Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

The consequences of asynapsis for mammalian meiosis

Abstract

During mammalian meiosis, synapsis of paternal and maternal chromosomes and the generation of DNA breaks are needed to allow reshuffling of parental genes. In mammals errors in synapsis are associated with a male-biased meiotic impairment, which has been attributed to a response to persisting DNA double-stranded breaks in the asynapsed chromosome segments. Recently it was discovered that the chromatin of asynapsed chromosome segments is transcriptionally silenced, providing new insights into the connection between asynapsis and meiotic impairment.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: An overview of meiosis.
Figure 2: Meiotic sex chromosome inactivation (MSCI) and the consequences of its failure.
Figure 3: Meiotic silencing as a potential cause of meiotic or post-meiotic failure.
Figure 4: The consequences of asynapsis in male and female meiosis.

Similar content being viewed by others

References

  1. de Boer, P. & de Jong, J. H. in Fertility and Chromosome Pairing: Recent Studies in Plants and Animals (ed. Gillies, C. B.) 37–76 (CRC, Boca Raton, Florida, 1989).

    Google Scholar 

  2. Vincent, M. C. et al. Cytogenetic investigations of infertile men with low sperm counts: a 25-year experience. J. Androl. 23, 18–22; discussion 44–45 (2002).

    PubMed  Google Scholar 

  3. Cohen, P. E., Pollack, S. E. & Pollard, J. W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr. Rev. 27, 398–426 (2006).

    CAS  PubMed  Google Scholar 

  4. Hunt, P. A. & Hassold, T. J. Sex matters in meiosis. Science 296, 2181–2183 (2002).

    CAS  PubMed  Google Scholar 

  5. Morelli, M. A. & Cohen, P. E. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130, 761–781 (2005).

    CAS  PubMed  Google Scholar 

  6. Wang, H. & Hoog, C. Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes. J. Cell Biol. 173, 485–495 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Hassold, T. & Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nature Rev. Genet. 2, 280–291 (2001).

    CAS  PubMed  Google Scholar 

  8. Baarends, W. M. et al. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol. Cell Biol. 25, 1041–1053 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Turner, J. M. et al. Silencing of unsynapsed meiotic chromosomes in the mouse. Nature Genet. 37, 41–47 (2005).

    CAS  PubMed  Google Scholar 

  10. Turner, J. M., Mahadevaiah, S. K., Ellis, P. J., Mitchell, M. J. & Burgoyne, P. S. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev. Cell 10, 521–529 (2006).

    CAS  PubMed  Google Scholar 

  11. Ferguson, K. A., Chow, V. & Ma, S. Silencing of unpaired meiotic chromosomes and altered recombination patterns in an azoospermic carrier of a t(8;13) reciprocal translocation. Hum. Reprod. 23, 988–995 (2008).

    CAS  PubMed  Google Scholar 

  12. Sciurano, R., Rahn, M., Rey-Valzacchi, G. & Solari, A. J. The asynaptic chromatin in spermatocytes of translocation carriers contains the histone variant γ-H2AX and associates with the XY body. Hum. Reprod. 22, 142–50 (2007).

    CAS  PubMed  Google Scholar 

  13. Hochwagen, A. & Amon, A. Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 16, R217–R228 (2006).

    CAS  PubMed  Google Scholar 

  14. Roeder, G. S. & Bailis, J. M. The pachytene checkpoint. Trends Genet. 16, 395–403 (2000).

    CAS  PubMed  Google Scholar 

  15. Ashley, T. in Results and Problems in Cell Differentiation Vol. 28 (ed. McElreavey, K.) 131–173 (Springer, Berlin, 2000).

    Google Scholar 

  16. de Rooij, D. G. & de Boer, P. Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet. Genome Res. 103, 267–276 (2003).

    CAS  PubMed  Google Scholar 

  17. Burgoyne, P. S. & Baker, T. G. Perinatal oocyte loss in XO mice and its implications for the aetiology of gonadal dysgenesis in XO women. J. Reprod. Fertil. 75, 633–645 (1985).

    CAS  PubMed  Google Scholar 

  18. Burgoyne, P. S., Mahadevaiah, S. K. & Mittwoch, U. A reciprocal autosomal translocation which causes male sterility in the mouse also impairs oogenesis. J. Reprod. Fertil. 75, 647–652 (1985).

    CAS  PubMed  Google Scholar 

  19. Mittwoch, U., Mahadevaiah, S. K. & Setterfield, L. A. Pachytene pairing and oocyte numbers in mice with two single Robertsonian translocations and the male-sterile compound with monobrachial homology. Cytogenet. Cell Genet. 53, 144–147 (1990).

    CAS  PubMed  Google Scholar 

  20. Setterfield, L. A., Mahadevaiah, S. K. & Mittwoch, U. Chromosome pairing and germ cell loss in male and female mice carrying a reciprocal translocation. J. Reprod. Fertil. 82, 369–379 (1988).

    CAS  PubMed  Google Scholar 

  21. Pittman, D. L. et al. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1, 697–705 (1998).

    CAS  PubMed  Google Scholar 

  22. Yoshida, K. et al. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell 1, 707–718 (1998).

    CAS  PubMed  Google Scholar 

  23. Romanienko, P. J. & Camerini-Otero, R. D. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell 6, 975–987 (2000).

    CAS  PubMed  Google Scholar 

  24. Baudat, F., Manova, K., Yuen, J. P., Jasin, M. & Keeney, S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell 6, 989–998 (2000).

    CAS  PubMed  Google Scholar 

  25. Edelmann, W. et al. Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nature Genet. 21, 123–127 (1999).

    CAS  PubMed  Google Scholar 

  26. Kneitz, B. et al. MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14, 1085–1097 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. de Vries, F. A. et al. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19, 1376–1389 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Libby, B. J. et al. The mouse meiotic mutation mei1 disrupts chromosome synapsis with sexually dimorphic consequences for meiotic progression. Dev. Biol. 242, 174–187 (2002).

    CAS  PubMed  Google Scholar 

  29. de Vries, S. S. et al. Mouse MutS-like protein MSH5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13, 523–531 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Deckbar, D. et al. Chromosome breakage after G2 checkpoint release. J. Cell Biol. 176, 749–755 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Marcon, E. & Moens, P. B. The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bioessays 27, 795–808 (2005).

    CAS  PubMed  Google Scholar 

  32. Burgoyne, P. S., Mahadevaiah, S. K. & Turner, J. M. The management of DNA double-strand breaks in mitotic G2, and in mammalian meiosis viewed from a mitotic G2 perspective. Bioessays 29, 974–986 (2007).

    CAS  PubMed  Google Scholar 

  33. Plug, A. W. et al. Changes in protein composition of meiotic nodules during mammalian meiosis. J. Cell Sci. 111, 413–423 (1998).

    CAS  PubMed  Google Scholar 

  34. Keegan, K. S. et al. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10, 2423–2437 (1996).

    CAS  PubMed  Google Scholar 

  35. Moens, P. B. et al. The association of ATR protein with mouse meiotic chromosome cores. Chromosoma 108, 95–102 (1999).

    CAS  PubMed  Google Scholar 

  36. Perera, D. et al. TopBP1 and ATR colocalization at meiotic chromosomes: role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol. Biol. Cell 15, 1568–1579 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Turner, J. M. et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr. Biol. 14, 2135–42 (2004).

    CAS  PubMed  Google Scholar 

  38. Scully, R. et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88, 265–275 (1997).

    CAS  PubMed  Google Scholar 

  39. Mahadevaiah, S. K. et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nature Genet. 27, 271–276 (2001).

    CAS  PubMed  Google Scholar 

  40. Mahadevaiah, S. K. et al. Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J. Cell Biol. 182, 263–276 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Barchi, M. et al. Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell Biol. 25, 7203–7215 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Hamer, G., Kal, H. B., Westphal, C. H., Ashley, T. & de Rooij, D. G. Ataxia telangiectasia mutated expression and activation in the testis. Biol. Reprod. 70, 1206–1212 (2004).

    CAS  PubMed  Google Scholar 

  43. Bolcun-Filas, E. et al. SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol. 176, 741–747 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Ashley, T., Gaeth, A. P., Creemers, L. B., Hack, A. M. & de Rooij, D. G. Correlation of meiotic events in testis sections and microspreads of mouse spermatocytes relative to the mid-pachytene checkpoint. Chromosoma 113, 126–136 (2004).

    PubMed  Google Scholar 

  45. O'Doherty, A. et al. An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science 309, 2033–2037 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Habermann, B. et al. DAZ (Deleted in AZoospermia) genes encode proteins located in human late spermatids and sperm tails. Hum. Reprod. 13, 363–369 (1998).

    CAS  PubMed  Google Scholar 

  47. Turner, J. M. A. & Burgoyne, P. S. in The Y Chromosome and Male Germ Cell Biology in Health and Diseases (eds Lau, Y.-F. C. & Chan, W. Y.) 27–46 (World Scientific, Hackensack, New Jersey, 2006).

    Google Scholar 

  48. Handel, M. A. The XY body: a specialized meiotic chromatin domain. Exp. Cell Res. 296, 57–63 (2004).

    CAS  PubMed  Google Scholar 

  49. Khil, P. P., Smirnova, N. A., Romanienko, P. J. & Camerini-Otero, R. D. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nature Genet. 36, 642–646 (2004).

    CAS  PubMed  Google Scholar 

  50. Monesi, V. Synthetic activities during spermatogenesis in the mouse. Exp. Cell Res. 39, 197–224 (1965).

    CAS  PubMed  Google Scholar 

  51. Moore, G. P. DNA-dependent RNA synthesis in fixed cells during spermatogenesis in mouse. Exp. Cell Res. 68, 462–465 (1971).

    CAS  PubMed  Google Scholar 

  52. Namekawa, S. H. et al. Postmeiotic sex chromatin in the male germline of mice. Curr. Biol. 16, 660–667 (2006).

    CAS  PubMed  Google Scholar 

  53. Turner, J. M. Meiotic sex chromosome inactivation. Development 134, 1823–1831 (2007).

    CAS  PubMed  Google Scholar 

  54. Solari, A. J. The behaviour of the XY pair in mammals. Int. Rev. Cytol. 38, 273–317 (1974).

    CAS  PubMed  Google Scholar 

  55. Fernandez-Capetillo, O. et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4, 497–508 (2003).

    CAS  PubMed  Google Scholar 

  56. Xu, X., Aprelikova, O., Moens, P., Deng, C. X. & Furth, P. A. Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice. Development 130, 2001–2012 (2003).

    CAS  PubMed  Google Scholar 

  57. Bellani, M. A., Romanienko, P. J., Cairatti, D. A. & Camerini-Otero, R. D. SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm−/− spermatocytes. J. Cell Sci. 118, 3233–3245 (2005).

    CAS  PubMed  Google Scholar 

  58. Bourc'his, D. & Bestor, T. H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96–9 (2004).

    CAS  PubMed  Google Scholar 

  59. Homolka, D., Ivanek, R., Capkova, J., Jansa, P. & Forejt, J. Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res. 17, 1431–1437 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Kolas, N. K. et al. Mutant meiotic chromosome core components in mice can cause apparent sexual dimorphic endpoints at prophase or X-Y defective male-specific sterility. Chromosoma 114, 92–102 (2005).

    PubMed  Google Scholar 

  61. Li, X. C. & Schimenti, J. C. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet. 3, e130 (2007).

    PubMed  PubMed Central  Google Scholar 

  62. Schimenti, J. Synapsis or silence. Nature Genet. 37, 11–13 (2005).

    CAS  PubMed  Google Scholar 

  63. Shiu, P. K., Raju, N. B., Zickler, D. & Metzenberg, R. L. Meiotic silencing by unpaired DNA. Cell 107, 905–916 (2001).

    CAS  PubMed  Google Scholar 

  64. Schoenmakers, S. et al. Increased frequency of asynapsis and associated meiotic silencing of heterologous chromatin in the presence of irradiation-induced extra DNA double strand breaks. Dev. Biol. 317, 270–281 (2008).

    CAS  PubMed  Google Scholar 

  65. Oakberg, E. F. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am. J. Anat. 99, 507–516 (1956).

    CAS  PubMed  Google Scholar 

  66. Wang, P. J. X chromosomes, retrogenes and their role in male reproduction. Trends Endocrinol. Metab. 15, 79–83 (2004).

    PubMed  Google Scholar 

  67. Rohozinski, J. & Bishop, C. E. The mouse juvenile spermatogonial depletion (jsd) phenotype is due to a mutation in the X-derived retrogene, mUtp14b. Proc. Natl Acad. Sci. USA 101, 11695–11700 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Bradley, J. et al. An X-to-autosome retrogene is required for spermatogenesis in mice. Nature Genet. 36, 872–876 (2004).

    CAS  PubMed  Google Scholar 

  69. Zhao, M. et al. Utp14b: a unique retrogene within a gene that has acquired multiple promoters and a specific function in spermatogenesis. Dev. Biol. 304, 848–859 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Khalil, A. M., Boyar, F. Z. & Driscoll, D. J. Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis. Proc. Natl Acad. Sci. USA 101, 16583–16587 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. van der Heijden, G. W. et al. Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nature Genet. 39, 251–258 (2007).

    CAS  PubMed  Google Scholar 

  72. Greaves, I. K., Rangasamy, D., Devoy, M., Marshall Graves, J. A. & Tremethick, D. J. The X and Y chromosomes assemble into H2A.Z, containing facultative heterochromatin, following meiosis. Mol. Cell Biol. 26, 5394–405 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Mueller, J. L. et al. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nature Genet. 40, 794–799 (2008).

    CAS  PubMed  Google Scholar 

  74. Peters, A. H., Plug, A. W. & de Boer, P. Meiosis in carriers of heteromorphic bivalents: sex differences and implications for male fertility. Chromosome Res. 5, 313–324 (1997).

    CAS  PubMed  Google Scholar 

  75. van der Laan, R. 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. 117, 5023–33 (2004).

    CAS  PubMed  Google Scholar 

  76. Di Giacomo, M. et al. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc. Natl Acad. Sci. USA 102, 737–742 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Sugimoto, M. & Abe, K. X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet. 3, e116 (2007).

    PubMed  PubMed Central  Google Scholar 

  78. Chuva de Sousa Lopes, S. M. et al. X chromosome activity in mouse XX primordial germ cells. PLoS Genet. 4, e30 (2008).

    Google Scholar 

  79. de Napoles, M., Nesterova, T. & Brockdorff, N. Early loss of Xist RNA expression and inactive X chromosome associated chromatin modification in developing primordial germ cells. PLoS ONE 2, e860 (2007).

    PubMed  PubMed Central  Google Scholar 

  80. Speed, R. M. 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 (1986).

    CAS  PubMed  Google Scholar 

  81. Celeste, A. et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biol. 5, 675–679 (2003).

    CAS  PubMed  Google Scholar 

  82. Wang, W. H. & Sun, Q. Y. Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Front. Biosci. 11, 620–636 (2006).

    CAS  PubMed  Google Scholar 

  83. Petronczki, M., Siomos, M. F. & Nasmyth, K. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112, 423–440 (2003).

    CAS  PubMed  Google Scholar 

  84. Yamamoto, A. et al. Spindle checkpoint activation at meiosis I advances anaphase II onset via meiosis-specific APC/C regulation. J. Cell Biol. 182, 277–288 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Ashley, T., Ried, T. & Ward, D. C. Detection of nondisjunction and recombination in meiotic and postmeiotic cells from XYSxr [XY, Tp(Y)1Ct] mice using multicolor fluorescence in situ hybridization. Proc. Natl Acad. Sci. USA 91, 524–528 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Burgoyne, P. S., Mahadevaiah, S. K., Sutcliffe, M. J. & Palmer, S. J. Fertility in mice requires X-Y pairing and a Y-chromosomal 'spermiogenesis' gene mapping to the long arm. Cell 71, 391–398 (1992).

    CAS  PubMed  Google Scholar 

  87. Evans, E. P., Burtenshaw, M. D. & Cattanach, B. M. Meiotic crossing over between the X and Y chromosomes of male mice carrying the sex-reversing (Sxr) factor. Nature 300, 443–445 (1982).

    CAS  PubMed  Google Scholar 

  88. Odorisio, T., Rodriguez, T. A., Evans, E. P., Clarke, A. R. & Burgoyne, P. S. The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nature Genet. 18, 257–261 (1998).

    CAS  PubMed  Google Scholar 

  89. Eaker, S., Pyle, A., Cobb, J. & Handel, M. A. Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. J. Cell Sci. 114, 2953–2965 (2001).

    CAS  PubMed  Google Scholar 

  90. Vogt, E., Kirsch-Volders, M., Parry, J. & Eichenlaub-Ritter, U. Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat. Res. 651, 14–29 (2008).

    CAS  PubMed  Google Scholar 

  91. Hunt, P., LeMaire, R., Embury, P., Sheean, L. & Mroz, K. Analysis of chromosome behaviour in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum. Mol. Genet. 4, 2007–2012 (1995).

    CAS  PubMed  Google Scholar 

  92. LeMaire-Adkins, R., Radke, K. & Hunt, P. A. Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J. Cell Biol. 139, 1611–1619 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Hodges, C. A., LeMaire-Adkins, R. & Hunt, P. A. Coordinating the segregation of sister chromatids during the first meiotic division: evidence for sexual dimorphism. J. Cell Sci. 114, 2417–2426 (2001).

    CAS  PubMed  Google Scholar 

  94. Hodges, C. A., Revenkova, E., Jessberger, R., Hassold, T. J. & Hunt, P. A. SMC1β-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nature Genet. 37, 1351–1355 (2005).

    CAS  PubMed  Google Scholar 

  95. Hunt, P. A. & Hassold, T. J. Human female meiosis: what makes a good egg go bad? Trends Genet. 24, 86–93 (2008).

    CAS  PubMed  Google Scholar 

  96. Jones, K. T. Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum. Reprod. Update 14, 143–158 (2008).

    CAS  PubMed  Google Scholar 

  97. Kouznetsova, A., Lister, L., Nordenskjold, M., Herbert, M. & Hoog, C. Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nature Genet. 39, 966–968 (2007).

    CAS  PubMed  Google Scholar 

  98. Lyon, M. F. & Hawker, S. G. Reproductive lifespan in irradiated and unirradiated chromosomally XO mice. Genet. Res. 21, 185–194 (1973).

    CAS  PubMed  Google Scholar 

  99. Woods, L. M. et al. Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J. Cell Biol. 145, 1395–1406 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Zickler, D. & Kleckner, N. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603–754 (1999).

    CAS  PubMed  Google Scholar 

  101. Moses, M. J. & Poorman, P. A. in Chromosomes Today Vol. 8 (eds Bennet, M. D., Gropp, A. & Wolf, U.) 80–103 (Allen and Unwin, London, 1984).

    Google Scholar 

  102. Baudat, F., Manova, K., Yuen, J. P., Jasin, M. & Keeney, S. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Cell 6, 989–998 (2000).

    CAS  Google Scholar 

  103. Wang, X. & Haber, J. E. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2, E21 (2004).

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul S. Burgoyne.

Related links

Related links

DATABASES

OMIM

ATM

ATR

BRCA1

H2AX

FURTHER INFORMATION

Burgoyne group homepage

Turner group homepage

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burgoyne, P., Mahadevaiah, S. & Turner, J. The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10, 207–216 (2009). https://doi.org/10.1038/nrg2505

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg2505

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing