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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
REFERENCES
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.
Borg, B. 1994.Mini review: Androgens in teleost fishes. Comp. Biochem. Physiol. C. 109: 219–245.
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.
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.
Consten, D. 2001. Stress response and pubertal development in the male common carp, Cyprinus carpio L. Thesis. University of Utrecht, Utrecht, The Netherlands.
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.
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.
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.
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.
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.
Monder, C. 1991. Corticosteroids, receptors, and the organ-specific functions of 11 beta-hydroxysteroid dehydrogenase.FASEB J.5: 3047–3054.
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.
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.
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.
Schulz, R.W. 1985.Measurement of five androgens in the blood of immature and mature male rainbow trout, Salmo gairdneri (Richardson).Steroids46:717–726.
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.
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.
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.
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.
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.
Wendelaar Bonga, S.E. 1997. The stress response in fish.Physiol. Rev.77: 591–625.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Consten, D., Keuning, E., Terlou, M. et al. Cortisol effects on the testicular androgen synthesizing capacity in common carp, Cyprinus carpio L.. Fish Physiology and Biochemistry 25, 91–98 (2001). https://doi.org/10.1023/A:1020538729104
Issue Date:
DOI: https://doi.org/10.1023/A:1020538729104