5α-Dihydrotestosterone is a potent androgen in the fathead minnow (Pimephales promelas)

General and Comparative Endocrinology

Volumn 171, Issue 3, 2011, Pages 309-318

  Margiotta Casaluci, Luigi ^a   Sumpter, John P ^a  

^a BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

11 Ketotestosterone; Androgens; Dihydrotestosterone; Fathead minnow; Gonad maturation; Intersex

Indexed keywords

11 OXOTESTOSTERONE; 5ALPHA PREGNANE 3,20 DIONE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; BODY WEIGHT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; FIN (ORGAN); GONAD DEVELOPMENT; GROWTH STIMULATION; HORMONE ACTION; HORMONE BLOOD LEVEL; IN VIVO STUDY; LYMPHOCYTE COUNT; MALE; NONHUMAN; OOCYTE; OVARY FUNCTION; PHYSIOLOGICAL PROCESS; PIMEPHALES PROMELAS; PRIORITY JOURNAL; SEX DIFFERENCE; SEX DIFFERENTIATION DISORDER; SPERMATOGENESIS; WATER CONTENT;

EID: 79953740245     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.02.012     Document Type: Article

References (92)

1. Adachi K., Wakamatsu K., Ito S., Matsubara H., Nomura K., Tanaka H., Kato K. A close relationship between androgen levels and eumelanogenesis in the teleost red seabream (Pagrus major): quantitative analysis of its seasonal variation and effects of oral treatment with methyl-testosterone. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2010, 156:184-189.
2. Ankley G.T., Jensen K.M., Makynen E.A., Kahl M.D., Korte J.J., Hornung M.W., Henry T.R., Denny J.S., Leino R.L., Wilson V.S., Cardon M.C., Hartig P.C., Gray L.E. Effects of the androgenic growth promoter 17-beta-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ. Toxicol. Chem. 2003, 22:1350-1360.
3. Ankley G.T., Villeneuve D.L. The fathead minnow in aquatic toxicology: past, present and future. Aquat. Toxicol. 2006, 78:91-102.
4. Asahina K., Suzuki K., Aida K., Hibiya T., Tamaoki B. Relationship between the structures and steroidogenic functions of the testes of the urohaze goby (Glossogobius olivaceus). Gen. Comp. Endocrinol. 1985, 57:281-292.
5. Bhandari R.K., Nakamura M., Kobayashi T., Nagahama Y. Suppression of steroidogenic enzyme expression during androgen-induced sex reversal in Nile tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 2006, 145:20-24.
6. Borg B. Androgens in teleost fishes. Comp. Biochem. Physiol. C, Pharmacol. Toxicol. Endocrinol. 1994, 109:219-245.
7. Borg B., Antonopoulou E., Andersson E., Carlberg T., Mayer I. Effectiveness of several androgens in stimulating kidney hypertrophy, a secondary sexual character, in castrated male 3-spined sticklebacks, Gasterosteus aculeatus. Can. J. Zool. 1993, 71:2327-2329.
8. Borg B., Mayer I., Lambert J., Granneman J., Schulz R. Metabolism of androstenedione and 11-ketotestosterone in the kidney of the 3-spined stickleback, Gasterosteus aculeatus. Gen. Comp. Endocrinol. 1992, 86:248-256.
9. Brantley R.K., Marchaterre M.A., Bass A.H. Androgen effects on vocal muscle structure in a teleost fish with inter-sexual and intra-sexual dimorphism. J. Morphol. 1993, 216:305-318.
10. Brantley R.K., Wingfield J.C., Bass A.H. Sex steroid-levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Horm. Behav. 1993, 27:332-347.
11. Brinkmann A.O., Blok L.J., de Ruiter P.E., Doesburg P., Steketee K., Berrevoets C.A., Trapman J. Mechanisms of androgen receptor activation and function. J. Steroid Biochem. Mol. Biol. 1999, 69:307-313.
12. Cavaco J.E.B., Bogerd J., Goos H., Schulz R.W. Testosterone inhibits 11-ketotestosterone-induced spermatogenesis in African catfish (Clarias gariepinus). Biol. Reprod. 2001, 65:1807-1812.
13. Cavaco J.E.B., Vilrokx C., Trudeau V.L., Schulz R.W., Goos H.J.T. Sex steroids and the initiation of puberty in male African catfish (Clarias gariepinus). Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 275:R1793-R1802.
14. Davis L.K., Fox B.K., Lim C., Lerner D.T., Hirano T., Grau E.G. Effects of 11-ketotestosterone and fishmeal in the feed on growth of juvenile tilapia (Oreochromis mossambicus). Aquaculture 2010, 305:143-149.
15. de Waal P.P., Wang D.S., Nijenhuis W.A., Schulz R.W., Bogerd J. Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction 2008, 136:225-234.
16. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
17. Diaz L.C., Das Gupta T.K., Beattie C.W. Effects of gonadal steroids on melanocytes in developing hamsters. Pediatr. Dermatol. 1986, 3:247-256.
18. Dijkstra P.D., Hekman R., Schulz R.W., Groothuis T.G.G. Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish. Behav. Ecol. Sociobiol. 2007, 61:599-609.
19. Fenske M., Segner H. Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat. Toxicol. 2004, 67:105-126.
20. Fitzpatrick M.S., Gale W.L., Schreck C.B. Binding characteristics of an androgen receptor in the ovaries of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 1994, 95:399-408.
21. George F.W., Wilson J.D. Sex determination and differentiation. The Physiology of Reproduction 1994, 3-28. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
22. Govoroun M., McMeel O.M., D'Cotta H., Ricordel M.J., Smith T., Fostier A., Guiguen Y. Steroid enzyme gene expressions during natural and androgen-induced gonadal differentiation in the rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 2001, 290:558-566.
23. Griggs R.C., Kingston W., Jozefowicz R.F., Herr B.E., Forbes G., Halliday D. Effect of testosterone on muscle mass and muscle protein synthesis. J. Appl. Physiol. 1989, 66:498-503.
24. Guan G.J., Kobayashi T., Nagahama Y. Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the Tilapia (Oreochromis niloticus). Biochem. Biophys. Res. Commun. 2000, 272:662-666.
25. Herrera S.M., Demesa V.T., Zamora N.S., Pena E.M. Anabolic effect induced by trenbolone acetate steroid on the Carassius auratus (Pisces:Cyprinidae) growth. Hidrobiologica 2008, 18:41-50.
26. Hofbauer L.C., Khosla S. Androgen effects on bone metabolism: recent progress and controversies. Eur. J. Endocrinol. 1999, 140:271-286.
27. Hossain M.S., Larsson A., Scherbak N., Olsson P.E., Orban L. Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol. Reprod. 2008, 78:361-369.
28. Ikeuchi T., Todo T., Kobayashi T., Nagahama Y. CDNA cloning of a novel androgen receptor subtype. J. Biol. Chem. 1999, 274:25205-25209.
29. Ikeuchi T., Todo T., Kobayashi T., Nagahama Y. Two subtypes of androgen and progestogen receptors in fish testes. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 2001, 129:449-455.
30. Jensen K.M., Korte J.J., Kahl M.D., Pasha M.S., Ankley G.T. Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 2001, 128:127-141.
31. Jobling S., Nolan M., Tyler C.R., Brighty G., Sumpter J.P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32:2498-2506.
32. Jorgensen A., Andersen O., Bjerregaard P., Rasmussen L.J. Identification and characterisation of an androgen receptor from zebrafish Danio rerio. Comp. Biochem. Physiol. C, Comp. Pharmacol. Toxicol. 2007, 146:561-568.
33. Joss J.M.P., Edwards A., Kime D.E. In vitro biosynthesis of androgens in the Australian lungfish, Neoceratodus forsteri. Gen. Comp. Endocrinol. 1996, 101:256-263.
34. Kadi F. Adaptation of human skeletal muscle to training and anabolic steroids. Acta Physiol. Scand. 2000, 168:2-52.
35. Katsu Y., Hinago M., Sone K., Urushitani H., Guillette L.J., Iguchi T. In vitro assessment of transcriptional activation of the estrogen and androgen receptors of mosquitofish, Gambusia affinis affinis. Mol. Cell. Endocrinol. 2007, 276:10-17.
36. Kearns A.E., Khosla S. Potential anabolic effects of androgens on bone Mayo. Clin. Proc. 2004, 79:S14-S18.
37. Kime D.E. Classical and non classical reproductive steroids in fish. Rev. Fish Biol. Fish. 1993, 3:160-180.
38. Kobayashi M., Nakanishi T. 11-Ketotestosterone induces male-type sexual behavior and gonadotropin secretion in gynogenetic crucian carp, Carassius auratus langsdorfii. Gen. Comp. Endocrinol. 1999, 115:178-187.
39. Kobayashi M., Tajima C., Sugimoto M. Effects of androgens on the development of nuptial coloration and chromatophores in the bitterling Rhodeus ocellatus ocellatus. Zool. Sci. 2009, 26:125-130.
40. Kobayashi T., Matsuda M., Kajiura-Kobayashi H., Suzuki A., Saito N., Nakamoto M., Shibata N., Nagahama Y. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dynam. 2004, 231:518-526.
41. Kortner T.M., Rocha E., Silva P., Castro L.F.C., Arukwe A. Genomic approach in evaluating the role of androgens on the growth of Atlantic cod (Gadus morhua) previtellogenic oocytes. Comp. Biochem. Physiol. Part D: Genomics Proteomics 2008, 3:205-218.
42. Korzan W.J., Robison R.R., Zhao S., Fernald R.D. Color change as a potential behavioral strategy. Horm. Behav. 2008, 54:463-470.
43. Latz M., Reinboth R. Androgen metabolism in the skin of the rainbow-trout (Oncorhynchus mykiss). Fish Physiol. Biochem. 1993, 11:281-286.
44. Lee S.T.L., Kime D.E., Chao T.M., Lim H.S., Chou R., Lam T.J., Tan C.H. In vitro metabolism of testosterone by gonads of the grouper (Epinephelus tauvina) before and after sex inversion with 17 alpha-methyltestosterone. Gen. Comp. Endocrinol. 1995, 99:41-49.
45. Li J., Al-Azzawi F. Mechanism of androgen receptor action. Maturitas 2009, 63:142-148.
46. Lindzey J., Kumar M.V., Grossman M., Young C., Tindall D.J. Molecular mechanisms of androgen action. Vitamins and Hormones 1994, vol. 49:383-432. Academic Press Inc., San Diego.
47. Lokman P.M., Harris B., Kusakabe M., Kime D.E., Schulz R.W., Adachi S., Young G. 11-Oxygenated androgens in female teleosts: prevalence, abundance, and life history implications. Gen. Comp. Endocrinol. 2002, 129:1-12.
48. Marchand O., Govoroun M., D'Cotta H., McMeel O., Lareyre J.J., Bernot A., Laudet V., Guiguen Y. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim. Biophys. Acta 2000, 1493:180-187.
49. Matsubara M., Lokman P.M., Senaha A., Kazeto Y., Ijiri S., Kambegawa A., Hirai T., Young G., Todo T., Adachi S., Yamauchi K. Synthesis and possible function of 11-ketotestosterone during oogenesis in eel (Anguilla spp.). Fish Physiol. Biochem. 2003, 28:353-354.
50. McDonald J.H. Handbook of Biological Statistics 2009, Sparky House Publishing, Baltimore. second ed.
51. Miguel-Queralt S., Avvakumov G.V., Blazquez M., Piferrer F., 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. 2005, 229:21-29.
52. Miguel-Queralt S., Knowlton M., Avvakumov G.V., Al-Nuono R., Kelly G.M., Hammond G.L. Molecular and functional characterization of sex hormone binding globulin in zebrafish. Endocrinology 2004, 145:5221-5230.
53. Miura T., Yamauchi K., Takahashi H., Nagahama Y. Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proc. Natl. Acad. Sci. USA 1991, 88:5774-5778.
54. Morthorst J.E., Holbech H., Bjerregaard P. Trenbolone causes irreversible masculinization of zebrafish at environmentally relevant concentrations. Aquat. Toxicol. 2010, 98:336-343.
55. Nitta H., Osawa Y., Bahr J.M. Multiple steroidogenic cell-populations in the thecal layer of preovulatory follicles of the chicken ovary. Endocrinology 1991, 129:2033-2040.
56. Olsson P.E., Berg A.H., von Hofsten J., Grahn B., Hellqvist A., Larsson A., Karlsson J., Modig C., Borg B., Thomas P. Molecular cloning and characterization of a nuclear androgen receptor activated by 11-ketotestosterone. Reprod. Biol. Endocrinol. 2005, 3:17.
57. Panter G.H., Hutchinson T.H., Hurd K.S., Sherren A., Stanley R.D., Tyler C.R. Successful detection of (anti-) androgenic and aromatase inhibitors in pre-spawning adult fathead minnows (Pimephales promelas) using easily measured endpoints of sexual development. Aquat. Toxicol. 2004, 70:11-21.
58. Parks L.G., LeBlanc G.A. Involvement of multiple biotransformation processes in the metabolic elimination of testosterone by juvenile and adult fathead minnows (Pimephales promelas). Gen. Comp. Endocrinol. 1998, 112:69-79.
59. Parrott J.L., Wood C.S., Boutot P., Dunn S. Changes in growth, secondary sex characteristics, and reproduction of fathead minnows exposed for a life cycle to bleached sulfite mill effluent. J. Toxicol. Environ. Health Part A 2004, 67:1755-1764.
60. Pasmanik M., Callard G.V. Aromatase and 5-alpha-reductase in the teleost brain, spinal-cord, and pituitary-gland. Gen. Comp. Endocrinol. 1985, 60:244-251.
61. Pasmanik M., Callard G.V. Changes in brain aromatase and 5-alpha-reductase activities correlate significantly with seasonal reproductive cycles in goldfish (Carassius auratus). Endocrinology 1988, 122:1349-1356.
62. Paulos P., Runnalls T.J., Nallani G., La Point T., Scott A.P., Sumpter J.P., Huggett D.B. Reproductive responses in fathead minnow and Japanese medaka following exposure to a synthetic progestin, Norethindrone. Aquat. Toxicol. 2010, 99:256-262.
63. Piferrer F., Baker I.J., Donaldson E.M. Effects of natural, synthetic, aromatizable, and nonaromatizable androgens in inducing male sex-differentiation in genotypic female chinook salmon (Oncorhynchus tshawytscha). Gen. Comp. Endocrinol. 1993, 91:59-65.
64. Pottinger T.G., Pickering A.D. The effects of 11-ketotestosterone and testosterone on the skin structure of brown trout, Salmo trutta L. Gen. Comp. Endocrinol. 1985, 59:335-342.
65. Scott A.P., Mackenzie D.S., Stacey N.E. Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. 2. Steroid-hormones. Gen. Comp. Endocrinol. 1984, 56:349-359.
66. Sharpe R.L., MacLatchy D.L., Courtenay S.C., Van Der Kraak G.J. Effects of a model androgen (methyl testosterone) and a model anti-androgen (cyproterone acetate) on reproductive endocrine endpoints in a short-term adult mummichog (Fundulus heteroclitus) bioassay. Aquat. Toxicol. 2004, 67:203-215.
67. Slominski A., Tobin D.J., Shibahara S., Wortsman J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 2004, 84:1155-1228.
68. Smith R.J.F. Seasonal changes in the histology of the gonads and dorsal skin of the fathead minnow, Pimephales promelas. Can. J. Zool. 1978, 56:2103-2109.
69. Sone K., Hinago M., Itamoto M., Katsu Y., Watanabe H., Urushitani H., Tooi O., Guillette L.J., Iguchi T. Effects of an androgenic growth promoter 17 beta-trenbolone on masculinization of mosquitofish (Gambusia affinis affinis). Gen. Comp. Endocrinol. 2005, 143:151-160.
70. Sperry T.S., Thomas P. Androgen binding profiles of two distinct nuclear androgen receptors in Atlantic croaker (Micropogonias undulatus). J. Steroid Biochem. Mol. Biol. 2000, 73:93-103.
71. Sperry T.S., Thomas P. Characterization of two nuclear androgen receptors in Atlantic croaker: comparison of their biochemical properties and binding specificities. Endocrinology 1999, 140:1602-1611.
72. Sperry T.S., Thomas P. Identification of two nuclear androgen receptors in kelp bass (Paralabrax clathratus) and their binding affinities for xenobiotics: Comparison with Atlantic croaker (Micropogonias undulatus) androgen receptors. Biol. Reprod. 1999, 61:1152-1161.
73. Staub N.L., DeBeer M. The role of androgens in female vertebrates. Gen. Comp. Endocrinol. 1997, 108:1-24.
74. Swart N., Pool E. Rapid detection of selected steroid hormones from sewage effluents using an ELISA in the kuils river water catchment area, South Africa. J. Immunoassay Immunochem. 2007, 28:395-408.
75. Tadokoro T., Itami S., Hosokawa K., Terashi H., Takayasu S. Human genital melanocytes as androgen target cells. J. Invest. Dermatol. 1997, 109:513-517.
76. Takeo J., Yamashita S. Rainbow trout androgen receptor-alpha fails to distinguish between any of the natural androgens tested in transactivation assay, not just 11-ketotestosterone and testosterone. Gen. Comp. Endocrinol. 2000, 117:200-206.
77. Tetsuka M., Hillier S.G. Androgen receptor gene expression in rat granulosa cells: the role of follicle-stimulating hormone and steroid hormones. Endocrinology 1996, 137:4392-4397.
78. Todo T., Ikeuchi T., Kobayashi T., Nagahama Y. Fish androgen receptor: cDNA cloning, steroid activation of transcription in transfected mammalian cells, and tissue mRNA levels. Biochem. Biophys. Res. Commun. 1999, 254:378-383.
79. Tong S.K., Chung B.C. Analysis of zebrafish cyp19 promoters. J. Steroid Biochem. Mol. Biol. 2003, 86:381-386.
80. Touhata K., Kinoshita M., Tokuda Y., Toyohara H., Sakaguchi M., Yokoyama Y., Yamashita S. Sequence and expression of a cDNA encoding the red seabream androgen receptor. Biochim. Biophys. Acta 1999, 1450:481-485.
81. Truscott B. Steroid metabolism in fish. 2. Testosterone metabolites in the bile of the marine winter flounder Pseudopleuronectes americanus and the fresh-water Atlantic salmon Salmo salar. Gen. Comp. Endocrinol. 1983, 51:460-470.
82. US EPA, Histopathology Guidelines for the Fathead Minnow (Pimephales promelas) 21-day Reproduction Assay, 2006.
83. van Aerle R., Pounds N., Hutchinson T.H., Maddix S., Tyler C.R. Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow, Pimephales promelas. Ecotoxicology 2002, 11:423-434.
84. van Aerle R., Runnalls T.J., Tyler C.R. Ontogeny of gonadal sex development relative to growth in fathead minnow. J. Fish Biol. 2004, 64:355-369.
85. Vizziano D., Baron D., Randuineau G., Mahe S., Cauty C., Guiguen Y. Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation. Biol. Reprod. 2008, 78:939-946.
86. Wells K., Van Der Kraak G. Differential binding of endogenous steroids and chemicals to androgen receptors in rainbow trout and goldfish. Environ. Toxicol. Chem. 2000, 19:2059-2065.
87. Wilson V.S., Cardon M.C., Gray L.E., Hartig P.C. Competitive binding comparison of endocrine-disrupting compounds to recombinant androgen receptor from fathead minnow, rainbow trout, and human. Environ. Toxicol. Chem. 2007, 26:1793-1802.
88. Wiren K.M., Zhang X.W., Chang C.S., Keenan E., Orwoll E.S. Transcriptional up-regulation of the human androgen receptor by androgen in bone cells. Endocrinology 1997, 138:2291-2300.
89. G.C. Wu, J.L. Du, Y.H. Lee, M.F. Lee, C.F. Chang, Current status of genetic and endocrine factors in the sex change of protandrous black porgy, Acanthopagrus schlegeli (Teleostean), in: H. Vaudry, E. Roubos, L. Schoofs, G. Fiik, D. Larhammar (Eds.), Trends in Comparative Endocrinology and Neurobiology, vol. 1040, 2005, pp. 206-214.
90. Zamora H.S., Hernandez A.A., Herrera S.M., Pena E.M. Anabolic and androgenic effect of steroid trenbolone acetate on guppy (Poecilia reticulata). Veterinaria Mexico 2008, 39:269-277.
91. Zar J.H. Biostatistical Analysis 1999, Prentice Hall, Upper Saddle River, NJ. fourth ed.
92. Zhou Z.X., Wong C.I., Sar M., Wilson E.M. The androgen receptor - an overview. Recent Progress in Hormone Research 1994, vol. 49:249-274. Academic Press Inc., San Diego.