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S-100 protein-immunoreactive cells in the bovine ovary.

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T H E ANATOMICAL RECORD 223:384-386 (1989)
S-100 Protein-lmmunoreactive Cells in
the Bovine Ovary
Department of Veterinary Anatomy, Nippon Veterinary and Zootechnical College,
Tokyo 180, Japan
The present study deals with an immunohistochemical localization
of 5-100 protein in the bovine ovary. Immunoreactivity for 5-100 was observed in
various types of cells, as well as in cells of the nervous system. The endothelial cells
of arterial vessels, blood capillaries, and lymph vessels; the epithelial cells of ovarian
cysts; and the oocytes of normal and atretic follicles showed a n S-100 protein positivity. The immunoreactivity also was found in the epithelial cells of the rete ovarii.
No cells other than these showed immunoreactivity to the anti-S-100 serum. S-100
protein can be a useful marker for providing information on ovarian function.
In 1965, Moore described for the first time the presence of s-100 protein in the nervous system of various
animals. This protein is localized mainly in glial elements in the central and peripheral nervous systems
(Nakajima et al., 1984) and has been regarded until
recently as a nervous system-specific protein. However,
it now has been demonstrated that S-100 protein is present also in various cells of non-nervous tissues, such as
myoepithelial cells, melanocytes, adipocytes, macrophages, Langerhans cells, follicular dendritic cells,
chondrocytes, and tumor cells derived from these cells
(Suzuki et al., 1982; Nakajima et al., 1984; Donato, 1986;
Vanstapel et aI., 1986; Sugimura et al., 1987). However,
the biological role of S-100 protein in these cells has not
been elucidated. Recently, it has been demonstrated that
in fat cells S-100 protein might serve as one of the
carrier proteins of free fatty acids (Haimoto et al., 1985;
Iwanaga et al., 1987). 5-100 protein has been reported to
induce hormone secretion in cultured prolactin cells
(Ishikawa et al., 1983). In addition, it was shown to
interact with 5-100 protein with the microtubule system
(Donato, 1986).
There have been many reports on S-100 protein in
various non-nervous tissues but only a few descriptions
of its occurrence in the ovary (Michetti et al., 1985;
Haimoto et al., 1987). To our knowledge, however, there
is no report describing the localization of S-100 protein
in the bovine ovary. The present study deals with a
peculiar localization of S-100-immunoreactive cells in
the bovine ovary.
Ovaries of 50 Holstein cows were obtained a t a slaughterhouse. The tissue blocks were fixed in 10%buffered
neutral formalin, dehydrated in ethanol, and embedded
in paraffin according to conventional procedures. Paraffin sections 3-6-pm thick were cut serially. Dewaxed
paraffin sections were submitted to the peroxidase-antiperoxidase (PAP) method (Polak and Noorden, 1986).
The antiserum used in this study was a polyclonal rabbit anti-S-100 protein antibody obtained commercially
(Dakopatts, Denmark and Advance, Japan). The sec01989 ALAN R. LISS, INC
tions were treated with 0.3% H202 in methanol for 30
min to block endogenous peroxidase activity and then
soaked in non-immune swine serum (diluted 1:20, Dakopatts) to inhibit non-specific binding of immunoglobulins. The sections were incubated with anti-S-100 protein
serum (1:1,000) for 1 hr or more. After rinsing, treatment followed with anti-rabbit IgG swine serum (190,
Dakopatts) and PAP solution (1:50, Dakopatts) for 30
mins. Finally, the sections were treated with diaminobenzidine and then counterstained with hematoxylin or
Fig. 1. Sequential sections of bovine ovary. a: Endothelial cells of the
artery (A) are immunoreactive for S-100 protein, while those of the
vein (V) are negative. Arrowheads indicate immunoreactive nerve
bundles. h: A control section exhibits low-level, nonspecific staining.
Fig. 2. Endothelial cells of both artery (A) and lymph vessel (L) react
to the S-100antiserum. ~ 7 5 .
Fig, 3. Endothelial cells of arteriol (A) and lymph vessel (L) are
immunoreactive for S-100 protein. ~ 1 5 0 .
Fig. 4. Oocytes in the primordial follicles are stained with S-100
protein antiserum. ~ 7 5 Insert:
Oocyte in the growing follicle reacts
to the S-100antiserum. x 150.
Fig. 5. Oocyte i n the growing secondary follicle is positive for S-100,
while other elements in t h e follicle a r e negative. ~ 7 5 .
Fig. 6. Endothelial cells of capillaries and oocyte in t h e atretic follicle
are immunoreactive for S-100 protein. ~ 7 5 .
Fig. 7. Luteal cells of the corpus luteum (CL) are stained negatively
with S-100 protein antiserum, but the endothelium of arteries (A) is
stained positively. ~ 7 5 .
Fig. 8. Epithelium of the ovarian cysts reacts to the S-100antiserum.
Fig. 9. Epithelial cells of the rete ovarii a r e stained positively with
S-100protein antiserum. ~ 7 5 .
Received April 1, 1988; accepted July 20, 1988.
Address reprint requests to Shinji Kamiya, Department of Veterinary Anatomy, Nippon Veterinary and Zootechnical College, 1-7-1
Kyonan-cho, Musashino, Tokyo 180, Japan.
methyl green. All reactions were done at room temperature.
Normal rabbit serum and antisera extensively absorbed with bovine S-100 protein were used instead of
the primary antibody as a control (Polak and Noorden,
1986; Sugimura et al., 1987).
The sections adjacent to immunostained sections were
stained with hematoxylin-eosin for histological observations.
protein would detect positive immunoreactivity in the
follicular and theca cells of the bovine ovary.
The present study demonstrated for the first time the
immunoreactivity of the epithelial cells of the rete ovarii
and of ovarian cysts to the anti-S-100 serum. Although
it is difficult to correlate these cells with other S-100containing cells in functional and embryological aspects,
it can be pointed out that cultured prolactin cells share
some biological properties with epithelial cells of the
rete ovarii. S-100 protein has been reported to induce
hormone secretion in cultured prolactin cells (Ishikawa
In the bovine ovary, immunoreactivity for S-100 pro- et al., 1983). Odend’hal et al. (1986) reported that the
tein was observed in the endothelial cells of arterial rete ovarii might respond to hormones and possibly even
vessels distributed throughout the ovary (Figs. 1-3). No produce hormones. Thus, the immunostaining with Sother cellular elements in the artery were immunola- 100 protein may be a useful method for identifying the
beled, except for those of the nervous system adjacent to function of the rete ovarii.
An ovarian cyst may be formed from the follicle, corand supplying the wall of the vessels (Fig. la). Control
sections showed negative staining for S-100protein (Fig. pus luteum, rete ovarii, or the cortical invaginations of
lb). The immunoreactivity for S-100 also was found in the surface epithelium (Odend’hal et al., 1986; Clement,
the endothelial cells of blood capillaries (Fig. 6) and 1987). It is suspected that if the epithelium of ovarian
lymph vessels (Figs. 2,3). In contrast, the endothelial cysts, immunopositive for S-100 protein in this study,
cells of venous vessels did not react to the S-100 anti- arises from the rete ovarii, immunostaining with S-100
serum (Fig. la).
protein could provide a useful method for distinguishing
Oocytes of normal and atretic follicles showed a posi- the rete cysts from the other cysts. At any rate, further
tive reaction to the anti-S-100 serum (Figs. 4-6). No study will be needed to clarify the correlation between
other elements in the follicle such as follicular epithelial 5-100 protein and intraovarian structures.
cells, were immunoreactive, except for the endothelial
cells of the blood capillaries (Fig. 6). The luteal cells of
The authors wish to express their thanks to Prof. M.
the corpus luteum did not react to the S-100protein (Fig.
7), but the epithelial cells of the ovarian cyst were posi- Sugimura, Department of Veterinary Anatomy, Faculty
tive for S-100 (Fig. 8). In addition, it was noticed that of Veterinary Medicine, Hokkaido University, for his
the epithelial cells of the rete ovarii were immunoreac- valuable suggestions, including criticism of the manuscript, during this study.
tive for S-100 protein (Fig. 9).
To now, there have been many reports indicating that
S-100 protein is present in various types of cells in the
intra- and extraneuronal tissues (Nakajima et al., 1984;
Donato, 1986; Vanstapel et al., 1986; Haimoto et al.,
1987; Sugimura et al., 19871, although the physiological
role of S-100 protein is still obscure. Recently, Iwanaga
et al. (1987) reported that immunoreactivity for S-100
protein was seen in the endothelial cells of arteries and
blood capillaries, but not in those of veins. In the present
study, similar results were obtained. Moreover, it has
been postulated that S-100 protein in the endothelial
cells may be involved in the mechanism of transcytosis
of fatty acid andior other substances (Haimoto et al.,
1985). However, there is no inclusive explanation for
this variety of cells sharing S-100 protein.
In the present study, immunoreactivity for S-100 protein was observed in the oocytes, in the epithelial cells
of rete ovarii, and in ovarian cysts. On the other hand,
contradictory results have been reported; for example,
no immunoreactivity was observed in any cell type of
the rat ovary (Michetti et al., 1985). Haimoto et al.
(1987),however, recently examined the localization of S100 protein in various human tissues by use of monoclonal antibodies. They stated that in the ovary, oocytes
and follicular cells of the primary folIicIe and the theca
cells of the corpus luteum were immunoreactive. The
reasons for these discrepancies are unclear. Vanstapel
et al. (1987)reported that monoclonal antibodies specific
for S-100 protein gave results different from those obtained using polyclonal antisera of the same specificity.
It is reasonable to assume that the use of antisera that
can recognize different portions in the sequence of S-100
Clement, P.B. 1987 Histology of the ovary. Am. J. Surg. Pathol., 11:277303.
Donato, R. 1986 S-100 proteins. Cell Calcium, 7,123-145.
Haimoto, H., S. Hosoda, and K. Kato 1987 Differential distribution of
immunoreactive S100-a and S100-0 proteins i n normal nonnervous
human tissues. Lab. Invest., 57:488-498.
Haimoto, H., K. Kato, F. Suzuki, and H. Nagura 1985 The ultrastructural changes of 5-100 protein localization during lipolysis in adipocytes: An immunoelectron-microscopic study. Am. J. Pathol.,
Ishikawa, H., H. Nogami, and N. Shirasawa 1983 Novel clonal strains
from adult r a t anterior pituitary producing S-100 protein. Nature,
Iwanaga, T., T. Fujita, Y. Takahashi, and T. Isobe 1987 Immunohistochemical demonstration of S-100 protein in the endothelial cells of
blood vessels in the pig and cattle. Biomed. Res., 8r329-334.
Michetti, F., L. Lauriola, M. Rende, V.M. Stolfi, F. Battaglia, and D.
Cocchia 1985 S-100 protein in the testis: An immunochemical and
immunohistochemical study. Cell Tissue Res., 240:137-142.
Moore, B.W. 1965 A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun., 19:739-744.
Nakajima, T., T. Kameya, S. Watanabe, T. Hirota, Y. Shimosato, and
T. lsobe 1984 S-100 protein distribution in normal and neoplastic
tissues. In: Advances in Immunohistochernistry. R.A. DeLellis, ed.
Masson, New York, pp. 141-158.
Odend’hal, S., J.G.W. Wenzel, and E.C. Player 1986 The rete ovarii of
cattle and deer communicates with the uterine tube. Anat. Rec.,
Polak, J.M., and S.V. Noorden 1986 Immunocytochemistry: Modern
Methods and Applications, 2nd ed. Wright, Bristol.
Sugimura, M., H. Ishimaru, Y. Atoji, and Y. Suzuki 1987 S-100protein
N subunit immunoreactivity of follicular dendritic cells in germinal
centers of canine and caprine lymph nodes. J p n . J. Vet. Sci.,
49: 1183-1185.
Suzuki, F., T. Nakajima, and K. Kato 1982 Peripheral distribution of
nervous system-specific 5.100 protein in rat. J. Biochem., 92335838.
Vanstapel, M.-J., K.C. Gatter, C.D. Wolf-Peetcm, D.Y. Mason, and V.D.
Desmet 1986 New site of human S-100 immunoreactivity detected
with monoclonal antibodies. Am. J. Clin. Pathol., 85,160-168.
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bovine, ovary, protein, 100, immunoreactivity, cells
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