Russian Journal of Genetics

, Volume 46, Issue 4, pp 385–393 | Cite as

Meiotic inactivation of sex chromosomes in mammals

  • E. A. Vaskova
  • S. V. Pavlova
  • A. I. Shevchenko
  • S. M. Zakian
Reviews and Theoretical Articles


During meiosis, heteromorphic mammalian X and Y chromosomes in males undergo transcription silencing and form a compact structure, the XY body, containing specific modifications of the chromatin. In this review, we consider the dynamics of sex chromosome inactivation and discuss the suggestion that the paternally inherited X-chromosome preserves inactivated state in zygote. This state results from meiotic silencing and is prone to imprinted inactivation, which is observed in mammalian females at early embryogenetic stages.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Kelly, W.G. and Aramayo, R., Meiotic Silencing and the Epigenetics of Sex, Chromosome Res., 2007, vol. 15, pp. 633–651.CrossRefPubMedGoogle Scholar
  2. 2.
    Turner, J.M., Meiotic Sex Chromosome Inactivation, Development, 2007, vol. 134, pp. 1823–1831.CrossRefPubMedGoogle Scholar
  3. 3.
    Namekawa, S.H., VandeBerg, J.L., McCarrey, J.R., and Lee, J.T., Sex Chromosome Silencing in the Marsupial Male Germ Line, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 9730–9735.CrossRefPubMedGoogle Scholar
  4. 4.
    Odorisio, T., Rodriguez, T.A., Evans, E.P., et al., The Meiotic Checkpoint Monitoring Synapsis Eliminates Spermatocytes via P53-Independent Apoptosis, Nat. Genet., 1998, vol. 18, pp. 257–261.CrossRefPubMedGoogle Scholar
  5. 5.
    Lifschytz, E. and Lindsley, D.L., The Role of X-Chromosome Inactivation during Spermatogenesis (Drosophila-Allocycly-Chromosome Evolution-Male Sterility-Dosage Compensation), Proc. Natl. Acad. Sci. USA, 1972, vol. 69, pp. 182–186.CrossRefPubMedGoogle Scholar
  6. 6.
    McKee, B.D. and Handel, M.A., Sex Chromosomes, Recombination, and Chromatin Conformation, Chromosoma, 1993, vol. 102, pp. 71–80.CrossRefPubMedGoogle Scholar
  7. 7.
    Ayoub, N., Richler, C., and Wahrman, J., Xist RNA Is Associated with the Transcriptionally Inactive XY Body in Mammalian Male Meiosis, Chromosoma, 1997, vol. 106, pp. 1–10.CrossRefPubMedGoogle Scholar
  8. 8.
    Turner, J.M., Mahadevaiah, S.K., Benavente, R., et al., Analysis of Male Meiotic “Sex Body” Proteins during XY Female Meiosis Provides New Insights into Their Functions, Chromosoma, 2000, vol. 109, pp. 426–432.CrossRefPubMedGoogle Scholar
  9. 9.
    Hoyer-Fender, S., Molecular Aspects of XY Body Formation, Cytogenet. Genome Res., 2003, vol. 103, pp. 245–255.CrossRefPubMedGoogle Scholar
  10. 10.
    Handel, M.A., The XY Body: A Specialized Meiotic Chromatin Domain, Exp. Cell Res., 2004, vol. 296, pp. 57–63.CrossRefPubMedGoogle Scholar
  11. 11.
    Holstein, A.F., Schulze, W., and Davidoff, M., Under-standing Spermatogenesis Is a Prerequisite for Treatment, Reprod. Biol. Endocrinol., 2003, vol. 1, p. 107.CrossRefPubMedGoogle Scholar
  12. 12.
    Bellani, M.A., Romanienko, P.J., Cairatti, D.A., and Camerini-Otero, R.D., SPO11 Is Required for Sex-Body Formation, and Spo11 Heterozygosity Rescues the Prophase Arrest of Atm-/-Spermatocytes, J. Cell Sci., 2005, vol. 118, pp. 3233–3245.CrossRefPubMedGoogle Scholar
  13. 13.
    Fernandez-Capetillo, O., Mahadevaiah, S.K., Celeste, A., et al., H2AX Is Required for Chromatin Remodelling and Inactivation of Sex Chromosomes in Male Mouse Meiosis, Dev. Cell, 2003, vol. 4, pp. 497–508.CrossRefPubMedGoogle Scholar
  14. 14.
    Khalil, A.M., Boyar, F.Z., and Driscoll, D.J., Dynamic Histone Modifications Mark Sex Chromosome Inactivation and Reactivation during Mammalian Spermatogenesis, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 16583–16587.CrossRefPubMedGoogle Scholar
  15. 15.
    Godmann, M., Auger, V., Ferraroni-Aguiar, V., et al., Dynamic Regulation of Histone H3 Methylation at Lysine 4 in Mammalian Spermatogenesis, Biol. Reprod., 2007, vol. 77, pp. 754–764.CrossRefPubMedGoogle Scholar
  16. 16.
    van der Heijden, G.W., Derijck, A.A., Posfai, E., et al., Chromosome-Wide Nucleosome Replacement and H3.3 Incorporation during Mammalian Meiotic Sex Chromosome Inactivation, Nat. Genet., 2007, vol. 39, pp. 251–258.CrossRefPubMedGoogle Scholar
  17. 17.
    Greaves, I.K., Rangasamy, D., Devoy, M., et al., The X and Y Chromosomes Assemble into H2A.Z-Containing Facultative Heterochromatin Following Meiosis, Mol. Cell Biol., 2006, vol. 26, pp. 5394–5405.CrossRefPubMedGoogle Scholar
  18. 18.
    Turner, J.M., Aprelikova, O., Xu, X., et al., BRCA1, Histone H2AX Phosphorylation, and Male Meiotic Sex Chromosome Inactivation, Curr. Biol., 2004, vol. 14, pp. 2135–2142.CrossRefPubMedGoogle Scholar
  19. 19.
    Mahadevaiah, S.K., Turner, J.M., Baudat, F., et al., Recombinational DNA Double-Strand Breaks in Mice Precede Synapsis, Nat. Genet., 2001, vol. 27, pp. 271–276.CrossRefPubMedGoogle Scholar
  20. 20.
    Solari, A.J., The Behavior of the XY Pair in Mammals, Int. Rev. Cytol., 1974, vol. 38, pp. 273–317.CrossRefPubMedGoogle Scholar
  21. 21.
    Costa, Y., Speed, R.M., Gautier, P., et al., Mouse MAELSTROM: The Link between Meiotic Silencing of Unsynapsed Chromatin and microRNA Pathway?, Hum. Mol. Genet., 2006, vol. 15, pp. 2324–2334.CrossRefPubMedGoogle Scholar
  22. 22.
    Meistrich, M.L., Bucci, L.R., Trostle-Weige, P.K., and Brock, W.A., Histone Variants in Rat Spermatogonia and Primary Spermatocytes, Dev. Biol., 1985, vol. 112, pp. 230–240.CrossRefPubMedGoogle Scholar
  23. 23.
    Wolfe, S.A. and Grimes, S.R., Histone H1t: A Tissue-Specific Model Used to Study Transcriptional Control and Nuclear Function during Cellular Differentiation, J. Cell Biochem., 1993, vol. 53, pp. 156–160.CrossRefPubMedGoogle Scholar
  24. 24.
    Baarends, W.M., Wassenaar, E., van der Laan, R., et al., Silencing of Unpaired Chromatin and Histone H2A Ubiquitination in Mammalian Meiosis, Mol. Cell Biol., 2005, vol. 25, pp. 1041–1053.CrossRefPubMedGoogle Scholar
  25. 25.
    de Vries, F.A., de Boer, E., Bosch, M., et al., Mouse Sycp1 Functions in Synaptonemal Complex Assembly, Meiotic Recombination, and XY Body Formation, Genes Dev., 2005, vol. 19, pp. 1376–1389.CrossRefPubMedGoogle Scholar
  26. 26.
    van der Laan, R., Uringa, E.J., Wassenaar, E., et al., Ubiquitin Ligase Rad18Sc Localizes to the XY Body and to Other Chromosomal Regions That Are Unpaired and Transcriptionally Silenced during Male Meiotic Prophase, J. Cell Sci., 2004, vol. 117, pp. 5023–5033.CrossRefPubMedGoogle Scholar
  27. 27.
    Baarends, W.M., Hoogerbrugge, J.W., Roest, H.P., et al., Histone Ubiquitination and Chromatin Remodeling in Mouse Spermatogenesis, Dev. Biol., 1999, vol. 207, pp. 322–333.CrossRefPubMedGoogle Scholar
  28. 28.
    Metzler-Guillemain, C., Luciani, J., Depetris, D., et al., HP1beta and HP1gamma, but not HP1alpha, Decorate the Entire XY Body during Human Male Meiosis, Chromosome Res., 2003, vol. 11, pp. 73–81.CrossRefPubMedGoogle Scholar
  29. 29.
    Ooi, S.L., Priess, J.R., and Henikoff, S., Histone H3.3 Variant Dynamics in the Germline of Caenorhabditis elegans, PLoS Genet., 2006, vol. 2, p. e97.CrossRefPubMedGoogle Scholar
  30. 30.
    van der Heijden, G.W., Derijck, A.A., Ramos, L., et al., Transmission of Modified Nucleosomes from the Mouse Male Germline to the Zygote and Subsequent Remodeling of Paternal Chromatin, Dev. Biol., 2006, vol. 298, pp. 458–469.CrossRefPubMedGoogle Scholar
  31. 31.
    Turner, J.M., Burgoyne, P.S., and Singh, P.B., M31 and macroH2A1.2 Colocalise at the Pseudoautosomal Region during Mouse Meiosis, J. Cell Sci., 2001, vol. 114, pp. 3367–3375.PubMedGoogle Scholar
  32. 32.
    Hoyer-Fender, S., Czirr, E., Radde, R., et al., Localisation of Histone macroH2A1.2 to the XY-Body Is not a Response to the Presence of Asynapsed Chromosome Axes, J. Cell Sci., 2004, vol. 117, pp. 189–198.CrossRefPubMedGoogle Scholar
  33. 33.
    Namekawa, S.H., Park, P.J., Zhang, L.F., et al., Postmeiotic Sex Chromatin in the Male Germline of Mice, Curr. Biol., 2006, vol. 16, pp. 660–667.CrossRefPubMedGoogle Scholar
  34. 34.
    Chen, H.Y., Sun, J.M., Zhang, Y., et al., Ubiquitination of Histone H3 in Elongating Spermatids of Rat Testes, J. Biol. Chem., 1998, vol. 273, pp. 13165–13169.CrossRefPubMedGoogle Scholar
  35. 35.
    Wang, P.J., Page, D.C., and McCarrey, J.R., Differential Expression of Sex-Linked and Autosomal Germ-Cell-Specific Genes during Spermatogenesis in the Mouse, Hum. Mol. Genet., 2005, vol. 14, pp. 2911–2918.CrossRefPubMedGoogle Scholar
  36. 36.
    Hornecker, J.L., Samollow, P.B., Robinson, E.S., et al., Meiotic Sex Chromosome Inactivation in the Marsupial Monodelphis domestica, Genesis, 2007, vol. 45, pp. 696–708.CrossRefPubMedGoogle Scholar
  37. 37.
    Mueller, J.L., Mahadevaiah, S.K., Park, P.J., et al., The Mouse X Chromosome Is Enriched for Multicopy Testis Genes Showing Postmeiotic Expression, Nat. Genet., 2008, vol. 40, pp. 794–799.CrossRefPubMedGoogle Scholar
  38. 38.
    Khil, P.P., Smirnova, N.A., Romanienko, P.J., and Camerini-Otero, R.D., The Mouse X Chromosome Is Enriched for Sex-Biased Genes not Subject to Selection by Meiotic Sex Chromosome Inactivation, Nat. Genet., 2004, vol. 36, pp. 642–646.CrossRefPubMedGoogle Scholar
  39. 39.
    Wang, P.J., McCarrey, J.R., Yang, F., and Page, D.C., An Abundance of X-Linked Genes Expressed in Spermatogonia, Nat. Genet., 2001, vol. 27, pp. 422–426.CrossRefPubMedGoogle Scholar
  40. 40.
    Wang, P.J., X-chromosomes, Retrogenes and Their Role in Male Reproduction, Trends Endocrinol. Metab., 2004, vol. 15, pp. 79–83.CrossRefPubMedGoogle Scholar
  41. 41.
    McCarrey, J.R. and Thomas, K., Human Testis-Specific PGK Gene Lacks Introns and Possesses Characteristics of a Processed Gene, Nature, 1987, vol. 326, pp. 501–505.CrossRefPubMedGoogle Scholar
  42. 42.
    Heard, E. and Disteche, C.M., Dosage Compensation in Mammals: Fine-Tuning the Expression of the X-chromosome, Genes Dev., 2006, vol. 20, pp. 1848–1867.CrossRefPubMedGoogle Scholar
  43. 43.
    McCarrey, J.R., Watson, C., Atencio, J., et al., X-Chromosome Inactivation during Spermatogenesis Is Regulated by an Xist/Tsix-Independent Mechanism in the Mouse, Genesis, 2002, vol. 34, pp. 257–266.CrossRefPubMedGoogle Scholar
  44. 44.
    Turner, J.M., Mahadevaiah, S.K., Elliott, D.J., et al., Meiotic Sex Chromosome Inactivation in Male Mice with Targeted Disruptions of Xist, J. Cell Sci., 2002, vol. 115, pp. 4097–4105.CrossRefPubMedGoogle Scholar
  45. 45.
    Shevchenko, A.I., Pavlova, S.V., Dementyeva, E.V., et al., Chromatin Modifications during X-Chromosome Inactivation in Female Mammals, Russ. J. Genet., 2006, vol. 42, no. 9, pp. 1225–1234.CrossRefGoogle Scholar
  46. 46.
    van Attikum, H. and Gasser, S.M., The Histone Code at DNA Breaks: A Guide to Repair?, Nat. Rev. Mol. Cell Biol., 2005, vol. 6, pp. 757–765.CrossRefPubMedGoogle Scholar
  47. 47.
    Vigodner, M., Sumoylation Precedes Accumulation of Phosphorylated H2AX on Sex Chromosomes during Their Meiotic Inactivation, Chromosome Res., 2009, vol. 17, no. 1, pp. 37–45.CrossRefPubMedGoogle Scholar
  48. 48.
    Turner, J.M., Mahadevaiah, S.K., Fernandez-Capetillo, O., et al., Silencing of Unsynapsed Meiotic Chromosomes in the Mouse, Nat. Genet., 2005, vol. 37, pp. 41–47.PubMedGoogle Scholar
  49. 49.
    Burgoyne, P.S., Mahadevaiah, S.K., and Turner, J.M., The Consequences of Asynapsis for Mammalian Meiosis, Nat. Rev. Genet., 2009, vol. 10, pp. 207–216.CrossRefPubMedGoogle Scholar
  50. 50.
    Lyon, M.F. and Rastan, S., Parental Source of Chromosome Imprinting and Its Relevance for X-chromosome Inactivation, Differentiation, 1984, vol. 26, pp. 63–67.CrossRefPubMedGoogle Scholar
  51. 51.
    McLaren, A. and Monk, M., X-Chromosome Activity in the Germ Cells of Sex-Reversed Mouse Embryos, J. Reprod. Fertil., 1981, vol. 63, pp. 533–537.PubMedCrossRefGoogle Scholar
  52. 52.
    Ooi, S.L. and Henikoff, S., Germline Histone Dynamics and Epigenetics, Curr. Opin. Cell Biol., 2007, vol. 19, pp. 257–265.CrossRefPubMedGoogle Scholar
  53. 53.
    Goto, T. and Kinoshita, T., Maternal Transcripts of Mitotic Checkpoint Gene, Xbub3, Are Accumulated in the Animal Blastomeres of Xenopus Early Embryo, DNA Cell Biol., 1999, vol. 18, pp. 227–234.CrossRefPubMedGoogle Scholar
  54. 54.
    Goto, Y. and Takagi, N., Tetraploid Embryos Rescue Embryonic Lethality Caused by an Additional Maternally Inherited X-chromosome in the Mouse, Development, 1998, vol. 125, pp. 3353–3363.PubMedGoogle Scholar
  55. 55.
    Okamoto, I. and Arnaud, D., Le Baccon P., et al., Evidence for de novo Imprinted X-Chromosome Inactivation Independent of Meiotic Inactivation in Mice, Nature, 2005, vol. 438, pp. 369–373.CrossRefPubMedGoogle Scholar
  56. 56.
    Govin, J., Caron, C., Lestrat, C., et al., The Role of Histones in Chromatin Remodelling during Mammalian Spermiogenesis, Eur. J. Biochem., 2004, vol. 271, pp. 3459–3469.CrossRefPubMedGoogle Scholar
  57. 57.
    Churikov, D., Zalenskaya, I.A., and Zalensky, A.O., Male Germline-Specific Histones in Mouse and Man, Cytogenet. Genome Res., 2004, vol. 105, pp. 203–214.CrossRefPubMedGoogle Scholar
  58. 58.
    Trostle-Weigem P.K., Meistrich, M.L., Brock, W.A., et al., Isolation and Characterization of TH2A, a Germ Cell-Specific Variant of Histone 2A in Rat Testis, J. Biol. Chem., 1982, vol. 257, pp. 5560–5567.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • E. A. Vaskova
    • 1
  • S. V. Pavlova
    • 1
  • A. I. Shevchenko
    • 1
  • S. M. Zakian
    • 1
  1. 1.Institute of Cytology and Genetics, Siberian BranchRussian Academy of SciencesNovosibirskRussia

Personalised recommendations