MACHO OU FÊMEA? COMO O SEXO DOS VERTEBRADOS É DETERMINADO.
DOI:
https://doi.org/10.35172/rvz.2021.v28.573Palavras-chave:
Determinação e diferenciação sexual, desenvolvimento gonadal, gônada, genes, peixes.Resumo
A reprodução sexual é a forma de propagação mais antiga e universal utilizada pelos vertebrados. Os mecanismos que controlam a determinação e diferenciação sexual nestes animais são diversos e dependem de uma grande variedade de fatores genéticos bem como em alguns casos de fatores ambientais. O sexo genético pode ser definido por fatores genéticos hereditários que são determinados na fecundação. Por outro lado, a diferenciação gonadal depende da ativação de fatores transcricionais que são expressos durante a janela de diferenciação sexual. Tais fatores podem ter sua expressão alterada por condições ambientais como a temperatura e a osmolaridade dentre outros. Estes processos sexuais são classicamente divididos em determinação e diferenciação sexual, respectivamente. Baseados em tai fatos, esta revisão tem como objetivo mostrar a fundamentação básica dos processos de determinação e diferenciação sexual em vertebrados com ênfase no grupo dos peixes teleósteos.
Referências
1. von Hofsten J, Olsson PE. Zebrafish sex determination and differentiation: involvement of FTZ-F1 genes. Reprod Biol Endocrinol. 2005;3:63. doi: 10.1186/1477-7827-3-63.
2. Trukhina AV, Lukina NA, Wackerow-Kouzova ND, Smirnov AF. The variety of vertebrate mechanisms of sex determination. Biomed Res Int. 2013;2013:587460. doi: 10.1155/2013/587460.
3. Graves JA. How to evolve new vertebrate sex determining genes. Dev Dyn. 2013;242(4):354-9. doi: 10.1002/dvdy.23887.
4. Kikuchi K, Hamaguchi S. Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn. 2013;242(4):339-53. doi: 10.1002/dvdy.23927.
5. Herpin A, Adolfi MC, Nicol B, Hinzmann M, Schmidt C, Klughammer J, Engel M, Tanaka M, Guiguen Y, Schartl M. Divergent expression regulation of gonad development genes in medaka shows incomplete conservation of the downstream regulatory network of vertebrate sex determination. Mol Biol Evol. 2013;30(10):2328-46. doi: 10.1093/molbev/mst130.
6. Heule C, Salzburger W, Böhne A. Genetics of sexual development: an evolutionary playground for fish. Genetics. 2014;196(3):579-91. doi: 10.1534/genetics.114.16115.
7. Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002;208(3–4):191-364. doi:10.1016/S0044-8486(02)00057-1.
8. Graham P, Penn JK, Schedl P. Masters change, slaves remain. Bioessays. 2003;25(1):1-4. doi: 10.1002/bies.
9. Herpin A, Schartl M. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep. 2015;16(10):1260-74. doi: 10.15252/embr.201540667.
10. Munger SC, Capel B. Sex and the circuitry: progress toward a systems-level understanding of vertebrate sex determination. Wiley Interdiscip Rev Syst Biol Med. 2012;4(4):401-12. doi: 10.1002/wsbm.1172.
11. Koopman P. Sex determination: the power of DMRT1. Trends Genet. 2009;25(11):479-81. doi: 10.1016/j.tig.2009.09.009.
12. Capel B. Sex in the 90s: SRY and the switch to the male pathway. Annu Rev Physiol. 1998;60:497-523. doi: 10.1146/annurev.physiol.60.1.497.
13. Temel SG, Gulten T, Yakut T, Saglam H, Kilic N, Bausch E, Jin WJ, Leipoldt M, Scherer G. Extended pedigree with multiple cases of XX sex reversal in the absence of SRY and of a mutation at the SOX9 locus. Sex Dev. 2007;1(1):24-34. doi: 10.1159/000096236.
14. Nishioka M, Miura I, Saitoh K. Sex chromosomes of Rana rugosa with special reference to local differences in sex determining mechanism. Sci. Rep. Lab. Amphibian Biol. 1993;(12):55–8. doi:10.15027/14532.
15. Roco ÁS, Olmstead AW, Degitz SJ, Amano T, Zimmerman LB, Bullejos M. Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis. Proc Natl Acad Sci U S A. 2015;112(34):E4752-61. doi: 10.1073/pnas.1505291112.
16. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A. 2008;105(7):2469-74. doi: 10.1073/pnas.0712244105.
17. Nanda I, Zend-Ajusch E, Shan Z, Grützner F, Schartl M, Burt DW, Koehler M, Fowler VM, Goodwin G, Schneider WJ, Mizuno S, Dechant G, Haaf T, Schmid M. Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination. Cytogenet Cell Genet. 2000;89(1-2):67-78. doi: 10.1159/000015567.
18. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature. 2009;461(7261):267-71. doi: 10.1038/nature08298.
19. Ayers KL, Sinclair AH, Smith CA. The molecular genetics of ovarian differentiation in the avian model. Sex Dev. 2013;7(1-3):80-94. doi: 10.1159/000342358.
20. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature. 1998 ;391(6668):691-5. doi: 10.1038/35618. PMID: 9490411.
21. Huang S, Ye L, Chen H. Sex determination and maintenance: the role of DMRT1 and FOXL2. Asian J Androl. 2017;19(6):619-624. doi: 10.4103/1008-682X.194420.
22. Mello MP, Assumpção JG, Hackel C. Genes envolvidos na determinação e diferenciação do sexo. Arq. Bras. Endocrinol. Metab. 2005;(49):14-25. doi:10.1590/S0004-27302005000100004
23. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A. 2008;105(7):2469-74. doi: 10.1073/pnas.0712244105.
24. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre JJ, Bernot A, Laudet V, Guiguen Y. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta. 2000;1493(1-2):180-7. doi: 10.1016/s0167-4781(00)00186-x.
25. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod. 2008;78(2):333-41. doi: 10.1095/biolreprod.107.064246.
26. Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun. 2005;330(3):950-7. doi: 10.1016/j.bbrc.2005.03.066.
27. Webster KA, Schach U, Ordaz A, Steinfeld JS, Draper BW, Siegfried KR. Dmrt1 is necessary for male sexual development in zebrafish. Dev Biol. 2017;422(1):33-46. doi: 10.1016/j.ydbio.2016.12.008.
28. Lin Q, Mei J, Li Z, Zhang X, Zhou L, Gui JF. Distinct and Cooperative Roles of amh and dmrt1 in Self-Renewal and Differentiation of Male Germ Cells in Zebrafish. Genetics. 2017;207(3):1007-1022. doi: 10.1534/genetics.117.300274.
29. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 2002;417(6888):559-63. doi: 10.1038/nature751.
30. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. 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(18):11778-83. doi: 10.1073/pnas.182314699.
31. Kang Y, Guan GJ, Hong YH. Insights of sex determination and differentiation from medaka as a teleost model. Yi Chuan. 2017;39(6):441-454. doi: 10.16288/j.yczz.17-140.
32. Matsuda M, Matsuda C, Hamaguchi S, Sakaizumi M. Identification of the sex chromosomes of the medaka, Oryzias latipes, by fluorescence in situ hybridization. Cytogenet Cell Genet. 1998;82(3-4):257-62. doi: 10.1159/000015113.
33. Thorgaard GH. Heteromorphic sex chromosomes in male rainbow trout. Science. 1977;196(4292):900-2. doi: 10.1126/science.860122.
34. Iturra P, Lam N, de la Fuente M, Vergara N, Medrano JF. Characterization of sex chromosomes in rainbow trout and coho salmon using fluorescence in situ hybridization (FISH). Genetica. 2001;111(1-3):125-31. doi: 10.1023/a:1013725717142.
35. Baroiller JF, D'Cotta H, Saillant E. Environmental effects on fish sex determination and differentiation. Sex Dev. 2009;3(2-3):118-35. doi: 10.1159/000223077.
36. Mair GC, Scott AG, Penman DJ, Skibinski DO, Beardmore JA. Sex determination in the genus Oreochromis : 2. Sex reversal, hybridisation, gynogenesis and triploidy in O. aureus Steindachner. Theor Appl Genet. 1991;82(2):153-60. doi: 10.1007/BF00226206.
37. Volff JN, Schartl M. Variability of genetic sex determination in poeciliid fishes. Genetica. 2001;111(1-3):101-10. doi: 10.1023/a:1013795415808.
38. Schartl M. A comparative view on sex determination in medaka. Mech Dev. 2004;121(7-8):639-45. doi: 10.1016/j.mod.2004.03.001.
39. Adolfi MC, Nakajima RT, Nóbrega RH, Schartl M. Intersex, Hermaphroditism, and Gonadal Plasticity in Vertebrates: Evolution of the Müllerian Duct and Amh/Amhr2 Signaling. Annu Rev Anim Biosci. 2019;7:149-172. doi: 10.1146/annurev-animal-020518-114955.
40. Valenzuela N, Adams DC, Janzen FJ. Pattern does not equal process: exactly when is sex environmentally determined? Am Nat. 2003;161(4):676-83. doi: 10.1086/368292.
41. Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T, Hirai T, Kamei Y, Kitano T. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev. 2010;77(8):679-86. doi: 10.1002/mrd.21203.
42. 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(8):3900-8. doi: 10.1210/en.2010-0228.
43. Raz E. Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet. 2003;4(9):690-700. doi: 10.1038/nrg1154.
44. Raz E, Reichman-Fried M. Attraction rules: germ cell migration in zebrafish. Curr Opin Genet Dev. 2006;16(4):355-9. doi: 10.1016/j.gde.2006.06.007.
45. Guerrero-Estévez S, Moreno-Mendoza N. Sexual determination and differentiation in teleost fish. Rev Fish Biol Fisheries. 2010;(20):101–121. https://doi.org/10.1007/s11160-009-9123-4.
46. Kimble J, Page DC. The mysteries of sexual identity. The germ cell's perspective. Science. 2007;316(5823):400-1. doi: 10.1126/science.1142109.
47. Saito D, Morinaga C, Aoki Y, Nakamura S, Mitani H, Furutani-Seiki M, Kondoh H, Tanaka M. Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai. Dev Biol. 2007;310(2):280-90. doi: 10.1016/j.ydbio.2007.07.039.
48. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics. 2012;191(1):163-70. doi: 10.1534/genetics.111.137497.
49. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 2012;8(7):e1002798. doi: 10.1371/journal.pgen.1002798.
50. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A. 2012;109(8):2955-9. doi: 10.1073/pnas.1018392109.
51. Gautier A, Le Gac F, Lareyre JJ. The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene. 2011;472(1-2):7-17. doi: 10.1016/j.gene.2010.10.014.
52. Herpin A, Schartl M. Molecular mechanisms of sex determination and evolution of the Y-chromosome: insights from the medakafish (Oryzias latipes). Mol Cell Endocrinol. 2009;306(1-2):51-8. doi: 10.1016/j.mce.2009.02.004.
53. Nakamura S, Watakabe I, Nishimura T, Picard JY, Toyoda A, Taniguchi Y, di Clemente N, Tanaka M. Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development. 2012;139(13):2283-7. doi: 10.1242/dev.076307.
54. Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol. 2012;22(15):1423-8. doi: 10.1016/j.cub.2012.05.045.
55. Hattori RS, Somoza GM, Fernandino JI, Colautti DC, Miyoshi K, Gong Z, Yamamoto Y, Strüssmann CA. The Duplicated Y-specific amhy Gene Is Conserved and Linked to Maleness in Silversides of the Genus Odontesthes. Genes (Basel). 2019;10(9):679. doi: 10.3390/genes10090679.
56. Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N, Mitani H, Furutani-Seiki M, Tanaka M, Kondoh H. The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci U S A. 2007;104(23):9691-6. doi: 10.1073/pnas.0611379104.
57. Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Abe S, Kitano T. Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun. 2004;322(2):508-13. doi: 10.1016/j.bbrc.2004.07.162.
58. Rodríguez-Marí A, Yan YL, Bremiller RA, Wilson C, Cañestro C, Postlethwait JH. Characterization and expression pattern of zebrafish Anti-Müllerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns. 2005;(5):655-67. doi: 10.1016/j.modgep.2005.02.008.
59. Wu GC, Chiu PC, Lyu YS, Chang CF. The expression of amh and amhr2 is associated with the development of gonadal tissue and sex change in the protandrous black porgy, Acanthopagrus schlegeli. Biol Reprod. 2010;83(3):443-53. doi: 10.1095/biolreprod.110.084681.
60. Wu GC, Chang CF. The switch of secondary sex determination in protandrous black porgy, Acanthopagrus schlegeli. Fish Physiol Biochem. 2013;39(1):33-8. doi: 10.1007/s10695-012-9618-0.
2. Trukhina AV, Lukina NA, Wackerow-Kouzova ND, Smirnov AF. The variety of vertebrate mechanisms of sex determination. Biomed Res Int. 2013;2013:587460. doi: 10.1155/2013/587460.
3. Graves JA. How to evolve new vertebrate sex determining genes. Dev Dyn. 2013;242(4):354-9. doi: 10.1002/dvdy.23887.
4. Kikuchi K, Hamaguchi S. Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn. 2013;242(4):339-53. doi: 10.1002/dvdy.23927.
5. Herpin A, Adolfi MC, Nicol B, Hinzmann M, Schmidt C, Klughammer J, Engel M, Tanaka M, Guiguen Y, Schartl M. Divergent expression regulation of gonad development genes in medaka shows incomplete conservation of the downstream regulatory network of vertebrate sex determination. Mol Biol Evol. 2013;30(10):2328-46. doi: 10.1093/molbev/mst130.
6. Heule C, Salzburger W, Böhne A. Genetics of sexual development: an evolutionary playground for fish. Genetics. 2014;196(3):579-91. doi: 10.1534/genetics.114.16115.
7. Devlin RH, Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002;208(3–4):191-364. doi:10.1016/S0044-8486(02)00057-1.
8. Graham P, Penn JK, Schedl P. Masters change, slaves remain. Bioessays. 2003;25(1):1-4. doi: 10.1002/bies.
9. Herpin A, Schartl M. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep. 2015;16(10):1260-74. doi: 10.15252/embr.201540667.
10. Munger SC, Capel B. Sex and the circuitry: progress toward a systems-level understanding of vertebrate sex determination. Wiley Interdiscip Rev Syst Biol Med. 2012;4(4):401-12. doi: 10.1002/wsbm.1172.
11. Koopman P. Sex determination: the power of DMRT1. Trends Genet. 2009;25(11):479-81. doi: 10.1016/j.tig.2009.09.009.
12. Capel B. Sex in the 90s: SRY and the switch to the male pathway. Annu Rev Physiol. 1998;60:497-523. doi: 10.1146/annurev.physiol.60.1.497.
13. Temel SG, Gulten T, Yakut T, Saglam H, Kilic N, Bausch E, Jin WJ, Leipoldt M, Scherer G. Extended pedigree with multiple cases of XX sex reversal in the absence of SRY and of a mutation at the SOX9 locus. Sex Dev. 2007;1(1):24-34. doi: 10.1159/000096236.
14. Nishioka M, Miura I, Saitoh K. Sex chromosomes of Rana rugosa with special reference to local differences in sex determining mechanism. Sci. Rep. Lab. Amphibian Biol. 1993;(12):55–8. doi:10.15027/14532.
15. Roco ÁS, Olmstead AW, Degitz SJ, Amano T, Zimmerman LB, Bullejos M. Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis. Proc Natl Acad Sci U S A. 2015;112(34):E4752-61. doi: 10.1073/pnas.1505291112.
16. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A. 2008;105(7):2469-74. doi: 10.1073/pnas.0712244105.
17. Nanda I, Zend-Ajusch E, Shan Z, Grützner F, Schartl M, Burt DW, Koehler M, Fowler VM, Goodwin G, Schneider WJ, Mizuno S, Dechant G, Haaf T, Schmid M. Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination. Cytogenet Cell Genet. 2000;89(1-2):67-78. doi: 10.1159/000015567.
18. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature. 2009;461(7261):267-71. doi: 10.1038/nature08298.
19. Ayers KL, Sinclair AH, Smith CA. The molecular genetics of ovarian differentiation in the avian model. Sex Dev. 2013;7(1-3):80-94. doi: 10.1159/000342358.
20. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature. 1998 ;391(6668):691-5. doi: 10.1038/35618. PMID: 9490411.
21. Huang S, Ye L, Chen H. Sex determination and maintenance: the role of DMRT1 and FOXL2. Asian J Androl. 2017;19(6):619-624. doi: 10.4103/1008-682X.194420.
22. Mello MP, Assumpção JG, Hackel C. Genes envolvidos na determinação e diferenciação do sexo. Arq. Bras. Endocrinol. Metab. 2005;(49):14-25. doi:10.1590/S0004-27302005000100004
23. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A. 2008;105(7):2469-74. doi: 10.1073/pnas.0712244105.
24. Marchand O, Govoroun M, D'Cotta H, McMeel O, Lareyre JJ, Bernot A, Laudet V, Guiguen Y. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta. 2000;1493(1-2):180-7. doi: 10.1016/s0167-4781(00)00186-x.
25. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod. 2008;78(2):333-41. doi: 10.1095/biolreprod.107.064246.
26. Guo Y, Cheng H, Huang X, Gao S, Yu H, Zhou R. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem Biophys Res Commun. 2005;330(3):950-7. doi: 10.1016/j.bbrc.2005.03.066.
27. Webster KA, Schach U, Ordaz A, Steinfeld JS, Draper BW, Siegfried KR. Dmrt1 is necessary for male sexual development in zebrafish. Dev Biol. 2017;422(1):33-46. doi: 10.1016/j.ydbio.2016.12.008.
28. Lin Q, Mei J, Li Z, Zhang X, Zhou L, Gui JF. Distinct and Cooperative Roles of amh and dmrt1 in Self-Renewal and Differentiation of Male Germ Cells in Zebrafish. Genetics. 2017;207(3):1007-1022. doi: 10.1534/genetics.117.300274.
29. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 2002;417(6888):559-63. doi: 10.1038/nature751.
30. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M. 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(18):11778-83. doi: 10.1073/pnas.182314699.
31. Kang Y, Guan GJ, Hong YH. Insights of sex determination and differentiation from medaka as a teleost model. Yi Chuan. 2017;39(6):441-454. doi: 10.16288/j.yczz.17-140.
32. Matsuda M, Matsuda C, Hamaguchi S, Sakaizumi M. Identification of the sex chromosomes of the medaka, Oryzias latipes, by fluorescence in situ hybridization. Cytogenet Cell Genet. 1998;82(3-4):257-62. doi: 10.1159/000015113.
33. Thorgaard GH. Heteromorphic sex chromosomes in male rainbow trout. Science. 1977;196(4292):900-2. doi: 10.1126/science.860122.
34. Iturra P, Lam N, de la Fuente M, Vergara N, Medrano JF. Characterization of sex chromosomes in rainbow trout and coho salmon using fluorescence in situ hybridization (FISH). Genetica. 2001;111(1-3):125-31. doi: 10.1023/a:1013725717142.
35. Baroiller JF, D'Cotta H, Saillant E. Environmental effects on fish sex determination and differentiation. Sex Dev. 2009;3(2-3):118-35. doi: 10.1159/000223077.
36. Mair GC, Scott AG, Penman DJ, Skibinski DO, Beardmore JA. Sex determination in the genus Oreochromis : 2. Sex reversal, hybridisation, gynogenesis and triploidy in O. aureus Steindachner. Theor Appl Genet. 1991;82(2):153-60. doi: 10.1007/BF00226206.
37. Volff JN, Schartl M. Variability of genetic sex determination in poeciliid fishes. Genetica. 2001;111(1-3):101-10. doi: 10.1023/a:1013795415808.
38. Schartl M. A comparative view on sex determination in medaka. Mech Dev. 2004;121(7-8):639-45. doi: 10.1016/j.mod.2004.03.001.
39. Adolfi MC, Nakajima RT, Nóbrega RH, Schartl M. Intersex, Hermaphroditism, and Gonadal Plasticity in Vertebrates: Evolution of the Müllerian Duct and Amh/Amhr2 Signaling. Annu Rev Anim Biosci. 2019;7:149-172. doi: 10.1146/annurev-animal-020518-114955.
40. Valenzuela N, Adams DC, Janzen FJ. Pattern does not equal process: exactly when is sex environmentally determined? Am Nat. 2003;161(4):676-83. doi: 10.1086/368292.
41. Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T, Hirai T, Kamei Y, Kitano T. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev. 2010;77(8):679-86. doi: 10.1002/mrd.21203.
42. 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(8):3900-8. doi: 10.1210/en.2010-0228.
43. Raz E. Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet. 2003;4(9):690-700. doi: 10.1038/nrg1154.
44. Raz E, Reichman-Fried M. Attraction rules: germ cell migration in zebrafish. Curr Opin Genet Dev. 2006;16(4):355-9. doi: 10.1016/j.gde.2006.06.007.
45. Guerrero-Estévez S, Moreno-Mendoza N. Sexual determination and differentiation in teleost fish. Rev Fish Biol Fisheries. 2010;(20):101–121. https://doi.org/10.1007/s11160-009-9123-4.
46. Kimble J, Page DC. The mysteries of sexual identity. The germ cell's perspective. Science. 2007;316(5823):400-1. doi: 10.1126/science.1142109.
47. Saito D, Morinaga C, Aoki Y, Nakamura S, Mitani H, Furutani-Seiki M, Kondoh H, Tanaka M. Proliferation of germ cells during gonadal sex differentiation in medaka: Insights from germ cell-depleted mutant zenzai. Dev Biol. 2007;310(2):280-90. doi: 10.1016/j.ydbio.2007.07.039.
48. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics. 2012;191(1):163-70. doi: 10.1534/genetics.111.137497.
49. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 2012;8(7):e1002798. doi: 10.1371/journal.pgen.1002798.
50. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A. 2012;109(8):2955-9. doi: 10.1073/pnas.1018392109.
51. Gautier A, Le Gac F, Lareyre JJ. The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene. 2011;472(1-2):7-17. doi: 10.1016/j.gene.2010.10.014.
52. Herpin A, Schartl M. Molecular mechanisms of sex determination and evolution of the Y-chromosome: insights from the medakafish (Oryzias latipes). Mol Cell Endocrinol. 2009;306(1-2):51-8. doi: 10.1016/j.mce.2009.02.004.
53. Nakamura S, Watakabe I, Nishimura T, Picard JY, Toyoda A, Taniguchi Y, di Clemente N, Tanaka M. Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development. 2012;139(13):2283-7. doi: 10.1242/dev.076307.
54. Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol. 2012;22(15):1423-8. doi: 10.1016/j.cub.2012.05.045.
55. Hattori RS, Somoza GM, Fernandino JI, Colautti DC, Miyoshi K, Gong Z, Yamamoto Y, Strüssmann CA. The Duplicated Y-specific amhy Gene Is Conserved and Linked to Maleness in Silversides of the Genus Odontesthes. Genes (Basel). 2019;10(9):679. doi: 10.3390/genes10090679.
56. Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N, Mitani H, Furutani-Seiki M, Tanaka M, Kondoh H. The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci U S A. 2007;104(23):9691-6. doi: 10.1073/pnas.0611379104.
57. Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Abe S, Kitano T. Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun. 2004;322(2):508-13. doi: 10.1016/j.bbrc.2004.07.162.
58. Rodríguez-Marí A, Yan YL, Bremiller RA, Wilson C, Cañestro C, Postlethwait JH. Characterization and expression pattern of zebrafish Anti-Müllerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns. 2005;(5):655-67. doi: 10.1016/j.modgep.2005.02.008.
59. Wu GC, Chiu PC, Lyu YS, Chang CF. The expression of amh and amhr2 is associated with the development of gonadal tissue and sex change in the protandrous black porgy, Acanthopagrus schlegeli. Biol Reprod. 2010;83(3):443-53. doi: 10.1095/biolreprod.110.084681.
60. Wu GC, Chang CF. The switch of secondary sex determination in protandrous black porgy, Acanthopagrus schlegeli. Fish Physiol Biochem. 2013;39(1):33-8. doi: 10.1007/s10695-012-9618-0.
Downloads
Publicado
2021-11-08
Como Citar
1.
de Oliveira MA. MACHO OU FÊMEA? COMO O SEXO DOS VERTEBRADOS É DETERMINADO. RVZ [Internet]. 8º de novembro de 2021 [citado 21º de novembro de 2024];28:1-13. Disponível em: https://rvz.emnuvens.com.br/rvz/article/view/573
Edição
Seção
Artigos de Revisão
Licença
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional.
