Diversity and biological significance of sex hormone-binding globulin in fish, an evolutionary perspective

Molecular and Cellular Endocrinology

Volumn 316, Issue 1, 2010, Pages 66-78

  Bobe, Julien ^a   Guiguen, Yann ^a   Fostier, Alexis ^a  

^a Campus de Beaulieu   (France)

Author keywords

Estradiol; Shbga; Shbgb; Steroids; Teleosts; Trout

Indexed keywords

ADRENOSTERONE; ESTRADIOL; HOMODIMER; MESSENGER RNA; MONOMER; RECOMBINANT PROTEIN; SEX HORMONE BINDING GLOBULIN; SEX HORMONE BINDING GLOBULIN ALPHA; SEX HORMONE BINDING GLOBULIN BETA; STEROID; TESTOSTERONE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

AMINO ACID SEQUENCE; BINDING AFFINITY; BLOOD; FISH; GENE EXPRESSION; GENE LOCATION; GENE STRUCTURE; GENETIC VARIABILITY; HORMONAL REGULATION; LIVER; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE MATURATION; OVARY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TRANSPORT; REPRODUCTION; REVIEW; SALMONID; SPECIES DIFFERENCE; STEROID RELEASE; TELEOST; TESTIS;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION; FISHES; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN BINDING; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT; SEX HORMONE-BINDING GLOBULIN; TISSUE DISTRIBUTION;

EID: 72549113005     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.09.017     Document Type: Review

References (91)

1. Allendorf F.W., and Thorgaard G.H. Tetraploidy and the evolution of salmonid fishes. In: Turner B.J. (Ed). The Evolutionary Genetics of Fishes (1984), Plenum Press, New York 1-53
2. Avvakumov G.V., Grishkovskaya I., Muller Y.A., and Hammond G.L. Resolution of the human sex hormone-binding globulin dimer interface and evidence for two steroid-binding sites per homodimer. J. Biol. Chem. 276 (2001) 34453-34457
3. Baker M.E. Albumin's role in steroid hormone action and the origins of vertebrates: is albumin an essential protein?. FEBS Lett. 439 (1998) 9-12
4. Baroiller J.F., Fostier A., Zohar Y., and Marcuzzi O. The metabolic clearance rate of estradiol-17 beta in rainbow trout, Salmo gairdneri R., estimated by both single injection and constant infusion methods: increase during oocyte maturation. Gen. Comp. Endocrinol. 66 (1987) 85-94
5. Bennetau-Pelissero C., Kaushik S., Sumpter J.P., Fostier A., Le Gac F., Valotaire Y., Davail-Cuisset B., and Le Menn F. Effets du soja et des phyto-oestrogènes sur la vitellogénèse et l'endocrinologie de la truite arc-en-ciel et de l'esturgeon sibérien. Approches in vivo et in vitro. Bull. Français Pêche Pisciculture 350-351 (1998) 571-583
6. Bobe, J., Jalabert, B., Fostier, A., 2008a. Oogenesis: post-vitellogenic events leading to a fertilizable oocyte. In: Rocha, M.J., Arukwe, A., Kapoor, B.G. (Eds.), Fish Reproduction. Science Publishers, Enfield, pp. 1-36.
7. Bobe J., Mahe S., Nguyen T., Rime H., Vizziano D., Fostier A., and Guiguen Y. A novel, functional, and highly divergent Sex Hormone-Binding Globulin that may participate in the local control of ovarian functions in salmonids. Endocrinology 149 (2008) 2980-2989
8. Bobe J., Maugars G., Nguyen T., and Jalabert B. Specific gene expression profiles are associated with follicular maturational competence acquisition in rainbow trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 28 (2003) 309-311
9. Bocchinfuso W.P., Ma K.L., Lee W.M., Warmels-Rodenhiser S., and Hammond G.L. Selective removal of glycosylation sites from sex hormone-binding globulin by site-directed mutagenesis. Endocrinology 131 (1992) 2331-2336
10. Boffa G.A., Martin B., Winchenne J.J., and Ozon R. Interactions stéroïdes-protéines dans le sérum de l'homme, d'un amphibien et d'un cyclostome. Biochimie 54 (1972) 1137-1145
11. Borg B. Androgens in teleost fishes. Comp. Biochem. Physiol. C 109 (1994) 219-245
12. Bryan M.B., Scott A.P., and Li W. The sea lamprey (Petromyzon marinus) has a receptor for androstenedione. Biol. Reprod. 77 (2007) 688-696
13. Bryan M.B., Scott A.P., and Li W. Sex steroids and their receptors in lampreys. Steroids 73 (2008) 1-12
14. Callard G.V., and Mak P. Exclusive nuclear location of estrogen receptors in Squalus testis. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 1336-1340
15. Chang C.F., and Chen M.R. Fluctuation in sex steroids and sex steroid-binding protein during the development and annual cycle of the male common carp, Cyprinus carpio. Comp. Biochem. Physiol. 97A (1990) 565-568
16. Chang C.F., and Lee Y.H. Purification of the sex steroid-binding protein from common carp (Cyprinus carpio) plasma. Comp. Biochem. Physiol. B 101 (1992) 587-590
17. Chang C.F., Lee Y.H., Yoshida T., and Sun L.T. Characterization of the plasma sex steroid-binding protein in eel (Anguilla japonica). Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 108B (1994) 189-197
18. Cousin P., Dechaud H., Grenot C., Lejeune H., Hammond G.L., and Pugeat M. Influence of glycosylation on the clearance of recombinant human sex hormone-binding globulin from rabbit blood. J. Steroid Biochem. Mol. Biol. 70 (1999) 115-121
19. Cuevas M.E., and Callard G. Androgen and progesterone receptors in shark (squalus) testis: characteristics and stage-related distribution. Endocrinology 130 (1992) 514-520
20. Danzo B.J., Black J.H., and Bell B.W. The microheterogeneity of rabbit testosterone-binding globulin is due to differential glycosylation of its single protomer. Biol. Reprod. 41 (1989) 957-965
21. Delsuc F., Brinkmann H., and Philippe H. Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 6 (2005) 361-375
22. Fast M.D., Hosoya S., Johnson S.C., and Afonso L.O. Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish. Immunol. 24 (2008) 194-204
23. Fitzpatrick M.S., Gale W.L., and Schreck C.B. Binding characteristics of an androgen receptor in the ovaries of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 95 (1994) 399-408
24. Fostier A., and Baek H. Inhibition of production of maturation inducing steroid in rainbow trout granulosa cells: effect of oestradiol on gonadotropin stimulated 20-beta-hydroxysteroid dehydrogenase activity. Reprod. Nutr. Dev. 33 (1993) 81-82
25. Fostier A., and Breton B. Binding of steroids by plasma of a teleost: the rainbow trout, Salmo gairdneri. J. Steroid Biochem. 6 (1975) 345-351
26. Fostier A., Weil C., Terqui M., Breton B., and Jalabert B. Plasma estradiol 17 beta and gonadotropin during ovulation in rainbow trout Salmo Gairdneri. Ann. Biol. Anim. Biochim. Biophys. 18 (1978) 929-936
27. Foucher J.L., Le Bail P.Y., and Le Gac F. Influence of hypophysectomy, castration, fasting, and spermiation on SBP concentration in male rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 85 (1992) 101-110
28. Foucher J.L., and Le Gac F. Evidence for an androgen binding protein in the testis of a teleost fish (Salmo gairdneri R.): a potential marker of Sertoli cell function. J. Steroid Biochem. 32 (1989) 545-552
29. Foucher J.L., Niu P.D., Mourot B., Vaillant C., and Le Gac F. In vivo and in vitro studies 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. Mol. Biol. 39 (1991) 975-986
30. Freeman H.C., and Idler D.R. Sex hormone binding proteins. II. Isolation from serum of an elasmobranch (Raja radiata). Gen. Comp. Endocrinol. 13 (1969) 83-91
31. Freeman H.C., and Idler D.R. Binding affinities of blood protens for sex hormones and corticosteroids in fish. Steroids 17 (1971) 233-250
32. Gale W.L., Patino R., and Maule A.G. Interaction of xenobiotics with estrogen receptors alpha and beta and a putative plasma sex hormone-binding globulin from channel catfish (Ictalurus punctatus). Gen. Comp. Endocrinol. 136 (2004) 338-345
33. Goetz F.W., Fostier A.Y., Breton B., and Jalabert B. Hormonal changes during meiotic maturation and ovulation in the brook trout (Salvelinus fontinalis). Fish Physiol. Biochem. 3 (1987) 203-211
34. Gouret P., Vitiello V., Balandraud N., Gilles A., Pontarotti P., and Danchin E.G. FIGENIX: intelligent automation of genomic annotation: expertise integration in a new software platform. BMC Bioinformatics 6 (2005) 198
35. Hammond G.L., and Bocchinfuso W.P. Sex hormone-binding globulin: gene organization and structure/function analyses. Horm. Res. 45 (1996) 197-201
36. Hammond G.L., Underhill D.A., Rykse H.M., and Smith C.L. The human sex hormone-binding globulin gene contains exons for androgen-binding protein and two other testicular messenger RNAs. Mol. Endocrinol. 3 (1989) 1869-1876
37. Ho S.M., Tsang P., and Callard I.P. Some properties of a steroid-binding protein in the plasma of an ovoviviparous dogfish, Squalus acanthias, at different stages of the life cycle. Biol. Reprod. 23 (1980) 281-289
38. Hobby A.C., Geraghty D.P., and Pankhurst N.W. 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 (2000) 249-259
39. Hryb D.J., Nakhla A.M., Kahn S.M., St George J., Levy N.C., Romas N.A., and Rosner W. Sex hormone-binding globulin in the human prostate is locally synthesized and may act as an autocrine/paracrine effector. J. Biol. Chem. 277 (2002) 26618-26622
40. Idler D.R., and Freeman H.C. Sex hormone binding proteins I. Binding of steroids by serum of an elasmobranch (Raja radiata). Gen. Comp. Endocrinol. 13 (1969) 75-82
41. Jalabert B., and Fostier A. The follicular sensitivity in vitro to maturation-inducing hormones in rainbow trout, Salmo gairdneri: role of oestradiol-17β. Aqua 43 (1984) 1-11
42. Jalabert B., and Fostier A. The modulatory effect in vitro of oestradiol-17β, testosterone or cortisol on the output of 17α-hydroxy-20β-dihydroprogesterone by rainbow trout (Salmo gairdneri) ovarian follicles stimulated by the maturational gonadotropin s-GtH. Reprod. Nutr. Develop. 24 (1984) 127-136
43. Jones R.E., and Baxter D.C. Gestation, with emphasis on corpus luteum biology, placentation, and parturition. In: Pang P.K.T., and Schreibman M.P. (Eds). Vertebrate Endocrinology: Fundamentals and Biomedical Implications (1991), Academic Press 205-302
44. Joseph D.R. Structure, function, and regulation of androgen-binding protein/sex hormone-binding globulin. Vitam. Horm. 49 (1994) 197-280
45. Joseph D.R., Hall S.H., and French F.S. Rat androgen-binding protein: evidence for identical subunits and amino acid sequence homology with human sex hormone-binding globulin. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 339-343
46. Joseph D.R., Sullivan P.M., Wang Y.M., Millhorn D.E., and Bayliss D.M. Complex structure and regulation of the ABP/SHBG gene. J. Steroid Biochem. Mol. Biol. 40 (1991) 771-775
47. Kahn S.M., Hryb D.J., Nakhla A.M., Romas N.A., and Rosner W. Sex hormone-binding globulin is synthesized in target cells. J. Endocrinol. 175 (2002) 113-120
48. Khan M.S., Hryb D.J., Hashim G.A., Romas N.A., and Rosner W. Delineation and synthesis of the membrane receptor-binding domain of sex hormone-binding globulin. J. Biol. Chem. 265 (1990) 18362-18365
49. Kloas W., Schrag B., Ehnes C., and Segner H. Binding of xenobiotics to hepatic estrogen receptor and plasma sex steroid binding protein in the teleost fish, the common carp (Cyprinus carpio). Gen. Comp. Endocrinol. 119 (2000) 287-299
50. Laidley C.W., and Thomas P. Partial characterization of a sex-steroid binding protein in the spotted seatrout (Cynoscion nebulosus). Biol. Reprod. 51 (1994) 982-992
51. Laidley C.W., and Thomas P. Changes in plasma sex steroid-binding protein levels associated with ovarian recrudescence in the spotted seatrout (Cynoscion nebulosus). Biol. Reprod. 56 (1997) 931-937
52. Larhammar D., and Risinger C. Molecular genetic aspects of tetraploidy in the common carp Cyprinus carpio. Mol. Phylogenet. Evol. 3 (1994) 59-68
53. Lazier C.B., Lonergan K., and Mommsen T.P. Hepatic estrogen receptors and plasma estrogen-binding activity in the Atlantic salmon. Gen. Comp. Endocrinol. 57 (1985) 234-245
54. Mak P., and Callard G.V. A novel steroid-binding protein in the testis of the dogfish Squalus acanthias. Gen. Comp. Endocrinol. 68 (1987) 104-112
55. Martin B. Steroid-protein interactions in nonmammalian vertebrates. I. Elasmobranch steroids-binding protein (E. SBP) in dogfish serum (Scyliorhinus canicula). Gen. Comp. Endocrinol. 25 (1975) 42-51
56. McPherson R., Hannum J., and Greco T. An investigation of an estrogen-binding component in the liver and plasma of brook char, Salvelinus fontinalis. Comp. Biochem. Physiol. A: Comp. Physiol. 89 (1988) 615-619
57. Miguel-Queralt S., Avvakumov G.V., Blazquez M., Piferrer F., and Hammond G.L. Sea bass (Dicentrarchus labrax) sex hormone binding globulin: molecular and biochemical properties and phylogenetic comparison of its orthologues in multiple fish species. Mol. Cell Endocrinol. 229 (2005) 21-29
58. Miguel-Queralt S., Blazquez M., Piferrer F., and Hammond G.L. Sex hormone-binding globulin expression in sea bass (Dicentrarchus labrax L.) throughout development and the reproductive season. Mol. Cell Endocrinol. 276 (2007) 55-62
59. Miguel-Queralt S., and Hammond G.L. Sex hormone-binding globulin in fish gills is a portal for sex steroids breached by xenobiotics. Endocrinology 149 (2008) 4269-4275
60. Miguel-Queralt S., Knowlton M., Avvakumov G.V., Al Nouno R., Kelly G.M., and Hammond G.L. Molecular and functional characterization of sex hormone binding globulin in zebrafish. Endocrinology 145 (2004) 5221-5230
61. Miguel-Queralt S., Underhill C., Devlin R.H., and Hammond G.L. Characterization and measurement of the plasma alpha- and beta-sex hormone-binding globulin paralogs in salmon. Endocrinology 150 (2009) 366-375
62. Milligan S.R., Khan O., and Nash M. 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 (1998) 89-95
63. Mommsen T., Vijayan M.M., and Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fisheries 9 (1999) 211-268
64. Nakhla A.M., Hryb D.J., Rosner W., Romas N.A., Xiang Z., and Kahn S.M. Human sex hormone-binding globulin gene expression-multiple promoters and complex alternative splicing. BMC Mol. Biol. 10 (2009) 37
65. Ng K.M., So M.T., and Lee W.M. Expression of rabbit sex hormone-binding globulin during pregnancy and prenatal development and identification of a novel isoform. Endocrinology 146 (2005) 1965-1972
66. Ovrevik J., Stenersen J., Nilssen K., and Tollefsen K.E. Partial characterization of a sex steroid-binding protein in plasma from Arctic charr (Salvelinus alpinus L.). Gen. Comp. Endocrinol. 122 (2001) 31-39
67. Pasmanik M., and Callard G. Characteristics of a testosterone-estradiol binding globulin (TEBG) in goldfish serum. Biol. Reprod. 35 (1986) 838-845
68. Petra P.H., Adman E.T., Orr W.R., Woodcock K.T., Groff C., and Sui L.M. Arginine-140 and isoleucine-141 determine the 17beta-estradiol-binding specificity of the sex-steroid-binding protein (SBP, or SHBG) of human plasma. Protein Sci. 10 (2001) 1811-1821
69. Piferrer F., and Blazquez M. Aromatase distribution and regulation in fish. Fish Physiol. Biochem. 31 (2005) 215-226
70. Pottinger T.G. Estrogen-binding sites in the liver of sexually mature male and female brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 61 (1986) 120-126
71. Pottinger T.G. Seasonal variation in specific plasma- and target-tissue binding of androgens, relative to plasma steroid levels, in the brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 70 (1988) 334-344
72. Pottinger T.G., and Pickering A.D. The effect of cortisol administration on hepatic and plasma estradiol-binding capacity in immature female rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 80 (1990) 264-273
73. Pryce-Hobby A.C., McMaster M.E., Hewitt L.M., and Van Der K.G. The effects of pulp mill effluent on the sex steroid binding protein in white sucker (Catostomus commersoni) and longnose sucker (C catostomus). Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 134 (2003) 241-250
74. Querat B., Hardy A., and Leloup-Hatey J. Etude de la liaison plasmatique des stéroïdes sexuels et du cortisol chez l'anguille femelle (Anguilla anguilla L.). Comptes Rendus l'Académie Sci. Sér. III 297 (1983) 119-122
75. Rosner W. Sex steroids and the free hormone hypothesis. Cell 124 (2006) 455-456
76. Rosner W., Christy N.P., and Kelly W.G. Partial purification and preliminary characterization of estrogen-binding globulins from human plasma. Biochemistry (Mosc) 8 (1969) 3100-3108
77. Scott A.P., Pinillos M.L., and Huertas M. The rate of uptake of sex steroids from water by Tinca tinca is influenced by their affinity for sex steroid binding protein in plasma. J. Fish Biol. 67 (2005) 182-200
78. Selva D.M., and Hammond G.L. Human sex hormone-binding globulin is expressed in testicular germ cells and not in sertoli cells. Horm. Metab. Res. 38 (2006) 230-235
79. Stacey N.E., Chojnacki A., Narayanan A., Cole T.B., and Murphy C.A. Hormonally derived sex pheromones in fish: exogenous cues and signals from gonad to brain. Can. J. Physiol. Pharmacol. 81 (2003) 329-341
80. Steinke D., Salzburger W., Braasch I., and Meyer A. Many genes in fish have species-specific asymmetric rates of molecular evolution. BMC Genomics 7 (2006) 20
81. Sullivan P.M., Petrusz P., Szpirer C., and Joseph D.R. Alternative processing of androgen-binding protein RNA transcripts in fetal rat liver. Identification of a transcript formed by trans splicing. J. Biol. Chem. 266 (1991) 143-154
82. Suresh D.V., Baile V.V., and Prasada Rao P.D. Annual reproductive phase-related profile of sex steroids and their carrier, SHBG, in the Indian major carp, Labeo rohita. Gen. Comp. Endocrinol. 159 (2008) 143-149
83. Thomas P., Dressing G., Pang Y., Berg H., Tubbs C., Benninghoff A., and Doughty K. Progestin, estrogen and androgen G-protein coupled receptors in fish gonads. Steroids 71 (2006) 310-316
84. Thorsteinson N., Ban F., Santos-Filho O., Tabaei S.M., Miguel-Queralt S., Underhill C., Cherkasov A., and Hammond G.L. In silico identification of anthropogenic chemicals as ligands of zebrafish sex hormone binding globulin. Toxicol. Appl. Pharmacol. 234 (2009) 47-57
85. Tollefsen K.E. Interaction of estrogen mimics, singly and in combination, with plasma sex steroid-binding proteins in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 56 (2002) 215-225
86. Tollefsen K.E., Meys J.F., Frydenlund J., and Stenersen J. Environmental estrogens interact with and modulate the properties of plasma sex steroid-binding proteins in juvenile Atlantic salmon (Salmo salar). Mar. Environ. Res. 54 (2002) 697-701
87. Tollefsen K.E., Ovrevik J., and Stenersen J. Binding of xenoestrogens to the sex steroid-binding protein in plasma from Arctic charr (Salvelinus alpinus L.). Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 139 (2004) 127-133
88. Van der Kraak G., and Biddiscombe S. Polyunsaturated fatty acids modulate the properties of the sex steroid binding protein in goldfish. Fish Physiol. Biochem. 20 (1999) 115-123
89. Vermeirssen E.L., and Scott A.P. Excretion of free and conjugated steroids in rainbow trout (Oncorhynchus mykiss): evidence for branchial excretion of the maturation-inducing steroid, 17,20beta-dihydroxy-4-pregnen-3-one. Gen. Comp. Endocrinol. 101 (1996) 180-194
90. Yoshikuni M., Matsushita H., Shibata N., and Nagahama Y. Purification and characterization of 17 alpha,20 beta-dihydroxy-4-pregnen-3-one binding protein from plasma of rainbow trout, Oncorhynchus mykiss. Gen. Comp .Endocrinol. 96 (1994) 189-196
91. Young G., Kagawa H., and Nagahama Y. Evidence for a decrease in aromatase activity in the ovarian granulosa cells of amago salmon (Oncorhynchus rhodurus) associated with final oocyte maturation. Biol. Reprod. 29 (1983) 310-315