Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-28T00:45:17.025Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression of Fas–Fas ligand system associated with atresia in murine ovary

Published online by Cambridge University Press:  26 September 2008

Ji Ping Xu ,
Xiang Li ,
Etsuko Mori ,
Eimei Sato ,
Shigeru Saito ,
Mao Wu Guo  and
Tsuneatsu Mori
Ji Ping Xu
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Xiang Li
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Etsuko Mori
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Eimei Sato
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Shigeru Saito
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Mao Wu Guo
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
Tsuneatsu Mori*
Affiliation:
Institute of Medical Science, University of Tokyo, and Nara Medical University, Japan.
*
T. Mori, Department of Immunology, Institute of Medical Science, University of Tokyo, 4-6-1 shirokanedai, Minato-ku, Tokyo 108, Japan. Telephone: +81-3-5449-5261. Fax: +81-3-5449-5402, e-mail: ts-mori@hgc.ims.u-tokyo.ac.jp.
Get access Rights & Permissions [Opens in a new window]

Summary

We detected that Fas receptor (Fas) was expressed at transcriptional levels in oocytes/eggs and some granulosa cells of murine ovary, whereas, Fas ligand (FasL) was found to be strongly expressed in granulosa cells by means of in situ hybridisation. These results were supported by an indirect immunofluorescence (IIF) test with anti-Fas monoclonal antibody (mAb)/FasL Ab. The lysates from granulosa cells were precipitated by anti-FasL Ab, exhibiting a specific band at 40 kDa. When zona pellucida (ZP)-free eggs were incubated with granulosa cells in vitro, apoptosis (DNA fragmentation) was induced in the eggs, as detected by the terminal deoxynucleotide transferase mediated dUTP-nick end labelling (TUNEL) method. To examine whether FasL-bearing cells can induce apoptosis in eggs expressing Fas through molecular interaction between FasL and Fas, we employed a baculovirus expression system to generate FasL on the surface of Spodoptera frugiperda (Sf9) cells. The co-incubation of eggs with Autographa californica nuclear polyhedrosis virus (AcNPV) and FasL transfected Sf9 (Sf9–FasL) cells in vitro was performed and resulted in the induction of apoptosis in eggs as detected by the TUNEL method. Apoptosis was absent in eggs co-incubated with AcNPV-1393 transfected Sf9 (Sf9−1393) cells. Thus, ovarian atresia was suggested to be induced by molecular interaction between FasL on granulosa cells and Fas on oocytes/eggs during oogenesis.

Keywords

Fas–Fas ligandOocyte/eggGranulosa cellSF9-FasL cellAtresia
Type
Article
Information
Zygote , Volume 5 , Issue 4 , November 1997 , pp. 321 - 327
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Dhein, J., Daniel, P.T., Trauth, B.C., Oehm, A.,Moller, P., & Krammer, P.H.. (1992). Induction of apoptosis by monoclonal antibody anti-APO-1 class switch variants is dependent on cross-linking of APO-1 cell surface antigens. J. Immunol. 149, 3166–73.CrossRefGoogle ScholarPubMed
Enari, M., Talanian, R.V., Wong, W.W., & Nagata, S.. (1996). Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380, 723–26.Google Scholar
Flaws, J.A., Kugu, K., Trbovich, A.M., Desanti, A., Tilly, K.I., Hirshfield, A.N., & Tilly, J.L.. (1995). Interleukin-1β-converting enzyme-related proteases (IRPs) and mammalian cell death: dissociation of IRP-induced oligonucleosomal endonuclease activity from morphological apoptosis in granulosa cells of the ovarian follicle. Endocrinology 136, 5042–53.CrossRefGoogle Scholar
French, L.E., Hahne, M., Viard, I., Radlgruber, G., Zanone, R., Becker, K., Muller, C., & Tschopp, J.. (1996). Fas and Fas ligand in embryos and adult mice: ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J. Cell Biol. 133, 335–43.Google Scholar
Greenwald, G.S.. (1989). Temporal and topographic changes in DNA synthesis after induced follicular atresia. Biol. Reprod. 40, 175–81.Google Scholar
Guo, M.W., Mori, E., Xu, J.P., & Mori, T.. (1994). Identification of Fas antigen associated with apoptotic cell death in murine ovary. Biochem. Biophys. Res. Commun. 203, 1438–46.CrossRefGoogle ScholarPubMed
Guo, M.W., Watanabe, T., Mori, E., & Mori, T.. (1995). Molecular structure and function of CD4 on murine egg plasma membrane. Zygote 3, 65–73.Google Scholar
Guo, M.W., Xu, J.P.. Mori, E., Sato, E., Saito, S., & Mori, T.. (1997 a). Expression of Fas ligand in murine ovary. Am. J. Reprod. Immunol. 37, 391–8.CrossRefGoogle ScholarPubMed
Guo, M.W., Xu, J.P., Mori, E., Sato, E., Saito, S., & Mori, T.. (1997 b). Expression of Fas–Fas ligand system in murine ovary and its role for atresia through apoptosis. J. Reprod. Dev. 43 (Suppl), 93–4.Google Scholar
Hirshfield, A.N.. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.CrossRefGoogle ScholarPubMed
Hogan, B., Costantini, F., & Lacy, E.. (1994). Manipulating the Mouse Embryo: A Laboratory Manual, 2nd edn, pp. 325–84. New York: Cold Spring Harbor Laboratory.Google Scholar
Hughes, F.M.J, & Gorospe, W.C.. (1991). Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129, 2415–22.CrossRefGoogle ScholarPubMed
Itoh, N., & Nagata, S.. (1993). A novel protein domain required for apoptosis. Mutational analysis of human Fas antigen. J. Biol. Chem. 268, 10932–7.CrossRefGoogle ScholarPubMed
Itoh, N., Yonehara, S., Ishii, A., Yonehara, M., Mizushima, S., Sameshima, M., Hase, A., Seto, Y., & Nagata, S.. (1991). The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66, 233–43.CrossRefGoogle ScholarPubMed
Itoh, N., Tsujimoto, Y., & Nagata, S.. (1993). Effect of bcl-2 on Fas antigen-mediated cell death. J. Immunol. 151, 621–7.Google Scholar
Kondo, H., Maruo, T., Peng, X., & Mochizuki, M.. (1996). Immunological evidence for the expression of the Fas antigen in the infant and adult human ovary during follicular regression and atresia. J. Clin. Endocrinol. Metab. 81, 2702–10.Google Scholar
Los, M., Craen, M.V., Penning, L.C., Schenk, H., Westendorp, M., Baeuerle, P.A., Droge, W., Krammer, P.H., Fiers, W., & Schulze-Osthoff, K.. (1995). Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 375, 81–3.CrossRefGoogle ScholarPubMed
Mariani, S.M., Matiba, B., Baumler, C., & Krammer, P.H.. (1995). Regulation of cell surface APO-1/Fas (CD95) ligand expression by metalloproteases. Eur. J. Immunol. 25, 2303–7.CrossRefGoogle ScholarPubMed
Mariani, S.M., Matiba, B., Sparna, T., & Krammer, P.H.. (1996). Expression of biologically active mouse and human CD95/APO-1/Fas ligand in the baculovirus system. J. Immunol. Methods 193, 63–70.CrossRefGoogle ScholarPubMed
Maruo, T.. (1995). Expression of oncogenes, growth factors and their receptors in follicular growth, regression and atresia: their roles in granulosa cell proliferation and differentiation. Acta Obstet. Gynaecol. Jpn. 47, 738–50.Google ScholarPubMed
Maxson, W.S., Haney, A.F., & Schomberg, D.W.. (1985). Steroidogenesis in porcine atretic follicles: loss of aromatase activity in isolated granulosa and theca. Biol. Reprod. 33, 495–501.CrossRefGoogle ScholarPubMed
Mori, T., Xu, J.P., Mori, E., Sato, E., Saito, S., & Guo, M.W.. (1997). Expression of Fas–Fas ligand system associated with atresia through apoptosis in murine ovary. Horm. Res. 48 (Suppl. 3), 11–19.CrossRefGoogle ScholarPubMed
Nagata, S., & Golstein, P.. (1995). The Fas death factor. Science 267, 1449–56.CrossRefGoogle ScholarPubMed
Ogasawara, J., Watanabe-Fukunaga, R., Adachi, M., Matsuzawa, A., Kasugai, T., Kitamura, Y., Ioth, N., Suda, T., & Nagata, S.. (1993). Lethal effect of the anti-Fas antibody in mice. Nature 364, 806–9.CrossRefGoogle ScholarPubMed
Owen-Schaub, L.B., Yonehara, S., IIICrump, W.L., & Grimm, E.A.. (1992). DNA fragmentation and cell death is selectively triggered in activated human lymphocytes by Fas antigen engagement. Cell Immunol. 140, 197–205.CrossRefGoogle ScholarPubMed
Quirk, S.M., Cowan, R.G., Joshi, S.G., & Henrikson, K.P.. (1995). Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol. Reprod. 52, 279–87.Google Scholar
Raff, M.C.. (1992). Social controls on cell survival and cell death. Nature 356, 397–400.CrossRefGoogle ScholarPubMed
Sakamaki, K., Yoshida, H., Nishimura, Y., Nishikawa, S., Manaba, N., & Yonehara, S.. (1997). Involvement of Fas antigen in ovarian follicular atresia and luteolysis. Mol. Reprod. Dev. 47, 11–18.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Schulze-Osthoff, K., Walczak, H., Droge, W., & Krammer, P.H.. (1994). Cell nucleus and DNA fragmentation are not required for apoptosis. J. Cell Biol. 127, 15–20.CrossRefGoogle Scholar
Smith, C.A., Farrah, T., & Goodwin, R.G.. (1994). The TNF-receptor superfamily of cellular and viral proteins: activation, costimulation, and death. Cell 76, 959–62.CrossRefGoogle ScholarPubMed
Spanel-Borowski, K.. (1981). Morphological investigations on follicular atresia in canine ovaries. Cell Tissue Res. 214, 155–68.Google Scholar
Suda, T., & Nagata, S.. (1994). Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med. 179, 873–9.Google Scholar
Suda, T., Takahashi, T., Golstein, P., & Nagata, S.. (1993). Molecular cloning and expression of the Fas ligand, a novel member of the tumour necrosis factor family. Cell 75, 1169–78.Google Scholar
Summer, M.D., & Smith, G.E.. (1987). A Manual of Methods for Baculovirus Vector and Insect Cell Culture Procedures. Texas Agriculture Experiment Station bulletin no. 1555.Google Scholar
Takahashi, T., Tanaka, M., Brannan, C.I., Jenkins, N.A., Copeland, N.G., Suda, T., & Nagata, S.. (1994). Generalised lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76, 969–76.Google Scholar
Takayama, S., Sato, T., Krajewski, S., Kochel, K., Irie, S., Millan, J.A., & Reed, J.C.. (1995). Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80, 279–84.Google Scholar
Tanaka, M., Suda, T., Takahashi, T., & Nagata, S.. (1995). Expression of the functional soluble form of human Fas ligand in activated lymphocytes. EMBO J. 14, 1129–35.CrossRefGoogle ScholarPubMed
Tartaglia, L.A., Ayres, T.M., Wong, G.H., & Goeddel, D.V.. (1993). A novel domain within the 55 kd TNF receptor signals cell death. Cell 74, 845–53.Google Scholar
Tilly, J.L., Kowaiski, K.I., Johnson, A.L., & Hsueh, A.J.. (1991). Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129, 2799–801.CrossRefGoogle ScholarPubMed
Tilly, J.L., Tilly, K.I., Kenton, M.L., & Johnson, A.L.. (1995). Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-x long messenger ribonucleic acid levels. Endocrinology 136, 232–41.CrossRefGoogle ScholarPubMed
Trauth, B.C., Klas, C., Peters, A.M., Matzku, S., Moller, P., Falk, W., Debatin, K.M., & Krammer, P.H.. (1989). Monoclonal antibody-mediated tumour regression by induction of apoptosis. Science 245, 301–5.CrossRefGoogle ScholarPubMed
Walker, N.I., Harmon, B.V., Gobe, G.C., & Kerr, J.F.R.. (1988). Patterns of cell death. Methods Achiev. Exp. Pathol. 13,18–54.Google ScholarPubMed
Watanabe-Fukunaga, R., Brannan, C.I., Itoh, N., Yonehara, S., Copeland, N.G., Jenkins, N.A., & Nagata, S.. (1992). The cDNA structure, expression, and chromosomal assignment of the mouse Fas antigen. J. Immunol. 148, 1274–79.Google Scholar
Whitten, W.K., & Biggers, J.D.. (1968). Complete development in vitro of the pre-implantation stages of the mouse in a simple chemically defined medium. J. Reprod. Fertil. 17, 399–401.CrossRefGoogle Scholar
Wong, G.H.W., & Goeddel, D.V.. (1994). Fas antigen and p55 TNF receptor signal apoptosis through distinct pathways. I. Immunol. 152, 1751–55.CrossRefGoogle ScholarPubMed
Zeleznik, A.J., Ihrig, L.L., & Bassett, S.G.. (1989). Developmental expression of Ca++/Mg++-dependent endonuclease activity in rat granulosa and luteal cells. Endocrinology. 125, 2218–20.Google Scholar