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Regulation of zebrafish gonadal sex differentiation

Biology, The Life Science Center, School of Science and Technology, Örebro University, Örebro 70282, Sweden

While the master regulator gene Sry on the mammalian Y chromosome controls the switch for initiating male sex differentiation, many other species rely on environmental factors for gonadal sex differentiation. Yet other species, like zebrafish, appears to rely on a multitude of genetic cues for gonadal sex differentiation. Zebrafish gonadal differentiation initiates with the onset of a juvenile ovary stage and depending on the influence of unknown genetic factors either maintains oocyte development or initiate apoptotic processes to override the female differentiation pathway. In this review, we explore the role of different factors and genes that have been reported to influence zebrafish gonadal sex differentiation. We also give a brief insight of primordial germ cell (PGC) involvement in shaping male and female signaling pathway in gonadal development.
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References

1. Dooley K, Zon LI (2000) Zebrafish: a model system for the study of human disease. Curr Opin Genet Dev 10: 252-256.    

2. Goldsmith JR, Jobin C (2012) Think Small: Zebrafish as a Model System of Human Pathology. J Biomed Biotechnol 2012: 817341.

3. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8: 353-367.    

4. Mandrekar N, Thakur NL (2009) Significance of the zebrafish model in the discovery of bioactive molecules from nature. Biotechnol Lett 31: 171-179.    

5. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4: 35-44.    

6. Skakkebaek NE, Jorgensen N, Main KM, et al. (2006) Is human fecundity declining? Int J Androl 29: 2-11.    

7. Dumesic DA, Abbott DH, Padmanabhan V (2007) Polycystic ovary syndrome and its developmental origins. Rev Endocr Metab Disord 8: 127-141.    

8. van der Zwan YG, Biermann K, Wolffenbuttel KP, et al. (2014) Gonadal Maldevelopment as Risk Factor for Germ Cell Cancer: Towards a Clinical Decision Model. Eur Urol 67: 692-701.

9. Wilhelm D, Palmer S, Koopman P (2007) Sex determination and gonadal development in mammals. Physiol Rev 87: 1-28.    

10. Angelopoulou R, Lavranos G, Manolakou P (2012) Sex determination strategies in 2012: towards a common regulatory model? Reprod Biol Endocrinol 10: 13.    

11. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364.

12. Liew WC, Bartfai R, Lim Z, et al. (2012) Polygenic sex determination system in zebrafish. PLoS One 7: e34397.    

13. Liew WC, Orban L (2013) Zebrafish sex: a complicated affair. Brief Funct Genom 13: 172-187.

14. Ser JR, Roberts RB, Kocher TD (2010) Multiple interacting loci control sex determination in lake Malawi cichlid fish. Evolution 64: 486-501.    

15. Vandeputte M, Dupont-Nivet M, Chavanne H, et al. (2007) A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176: 1049-1057.

16. Matsuda M, Nagahama Y, Shinomiya A, et al. (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559-563.    

17. Barske LA, Capel B (2008) Blurring the edges in vertebrate sex determination. Curr Opin Genet Dev 18: 499-505.    

18. Sato E, Endo T, Yamahira K, et al. (2005) Induction of female-to-male sex reversal by high temperature treatment in Medaka, Oryzias latipes. Zoolog Sci 22: 985-988.    

19. Ospina-Alvarez N, Piferrer F (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.    

20. Takahashi H (1977) Juvenile Hermaphroditism in the Zebrafish, Brachydanio rerio. Bull Fac Fish Hokkaido Univ 28: 57-65.

21. Wang XG, Bartfai R, Sleptsova-Freidrich I, et al. (2007) The timing and extent of 'juvenile ovary' phase are highly variable during zebrafish testis differentiation. J Fish Biol 70: 33-44.    

22. Siegfried KR, Nusslein-Volhard C (2008) Germ line control of female sex determination in zebrafish. Dev Biol 324: 277-287.    

23. Luzio A, Monteiro SM, Garcia-Santos S, et al. (2015) Zebrafish sex differentiation and gonad development after exposure to 17alpha-ethinylestradiol, fadrozole and their binary mixture: A stereological study. Aquat Toxicol 166: 83-95.    

24. Uchida D, Yamashita M, Kitano T, et al. (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205: 711-718.

25. Pradhan A, Khalaf H, Ochsner SA, et al. (2012) Activation of NF-kappaB protein prevents the transition from juvenile ovary to testis and promotes ovarian development in zebrafish. J Biol Chem 287: 37926-37938.    

26. Sola L, Gornung E (2001) Classical and molecular cytogenetics of the zebrafish, Danio rerio (Cyprinidae, Cypriniformes): an overview. Genetica 111: 397-412.    

27. Wallace B-M, Wallace H (2003) Synaptonemal complex karyotype of zebrafish. Heredity 90: 136-140.    

28. Traut W, Winking H (2001) Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platypus and guppy. Chromosome Res 9: 659-672.    

29. Phillips RB, Reed KM (2000) Localization of repetitive DNAs to zebrafish (Danio rerio) chromosomes by fluorescence in situ hybridization (FISH). Chromosome Res 8: 27-35.    

30. Singer A, Perlman H, Yan Y, et al. (2002) Sex-specific recombination rates in zebrafish (Danio rerio). Genetics 160: 649-657.

31. Tong SK, Hsu HJ, Chung BC (2010) Zebrafish monosex population reveals female dominance in sex determination and earliest events of gonad differentiation. Dev Biol 344: 849-856.    

32. Sharma KK, Sharma OP, Tripathi NK (1998) Female heterogamety in Danio rerio (Cypriniformes: Cyprinidae). Proc Natl Acad Sci India Sect B 68: 123-126.

33. Wilson CA, High SK, McCluskey BM, et al. (2014) Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198: 1291-1308.    

34. Shang EH, Yu RM, Wu RS (2006) Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ Sci Technol 40: 3118-3122.    

35. Villamizar N, Ribas L, Piferrer F, et al. (2012) Impact of daily thermocycles on hatching rhythms, larval performance and sex differentiation of zebrafish. PLoS One 7: e52153.    

36. Luzio A, Santos D, Fontainhas-Fernandes AA, et al. (2016) Effects of 17alpha-ethinylestradiol at different water temperatures on zebrafish sex differentiation and gonad development. Aquat Toxicol 174: 22-35.    

37. Bradley KM, Breyer JP, Melville DB, et al. (2011) An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda) 1: 3-9.    

38. Anderson JL, Rodriguez Mari A, Braasch I, et al. (2012) Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS One 7: e40701.    

39. Mishima Y, Giraldez AJ, Takeda Y, et al. (2006) Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr Biol 16: 2135-2142.    

40. Staton AA, Knaut H, Giraldez AJ (2011) miRNA regulation of Sdf1 chemokine signaling provides genetic robustness to germ cell migration. Nat Genet 43: 204-211.    

41. von Hofsten J, Olsson PE (2005) Zebrafish sex determination and differentiation: involvement of FTZ-F1 genes. Reprod Biol Endocrinol 3: 63.    

42. Orban L, Sreenivasan R, Olsson PE (2009) Long and winding roads: testis differentiation in zebrafish. Mol Cell Endocrinol 312: 35-41.    

43. Rodriguez-Mari A, Yan YL, Bremiller RA, et al. (2005) Characterization and expression pattern of zebrafish Anti-Mullerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 5: 655-667.

44. Luzio A, Coimbra AM, Benito C, et al. (2015) Screening and identification of potential sex-associated sequences in Danio rerio. Mol Reprod Dev 82: 756-764.    

45. Sim H, Argentaro A, Harley VR (2008) Boys, girls and shuttling of SRY and SOX9. Trends Endocrinol Metab 19: 213-222.    

46. Biason-Lauber A (2010) Control of sex development. Best Pract Res Clin Endocrinol Metab 24: 163-186.    

47. Koopman P (2005) Sex determination: a tale of two Sox genes. Trends Genet 21: 367-370.    

48. Sekido R, Lovell-Badge R (2009) Sex determination and SRY: down to a wink and a nudge? Trends Genet 25: 19-29.    

49. Ross AJ, Capel B (2005) Signaling at the crossroads of gonad development. Trends Endocrinol Metab 16: 19-25.    

50. Jakob S, Lovell-Badge R (2011) Sex determination and the control of Sox9 expression in mammals. FEBS J 278: 1002-1009.    

51. Kocer A, Reichmann J, Best D, et al. (2009) Germ cell sex determination in mammals. Mol Hum Reprod 15: 205-213.    

52. Sreenivasan R, Cai M, Bartfai R, et al. (2008) Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the zebrafish gonad and brain. PLoS One 3: e1791.    

53. Jorgensen A, Morthorst JE, Andersen O, et al. (2008) Expression profiles for six zebrafish genes during gonadal sex differentiation. Reprod Biol Endocrinol 6: 25.    

54. Bowles J, Feng CW, Spiller C, et al. (2010) FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev Cell 19: 440-449.    

55. Jameson SA, Lin YT, Capel B (2012) Testis development requires the repression of Wnt4 by Fgf signaling. Dev Biol 370: 24-32.    

56. Colvin JS, Green RP, Schmahl J, et al. (2001) Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104: 875-889.    

57. Lasala C, Carre-Eusebe D, Picard JY, et al. (2004) Subcellular and molecular mechanisms regulating anti-Mullerian hormone gene expression in mammalian and nonmammalian species. DNA Cell Biol 23: 572-585.    

58. Lourenco D, Brauner R, Rybczynska M, et al. (2011) Loss-of-function mutation in GATA4 causes anomalies of human testicular development. Proc Natl Acad Sci U S A 108: 1597-1602.    

59. Miyamoto Y, Taniguchi H, Hamel F, et al. (2008) A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol Biol 9: 44.    

60. Hattori RS, Murai Y, Oura M, et al. (2012) A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 109: 2955-2959.    

61. Wang XG, Orban L (2007) Anti-Mullerian hormone and 11 beta-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males. Dev Dyn 236: 1329-1338.    

62. Kluver N, Pfennig F, Pala I, et al. (2007) Differential expression of anti-Mullerian hormone (amh) and anti-Mullerian hormone receptor type II (amhrII) in the teleost medaka. Dev Dyn 236: 271-281.    

63. Kamiya T, Kai W, Tasumi S, et al. (2012) A Trans-Species Missense SNP in Amhr2 Is Associated with Sex Determination in the Tiger Pufferfish, Takifugu rubripes (Fugu). PLoS Genet 8: e1002798.

64. Pradhan A, Olsson PE (2014) Juvenile Ovary to Testis Transition in Zebrafish Involves Inhibition of Ptges. Biol Reprod 91: 33.    

65. Sreenivasan R, Jiang J, Wang X, et al. (2013) Gonad Differentiation in Zebrafish Is Regulated by the Canonical Wnt Signaling Pathway. Biol Reprod 90: 45.

66. Kazanskaya O, Glinka A, del Barco Barrantes I, et al. (2004) R-Spondin2 is a secreted activator of Wnt/beta-catenin signaling and is required for Xenopus myogenesis. Dev Cell 7: 525-534.    

67. Jin YR, Yoon JK (2012) The R-spondin family of proteins: emerging regulators of WNT signaling. Int J Biochem Cell Biol 44: 2278-2287.    

68. Zhang Y, Li F, Sun D, et al. (2011) Molecular analysis shows differential expression of R-spondin1 in zebrafish (Danio rerio) gonads. Mol Biol Rep 38: 275-282.    

69. Smith CA, Shoemaker CM, Roeszler KN, et al. (2008) Cloning and expression of R-Spondin1 in different vertebrates suggests a conserved role in ovarian development. BMC Dev Biol 8: 72.    

70. Yoon JK, Lee JS (2012) Cellular signaling and biological functions of R-spondins. Cell Signal 24: 369-377.    

71. Eisinger AL, Nadauld LD, Shelton DN, et al. (2007) Retinoic acid inhibits beta-catenin through suppression of Cox-2: a role for truncated adenomatous polyposis coli. J Biol Chem 282: 29394-29400.    

72. Goessling W, North TE, Loewer S, et al. (2009) Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 136: 1136-1147.    

73. Pannetier M, Fabre S, Batista F, et al. (2006) FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 36: 399-413.    

74. Fleming NI, Knower KC, Lazarus KA, et al. (2010) Aromatase Is a Direct Target of FOXL2: C134W in Granulosa Cell Tumors via a Single Highly Conserved Binding Site in the Ovarian Specific Promoter. PLoS One 5: e14389.    

75. Nef S, Vassalli JD (2009) Complementary pathways in mammalian female sex determination. J Biol 8: 74.    

76. Guiguen Y, Fostier A, Piferrer F, et al. (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165: 352-366.    

77. Fenske M, Segner H (2004) Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat Toxicol 67: 105-126.    

78. Takatsu K, Miyaoku K, Roy SR, et al. (2013) Induction of female-to-male sex change in adult zebrafish by aromatase inhibitor treatment. Sci Rep 3: 3400.

79. Brion F, Tyler CR, Palazzi X, et al. (2004) Impacts of 17beta-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat Toxicol 68: 193-217.    

80. Orn S, Holbech H, Norrgren L (2016) Sexual disruption in zebrafish (Danio rerio) exposed to mixtures of 17alpha-ethinylestradiol and 17beta-trenbolone. Environ Toxicol Pharmacol 41: 225-231.    

81. Schulz RW, Bogerd J, Male R, et al. (2007) Estrogen-induced alterations in amh and dmrt1 expression signal for disruption in male sexual development in the zebrafish. Environ Sci Technol 41: 6305-6310.

82. Reyhanian Caspillo N, Volkova K, Hallgren S, et al. (2014) Short-term treatment of adult male zebrafish (Danio Rerio) with 17alpha-ethinyl estradiol affects the transcription of genes involved in development and male sex differentiation. Comp Biochem Physiol C Toxicol Pharmacol 164: 35-42.    

83. Lor Y, Revak A, Weigand J, et al. (2015) Juvenile exposure to vinclozolin shifts sex ratios and impairs reproductive capacity of zebrafish. Reprod Toxicol 58: 111-118.    

84. Baumann L, Knorr S, Keiter S, et al. (2014) Persistence of endocrine disruption in zebrafish (Danio rerio) after discontinued exposure to the androgen 17beta-trenbolone. Environ Toxicol Chem 33: 2488-2496.    

85. Mukhi S, Torres L, Patino R (2007) Effects of larval-juvenile treatment with perchlorate and co-treatment with thyroxine on zebrafish sex ratios. Gen Comp Endocrinol 150: 486-494.    

86. Sharma P, Tang S, Mayer GD, et al. (2016) Effects of thyroid endocrine manipulation on sex-related gene expression and population sex ratios in Zebrafish. Gen Comp Endocrinol 235: 38-47.    

87. Sharma P, Patino R (2013) Regulation of gonadal sex ratios and pubertal development by the thyroid endocrine system in zebrafish (Danio rerio). Gen Comp Endocrinol 184: 111-119.    

88. Aggarwal BB, Sethi G, Nair A, et al. (2006) Nuclear factor- κB: A holy grail in cancer prevention and therapy. Curr Signal Transduct Ther 1: 25-52.    

89. Li X, Stark GR (2002) NF-κB-dependent signaling pathways. Exp Hematol 30: 285-296.    

90. Ghosh S, May MM, Kopp EB (1998) NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225-260.    

91. Siebenlist U, Franzoso G, Brown K (1994) Structure, regulation and function of NF-κB. Annu Rev Cell Biol 10: 405-455.

92. Xiao W (2004) Advances in NF-kappaB signaling transduction and transcription. Cell Mol Immunol 1: 425-435.

93. Beg AA, Baldwin AS (1993) The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev 7: 2064-2070.    

94. Ghosh S, Karin M (2002) Missing pieces in the NFkB puzzle. Cell Metab 109: 81-96.

95. Beg AA, Finco TS, Nantermet PV, et al. (1993) Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol Cell Biol 13: 3301-3310.    

96. Finco TS, Beg AA, Baldwin AS Jr (1994) Inducible phosphorylation of I kappa B alpha is not sufficient for its dissociation from NF-kappa B and is inhibited by protease inhibitors. Proc Natl Acad Sci U S A 91: 11884-11888.    

97. Shishodia S, Aggarwal BB (2002) Nuclear factor-κB activation: A question of life or death. J Biochem Mol Biol 35: 28-40.    

98. Rao NA, McCalman MT, Moulos P, et al. (2011) Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res 21: 1404-1416.    

99. Palvimo JJ, Reinikainen P, Ikonen T, et al. (1996) Mutual transcriptional interference between RelA and androgen receptor. J Biol Chem 271: 24151–24156.

100. McKay LI, Cidlowski JA (1998) Cross-talk between Nuclear factor-kB and the steroid hormone receptors: Mechanisms of mutual antagonism. Mol Endocrinol 12: 45-56.    

101. Delfino F, Walker WH (1998) Stage-specific nuclear expression of NF-κB in mammalian testis. Mol Endocrinol 12: 1696-1707.

102. Hong CY, Park JH, Seo KH, et al. (2003) Expression of MIS in the Testis Is Downregulated by Tumor Necrosis Factor Alpha through the Negative Regulation of SF-1 Transactivation by NF-κB. Mol Cell Biol 23: 6000-6012.    

103. Sobolewski C, Cerella C, Dicato M, et al. (2010) The role of cyclooxygenase-2 in cell proliferation and cell death in human malignancies. Int J Cell Biol 2010: 215158.

104. Simmons DL, Botting RM, Hla T (2004) Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56: 387-437.    

105. Kang YJ, Mbonye UR, DeLong CJ, et al. (2007) Regulation of intracellular cyclooxygenase levels by gene transcription and protein degradation. Prog Lipid Res 46: 108-125.    

106. Morita I (2002) Distinct functions of COX-1 and COX-2. Prostaglandins Other Lipid Mediat 68-69: 165-175.    

107. Tanabe T, Tohnai N (2002) Cyclooxygenase isozymes and their gene structures and expression. 68-69: 95-114.

108. Klein T, Shephard P, Kleinert H, et al. (2007) Regulation of cyclooxygenase-2 expression by cyclic AMP. Biochim Biophys Acta 1773: 1605-1618.    

109. Schmedtje JF, Ji YS, Liu RN, et al. (1997) Hypoxia induces cyclooxygenase-2 via the NF-kB p65 transcription factor in human vascular endothelial cells. J Biol Chem 272: 601-608.    

110. Tsatsanis C, Androulidaki A, Venihaki M, et al. (2006) Signalling networks regulating cyclooxygenase-2. Int J Biochem Cell Biol 38: 1654-1661.    

111. Poligone B, Baldwin AS (2001) Positive and negative regulation of NF-kappaB by COX-2: roles of different prostaglandins. J Biol Chem 276: 38658-38664.    

112. Grosser T, Yusuff S, Cheskis E, et al. (2002) Developmental expression of functional cyclooxygenases in zebrafish. Proc Natl Acad Sci U S A 99: 8418-8423.    

113. Adams IR, McLaren A (2002) Sexually dimorphic devlopment of mouse primordial germ cells: switch from oogenesis to spermatogenesis. Development 129: 1155-1164.

114. Wilhelm D, Hiramatsu R, Mizusaki H, et al. (2007) SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 282: 10553-10560.    

115. Breyer RM, Bagdassarian CK, Myers SA, et al. (2001) Prostanoid receptors: subtypes and signaling. Annu Rev Pharmacol Toxicol 41: 661-690.    

116. Cai Z, Kwintkiewicz J, Young ME, et al. (2007) Prostaglandin E2 increases Cyp19 expression in Rat Granulosa Cells: Implication of GATA-4. Mol Cell Endocrinol 263: 181-189.    

117. Guan Y, Zhang Y, Schneider A, et al. (2001) Urogenital distribution of a mouse membrane-associated prostaglandin E2 synthase. Am J Physiol Renal Physiol 281: 1173-1177.    

118. Sun T, Deng WB, Diao HL, et al. (2006) Differential expression and regulation of prostaglandin E synthases in the mouse ovary during sexual maturation and luteal development. J Endocrinol 189: 89-101.    

119. Bayne RA, Eddie SL, Collins CS, et al. (2009) Prostaglandin E2 as a regulator of germ cells during ovarian development. J Clin Endocrinol Metab 94: 4053-4060.    

120. Takahashi T, Morrow JD, Wang H, et al. (2006) Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem 281: 37117-37129.    

121. Mank JE, Promislow DEL, Avise JC (2006) Evolution of alternative sex-determining mechanisms in teleost fishes. Biol J Linn Soc 87: 83-93.    

122. Slanchev K, Stebler J, de la Cueva-Mendez G, et al. (2005) Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci U S A 102: 4074-4079.    

123. Kurokawa H, Saito D, Nakamura S, et al. (2007) Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci U S A 104: 16958-16963.    

124. Tzung KW, Goto R, Saju JM, et al. (2014) Early Depletion of Primordial Germ Cells in Zebrafish Promotes Testis Formation. Stem Cell Rep 4: 61-73.

125. McLaren A (2003) Primordial germ cells in the mouse. Dev Biol 262: 1-15.    

126. DiNapoli L, Capel B (2007) Germ cell depletion does not alter the morphogenesis of the fetal testis or ovary in the red-eared slider turtle (Trachemys scripta). J Exp Zool B Mol Dev Evol 308: 236-241.

127. Goto R, Saito T, Takeda T, et al. (2012) Germ cells are not the primary factor for sexual fate determination in goldfish. Dev Biol 370: 98-109.    

128. Fujimoto T, Nishimura T, Goto-Kazeto R, et al. (2010) Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish. Proc Natl Acad Sci U S A 107: 17211-17216.    

129. Petersen AM, Earp NC, Redmond ME, et al. (2016) Perchlorate Exposure Reduces Primordial Germ Cell Number in Female Threespine Stickleback. PLoS One 11: e0157792.    

130. Dranow DB, Tucker RP, Draper BW (2013) Germ cells are required to maintain a stable sexual phenotype in adult zebrafish. Dev Biol 376: 43-50.    

131. Rodriguez-Mari A, Canestro C, Bremiller RA, et al. (2010) Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet 6: e1001034.    

132. Rios-Rojas C, Bowles J, Koopman P (2015) On the role of germ cells in mammalian gonad development: quiet passengers or back-seat drivers? Reproduction 149: R181-191.    

133. Behringer RR, Cate RL, Froelick GJ, et al. (1990) Abnormal sexual development in transgenic mice chronically expressing mullerian inhibiting substance. Nature 345: 167-170.    

134. Couse JF, Hewitt SC, Bunch DO, et al. (1999) Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 286: 2328-2331.    

135. Maatouk DM, Mork L, Hinson A, et al. (2012) Germ cells are not required to establish the female pathway in mouse fetal gonads. PLoS One 7: e47238.    

136. Molyneaux K, Wylie C (2004) Primordial germ cell migration. Int J Dev Biol 48: 537-544.    

137. Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4: 59-66.

138. Kashimada K, Svingen T, Feng CW, et al. (2011) Antagonistic regulation of Cyp26b1 by transcription factors SOX9/SF1 and FOXL2 during gonadal development in mice. FASEB J 25: 3561-3569.    

139. Bowles J, Knight D, Smith C, et al. (2006) Retinoid signaling determines germ cell fate in mice. Science 312: 596-600.    

140. Koubova J, Menke DB, Zhou Q, et al. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci U S A 103: 2474-2479.    

141. Moniot B, Ujjan S, Champagne J, et al. (2014) Prostaglandin D2 acts through the Dp2 receptor to influence male germ cell differentiation in the foetal mouse testis. Development 141: 3561-3571.    

142. Kipp JL, Golebiowski A, Rodriguez G, et al. (2011) Gene expression profiling reveals Cyp26b1 to be an activin regulated gene involved in ovarian granulosa cell proliferation. Endocrinology 152: 303-312.    

143. Pradhan A, Olsson PE (2015) Inhibition of retinoic acid synthesis disrupts spermatogenesis and fecundity in zebrafish. Gen Comp Endocrinol 217-218: 81-91.    

144. Alsop D, Matsumoto J, Brown S, et al. (2008) Retinoid requirements in the reproduction of zebrafish. Gen Comp Endocrinol 156: 51-62.    

145. Rodriguez-Mari A, Canestro C, BreMiller RA, et al. (2013) Retinoic acid metabolic genes, meiosis, and gonadal sex differentiation in zebrafish. PLoS One 8: e73951.    

146. Azziz R, Marin C, Hoq L, et al. (2005) Health care-related economic burden of the polycystic ovary syndrome during the reproductive life span. J Clin Endocrinol Metab 90: 4650-4658.    

147. Agrawal R, Sharma S, Bekir J, et al. (2004) Prevalence of polycystic ovaries and polycystic ovary syndrome in lesbian women compared with heterosexual women. Fertil Steril 82: 1352-1357.    

148. Abbott DH, Barnett DK, Bruns CM, et al. (2005) Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Hum Reprod Update 11: 357-374.    

149. Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16: 972-978.    

150. Juul A, Almstrup K, Andersson AM, et al. (2014) Possible fetal determinants of male infertility. Nat Rev Endocrinol 10: 553-562.    

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