Skip to main content
SpringerLink
Log in

Effects of cortisol and triiodo-L-thyronine on the steroidogenic capacity of rainbow trout ovarian follicles at two stages of oocyte maturation

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

Abstract

The in vitro basal and salmon gonadotropin (sGTH)-stimulated steroidogenic capacity of rainbow trout follicles was examined at four stages [early (EV)-, mid (MV)- and peak-vitellogenic (PV), and pre-ovulatory, post-vitellogenic (PO)] of gonadal recrudescence using radioimmunoassays (RIAs) to measure 17β-estradiol (E2) and testosterone (T) production. In addition, follicles were incubated in the presence of [3H]pregnenolone ([3H]P5) and the radiolabelled steroid metabolites produced were separated using high performance liquid chromatography (HPLC). Peak basal and sGTH-stimulated E2 and T production was found in PV stage follicles and lowest in PO stage follicles, and there were marked differences in the HPLC profiles of steroid metabolites. For EV stage follicles the major metabolite eluted as a peak that co-eluted with the androstenedione (A4) and 17α-hydroxyprogesterone (17α-OHP) standards. A smaller peak that co-eluted with 11β-hydroxyandrostenedione (11β-OHA4) and very small peaks co-eluting with 20α-dihydroprogesterone (20α-DHP) and E2 were also seen. MV and PV stage follicles produced predominantly E2, together with a small combined A4 + 17α-DHP peak, traces of 11β-OHA4 and two peaks that did not co-elute with any of the reference standards. The PO stage follicles produced only 17, 20β-dihydroxy-4-pregnene-3-one (17,20β-P).

In addition, the effects of cortisol and triiodothyronine (T3) on steroidogeneis were investigated in PV and PO stage ovarian follicles. For PV stage follicles, cortisol at 100 ng ml−1 in the incubation medium significantly suppressed both basal and sGtH- stimulated T and E2 production relative to control treatments. T3 at 10 ng ml−1 in the medium had no significant effect on either basal or sGtH-stimulated T or E2 production compared to the controls, nor did it have any beneficial effect over the suppressive effect of cortisol. PO phase follicles taken 1 to 2 weeks prior to anticipated spawning had very low E2 and T production, and there was no effect of cortisol or T3, alone or in combination, on E2 or T production. For PV stage follicles incubated in the presence of [3H]P5, cortisol suppressed T and E2 production, but did not block the steroid pathway at any specific level; T3 had no apparent affect on the metabolism of [3H]P5. The PO stage follicles produced little or no E2; the major metabolite was 17,20β-P. Cortisol and T3 had no apparent effect on either basal or sGtH-stimulated 17,20β-P production by the follicles at this stage of maturation.

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

  • Barry, T.P., Malison, J.A., Lapp, A.F. and Procarione, L.S. 1995. Effects of selected hormones and male cohorts on final oocyte maturation, ovulation, and steroid production in walleye (Stizostedion vitreum). Aquaculture 138: 331–347.

    Google Scholar 

  • Campbell, P.M., Pottinger, T.G. and Sumpter, J.P. 1992. Stress reduces the quality of gametes produced by rainbow trout. Biol. Reprod. 47: 1140–1150.

    Google Scholar 

  • Campbell, P.M., Pottinger, T.G. and Sumpter, J.P. 1994. Preliminary evidence that chronic confinement stress reduces the quality of gametes produced by brown and rainbow trout. Aquaculture 120: 151–169.

    Google Scholar 

  • Carragher, J.F. and Sumpter, J.P. 1990. The effect of cortisol on the secretion of sex steroids from cultured ovarian follicles of rainbow trout. Gen. Comp. Endocrinol. 77: 403–407.

    Google Scholar 

  • Carragher, J.F., Sumpter, J.P., Pottinger, T.G. and Pickering, A.D. 1989. The deleterious effects of cortisol implantation on reproductive function in two species of trout, Salmo trutta L. and Salmo gairdneri Richardson. Gen. Comp. Endocrinol. 76: 310–321.

    Google Scholar 

  • Chakraborty, P., Maitra, G. and Bhattacharya, S. 1986. Binding of thyroid hormone to isolated ovarian nuclei from a freshwater perch, Anabas testudineus. Gen. Comp. Endocrinol. 62: 239–246.

    Google Scholar 

  • Cyr, D.G. and Eales, J.G. 1988. In vitro effects of thyroid hormones on gonadotropin-induced estradiol-17β secretion by ovarian follicles of rainbow trout, Salmo gairdneri. Gen Comp. Endocrinol. 69: 80–87.

    Google Scholar 

  • Donaldson, E.M. 1973. Reproductive endocrinology of fishes. Am. Zool. 13: 909–927.

    Google Scholar 

  • Donaldson, E.M., Yamazaki, F., Dye, H.M. and Philleo, W.W. 1972. Preparation of gonadotropin from salmon (Oncorhynchus tshawytscha) pituitary glands. Gen. Comp. Endocrinol. 18: 469–481.

    Google Scholar 

  • Epler, P. and Bieniarz, K. 1983. Effects of triiodothyronine and some of gonadotropic and steroid hormones on the maturation of carp (Cyprinus carpio L.) oocytes in vitro. Repro. Nutr. Dev. 23: 1011–1017.

    Google Scholar 

  • Foo, J.T.W. and Lam, T.J. 1993a. Retardation of ovarian growth and depression of serum steroid levels in tilapia, Oreochromis mossambicus by cortisol implantation. Aquaculture 115: 133–143.

    Google Scholar 

  • Foo, J.T.W. and Lam, T.J. 1993b. Serum cortisol response to handling stress and the efeect of cortisol implantation on testosterone level in the tilapia, Oreochromis mossambicus. Aquaculture 115: 145–158.

    Google Scholar 

  • Gillet, C., Billard, R. and Breton, B. 1981. La réproduction du poisson rouge Carassius auratus élevé a 30 °C: éffet de la photoperiode, de l'alimentation et de l'oxygenation. Cah. Lab. Montereau. 11: 49–56.

    Google Scholar 

  • Goswami, S.V. and Sundararaj, B.I. 1974. Effects of C18, C19, and C21 steroids on in vitro maturation of oocytes of the catfish, Heteropneustes fossilis (Bloch). Gen. Comp. Endocrinol. 23: 282–285.

    Google Scholar 

  • Holloway, A.C., Sheridan, M.A., Van Der Kraak, G. and Leatherland, J.F. 1999. Correlations of plasma growth hormone with somatostatin, gonadal steroid hormones and thyroid hormones in rainbow trout during sexual recrudescence. Comp. Biochem. Physiol. (In press).

  • Hurlburt, M.E. 1977. Role of thyroid gland in ovarian maturation of the goldfish, Carassius auratus L. Can. J. Zool. 55: 1906–1913.

    Google Scholar 

  • Jalabert, B. and Fostier, A. 1984. The modulatory effect of in vitro of oestradiol-17β, testosterone or cortisol on the output of 17α-hydroxy-20β-dihydroxyprogesterone by rainbow trout (Salmo gairdneri) ovarian follicles stimulated by the maturational gonadotropin s-GtH. Reprod. Nutr. Dev. 24: 127–136.

    Google Scholar 

  • Khan, M.N., Reddy, P.K., Renaud, R.L. and Leatherland, J.F. 1997. Effect of cortisol on the metabolism of 17-hydroxyprogesterone by Arctic charr and rainbow trout embryos. Fish Physiol. Biochem. 16: 197–209.

    Google Scholar 

  • Kime, D.E. 1993. ‘Classical’ and ‘non-classical’ reproductive steroids in fish. Rev. Fish Biol. Fish. 3: 160–168.

    Google Scholar 

  • Kime, D.E., Venkatesh, B. and Tan, C.H. 1991. 5α-Pregnane-3β,7α,17,20α-and —20β-tetrols as metabolites of progesterone and 17-hydroxyprogesterone in carp (Cyprinus carpio) ovarian incubations. Gen. Comp. Endocrinol. 84: 401–404.

    Google Scholar 

  • Maitra, G. and Bhattacharya, S. 1989. Seasonal changes of triiodothyronine binding to piscine ovarian nuclei. Zool. Sci. 6: 771–775.

    Google Scholar 

  • Marte, C.L. and Lacanilo, F. 1986. Spontaneous maturation and spawning of milkfish in floating net cages. Aquaculture 53: 115–132.

    Google Scholar 

  • McMaster, M.E., Munkittrick, J.J., Robinson, R.D. and Van Der Kraak, G.J. 1995. Protocol for measuring in vitro steroid production by fish gonadal tissue. Can. Tech. Rept. Fish. Aquat. Sci. 1961: 78p.

  • Morrison, P.F., Leatherland, J.F. and Sonstegard, R.A. 1985. Plasma cortisol and sex steroid levels in Great Lakes coho salmon (Oncorhynchus kisutch) in relation to fecundity and egg survival. Comp. Biochem. Physiol. 80A: 61–68.

    Google Scholar 

  • Nagahama, Y. 1987. 17α,20β-Dihydroxy-4-pregnen-3-one: A teleost maturation-inducing hormone. Dev. Growth Differ. 29: 1–12.

    Google Scholar 

  • Nagahama, Y., Yoshikuni, M., Yamashita, M., Sakai, N. and Tanaka, M. 1993. Molecular endocrinology of oocyte growth and maturation in fish. Fish Physiol. Biochem. 11: 3–14.

    Google Scholar 

  • Pankhurst, N.W. 1998. Further evidence of the equivocal effects of cortisol on in vitro steroidogenesis by ovarian follicles of rainbow trout Oncorhynchus mykiss. Fish Physiol. Biochem. 19: 315–323.

    Google Scholar 

  • Pankhurst, N.W. and Dedual, M. 1994. Effects of capture and recovery on plasma levels of cortisol, lactate and gonadal steroids in a natural populations of rainbow trout, Oncorhynchus mykiss. J. Fish Biol. 45: 1013–1025.

    Google Scholar 

  • Pankhurst, N.W., Van Der Kraak, G. and Peter, R.E. 1995. Evidence that the inhibitory effect of stress on reproduction in teleost fish is not mediated by the action of cortisol on ovarian steroidogenesis. Gen. Comp. Endocrinol. 99: 249–257.

    Google Scholar 

  • Payne, D.W., Holtzclaw, W.D. and Adashi, E.Y. 1989. A conventional unified scheme for the differential extraction of conjugated and unconjugated serum C19 steroids on Sep-Pak C18-cartridges. J. Steroid Biochem. 33: 289–295.

    Google Scholar 

  • Pickering, A.D. and Christie, P. 1981. Changes in the concentration of plasma cortisol and thyroxine during sexual maturation of the hatchery-reared brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 44: 487–496.

    Google Scholar 

  • Pickering, A.D., Pottinger, T.G., Carragher, J.F. and Sumpter, J.P. 1987. The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta L. Gen Comp. Endocrinol. 68: 249–259.

    Google Scholar 

  • Scott, D.B.C. 1979. Environmental timing and the control of reproduction in teleost fish. Symp. Zool. Soc., London 44: 105–132.

    Google Scholar 

  • Scott, A.P. and Canario, A.V.M. 1992. 17α,20β-Dihydroxy-4-pregnen-3-one 20-sulphate: A major new metabolite of teleost oocyte maturation-inducing steroid. Gen. Comp. Endocrinol. 85: 91–100.

    Google Scholar 

  • Scott, A.P., Nagahama, Y., Van Der Kraak, G. and Nagler, J.J. 1995. Sulfation and uptake of the maturation inducing steroid, 17α,20β-dihydroxy-4-pregnen-3-one by rainbow trout ovarian follicles. Fish Physiol. Biochem. 14: 301–311.

    Google Scholar 

  • Soyano, K., Saito, T., Nagae, M. and Yamauchi, K. 1993. Effects of thyroid hormone on gonadotropin-induced steroid production in medaka, Oryzias latipes, ovarian follicles. Fish Physiol. Biochem. 11: 265–272.

    Google Scholar 

  • Sumpter, J.P., Carragher, J.F., Pottinger, T.G. and Pickering, A.D. 1987. Interaction of stress and reproduction in trout. In Reproductive Physiology of Fish 1987. pp. 299–302. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University of Newfoundland Press, St. John's.

  • Tambets, M., Mölsä, H. and Saat, T. 1997. Effect of triiodothyronine on in vitro maturation of vendace (Coregonus albula) oocytes under unfavourable influences. Ann. Zool. Fenn. 34: 213–216.

    Google Scholar 

  • Van Der Kraak, G. and Donaldson, E.M. 1986. Steroidogenic capacity of coho salmon ovarian follicles throughout the periovulatory period. Fish Physiol. Biochem. 1: 179–184.

    Google Scholar 

  • Venkatesh, B., Tan, C.H., Kime, D.E. and Lam, T.J. 1992. Steroid metabolism in teleost gonads: purification and identification of metabolites by high-performance liquid chromatography. Steroids 57: 276–281.

    Google Scholar 

  • Venkatesh, B., Tan, C.H. and Lam, T.J. 1989. Blood steroid levels in the goldfish: measurement of six ovarian steroids in small volumes of serum by reverse-phase high-performance liquid chromatography and radioimmunoassay. Gen. Comp. Endocrinol. 76: 398–407.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Guelph, Ontario, N1G 2W1, Canada

    P.K. Reddy, R. Renaud & J.F. Leatherland

Authors
  1. P.K. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Renaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J.F. Leatherland
    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

Reddy, P., Renaud, R. & Leatherland, J. Effects of cortisol and triiodo-L-thyronine on the steroidogenic capacity of rainbow trout ovarian follicles at two stages of oocyte maturation. Fish Physiology and Biochemistry 21, 129–140 (1999). https://doi.org/10.1023/A:1007800707094

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1007800707094

Search

Navigation