Skip to main content
SpringerLink
Log in

The cytochrome P450 system of Atlantic salmon (Salmo salar): II. Variations in hepatic catalytic activities and isozyme patterns during an annual reproductive cycle

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

Abstract

A group of Atlantic salmon (Salmo salar) was followed through their first year of maturation and spawning. At monthly intervals, starting with juvenile fish in December, 5–7 fish of each sex were killed, and liver and plasma were sampled. The last sampling point was of spawning fish in November a year later. Variables in the cytochrome P450 (P450) system were studied in hepatic microsomes, and estradiol 17β was measured in the plasma of females to assess the maturational status. The P450 1A1-mediated 7-ethoxyresorufin O-deethylase (EROD) started at high levels in winter, but decreased to non-detectable activities in pre-spawning females. Decreases, but not to the same extent, were also observed during this period in total cytochrome P450, cytochrome b5, NADPH-cytochrome P450 reductase, and in the content of two immunochemically determined P450 isozymes. At the same time, LSI levels increased in maturing females (starting in July), and GSI levels increased in both sexes (starting in May). Sex specific differences were observed in pre-spawning fish in September and October, with levels of total P450, b5, NADPH-cytochrome P450 reductase, EROD and P450 isozymes significantly lower in females. At the same time, plasma estradiol-17β levels reached peak values in females. The results point to the important role of sex steroids such as estradiol-17β as major factors in the regulation of final sexual maturation. However, this study also indicates that there may be estradiol-17β independent events of equal importance in the early stages of gonadal maturation that may involve the P450 system. The changes observed in the P450 system (as a major drug and steroid metabolizing system) of Atlantic salmon during sexual maturation may be of importance both in the endogenous transduction of hormonal signals, and as a pharmacological basis for designing therapeutic treatment of diseases in the aquaculture industry.

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 cited

  • Andersson, T. 1989. Sex differences in cytochrome P-450-dependent xenobiotic and steroid metabolism in the mature rainbow trout kidney. J. Endocrinol. 126: 9–16.

    Google Scholar 

  • Bagenal, T.B. and Tesch, F.W. 1978. Methods for assessment of fish production in fresh waters. Age and Growth. Blackwell Scientific Publication, Oxford.

    Google Scholar 

  • Celander, M. Ronis, M. and Förlin, L. 1989. Initial characterization of a constitutive cytochrome P-450 isoenzyme in rainbow trout liver. Mar. Environ. Res 28: 9–14.

    Google Scholar 

  • Edwards, A.J., Addison, R.F., Willis, D.E. and Renton, K.W. 1988. Seasonal variation of hepatic mixed function oxidases in winter flounder (Pseudopleuronectes americanus). Mar. Environ. Res. 26: 299–309.

    Google Scholar 

  • Förlin, L. 1980. Effects of Clophen A50,3-methylcholanthrene, pregnenolone-16α-carbonitrile, and phenobarbital on the hepatic microsomal cytochrome P-450-dependent monooxygenase system in rainbow trout, Salmo gairdneri, of different age and sex. Toxicol. Appl. Pharmacol. 54: 420–430.

    Google Scholar 

  • Förlin, L. and Hansson, T. 1982. Effects of oestradiol-17β and hypophysectomy on hepatic mixed function oxidases in rainbow trout. J. Endocrinol. 95: 245–252.

    Google Scholar 

  • Förlin, L. and Haux, C. 1990. Sex differences in hepatic cytochrome P-450 monooxygenase activities in rainbow trout during an annual reproductive cycle. J. Endocrinol. 124: 207–213.

    Google Scholar 

  • George, S., Young, P., Leaver, M. and Clarke, D. 1990. Activities of pollutant metabolising and detoxication systems in the liver of the plaice, Pleuronectes platessa: Sex and seasonal variations in non-induced fish. Comp. Biochem. Physiol. 96C: 185–192.

    Google Scholar 

  • Goksøyr, A. 1985. Purification of hepatic microsomal cytochromes P-450 from β-naphthoflavone-treated Atlantic cod (Gadus morhua), a marine teleost fish. Biochim. Biophys. Acta 840: 409–417.

    Google Scholar 

  • Goksøyr, A. 1991. A semi-quantitative cytochrome P450IA1 ELISA: A simple method for studying the monooxygenase induction response in environmental monitoring and ecotoxicological testing of fish. Sci. Tot. Envir. 101: 255–262.

    Google Scholar 

  • Goksøyr, A. and Larsen, H.E. 1991. The cytochrome P450 system of Atlantic salmon (Salmo salar): I. Basal properties and induction of P450 1A1 in liver of immature and mature fish. Fish Physiol. Biochem. 9: 339–349.

    Google Scholar 

  • Goksøyr, A., Larsen H.E. and Husøy, A.-M. 1991a. Application of a cytochrome P450 IA1-ELISA in environmental monitoring and toxicological testing of fish. Comp. Biochem. Physiol. 100C: 157–160.

    Google Scholar 

  • Goksøyr, A., Andersson, T., Buhler, D.R., Stegeman, J.J., Williams, D.E. and Förlin, L. 1991b. Immunochemical cross-reactivity of β-naphtoflavone-inducible cytochrome P-450 (P4501A) in liver microsomes from different fish species and rat. Fish Physiol. Biochem. 9: 1–13.

    Google Scholar 

  • Goksøyr, A. and Förlin, L. 1992. The cytochrome P450 system in fish, aquatic toxicology, and environmental monitoring. Aquat. Toxicol. 22: 287–312.

    Google Scholar 

  • Hansson, T. and Gustafsson, J.-Å. 1981. In-vitro metabolism of 4-androstene-3,17-dione by hepatic microsomes from the rainbow trout (Salmo gairdnerii): Effects of hypophysectomy and oestradiol-17β. J. Endocrinol. 90: 103–112.

    Google Scholar 

  • Klotz, A.V., Stegeman, J.J. and Walsh, C. 1984. An alternative 7-ethoxyresorufin O-deethylase activity assay: a continuous visible spectrophotometric method for measurement of cytochrome P-450 monooxygenase activity. Anal. Biochem. 140: 138–145.

    Google Scholar 

  • Koivusaari, U., Harri, M. and Hanninen, O. 1981. Seasonal variation of hepatic biotransformation in female and male rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 70: 149–157.

    Google Scholar 

  • Larsen, H.E. and Goksøyr, A. 1989. Characterization of the hepatic cytochrome P-450 system in Atlantic salmon (Salmo salar). Mar. Environ. Res. 28: 148.

    Google Scholar 

  • Lindström-Seppä, P. 1985. Seasonal variation of the xenobiotic metabolizing enzyme activities in the liver of male and female vendace (Coregonus albula L.). Aquat. Toxicol. 6: 323–331.

    Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193: 265–275.

    Google Scholar 

  • Matsubara, T. Prough, R.A., Burke, M.D. and Estabrook, R.W. 1974. The preparation of microsomal fractions of rodent respiratory tract and their characterization. Cancer Res. 34: 2196–2203.

    Google Scholar 

  • Miranda, C.L., Wang, J.-L., Henderson, M.C. and Buhler, D.R. 1990. Immunological characterization of constitutive isozymes of cytochrome P-450 from rainbow trout. Evidence for homology with phenobarbital-induced rat P-450s. Biochem. Biophys. Acta 1037: 155–160.

    Google Scholar 

  • Mommsen, P.T. and Walsh, P.J. 1988. Vitellogenesis and oocyte assembly. Fish Physiology. Academic Press, New York.

    Google Scholar 

  • Nebert, D.W., Adesnik, M. Coon, M.J., Estabrook, R.W., Gonzalez, F.J., Guengerich, F.P., Gunsalus, I.C., Johnson, E.F., Kemper, B., Levin, W., Phillips, I.R., Sato, R. and Waterman, M.R. 1987. The P450 gene superfamily: Recommended nomenclature. DNA 6: 1–11.

    Google Scholar 

  • Nebert, D.W., Nelson, D.R., Coon, M.J., Estabrook, R.W., Feyereisen, R., Fujii-Kuriyama, Y., Gonzalez, F., Guengerich, F.P., Gunsalus, I.C., Johnson, E.F., Loper, J.C., Sato, R., Waterman, M.R. and Waxman, D.J. 1991. The P450 superfamily: Update on new sequences, gene mapping, and recommended nomenclature. DNA Cell Biol. 10: 1–14.

    Google Scholar 

  • Omura, T. and Sato, R. 1964. The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J. Biol. Chem. 239: 2370–2378.

    Google Scholar 

  • Oppen-Berntsen, D.O., Gram-Jensen, E. and Walther, B.T. 1991. Origin of teleostean eggshell zr-proteins and their significance during oogenesis: In vitro liver synthesis of eggshell proteins induced by estradiol-17β. Proc. 4th Int. Symp. Reproductive Physiology of Fish, Norwich, pp. 306–309. Edited by A.P. Scott, J.P. Sumpter, D.E. Kime and M.S. Rolfe. FishSymp91, Sheffield.

  • Pajor, A.M., Stegeman, J.J., Thomas, P. and Woodin, B.R. 1990. Feminization of the hepatic microsomal cytochrome P-450 system in brook trout by oestradiol, testosterone and pituitary factors. J. Exp. Zool. 253: 51–60.

    Google Scholar 

  • Payne, J.F., Fancey, L.L., Rahimtula, A.D. and Porter, E.L. 1987. Review and perspective on the use of mixed-function oxygenase enzymes in biological monitoring. Comp. Biochem. Physiol. 86C: 233–245.

    Google Scholar 

  • Prough, R.A., Burke, M.D. and Mayer, R.T. 1978. Direct fluorometric methods for measuring mixed-function oxidase activity. Meth. Enzymol. 52: 372–377.

    Google Scholar 

  • Snegaroff, J. and Bach, J. 1990. The effects of temperature on the basal activity of cytochrome P-450 in rainbow trout (Salmo gairdneri). Comp. Biochem. Physiol. 95B: 515–519.

    Google Scholar 

  • Stegeman, J.J. 1989. Cytochrome P450 forms in fish: catalytic, immunological and sequence similarities. Xenobiot. 19: 1093–1110.

    Google Scholar 

  • Stegeman, J.J. and Chevion, M. 1980. Sex differences in cytochrome P-450 and mixed-function oxygenase activity in gonadally mature trout. Biochem. Pharmacol. 29: 553–558.

    Google Scholar 

  • Stegeman, J.J., Pajor, A.M. and Thomas, P. 1982. Influence of estradiol and testosterone on cytochrome P-450 and monooxygenase activity in immature brook trout, Salvelinus fontinalis. Biochem. Pharmacol. 31: 3979–3989.

    Google Scholar 

  • Tarlebø, J., Solbakken, J.E. and Palmork, K.H. 1985. Variation in hepatic aryl hydrocarbon hydroxylase activity in flounder, Platichtys flesus: A baseline study. Helgol. Meer. Unters. 39: 187–199.

    Google Scholar 

  • Walton, D.G., Fancey, L.L., Greene, J.M., Kiceniuk, J.W. and Penrose, W.R. 1983. Seasonal changes in aryl hydrocarbon hydroxylase activity of a marine fish Tautogolabrus adspersus (Walbaum) with and without petroleum exposure. Comp. Biochem. Physiol. 76: 247–253.

    Google Scholar 

  • Williams, D.E., Masters, B.S.S., Lech, J.J. and Buhler, D.R. 1986. Sex differences in cytochrome P-450 isozyme composition and activity in microsomes of mature rainbow trout. Biochem. Pharmacol. 35: 2017–2023.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Marine Molecular Biology, University of Bergen, HIB, N-5020, Bergen, Norway

    Håvard E. Larsen & Anders Goksøyr

  2. Department of Zoophysiology, University of Göteborg, Medicinaregatan 18, S-413 90, Göteborg, Sweden

    Malin Celander

Authors
  1. Håvard E. Larsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Malin Celander
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anders Goksøyr
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Parts of this work were presented at the 5th International Symposium on Responses of Marine Organisms to Pollutants, April 1989 in Plymouth, United Kingdom (Larsen and Goks\/oyr 1989).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Larsen, H.E., Celander, M. & Goksøyr, A. The cytochrome P450 system of Atlantic salmon (Salmo salar): II. Variations in hepatic catalytic activities and isozyme patterns during an annual reproductive cycle. Fish Physiol Biochem 10, 291–301 (1992). https://doi.org/10.1007/BF00004478

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00004478

Keywords

Search

Navigation