Homeostatic control of recombination is implemented progressively in mouse meiosis (original) (raw)

References

  1. Hassold, T., Hall, H. & Hunt, P. The origin of human aneuploidy: where we have been, where we are going. Hum. Mol. Genet. 16 (Spec No. 2), R203–R208 (2007).
    Article CAS Google Scholar
  2. Keeney, S. in Recombination and Meiosis (eds Egel, R. & Lankenau, D-H.) 81–123 (Springer, 2007).
    Google Scholar
  3. Chen, S. Y. et al. Global analysis of the meiotic crossover landscape. Dev. Cell 15, 401–415 (2008).
    Article CAS Google Scholar
  4. Hillers, K. J. & Villeneuve, A. M. Chromosome-wide control of meiotic crossing over in C. elegans. Curr. Biol. 13, 1641–1647 (2003).
    Article CAS Google Scholar
  5. Martini, E., Diaz, R. L., Hunter, N. & Keeney, S. Crossover homeostasis in yeast meiosis. Cell 126, 285–295 (2006).
    Article CAS Google Scholar
  6. Roig, I. & Keeney, S. Probing meiotic recombination decisions. Dev. Cell 15, 331–332 (2008).
    Article CAS Google Scholar
  7. Youds, J. L. et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327, 1254–1258 (2010).
    Article CAS Google Scholar
  8. Rosu, S., Libuda, D. E. & Villeneuve, A. M. Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334, 1286–1289 (2011).
    Article CAS Google Scholar
  9. Jones, G. H. & Franklin, F. C. Meiotic crossing-over: obligation and interference. Cell 126, 246–248 (2006).
    Article CAS Google Scholar
  10. 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).
    Article CAS Google Scholar
  11. Anderson, L. K., Reeves, A., Webb, L. M. & Ashley, T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151, 1569–1579 (1999).
    CAS PubMed PubMed Central Google Scholar
  12. Holloway, J. K., Booth, J., Edelmann, W., McGowan, C. H. & Cohen, P. E. MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet. 4, e1000186 (2008).
    Article Google Scholar
  13. 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).
    Article CAS Google Scholar
  14. Kauppi, L. et al. Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331, 916–920 (2011).
    Article CAS Google Scholar
  15. Mahadevaiah, S. K. et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27, 271–276 (2001).
    Article CAS Google Scholar
  16. Larocque, J. R. & Jasin, M. Mechanisms of recombination between diverged sequences in wild-type and BLM-deficient mouse and human cells. Mol. Cell Biol. 30, 1887–1897 (2010).
    Article CAS Google Scholar
  17. Zhang, L., Kleckner, N. E., Storlazzi, A. & Kim, K. P. Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc. Natl Acad. Sci. USA 108, 20036–20041 (2011).
    Article CAS Google Scholar
  18. Kleckner, N. et al. A mechanical basis for chromosome function. Proc. Natl Acad. Sci. USA 101, 12592–12597 (2004).
    Article CAS Google Scholar
  19. Stahl, F. W. & Foss, H. M. A two-pathway analysis of meiotic crossing over and gene conversion in Saccharomyces cerevisiae. Genetics 186, 515–536 (2010).
    Article CAS Google Scholar
  20. de Boer, E., Stam, P., Dietrich, A. J., Pastink, A. & Heyting, C. Two levels of interference in mouse meiotic recombination. Proc. Natl Acad. Sci. USA 103, 9607–9612 (2006).
    Article CAS Google Scholar
  21. Cole, F., Keeney, S. & Jasin, M. Evolutionary conservation of meiotic DSB proteins: more than just Spo11. Genes Dev. 24, 1201–1207 (2010).
    Article CAS Google Scholar
  22. Mancera, E., Bourgon, R., Brozzi, A., Huber, W. & Steinmetz, L. M. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454, 479–485 (2008).
    Article CAS Google Scholar
  23. Dernburg, A. F. et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94, 387–398 (1998).
    Article CAS Google Scholar
  24. Barchi, M. et al. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLoS Genet. 4, e1000076 (2008).
    Article Google Scholar
  25. Lange, J. et al. ATM controls meiotic double-strand-break formation. Nature 479, 237–240 (2011).
    Article CAS Google Scholar
  26. Goldfarb, T. & Lichten, M. Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol. 8, e1000520 (2010).
    Article Google Scholar
  27. Mets, D. G. & Meyer, B. J. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139, 73–86 (2009).
    Article CAS Google Scholar
  28. Cole, F., Keeney, S. & Jasin, M. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39, 700–710 (2010).
    Article CAS Google Scholar
  29. Coop, G., Wen, X., Ober, C., Pritchard, J. K. & Przeworski, M. High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319, 1395–1398 (2008).
    Article CAS Google Scholar
  30. Baker, S. M. et al. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13, 336–342 (1996).
    Article CAS Google Scholar
  31. de Boer, E., Dietrich, A. J., Hoog, C., Stam, P. & Heyting, C. Meiotic interference among MLH1 foci requires neither an intact axial element structure nor full synapsis. J. Cell Sci. 120, 731–736 (2007).
    Article CAS Google Scholar
  32. Koehler, K. E., Schrump, S. E., Cherry, J. P., Hassold, T. J. & Hunt, P. A. Near-human aneuploidy levels in female mice with homeologous chromosomes. Curr. Biol. 16, R579–R580 (2006).
    Article CAS Google Scholar
  33. Ferguson, K. A., Leung, S., Jiang, D. & Ma, S. Distribution of MLH1 foci and inter-focal distances in spermatocytes of infertile men. Hum. Reprod. 24, 1313–1321 (2009).
    Article CAS Google Scholar
  34. Lenzi, M. L. et al. Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis i in human oocytes. Am. J. Hum. Genet. 76, 112–127 (2005).
    Article CAS Google Scholar
  35. Bellani, M. A., Boateng, K. A., McLeod, D. & Camerini-Otero, R. D. The expression profile of the major mouse SPO11 isoforms indicates that SPO11β introduces double strand breaks and suggests that SPO11α has an additional role in prophase in both spermatocytes and oocytes. Mol. Cell Biol. 30, 4391–4403 (2010).
    Article CAS Google Scholar
  36. Heyting, C. & Dietrich, A. J. Meiotic chromosome preparation and protein labeling. Methods Cell Biol. 35, 177–202 (1991).
    Article CAS Google Scholar
  37. Dray, E. et al. Molecular basis for enhancement of the meiotic DMC1 recombinase by RAD51 associated protein 1 (RAD51AP1). Proc. Natl Acad. Sci. USA 108, 3560–3565 (2011).
    Article CAS Google Scholar
  38. Roig, I. et al. Mouse TRIP13/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis. PLoS Genet. 6, e1001062 (2010).
    Article Google Scholar
  39. Neale, M. J., Pan, J. & Keeney, S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053–1057 (2005).
    Article CAS Google Scholar
  40. Cohen, J. Statistical Power Analysis for the Behavioral Sciences 2nd edn (Lawrence Erlbaum Associates, Inc., 1988).
    Google Scholar

Download references