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Mammalian follicle-stimulating hormone stimulates DNA synthesis in secondary spermatogonia and Sertoli cells in organ culture of testes fragments from the newt, Cynops pyrrhogaster

Published online by Cambridge University Press:  26 September 2008

Zai Si Ji
Affiliation:
Department of Biological Science, Faculty of Science, Kumamoto University, Kumamoto, Japan.
Shin-Ichi Abeé*
Affiliation:
Department of Biological Science, Faculty of Science, Kumamoto University, Kumamoto, Japan.
*
Shin-Ichi Abé, Department of Biological Science, Faculty of Science, Kumamoto University, Kumamoto 860, Japan. Telephone: 096 (344) 2111(ext. 3437). Fax: 096 (345) 4196.

Summary

We previously showed in organ culture of testes fragments from Cynops pyrrhogaster that mammalian folicle-stimulating hormone (FSH) stimulates secondary spermatogonia to differentiate into primary spermatocytes. In this report, we demonstrate in organ culture that FSH stimulates DNA synthesis in secondary spermatogonia and Sertoli cells: the numbers of secondary spermatogonia and Sertoli cells incorporating 5-bromo-2′ -deoxyuridine (BrdU)throughout the culture period in the presence of FSH were 3-5 times those incorporating BrdU in the absence of FSH. Moreover, addition of FSH, induced after a day a remarkable increase in the number of spermatogonia and Sertoli cells incorporating BrdU. The above results indicate that FSH stimulates and induces DNA synthesis in spermatogonia and Sertoli cells. Most of the spermatogonia within a cyst were labelled simultaneously and at the same density, indicating that they underwent synchronous DNA synthesis, whereas all the Sertoli cells within a cyst were not labelled simultaneously, indicating that they synthesised DNA asynchronously. When testes fragments pulse-labelled with Brdu were cultured in FSH for 14 days, the secondary spermatogonia differentiated into primary spermatocytes, whereas in the absence of FSH they failed to differentiate and most died by the 7th day. The above results together show that FSH is required for the proliferation of both secondary spermatogonia and Sertoli cells as well as the differentiation of secondary spermatogonia into primary spermatocytes.

Type
Commentary
Copyright
Copyright © Cambridge University Press 1994

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References

Abé, S.-I. (1981). Meiosis of primary spermatocytes and early spermiogenesis in the resultant spermatids in newt, Cynops pyrrhogaster in vitro. Differntiation 20, 6570.CrossRefGoogle ScholarPubMed
Abé, S.-I. (1987). Differentiation of spermatogenic cells from vertebrates in vitro. Int. Rev. Cytol. 109, 159209.CrossRefGoogle ScholarPubMed
Abé, S.-I. (1988). Cell culture of spermatogenic cells from amphibians. Dev. Growth Differ. 30, 209–18.CrossRefGoogle ScholarPubMed
Abé, S.-I. & Tanaka, S. (1980). Behavior of secondary spermatogonia of the newt, Cynops pyrrhogaster, in in vitro culture. Dew. Growth Differ. 22, 851–7.CrossRefGoogle ScholarPubMed
Andrieux, B., Collenot, A., Collenot, G. & Pergrale, C. (1973). Aspects morphologiques de l'action d'hormones gonadotropes mammaliennes sur l'activité testiculaire du triton Pleurodeles mature hypophysectomise. Ann. Endocrinol. (Paris) 34, 711–12.Google Scholar
Anthony, C.T., Kovacs, W.J. & Skinner, M.K. (1989). Analysis of the androgen receptor in isolated testicular cell types with a microassay that uses an affinity ligand. Endocrinology 125, 2628–35.CrossRefGoogle ScholarPubMed
Asakawa, Y., Kobayashi, T. & Iwasawa, H. (1991). Immunohistochemical detection of the proliferative activity of spermatogonia in Xenopus laevis by application of bromodeoxyuridine. Biomed. Res. 12, 269–72.CrossRefGoogle Scholar
Bortolussi, M., Zanchetta, R., Belvedere, P. & Colombo, L. (1990).Sertoli and Leydig cell numbers and gonadotropin receptors in rat testis from birth to puberty. Cell Tissue Res. 260, 185–91.CrossRefGoogle ScholarPubMed
Burgos, M.H. & Ladman, A.J. (1957). The effects of purified gonadotrophins on the morphology of the testes and thumb pads of the normal and hypophysectomized autumn frog (Rana pipiens), Endocrinology 96, 283–99.Google Scholar
Buzek, S.W. & Sanborn, B.M. (1990). Nuclear androgen receptor dynamics in testicular peritubular and Sertoli cells J. Androl. 11, 514–20.CrossRefGoogle ScholarPubMed
Callard, G.V. (1991). Spermatogenesis. In: Vertebrate Endocrinology: Fundamentals and Biomedical Implications, ed. Pang, P.K.T. & Schreibman, M.T., vol. 4, part A, pp.303–41. New York: Academic Press.Google Scholar
Callard, I.P., Callard, G.V., Lance, V., Bolaffi, J.L. & Rosset, J.S. (1978). Testicular regulation in nonmammalian vertebrates. Biol. Reprod. 18, 1643.CrossRefGoogle ScholarPubMed
Dorrington, J.H. & Armstrong, D.T. (1979). Effects of FSH on gonadal functions. Recent Prog. Horm. Res. 35, 301–42.Google ScholarPubMed
Fritz, I.B. (1978). Sites of action of androgens and follicle stimulating hormone on cells of the seminiferous tubule. In: Biochemical Actions of Hormones, ed. Litwack, G. vol. V, pp. 249–81. New York: Academic Press.CrossRefGoogle Scholar
Griswold, M.D., Morales, C. & Sylvester, S.R. (1988).Molecular biology of the Sertoli cell. In: Oxford Reviews of Reproductive Biology, ed. Clarke, J.R., vol. 10, pp. 125–61. Oxford: Oxford University Press.Google Scholar
Grootegoed, J.A., Peters, M.J., Mulder, E., Rommerts, F.F.G. & van der Molen, H.J. (1977). Absence of a nuclear androgen receptor in isolated germinal cells of rat testis. Mol. Cell Endocrinol. 9, 159–67.CrossRefGoogle ScholarPubMed
Grootegoed, J.A., Oonk, R.B., Jansen, R. & van der Molen, H.J. (1985). Spermatogenic cells utilize metabolic intermediates from Sertoli cells. In: Gamete Quality and Fertility Regulation, ed. Roland, R., Heineman, M.J., Hillier, S.G. & Vemer, H., pp. 225–37. Amsterdam: Elsevier.Google Scholar
Heckert, L.L. & Griswold, M.D. (1991). Expression of follicle-stimulating hormone receptor mRNA in rat testes and Sertoli cells. Mol. Endocrinol. 5, 670–7.CrossRefGoogle ScholarPubMed
Ji, Z.-S., Kubokawa, K., Ishii, S. & Abé, S.-I. (1992). Differentiation of secondary spermatogonia to primary spermatocytes by mammalian follicle-stimulating hormone in organ culture of testes fragments from the newt, Cynops pyrrhogaster. Dev. Growth Differ. 34, 649–60.CrossRefGoogle ScholarPubMed
Kobayashi, T. & Iwasawa, H. (1992). Timing of proliferation of spermatogonia and spermatogonium-supporting Sertoli cells in the newt Cynops pyrrhogaster. Biomed. Res. 13, 167–72.CrossRefGoogle Scholar
Kubokawa, K. & Ishii, S. (1980). Follicle-stimulating hormone (FSH)receptors in the testis of the newt, Cynops pyrrhogaster, and comparison of temperature dependency of the receptors with those of the other vertebrates. Gen. Comp. Endocrinol. 40, 425–33.CrossRefGoogle ScholarPubMed
Lance, V. & Callard, I.P. (1980). Phylogenetic trends in hormonal control of gonadal steroidogenesis. In: Evolution of Vertebrate Endocrine Systems, ed. P.K.T, Pang & Epple, A., pp. 167231. Texas: Texas Technical University Press.Google Scholar
Licht, P. (1979). Reproductive endocrinology of reptiles and amphibians: gonadotropins. Annu. Rev. Physiol. 41, 337–51.CrossRefGoogle ScholarPubMed
Licht, P., Papkoff, H., Farmer, S.W., Muller, C.H., Tsui, H.W. & Crews, D. (1977). Evolution of gonadotropin structure and function. Recent Prog. Horm. Res. 33, 169248.Google Scholar
Lofts, B. (1961). The effects of follicle-stimulating hormone and luteinizing hormone on the testis of hypophysectomized frogs (Rana temporaria). Gen. Comp. Endocrinol. 1, 179–89.CrossRefGoogle ScholarPubMed
Lofts, B. (1987). Testicular function. In: Hormones and Reproduction in Fishes, Amphibians, and Reptiles, ed. Norris, D.D. & Jones, R.E., pp. 283325. York: Plenum Press.CrossRefGoogle Scholar
Means, A.R., Fakunding, J.L., Huckins, C., Tindall, D.J. & Vitale, R. (1976). Follicle-stimulating hormone, the Sertoli cell, and spermatogenesis. Recent Prog. Horm. Res. 32, 3270.Google ScholarPubMed
Means, A.R., Dedman, J.R., Tash, J.S., Tindall, D.J., van Sickle, M. & Welsh, M.J. (1980). Regulation of the testis Sertoli cell by follicle-stimulating hormone. Annu. Rev. Physiol. 42, 5970.CrossRefGoogle ScholarPubMed
Moore, F.L. (1975). Spermatogenesis in larval Ambystoma tigrinum: positive and negative interactions of FSH and testosterone. Gen. Comp. Endocrinal. 26, 525–33.CrossRefGoogle ScholarPubMed
Nishikawa, A. & Abé, S.-I. (1983). Progression throughout all stages of meiosis from the early prophase of newt primary spermatocytes in vitro. Dev. Growth Differ. 25, 323–31.CrossRefGoogle ScholarPubMed
Parvinen, M., Vihko, K.K. & Toppari, J. (1986). Cell interactions during the seminiferous epithelial cycle. Int. Rev. Cytol. 104, 115–51.CrossRefGoogle ScholarPubMed
Russel, L.D., Alger, L.E. & Nequim, L.G. (1987). Hormonal control of pubertal spermatogenesis. Endocrinology. 120, 1615–32.CrossRefGoogle Scholar
Sanborn, B.M., Wagle, J.R., Steinberger, A. & Lamb, D.J. (1983). Sertoli cell as an androgen target In: Recent Advances in Male Reproduction: Molecular Basis and Clinical Implications, ed. D'Agata, R., Lipsett, M.B., Polosa, P. & van der Molen, H.J., pp. 6978. New York: Raven Press.Google Scholar
Sar, M., Lubahn, D.B., French, F.S. & Wilson, E.M. (1990). Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology. 127, 3180–6.CrossRefGoogle ScholarPubMed
Skinner, M.K. (1991). Cell-cell interactions in the testis Endocr. Rev. 12, 4577.CrossRefGoogle ScholarPubMed
Steinberger, E. (1971). Hormonal control of mammalian spermatogenesis. Physiol. Rev. 51, 122.CrossRefGoogle ScholarPubMed
Steinberger, A. & Steinberger, E. (1970). Invitro growth and development of mammalian testes. In: The Testis, ed. Johnson, A.D., Gomes, W.R. & van Demark, N.L., vol. 2, pp. 363–91. New York: Academic Press.CrossRefGoogle Scholar
Steinberger, E. & Steinberger, A. (1972). Testis: basic and clinical aspects. In: Reproductive Biology, ed. Balin, H. & Glasser, S., pp. 144267. Amsterdam: Excerpta Medica.Google Scholar
Tanaka, S. & Takikawa, H. (1984). Amphibian and reptilian gonadotropin: biological activity. In: Gunma Symposia on Endocrinology, ed. Takikawa, H., vol. 21, pp. 3761. Tokyo: Center for Academic Publications Japan.Google Scholar
Tanaka, S., Takikawa, H. & Wakabayashi, K. (1981). Seasonal variation in pituitary gonadotropin in the adult male newt, Cynops pyrrhogaster, revealed by isoelectric focusing technique and radioreceptor assay. Endocrinol. Japon. 28, 335–45.CrossRefGoogle ScholarPubMed
Tanaka, S., Hattori, M. & wakabayashi, K. (1987). Steroidogenic activity of isoelectric gonadotropin components in the pituitary of adult male newt, Cynops pyrrhogaster pyrrhogaster. Zool. Sci. 4, 115–22.Google Scholar