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Epigenomics pp 301-318 | Cite as

Meiotic Silencing, Infertility and X Chromosome Evolution

  • James M.A. Turner

Keywords

Synaptonemal Complex Dosage Compensation Meiotic Silence Chromosome Synapsis Pachytene Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aramayo, R. and Metzenberg, R. L. (1996). Meiotic transvection in fungi. Cell 86, 103–113.PubMedCrossRefGoogle Scholar
  2. Ashley, T. (1995). Dynamic changes in Rad51 distribution during meiosis in male and female vertebrates. Chromosome 104, 19–28.CrossRefGoogle Scholar
  3. Baarends, W.M., Hoogerbrugge, J.W., Roest, H.P., Ooms, M., Vreeburg, J., Hoeijmakers, J.H. and Grootegoed, J.A. (1999). Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol. 207, 322–333.PubMedCrossRefGoogle Scholar
  4. Baarends, W.M., Wassenaar, E., van der Laan, R., Hoogerbrugge, J., Sleddens-Linkels, E., Hoeijmakers, J.H., de Boer, P. and Grootegoed, J.A. (2005). Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol. 25, 1041–1053.Google Scholar
  5. Baarends W.M., Wassenaar E, Hoogerbrugge J.W., Schoenmakers S, Sun Z.W. and Grootegoed J.A. (2007). Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome. J Cell Sci. 120, 1841–1851.PubMedCrossRefGoogle Scholar
  6. Baudat F and de Massy B. (2007). Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res. 15, 565–577.PubMedCrossRefGoogle Scholar
  7. Bean, C.J., Schaner, C.E. and Kelly, W.G. (2004). Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet. 36, 100–105.PubMedCrossRefGoogle Scholar
  8. Bellani, M.A., Romanienko, P.J., Cairatti, D.A. and Camerini-Otero, R.D. (2005). SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of {Atm-/-} spermatocytes. J Cell Sci. 118, 3233–3245.PubMedCrossRefGoogle Scholar
  9. Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, De Rooij D.G, Cooke H.J. (2007). SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol. 176, 741–747.PubMedCrossRefGoogle Scholar
  10. Burgoyne P. and Baker T. G. (1985). Perinatal oocyte loss in XO mice and its implications for the aetiology of gonadal dysgenesis in XO women. J Reprod Fertil. 75, 633–645.PubMedCrossRefGoogle Scholar
  11. Chu D.S., Liu H., Nix P., Wu T.F., Ralston E.J., Yates J.R 3rd. and Meyer B.J. (2006). Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature. 443, {101–105}.PubMedCrossRefGoogle Scholar
  12. Clotman F., De Backer O., De Plaen E., Boon T. and Picard J. (2000). Cell- and stage-specific expression of mage genes during mouse spermatogenesis. Mamm Genome. 11, 696-699.PubMedCrossRefGoogle Scholar
  13. Cooper D.W. (1971). Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature. 230, 292–294.PubMedCrossRefGoogle Scholar
  14. Costa Y., Speed R.M, Gautier P, Semple C.A., Maratou K., Turner J.M. and Cooke H.J. (2006). Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway? Hum Mol Genet. 15, 2324–34.PubMedCrossRefGoogle Scholar
  15. Davidow L.S., Breen M., Duke S.E., Samollow P.B., McCarrey J.R. and Lee J.T. (2007). The search for a marsupial XIC reveals a break with vertebrate synteny. Chromosome Res. 15, 137–146.PubMedCrossRefGoogle Scholar
  16. de Vries S.S., Baart E.B., Dekker M., Siezen A., de Rooij D.G., de Boer P., te Riele H. (1999). Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13, 523–531.PubMedCrossRefGoogle Scholar
  17. De Vries, F.A., de Boer, E., van den Bosch, M., Baarends, W.M., Ooms, M., Yuan, L., Liu, J.G., van Zeeland, A.A., Heyting, C. and Pastink, A. (2005). Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation.Genes Dev. 19, 1376–1389.PubMedCrossRefGoogle Scholar
  18. Duret L., Chureau C., Samain S., Weissenbach J. and Avner P. (2006). The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science. 312, 1653–1655.PubMedCrossRefGoogle Scholar
  19. Edelmann W., Cohen P.E., Kneitz B., Winand N., Lia M., Heyer J., Kolodner R., Pollard J.W. and Kucherlapati R. (1999). Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat Genet. 21, 123–127.PubMedCrossRefGoogle Scholar
  20. Ferguson-Smith A.C. (2004). X Inactivation: Pre- or Post-Fertilisation Turn-off? Current Biol. 14, R323–R325.CrossRefGoogle Scholar
  21. Fernandez-Capetillo, O., Mahadevaiah, S.K., Celeste, A., Romanienko, P.J., Camerini-Otero R,D., Bonner, W.M., Manova, K., Burgoyne, P. and Nussenzweig A. (2003). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4, 497–508.PubMedCrossRefGoogle Scholar
  22. Findley S.D., Tamanaha M., Clegg N.J. and Ruohola-Baker H. (2003). Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development. 130, 859–871.PubMedCrossRefGoogle Scholar
  23. Ford, C.E. and Evans E.P. (1964). A reciprocal translocation in the mouse between the X chromosome and a short autosome. Cytogenetics 3, 295–305.CrossRefGoogle Scholar
  24. Goldstein, P. (1982) The synaptonemal complexes of Caenorhabditis elegans: pachytene karyotype analysis of male and hermaphrodite wild-type and him mutants. Chromosoma 86, 577–593.PubMedCrossRefGoogle Scholar
  25. Govin, J., Escoffier, E., Rousseaux, S., Kuhn, L., Ferro, M., Thevenon, J., Catena, R., Davidson, I., Garin, J., Khochbin, S. and Caron, C. (2007). Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis.J Cell Biol, 176, 283–294.PubMedCrossRefGoogle Scholar
  26. Greaves, I.K., Rangasamy, D., Devoy, M., Marshall Graves, J.A. and Tremethick, D.J. (2006). The X and Y chromosomes assemble into H2A.Z, containing facultative heterochromatin, following meiosis. Mol Cell Biol. 26, 5394–5405.PubMedCrossRefGoogle Scholar
  27. Hassold T., Hall H. and Hunt P. (2007). The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet. 16, R203–R208.PubMedCrossRefGoogle Scholar
  28. Heard E. and Disteche C.M. (2006). Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev. 20, 1848–1867.PubMedCrossRefGoogle Scholar
  29. Hendriksen, P.J., Hoogerbrugge, J.W., Themmen, A.P., Koken, M.H., Hoeijmakers, J.H., Oostra, B.A., van der Lende, T. and Grootegoed, J.A. (1995). Postmeiotic transcription of X and Y chromosomal genes during spermatogenesis in the mouse. Dev Biol. 170, 730–733.Google Scholar
  30. Homolka D., Ivanek R., Capkova J., Jansa P. and Forejt J. (2007). Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res. 17, 1431–1437PubMedCrossRefGoogle Scholar
  31. Hore T.A., Koina E., Wakefield M.J. and Marshall Graves J.A. (2007). The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res. 15, 147–161.PubMedCrossRefGoogle Scholar
  32. Huynh, K.D. and Lee, J.T. (2003). Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 426, 857–862.PubMedCrossRefGoogle Scholar
  33. Kelly, W.G. and Aramayo, R. (2007). Meiotic silencing and the epigenetics of sex. Chromosome Res. 15(5), 633–51.PubMedCrossRefGoogle Scholar
  34. Khalil, A.M., Boyar, F.Z. and Driscoll, D.J. (2004) Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis. Proc. Natl. Acad.Sci. 101, 16583–16587PubMedCrossRefGoogle Scholar
  35. Khil, P.P., Smirnova, N.A., Romanienko, P.J. and Camerini-Otero, R.D. (2004). The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet. 36, 642–664.PubMedCrossRefGoogle Scholar
  36. Lahn B.T., Page D.C. (1999). Four evolutionary strata on the human X chromosome. Science. 286, 964–967.PubMedCrossRefGoogle Scholar
  37. Lee, D.W., Pratt, R.J., McLaughlin, M. and Aramayo, R. (2003). An argonaute-like protein is required for meiotic silencing. Genetics 164, 821–828Google Scholar
  38. Lydall D., Nikolsky Y., Bishop D.K. and Weinert T. (1996). A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature. 383, 840–843.PubMedCrossRefGoogle Scholar
  39. Mahadevaiah, S.K., Bourc’his, D., de Rooj, D.G., Bestor, T.H., Turner, J.M.A. and Burgoyne, P.S. (2008). Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J Cell Biol. 182(2), 263–76.PubMedCrossRefGoogle Scholar
  40. Mahadevaiah, S.K., Turner, J.M., Baudat, F., Rogakou, E.P., de Boer, P., Blanco-Rodriguez, J., Jasin, M., Keeney, S., Bonner, W.M. and Burgoyne, P.S. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet. 27, 271–276.PubMedCrossRefGoogle Scholar
  41. Maine, E. M., J. Hauth, T. Ratliff, V. E. Vought, X. She et al., (2005). EGO-1, a putative RNA-dependent RNA polymerase, is required for heterochromatin assembly on unpaired dna during C. elegans meiosis. Curr Bio. 15, 1972–1978.Google Scholar
  42. Martienssen, R. A., Zaratiegui, M. and Goto, D. B. (2005), RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe Trends Genet 21: 450–456.CrossRefGoogle Scholar
  43. McCarrey JR. (2001). X-chromosome inactivation during spermatogenesis: The original dosage compensation mechanism in mammals? In: Xue G, Xue Y, Xu Z, Holmes R, Hammond GL, Lim HA, editors. Gene families: Studies of DNA, RNA, enzymes and proteins. New Jersey: World Scientific. pp. 59–72.Google Scholar
  44. McKee, B.D. and Handel, M.A. (1993). Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102, 71–80.PubMedCrossRefGoogle Scholar
  45. Moens, P.B., Chen, D.J., Shen, Z., Kolas, N., Tarsounas, M., Heng, H.H.Q. and Spyropoulos, B. (1997). Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosome. 106(4), 207–15.CrossRefGoogle Scholar
  46. Mueller J., Mahadevaiah L., Park S.K., Klarburton P.J., Page D.C. and Turner, J.M. (2008). The mouse X Chromosome is enriched for multicopy tested genes showing post-meiotic expression. Nat Genet. 40(6), 794–799.PubMedCrossRefGoogle Scholar
  47. Namekawa, S.H., Park, P.J., Zhang, L.F., Shima, J.E., McCarrey, J.R., Griswold, M.D. and Lee, J.T. (2006). Postmeiotic sex chromatin in the male germline of mice. Curr Biol. 16, 660–667.PubMedCrossRefGoogle Scholar
  48. Odorisio T., Rodriguez T.A., Evans E.P., Clarke A.R. and Burgoyne P.S. (1998). The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet. 18, 257–261.PubMedCrossRefGoogle Scholar
  49. Okamoto, I., Otte, A.P., Allis, C.D., Reinberg, D. and Heard, E. (2004). Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303, 644–649.Google Scholar
  50. Okamoto I., Arnaud D., Le Baccon P., Otte A.P., Disteche C.M., Avner P. and Heard E. (2005). Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice. Nature. 438, 369–373.PubMedCrossRefGoogle Scholar
  51. Ooi S.L., Priess J.R. and Henikoff S. (2006). Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet. 2, e97.PubMedCrossRefGoogle Scholar
  52. Padmore R., Cao L. and Kleckner N. (1991). Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 66, 1239–1256.PubMedCrossRefGoogle Scholar
  53. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, et al. (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science. 299, 697–700.PubMedCrossRefGoogle Scholar
  54. Peters A.H., Plug A.W. and de Boer P. (1997). Meiosis in carriers of heteromorphic bivalents: sex differences and implications for male fertility. Chromosome Res. 5, 313–324.PubMedCrossRefGoogle Scholar
  55. Pittman D.L., Cobb J., Schimenti K.J., Wilson L.A., Cooper D.M., Brignull E., Handel M.A., Schimenti J.C. (1998). Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell. 1, 697–705.PubMedCrossRefGoogle Scholar
  56. Pratt, R.J., Lee D.W. and Aramayo, R. (2004). DNA Methylation Affects Meiotic trans-sensing, Not Meiotic Silencing, in Neurospora. Genetics. 168, 1925–1935.PubMedCrossRefGoogle Scholar
  57. Raju, N. B., (1992) Genetic control of the sexual cycle in Neurospora. Mycological Research 96, 241–262.CrossRefGoogle Scholar
  58. Rassoulzadegan, M., Magliano, M. and Cuzin, F. (2002). Transvection effects involving DNA methylation during meiosis in the mouse. EMBO J. 21, 440–450PubMedCrossRefGoogle Scholar
  59. Reinke V., Gil I.S., Ward S. and Kazmer K. (2004). Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development. 131, 311–323.PubMedCrossRefGoogle Scholar
  60. Reynard L.N., Turner J.M., Cocquet J., Mahadevaiah S.K., Touré A., Höög C. and Burgoyne P.S. (2007). Expression analysis of the mouse multi-copy X-linked gene Xlr-related, meiosis-regulated (Xmr), reveals that Xmr encodes a spermatid-expressed cytoplasmic protein, SLX/XMR. Biol Reprod. 77, 329–335.PubMedCrossRefGoogle Scholar
  61. Rice, W.R. (1984). Sex-chromosomes and the evolution of sexual dimorphism. Evolution 38, {735–742}.CrossRefGoogle Scholar
  62. Rodriguez T.A. and Burgoyne P.S. (2000). Evidence that sex chromosome asynapsis, rather than excess Y gene dosage, is responsible for the meiotic impairment of XYY mice. Cytogenet Cell Genet. 89, 38–43.PubMedCrossRefGoogle Scholar
  63. Roeder G.S and Bailis J.M. (2000). The pachytene checkpoint. Trends Genet. 16, 395–403.PubMedCrossRefGoogle Scholar
  64. Schimenti, J. (2005). Synapsis or silence. Nat Genet. 37, 11–13.PubMedCrossRefGoogle Scholar
  65. Shevchenko, A., Zakharova, I., Elisaphenko, E., Kolesnikov, N., Whitehead, S., Bird, C., Ross, M., Weidman, J., Jirtle, R., Karamysheva, T., Rubtsov, N., VandeBerg, J., Mazurok, N., Nesterova, T., Brockdorff, N. and Zakian, S. (2007). Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials. Chromosome Res. 15(2), 127–86.PubMedCrossRefGoogle Scholar
  66. Shiu PK, Raju NB, Zickler D, and Metzenberg RL. (2001). Meiotic silencing by unpaired DNA. Cell 107, 905–916.PubMedCrossRefGoogle Scholar
  67. Solari, A. J. (1974). The behavior of the XY pair in mammals. Rev. Cytol. 38, 273–317.CrossRefGoogle Scholar
  68. Speed, R.M. (1986). Oocyte development in XO foetuses of man and mouse: the possible role of heterologous X-chromosome pairing in germ cell survival. Chromosoma 94, 115–124.PubMedCrossRefGoogle Scholar
  69. Tanphaichitr N., Sobhon P., Taluppeth N. and Chalermisarachai P. (1978). Basic nuclear proteins in testicular cells and ejaculated spermatozoa in man. Exp Cell Res. 117, 347–356.PubMedCrossRefGoogle Scholar
  70. Toure, A., Szot, M., Mahadevaiah, S.K., Rattigan, A., Ojarikre, O.A. and Burgoyne, P.S. (2004). A new deletion of the mouse Y chromosome long arm associated with the loss of Ssty expression, abnormal sperm development and sterility.Genetics 166, 901–912.PubMedCrossRefGoogle Scholar
  71. Turner, J.M., Aprelikova, O., Xu, X., Wang, R., Kim, S., Chandramouli, G.V., Barrett, J.C., Burgoyne, P.S. and Deng, C.X. (2004). BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol. 14, 2135–2142.PubMedCrossRefGoogle Scholar
  72. Turner, J.M., Mahadevaiah, S.K., Fernandez-Capetillo, O., Nussenzweig, A., Xu, X., Deng, C.X. and Burgoyne, P.S. (2005). Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet. 37, 41–47.PubMedGoogle Scholar
  73. Turner, J.M., Mahadevaiah, S.K., Ellis, P.J., Mitchell, M.J. and Burgoyne PS. (2006). Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell. 10, 521–529.PubMedCrossRefGoogle Scholar
  74. Turner, J.M. (2007). Meiotic sex chromosome inactivation. Development. 134, 1823–1831.PubMedCrossRefGoogle Scholar
  75. VandeBerg J.L. (1983). Developmental aspects of X chromosome inactivation in eutherian and metatherian mammals. J Exp Zool. 228(2), 271–86.CrossRefGoogle Scholar
  76. van der Heijden G.W., Derijck A.A., Pósfai E., Giele M., Pelczar P., Ramos L., Wansink D.G., van der Vlag J., Peters A.H. and de Boer P. (2007). Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet. 39, 251–258.PubMedCrossRefGoogle Scholar
  77. Wang, P.J. (2004). X chromosomes, retrogenes and their role in male reproduction. Trends Endocrinol Metab. 15, 79–83.PubMedCrossRefGoogle Scholar
  78. Xu, X., Aprelikova, O., Moens, P., Deng, C.X. and Furth, P.A.(2003). Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice. Development 130, 2001–2012.Google Scholar
  79. Yang F., De La Fuente R., Leu N.A., Baumann C., McLaughlin K.J. and Wang P.J. (2006). Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol. 173, 497–507.PubMedCrossRefGoogle Scholar
  80. Yoshida K., Kondoh G., Matsuda Y., Habu T., Nishimune Y. and Morita T. (1998). The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cell. 1, 707–718.PubMedCrossRefGoogle Scholar
  81. Yoshioka H., Geyer C.B., Hornecker J.L., Patel K.T. and McCarrey J.R. (2007). In Vivo Analysis of Developmentally and Evolutionarily Dynamic Protein-DNA Interactions Regulating Transcription of the Pgk2 Gene during Mammalian Spermatogenesis. Mol Cell Biol. 27, 7871–7885.Google Scholar
  82. Yuan L., Liu J.G., Zhao J., Brundell E., Daneholt B. and Höög C. (2000). The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell. 5, 73–83.PubMedCrossRefGoogle Scholar
  83. Zickler D, and Kleckner N. (1998). The leptotene-zygotene transition of meiosis. Annu Rev Genet. 32, 619–697.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • James M.A. Turner
    • 1
  1. 1.Division of Stem Cell Research and Developmental GeneticsMRC National Institute for Medical ResearchLondonUK

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