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Effects of insulin-like growth factor-I on final oocyte maturation and steroid production in Fundulus heteroclitus

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Abstract

Recent evidence has indicated the presence of IGF-I and IGF-I receptors in mammalian and teleost ovarian follicles. Since growth hormone (GH), which can be secreted from the pituitary concomitant with a gonadotropin as a response to gonadotropin-releasing hormone, generally acts to release IGF-I from tissues including the ovary, the effect of IGF-I itself on ovarian steroidogenesis and oocyte maturation was investigated in the model teleost, Fundulus heteroclitus. IGF-I was found to be without effect on ovarian follicle steroidogenesis, but initiated oocyte maturation in a dose-dependent manner even more rapidly and effectively than 17α,20β-dihydroxy-4-pregnene-3-one (DHP), the naturally occurring maturation-inducing steroid. IGF-II also induced oocyte maturation in a dose-dependent manner. IGF-I induction of oocyte maturation occurred in the absence of DHP production by the granulosa cells (which is normally stimulated by gonadotropin), and could be inhibited by cycloheximide but not actinomycin D, thus implicating the role of protein synthesis. These results suggest that GH-stimulated release of ovarian IGF-I may have an even more direct role than DHP on the reinitiation of oocyte maturation.

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References

  • Adashi, E.Y. 1994. Growth factors and ovarian function: The IGF-I paradigm. Horm. Res. 42: 44–48.

    PubMed  Google Scholar 

  • Anderson, T.A., Bennett, L.R., Conlon, M.A. and Owens, P.C. 1993. Immunoreactive and receptor active insulin-like growth factor-I and IGF-binding protein in blood plasma from the freshwater fish Macquaria ambigua (golden perch). J. Endocrinol. 136: 191–198.

    PubMed  Google Scholar 

  • Apa, R., Lanzone, A., Miceli, F., Mastrandrea, M., Caruso, A., Mancuso, S. and Canipari, R. 1994. Growth hormone induces in vitro maturation of follicle-cumulus-enclosed rat oocytes. Mol. Cell. Endocrinol. 106: 207–212.

    Article  PubMed  Google Scholar 

  • Cao, Q.P., Duguay, S.J., Plietskaya, E., Steiner, D.F. and Chan, S.J. 1989. Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA. Mol. Endocrinol. 3: 2005–2010.

    PubMed  Google Scholar 

  • Davoren, J.B. and Hsueh, A.J.W. 1986. Growth hormone increases ovarian levels of immunoreactive somatomedin C/insulin-like growth factor I in vivo. Endocrinology 118: 888–890.

    PubMed  Google Scholar 

  • Drakenberg, K., Sara, V.R., Lindahl, K. and Kewish, B. 1989. Study of insulin-like growth factors in tilapia, Oreochromis mossambicus. Gen. Comp. Endocrinol. 74: 173–180.

    PubMed  Google Scholar 

  • Duan, C. and Hirano, T. 1990. Stimulation of [35S]sulfate uptake by mammalian insulin-like growth factors I and II in cultured cartilages of the Japanese eel, Anguilla japonica. J. Exp. Zool. 256: 347–350.

    Google Scholar 

  • Duan, C. and Hirano, T. 1992. Effects of insulin-like growth factor I and insulin on the in vitro uptake of sulfate by eel branchial cartilage: Evidence for the presence of independent hepatic and pancreatic sulfation factors. J. Endocrinol. 133: 211–219.

    PubMed  Google Scholar 

  • Duan, C., Duguay, S.J. and Plisetskaya, E.M. 1993. Insulin-like growth factor I mRNA expression in coho salmon, Oncorhynchus kisutch: tissue distribution and effects of growth hormone/prolactin family proteins. Fish Physiol. Biochem. 11: 371–379.

    Google Scholar 

  • Duguay, S.J., Park, L.K., Samadpour, M. and Dickhoff, W.W. 1992. Nucleotide sequence and tissue distribution of three insulin-like growth factor I prohormones in salmon. Mol. Endocrinol. 6: 1202–1210.

    Article  PubMed  Google Scholar 

  • Fukazawa, Y., Siharath, K., Iguchi, T. and Bern, H.A. 1995. In vitro secretion of insulin-like growth factor-binding proteins from liver of striped bass, Morone saxatilis. Gen. Comp. Endocrinol. 99: 239–247.

    Article  PubMed  Google Scholar 

  • Giudice, L.C. 1992. Insulin-like growth factors and ovarian follicular development. Endocr. Rev. 13: 641–669.

    Article  PubMed  Google Scholar 

  • Gray, E.S. and Kelley, K.M. 1991. Growth regulation in the gobiid teleost, Gillichthys mirabilis: Roles of growth hormone, hepatic growth hormone receptors and insulin-like growth factor-I. J. Endocrinol. 131: 57–66.

    PubMed  Google Scholar 

  • Greeley, M.S., Jr., Calder, D.R., Taylor, M.H., Hols, H. and Wallace, R.A. 1986. Oocyte maturation in the mummichog (Fundulus heteroclitus): Effects of steroids on germinal vesicle breakdown of intact follicles in vitro. Gen. Comp. Endocrinol. 62: 281–289.

    Article  PubMed  Google Scholar 

  • Grigorescu, F., Baccara, M-T., Rouard, M. and Renard, E. 1994. Insulin and IGF-I signaling in oocyte maturation. Horm. Res. 42: 55–61.

    PubMed  Google Scholar 

  • Gutierrez, J., Parrizas, M., Carneiro, N., Maestro, J.L., Maestro, M.A. and Planas, J. 1993. Insulin and IGF-I receptors and tyrosine kinase activity in carp ovaries: Changes with reproductive cycle. Fish Physiol. Biochem. 11: 247–254.

    Google Scholar 

  • Hainaut, P., Kowalski, A., Giorgetti, S., Baon, V. and Van Obberghen, E. 1991. Insulin and insulin-like growth factor-I receptors in Xenopus laevis oocytes. Biochem. J. 273: 673–678.

    PubMed  Google Scholar 

  • Hsu, C.-J. and Hammond, J.M. 1987a. Gonadotropins and estradiol stimulate immunoreactive insulin-like growth factor-I production by porcine granulosa cells in vitro. Endocrinology 120: 198–207.

    PubMed  Google Scholar 

  • Hsu, C.-J. and Hammond, J.M. 1987b. Concomitant effects of growth hormone on secretion of insulin-like growth factor-I and progesterone by cultured porcine granulosa cells. Endocrinology 121: 1343–1348.

    PubMed  Google Scholar 

  • Humbel, R.E. 1990. Insulin-like growth factors I and II. Eur. J. Biochem. 190: 445–462.

    PubMed  Google Scholar 

  • Kagawa, H., Kobayashi, M., Hasegawa, Y. and Aida, K. 1994. Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen. Comp. Endocrinol. 95: 293–300.

    Article  PubMed  Google Scholar 

  • Kagawa, H., Moriyama, S. and Kawauchi, H. 1995. Immunocytochemical localization of IGF-I in the ovary of the red seabream, Pagrus major. Gen. Comp. Endocrinol. 99: 307–315.

    Article  PubMed  Google Scholar 

  • Katsu, Y., Yamashita, M., Kajiura, H. and Nagahama, Y. 1993. Behavior of the components of maturation-promoting factor, cdc2 kinase and cyclin B, during oocyte maturation of goldfish. Dev. Biol. 160: 99–107.

    Article  PubMed  Google Scholar 

  • Lin, X.W., Lin, H.R. and Peter, R. 1993. Growth hormone secretion in the common carp (Cyprinus carpio L.): In vitro interactions of gonadotropin-releasing hormone, somatostatin, and the dopamine agonist apomorphine. Gen. Comp. Endocrinol. 89: 62–71.

    Article  PubMed  Google Scholar 

  • Lin, Y.-W.P., LaMarca, M.J. and Wallace, R.A. 1987. Fundulus heteroclitus gonadotropin(s) I. Homologous bioassay using oocyte maturation and steroid production by isolated ovarian follicles. Gen. Comp. Endocrinol. 67: 126–141.

    PubMed  Google Scholar 

  • Lindahl, K.I., Sara, V.R., Fridberg, G. and Nishimiya, T. 1985. The presence of somatomedin in the Baltic salmon, Salmo salar, with special reference to smoltification. Aquaculture 45: 177–183.

    Article  Google Scholar 

  • Maestro, M.A., Planas, J.V., Moriyama, S., Gutierrez, J., Planas, J. and Swanson, P. 1997. Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. Gen. Comp. Endocrinol. 106: 189–201.

    Article  PubMed  Google Scholar 

  • Marchant, T.A., Chang, J.P., Nahorniak, C.S. and Peter, R.E. 1989. Evidence that gonadotropin-releasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 124: 2509–2518.

    PubMed  Google Scholar 

  • McCormick, S.D., Kelley, K.M., Young, G., Nishioka, R.S. and Bern, H.A. 1992. Stimulation of coho salmon growth by insulin-like growth factor I. Gen. Comp. Endocrinol. 86: 398–406.

    PubMed  Google Scholar 

  • Moriyama, S., Dickhoff, W.W. and Plisetskaya, E.M. 1995. Isolation and characterization of insulin-like growth factor-I from rainbow trout, Oncorhynchys mykiss. Gen. Comp. Endocrinol. 99: 221–229.

    Article  PubMed  Google Scholar 

  • Murthy, C.K., Turner, R.J., Wong, A.O.L., Rao, P.D., Rivier, J.E. and Peter, R.E. 1994. Differential actions of a mammalian gonadotropin-releasing hormone antagonist on gonadotropin-II and growth hormone release in goldfish, Carassius auratus. Neuroendocrinology 59: 561–571.

    PubMed  Google Scholar 

  • Negatu, Z. and Meier, A.H. 1995. In vitro incorporation of [14C]Glycine into muscle protein of Gulf killifish (Fundulus grandis) in response to insulin-like growth factor-I. Gen. Comp. Endocrinol. 98: 193–201.

    Article  PubMed  Google Scholar 

  • Niu, P.-D. and LeBail, P.-Y. 1993. Presence of insulin-like growth factor binding protein in rainbow trout (Oncorhynchus mykiss) serum. J. Exp. Zool. 265: 627–636.

    Google Scholar 

  • Petrino, T.R., Lin, Y.-W.P. and Wallace, R.A. 1989. Steroidogenesis in Fundulus heteroclitus I. Production of 17α-hydroxy,20β-dihydroprogestero ne, testosterone, and 17β-estradiol by prematurational follicles in vitro. Gen. Comp. Endocrinol. 73: 147–156.

    PubMed  Google Scholar 

  • Petrino, T.R., Lin, Y.-W.P., Netherton, J.C., Powell, D.H. and Wallace, R.A. 1993. Steroidogenesis in Fundulus heteroclitus V. Purification, characterization, and metabolism of 17α,20β-dihydroxy-4-pregnen-3-one by intact follicles and its role in oocyte maturation. Gen. Comp. Endocrinol. 92: 1–15.

    Article  PubMed  Google Scholar 

  • Samaras, S.E., Canning, S.F., Barber, J.A., Simmen, F.A. and Hammond, J.M. 1996. Regulation of insulin-like growth factor I biosynthesis in porcine granulosa cells. Endocrinology 137: 4657–4664.

    Article  PubMed  Google Scholar 

  • Selman, K. and Wallace, R.A. 1986. Gametogenesis in Fundulus heteroclitus. Am. Zool. 26: 173–192.

    Google Scholar 

  • Shamblott M.J. and Chen, T.T. 1992. Identification of a second insulin-like growth factor in a fish species. Proc. Nat. Acad. Sci., USA 89: 8913–8917.

    PubMed  Google Scholar 

  • Singh, H., Griffith, R.W., Takahashi, A., Kawauchi, H., Thomas, P. and Stegeman, J.J. 1988. Regulation of gonadal steroidogenesis in Fundulus heteroclitus by recombinant salmon growth hormone and purified salmon prolactin. Gen. Comp. Endocrinol. 72: 144–153.

    PubMed  Google Scholar 

  • Srivastava, R.K. and Van Der Kraak, G. 1994a. Regulation of DNA synthesis in goldfish vitellogenic ovarian follicles by hormones and growth factors. J. Exp. Zool. 270: 263–272.

    Google Scholar 

  • Srivastava, R.K. and Van Der Kraak, G. 1994b. Insulin as an amplifier of gonadotropin action on steroid production: Mechanisms and sites of action in goldfish prematurational full-grown ovarian follicles. Gen. Comp. Endocrinol. 95: 60–70.

    Article  PubMed  Google Scholar 

  • Van Der Kraak, G., Rosenblum, P.M. and Peter, R.E. 1990. Growth hormone-dependent potentiation of gonadotropin-stimulated steroid production by ovarian follicles of the goldfish. Gen. Comp. Endocrinol. 79: 233–239.

    PubMed  Google Scholar 

  • Wallace, R.A. and Selman, K. 1978. Oogenesis in Fundulus heteroclitus I. Preliminary observations on oocyte maturation in vivo and in vitro. Dev. Biol. 62: 354–369.

    PubMed  Google Scholar 

  • Yamashita, M., Fukada, S., Yoshikuni, M., Bulet, P., Hirai, T., Yamaguchi, A., Lou, Y.H., Zhao, Z. and Nagahama, Y. 1992. Purification and characterization of maturation-promoting factor in fish. Dev. Biol. 148: 8–15.

    Google Scholar 

  • Yamashita, M., Kajiura, H., Tanaka, T., Onoe, S. and Nagahama, Y. 1995. Molecular mechanisms of the activation of maturation-promoting factor during goldfish oocyte maturation. Dev. Biol. 168: 62–75.

    Article  PubMed  Google Scholar 

  • Yoshikuni, M., Shibata, N. and Nagahama, Y. 1993. Specific binding of [3H] 17α, 20β-dihydroxy-4-pregnen-3-one to oocyte cortices of rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 11: 15–24.

    Google Scholar 

  • Yoshimura, Y., Mitsutoshi, I., Karube, M., Oda, T., Akiba, M., Shiokawa, S., Ando, M., Yoshinaga, A. and Nakamura, Y. 1994. Growth hormone stimulates follicular development by stimulating ovarian production of insulin-like growth factor-I. Endocrinology 135: 887–894.

    Article  PubMed  Google Scholar 

  • Young, G., Ueda, H. and Nagahama, Y. 1983. Estradiol-17β and 17α,20β-dihydroxy-4-pregnen-3-one production by isolated ovarian follicles of amago salmon (Oncorhynchus rhodurus) in response to mammalian pituitary and placental hormones and salmon gonadotropin. Gen. Comp. Endocrinol. 52: 329–335.

    Article  PubMed  Google Scholar 

  • Yu, K.L., Peng, C. and Peter, R.E. 1991. Changes in brain levels of gonadotropin-releasing hormone and serum levels of gonadotropin and growth hormone in goldfish during spawning. Can. J. Zool. 69: 182–188.

    Google Scholar 

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Correspondence to S.M. Hsiao.

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Negatu, Z., Hsiao, S. & Wallace, R. Effects of insulin-like growth factor-I on final oocyte maturation and steroid production in Fundulus heteroclitus. Fish Physiology and Biochemistry 19, 13–21 (1998). https://doi.org/10.1023/A:1007777926238

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