Skip to main content
SpringerLink
Log in

Spermatogenesis and its endocrine regulation

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Three major phases compose spermatogenesis: mitotic proliferation of spermatogonia, meiosis of spermatocytes, and spermiogenesis, the restructuring of spermatids into flagellated spermatozoa. The process is fuelled by stem cells that, when dividing, either self-renew or produce spermatogonia that are committed to proliferation, meiosis, and spermiogenesis. During all phases, germ cells are in close contact with and require the structural and functional support of Sertoli cells. In contrast to germ cells, these somatic cells express receptors for sex steroids and follicle-stimulating hormone (FSH), the most important hormones that regulate spermatogenesis. A typical Sertoli cell response to an endocrine stimulus would be to change the release of a growth factor that would then mediate the hormone's effect to the germ cells. Recent studies in the Japanese eel have shown, for example, that in the absence of gonadotropin Sertoli cells produce a growth factor (an orthologue of anti-Müllerian hormone) that restricts stem cell divisions to the self-renewal pathway; also estrogens stimulate stem cell renewal divisions but not spermatogonial proliferation. Gonadotropin or 11-ketotestosterone (11-KT) stimulation, however, induces spermatogonial proliferation, which is in part mimicked by another Sertoli cell-derived growth factor (activin B). Since FSH (besides luteinizing hormone, LH) stimulates steroidogenesis in fish, and since FSH is the only gonadotropin detected in the plasma of sexually immature salmonids, increased FSH signalling may be sufficient to initiate spermatogenesis by activating both Sertoli cell functions and 11-KT production. Another important androgen is testosterone (T), which seems to act via feedback mechanisms that can compromise FSH-dependent signalling or steroidogenesis. The testicular production of T and 11-KT therefore needs to be balanced adequately. Further research is required to elucidate in what way(s) 11-KT stimulates later stages of development, such as entry into meiosis and spermiogenesis. At this period, LH becomes increasingly important for the regulation of androgen production. Results from mammalian models suggest that during the later phases, the control of germ cell apoptosis via Sertoli cell factors is an important regulatory mechanism. In many species, sperm cells cannot fertilize eggs until having passed a maturation process known as capacitation, which includes the acquisition of motility. Progestins that are produced under the influence of LH appear to play an important role in this context, which involves the control of the composition of the seminal plasma (e.g., pH values).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amer, M.A., Miura, T., Miura, C. and Yamauchi, K. 2001. Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol. Reprod. 65: 1057–1066.

    Article  PubMed  CAS  Google Scholar 

  • Arey, B.J., Stevis, P.E., Deecher, D.C., Shen, E.S., Frail, D.E., Negrovilar, A. and Lopez, F.J. 1997. Induction of promiscuous G protein coupling of the follicle-stimulating hormone (FSH) receptor: A novel mechanism for transducing pleiotropic actions of FSH isoforms. Mol. Endocrinol. 11: 517–526.

    Article  PubMed  CAS  Google Scholar 

  • Bartlett, J.M.S., Kerr, J.B. and Sharpe, R.M. 1986. The effect of selective destruction and regeneration of rat Leydig cells on the intratesticular distribution of testosterone and morphology of the seminiferous epithelium. J. Androl. 7: 240–253.

    PubMed  CAS  Google Scholar 

  • Billard, R., Fostier, A., Weil, C. and Breton B. 1982. Endocrine control of spermatogenesis in teleost fish. Can. J. Fish Aquat. Sci. 39: 65–79.

    Article  CAS  Google Scholar 

  • Billard, R. 1969a. La spermatogénèse de Poecilia reticulata I. Estimation du nombre de générations goniales et rendement de la spermatogénèse. Ann. Biol. Anim. Bioch. Biophys. 9: 251–271.

    Article  Google Scholar 

  • Billard, R. 1969b. Hypophysectomie et spermatogénèse chez Poecilia reticulata (poisson Cyprinodontidae). C. R. Acad. Sci. 268: 1856–1859.

    CAS  Google Scholar 

  • Billard, R. 1968. Influence de la température sur la durée et l'efficacité de la spermatogénèse du Guppy Poecilia reticulata. C. R. Acad. Sci. 266: 2287–2290.

    Google Scholar 

  • Bogerd, J., Blomenröhr, M., Andersson, E., Putten van der, H.H.A.G.M., Tensen, C.P., Vischer, H.F., Granneman, J.C.M., Jannssen-Dommerholt, C., Goos, H.J.Th. and Schulz, R.W. 2001. Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish, Clarias gariepinus. Biol. Reprod. 64: 1633–1643.

    Article  PubMed  CAS  Google Scholar 

  • Boitani, C., Stefanini, M., Fragale, A. and Morena, A.R. 1995. Activin stimulates Sertoli cell proliferation in a defined period of rat testis development. Endocrinology 136: 5438–5444.

    Article  PubMed  CAS  Google Scholar 

  • Borg, B. 1994. Androgens in teleost fishes. Comp. Biochem. Physiol. 109C: 219–245.

    CAS  Google Scholar 

  • Bremner, W.J., Millar, M.R., Sharpe, R.M. and Saunders, P.T.K. 1994. Immunohistochemical localization of androgen receptors in the rat testis: Evidence for stage-dependent expression and regulation by androgens. Endocrinology 135: 1227–1234.

    Article  PubMed  CAS  Google Scholar 

  • Budworth, P.R., Senger, P.L., Griswold, M.D. and Donaldson, E.M. 1994 Relationship of plasma steroids to germ cell development and the presence of protamine mRNA in rainbow trout during the induction of spermatogenesis with partially purified salmon gonadotropin. J. Fish Biol. 44: 983–995.

    Article  CAS  Google Scholar 

  • Cavaco, J.E.B., Bogerd, J., Goos, H.J.T. and Schulz, R.W. 2001. Testosterone inhibits 11–ketotestosterone-induced spermatogenesis in African catfish, Clarias gariepinus. Biol. Reprod. 65: 1807–1812.

    Article  PubMed  CAS  Google Scholar 

  • Cavaco, J.E.B., Blijswijk van, B., Leatherland, J.F., Goos, H.J.T. and Schulz, R.W. 1999. Androgen-induced changes in Leydig cell ultrastructure and steroidogenesis in juvenile African catfish, Clarias gariepinus. Cell Tissue Res. 297: 291–299.

    Article  PubMed  CAS  Google Scholar 

  • Cavaco, J.E.B., Vilrokx, C., Trudeau, V.L., Schulz, R.W. and Goos, H.J.T. 1998. Sex steroids and the initiation of puberty in male African catfish, Clarias gariepinus. Amer. J. Physiol. 44: R1793–R1802.

    Google Scholar 

  • Cavaco, J.E.B., Vischer, H.F., Lambert, J.G.D., Goos, H.J.T. and Schulz, R.W. 1997. Mismatch between patterns of circulating and testicular androgens in African catfish, Clarias gariepinus. Fish Physiol. Biochem. 17: 155–162.

    Article  CAS  Google Scholar 

  • Chiarini-Garcia, H. and Russell, L.D. 2001. High-resolution light microscopic characterization of mouse spermatogonia. Biol. Reprod. 65: 1170–1178.

    Article  PubMed  CAS  Google Scholar 

  • Cooke, P.S., Zhao, Y.D. and Bunick, D. 1994. Triiodothyronine inhibits proliferation and stimulates differentiation of cultured neonatal Sertoli cells: Possible mechanism for increased adult testis weight and sperm production induced by neonatal goitrogen treatment. Biol. Reprod. 51: 1000–1005.

    Article  PubMed  CAS  Google Scholar 

  • Cunningham, G.R., Tindall, D.J., Huckins, C. and Means, A.R. 1978. Mechanisms for the testicular hypertrophy which follows hemicastration. Endocrinology 102: 16–23.

    Article  PubMed  CAS  Google Scholar 

  • Dickey, J. T. and Swanson, P. 1998. Effects of sex steroids on gonadotropin (FSH and LH) regulation in coho salmon (Oncorhynchus kisutch). J. Mol. Endocrinol. 21: 291–306.

    Article  PubMed  CAS  Google Scholar 

  • Dobson, S. and Dodd, J.M. 1977. Endocrine control of the testis in the dogfish Scyliorhinus canicula L. II. Histological and ultrastructural changes in the testis after partial hypophysectomy (ventral lobectomy). Gen. Comp. Endocrinol. 32: 53–71.

    Article  PubMed  CAS  Google Scholar 

  • Ewing, H.H. 1972. Spermatogenesis in the zebrafish, Brachydanio rerio. Anat. Rec. 173: 308.

    Google Scholar 

  • França de, L.R., Ogawa, T., Avarbock, M.R., Brinster, R.L. and Russell, L.D. 1998a. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol. Reprod. 59: 1371–1377.

    Article  Google Scholar 

  • França de, L.R., Parreira, G.G., Gates, R.J. and Russell, L.D. 1998b. Hormonal regulation of spermatogenesis in the hypophysectomized rat: Quantitation of germ-cell population and effect of elimination of residual testosterone after long-term hypophysectomy. J. Androl. 19: 335–340.

    Google Scholar 

  • Funk, J.D. and Donaldson, E.M. 1972. Induction of precocious sexual maturity in male pink salmon (Oncorhynchus gorbuscha). Can. J. Zool. 50: 1413–1419.

    Article  PubMed  CAS  Google Scholar 

  • Gomez, J.M., Weil, C., Ollitrault, M., LeBail, P.Y., Breton, B. and LeGac, F. 1999. Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 113: 413–428.

    Article  PubMed  CAS  Google Scholar 

  • Grier, H.J. and Taylor, R.G. 1998. Testicular maturation and regression in the common snook. J. Fish Biol. 53: 521–542.

    Article  Google Scholar 

  • Griswold, M.D. 1998. The central role of Sertoli cells in spermatogenesis. Sem. Cell Dev. Biol. 9: 411–416.

    Article  CAS  Google Scholar 

  • Ikeuchi, T., Todo, T., Kobayashi. T. and Nagahama, Y. 2001. Two subtypes of androgen and progestogen receptors in fish testes. Comp. Biochem. Physiol. 129B: 449–455.

    CAS  Google Scholar 

  • Johnston, D.S., Russell, L.D., Friel, P.J. and Griswold, M.D. 2001. Murine germ cells do not require functional androgen receptors to complete spermatogenesis following spermatogonial stem cell transplantation. Endocrinology 142: 2405–2408.

    Article  PubMed  CAS  Google Scholar 

  • Kawauchi, H., Suzuki, K., Itoh, H., Swanson, P., Naito, N., Nagahama, Y., Nozaki, M., Nakai, Y. and Itoh, S. 1989. The duality of teleost gonadotropins. Fish Physiol. Biochem. 7: 29–38.

    Article  CAS  Google Scholar 

  • Khan, I.A., Lopez, E. and Leloup-Hatey, J. 1987. Induction of spermatogenesis and spermiation by a single injection of human chorionic gonadotropin in intact and hypophysectomized immature European eel (Anguilla anguilla L.). Gen. Comp. Endocrinol. 68: 91–103.

    Article  PubMed  CAS  Google Scholar 

  • Khan, I.A., Lopez, E. and Leloup-Hatey, J. 1986. Effects of hypophysectomy on the testis of the European eel (Anguilla anguilla L.). Gen. Comp. Endocrinol. 62: 411–418.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J.J. and Fazleabas, A.T. 1998 Growth Factors. In: Encyclopedia of Reproduction Vol 2. pp. 573–583. Edited by E. Knobil and J.D. Neill, Academic Press, San Diego.

    Google Scholar 

  • Kobayashi, M., Sorensen, P.W. and Stacey, N.E. 2002. Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol. Biochem, 26: 71–84.

    Article  CAS  Google Scholar 

  • Kobayashi, M., Aida, K. and Stacey, N.E. 1991. Induction of testis development by implantation of 11–ketotestosterone in female goldfish. Zool. Sci. 8: 389–393.

    CAS  Google Scholar 

  • Krishnamurthy, H., Babu, P.S., Morales, C.R. and Sairam, M.R. 2001. Delay in sexual maturity of the follicle-stimulating hormone receptor knockout malemouse. Biol. Reprod. 65: 522–531.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, R.S., Ijiri, S. and Trant, J.M. 2001. Molecular biology of the channel catfish gonadotropin receptors: 2. Complementary DNA cloning, functional expression, and seasonal gene expression of the follicle-stimulating hormone receptor. Biol. Reprod. 65: 710–717.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, T.R., Wang, Y., Lu, N. and Matzuk, M.M. 1997. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics 15: 201–204.

    Article  PubMed  CAS  Google Scholar 

  • Laan, M., Richmond, H., He, C. and Campbell, R.K. 2002. Zebrafish as a model for vertebrate reproduction: Characterization of the first functional zebrafish (Danio rerio) gonadotropin receptor. Gen. Comp. Endocrinol. 125: 349–364.

    Article  PubMed  CAS  Google Scholar 

  • LeGac, F., Loir, M., LeBail, P.Y. and Ollitrault, M. 1996. Insulin-like growth factor (IGF-I) mRNA and IGF-I receptor in trout testis and in isolated spermatogenic and Sertoli cells. Mol. Reprod. Dev. 44: 23–35.

    Article  CAS  Google Scholar 

  • Lejeune, H., Chuzel, F., Thomas, T., Avallet, O., Habert, R., Durand, P. and Saez, J. 1996. Paracrine regulation of Leydig cells. Annal. d'Endocrinol. 57: 55–63.

    CAS  Google Scholar 

  • Li, H., Papadopoulos, V., Vidic, B., Dym, M. and Culty, M. 1997. Regulation of rat testis gonocyte proliferation by plateletderived growth factor and estradiol: Identification of signaling mechanisms involved. Endocrinology 138: 1289–1298.

    Article  PubMed  CAS  Google Scholar 

  • Loir, M. 2001. Adenosine receptor-adenylate cyclase system in the trout testis: Involvement in the regulation of germ cell proliferation. Mol. Reprod. Dev. 58: 307–317.

    Article  PubMed  CAS  Google Scholar 

  • Loir, M., Sourdaine, P., Mendis-Handagama, S.M.L.C. and Jégou, B. 1995. Cell-cell interactions in the testis of teleosts and elasmobranchs. Microsc. Res. Techn. 32: 533–552.

    Article  CAS  Google Scholar 

  • Loir, M. 1994. In vitro approach to the control of spermatogonia proliferation in the trout. Mol. Cell. Endocrinol. 102: 141–150.

    Article  PubMed  CAS  Google Scholar 

  • Loir, M. and LeGac, F. 1994. Insulin-like growth factor I and II binding and action on DNA synthesis in rainbow trout spermatogonia and spermatocytes. Biol. Reprod. 51: 1154–1163.

    Article  PubMed  CAS  Google Scholar 

  • Loir, M., Cauty, C., Planquette, P. and LeBail, P.Y. 1989. Comparative study of the male reproductive tract in seven families of South-American catfishes. Aquat. Living Resour. 2: 45–56.

    Article  Google Scholar 

  • Lyon, M.F., Glenister, P.H. and Lamoreux, M.L. 1975. Normal spermatozoa from androgen resistant germ cells of chimaeric mice and the role of androgen in spermatogenesis. Nature 258: 620–622.

    Article  PubMed  CAS  Google Scholar 

  • Mather, J.P., Attie, K.M., Woodruff, T.K., Rice, G.C. and Phillips, D.M. 1990. Activin stimulates spermatogonial proliferation in germ-Sertoli cell cocultures from immature rat testis. Endocrinology 127: 3206–3214.

    Article  PubMed  CAS  Google Scholar 

  • Matta, S.L.P., Vilela, D.A.R., Godinho, H.P. and França, L.R. 2002. The goitrogen 6–n-propyl-2–thiouracil (PTU) given during testis development increases Sertoli and germ cell numbers per cyst in fish: the tilapia (Oreochromis niloticus) model. Endocrinology 143: 970–978.

    Article  PubMed  CAS  Google Scholar 

  • Mayer, I., Borg, B. and Schulz, R. 1990. Conversion of 11–ketoandrostenedione to 11–ketotestosterone by blood cells of six fish species. Gen. Comp. Endocrinol. 77: 70–74.

    Article  PubMed  CAS  Google Scholar 

  • Miura, T., Miura, C., Konda, Y. and Yamauchi, K. 2002. Spermatogenesis-preventing substance in Japanese eel. Development 129: 2689–2697.

    PubMed  CAS  Google Scholar 

  • Miura, T., Miura, C., Ohta, T., Nader, M.R., Todo, T. and Yamauchi, K. 1999. Estradiol-17β stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Com. 264: 230–234.

    Article  PubMed  CAS  Google Scholar 

  • Miura, T., Kawamura, S., Miura, C. and Yamauchi, K. 1997. Impaired spermatogenesis in the Japanese eel, Anguilla japonica: Possibility for the existence of factors that regulate entry of germ cells into meiosis. Dev. Growth. Differ. 39: 685–691.

    Article  PubMed  CAS  Google Scholar 

  • Miura, T., Kasugai, T., Nagahama, Y. and Yamauchi, K. 1995a. Acquisition of potential for sperm motility in vitro in Japanese eel Anguilla japonica. Fisheries Sci. 61: 533–534.

    CAS  Google Scholar 

  • Miura, T., Miura, C., Yamauchi, K. and Nagahama, Y. 1995b. Human recombinant activin induces proliferation of spermatogonia in vitro in the Japanese eel Anguilla japonica. Fisheries Sci. 63: 434–437.

    Google Scholar 

  • Miura, T., Yamauchi, K., Takahashi, H., and Nagahama, Y. 1992. The role of hormones in the acquisition of sperm motility in salmonid fish. J. Exp. Zool. 261: 359–363.

    Article  PubMed  CAS  Google Scholar 

  • Miura, T., Yamauchi, K., Takahashi, H. and Nagahama, Y. 1991a. Involvement of steroid hormones in gonadotropin-induced testicular maturation in male Japanese eel (Anguilla japonica). Biomed. Res. 12: 241–248.

    CAS  Google Scholar 

  • Miura, T., Yamauchi, K., Nagahama, Y. and Takahashi, H. 1991b. Induction of spermatogenesis in male Japanese eel, Anguilla japonica, by a single injection of human chorionic gonadotropin. Zool. Sci. 8: 63–73.

    CAS  Google Scholar 

  • Miura, T., Yamauchi, K., Takahashi, H. and Nagahama, Y. 1991c. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc. Natl. Acad. Sci. USA 88: 5774–5778.

    Article  PubMed  CAS  Google Scholar 

  • Miwa, S., Yan, L. and Swanson, P. 1994. Localization of two gonadotropin receptors in the salmon gonad by in vitro ligand autoradiography. Biol. Reprod. 59: 629–642.

    Article  Google Scholar 

  • Morisawa, S. and Morisawa, M. 1988. Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136: 13–22.

    PubMed  CAS  Google Scholar 

  • Morisawa, S. and Morisawa, M. 1986. Acquisition of potential for sperm motility in rainbow trout and chum salmon. J. Exp. Biol. 126: 89–96.

    PubMed  CAS  Google Scholar 

  • Nader, M.R., Miura, T., Ando, N., Miura, C. and Yamauchi, K. 1999. Recombinant human insulin-like growth factor I stimulates all stages of 11–ketotestosterone-induced spermatogenesis in the Japanese eel, Anguilla japonica, in vitro. Biol. Reprod. 61: 944–947.

    Article  PubMed  CAS  Google Scholar 

  • Oba, Y., Hirai, T., Yoshiura, Y., Yoshikuni, M., Kawauchi, H. and Nagahama, Y. 1999a. Cloning, functional characterization, and expression of a gonadotropin receptor cDNA in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem. Biophys. Res. Commun. 263: 584–590.

    Article  PubMed  CAS  Google Scholar 

  • Oba, Y., Hirai, T., Yoshiura, Y., Yoshikuni, M., Kawauchi, H. and Nagahama, Y. 1999b. The duality of fish gonadotropin receptors: Cloning and functional characterization of a second gonadotropin receptor cDNA expressed in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem. Biophys. Res. Commun. 265: 366–371.

    Article  PubMed  CAS  Google Scholar 

  • O'Donnell, L., Robertson, K.M., Jones, M.E. and Simpson, E.R. 2001. Estrogen and spermatogenesis. Endocrine Rev. 22: 289–318.

    Article  Google Scholar 

  • Ohta, H., Ikeda, K. and Izawa, T. 1997. Increase in concentrations of potassium and bicarbonate ions promote acquisition of motility in vitro by Japanese eel spermatozoa. J. Exp. Zool. 277: 171–180.

    Article  CAS  Google Scholar 

  • Okuzawa, K. 2002. Puberty in teleosts. Fish Physiol. Biochem. 26: 31–41.

    Article  CAS  Google Scholar 

  • Patiño, R. and Sullivan, C.V. 2002. Ovarian follicle growth, maturation, and ovulation in teleost fishes. Fish Physiol. Biochem. 26: 57–70.

    Article  Google Scholar 

  • Payne, A.H. and Youngblood, G.L. 1995. Regulation of expression of steroidogenic enzymes in Leydig cells. Biol. Reprod. 52: 217–225.

    Article  PubMed  CAS  Google Scholar 

  • Planas, J. V. and Swanson, P. 1995. Maturation-associated changes in the response of the salmon testis to the steroidogenic actions of gonadotropins (GTH I and GTH II) in vitro. Biol. Reprod. 52: 697–704.

    Article  PubMed  CAS  Google Scholar 

  • Plant, T.M. and Marshall, G.R. 2001. The functional significance of FSH in spermatogenesis and the control of its secretion in male primates. Endocr. Rev. 22: 764–786.

    Article  PubMed  CAS  Google Scholar 

  • Prat, F., Sumpter, J. P. and Tyler, C. R. 1996. Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 54: 1375–1382.

    Article  PubMed  CAS  Google Scholar 

  • Quérat, B., Tonnerre-Doncarli, C., Genies, F. and Salmon, C. 2001. Duality of gonadotropins in gnathostomes. Gen. Comp. Endocrinol. 124: 308–314.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, K.M., O'Donnell, L., Jones, M.E.E., Meachem, S.J., Boon, W.C., Fisher, C.R., Graves, K.H., McLachlan, R.I. and Simpson, E.R. 1999. Impairment of spermatogenesis in mice lacking a functional aromatase (Cyp 19) gene. Proc. Natl. Acad. Sci. U.S.A. 96: 7986–7991.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, O.H. 1958. Accelerated development of testis after unilateral gonadectomy, with observations on normal testis of rainbow trout. Fish. Bull. 58: 9–30.

    Google Scholar 

  • Rooij de, D. G. and Russell, L.D. 2000. All you wanted to know about spermatogonia but were afraid to ask. J. Andrology. 21: 776–798.

    Google Scholar 

  • Russel, L.D., Ettlin, R.A., Sinha Hikim, A.P. and Clegg E.D. 1990. Histological and histopathological evaluation of the testis. Cache River Press (Clearwater, Florida, U.S.A.), pp. 1–37.

    Google Scholar 

  • Schulz, R.W., Bogerd, J. and Goos, H.J.Th. 1999. Spermatogenesis and its endocrine regulation. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 225–232. Edited by Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O., Fish Symp 99, Bergen.

  • Schulz, R. and Blüm, V. 1990. Steroid secretion of rainbow trout testis in vitro: variation during the reproductive cycle. Gen. Comp. Endocrinol. 80: 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Schulz, R. 1984. Serum levels of 11–oxotestosterone in male and 17β-estradiol in female rainbow trout (Salmo gairdneri) during the first reproductive cycle. Gen. Comp. Endocrinol. 56: 111–120.

    Article  PubMed  CAS  Google Scholar 

  • Shan, L.X., Bardin, C.W. and Hardy, M.P. 1997. Immunohistochemical analysis of androgen effects on androgen receptor expression in developing Leydig and Sertoli cells. Endocrinology 138: 1259–1266.

    Article  PubMed  CAS  Google Scholar 

  • Shibata, N. and Hamaguchi, S. 1988. Evidence for the sexual bipotentiality of spermatogonia in the fish, Oryzias latipes. J. Exptl. Zool. 245: 71–77.

    Article  CAS  Google Scholar 

  • Siller, S. 2001. Sexual selection and the maintenance of sex. Nature 411: 689–692.

    Article  PubMed  CAS  Google Scholar 

  • Sinha-Hikim, A.P.S., Rajavashisth, T.B., Hikim, I.S., Lue, Y.H., Bonavera, J.J., Leung, A., Wang, C. and Swerdloff, R.S. 1997. Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol. Reprod. 57: 1193–1201.

    Article  PubMed  CAS  Google Scholar 

  • Socorro, S., Power, D.M., Olsson, P.-E. and Canario, A.V.M. 2000. Two estrogen receptors expressed in the teleost fish, Sparus aurata: cDNA cloning, characterization and tissue distribution. J. Endocrinol. 166: 293–306.

    Article  PubMed  CAS  Google Scholar 

  • Sperry, T.S. and Thomas, P. 1999. Characterization of two nuclear androgen receptors in Atlantic croaker: Comparison of their biochemical properties and binding specificities. Endocrinology 140: 1602–1611.

    Article  PubMed  CAS  Google Scholar 

  • Sprando, R.L., Heidinger, R.C. and Russell, L.D. 1988. Spermiogenesis in the bluegill (Lepomis macrochirus): a study of cytoplasmic events including cell volume changes and cytoplasmic elimination. J. Morphol. 198: 165–177.

    Article  PubMed  CAS  Google Scholar 

  • Sprando, R.L. and Russell, L.D. 1987. Germ cell-somatic cell relationships: a comparative study of intercellular junctions during spermatogenesis in selected non-mammalian vertebrates. Scanning Microsc. 1: 1249–1255.

    PubMed  CAS  Google Scholar 

  • Swanson, P., Bernard, M., Nozaki, M., Suzuki, K., Kawauchi, H. and Dickhoff, W.W. 1989. Gonadotropins I and II in juvenile coho salmon. Fish Physiol. Biochem. 7: 169–176.

    Article  CAS  Google Scholar 

  • Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. 2002. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech. Dev. 113: 29–39.

    Article  PubMed  CAS  Google Scholar 

  • Takeo, J. and Yamashita, S. 2000. Rainbow trout androgen receptor-α fails to distinguish between any of the natural androgens tested in transactivation assay, not just 11–ketotestosterone and testosterone. Gen. Comp. Endocrinol. 117: 200–206.

    Article  PubMed  CAS  Google Scholar 

  • Takeo, J. and Yamashita, S. 1999. Two distinct isoforms of cDNA encoding rainbow trout androgen receptors. J. Biol. Chem. 274: 5674–5680.

    Article  PubMed  CAS  Google Scholar 

  • Themmen, A.P.N., Kraaij, R. and Grootegoed, J.A. 1994. Regulation of gonadotropin receptor gene expression. Mol. Cell. Endocrinol. 100: 15–19.

    Article  PubMed  CAS  Google Scholar 

  • Uchida, D., Yamashita, M., Kitano, T. and Iguchi, T. 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exptl. Biol. 205: 711–718.

    Google Scholar 

  • Vischer, H.F., Teves, A.C.C., Ackermans, J.C.M., van Dijk, W., Schulz, R.W. and Bogerd, J. 2003. Cloning and spatiotemporal expression of the follicle-stimulating hormone β subunit complementary DNA in the African Catfish (Clarias gariepinus). Biol. Reprod. 68 (in press).

  • Viveiros, A.T., Eding, E.H. and Komen, J. 2001. Effects of 17α-methyltestosterone on seminal vesicle development and semen release response in the African catfish, Clarias gariepinus. Reproduction 122: 817–827.

    Article  PubMed  CAS  Google Scholar 

  • Wu, C., Patiño, R., Davis, K.B. and Chang, X. 2001. Localization of estrogen receptor α and β RNA in germinal and nongerminal epithelia of channel catfish testis. Gen. Comp. Endocrinol. 124: 12–20.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe, A. and Onitake, K. 1995. Changes in the distribution of fibroblast growth factor in the teleostean testis during spermatogenesis. J. Exptl. Zool. 272: 475–483.

    Article  CAS  Google Scholar 

  • Yamazaki, F. and Donaldoson, E.M. 1969. Involvement of gonadotropin and steroid hormones in the spermiation of the gold-fish (Carassius auratus). Gen. Comp. Endocrinol. 12: 491–497.

    Article  PubMed  CAS  Google Scholar 

  • Yan, L.G., Swanson, P. and Dickhoff, W.W. 1992. A two-receptor model for salmon gonadotropins (GTH-I and GTH-II). Biol. Reprod. 47: 418–427.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, G.Q., Deng, K., Labosky, P.A., Liaw, L. and Hogan, B.L.M. 1996. The gene encoding bone morphogenetic protein 8B (BMP8B) is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev. 10: 1657–1669.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Biology, Research Group Endocrinology, University of Utrecht, Padualaan 8, room Z203, NL-3584 CH, Utrecht, The Netherlands (Phone

    Rüdiger W. Schulz

  2. Faculty of Agriculture, Laboratory of Fish Reproductive Physiology, Ehime University, 3-5-7 Tarumi, Matsuyama, 790-8566, Japan (Phone

    Takeshi Miura

Authors
  1. Rüdiger W. Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takeshi Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schulz, R.W., Miura, T. Spermatogenesis and its endocrine regulation. Fish Physiology and Biochemistry 26, 43–56 (2002). https://doi.org/10.1023/A:1023303427191

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023303427191

Keywords

Search

Navigation