Fish Physiology and Biochemistry

, Volume 19, Issue 1, pp 13–21 | Cite as

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

  • Z. Negatu
  • S.M. Hsiao
  • R.A. Wallace


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.

estradiol Fundulus heteroclitus growth hormone IGF-I IGF-II oocyte maturation ovarian follicle steroidogenesis signal transduction testosterone 


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  1. Adashi, E.Y. 1994. Growth factors and ovarian function: The IGF-I paradigm. Horm. Res. 42: 44–48.PubMedGoogle Scholar
  2. 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.PubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.PubMedGoogle Scholar
  5. 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.PubMedGoogle Scholar
  6. 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.PubMedGoogle Scholar
  7. 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
  8. 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.PubMedGoogle Scholar
  9. 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
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. Giudice, L.C. 1992. Insulin-like growth factors and ovarian follicular development. Endocr. Rev. 13: 641–669.CrossRefPubMedGoogle Scholar
  13. 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.PubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. Grigorescu, F., Baccara, M-T., Rouard, M. and Renard, E. 1994. Insulin and IGF-I signaling in oocyte maturation. Horm. Res. 42: 55–61.PubMedGoogle Scholar
  16. 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
  17. 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.PubMedGoogle Scholar
  18. 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.PubMedGoogle Scholar
  19. 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.PubMedGoogle Scholar
  20. Humbel, R.E. 1990. Insulin-like growth factors I and II. Eur. J. Biochem. 190: 445–462.PubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.PubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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
  34. 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.PubMedGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. Selman, K. and Wallace, R.A. 1986. Gametogenesis in Fundulus heteroclitus. Am. Zool. 26: 173–192.Google Scholar
  38. 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.PubMedGoogle Scholar
  39. 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.PubMedGoogle Scholar
  40. 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
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.PubMedGoogle Scholar
  43. 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.PubMedGoogle Scholar
  44. 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
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. 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

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  1. 1.Whitney Laboratory of University of FloridaUSA
  2. 2.Department of Anatomy and Cell Biology, College of MedicineUniversity of FloridaGainesvilleUSA

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