Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis

Cell

Volumn 147, Issue 1, 2011, Pages 158-172

  Matos, Joao ^a   Blanco, Miguel G ^a   Maslen, Sarah ^a   Skehel, J Mark ^a   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; FUNGAL DNA; FUNGAL PROTEIN; MMS4 PROTEIN; MUS81 PROTEIN; UNCLASSIFIED DRUG; YEN1 PROTEIN;

ARTICLE; CELL CYCLE PROGRESSION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CROSSING OVER; DNA RECOMBINATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FUNGAL GENETICS; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; MEIOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; YEAST CELL;

EID: 80053544629     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.08.032     Document Type: Article

References (59)

1. T. Allers, and M. Lichten Differential timing and control of noncrossover and crossover recombination during meiosis Cell 106 2001 47 57 (Pubitemid 32709957)
2. M.G. Blanco, J. Matos, U. Rass, S.C.Y. Ip, and S.C. West Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S. cerevisiae DNA Repair (Amst.) 9 2010 394 402
3. M.N. Boddy, P.H.L. Gaillard, W.H. McDonald, P. Shanahan, J.R. Yates 3rd, and P. Russell Mus81-Eme1 are essential components of a Holliday junction resolvase Cell 107 2001 537 548 (Pubitemid 33152788)
4. R.S. Chaganti, S. Schonberg, and J. German A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes Proc. Natl. Acad. Sci. USA 71 1974 4508 4512
5. S. Chu, J. DeRisi, M. Eisen, J. Mulholland, D. Botstein, P.O. Brown, and I. Herskowitz The transcriptional program of sporulation in budding yeast Science 282 1998 699 705 (Pubitemid 28489376)
6. R.K. Clyne, V.L. Katis, L. Jessop, K.R. Benjamin, I. Herskowitz, M. Lichten, and K. Nasmyth Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I Nat. Cell Biol. 5 2003 480 485 (Pubitemid 36592273)
7. T. de los Santos, N. Hunter, C. Lee, B. Larkin, J. Loidl, and N.M. Hollingsworth The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast Genetics 164 2003 81 94 (Pubitemid 36617695)
8. T. de los Santos, J. Loidl, B. Larkin, and N.M. Hollingsworth A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae Genetics 159 2001 1511 1525 (Pubitemid 34087593)
9. A.E. Elia, P. Rellos, L.F. Haire, J.W. Chao, F.J. Ivins, K. Hoepker, D. Mohammad, L.C. Cantley, S.J. Smerdon, and M.B. Yaffe The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain Cell 115 2003 83 95 (Pubitemid 37255320)
10. W.M. Fricke, and S.J. Brill Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3 Genes Dev. 17 2003 1768 1778 (Pubitemid 36870339)
11. Y. Fu, and W. Xiao Functional domains required for the Saccharomyces cerevisiae Mus81-Mms4 endonuclease complex formation and nuclear localization DNA Repair (Amst.) 2 2003 1435 1447 (Pubitemid 37464820)
12. S. Gangloff, J.P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase Mol. Cell. Biol. 14 1994 8391 8398 (Pubitemid 24373588)
13. J.E. Haber, and W.D. Heyer The fuss about Mus81 Cell 107 2001 551 554 (Pubitemid 34014855)
14. T. Hassold, and P. Hunt To err (meiotically) is human: the genesis of human aneuploidy Nat. Rev. Genet. 2 2001 280 291 (Pubitemid 33674776)
15. C.K. Ho, G. Mazón, A.F. Lam, and L.S. Symington Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast Mol. Cell 40 2010 988 1000
16. N. Hunter, and N. Kleckner The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination Cell 106 2001 59 70 (Pubitemid 32709958)
17. S.C.Y. Ip, U. Rass, M.G. Blanco, H.R. Flynn, J.M. Skehel, and S.C. West Identification of Holliday junction resolvases from humans and yeast Nature 456 2008 357 361
18. G. Ira, A. Malkova, G. Liberi, M. Foiani, and J.E. Haber Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast Cell 115 2003 401 411 (Pubitemid 37456803)
19. L. Jessop, B. Rockmill, G.S. Roeder, and M. Lichten Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1 PLoS Genet. 2 2006 e155
20. V. Kaliraman, J.R. Mullen, W.M. Fricke, S.A. Bastin-Shanower, and S.J. Brill Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease Genes Dev. 15 2001 2730 2740 (Pubitemid 32988882)
21. S. Keeney, C.N. Giroux, and N. Kleckner Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family Cell 88 1997 375 384 (Pubitemid 27131379)
22. K.P. Kim, B.M. Weiner, L.R. Zhang, A. Jordan, J. Dekker, and N. Kleckner Sister cohesion and structural axis components mediate homolog bias of meiotic recombination Cell 143 2010 924 937
23. S. Kosugi, M. Hasebe, M. Tomita, and H. Yanagawa Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs Proc. Natl. Acad. Sci. USA 106 2009 10171 10176
24. B.H. Lee, and A. Amon Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation Science 300 2003 482 486 (Pubitemid 36444328)
25. M. Loog, and D.O. Morgan Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates Nature 434 2005 104 108 (Pubitemid 40349393)
26. J.R. Mullen, V. Kaliraman, S.S. Ibrahim, and S.J. Brill Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae Genetics 157 2001 103 118
27. H. Niu, L. Wan, B. Baumgartner, D. Schaefer, J. Loidl, and N.M. Hollingsworth Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1 Mol. Biol. Cell 16 2005 5804 5818 (Pubitemid 41752228)
28. S.D. Oh, J.P. Lao, P.Y.H. Hwang, A.F. Taylor, G.R. Smith, and N. Hunter BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules Cell 130 2007 259 272 (Pubitemid 47081131)
29. S.D. Oh, J.P. Lao, A.F. Taylor, G.R. Smith, and N. Hunter RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination Mol. Cell 31 2008 324 336
30. F. Osman, J. Dixon, C.L. Doe, and M.C. Whitby Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis Mol. Cell 12 2003 761 774 (Pubitemid 37222495)
31. M. Petronczki, J. Matos, S. Mori, J. Gregan, A. Bogdanova, M. Schwickart, K. Mechtler, K. Shirahige, W. Zachariae, and K. Nasmyth Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1 Cell 126 2006 1049 1064 (Pubitemid 44380290)
32. I. Poser, M. Sarov, J.R. Hutchins, J.K. Hériché, Y. Toyoda, A. Pozniakovsky, D. Weigl, A. Nitzsche, B. Hegemann, and A.W. Bird BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals Nat. Methods 5 2008 409 415 (Pubitemid 351619099)
33. U. Rass, S.A. Compton, J. Matos, M.R. Singleton, S.C.Y. Ip, M.G. Blanco, J.D. Griffith, and S.C. West Mechanism of Holliday junction resolution by the human GEN1 protein Genes Dev. 24 2010 1559 1569
34. B. Rockmill, J.C. Fung, S.S. Branda, and G.S. Roeder The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over Curr. Biol. 13 2003 1954 1962 (Pubitemid 37425204)
35. P. Schöffski Polo-like kinase (PLK) inhibitors in preclinical and early clinical development in oncology Oncologist 14 2009 559 570
36. A. Schwacha, and N. Kleckner Identification of double Holliday junctions as intermediates in meiotic recombination Cell 83 1995 783 791 (Pubitemid 3006321)
37. A. Sourirajan, and M. Lichten Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis Genes Dev. 22 2008 2627 2632
38. Y.D. Tay, and L. Wu Overlapping roles for Yen1 and Mus81 in cellular Holliday junction processing J. Biol. Chem. 285 2010 11427 11432
39. T. Wechsler, S. Newman, and S.C. West Aberrant chromosome morphology in human cells defective for Holliday junction resolution Nature 471 2011 642 646
40. L. Wu, and I.D. Hickson The Bloom's syndrome helicase suppresses crossing over during homologous recombination Nature 426 2003 870 874 (Pubitemid 38056876)
41. Benjamin, K.R., Zhang, C., Shokat, K.M., and Herskowitz, I. (2003). Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev. 17, 1524-1539. (Pubitemid 36734709)
42. Blanco, M.G., Matos, J., Rass, U., Ip, S.C.Y., and West, S.C. (2010). Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA damage repair in S. cerevisiae. DNA Repair (Amst.) 9, 394-402.
43. Carlile, T.M., and Amon, A. (2008). Meiosis I is established through division-specific translational control of a cyclin. Cell 133, 280-291. (Pubitemid 351508302)
44. Deans, A.J., and West, S.C. (2009). FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol. Cell 36, 943-953.
45. Gietz, R.D., and Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six base pair restriction sites. Gene 74, 527-534. (Pubitemid 19060666)
46. Hunter, N., and Kleckner, N. (2001). The single-end invasion: An asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106, 59-70. (Pubitemid 32709958)
47. Ip, S.C.Y., Rass, U., Blanco, M.G., Flynn, H.R., Skehel, J.M., and West, S.C. (2008). Identification of Holliday junction resolvases from humans and yeast. Nature 456, 357-361.
48. Kim, K.P., Weiner, B.M., Zhang, L.R., Jordan, A., Dekker, J., and Kleckner, N. (2010). Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143, 924-937.
49. Kinoshita-Kikuta, E., Aoki, Y., Kinoshita, E., and Koike, T. (2007). Label-free kinase profiling using phosphate affinity polyacrylamide gel electrophoreses. Mol. Cell Proteomics 6, 356-366. (Pubitemid 46359522)
50. Knop, M., Siegers, K., Pereira, G., Zachariae, W., Winsor, B., Nasmyth, K., and Schiebel, E. (1999). Epitope tagging of yeast strains using a PCR-based strategy: more tags and improved prctical routines. Yeast 15, 963-972.
51. Lee, B.H., and Amon, A. (2003). Role of Polo-like kinase Cdc5 in programming meiosis I chromosome segregation. Science 300, 482-486. (Pubitemid 36444328)
52. Martini, E., Diaz, R.L., Hunter, N., and Keeney, S. (2006). Crossover homeostasis in yeast meiosis. Cell 126, 285-295. (Pubitemid 44092965)
53. Matos, J., Lipp, J.J., Bogdanova, A., Guillot, S., Okaz, E., Junqueira, M., Shevchenko, A., and Zachariae, W.G. (2008). Dbf4-dependent Cdc7 kinase links DNA replication to the segregation of homologous chromosomes in meiosis I. Cell 135, 662-678.
54. Petronczki, M., Matos, J., Mori, S., Gregan, J., Bogdanova, A., Schwickart, M., Mechtler, K., Shirahige, K., Zachariae, W., and Nasmyth, K. (2006). Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126, 1049-1064.
55. Poser, I., Sarov, M., Hutchins, J.R., Heriche, J.K., Toyoda, Y., Pozniakovsky, A., Weigl, D., Nitzsche, A., Hegemann, B., Bird, A.W., et al. (2008). BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods 5, 409-415.
56. Salah, S.M., and Nasmyth, K. (2000). Destruction of the securing Pds1p occurs at the onset of anaphase during both meiotic divisions in yeast. Chromosoma 109, 27-34. (Pubitemid 30433294)
57. Schuyler, S.C., and Murray, A.W. (2009). An in vitro assay for Cdc20-dependent mitotic anaphase-promoting complex activity from budding yeast. Methods Mol. Biol. 545, 271-285.
58. Schwacha, A., and Kleckner, N. (1995). Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83, 783-791. (Pubitemid 3006321)
59. Zhang, Y.M., Buchholz, F., Muyrers, J.P.P., and Stewart, A.F. (1998). A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet. 20, 123-128. (Pubitemid 28455443)