Homologue engagement controls meiotic DNA break number and distribution

Nature

Volumn 510, Issue 7504, 2014, Pages 241-246

  Thacker, Drew ^a,b   Mohibullah, Neeman ^a   Zhu, Xuan ^a,b   Keeney, Scott ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA HOMOLOG; OLIGONUCLEOTIDE; PROTEIN ZMM; REGULATOR PROTEIN; SPO11 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NDT80; UNCLASSIFIED DRUG;

CHROMOSOME; DNA; GENETIC DIFFERENTIATION; HOMOLOGY; MUTATION; PROTEIN; RECOMBINATION;

ARTICLE; CHROMOSOME SIZE; CHROMOSOME STRUCTURE; COMPLEX FORMATION; DOUBLE STRANDED DNA BREAK; MEIOSIS; MEIOTIC RECOMBINATION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

CHROMOSOME PAIRING; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; EPISTASIS, GENETIC; GENOME, FUNGAL; HOMOLOGOUS RECOMBINATION; MEIOSIS; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84902344047     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13120     Document Type: Article

References (41)

1. Keeney, S. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1-53 (2001).
2. Lange, J. et al. ATM controls meiotic double-strand-break formation. Nature 479, 237-240 (2011).
3. Joyce, E. F. et al. Drosophila ATMand ATR have distinct activities in the regulation of meiotic DNA damage and repair. J. Cell Biol. 195, 359-367 (2011).
4. Zhang, L., Kim, K. P., Kleckner, N. E. & Storlazzi, A. 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).
5. Carballo, J. A. et al. Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSBmachinery. PLoS Genet. 9, e1003545 (2013).
6. Bhagat, R., Manheim, E. A., Sherizen, D. E. & McKim, K. S. Studies on crossoverspecific mutants and the distribution of crossing over in Drosophila females. Cytogenet. Genome Res. 107, 160-171 (2004).
7. Henzel, J. V. et al. An asymmetric chromosome pair undergoes synaptic adjustment and crossover redistribution during Caenorhabditis elegans meiosis: implications for sex chromosome evolution. Genetics 187, 685-699 (2011).
8. Kauppi, L. et al. Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev. 27, 873-886 (2013).
9. Lynn, A., Soucek, R. & Borner, G. V. ZMMproteins during meiosis: crossover artists at work. Chromosome Res. 15, 591-605 (2007).
10. Neale, M. J., Pan, J. & Keeney, S. Endonucleolytic processing of covalent proteinlinked DNA double-strand breaks. Nature 436, 1053-1057 (2005).
11. Pan, J. et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144, 719-731 (2011).
12. Xu, L., Ajimura, M., Padmore, R., Klein, C. & Kleckner, N. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 6572-6581 (1995).
13. Sym, M., Engebrecht, J. A. & Roeder, G. S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72, 365-378 (1993).
14. Ross-Macdonald, P. & Roeder, G. S. Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79, 1069-1080 (1994).
15. Hollingsworth, N. M., Ponte, L.&Halsey, C.MSH5, a novelMutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev. 9, 1728-1739 (1995).
16. Chua, P. R. & Roeder, G. S. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93, 349-359 (1998).
17. Agarwal, S. & Roeder, G. S. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102, 245-255 (2000).
18. Tsubouchi, T., Zhao, H. & Roeder, G. S. The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev. Cell 10, 809-819 (2006).
19. Shinohara, M., Oh, S. D., Hunter, N. & Shinohara, A. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nature Genet. 40, 299-309 (2008).
20. Borner, G. V., Kleckner, N. & Hunter, N. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29-45 (2004).
21. Allers, T. & Lichten, M. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106, 47-57 (2001).
22. Gray, S., Allison, R. M., Garcia, V., Goldman, A. S.& Neale, M. J. Positive regulation of meiotic DNA double-strand break formation by activation of the DNA damage checkpoint kinase Mec1(ATR). Open Biol. 3, 130019 (2013).
23. Rockmill, B. et al. High throughput sequencing reveals alterations in the recombination signatures with diminishing Spo11 activity. PLoS Genet. 9, e1003932 (2013).
24. Tung, K. S., Hong, E. J. & Roeder, G. S. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc. Natl Acad. Sci. USA 97, 12187-12192 (2000).
25. Rosu, S. et al. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genet. 9, e1003674 (2013).
26. Stamper, E. L. et al. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 9, e1003679 (2013).
27. Wojtasz, L. et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet. 5, e1000702 (2009).
28. Smith, A. V.& Roeder, G. S. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136, 957-967 (1997).
29. Kee, K., Protacio, R. U., Arora, C. & Keeney, S. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J. 23, 1815-1824 (2004).
30. Chen, S. Y. et al. Global analysis of the meiotic crossover landscape. Dev. Cell 15, 401-415 (2008).
31. Nakagawa, T. & Ogawa, H. The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control inmeiosis.EMBOJ. 18, 5714-5723 (1999).
32. Jessop, L., Rockmill, B., Roeder, G. S. & Lichten, M. Meiotic chromosome synapsispromoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet. 2, e155 (2006).
33. Falk, J. E., Chan, A. C., Hoffmann, E. & Hochwagen, A. A. Mec1-and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev. Cell 19, 599-611 (2010).
34. Lichten, M. in Recombination and Meiosis: Models, Means, and Evolution Vol. 3 (eds R. Egel & D. H. Lankenau) 165-193 (Springer-Verlag, 2008).
35. Kaback, D. B., Guacci, V., Barber, D. & Mahon, J. W. Chromosome size-dependent control of meiotic recombination. Science 256, 228-232 (1992).
36. Blitzblau, H. G., Bell, G. W., Rodriguez, J., Bell, S. P. & Hochwagen, A. Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres. Curr. Biol. 17, 2003-2012 (2007).
37. Buhler, C., Borde, V. & Lichten, M. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol. 5, e324 (2007).
38. Panizza, S. et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146, 372-383 (2011).
39. Serrentino, M. E.,Chaplais, E.,Sommermeyer, V.&Borde, V. Differential association of the conserved SUMOligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet. 9, e1003416 (2013).
40. Borde, V. & de Massy, B. Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr. Opin. Genet. Dev. 23, 147-155 (2013).
41. Pineda-Krch, M. & Redfield, R. J. Persistence and loss of meiotic recombination hotspots. Genetics 169, 2319-2333 (2005).