Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation

Biology of Reproduction

Volumn 78, Issue 5, 2008, Pages 939-946

  Vizziano, Denise ^a,b   Baron, Daniel ^b   Randuineau, Gwenaëlle ^b   Mahè, Sophie ^b   Cauty, Chantal ^b   Guiguen, Yann ^b  

^a FACULTAD DE CIENCIAS   (Uruguay)

^b CEMAGREF   (France)

Author keywords

Early development; Gene regulation; Ovary; Steroid hormones; Testis

Indexed keywords

11BETA ANDROSTENEDIONE; 11BETA HYDROXYANDROSTENEDIONE; ANDROSTA 1,4,6 TRIENE 3,17 DIONE; ANDROSTENEDIONE DERIVATIVE; AROMATASE INHIBITOR; ESTROGEN;

AMH GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYP11B2.1 GENE; CYP11B2.2 GENE; CYP17A GENE; CYP19A1 GENE; DAX1 GENE; DMRT1 GENE; DOWN REGULATION; EMBRYO DEVELOPMENT; ESTROGEN SYNTHESIS; FEMALE; FOXL2A GENE; FSHB GENE; FST GENE; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; HSD3B1 GENE; MALE; NONHUMAN; NR0B1 GENE; NR5A1 GENE; PDGFRA GENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERTOLI CELL; SEX DIFFERENTIATION; SOX9A2 GENE; STAR GENE; TESTIS DEVELOPMENT; UPREGULATION; VIRILIZATION;

ANDROGENS; ANDROSTATRIENES; ANDROSTENEDIONE; ANIMALS; AROMATASE; DNA-BINDING PROTEINS; ENZYME INHIBITORS; ESTROGENS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENOTYPE; MALE; ONCORHYNCHUS MYKISS; OVARY; PHENOTYPE; RECEPTORS, RETINOIC ACID; REPRESSOR PROTEINS; SEX DIFFERENTIATION; TESTIS; TRANSCRIPTION FACTORS;

ONCORHYNCHUS MYKISS;

EID: 43249127860     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.065961     Document Type: Article

References (55)

1. Baroiller JF, Guiguen Y, Fostier A. Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 1999; 55:910-931.
2. Baroiller JF, Guiguen Y. Endocrine and environmental aspects of sex differentiation in gonochoristic fish. EXS 2001; 91:177-201.
3. Hayes TB. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool 1998; 281:373-399.
4. Pieau C, Dorizzi M. Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J Endocrinol 2004; 181: 367-377.
5. Smith CA, Sinclair AH. Sex determination: insights from the chicken. Bioessays 2004; 26:120-132.
6. Clinton M, Haines LC. An overview of factors influencing sex determination and gonadal development in birds. EXS 2001; 91:97-115.
7. Coveney D, Shaw G, Renfree MB. Estrogen-induced gonadal sex reversal in the tammar wallaby. Biol Reprod 2001; 65:613-621.
8. Renfree MB, Shaw G. Germ cells, gonads and sex reversal in marsupials. Int J Dev Biol 2001; 45:557-567.
9. Fenske M, Segner H. Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat Toxicol 2004; 67:105-126.
10. Guiguen Y, Baroiller JF, Ricordel MJ, Iseki K, Mcmeel OM, Martin SA, Fostier A. Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol Reprod Dev 1999; 54:154-162.
11. Chardard D, Dournon C. Sex reversal by aromatase inhibitor treatment in the newt Pleurodeles waltl. J Exp Zool 1999; 283:43-50.
12. Miyata S, Kubo T. In vitro effects of estradiol and aromatase inhibitor treatment on sex differentiation in Xenopus laevis gonads. Gen Comp Endocrinol 2000; 119:105-110.
13. Wibbels T, Crews D. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J Endocrinol 1994; 141:295-299.
14. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C. Endocrine sex reversal of gonads by the aromatase inhibitor Letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 1995; 100:314-326.
15. Wartenberg H, Lenz E, Schweikert HU. Sexual differentiation and the germ cell in sex reversed gonads after aromatase inhibition in the chicken embryo. Andrologia 1992; 24:1-6.
16. Vaillant S, Guemene D, Dorizzi M, Pieau C, Richard-Mercier N, Brillard JP. Degree of sex reversal as related to plasma steroid levels in genetic female chickens (Gallus domesticus) treated with Fadrozole. Mol Reprod Dev 2003; 65:420-428.
17. Piferrer F, Baker IJ, Donaldson EM. 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.
18. Papoulias DM, Noltie DB, Tillitt DE. Effects of methyl testosterone exposure on sexual differentiation in medaka, Oryzias latipes. Mar Environ Res 2000; 50:181-184.
19. Govoroun M, Mcmeel OM, D'Cotta H, Ricordel MJ, 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.
20. van den HR, van Oordt PG. Effects of natural androgens and corticosteroids on gonad differentiation in the rainbow trout, Salmo gairdneri. Gen Comp Endocrinol 1985; 57:216-222.
21. Chardard D, Kuntz S, Chesnel A, Flament S. Effects of androgens on sex differentiation of the urodele Pleurodeles waltl. J Exp Zoolog A Comp Exp Biol 2003; 296:46-55.
22. Faucounau N, Ichas F, Stoll R, Maraud R. Action of testosterone on the estradiol-induced feminization of the male chick embryo. Anat Embryol (Berl) 1995; 191:377-379.
23. Kitano T, Takamune K, Nagahama Y, Abe SI. Aromatase inhibitor and 17alpha-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol Reprod Dev 2000; 56:1-5.
24. Bhandari RK, 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.
25. Baron D, Houlgatte R, Fostier A, Guiguen Y. Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 2005; 73:959-966.
26. Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn 2007; 236:2198-2206.
27. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001; 98:5116-5121.
28. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006; 411:134-193.
29. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004; 20:1453-1454.
30. Saldanha AJ. Java Treeview - extensible visualization of microarray data. Bioinformatics 2004; 20:3246-3248.
31. Bhandari RK, Alam MA, Higa M, Soyano K, Nakamura M. Evidence that estrogen regulates the sex change of honeycomb grouper (Epinephelus merra), a protogynous hermaphrodite fish. J Exp Zool A Comp Exp Biol 2005; 303:497-503.
32. D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF. Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol Reprod Dev 2001; 59:265-276.
33. Pailhoux E, Vigier B, Schibler L, Cribiu EP, Cotinot C, Vaiman D. Positional cloning of the PIS mutation in goats and its impact on understanding mammalian sex-differentiation. Genet Sel Evol 2005; 37(suppl 1):S55-S64.
34. Govoroun MS, Pannetier M, Pailhoux E, Cocquet J, Brillard JP, Couty I, Batellier F, Cotinot C. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev Dyn 2004; 231:859-870.
35. Baron D, Cocquet J, Xia X, Fellous M, Guiguen Y, Veitia RA. An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J Mol Endocrinol 2004; 33:705-715.
36. Nakamoto M, Matsuda M, Wang DS, Nagahama Y, Shibata N. Molecular cloning and analysis of gonadal expression of Foxl2 in the medaka, Oryzias latipes. Biochem Biophys Res Commun 2006; 344:353-361.
37. Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pepin B, Cotinot C, Veitia R, Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 2006; 36:399-413.
38. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 2007; 21:712-725.
39. Hudson QJ, Smith CA, Sinclair AH. Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 2005; 233:1052-1055.
40. Yao HH. The pathway to femaleness: current knowledge on embryonic development of the ovary. Mol Cell Endocrinol 2005; 230:87-93.
41. Yao HH, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 2004; 230:210-215.
42. Yao HH, Aardema J, Holthusen K. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol Reprod 2006; 74:978-983.
43. Peng C, Ohno T, Khorasheh S, Leung PC. Activin and follistatin as local regulators in the human ovary. Biol Signals 1996; 5:81-89.
44. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun 2007; 359:935-940.
45. Nakamoto M, Wang DS, Suzuki A, Matsuda M, Nagahama Y, Shibata N. Dax1 suppresses P450arom expression in medaka ovarian follicles. Mol Reprod Dev 2007; 74:1239-1246.
46. Wang ZJ, Jeffs B, Ito M, Achermann JC, Yu RN, Hales DB, Jameson JL. Aromatase (Cyp19) expression is up-regulated by targeted disruption of Dax1. Proc Natl Acad Sci U S A 2001; 98:7988-7993.
47. Loir M, Le Gac F. Insulin-like growth factor-I and -II binding and action on DNA synthesis in rainbow trout spermatogonia and spermatocytes. Biol Reprod 1994; 51:1154-1163.
48. Luukko K, Ylikorkala A, Makela TP. Developmentally regulated expression of Smad3, Smad4, Smad6, and Smad7 involved in TGF-beta signaling. Mech Dev 2001; 101:209-212.
49. Cui S, Ross A, Stallings N, Parker KL, Capel B, Quaggin SE. Disrupted gonadogenesis and male-to-female sex reversal in Pod1 knockout mice. Development 2004; 131:4095-4105.
50. Rey R, Lukas-Croisier C, Lasala C, Bedecarras P. AMH/MIS: what we know already about the gene, the protein and its regulation. Mol Cell Endocrinol 2003; 211:21-31.
51. Ingraham HA, Hirokawa Y, Roberts LM, Mellon SH, McGee E, Nachtigal MW, Visser JA. Autocrine and paracrine Mullerian inhibiting substance hormone signaling in reproduction. Recent Prog Horm Res 2000; 55:53-67.
52. Josso N, di Clemente N, Gouedard L. Anti-Mullerian hormone and its receptors. Mol Cell Endocrinol 2001; 179:25-32.
53. Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N, Mitani H, Furutani-Seiki M, Tanaka M, Kondoh H. The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci U S A 2007; 104: 9691-9696.
54. Miura T, Miura C, Konda Y, Yamauchi K. Spermatogenesis-preventing substance in Japanese eel. Development 2002; 129:2689-2697.
55. Baron D, Montfort J, Houlgatte R, Fostier A, Guiguen Y. Androgen-induced masculinization in rainbow trout results in a marked dysregulation of early gonadal gene expression profiles. BMC Genomics 2007; 8:357.