAS, Alcian blue and toluidin blue.
The hyaline cuticle lining the lumen of
the sweat duct was tested for the presence
of the sulfhydryl (-SH ) group, by Chhremont and Frkderic’s (’43) ferricyanide
method, control sections being pre-treated
with saturated aqueous mercuric chloride
at 60°C for three days to prevent any
(-SH) group present from giving a positive result. Pearse’s (’51) performic acidSchiff (PFAS) method was used to indicate the disulfide group (-S-s-).
Since
lipids with unsaturated bonds also give a
positive PFAS reaction, staining with Sudan black B was used to detect their presence.
OBSERVATIONS AND RESULTS
The eccrine sweat glands
By using hematoxylin and eosin, Masson’s trichrome or Heidenhain’s iron hematoxylin, the epithelial cells of the eccrine secretory coil can be differentiated,
not very obviously, into two kinds, termed
“clear” and “ d a r k by Montagna (’53).
The “clear” cells are usually larger and
have round or oval vesicular nuclei, the
cytoplasm being pale with occasional intra-cytoplasmic vacuoles. They are usually attached to the basement membrane
by a broader base, and often have narrower
and rounded distal ends, which may fail
to reach the lumen as they are frequently
overlapped by the neighboring “ d a r k cells.
The latter are usually fewer, but the proportion of the two types varies from tubule
to tubule. The “dark” cells are more basophilic with coarse light-bluish granules in
the apical cytoplasm. Where a “ d a r k cell
is interposed between “clear” cells, its basal
part is compressed into a narrow stalk; its
distal portion usually extends beyond the
“clear” cells and expands to overlap them
on the lumen border (fig. 3 ) . The dark,
rod-like nucleus of this type of cell may
be situated in the cytoplasmic stalk; when
i t lies in the expanded portion of the cy-
toplasm, it is more vesicular and occupies
a higher level than the nuclei of the neighboring “clear” cells, giving the lining epithelium a stratified appearance. When two
or three “ d a r k cells happen to lie adjacent to each other, they are seen as
simple columnar cells equally wide at
apex and base (figs. 1 , 2).
In saliva-digested PAS sections, the distal cytoplasm of the “dark” cells contains
coarse positive granules (figs. 3, 4), which
vary greatly in number, and may be absent
in some situations. In the latter case the
“ d a r k cells are recognizable only by their
location and morphology.
On some occasions another type of PASpositive saliva-resistant granule is found
in both “clear” and “ d a r k cells. When
present, they are large, few in number and
randomly distributed. It is believed that
they contain glyco- or other lipid groups,
since they can be stained with Sudan black
B, and are also PFAS positive. The PFAS
reaction is indicative of two substances:
unsaturated lipids and keratin or keratinoid substances containing (-s-s-) groups
(Pearse, ’53).
The apical granules in the “ d a r k cells
are also Alcian blue positive (figs. 1, 2).
Steedman (’50) first showed that Alcian
blue SGS, when carefully applied, is a
specific stain for mucin, which is stained
a clear blue-green color. After incubating
control sections with hyaluronidase, the
staining intensity of the granules in the
“dark’ cells, by either PAS or Alcian blue,
does not diminish, hence hyaluronic acid
can be excluded as a component.
When stained with toluidin blue, the
Alcian blue positive granules in the apices
of the “ d a r k cells are invariably metachromatic throughout the pH range used
(pH 3.5 to 7.0). At low pH values they
are violet pink; at high values they become
dark bluish-purple. Aside from the metachromatic granules in the distal cytoplasm,
the remainder of the cytoplasm of the
“dark” cells is moderately basophilic, but
that of the “clear” cells is comparatively
pale. Ribonuclease removes the cytoplasmic basophilia at pH 5. According to Montagna (’51) this is due to loss of cytoplasmic RNA. In the present experiments the
metachromatic granules in the “ d a r k cells
became more distinct after treatment with
H U M A N ECCRINE GLANDS
ribonuclease, possibly due to the removal
of orthochromatic cytoplasmic RNA with
consequent unmasking of metachromatic
acid mucopolysacch arides.
Helly-fixed sections are more suitable
for demonstrating acid mucopolysaccharides in the sweat glands than are those
fixed in 10% formalin or in Bouin’s fluid.
When fixed in 85% alcohol no acid mucopolysaccharides were found in the
“ d a r k cells. No appreciable differences in
the mucin content of the “dark” cells of
the eccrine glands were found to be related to the regions studied, to the sex or
age of the individual or to the seasons of
the year, and mucin granules were demonstrated equally well in necroptic and surgical specimens.
The eccrine sweat d u cts
The sweat duct consists of dermal and
epidermal portions. The dermal portion
contains a coiled part, continuous with the
secretory coil, and a straight or undulating
part, running from the coil to the epidermis. Both portions are lined by two layers
of cuboidal cells. The transition from
glandular to ductal epithelium is abrupt.
The boundary of the epithelial cells lining
the duct is indistinct, but the size and degree of crowding of the nuclei indicate that
the superficial cells are larger than those
of the basal layer. The nuclei of the
former are large and vesicular, those of the
latter smaller and more deeply stained.
Frequently three distinct layers of cells
line the sweat duct, especially in the undulating portion near its junction with
the epidermis. On the luminal border of
the superficial cells there is a homogeneous
acidophilic hyaline cuticle and in contrast
to the epithelial cells, these possess a clear
cell boundary.
The duct pierces the epidermis at the
apex of a rete peg, and then forms a number of tight spirals winding upwards to
open on the surface. The caliber of the
lumen is usually narrow in the lower portion, but enlarges as it nears the surface.
For convenience of description, the epidermal portion of the duct may be divided
into three parts:
1. Upper part-In the stratum corneum
and stratum lucidum, the sweat duct lacks
99
a cellular lining of its own but forms a
channel in the keratinized substance, with
the flaky “keratin ring” of OBrien encircling it (Lobitz et al., ’54a).
2. Middle part-In the stratum granulosum and the upper half of the Malpighian layer, the sweat duct appears to have
been formed by an epidermal invagination.
The lumen is surrounded by flaky keratinized material which can be traced upwards
to where it becomes continuous with the
stratum corneum. On the outside are one
or two layers of flattened, concentrically
arranged cells containing darkly staining
keratohyalin granules; these are directly
continuous with the stratum granulosum
of the epidermis.
3. Lower part-In the lower half of the
Malpighian layer, the sweat duct begins
to have its own lining. It is lined by a
single layer of cuboidal cells, with clear
cytoplasm, vesicular nuclei and a distinct
surface hyaline cuticle, resembling the
superficial cells of the dermal sweat duct.
Few keratohyalin granules can be seen in
the cytoplasm and are apparently continuous with those in the middle part. Outside this layer, the Malpighian cells of the
epidermis are flattened and concentrically
arranged around the duct. Tracing the
epidermal duct into the dermis, the cuticlelined luminal cells are continuous with the
corresponding superficial cells of the dermal duct; the flattened Malpighian cells
outside this layer merge into the middle
Iayer and the cells of the stratum basale
of the epidermis continue with the basal
layer of the dermal duct. The melanin
granules in the stratum basale disappear
abruptly at the junction, and are absent in
the wall of the dermal sweat duct (figs.
7 , 9, 10, 11).
Two features distinguish the cuticular
lining of the lower portion from the keratin lining of the middle and upper portions
of the epidermal sweat duct: (1) The
hyaline cuticle is a homogeneous compact
substance transformed from the luminal
border of the lining cells; the keratin lining, formed from dead epidermal cells, is
irregular and flaky and arranged in segregated rings. ( 2 ) The two regions possess
different staining reactions. In Masson’s
trichrome the keratin lining is stained a
vivid red, and the hyaline cuticle a pale
100
MARJORIE M . C . LEE
green (fig. 10). With Heidenhain’s iron
hematoxylin the keratin stains a dark bluish-black and the cuticle is greyish.
A saliva-resistant PAS-reactive substance is commonly present in the lumen
throughout the length of the sweat duct.
This substance is also stained by Alcian
blue 8GS and shows metachromasia with
toluidin blue. It is probable that acid mucopolysaccharides in the duct, thus shown
to be present, are secreted by the “dark”
cells of the sweat gland. The amount of
this mucus-like material varies; it usually
forms only a thin layer on the surface of
the lumen, but may accumulate into a mass
in the more dilated portion of the duct
(fig. 8). In the upper more dilated and
tightly spiraled part of the epidermal duct,
the mucus tends to occur in larger quantity, frequently forming plugs which obliterate the duct lumen (figs. 6, 7). It
may reach the skin surface. Lobitz et al.
(’54a, ’54b and ’55) have also described
this Schiff-positive, saliva-resistant material lining the duct and refer to it as
the “hyaline ring” occurring in the upper
part of the epidermal sweat duct within
the keratin ring. They also reported its
metachromatic nature when stained with
toluidin blue buffered to pH 5. The term
“hyaline ring” as they use it, suggests
that it is a definite part of the duct wall
rather than contained material. That it
is composed of lumen contents is supported by the following observations : ( 1)
It does not usually occur in a uniform
layer, but is slightly granular, often thinner or even absent on one side; (2) It may
form a mass filling the center of the lumen
often partially adherent to the wall.
Chhremont and FrCderic’s ferricyanide
method for (-SH) groups can be used with
paraffin sections of alcohol fixed tissues.
With controls, the hyaline cuticle of the
duct gives moderately to strongly positive
reactions (fig. 5). The stratum lucidum
and the keratohyalin granules of the stratum granulosum are also moderately positive. Pearse’s PFAS method can be used
with paraffin sections of Helly-fixed tissues. The cuticle of the duct is usually
non-reactive, occasionally there is a pinkish tinge. The skin tissues normally giving a positive PFAS reactions are: hair,
most strongly reactive; inner root sheath
of the hair follicle, reacting less strongly;
and stratum lucidum of the epidermis,
usually weakly reactive.
DISCUSSION
Two types of cells occur in the human
eccrine sweat gland, termed “clear” and
“ d a r k by Montagna (’53) who differentiated them by their staining reactions, especially to toluidin blue. The histochemical tests here reported indicate that the
distal cytoplasm of the “dark” cells contains mucin granules and that mucus-like
material is found in the ducts. The probable prima-ry function of the “ d a r k cells is
therefore, the secretion of mucin. No direct evidence of the function of the “clear”
cells has been found but they probably
produce sweat. Indirect evidence supports
this hypothesis : ( 1) “clear” cells are more
numerous in the secretory coil. ( 2 ) Shelley et al. (’52) confirmed that glycogen
in the cytoplasm of the secretory coil of
the resting sweat gland is reduced or disappears after intense sweating. The present experiments confirm Montagna’s (’53)
statement that although both “ d a r k and
“clear” cells contain glycogen, there is
more of it in the “clear” cells. Therefore
the more heavily glycogen-laden “clear”
cells are probably the main sweat-secreting
cells. It is suggested that more appropriate
terms would indicate the functions of the
two types of secretory cells in human eccrine glands; and that the “clear” cells be
known as “chief cells” and that the “dark”
cells be called “mucin cells.”
Mucus is secreted onto the surface of
the mucous membrane in many places in
the body, probably with lubricating and
protective functions. The protective role is
two-fold: ( 1 ) Physical, by forming an
adsorptive medium or surface coating, ( 2 )
Chemical, since mucin may alter the harmful nature of an agent. In this connection
Babkin (’50), has stated that gastric mucus contains mucoitin-sulphuric acid, a
hydrolyzed product of mucin which possesses an antipeptic function and so prevents autodigestion of the gastric mucosa.
Skin is liable to be in contact with various harmful agents against which the keratinized stratum corneum forms the main
defensive barrier. Infection of the skin
usually starts in the hair follicles and
101
HUMAN ECCRINE GLANDS
less frequently in the sweat glands. If the
sweat glands possessed no special mechanisms for defense, the occurrence of more
frequent and serious skin ailments would
be expected. Skin mucus is present in
some lower animals, therefore the “mucin
cells” of the sweat glands are not a recent
evolutionary development. Mucus, normally acting as a lubricant, would be undesirable on the skin surface, especially on
the palm and sole. Nevertheless, sections
show that mucus secreted by the sweat
glands does pass through the ducts to
reach the surface, and Jirka and Kotas
(’57) have demonstrated the presence of
mucoproteins in human sweat, which elaborates hexosamines after hydrolysis. Although sweat gland mucus reaches the
skin surface, no “mucoid sensation is
felt on human skin, which may imply that
sweat gland mucin has different physical
properties from visceral mucin. In the
experiments here reported it was found
that sweat gland mucin differs from intestinal goblet cell mucin in that the
former cannot be preserved by alcohol fixation, an observation which indicates
special chemical properties in the sweat
gland mucin. Bunting (’48) was unable
to demonstrate any metachromatic element in the human eccrine sweat gland,
possibly due to his having used basic lead
acetate as a fixative, which may not be a
suitable substance for preserving sweat
gland mucin.
The histochemical demonstration of protein-bound (-SH) and (-S-s-)
groups is
believed to indicate the presence of prekeratin and keratin substances. Montagna
(’54) who used Barrnett and Seligman’s method to demonstrate (-SH) and
(-S-S-)
groups in skin, found that the
cuticle of the sweat duct reacts moderately
to the (-SH) group and intensely to the
(-S-S-)
group. The present experiments
show that the sweat duct cuticle reacts
moderately to strongly with the ferricyanide method for (-SH) groups, but with
Pearse’s PFAS method for the (-S-S-)
group negative or only faintly positive reactions were obtained. The keratin of the
stratum corneum is also PFAS negative,
and only the inner root sheath and the hair
itself react strongly. Scott and Flesch (’54)
measured the (-SH) and (-S-S-)
con-
tent of human skin, and found the percentage of sulfur (-SH plus -S-S-) to be
5.7 for hair and 0.343 for keratin in the
plantar skin. This suggests that the PFAS
reaction is not as sensitive as Barrnett and
Seligman’s method for (-S-S-), and that
groups may be present
although (-S-S-)
in the sweat duct cuticle they are quantitatively insignificant. The sweat duct cuticle is homogeneous and refractile, and
the contained prekeratin and keratin indicate that it acts as a protective barrier.
Sweat ducts in the stratum corneum are
dilated and plugs of mucus in some of
the spirals are common. The spirals may
constitute a water-trap-like device, in
which fluid may be caught at the bends;
the mucous plugs thus formed near the
exit would effectively prevent access to the
system. In addition, the keratinoid cuticle
lining the duct acts as a physical barrier.
In the secretory coil of the eccrine gland,
the apical expansions of the “mucin” cells
tend to overlap the adjacent “chief” cells,
preventing them from reaching the surface. Thus three lines of defense protect
the system from invasion through the epidermal sweat ducts.
SUMMARY
1. The small “ d a r k cells in the secretory coils of the human eccrine sweat
glands contain m u c h granules in their
apical cytoplasm. The name “mucin cells”
is proposed for them, and “chief cells” for
the large “clear” cells which are also found
in the epithelial lining of the coils.
2. The lumen of the sweat duct contains
mucus, which tends to form plugs in the
spirals within the stratum corneum of the
epidermal sweat duct.
3. It is suggested that the sweat gland
mucin may have both physical and chemical functions in defense against contamination through the sweat pores. It is suggested also that the tight spirals of the
epidermal sweat ducts function as mechanical “traps” in which mucus-plugs
temporarily block the ducts.
4. The upper two thirds of the epidermal sweat duct is lined by a keratin ring
derived from the stratum corneum of the
epidermis; the lower third of the epidermal
and remainder of the dermal duct are lined
by a type of cell possessing a hyaline
102
MARJORIE M. C . LEE
cuticle. The cuticle contains prekeratin,
and probably also keratin, thus providing
a further defense barrier.
ACKNOWLEDGMENTS
I am indebted to Mr. R. B. Maneely for
his advice in techniques and in the preparation of this paper. Thanks are also extended to Professor K. S. F. Chang, Head
of the Department, for having read and
criticized the manuscript. Finally I should
like to record my sincere appreciation to
Dr. E. V. Cowdry for his helpful suggestions during a visit to this Department.
LITERATURE CITED
Babkin, B. P. 1950 Secretory Mechanism of
the Digestive Glands. 2nd ed. P. B. Hoeber,
Inc. New York, p. 256.
Bunting, H., G . B. Wislocki and E. W. Dempsey
1948 The chemical histology of human accrine and apocrine sweat glands. Anat, Rec.,
ZOO: 61-78.
Chkvremont, M., and J. Frdderic 1943 Arch
Biol., 54: 589. (quoted from Pearse 1953, pp.
419420).
Jirka, M., and J. Kotas 1957 The occurrence
of mucoproteins in human sweat. Clin. Chim.
Acta, 2: 292-296.
Lobitz, W. C. Jr., J. B. Holyoke and W. Montagna
1954a The epidermal eccrine sweat duct unit.
J. Invest. Dermat., 22: 157-158.
195413 Responses
of
the human ecIbid.,
rrine
sweat duct to controlled iniurv.
.__..
.
.
23: 329-344.
Lobitz. W. C. Jr., J. H. Holyoke and D. Brophy
1955 Histochemical evidence for human eccrine sweat duct activity. A.M.A. Arch. Derm.,
72: 229-236.
Montagna, W., H. B. Chase and H. P. Melaragno
1 9 5 1 Histology and cytochemistry of human
skin. I. Metachromasia i n the mons pubis. J.
Nat. Cancer. Inst., 12: 591-597.
Montagna, W., H. B. Chase and W. C. Lobitz
1953 Histology and cytochemistry of human
skin. IV. The eccrine sweat glands. J. Invest.
Derm., 20: 4 1 5 4 2 3 .
Montagna, W., A. Z. Eisen, A. H. Radeniacher
and H. B. Chase 1954 Histology and cytochemistry of human skin. VI. The distribution
of sulfhydryl and disulfide groups. Ibid., 23:
23-32.
Pearse, A. G. E. 1951 J. Clin. Path., 4: 1
(quoted from Pearse, 1953, pp. 4 2 1 4 2 2 ) .
1953 Theoretical and Applied Histochemistry. J. and A. Churchill Ltd., London,
pp. 78 and 184.
Scott, E. J., and P. Flesch 1954 Sulfhydryl
and disulfide in keratinization. Science, 119:
70-71.
Shelley, W. B., and H. Mescon 1952 Histochemical demonstration of secretory activity
i n human eccrine sweat glands. J. Invest.
Derm., 18: 289-301.
Steedman, H. F. 1950 Alcian Blue 8GS: A new
stain for mucin. Quart. J. Micr. Sci., 92:
477479.
Wislocki, G. B., H. Bunting and E. W. Dempsey
1947 Metacromasia in mammalian tissues
and its relationship to mucopolysaccharides.
Am. J. Anat., 82: 1-35.
PLATE 1
EXPLANATION O F FIGURES
1
Secretory coil of eccrine sweat gland stained with Alcian blue, nuclei counter-stained
with Mayer’s hemalum. From palmar skin of 57-year-old male. X 500.
2
Section treated as in figure 1. From scalp of 30-year-old man. X 900.
3
Secretory coil of eccrine sweat gland, PAS technique after saliva digestion, counterstained with Mayer’s hemalum. From skin of sole of 68-year-old female. X 500.
4
Section treated as in figure 3. From axillary skin of 45-year-old female. X 1200.
5
Paraffin section of coiled portion of dermal sweat duct, from alcohol fixed tissue treated
with Chhvremont and Frdderic’s ferricyanide method for (-SH) groups. From palmar
skin of 61-year-old female. X 400.
HUMAN ECCRINE GLANDS
Marjorie M. C. Lee
PLATE 1
103
PLATE 2
EXPLANATION OF FIGURES
6
Spirals of sweat duct in the thick stratum corneum of palmar skin, PAS technique after
saliva digestion, Mayer’s hemalum used as counter-stain. From a 48-year-old man.
x 200.
7
Spirals of sweat duct in the thin epidermis of the abdominal skin, section treated as i n
figure 6. From 19-year-old male. x 200.
8
Two sections of undulating portion of dermal ducts, showing that the PAS-positive,
saliva-resistant substance forms only a thin layer lining one duct but fills the lumen
of another. From scalp of 30-year-old male. X 400.
9
Junction of dermal and epidermal portion of sweat duct, Masson’s trichrome stain.
From scalp of 50-year-old man. X 300.
10 Epidermal portion of eccrine sweat duct, Masson’s trichrome stain. From scalp of
50-year-old male. X 400.
11
104
Diagrammatic drawing summarizing features shown in figures 7, 9 and 10, showing:
A, Keratin lined epidermal sweat duct in stratum corneum and upper half of Malpighian
layer. B, Large clear cells with surface cuticle lining the portion of the epidermal sweat
duct i n the lower half of the Malphighian layer as well as the dermal sweat duct. C,
Keratohyalin granules continuing down from the stratum granulosum into the large
luminal cells lining the lower portion of the epidermal sweat duct. D, Continuation of
the various epidermal cells into the different layers of the dermal sweat duct. E, Melanin
granules disappear abruptly from basal cells a t the junction of the dermal sweat duct
to the epidermis.
HUMAN ECCRINE GLANDS
Marjorie M. C. Lee
PLATE 2
105
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