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A comparison of sex steroid binding protein (SBP) in four species of teleost fish

Abstract

A sex steroid binding protein (SBP) binding E2 with high affinity has been detected in a pleuronectid (greenback flounder Rhombosolea tapirina), two sparids (black bream Acanthopagrus butcheri and snapper Pagrus auratus), and its presence has been confirmed in a salmonid (rainbow trout Oncorhynchus mykiss). SBP binding characteristics were measured using a hot saturation assay for trout, bream and snapper, and a cold saturation assay for flounder. Bound and unbound steroid were separated by incubation with dextran-coated charcoal (DCC). Affinity for E2 was highest in trout (kD=0.44 nM), followed by bream (kD=3.39 nM) and snapper (kD=10.7 nM). The lowest affinity was found in flounder (kD=84.7 nM). Binding capacity, however, was greatest in flounder (Bmax=164 nM), followed by trout (Bmax=92 nM), and then bream and snapper (Bmax=50 and 39 nM, respectively). Binding of E2 to SBP had a very rapid rate of association, and most dissociation occurred within 5 min. To confirm that the plasma protein measured here was SBP, the relative binding affinities of SBP for a range of steroids were measured. In trout, bream and snapper, SBP bound E2 with the highest affinity, followed by T. In contrast, the relative affinity of T for flounder SBP was more than twice that of E2. The rank orders of affinity of binding indicate the importance of an unhindered 17β-hydroxyl group, and a 3-hydroxyl or 3-ketone group for high affinity binding to SBP. These requirements for high affinity binding are present in most animals possessing SBP and indicate conservation of the SBP molecule through evolution.

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References

  • Barnett, C.W. and Pankhurst, N.W. 1999. Reproductive biology and endocrinology of greenback flounder Rhombosolea tapirina(Günther 1862). Mar. Freshwater Res. 50: 35-42.

    Google Scholar 

  • Caldwell, C.A., Kattesh, H.G. and Strange, R. 1991. Distribution of cortisol among its free and protein-bound fractions in rainbow trout (Oncorhynchus mykiss): evidence of control by sexual maturation. Comp. Biochem. Physiol. 99A: 593-595.

    Google Scholar 

  • Callard, I.P. and Callard, G.V. 1987. Sex steroid receptors and nonreceptor binding proteins. In: Hormones and Reproduction in Fishes, Amphibians, and Reptiles. pp. 355-384. Edited by D.O. Norris and R.E. Jones. Plenum Press, New York.

    Google Scholar 

  • Chang, C.F. and Lee, Y.H. 1992. Purification of the sex steroidbinding protein from common carp (Cyprinus carpio) plasma. Comp. Biochem. Physiol. 101B: 587-590.

    Google Scholar 

  • Cleary, J.J. 1997. The effect of stress on reproduction in snapper, Pagrus auratus(Sparidae). PhD Thesis, University of Tasmania, Launceston.

    Google Scholar 

  • Fostier, A. and Breton, B. 1975. Binding of steroids by plasma of a teleost: the rainbow trout, Salmo gairdnerii. J. Steroid Biochem. 6: 345-351.

    Google Scholar 

  • Foucher, J.-L. and Le Gac, F. 1989. Evidence for an androgen binding protein in the testis of a teleost fish (Salmo gairdneriR.): a potential marker of sertoli cell function. J. Steroid Biochem. 32: 545-552.

    Google Scholar 

  • Foucher, J.L., Niu, P.D., Mourot, B., Vaillant, C. and Le Gac, F. 1991. In vivoand in vitrostudies on sex steroid binding protein (SBP) regulation in rainbow trout (Oncorhynchus mykiss): influence of sex steroid hormones and of factors linked to growth and metabolism. J. Steroid Biochem. Molec. Biol. 39: 975-986.

    Google Scholar 

  • Foucher, J.L., Le Bail, P.-Y. and Le Gac, F. 1992. Influence of hypophysectomy, castration, fasting, and spermiation on SBP concentration in male rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 85: 101-110.

    Google Scholar 

  • Freeman, H.C. and Idler, D.R. 1971. Binding affinities of blood proteins for sex hormones and corticosteroids in fish. Steroids 17: 233-250.

    Google Scholar 

  • Haddy, J.A. and Pankhurst, N.W. 1998. Annual change in reproductive condition and plasma concentrations of sex steroids in black bream, Acanthopagrus butcheri(Munro) (Sparidae). Mar. Freshwater Res. 49: 389-397.

    Google Scholar 

  • Ho, S.M., Tsang, P. and Callard, I.P. 1980. Some properties of a steroid-binding protein in the plasma of an ovoviviparous dog-fish, Squalus acanthias, at different stages of the life cycle. Biol. Reprod. 23: 281-289.

    Google Scholar 

  • Ho, S.M., Lance, V. and Megaloudis, M. 1987. Plasma sexsteroid binding protein in a seasonally breeding reptile, Alligator mississippiensis. Gen. Comp. Endocrinol. 65: 121-132.

    Google Scholar 

  • Hobby, A.C. and Pankhurst, N.W. 1997a. The relationship between plasma and ovarian levels of gonadal steroids in the repeat spawning marine fishes Pagrus auratus(Sparidae) and Chromis dispilus(Pomacentridae). Fish Physiol. Biochem. 16: 65-75.

    Google Scholar 

  • Hobby, A.C. and Pankhurst, N.W. 1997b. Comparative aspects of steroid binding protein (SBP) in four fishes: a salmonid, a pleuronectid and two sparids. In: Advances in Comparative Endocrinology. pp. 1369-1373. Edited by S. Kawashima and S. Kikuyama. Monduzzi Editore, Bologna.

    Google Scholar 

  • Hobby, A.C., Geraghty, D.P. and Pankhurst, N.W. 2000. Differences in binding characteristics of sex steroid binding protein in reproductive and nonreproductive female rainbow trout (Oncorhynchus mykiss), black bream (Acanthopagrus butcheri), and greenback flounder (Rhombosolea tapirina). Gen. Comp. Endocrinol. 120: 249-259.

    Google Scholar 

  • Hryb, D.J., Khan, M.S., Romas, N.A. and Rosner, W. 1990. The control of the interaction of sex hormone-binding globulin with its receptor by steroid hormones. J. Biol. Chem. 265: 6048-6054.

    Google Scholar 

  • Johnson, A.R., Holmes, S.D., Lipshultz, L.I. and Smith, R.G. 1985. Rapid method for quantification of androgen binding protein in sertoli cell cultures and its use for measurement of binding kinetics. J. Steroid Biochem. 22: 9-14.

    Google Scholar 

  • Joseph, D.R. 1994. Structure, function, and regulation of androgen-binding protein/sex hormone-binding globulin. Vitam. Horm. 49: 197-280.

    Google Scholar 

  • Laidley, C.W. and Thomas, P. 1994. Partial characterization of a sex-steroid binding protein in the spotted seatrout (Cynoscion nebulosus). Biol. Reprod. 51: 982-992.

    Google Scholar 

  • Lazier, C.B., Lonergan, K. and Mommsen, T.P. 1985. Hepatic estrogen receptors and plasma estrogen-binding activity in the Atlantic salmon. Gen. Comp. Endocrinol. 57: 234-245.

    Google Scholar 

  • Lobl, T.J. 1981. Androgen transport proteins: physical properties, hormonal regulation, and possible mechanism of TeBG and ABP action. Arch. Androl. 7: 133-151.

    Google Scholar 

  • McPherson, G.A. 1985. Analysis of radioligand binding experiments. A collection of computer programs for the IBM PC. J. Pharmacological Methods 14: 213-228.

    Google Scholar 

  • McPherson, R., Hannum, J. and Greco, T. 1988. An investigation of an estrogen-binding component in the liver and plasma of brook char, Salvelinus fontinalis. Comp. Biochem. Physiol. 89A: 615-619.

    Google Scholar 

  • Mercier-Bodard, M., Alfsen, A. and Baulieu, E.E. 1970. Sex steroid binding plasma protein (SBP). Acta Endocrinol. Suppl. 147: 204-224.

    Google Scholar 

  • Milligan, S.R., Khan, O. and Nash, M. 1998. Competitive binding of xenobiotic oestrogens to rat alpha-fetoprotein and to sex steroid binding proteins in human and rainbow trout (Oncorhynchus mykiss) plasma. Gen. Comp. Endocrinol. 112: 89-95.

    Google Scholar 

  • Munson, P.J. and Rodbard, D. 1980. LIGAND: A versatile computerized approach for characterization of ligand-binding systems. Anal. Biochem. 107: 220-239.

    Google Scholar 

  • Pankhurst, N.W. and Thomas, P.M. 1998. Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout Oncorhynchus mykissto luteinizing hormone releasing hormone analogue. Aquaculture 166: 163-177.

    Google Scholar 

  • Paolucci, M. and Di Fiore, M.M. 1994. Sex steroid binding proteins in the plasma of the green frog, Rana esculenta: Changes during the reproductive cycle and dependence on pituitary gland and gonads. Gen. Comp. Endocrinol. 96: 401-411.

    Google Scholar 

  • Paolucci, M., De Fiore, M.M., Ciarcia, G. and Botte, V. 1992. Plasma sex steroid binding proteins (SSBP) in the male lizard, Podarcis s. sicula, during the reproductive cycle. Gen. Comp. Endocrinol. 87: 232-239.

    Google Scholar 

  • Pasmanik, M. and Callard, G. 1986. Characteristics of testosterone-estradiol binding globulin (TEBG) in goldfish serum. Biol. Reprod. 35: 838-845.

    Google Scholar 

  • Petra, P.H. 1991. The plasma sex steroid binding protein (SBP or SHBG). A critical review of recent developments on the structure, molecular biology and function. J. Steroid Biochem. Molec. Biol. 40: 735-753.

    Google Scholar 

  • Porto, C.S., Gunsalus, G.L., Bardin, C.W., Phillips, D.M. and Musto, N.A. 1991. Receptor-mediated endocytosis of an extracellular steroid-binding protein (TeBG) in MCF-7 human breast cancer cells. Endocrinology 129: 436-445.

    Google Scholar 

  • Pottinger, T.G. 1986. Estrogen-binding sites in the liver of sexually mature male and female brown trout, Salmo truttaL. Gen. Comp. Endocrinol. 61: 120-126.

    Google Scholar 

  • Pottinger, T.G. 1987. Androgen binding in the skin of mature male brown trout, Salmo truttaL. Gen. Comp. Endocrinol. 66: 224-232.

    Google Scholar 

  • Pottinger, T.G. 1988. Seasonal variation in specific plasma-and target-tissue binding of androgens, relative to plasma steroid levels, in the brown trout, Salmo truttaL. Gen. Comp. Endocrinol. 70: 334-344.

    Google Scholar 

  • Pottinger, T.G., and Pickering, A.D. 1990. The effect of cortisol administration on hepatic and plasma estradiol-binding capacity in immature female rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 80: 264-273.

    Google Scholar 

  • Scott, A.P., Bye, V.J. and Baynes, S.M. 1980. Seasonal variations in sex steroids of female rainbow trout (Salmo gairdneriRichardson). J. Fish Biol. 17: 587-592.

    Google Scholar 

  • Slaunwhite, W.R. and Rosenthal, H. 1976. Quantitation of specific binding proteins. In: Hormones in Human Blood. Detection and Assay. pp. 777-794. Edited by H.N. Antoniades. Harvard University Press, Cambridge.

    Google Scholar 

  • Thomas, P.M., Pankhurst, N.W. and Bremner, H.A. 1999. The effect of stress and exercise on post-mortem biochemistry of Atlantic salmon and rainbow trout. J. Fish Biol. 54: 1177-1196.

    Google Scholar 

  • Van Der Kraak, G. and Biddiscombe, S. 1999. Polyunsaturated fatty acids modulate the properties of the sex steroid binding protein in goldfish. Fish Physiol. Biochem. 20: 115-123.

    Google Scholar 

  • Westphal, U. 1978. Steroid-binding serum globulins: Recent results. In: Receptors and Hormone Action. pp. 443-472. Edited by B.W. O'Malley and L. Birnbaumer. Academic Press, New York.

    Google Scholar 

  • Westphal, U. 1986. Steroid-Protein Interactions II, Monographs on Endocrinology 27, Springer-Verlag, New York.

    Google Scholar 

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Hobby, A., Pankhurst, N. & Geraghty, D. A comparison of sex steroid binding protein (SBP) in four species of teleost fish. Fish Physiology and Biochemistry 23, 245–256 (2000). https://doi.org/10.1023/A:1007869713348

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  • DOI: https://doi.org/10.1023/A:1007869713348

  • estradiol
  • salmonid
  • pleuronectid
  • sparid
  • teleost reproduction
  • binding protein