Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish

General and Comparative Endocrinology - Tập 165 Số 3 - Trang 352-366 - 2010
Yann Guiguen1, Alexis Fostier1, Francesc Piferrer2, Ching‐Fong Chang3
1INRA, UR1037 SCRIBE, IFR140, Ouest-Genopole, F-35000 Rennes, France
2Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Passeig Marítim 37-49, 08003 Barcelona, Spain
3Department of Aquaculture, National Taiwan Ocean University, Keelung, 202, Taiwan

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Afonso, 2001, Sex reversal in Nile tilapia (Oreochromis niloticus) using a nonsteroidal aromatase inhibitor, J. Exp. Zool., 290, 177, 10.1002/jez.1047

Alam, 2006, Induction of sex change within two full moons during breeding season and spawning in grouper, Aquaculture, 255, 532, 10.1016/j.aquaculture.2006.01.008

Alam, 2007, Efferent duct differentiation during female-to-male sex change in honeycomb grouper Epinephelus merra, J. Fish Biol., 71, 1192, 10.1111/j.1095-8649.2007.01592.x

Anderson, 2001, Administration of oestradiol to barramundi, Lates calcarifer, induces protandrous sex change, 155

Ashby, 1957, The effect of steroid hormones on the brown trout (Salmo trutta L.) during the period of gonadal differentiation, J. Embryol. Exp. Morph., 5, 225

Baroiller, 1999, Endocrine and environmental aspects of sex differentiation in fish, Cell. Mol. Life Sci., 55, 910, 10.1007/s000180050344

Baroiller, 2001, Environment and sex determination in farmed fish, Comp. Biochem. Physiol. C, 130, 399

Baroiller, 2001, Endocrine and environmental aspects of sex differentiation in gonochoristic fish, EXS, 91, 177

Baron, 2004, An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation, J. Mol. Endocrinol., 33, 705, 10.1677/jme.1.01566

Baron, 2005, Foxl2 gene and the development of the ovary: a story about goat, mouse, fish and woman, Reprod. Nutr. Dev., 45, 377, 10.1051/rnd:2005028

Baron, 2005, Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout, Biol. Reprod., 73, 959, 10.1095/biolreprod.105.041830

Baron, 2007, Androgen-induced masculinization in rainbow trout results in a marked dysregulation of early gonadal gene expression profiles, BMC Genomics, 8, 357, 10.1186/1471-2164-8-357

Baron, 2008, Expression profiling of candidate genes during ovary-to-testis trans-differentiation in rainbow trout masculinized by androgens, Gen. Comp. Endocrinol., 156, 369, 10.1016/j.ygcen.2008.01.016

Belaid, 2001, Sex reversal and aromatase in the European pond turtle: treatment with letrozole after the thermosensitive period for sex determination, J. Exp. Zool., 290, 490, 10.1002/jez.1092

Bhandari, 2003, Treatment with an aromatase inhibitor induces complete sex change in the protogynous honeycomb grouper (Epinephelus merra), Fish Physiol. Biochem., 28, 141, 10.1023/B:FISH.0000030501.23595.2e

Bhandari, 2004, Aromatase inhibitor induces complete sex change in the protogynous honeycomb grouper (Epinephelus merra), Mol. Reprod. Dev., 67, 303, 10.1002/mrd.20027

Bhandari, 2004, Sex inversion of sexually immature honeycomb grouper (Epinephelus merra) by aromatase inhibitor, Zool. Sci., 21, 305, 10.2108/zsj.21.305

Bhandari, 2005, Evidence that estrogen regulates the sex change of honeycomb grouper (Epinephelus merra), a protogynous hermaphrodite fish, J. Exp. Zool. A. Comp. Exp. Biol., 303A, 497, 10.1002/jez.a.178

Bhandari, 2006, Induction of female-to-male sex change in the honeycomb grouper (Epinephelus merra) by 11-ketotestosterone treatments, Zool. Sci., 23, 65, 10.2108/zsj.23.65

Bhandari, 2006, Suppression of steroidogenic enzyme expression during androgen-induced sex reversal in Nile tilapia (Oreochromis niloticus), Gen. Comp. Endocrinol., 145, 20, 10.1016/j.ygcen.2005.06.014

Bhandari, 2006, Estrogen is essential for the maintenance of female sex in fish, J. Exp. Zool. A., 305A, 111

Bjerregaard, 2008, Sex hormone concentrations and gonad histology in brown trout (Salmo trutta) exposed to 17 beta-estradiol and bisphenol A, Ecotoxicology, 17, 252, 10.1007/s10646-008-0192-2

Black, 2004, Socially induced sex change regulates forebrain isotocin in Lythrypnus dalli, Neuroreport, 15, 185, 10.1097/00001756-200401190-00036

Blázquez, 2004, Cloning, sequence analysis, tissue distribution, and sex-specific expression of the neural form of P450 aromatase in juvenile sea bass (Dicentrarchus labrax), Mol. Cell. Endocrinol., 219, 83, 10.1016/j.mce.2004.01.006

Blázquez, 2008, Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax), Gen. Comp. Endocrinol., 158, 95, 10.1016/j.ygcen.2008.06.001

Bobe, 2008, A novel, functional, and highly divergent sex hormone-binding globulin that may participate in the local control of ovarian functions in salmonids, Endocrinology, 149, 2980, 10.1210/en.2007-1652

Brennan, 2004, One tissue, two fates: molecular genetic events that underlie testis versus ovary development, Nat. Rev. Genet., 5, 509, 10.1038/nrg1381

Britt, 2001, The ovarian phenotype of the aromatase knockout (ArKO) mouse, J. Steroid Biochem. Mol. Biol., 79, 181, 10.1016/S0960-0760(01)00158-3

Britt, 2002, Estrogen regulates development of the somatic cell phenotype in the eutherian ovary, FASEB J., 16, 1389, 10.1096/fj.01-0992com

Britt, 2003, Regulation of the phenotype of ovarian somatic cells by estrogen, Mol. Cell. Endocrinol., 202, 11, 10.1016/S0303-7207(03)00055-8

Callard, 1997, Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish, J. Steroid Biochem. Mol. Biol., 61, 387, 10.1016/S0960-0760(97)80037-4

Cardwell, 1991, Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride, Gen. Comp. Endocrinol., 81, 7, 10.1016/0016-6480(91)90120-U

Chan, 1983, Sex control and sex reversal in fish under natural conditions, vol. 9B, 171, 10.1016/S1546-5098(08)60304-0

Chang, 1994, Estradiol-17-Beta Associated with the Sex Reversal in Protandrous Black Porgy, Acanthopagrus schlegeli, J. Exp. Zool., 268, 53, 10.1002/jez.1402680107

Chang, 1995, Estradiol-17 beta suppresses testicular development and stimulates sex reversal in protandrous black porgy, Acanthopagrus schlegeli, Fish Physiol. Biochem., 14, 481, 10.1007/BF00004348

Chang, 1995, Stimulation of spermatogenesis or of sex reversal according to the dose of exogenous estradiol-17beta in juvenile males of protandrous black porgy, Acanthopagrus schlegeli, Gen. Comp. Endocrinol., 100, 355, 10.1006/gcen.1995.1166

Chang, 1998, Estradiol-17 beta stimulates aromatase activity and reversible sex change in protandrous black porgy, Acanthopagrus schlegeli, J. Exp. Zool., 280, 165, 10.1002/(SICI)1097-010X(19980201)280:2<165::AID-JEZ7>3.0.CO;2-M

Chang, 2005, Two types of distribution aromatase with different encoding genes, tissue and developmental expression in Nile tilapia (Oreochromis niloticus), Gen. Comp. Endocrinol., 141, 101, 10.1016/j.ygcen.2004.11.020

Cheshenko, 2008, Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish, Gen. Comp. Endocrinol., 155, 31, 10.1016/j.ygcen.2007.03.005

Chiang, 2001, Two Cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain, Mol. Biol. Evol., 18, 542, 10.1093/oxfordjournals.molbev.a003833

Chourasia, 2008, Ovarian P450 aromatase activity in the catfish Heteropneustes fossilis: Seasonal changes and effects of catecholestrogens, Gen. Comp. Endocrinol., 156, 537, 10.1016/j.ygcen.2008.02.018

Cochran, 1991, Regulation of sexual succession in the protogynous black-sea bass, Centropristis striatus (Osteichthyes, Serranidae), Gen. Comp. Endocrinol., 82, 69, 10.1016/0016-6480(91)90297-J

Conley, 2001, Mammalian aromatase, Reproduction, 121, 685, 10.1530/rep.0.1210685

Conover, 1981, Environmental sex determination—Interaction of temperature and genotype in a fish, Science, 213, 577, 10.1126/science.213.4507.577

Coveney, 2001, Estrogen-induced gonadal sex reversal in the tammar wallaby, Biol. Reprod., 65, 613, 10.1095/biolreprod65.2.613

Dalla Valle, 2002, European sea bass (Dicentrarchus labrax L.) cytochrome P450arom: cDNA cloning, expression and genomic organization, J. Steroid Biochem. Mol. Biol., 80, 25, 10.1016/S0960-0760(01)00170-4

Dalla Valle, 2002, Cloning of two mRNA variants of brain aromatase cytochrome P450 in rainbow trout (Oncorhynchus mykiss Walbaum), J. Steroid Biochem. Mol. Biol., 82, 19, 10.1016/S0960-0760(02)00143-7

Dalla Valle, 2005, Genomic organization of the CYP19b genes in the rainbow trout (Oncorhynchus mykiss Walbaum), J. Steroid Biochem. Mol. Biol., 94, 49, 10.1016/j.jsbmb.2005.01.010

Davis, 1990, Hormonal sex manipulation and evidence for female homogamety in channel catfish, Gen. Comp. Endocrinol., 78, 218, 10.1016/0016-6480(90)90008-A

Davis, 1992, Influence of dihydrotestosterone on sex determination in channel catfish and blue catfish—Period of developmental sensitivity, Gen. Comp. Endocrinol., 86, 147, 10.1016/0016-6480(92)90136-8

D’Cotta, 2001, Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus, Mol. Reprod. Dev., 59, 265, 10.1002/mrd.1031

de Jesus, 1992, Changes in whole-body concentrations of cortisol, thyroid-hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta, Gen. Comp. Endocrinol., 85, 55, 10.1016/0016-6480(92)90171-F

Devlin, 2002, Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences, Aquaculture, 208, 191, 10.1016/S0044-8486(02)00057-1

Elbrecht, 1992, Aromatase enzyme activity and sex determination in chickens, Science, 255, 467, 10.1126/science.1734525

Esterhuyse, 2008, Temporal expression of two Cytochrome P450 Aromatase isoforms during development in Oreochromis mossambicus, in association with histological development, Comp. Biochem. Physiol. D, 297

Feist, 1990, Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation, Gen. Comp. Endocrinol., 80, 299, 10.1016/0016-6480(90)90174-K

Feist, 1996, Brain-pituitary-gonadal axis during early development and sexual differentiation in the rainbow trout, Oncorhynchus mykiss, Gen. Comp. Endocrinol., 102, 394, 10.1006/gcen.1996.0083

Fenske, 2004, Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio), Aquat. Toxicol., 67, 105, 10.1016/j.aquatox.2003.10.008

Fernandino, 2008, Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature-dependent sex determination, Dev. Dyn., 237, 3192, 10.1002/dvdy.21731

Fitzpatrick, 1993, In vitro steroid secretion during early development of mono-sex rainbow trout: sex differences, onset of pituitary control, and effects of dietary steroid treatment, Gen. Comp. Endocrinol., 91, 199, 10.1006/gcen.1993.1119

Fostier, 1983, The gonadal steroids, vol. 9A, 277, 10.1016/S1546-5098(08)60291-5

Frisch, 2004, Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish, Rev. Fish Biol. Fisher., 14, 481, 10.1007/s11160-005-3586-8

Galay-Burgos, 2006, Cloning of the promoter from the gonadal aromatase gene of the European sea bass and identification of single nucleotide polymorphisms, Comp. Biochem. Physiol. A, 145, 47, 10.1016/j.cbpa.2006.04.028

Gardner, 2005, Sex change strategy and the aromatase genes, J. Steroid Biochem. Mol. Biol., 94, 395, 10.1016/j.jsbmb.2004.12.045

González, 2002, Characterization of aromatase activity in the sea bass: Effects of temperature and different catalytic properties of brain and ovarian homogenates and microsomes, J. Exp. Zool., 293, 500, 10.1002/jez.90005

Govoroun, 2001, Steroid enzyme gene expressions during natural and androgen-induced gonadal differentiation in the rainbow trout, Oncorhynchus mykiss, J. Exp. Zool., 290, 558, 10.1002/jez.1106

Govoroun, 2001, 17beta-estradiol treatment decreases steroidogenic enzyme messenger ribonucleic acid levels in the rainbow trout testis, Endocrinology, 142, 1841, 10.1210/en.142.5.1841

Govoroun, 2004, Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development, Dev. Dyn., 231, 859, 10.1002/dvdy.20189

Grober, 1996, Serial adult sex change involves rapid and reversible changes in forebrain neurochemistry, Neuroreport, 7, 2945, 10.1097/00001756-199611250-00029

Guiguen, 1993, Changes in plasma and gonadal steroid hormones in relation to the reproductive cycle and the sex inversion process in the protandrous seabass, Lates calcarifer, Gen. Comp. Endocrinol., 92, 327, 10.1006/gcen.1993.1170

Guiguen, 1995, Gonadal in vitro androstenedione metabolism and changes in some plasma and gonadal steroid hormones during sex inversion of the protandrous sea bass, Lates calcarifer, Gen. Comp. Endocrinol., 100, 106, 10.1006/gcen.1995.1139

Guiguen, 1999, 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., 54, 154, 10.1002/(SICI)1098-2795(199910)54:2<154::AID-MRD7>3.0.CO;2-5

Guiguen, 2000, Implication of steroids in fish gonadal sex differentiation and sex inversion, Curr. Top. Steroid Res., 3, 127

Hano, 2005, Quantitative bio-imaging analysis for evaluation of sexual differentiation in germ cells of olvas-GFP/ST-II YI medaka (Oryzias latipes) nanoinjected in ovo with ethinylestradiol, Environ. Toxicol. Chem., 24, 70, 10.1897/03-610.1

Herpin, 2007, Inhibition of primordial germ cell proliferation by the medaka male determining gene DmrtlbY, BMC Dev. Biol., 7, 99, 10.1186/1471-213X-7-99

Higa, 2003, Role of steroid hormones in sex change of protogynous wrasse, Fish Physiol. Biochem., 28, 149, 10.1023/B:FISH.0000030505.28138.d1

Hines, 1999, Steroid levels and steroid metabolism in relation to early gonadal development in the tilapia Oreochromis niloticus (Teleostei: Cyprinoidei), Gen. Comp. Endocrinol., 114, 235, 10.1006/gcen.1998.7244

Hinfray, 2006, Inhibition of rainbow trout (Oncorhynchus mykiss) P450 aromatase activities in brain and ovarian microsomes by various environmental substances, Comp. Biochem. Physiol. C, 144, 252

Ho, 1991, Vitellogenesis, 91

Hudson, 2005, Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary, Dev. Dyn., 233, 1052, 10.1002/dvdy.20388

Ijiri, 2000, Characterization of gonadal and extra-gonadal forms of the cDNA encoding the Atlantic stingray (Dasyatis sabina) cytochrome P450 aromatase (CYP19), Mol. Cell. Endocrinol., 164, 169, 10.1016/S0303-7207(00)00228-8

Ijiri, 2008, Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus, Biol. Reprod., 78, 333, 10.1095/biolreprod.107.064246

Ito, 2003, Histological process and dynamics of germ cell degeneration in pejerrey Odontesthes bonariensis larvae and juveniles during exposure to warm water, J. Exp. Zool. A. Comp. Exp. Biol., 297, 169, 10.1002/jez.a.10249

Iwamatsu, 2005, Estradiol-17beta content in developing eggs and induced sex reversal of the medaka (Oryzias latipes), J. Exp. Zool. A. Comp. Exp. Biol., 303A, 161, 10.1002/jez.a.120

Iwamatsu, 2006, Testosterone content of developing eggs and sex reversal in the medaka (Oryzias latipes), Gen. Comp. Endocrinol., 145, 67, 10.1016/j.ygcen.2005.07.003

Jeng, 2005, Differential expression of neural and gonadal aromatase enzymatic activities in relation to gonadal development in Japanese eel, Anguilla japonica, J. Exp. Zool. A. Comp. Exp. Biol., 303A, 802, 10.1002/jez.a.194

Jobling, 1998, Widespread sexual disruption in wild fish, Environ. Sci. Technol., 32, 2498, 10.1021/es9710870

Johnson, 1998, Seasonal cycles of gonadal development and plasma sex steroid levels in Epinephelus morio, a protogynous grouper in the eastern Gulf of Mexico, J. Fish Biol., 52, 502

Kagawa, 2003, Effects of luteinizing hormone and follicle-stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicles of red seabream, Pagrus major, Biol. Reprod., 68, 1562, 10.1095/biolreprod.102.008219

Kallivretaki, 2007, The zebrafish, brain-specific, aromatase cyp19a2 is neither expressed nor distributed in a sexually dimorphic manner during sexual differentiation, Dev. Dyn., 236, 3155, 10.1002/dvdy.21344

Kanamori, 1988, Developmental changes in steroidogenic responses of ovarian follicles of amago salmon (Oncorhynchus rhodurus) to chum salmon gonadotropin during oogenesis, Gen. Comp. Endocrinol., 72, 13, 10.1016/0016-6480(88)90176-1

Kanda, 2006, Transcriptional regulation of the rainbow trout CYP19a gene by FTZ-F1 homologue, J. Steroid Biochem. Mol. Biol., 99, 85, 10.1016/j.jsbmb.2005.12.005

Karube, 2007, Characterization and expression profile of the ovarian cytochrome p-450 aromatase (cyp19A1) gene during thermolabile sex determination in pejerrey, Odontesthes bonariensis, J. Exp. Zool. A. Ecol. Gen. Physiol., 308A, 625, 10.1002/jez.416

Kaufmann, 1996, Five years on the wings of fork head, Mech. Dev., 57, 3, 10.1016/0925-4773(96)00539-4

Kawahara, 2000, Estrogen-independent ovary formation in the medaka fish, Oryzias latipes, Zool. Sci., 17, 65, 10.2108/zsj.17.65

Khan, 1997, Metabolism of estrogens and androgens by embryonic tissues of Arctic charr, Salvelinus alpinus, Gen. Comp. Endocrinol., 107, 118, 10.1006/gcen.1997.6908

Kitano, 1999, Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus), J. Mol. Endocrinol., 23, 167, 10.1677/jme.0.0230167

Kitano, 2000, 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., 56, 1, 10.1002/(SICI)1098-2795(200005)56:1<1::AID-MRD1>3.0.CO;2-3

Kitano, 2007, Tamoxifen induces masculinization of genetic females and regulates P450 aromatase and Mullerian inhibiting substance mRNA expression in Japanese flounder (Paralichthys olivaceus), Mol. Reprod. Dev., 74, 1171, 10.1002/mrd.20603

Kobayashi, 1991, Induction of testis development by implantation of 11-ketotestosterone in female goldfish, Zool. Sci., 8, 389

Kobayashi, 2003, Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia, Cytogenet. Genome Res., 101, 289, 10.1159/000074351

Kobayashi, 2004, Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes, Dev. Dyn., 231, 518, 10.1002/dvdy.20158

Kobayashi, 2005, Sex reversal in the medaka Oryzias latipes by brief exposure of early embryos to estradiol-17beta, Zool. Sci., 22, 1163, 10.2108/zsj.22.1163

Kobayashi, 2005, Promoter analysis of two aromatase genes in the serial-sex changing gobiid fish, Trimma okinawae, Fish Physiol. Biochem., 31, 123, 10.1007/s10695-006-0013-6

Kojima, 2008, Sex change of adult initial-phase male wrasse, Halichoeres trimaculatus by estradiol-17beta treatment, Gen. Comp. Endocrinol., 156, 628, 10.1016/j.ygcen.2008.02.003

Kokokiris, 2006, Gonadal changes and blood sex steroids levels during natural sex inversion in the protogynous Mediterranean red porgy, Pagrus pagrus (Teleostei: Sparidae), Gen. Comp. Endocrinol., 149, 42, 10.1016/j.ygcen.2006.05.002

Komatsu, 2006, Masculinization of female golden rabbitfish Siganus guttatus using an aromatase inhibitor treatment during sex differentiation, Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 143, 402, 10.1016/j.cbpc.2006.04.015

Kroon, 2000, The role of steroid hormones in protogynous sex change in the Blackeye goby, Coryphopterus nicholsii (Teleostei: Gobiidae), Gen. Comp. Endocrinol., 118, 273, 10.1006/gcen.2000.7459

Kroon, 2005, Aromatase pathway mediates sex change in each direction, Proc. Biol. Sci., 272, 1399, 10.1098/rspb.2005.3097

Kurokawa, 2007, Germ cells are essential for sexual dimorphism in the medaka gonad, Proc. Natl. Acad. Sci. USA, 104, 16958, 10.1073/pnas.0609932104

Kwon, 2001, Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus, Mol. Reprod. Dev., 59, 359, 10.1002/mrd.1042

Kwon, 2002, Treatment with an aromatase inhibitor suppresses high-temperature feminization of genetic male (YY) Nile tilapia, J. Fish Biol., 60, 625, 10.1111/j.1095-8649.2002.tb01689.x

Lareyre, 2008, Two new TGF beta members are restricted to the gonad and differentially expressed during sex differentiation and gametogenesis in trout, Cybium, 32, 202

Lebrun, 1982, Changes in the number of germ-cells in the gonads of the rainbow-trout (Salmo-Gairdneri) during the first 10 post-hatching weeks, Reprod. Nut. Dev., 22, 405, 10.1051/rnd:19820312

Lee, 2000, Profiles of gonadal development, sex steroids, aromatase activity, and gonadotropin II in the controlled sex change of protandrous black porgy, Acanthopagrus schlegeli Bleeker, Gen. Comp. Endocrinol., 119, 111, 10.1006/gcen.2000.7499

Lee, 2001, Sex change in the protandrous black porgy, Acanthopagrus schlegeli: a review in gonadal development, estradiol, estrogen receptor, aromatase activity and gonadotropin, J. Exp. Zool., 290, 715, 10.1002/jez.1122

Lee, 2002, Aromatase inhibitors block natural sex change and induce male function in the protandrous black porgy, Acanthopagrus schlegeli Bleeker: possible mechanism of natural sex change, Biol. Reprod., 66, 1749, 10.1095/biolreprod66.6.1749

Lee, 2008, Development of ovarian tissue and female germ cells in the protandrous black porgy, Acanthopagrus schlegeli (Perciformes, Sparidae), Zool. Stud., 47, 302

Lewis, 2008, Female-specific increase in primordial germ cells marks sex differentiation in Threespine Stickleback (Gasterosteus aculeatus), J. Morphol., 269, 909, 10.1002/jmor.10608

Li, 2005, Aromatase inhibitor letrozole induces sex inversion in the protogynous red spotted grouper (Epinephelus akaara), Shengli Xuebao, 57, 473

Li, 2006, Gonadal development, aromatase activity and P450 aromatase gene expression during sex inversion of protogynous red-spotted grouper Epinephelus akaara (Temminck and Schlegel) after implantation of the aromatase inhibitor, Fadrozole. Aquac. Res., 37, 484, 10.1111/j.1365-2109.2005.01453.x

Li, 2007, Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara), Anim. Reprod. Sci., 99, 156, 10.1016/j.anireprosci.2006.05.015

Liu, 2007, Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation, J. Endocrinol., 194, 223, 10.1677/JOE-07-0135

Liu, J.F., Guiguen, Y., Liu, S.J., in press. Aromatase (P450arom) and 11beta-hydroxylase (P45011beta) genes are differentially expressed during the sex change process of the protogynous rice field eel, Monopterus albus. Fish Physiol. Biochem., doi:10.1007/s10695-008-9255-9.

Luckenbach, 2005, Aromatase cytochrome P450: cloning, intron variation, and ontogeny of gene expression in southern flounder (Paralichthys lethostigma), J. Exp. Zool. A, 303A, 643, 10.1002/jez.a.198

Magliulo-Cepriano, 1994, Distribution of variant forms of immunoreactive gonadotropin-releasing hormone and b-gonadotropins I and II in the platyfish, Xiphophorus maculatus, from birth to sexual maturity, Gen. Comp. Endocrinol., 94, 135, 10.1006/gcen.1994.1067

Matsuda, 2002, DMY is a Y-specific DM-domain gene required for male development in the medaka fish, Nature, 417, 559, 10.1038/nature751

McAllister, 2003, Early life exposure to environmental levels of the aromatase inhibitor tributyltin causes masculinisation and irreversible sperm damage in zebrafish (Danio rerio), Aquat. Toxicol., 65, 309, 10.1016/S0166-445X(03)00154-1

Merchant-Larios, 1997, Correlation among thermosensitive period, estradiol response, and gonad differentiation in the sea turtle Lepidochelys olivacea, Gen. Comp. Endocrinol., 107, 373, 10.1006/gcen.1997.6946

Miranda, 2001, Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis, Gen. Comp. Endocrinol., 124, 45, 10.1006/gcen.2001.7687

Mishra, 2006, HPLC-electrochemical detection of ovarian estradiol-17 beta and catecholestrogens in the catfish Heteropneustes fossilis: Seasonal and periovulatory changes, Gen. Comp. Endocrinol., 145, 84, 10.1016/j.ygcen.2005.07.006

Moles, 2005, Temporal profile of brain and pituitary GnRHs, GnRH-R, and gonadotropin mRNA expression and content during early development in European sea bass (Dicentrarchus labrax L.), Gen. Comp. Endocrinol., 150, 75, 10.1016/j.ygcen.2006.07.012

Montserrat, 2004, Effects of follicle stimulating hormone on estradiol-17b production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro, Gen. Comp. Endocrinol., 137, 123, 10.1016/j.ygcen.2004.02.011

Morinaga, 2007, The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development, Proc. Natl. Acad. Sci. USA, 104, 9691, 10.1073/pnas.0611379104

Nagahama, 2002, Ontogeny and plasticity of sex determination/gonadal differentiation in fishes, Biol. Reprod., 66, 75

Nagahama, 2004, Sexual plasticity in fish: a possible target of endocrine disruptor action, Environ. Sci., 11, 73

Nakamoto, 2006, Molecular cloning and analysis of gonadal expression of Foxl2 in the medaka, Oryzias latipes, Biochem. Biophys. Res. Commun., 344, 353, 10.1016/j.bbrc.2006.03.137

Nakamoto, 2007, Dax1 suppresses P450arom expression in medaka ovarian follicles, Mol. Reprod. Dev., 74, 1239, 10.1002/mrd.20689

Nakamura, 1989, Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey, Environ. Biol. Fish, 24, 117, 10.1007/BF00001282

Nakamura, 1993, Ultrastructural-study on the differentiation and development of steroid-producing cells during ovarian-differentiation in the amago salmon, Oncorhynchus rhodurus, Aquaculture, 112, 237, 10.1016/0044-8486(93)90449-9

Nakamura, 2003, The role estrogens play in sex differentiation and sex changes of fish, Fish Physiol. Biochem., 28, 113, 10.1023/B:FISH.0000030495.99487.17

Nakamura, 2005, Sex change in fish, Zool. Sci., 22, 1399

Nakamura, 2007, Role of sex hormones in sex change of grouper, J. Mar. Sci. Technol., 15, 23, 10.51400/2709-6998.2055

Navarro-Martín, 2009, Masculinization of the European sea bass (Dicentrarchus labrax) by treatment with an androgen or aromatase inhibitor involves different gene expression and has distinct lasting effects on maturation, Gen. Comp. Endocrinol., 160, 3, 10.1016/j.ygcen.2008.10.012

Nocillado, 2007, Cytochrome P450 aromatase in grey mullet: cDNA and promoter isolation; brain, pituitary and ovarian expression during puberty, Mol. Cell. Endocrinol., 263, 65, 10.1016/j.mce.2006.08.013

Ogawa, 2008, ‘Post-sex differentiational’ sex reversal in the female common carp (Cyprinus carpio), Cybium, 32, 102

Orlando, 2007, Sexual dimorphic responses in wildlife exposed to endocrine disrupting chemicals, Environ. Res., 104, 163, 10.1016/j.envres.2006.06.002

Ospina-Álvarez, 2008, Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change, PloS ONE, 3, e2837, 10.1371/journal.pone.0002837

Pandian, 1995, Hormonal induction of sex reversal in fish, Aquaculture, 138, 1, 10.1016/0044-8486(95)01075-0

Pandolfi, 2006, Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation, Anat. Embryol., 211, 355, 10.1007/s00429-006-0086-0

Pannetier, 2006, FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development, J. Mol. Endocrinol., 36, 399, 10.1677/jme.1.01947

Park, 2004, Sex differentiation and hormonal sex reversal in the bagrid catfish Pseudobagrus fulvidraco (Richardson), Aquaculture, 232, 183, 10.1016/S0044-8486(03)00481-2

Patil, 2008, Tissue and sexually dimorphic expression of ovarian and brain aromatase mRNA in the Japanese medaka (Oryzias latipes): Implications for their preferential roles in ovarian and neural differentiation and development, Gen. Comp. Endocrinol., 158, 131, 10.1016/j.ygcen.2008.05.016

Paul-Prasanth, 2006, Knock-down of DMY initiates female pathway in the genetic male medaka, Oryzias latipes, Biochem. Biophys. Res. Commun., 351, 815, 10.1016/j.bbrc.2006.10.095

Penman, 2008, Fish gonadogenesis. Part I: Genetic and environmental mechanisms of sex determination, Rev. Fish. Sci., 16, 16, 10.1080/10641260802324610

Petkam, 2002, In vitro metabolism of progesterone, androgens and estrogens by rainbow trout embryos, Fish Physiol. Biochem., 27, 117, 10.1023/B:FISH.0000021867.71729.22

Petrino, 1989, Steroidogenesis in Fundulus heteroclitus. II. Production of 17alpha-hydroxy-20beta-dihydroprogesterone, testosterone, and 17beta-estradiol by various components of the ovarian follicle, Gen. Comp. Endocrinol., 76, 230, 10.1016/0016-6480(89)90154-8

Pieau, 2004, Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads, J. Endocrinol., 181, 367, 10.1677/joe.0.1810367

Piferrer, 1994, Brief treatment with an aromatase inhibitor during sex-differentiation causes chromosomally female salmon to develop as normal, functional males, J. Exp. Zool., 270, 255, 10.1002/jez.1402700304

Piferrer, 2001, Endocrine sex control strategies for the feminization of teleost fish, Aquaculture, 197, 229, 10.1016/S0044-8486(01)00589-0

Piferrer, 2005, Aromatase distribution and regulation in fish, Fish Physiol. Biochem., 31, 215, 10.1007/s10695-006-0027-0

Piferrer, 2008, Fish gonadogenesis. Part II: Molecular biology and genomics of sex differentiation, Rev. Fish Sci., 16, 35, 10.1080/10641260802324644

Piferrer, F., Navarro-Martín, L., Ospina-Álvarez, N., Blázquez, M., Viñas, J., 2008. Temperature-dependent sex determination in fish, effects of temperature on gonadal aromatase gene expression, and epigenetic regulation after early exposure to high water temperature. Proc. Sixth Int. Symp. Fish Endocrinol. Calgary, June 22–27, p. 63 (Abstract).

Ponthier, 1998, Seasonal changes in the production of two novel and abundant ovarian steroids in the channel catfish (Ictalurus punctatus), Gen. Comp. Endocrinol., 111, 141, 10.1006/gcen.1998.7096

Rashid, 2007, Fugu (Takifugu rubripes) sexual differentiation: CYP19 regulation and aromatase inhibitor induced testicular development, Sex Dev., 1, 311, 10.1159/000108935

Reed, 2005, Steroid sulfatase: Molecular biology, regulation, and inhibition, Endocr. Rev., 26, 171, 10.1210/er.2004-0003

Reinboth, 1980, Can sex inversion be environmentally induced?, Biol. Reprod., 2, 49, 10.1095/biolreprod22.1.49

Reinboth, 1982, The problem of sexual bipotentiality as exemplified by teleosts, Reprod. Nut. Dev., 22, 397, 10.1051/rnd:19820311

Reinboth, 1983, The peculiarities of gonad transformation in teleosts, Differentiation, 23, S82

Rothbard, 1987, Changes in steroid concentrations during sexual ontogenesis in tilapia, Aquaculture, 61, 59, 10.1016/0044-8486(87)90338-3

Rougeot, 2007, Sex steroid dynamics during embryogenesis and sexual differentiation in Eurasian perch, Perca fluviatilis, Theriogenology, 67, 1046, 10.1016/j.theriogenology.2006.12.006

Rowell, 2002, Androgen and estrogen metabolism during sex differentiation in mono-sex populations of the Nile tilapia, Oreochromis niloticus, Gen. Comp. Endocrinol., 125, 151, 10.1006/gcen.2001.7691

Sadovy, 1987, Criteria for the diagnosis of hermaphroditism in fishes, Copeia, 1, 136, 10.2307/1446046

Saga, 1993, Salmonid pituitary adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus), Gen. Comp. Endocrinol., 92, 233, 10.1006/gcen.1993.1159

Saito, 2007, Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai, Dev. Biol., 310, 280, 10.1016/j.ydbio.2007.07.039

Sakai, 2008, Stability in aromatase immunoreactivity of steroid-producing cells during early development of XX gonads of the Nile tilapia, Oreochromis niloticus: an organ culture study, Zool. Sci., 25, 344, 10.2108/zsj.25.344

Sawatari, 2007, A novel transforming growth factor-beta superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss), Dev. Biol., 301, 266, 10.1016/j.ydbio.2006.10.001

Scheib, 1983, Effects and role of estrogens in avian gonadal differentiation, Differentiation, 23, S87

Shapiro, 1989, Plasma hormones and gonadal histology of a protogynous grouper during an experimental attempt to induce adult sex change, J. Zool., 193, 105, 10.1111/j.1469-7998.1981.tb01494.x

Shilling, 1999, Rainbow trout, Oncorhynchus mykiss, as a model for aromatase inhibition, J. Steroid Biochem. Mol. Biol., 70, 89, 10.1016/S0960-0760(99)00090-4

Shimizu, 2008, Appearances and chronological changes of mummichog Fundulus heteroclitus FSH cells and LH cells during ontogeny, sexual differentiation, and gonadal development, Gen. Comp. Endocrinol., 156, 312, 10.1016/j.ygcen.2008.01.022

Shinomiya, 2001, Sexual differentiation of germ cell deficient gonads in the medaka, Oryzias latipes, J. Exp. Zool., 290, 402, 10.1002/jez.1081

Shiraishi, 2007, Mullerian inhibiting substance is required for germ cell proliferation during early gonadal differentiation in medaka (Oryzias latipes), Endocrinology, 149, 1813, 10.1210/en.2007-1535

Sire, 1981, In vitro effect of a fish gonadotropin on aromatase and 17 beta-hydroxysteroid dehydrogenase activities in the ovary of the rainbow trout (Salmo gairdneri Rich.), Reprod. Nutr. Dev, 21, 715, 10.1051/rnd:19810511

Slanchev, 2005, Development without germ cells: the role of the germ line in zebrafish sex differentiation, Proc. Natl. Acad. Sci. USA, 102, 4074, 10.1073/pnas.0407475102

Siegfried, 2008, Germ line control of female sex determination in zebrafish, Dev. Biol., 324, 277, 10.1016/j.ydbio.2008.09.025

Simpson, 1994, Aromatase cytochrome-P450, the enzyme responsible for estrogen biosynthesis, Endocr. Rev., 15, 342

Socorro, 2007, A cDNA for European sea bass (Dicentrachus labrax) 11 beta-hydroxylase: Gene expression during the thermosensitive period and gonadogenesis, Gen. Comp. Endocrinol., 150, 164, 10.1016/j.ygcen.2006.07.018

Strüssmann, 1998, Heat-induced germ cell deficiency in the teleosts Odontesthes bonariensis and Patagonina hatcheri, Comp. Biochem. Physiol. A, 119, 637, 10.1016/S1095-6433(97)00477-7

Strüssmann, 2002, Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes, Fish Physiol. Biochem., 26, 13, 10.1023/A:1023343023556

Sudhakumari, 2003, Expression of cytochrome P-450aromatases in the sex-reversed Nile tilapia, Fish Physiol. Biochem., 28, 177, 10.1023/B:FISH.0000030519.16010.34

Sudhakumari, 2005, Ontogenic expression patterns of several nuclear receptors and cytochrome P450 aromatases in brain and gonads of the Nile tilapia Oreochromis niloticus suggests their involvement in sex differentiation, Fish Physiol. Biochem., 31, 129, 10.1007/s10695-006-0014-5

Sun, 2007, Tamoxifen effects on the early life stages and reproduction of Japanese medaka (Oryzias latipes), Environ. Toxicol. Phar., 24, 23, 10.1016/j.etap.2007.01.003

Suzuki, 2004, Expression of aromatase mRNA and effects of aromatase inhibitor during ovarian development in the medaka, Oryzias latipes, J. Exp. Zool. A, 301, 266, 10.1002/jez.a.20027

Tanaka, 1995, Structure and promoter analysis of the cytochrome P-450 aromatase gene of the teleost fish, medaka (Oryzias latipes), J. Biochem., 117, 719, 10.1093/oxfordjournals.jbchem.a124768

Tanaka, 2008, Cross talk between germ cells and gonadal somatic cells is critical for sex differentiation of the gonads in the teleost fish, medaka (Oryzias latipes), Dev. Growth Differ., 50, 273, 10.1111/j.1440-169X.2008.01015.x

Tchoudakova, 1998, Identification of multiple CYP 19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary, Endocrinology, 139, 2179, 10.1210/en.139.4.2179

Todo, 2008, In vitro induction of gonadal sex change in a protogynous fish, three-spotted wrasse (Halichoeres trimaculatus), Cybium, 32, 106

Tzchori, 2004, Masculinization of genetic females of the common carp (Cyprinus carpio L.) by dietary administration of an aromatase inhibitor, Israeli J. Aqua., 56, 239

Uchida, 2002, Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish, J. Exp. Biol., 205, 711, 10.1242/jeb.205.6.711

Uchida, 2004, An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal, Comp. Biochem. Physiol. A. Mol. Integr. Physiol., 137, 11, 10.1016/S1095-6433(03)00178-8

van den Hurk, 1982, Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiation, Reprod. Nutr. Dev., 22, 413, 10.1051/rnd:19820313

van Nes, 2006, Temperature effects on sex determination and ontogenetic gene expression of the aromatases cyp19a and cyp19b, and the estrogen receptors esr1 and esr2 in atlantic halibut (Hippoglossus hippoglossus), Mol. Reprod. Dev., 73, 1481, 10.1002/mrd.20514

Villalpando, 2000, The P450 aromatase (P450 arom) gene is asymmetrically expressed in a critical period for gonadal sexual differentiation in the chick, Gen. Comp. Endocrinol., 117, 325, 10.1006/gcen.2000.7425

Vizziano, 2007, Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss, Dev. Dyn., 236, 2198, 10.1002/dvdy.21212

Vizziano, 2008, Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen aupplementation, Biol. Reprod., 78, 939, 10.1095/biolreprod.107.065961

Vizziano-Cantonnet, 2008, Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal trans-differentiation, J. Mol. Endocrinol., 41, 277, 10.1677/JME-08-0039

Wang, 2001, Aromatase (Cyp19) expression is up-regulated by targeted disruption of Dax1, Proc. Natl. Acad. Sci. USA, 98, 7988, 10.1073/pnas.141543298

Wang, 2007, 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., 21, 712, 10.1210/me.2006-0248

Wang, D.S., Nagahama, Y., 2008. DMRT1 represses AD4BP/SF1/FOXL2 activated aromatase gene transcription: a possible mechanism favoring the male pathway in tilapia. Proc. Sixth Int. Symp. Fish Endocrinol. Calgary, June 22–27, p. 62 (Abstract).

Wang, 2007, Anti-Mullerian hormone and 11beta-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males, Dev. Dyn., 236, 1329, 10.1002/dvdy.21129

Watanabe, 1999, Medaka (Oryzias latipes) FTZ-F1 potentially regulates the transcription of P-450 aromatase in ovarian follicles: cDNA cloning and functional characterization, Mol. Cell. Endocrinol., 149, 221, 10.1016/S0303-7207(99)00006-4

Wibbels, 1994, Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination, J. Endocrinol., 141, 295, 10.1677/joe.0.1410295

Wong, 2006, Molecular biology of ovarian aromatase in sex reversal: complementary DNA and 5′-flanking region isolation and differential expression of ovarian aromatase in the gilthead seabream (Sparus aurata), Biol. Reprod., 74, 857, 10.1095/biolreprod.105.045351

Wu, 2008, The expression of nr0b1 and nr5a4 during gonad development and sex change in protandrous black porgy fish, Acanthopagrus schlegeli, Biol. Reprod., 78, 200, 10.1095/biolreprod.107.062612

Wu, 2008, Dual roles of cyp19a1a in gonadal sex differentiation and development in the protandrous black porgy, Acanthopagrus schlegeli, Biol. Reprod., 79, 1111, 10.1095/biolreprod.108.069146

Yamaguchi, 2007, 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., 359, 935, 10.1016/j.bbrc.2007.05.208

Yamamoto, 1969, Sex differentiation, vol. 3, 117

Yao, 2004, Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis, Dev. Dyn., 230, 210, 10.1002/dvdy.20042

Yeh, 2003, 17alpha-methyltestosterone induced sex change in the unilateral ovariectomized protogynous orange-spotted grouper, Epinephelus coioides, J. Fisher Soc. Taiwan, 30, 91

Yeh, 2003, The effects of exogenous androgens on ovarian development and sex change in female orange-spotted protogynous grouper, Epinephelus coioides, Aquaculture, 218, 729, 10.1016/S0044-8486(02)00565-3

Yeoh, 1996, Endogenous steroid metabolism is indicated by fluctuations of endogenous steroid and steroid glucuronide levels in early development of the steelhead trout (Oncorhynchus mykiss), Gen. Comp. Endocrinol., 103, 107, 10.1006/gcen.1996.0099

Yeoh, 1996, In vivo steroid metabolism in embryonic and newly hatched steelhead trout (Oncorhynchus mykiss), Gen. Comp. Endocrinol., 102, 197, 10.1006/gcen.1996.0061

Yeung, 1987, The plasma sex steroid profiles in the fresh-water, sex-reversing teleost fish, Monopterus albus (Zuiew), Gen. Comp. Endocrinol., 65, 233, 10.1016/0016-6480(87)90171-7

Young, 1983, 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, 310, 10.1095/biolreprod29.2.310

Yu, 2008, Cloning, structure, and expression pattern of the P-450 aromatase gene in rice field eel (Monopterus albus), Biochem. Genet., 46, 267, 10.1007/s10528-008-9154-x

Zhang, 2004, Two distinct cytochrome P450 aromatases in the orange-spotted grouper (Epinephelus coioides): cDNA cloning and differential mRNA expression, J. Steroid Biochem. Mol. Biol., 92, 39, 10.1016/j.jsbmb.2004.05.010

Zhao, 2001, Different catalytic properties and inhibitor responses of the goldfish brain and ovary aromatase isozymes, Gen. Comp. Endocrinol., 123, 180, 10.1006/gcen.2001.7661