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Sex inversion and epigenetic regulation in vertebrates

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Abstract

This review discusses issues related to the regulation of sex determination and differentiation in various groups of Vertebrates. Special attention was paid to factors of external and internal control for various genetic systems of sex determination, as well as to the epigenetic control of this process. Opportunities for sex inversion in various animals were also discussed.

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References

  1. Cutting, A., Chue, J., and Smith, C.A., Just how conserved is vertebrate sex determination?, Dev. Dyn., 2013, vol. 242, pp. 380–387.

    Article  CAS  PubMed  Google Scholar 

  2. Gamble, T. and Zarkower, D., Sex determination, Curr. Biol., 2012, vol. 22, no. 8, pp. R257–R262.

    Article  CAS  PubMed  Google Scholar 

  3. Shen, Z.G. and Wang, H.P., Molecular players involved in temperature-dependent sex determination and sex differentiation in Teleost fish, Genet. Sel. Evol., 2014, vol. 46, no. 1, p. 26.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Kobayashi, Y., Nagahama, Y., and Nakamura, M., Diversity and plasticity of sex determination and differentiation in fishes, Sex Dev., 2013, vol. 7, nos. 1–3, pp. 115–125.

    Article  CAS  PubMed  Google Scholar 

  5. Kohno, S., Parrott, B.B., Yatsu, R., et al., Gonadal differentiation in reptiles exhibiting environmental sex determination, Sex Dev., 2014. doi 10.1159/000358892

    Google Scholar 

  6. Russo, V.E.A., Martienssen, R.A., and Riggs, A.D., Epigenetic Mechanisms of Gene Regulation, Woodbury: Cold Spring Harbour Laboratory, 1996, vol. 32.

    Google Scholar 

  7. Piferrer, F., Epigenetics of sex determination and gonadogenesis, Dev. Dyn., 2013, vol. 242, no. 4, pp. 360–370.

    Article  CAS  PubMed  Google Scholar 

  8. Guerrero-Estévez, S. and Moreno-Mendoza, N., Sexual determination and differentiation in Teleost fish, Rev. Fish Biol. Fish., 2010, vol. 20, pp. 101–121.

    Article  Google Scholar 

  9. Gorelick, R., Evolution of dioecy and sex chromosomes via methylation driving Mullers ratchet, Biol. J. Linn. Soc., 2003, vol. 80, no. 2, pp. 353–368.

    Article  Google Scholar 

  10. Navarro-Martín, L., Viñas, J., Ribas, 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, vol. 7, no. 12. e1002447

    Article  PubMed Central  PubMed  Google Scholar 

  11. Shao, C., Li, Q., Chen, S., et al., Epigenetic modification and inheritance in sexual reversal of fish, Genome Res., 2014, vol. 24, no. 40, pp. 604–615.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Perrin, N., Sex reversal: a fountain of youth for sex chromosomes?, Evolution, 2009, vol. 63, no. 12, pp. 3043–3049.

    Article  PubMed  Google Scholar 

  13. Nakamura, M., Is a sex-determining gene(s) necessary for sex-determination in amphibians? Steroid hormones may be the key factor, Sex Dev., 2013, vol. 7, nos. 1–3, pp. 104–114.

    Article  CAS  PubMed  Google Scholar 

  14. Yoshimoto, S. and Ito, M., A ZZ/ZW-type sex determination in Xenopus laevis, FEBS J., 2011, vol. 278, no. 7, pp. 1020–1026.

    Article  CAS  PubMed  Google Scholar 

  15. Nakamura, M., The mechanism of sex determination in vertebrates—are sex steroids the key-factor?, J. Exp. Zool., Part A, 2010, vol. 313, no. 7, pp. 381–398.

    Article  Google Scholar 

  16. Merchant-Larios, H. and Daz-Hernández, V., Environmental sex determination mechanisms in reptiles, Sex Dev., 2013, vol. 7, nos. 1–3, pp. 95–103.

    Article  CAS  PubMed  Google Scholar 

  17. Pieau, C., Dorizzi, M., and Richard-Mercier, N., Temperature-dependent sex determination and gonadal differentiation in reptiles, in Genes and Mechanisms in Vertebrate Sex Determination, Scherer, G. and Schmid, M., Eds., EXS, 2001, vol. 91, pp. 117–141.

    Article  CAS  Google Scholar 

  18. Matsumoto, Y. and Crews, D., Molecular mechanisms of temperature-dependent sex determination in the context of ecological developmental biology, Mol. Cell. Endocrinol., 2012, vol. 354, nos. 1–2, pp. 103–110.

    Article  CAS  PubMed  Google Scholar 

  19. Ayling, L.-J. and Griffin, D.K., The evolution of sex chromosomes, Cytogenet. Genome Res., 2002, vol. 99, nos. 1–4, pp. 125–140.

    Article  PubMed  Google Scholar 

  20. Matsumoto, Y., Buemio, A., Chu, R., et al., Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red eared slider turtles, PLoS One, 2013, vol. 8, no. 6. e63599

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Mork, L., Czerwinski, M., and Capel, B., Predetermination of sexual fate in a turtle with temperature-dependent sex determination, Dev. Biol., 2014, vol. 386, no. 1, pp. 264–271.

    Article  CAS  PubMed  Google Scholar 

  22. Parrott, B.B., Kohno, S., Cloy-McCoy, J.A., et al., Differential incubation temperatures result in dimorphic DNA methylation patterning of the sox9 and aromatase promoters in gonads of alligator (Alligator mississippiensis) embryos, Biol. Reprod., 2014, vol. 90, no. 12, pp. 1–11.

    Google Scholar 

  23. Ditewig, A.C., Organogenesis of the ovary: a comparative review on vertebrate ovary formation, Organogenesis, 2005, vol. 2, no. 2, pp. 36–41.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Smirnov, A.F. and Trukhina, A.V., Sex determination in birds, in Birds: Evolution and Behavior, Breeding Strategies, Migration and Spread of Diseases, Ruiz, L. and Iglesias, F., Eds., New York: Nova Science, 2013, pp. 1–24.

    Google Scholar 

  25. Ayers, K.L., Sinclair, A.H., and Smith, C.A., The molecular genetics of ovarian differentiation in the avian model, Sex Dev., 2013, vol. 7, nos. 1–3, pp. 80–94.

    Article  CAS  PubMed  Google Scholar 

  26. Lambeth, L.S., Raymond, C.S., Roeszler, K.N., et al., Over-expression of dmrt1 induces the male pathway in embryonic chicken gonads, Dev. Biol., 2014, vol. 389, no. 2, pp. 160–172.

    Article  CAS  PubMed  Google Scholar 

  27. Ellis, H.L., Shioda, K., Rosenthal, N.F., et al., Masculine epigenetic sex marks of the cyp19a1/aromatase promoter in genetically male chicken embryonic gonads are resistant to estrogen-induced phenotypic sex conversion, Biol. Reprod., 2012, vol. 87, no. 1, pp. 1–12.

    Article  Google Scholar 

  28. Teranishi, M., Shimada, Y., Hori, T., et al., Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the dmrt1 locus, Chromosome Res., 2001, vol. 9, no. 2, pp. 147–165.

    Article  CAS  PubMed  Google Scholar 

  29. Bisoni, L., Batlle-Morera, L., Bird, A.P., et al., Female-specific hyperacetylation of histone H4 in the chicken Z chromosome, Chromosome Res., 2005, vol. 13, no. 2, pp. 205–214.

    Article  CAS  PubMed  Google Scholar 

  30. Itoh, Y., Kampf, K., and Arnold, A.P., Possible differences in the two Z chromosomes in male chickens and evolution of MHM sequences in galliformes, Chromosoma, 2011, vol. 120, pp. 587–598.

    Article  CAS  PubMed  Google Scholar 

  31. Melamed, E. and Arnold, A.P., Regional differences in dosage compensation on the chicken Z chromosome, Genome Biol., 2007, vol. 8, no. 9, p. R202.

    Article  PubMed Central  PubMed  Google Scholar 

  32. Itoh, Y., Replogle, K., Kim, Y.H., et al., Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds, Genome Res., 2010, vol. 20, no. 4, pp. 512–518.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Yang, X., Zheng, J., Xu, G., et al., Exogenous cMHM regulates the expression of dmrt1 and ER alpha in avian testes, Mol. Biol. Rep., 2010, vol. 37, no. 4, pp. 1841–1847.

    Article  CAS  PubMed  Google Scholar 

  34. Roeszler, K.N., Itman, C., Sinclair, A.H., and Smith, C.A., The long non-coding RNA, MHM, plays a role in chicken embryonic development, including gonadogenesis, Dev. Biol., 2012, vol. 366, no. 2, pp. 317–326.

    Article  CAS  PubMed  Google Scholar 

  35. Yang, X., Zheng, J., Qu, L., et al., Methylation status of cMHM and expression of sex-specific genes in adult sex-reversed female chickens, Sex Dev., 2011, vol. 5, no. 3, pp. 147–154.

    Article  CAS  PubMed  Google Scholar 

  36. Caetano, L.C. and Gennaro, F.G., Coelho, K., et al., Differential expression of the MHM region and of sex-determining-related genes during gonadal development in chicken embryos, Genet. Mol. Res., 2014, vol. 13, no. 1, pp. 838–849.

    Article  CAS  PubMed  Google Scholar 

  37. Cutting, A.D., Bannister, S.C., and Doran, T.J., et al., The potential role of microRNAs in regulating gonadal sex differentiation in the chicken embryo, Chromosome Res., 2012, vol. 20, no. 1, pp. 201–213.

    Article  CAS  PubMed  Google Scholar 

  38. Feng, Y.P., Chen, J.F., Huang, P., et al., Expression analysis of differentially expressed miRNAs in male and female chicken embryos, Genet. Mol. Res., 2014, vol. 13, no. 2, pp. 3060–3068.

    Article  CAS  PubMed  Google Scholar 

  39. Pask, A.J., A role for estrogen in somatic cell fate of the mammalian gonad, Chromosome Res., 2012, vol. 20, no. 1, pp. 239–245.

    Article  CAS  PubMed  Google Scholar 

  40. Kuroki, S., Matoba, S., Akiyoshi, M., et al., Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a, Science, 2013, vol. 341, no. 6150, pp. 1106–1109.

    Article  CAS  PubMed  Google Scholar 

  41. Larney, C., Bailey, T.L., and Koopman, P., Switching on sex: transcriptional regulation of the testis-determining gene sry, Development, 2014, vol. 141, no. 11, pp. 2195–2205.

    Article  CAS  PubMed  Google Scholar 

  42. Lybaek, H., de Bruijn, D., den Engelsman-van Dijk, A.H., et al., RevSex duplication-induced and sex-related differences in the SOX9 regulatory region chromatin landscape in human fibroblasts, Epigenetics, 2014, vol. 9, no. 3, pp. 416–427.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Kobayashi, H., Sakurai, T., Miura, F., et al., High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice, Genome Res., 2013, vol. 23, no. 4, pp. 616–627.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Nishino, K., Hattori, N., Tanaka, S., et al., DNA methylation-mediated control of sry gene expression in mouse gonadal development, J. Biol. Chem., 2004, vol. 279, no. 21, pp. 22306–22313.

    Article  CAS  PubMed  Google Scholar 

  45. Pannetier, M., Elzaiat, M., Thépot, D., and Pailhoux, E., Telling the story of XX sex reversal in the goat: high-lighting the sex-crossroad in domestic mammals, Sex Dev., 2012, vol. 6, nos. 1–3, pp. 33–45.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Genetics and Biotechnology, St.Petersburg State University, St. Petersburg-Old Peterhof, 199034, Russia

    A. V. Trukhina, N. A. Lukina, A. A. Nekrasova & A. F. Smirnov

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  1. A. V. Trukhina
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  2. N. A. Lukina
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  3. A. A. Nekrasova
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  4. A. F. Smirnov
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Correspondence to A. V. Trukhina.

Additional information

Original Russian Text © A.V. Trukhina, N.A. Lukina, A.A. Nekrasova, A.F. Smirnov, 2015, published in Genetika, 2015, Vol. 51, No. 3, pp. 290–297.

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Trukhina, A.V., Lukina, N.A., Nekrasova, A.A. et al. Sex inversion and epigenetic regulation in vertebrates. Russ J Genet 51, 231–237 (2015). https://doi.org/10.1134/S1022795415020155

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  • DOI: https://doi.org/10.1134/S1022795415020155

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