Fish Physiology and Biochemistry

, Volume 25, Issue 2, pp 91–98 | Cite as

Cortisol effects on the testicular androgen synthesizing capacity in common carp, Cyprinus carpio L.

  • D. Consten
  • E.D. Keuning
  • M. Terlou
  • J.G.D. Lambert
  • H.J.Th. Goos
Article

Abstract

Our previous studies on the effect of stress on pubertal development in carp have shown that repeated temperature changes caused an increase in cortisol levels and a retardation of the first waves of spermatogenesis. Identical effects, accompanied by a decrease in 11-ketotestosterone (11KT) plasma levels and the gonadosomatic index (GSI) were induced by cortisol administration via cortisol containing food pellets. The decrease in plasma 11KT is caused by a direct effect of cortisol on the steroid producing capacity of the testis, independent of luteinizing hormone (LH) levels. However, the mechanism through which cortisol interferes with testicular steroidogenesis is unknown. In the present study, we showed that in vitro physiological levels of cortisol can inhibit the conversion of 11β-hydroxyandrostenedione (OHA) into androstenetrione (OA), which is the precursor of 11KT, possibly by competing for the enzyme 11β-hydroxysteroid dehydrogenase (11β-HSD). The same mechanism may occur in vivo. However, our results demonstrate that an elevation of plasma cortisol levels during acute cortisol treatment did not result in lower plasma levels of OA and 11KT, but we did observe an accumulation of OHA. We suggest that the previously observed decrease in 11-oxygenated androgens, as an effect of long-term cortisol treatment, is caused by a retardation of testicular development. This results in a lower steroid synthesizing capacity of the testis as a whole. Although the in vitro observed cortisol inhibition of the conversion of OHA into 11KT plays a role in the accumulation of OHA, it apparently has no effect on the final 11KT plasma concentration.

androgens cortisol puberty spermatogenesis steroidogenesis stress testis 11β-HSD 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Bongers, A.B.J., Ben-Ayed, M.Z., Zandieh-Doulabi, B., Komen, J. and Richter, C.J.J. 1997. Origin of variation in isogenic, gynogenetic and androgenetic strains of common carp, Cyprinus carpio.J. Exp. Zool.277: 72–79.CrossRefGoogle Scholar
  2. Borg, B. 1994.Mini review: Androgens in teleost fishes. Comp. Biochem. Physiol. C. 109: 219–245.CrossRefGoogle Scholar
  3. Chrousos, G.P. and Gold, P.W. 1992. The concepts of stress and stress system disorders. Overview of physical and behavioural homeostasis.J. Am. Med. Assoc.267:1244–1252.CrossRefGoogle Scholar
  4. Consten, D., Lambert, J.G.D. and Goos, H.J.Th. 2000. Inhibitory effects of cortisol on in vivo and in vitro androgen secretion in male common carp, Cyprinus carpio. In: Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish. p.192. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson S.O. Bergen, Norway.Google Scholar
  5. Consten, D. 2001. Stress response and pubertal development in the male common carp, Cyprinus carpio L. Thesis. University of Utrecht, Utrecht, The Netherlands.Google Scholar
  6. Consten, D., Bogerd, J., Komen, J., Lambert, J.G.D. and Goos, H.J.Th. 2001a.Long-term cortisol treatment inhibits pubertal development in male common carp, Cyprinus carpio L.Biol. Reprod.64: 1063–1071.PubMedCrossRefGoogle Scholar
  7. Consten, D., Lambert, J.G.D. and Goos, H.J.Th. 2001b. Cortisol affects testicular development in male common carp, Cyprinus carpio L., but not via an effect on LH secretion.Comp. Biochem. Physiol. (B). 129: 671–677.CrossRefGoogle Scholar
  8. De Man, A.J.M., Hofman, J.A., Hendriks, Th., Rosmalen, F.M.A., Ross, H.A. and Benraad, Th.J. 1980.A direct radioimmunoassay for plasma aldosterone: significance of endogenous cortisol.Neth. J. Medicine23:79–83.Google Scholar
  9. Komen, J., Bongers, A.B.J., Richter, C.J.J., Van Muiswinkel, W.B. and Huisman, E.A. 1991. Gynogenesis in common carp (Cyprinus carpio L.) II: The production of homozygous gynogenetic clones and F1 hybrids.Aquaculture92:127–142.CrossRefGoogle Scholar
  10. Michael, A.E. and Cooke, B.A. 1994.A working hypothesis for the regulation of steroidogenesis and germ cell development in the gonads by glucocorticoids and 11β-hydroxysteroid dehydrogenase (11β-HSD).Mol. Cell. Endocrinol.100:55–63.PubMedCrossRefGoogle Scholar
  11. Monder, C. 1991. Corticosteroids, receptors, and the organ-specific functions of 11 beta-hydroxysteroid dehydrogenase.FASEB J.5: 3047–3054.PubMedGoogle Scholar
  12. Pankhurst, N.W. and Van der Kraak, G. 2000. Evidence that acute stress inhibits ovarian steroidogenesis in rainbow trout in vivo, through the action of cortisol.Gen. Comp. Endocrinol.117:225–237.PubMedCrossRefGoogle Scholar
  13. Pickering, A.D., Pottinger, T.G. and Sumpter, J.P. 1987. On the use of dexamethasone to block the pituitary-interrenal axis in the brown trout, Salmo trutta L. Gen. Comp. Endocrinol.65: 346–353.PubMedCrossRefGoogle Scholar
  14. Schultz, R., Isola, J., Parvinen, M., Honkaniemi, J., Wikström, A., Gustafsson, J-Å. and Pelto-Huikko, M. 1993.Localization of the glucocorticoid receptor in testis and accessory sexual organs of male rat.Mol. Cell. Endocrinol.95: 115–120.PubMedCrossRefGoogle Scholar
  15. Schulz, R.W. 1985.Measurement of five androgens in the blood of immature and mature male rainbow trout, Salmo gairdneri (Richardson).Steroids46:717–726.PubMedCrossRefGoogle Scholar
  16. Schulz, R.W., Lubberink, K., Zandbergen, M.A., Janssen-Dommerholt, C., Peute, J. and Goos, H.J.Th. 1996. Testicular responsiveness to gonadotropic hormone in vitro and Leydig and Sertoli cell ultrastructure during pubertal development of male African catfish (Clarias gariepinus).Fish Physiol. Biochem.15: 243–254.CrossRefGoogle Scholar
  17. Simpson, T.H. and Wright R.S. 1977.A radioimmunoassay for 11-oxotestosterone: its application in the measurement of levels in bloodserum of rainbow trout (S. gairdneri).Steroids29:383–398.PubMedCrossRefGoogle Scholar
  18. Takeo, J., Hata, J., Segawa, C., Toyohara, H., and Yamashita, S. 1996. Fish glucocorticoid receptor with splicing variants in the DNA binding domain.FEBS Lett.389: 244–248.PubMedCrossRefGoogle Scholar
  19. Tanck, M.W.T., Booms, G.H.R., Eding, E.H., Wendelaar Bonga, S.E. and Komen, J.2000 Cold shock: A stressor for common carp, Cyprinus carpio L.J. Fish Biol.57:881–894.CrossRefGoogle Scholar
  20. Van Dijk, P.L.M., Van den Thillart, G.E.E.J.M., Balm, P.H.M. and Wendelaar Bonga, S.E. 1993. The influence of gradual water acidification on the acid/base status and plasma hormone levels in carp.J. Fish Biol.42: 661–671.CrossRefGoogle Scholar
  21. Wendelaar Bonga, S.E. 1997. The stress response in fish.Physiol. Rev.77: 591–625.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • D. Consten
    • 1
  • E.D. Keuning
    • 1
  • M. Terlou
    • 1
  • J.G.D. Lambert
    • 1
  • H.J.Th. Goos
    • 1
  1. 1.Graduate School for Developmental Biology, Research Group for Comparative EndocrinologyUtrecht UniversityUtrechtThe Netherlands

Personalised recommendations