Environmental stress-induced testis differentiation: Androgen as a by-product of cortisol inactivation

General and Comparative Endocrinology

Volumn 192, Issue , 2013, Pages 36-44

  Fernandino, Juan I ^a   Hattori, Ricardo S ^b   Moreno Acosta, Omar D ^a   Strüssmann, Carlos A ^b   Somoza, Gustavo M ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

11 HSD; Environmental sex determination; Masculinization; Stress

Indexed keywords

11 OXOTESTOSTERONE; 11BETA HYDROXYSTEROID DEHYDROGENASE; AROMATASE; CORTISONE; GLUCOCORTICOID; HYDROCORTISONE; SEX HORMONE;

ANDROGEN SYNTHESIS; APOPTOSIS; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; ENZYME MECHANISM; ENZYME REGULATION; HIGH TEMPERATURE; HORMONAL REGULATION; HORMONE INHIBITION; HYPOXIA; LARVAL STAGE; MASCULINITY; MOLECULAR INTERACTION; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEX DETERMINATION PROCESS; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; TELEOST; TEMPERATURE SENSITIVITY; TEMPERATURE STRESS; TESTIS DEVELOPMENT;

11Β-HSD; ENVIRONMENTAL SEX DETERMINATION; MASCULINIZATION; STRESS;

11-BETA-HYDROXYSTEROID DEHYDROGENASES; ANDROGENS; ANIMALS; FISHES; GLUCOCORTICOIDS; MALE; SEX DIFFERENTIATION; STRESS, PHYSIOLOGICAL; TESTIS;

EID: 84884414567     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.05.024     Document Type: Review

References (136)

1. Abozaid H., Wessels S., Hörstgen-Schwark G. Elevated temperature applied during gonadal transformation leads to male bias in Zebrafish (Danio rerio). Sex. Dev. 2012, 6:201-209.
2. Abucay J.S., Mair G.C., Skibinski D.O.F., Beardmore J.A. Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 1999, 173:219-234.
3. Albiston A.L., Obeyesekere V.R., Smith R.E., Krozowski Z.S. Cloning and tissue distribution of the human 11 beta-hydroxysteroid dehydrogenase type 2 enzyme. Mol. Cell. Endocrinol. 1994, 105:R11-R17.
4. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in zebrafish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294.
5. Aluru N., Vijayan M.M. Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen. Comp. Endocrinol. 2009, 164:142-150.
6. Badcock J. Aspects of the reproductive biology of Gonostoma bathyphilum (Gonostomatidae). J. Fish Biol. 1986, 29:589-603.
7. Baker M.E. Evolutionary analysis of 11beta-hydroxysteroid dehydrogenase-type 1, -type 2, -type 3 and 17beta-hydroxysteroid dehydrogenase-type 2 in fish. FEBS Lett. 2004, 574:167-170.
8. Baroiller J., Guiguen Y., Fostier A. Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 1999, 55:910-931.
9. Baroiller J.F., Chourrout D., Fostier A., Jalabert B. Temperature and sex chromosomes govern sex ratios of the mouthbrooding Cichlid fish Oreochromis niloticus. J. Exp. Zool. 1995, 273:216-223.
10. Baroiller J.F., D'Cotta H., Saillant E. Environmental effects on fish sex determination and differentiation. Sex. Dev. 2009, 3:118-135.
11. Baroiller J.F., Nakayama I., Foresti F., Chourrout D. Sex determination studies in two species of teleost fish, Oreochromis niloticus and Leporinus elongatus. Zool. Stud. 1996, 35:279-285.
12. Barón B.S., Bückle F.R., Espina S. Environmental factors and sexual differentiation in Poecilia sphenops Valenciennes (Pisces: Poeciliidae). Aquac. Res. 2002, 33:615-619.
13. Barske L.A., Capel B. Blurring the edges in vertebrate sex determination. Curr. Opin. Genet. Dev. 2008, 18:499-505.
14. Beato M., Klug J. Steroid hormone receptors: an update. Hum. Reprod. Update. 2000, 6:225-236.
15. Beullens K., Eding E.H., Gilson P., Ollevier F., Komen J., Richter C.J.J. Gonadal differentiation, intersexuality and sex ratios of European eel (Anguilla anguilla L.) maintained in captivity. Aquaculture 1997, 153:135-150.
16. Blasco M., Fernandino J.I., Guilgur L.G., Strussmann C.A., Somoza G.M., Vizziano-Cantonnet D. Molecular characterization of cyp11a1 and cyp11b1 and their gene expression profile in pejerrey (Odontesthes bonariensis) during early gonadal development. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 156:110-118.
17. Blazquez M., Navarro-Martin L., Piferrer F. Expression profiles of sex differentiation-related genes during ontogenesis in the European sea bass acclimated to two different temperatures. J. Exp. Zool. B Mol. Dev. Evol. 2009, 312:686-700.
18. Blazquez M., Somoza G.M. Fish with thermolabile sex determination (TSD) as models to study brain sex differentiation. Gen. Comp. Endocrinol. 2010, 166:470-477.
19. Blázquez M., Zanuy S., Carillo M., Piferrer F. Effects of rearing temperature on sex differentiation in the European sea bass (Dicentrarchus labrax L.). J. Exp. Zool. 1998, 281:207-216.
20. Borg B. Androgen in teleost fishes. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1994, 109:219-245.
21. Breitburg D.L., Hondorp D.W., Davias L.A., Diaz R.J. Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Annu. Rev. Mar. Sci. 2009, 1:329-349.
22. Bury N.R., Sturm A. Evolution of the corticosteroid receptor signalling pathway in fish. Gen. Comp. Endocrinol. 2007, 153:47-56.
23. Cavaco J.E.B., Vischer H.F., Lambert J.G.D., Goos H.J.T., Schulz R.W. Mismatch between patterns of circulating and testicular androgens in African catfish, Clarias gariepinus. Fish Physiol. Biochem. 1997, 17:155-162.
24. Colombo G., Grandi G. Histological study of the development and sex differentiation of the gonad in the European eel. J. Fish Biol. 1996, 48:493-512.
25. Conover D.O., Fleisher M.H. Temperature-sensitive period of sex determination in the Atlantic silverside, Menidia menidia. Can. J. Fish Aquat. Sci. 1986, 43:514-520.
26. Consten D., Keuning E.D., Bogerd J., Zandbergen M.A., Lambert J.G., Komen J., et al. Sex steroids and their involvement in the cortisol-induced inhibition of pubertal development in male common carp, Cyprinus carpio L. Biol. Reprod. 2002, 67:465-472.
27. Chang H., Hu J., Shao B. Occurrence of natural and synthetic glucocorticoids in sewage treatment plants and receiving river waters. Environ. Sci. Technol. 2007, 41:3462-3468.
28. Chiba H., Iwata M., Yakoh K., Satoh R., Yamada H. Possible influence of social stress on sex differentiation in Japanese eel. Fish Sci. 2002, 68:413-414.
29. Chu Y.W., Han Y.S., Wang C.H., You C.F., Tzeng W.N. The sex-ratio reversal of the Japanese eel Anguilla japonica in the kaoping river of Taiwan: the effect of cultured eels and its implication. Aquaculture 2006, 261:1230-1238.
30. Davey A.J.H., Jellyman D.J. Sex determination in freshwater eels and management options for manipulation of sex. Rev. Fish Biol. Fish. 2005, 15:37-52.
31. Degani G., Kushnirov D. Effects of 17β-estradiol and grouping on sex determination of European eels. Prog. Fish Cult. 1992, 54:88-91.
32. 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.
33. Duffy T.A., Picha M.E., Won E.T., Borski R.J., McElroy A.E., Conover D.O. Ontogenesis of gonadal aromatase gene expression in Atlantic silverside (Menidia menidia) populations with genetic and temperature-dependent sex determination. J. Exp. Zool. A Ecol. Genet. Physiol. 2010, 313:421-431.
34. Egusa S. Notes on the culture of the European eel (Anguilla anguilla L.) in Japanese eel-farming ponds. Rapp. P.-V. Réun. Cons. Int. Explor. Mer. 1979, 174:51-58.
35. Fan Z., Wu S., Chang H., Hu J. Behaviors of glucocorticoids, androgens and progestogens in a municipal sewage treatment plant: comparison to estrogens. Environ. Sci. Technol. 2011, 45:2725-2733.
36. Fernandino J.I., Hattori R.S., Kishi A., Strüssmann C.A., Somoza G.M. The cortisol and androgen pathways cross talk in high-temperature induced masculinization: 11β-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 2012, 153:6003-6011.
37. Fernandino J.I., Popesku J., Paul-Prasanth B., Xiong H., Hattori R.S., Oura M., et al. Analysis of sexually dimorphic expression of genes at early gonadogenesis of pejerrey Odontesthes bonariensis using a heterologous microarray. Sex. Dev. 2011, 5:89-101.
38. Francis R.C. Experiential effects on agonistic behavior in the paradise fish, (Macropodus opercularis). Behaviour 1983, 85:292-313.
39. Francis R.C. The effects of bidirectional selection for social dominance on agonistic behavior and sex ratios in the paradise fish (Macropodus opercularis). Behaviour 1984, 90:25-45.
40. Francis R.C. Temperament in a fish: a longitudinal study of the development of individual differences in aggression and social rank in the Midas cichlid. Ethology 1990, 86:311-325.
41. Francis R.C., Barlow G.W. Social control of primary sex differentiation in the Midas cichlid. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10673-10675.
42. Friesen C.N., Aubin-Horth N., Chapman L.J. The effect of hypoxia on sex hormones in an African cichlid Pseudocrenilabrus multicolor victoriae. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2012, 162:22-30.
43. Fuzzen M.L.M., Alderman S.L., Bristow E.N., Bernier N.J. Ontogeny of the corticotropin-releasing factor system in rainbow trout and differential effects of hypoxia on the endocrine and cellular stress responses during development. Gen. Comp. Endocrinol. 2011, 170:604-612.
44. Gardner L., Anderson T., Place A.R., Elizur A. Sex change strategy and the aromatase genes. Fish Physiol. Biochem. 2003, 28:147-148.
45. Greenwood A.K., Butler P.C., White R.B., DeMarco U., Pearce D., Fernald R.D. Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. Endocrinology 2003, 144:4226-4236.
46. Guiguen Y. Implications of steroids in fish gonadal sex differentiation and sex inversion. Curr. Top. Steroid Res. 2000, 3:127-143.
47. Guiguen Y., Fostier A., Piferrer F., Chang C.F. Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen. Comp. Endocrinol. 2010, 165:352-366.
48. Hattori R.S., Fernandino J.I., Kishii A., Kimura H., Kinno T., Oura M., et al. Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination?. PLoS One 2009, 4:e6548.
49. Hattori R.S., Gould R.J., Fujioka T., Saito T., Kurita J., Strüssmann C.A., et al. Temperature-dependent sex determination in Hd-rR medaka Oryzias latipes: gender sensitivity, thermal threshold, critical period, and DMRT1 expression profile. Sex. Dev. 2007, 1:138-146.
50. Hattori R.S., Murai Y., Oura M., Masuda S., Majhi S.K., Sakamoto T., et al. A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2955-2959.
51. Hayashi Y., Kobira H., Yamaguchi T., Shiraishi E., Yazawa T., Hirai T., et al. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol. Reprod. Dev. 2010, 77:679-686.
52. Herrero P., Borrull F., Pocurull E., Marcé R.M. Determination of glucocorticoids in sewage and river waters by ultra-high performance liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 2012, 1224:19-26.
53. Hobbs J.P., Munday P.L., Jones G.P. Social induction of maturation and sex determination in a coral reef fish. Proc. Biol. Sci. 2004, 271:2109-2114.
54. Holmgren K. Effect of water temperature and growth variation on the sex ratio of experimentally reared eels. Ecol. Freshwater Fish 1996, 5:203-212.
55. Ijiri S., Kaneko H., Kobayashi T., Wang D.S., Sakai F., Paul-Prasanth B., et al. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 2008, 78:333-341.
56. Kamiya T., Kai W., Tasumi S., Oka A., Matsunaga T., Mizuno N., et al. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger Pufferfish, Takifugu rubripes (Fugu). PLoS Genet. 2012, 8:e1002798.
57. Kitano T., Takamune K., Kobayashi T., Nagahama Y., Abe S.I. 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. 1999, 23:167-176.
58. Kobayashi Y., Nagahama Y., Nakamura M. Diversity and plasticity of sex determination and differentiation in fishes. Sex. Dev. 2013, 7:115-125.
59. Koumoundouros G., Pavlidis M., Anezaki L., Kokkari C., Sterioti A., Divanach P., et al. Temperature sex determination in the European sea bass, Dicentrarchus labrax (L., 1758) (Teleostei, Perciformes, Moronidae): critical sensitive ontogenetic phase. J. Exp. Zool. 2002, 292:573-579.
60. Krueger W.H., Oliveira K. Evidence for environmental sex determination in the American eel, Anguilla rostrata. Environ. Biol. Fishes 1999, 55:381-389.
61. Kusakabe M., Nakamura I., Young G. 11beta-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. Endocrinology 2003, 144:2534-2545.
62. Lejeune P. The effect of local stock density on social behavior and sex change in the Mediterranean labrid Coris julis. Environ. Biol. Fishes 1987, 18:135-141.
63. Lokman P.M., Harris B., Kusakabe M., Kime D.E., Schulz R.W., Adachi S., et al. 11-Oxygenated androgens in female teleosts: prevalence, abundance, and life history implications. Gen. Comp. Endocrinol. 2002, 129:1-12.
64. Lu N.Z., Wardell S.E., Burnstein K.L., Defranco D., Fuller P.J., Giguere V., et al. International union of pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol. Rev. 2006, 58:782-797.
65. Luckenbach J.A., Godwin J., Daniels H.V., Borski R.J. Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma). Aquaculture 2003, 216:315-327.
66. Lutnesky M.M.F. Density-dependent protogynous sex change in territorial-haremic fishes: models and evidence. Behav. Ecol. 1994, 5:375-383.
67. Manabe H., Ishimura M., Shinomiya A., Sunobe T. Field evidence for bi-directional sex change in the polygynous gobiid fish Trimma okinawae. J. Fish Biol. 2007, 70:600-609.
68. Manabe H., Matsuoka M., Goto K., Dewa S.I., Shinomiya A., Sakurai M., et al. Bi-directional sex change in the gobiid fish Trimma sp.: does size-advantage exist?. Behaviour 2008, 145:99-113.
69. Matsuda M. Sex determination in fish: lessons from the sex-determining gene of the teleost medaka, Oryzias latipes. Dev. Growth Differ. 2003, 45:397-403.
70. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
71. Middaugh D.P., Hemmer M.J. Influence of environmental temperature on sex-ratios in the tidewater silverside, Menidia peninsulae (Pisces: Atherinidae). Copeia 1987, 1987:958-964.
72. Milla S., Wang N., Mandiki S.N.M., Kestemont P. Corticosteroids: friends or foes of teleost fish reproduction?. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 153:242-251.
73. Miura S., Horiguchi R., Nakamura M. Immunohistochemical evidence for 11beta-hydroxylase (P45011beta) and androgen production in the gonad during sex differentiation and in adults in the protandrous anemonefish Amphiprion clarkii. Zool. Sci. 2008, 25:212-219.
74. Mommsen T., Vijayan M.M., Moon T. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Fish Physiol. Biochem. 1999, 211-268.
75. Morohashi K., Baba T., Tanaka M. Steroid hormones and the development of reproductive organs. Sex. Dev. 2013, 7:61-79.
76. Nakamura M. The mechanism of sex determination in vertebrates-are sex steroids the key-factor?. J. Exp. Zool. A Ecol. Genet. Physiol. 2010, 313:381-398.
77. Nakamura S., Watakabe I., Nishimura T., Toyoda A., Taniguchi Y., Tanaka M. Analysis of medaka sox9 orthologue reveals a conserved role in germ cell maintenance. PLoS One 2012, 7:e29982.
78. Nanda I., Kondo M., Hornung U., Asakawa S., Winkler C., Shimizu A., et al. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11778-11783.
79. Navarro-Martin L., Vinas J., Ribas L., Diaz N., Gutierrez A., Di Croce L., et al. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet. 2011, 7:e1002447.
80. Oldfield R.G., McCrary J., McKaye K.R. Habitat use, social behavior, and female and male size distributions of juvenile midas cichlids, Amphilophus cf. citrinellus, in Lake Apoyo, Nicaragua. Caribb. J. Sci. 2006, 42:197-207.
81. Oppermann U.C.T., Persson B., Jörnvall H. The 11β-hydroxysteroid dehydrogenase system, a determinant of glucocorticoid and mineralocorticoid action. Eur. J. Biochem. 1997, 249:355-360.
82. Ospina-Álvarez N., Piferrer F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 2008, 3:e2837.
83. Ozaki Y., Higuchi M., Miura C., Yamaguchi S., Tozawa Y., Miura T. Roles of 11beta-hydroxysteroid dehydrogenase in fish spermatogenesis. Endocrinology 2006, 147:5139-5146.
84. Pavlidis M., Koumoundouros G., Sterioti A., Somarakis S., Divanach P., Kentouri M. Evidence of temperature-dependent sex determination in the european sea bass (Dicentrarchus labrax L.). J. Exp. Zool. 2000, 287:225-232.
85. Penman D.J., Piferrer F. Fish gonadogenesis. part I: genetic and environmental mechanisms of sex determination. Rev. Fisheries Sci. 2008, 16:14-32.
86. Perry A.N., Grober M.S. A model for social control of sex change: interactions of behavior, neuropeptides, glucocorticoids, and sex steroids. Horm. Behav. 2003, 43:31-38.
87. Piferrer F. Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 2001, 197:229-281.
88. Pollock M.S., Dubé M.G., Schryer R. Investigating the link between pulp mill effluent and endocrine disruption: Attempts to explain the presence of intersex fish in the Wabigoon River, Ontario. Can. Environ. Toxicol. Chem. 2010, 29:952-965.
89. Raghuveer K., Senthilkumaran B., Sudhakumari C.C., Sridevi P., Rajakumar A., Singh R., et al. Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sex. Dev. 2011, 5:213-223.
90. Römer U., Beisenherz W. Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). J. Fish Biol. 1996, 48:714-725.
91. Rubin D.A. Effect of pH on sex ratio in cichlids and a poeciliid (Teleostei). Copeia 1985, 1985:233-235.
92. Saito D., Morinaga C., Aoki Y., Nakamura S., Mitani H., Furutani-Seiki M., et al. Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai. Dev. Biol. 2007, 310:280-290.
93. Saito D., Tanaka M. Comparative aspects of gonadal sex differentiation in medaka: a conserved role of developing oocytes in sexual canalization. Sex. Dev. 2009, 3:99-107.
94. Sakamoto T., McCormick S.D. Prolactin and growth hormone in fish osmoregulation. Gen. Comp. Endocrinol. 2006, 147:24-30.
95. Salas-Leiton E., Coste O., Asensio E., Infante C., Cañavate J.P., Manchado M. Dexamethasone modulates expression of genes involved in the innate immune system, growth and stress and increases susceptibility to bacterial disease in Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol. 2012, 32:769-778.
96. Sandra G.E., Norma M.M. Sexual determination and differentiation in teleost fish. Rev. Fish Biol. Fish. 2010, 20:101-121.
97. Sarre S.D., Georges A., Quinn A. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 2004, 26:639-645.
98. Schaaf M.J., Chatzopoulou A., Spaink H.P. The zebrafish as a model system for glucocorticoid receptor research. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 153:75-82.
99. Schreck C.B. Stress and fish reproduction: the roles of allostasis and hormesis. Gen. Comp. Endocrinol. 2010, 165:549-556.
100. Selim K.M., Shinomiya A., Otake H., Hamaguchi S., Sakaizumi M. Effects of high temperature on sex differentiation and germ cell population in medaka, Oryzias latipes. Aquaculture 2009, 289:340-349.
101. Shang E.H.H., Wu R.S.S. Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ. Sci. Technol. 2004, 38:4763-4767.
102. Shang E.H.H., Yu R.M.K., Wu R.S.S. Hypoxia affects sex differentiation and development leading to a male-dominated population in zebrafish (Danio rerio). Environ. Sci. Technol. 2006, 40:3118-3122.
103. Shinoda T., Miranda L.A., Okuma K., Hattori R.S., Fernandino J.I., Yoshizaki G., et al. Molecular cloning and expression analysis of Fshr and Lhr in relation to Fshb and Lhb subunits during the period of temperature-dependent sex determination in pejerrey Odontesthes bonariensis. Mol. Reprod. Dev. 2010, 77:521-532.
104. Socorro S., Martins R.S., Deloffre L., Mylonas C.C., Canario A.V.M. A cDNA for European sea bass (Dicentrachus labrax) 11β-hydroxylase: Gene expression during the thermosensitive period and gonadogenesis. Gen. Comp. Endocrinol. 2007, 150:164-173.
105. Stavreva D.A., George A.A., Klausmeyer P., Varticovski L., Sack D., Voss T.C., et al. Prevalent glucocorticoid and androgen activity in US water sources. Sci. Rep. 2012, 2:937.
106. Strüssmann C., Karube M., Miranda L.A., Patiño R., Somoza G., Uchida D., et al. Methods of sex control in fishes and an overview of novel hypotheses concerning the mechanisms of sex differentiation. Fish Genetics and Aquaculture Biotechnology 2004, 65-79. Oxford & IBH Publishing/Science Publishers, New Delhi, India/Enfield, USA. T. Pandian, C.A. Strüssmann, M.P. Marian (Eds.).
107. Strüssmann C.A., Calsina Cota J.C., Phonlor G., Higuchi H., Takashima F. Temperature effects on sex differentiation of two South American atherinids, Odontesthes argentinensis and Patagonina hatcheri. Environ. Biol. Fish 1996, 47:143-154.
108. Strüssmann C.A., Conover D.O., Somoza G.M., Miranda L.A. Implications of climate change for the reproductive capacity and survival of Atherinopsid fish species. J. Fish Biol. 2010, 77:1818-1834.
109. Strüssmann C.A., Kitahara A., Yamashita M. Role of apoptosis in temperature-dependent sex determination of pejerrey Odontesthes bonariensis. Cybium 2008, 32:77-79.
110. Strüssmann C.A., Nakamura M. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol. Biochem. 2002, 26:13-29.
111. Strüssmann C.A., Saito T., Usui M., Yamada H., Takashima F. Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J. Exp. Zool. 1997, 278:167-177.
112. Sunobe T., Nakazono A. Sex change in both directions by alteration of social dominance in Trimma okinawae (Pisces: Gobiidae). Ethology 1993, 94:339-345.
113. Tanaka M., Saito D., Morinaga C., Kurokawa H. 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. 2008, 50:273-278.
114. Tesone M., Charreau E.H. Steroid biosynthesis in the gonads of the teleost fish Jenynsia lineata. Comp. Biochem. Physiol. 1980, 65:631-637.
115. Tessema M., Müller-Belecke A., Hörstgen-Schwark G. Effect of rearing temperatures on the sex ratios of Oreochromis niloticus populations. Aquaculture 2006, 258:270-277.
116. Thomas P., Rahman M.S. Extensive reproductive disruption, ovarian masculinization and aromatase suppression in Atlantic croaker in the northern Gulf of Mexico hypoxic zone. Proc. Biol. Sci. 2012, 279:28-38.
117. Tzchori I., Degani G., Hurvitz A., Moav B. Cloning and developmental expression of the cytochrome P450 aromatase gene (CYP19) in the European eel (Anguilla anguilla). Gen. Comp. Endocrinol. 2004, 138:271-280.
118. Uchida D., Yamashita M., Kitano T., Iguchi T. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol. 2002, 205:711-718.
119. Uchida D., Yamashita M., Kitano T., Iguchi T. 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. 2004, 137:11-20.
120. Valenzuela N., Adams D.C., Janzen F.J. Pattern does not equal process: Exactly when is sex environmentally determined?. Am. Nat. 2003, 161:676-683.
121. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R., Lee D.-H., et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endoc. Rev. 2012, 33:378-455.
122. Vijayan M.M., Reddy P.K., Leatherland J.F., Moon T.W. The effects of cortisol on hepatocyte metabolism in rainbow trout: a study using the steroid analogue RU486. Gen. Comp. Endocrinol. 1994, 96:75-84.
123. Villamizar N., Ribas L., Piferrer F., Vera L.M., Sánchez-Vázquez F.J. Impact of daily thermocycles on hatching rhythms, larval performance and sex differentiation of zebrafish. PLoS One 2012, 7:e52153.
124. 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.
125. Volff J.N., Kondo M., Schartl M. Medaka dmY/dmrt1Y is not the universal primary sex-determining gene in fish. Trends Genet. 2003, 19:196-199.
126. Wendelaar Bonga S.E. The stress response in fish. Physiol. Rev. 1997, 77:591-625.
127. Wernerus F.M., Tessari V. The influence of population density on the mating system of Thalassoma pavo, a protogynous Mediterranean labrid fish. Mar. Ecol. 1991, 12:361-368.
128. Wessels S., Hörstgen-Schwark G. Selection experiments to increase the proportion of males in Nile tilapia (Oreochromis niloticus) by means of temperature treatment. Aquaculture 2007, 272:S80-S87.
129. Wu G.-C., Tomy S., Lee M.-F., Lee Y.-H., Yueh W.-S., Lin C.-J., et al. Sex differentiation and sex change in the protandrous black porgy, Acanthopagrus schlegeli. Gen. Comp. Endocrinol. 2010, 167:417-421.
130. Wu R.S.S., Zhou B.S., Randall D.J., Woo N.Y.S., Lam P.K.S. Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ. Sci. Technol. 2003, 37:1137-1141.
131. Yamaguchi T., Kitano T. High temperature induces cyp26b1 mRNA expression and delays meiotic initiation of germ cells by increasing cortisol levels during gonadal sex differentiation in Japanese flounder. Biochem. Biophys. Res. Commun. 2012, 419:287-292.
132. Yamaguchi T., Yoshinaga N., Yazawa T., Gen K., Kitano T. Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 2010, 151:3900-3908.
133. Yamamoto T. Sex differentiation. Fish Physiol. A 1969, 9:117-372.
134. Yano A., Guyomard R., Nicol B., Jouanno E., Quillet E., Klopp C., et al. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 2012, 22:1423-1428.
135. Yaron Z. Endocrine control of gametogenesis and spawning induction in the carp. Aquaculture 1995, 129:49-73.
136. Yu R.M.K., Chu D.L.H., Tan T.F., Li V.W.T., Chan A.K.Y., Giesy J.P., et al. Leptin-mediated modulation of steroidogenic gene expression in hypoxic zebrafish embryos: Implications for the disruption of sex steroids. Environ. Sci. Technol. 2012, 46:9112-9119.