A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair

Genes and Development

Volumn 23, Issue 3, 2009, Pages 291-303

  Jain, Suvi ^a   Sugawara, Neal ^a   Lydeard, John ^a   Vaze, Moreshwar ^a,b   Gac, Nicolas Tanguy Le ^a,c   Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b Cequent Pharmaceuticals Inc   (United States)

^c INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

BIR; Gene conversion; Pol32; Sgs1; SSA

Indexed keywords

DOUBLE STRANDED DNA; GENOMIC DNA; PHOSPHORUS 32; RAD51 PROTEIN; RECQ HELICASE; SGS1 HELICASE; UNCLASSIFIED DRUG;

ARTICLE; BREAK INDUCED REPLICATION; CHROMATIN IMMUNOPRECIPITATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; ENZYME ACTIVITY; GENE CONVERSION; GENETIC RECOMBINATION; HOMOLOGOUS RECOMBINATION; ISOTOPE LABELING; KINETICS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SOUTHERN BLOTTING; YEAST CELL;

DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; EVOLUTION, MOLECULAR; GENE CONVERSION; KINETICS; MODELS, BIOLOGICAL; MODELS, GENETIC; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 59949092789     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1751209     Document Type: Article

References (58)

1. Adams, M.D., McVey, M., and Sekelsky, J.J. 2003. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299: 265-267.
2. Bachrati, C.Z. and Hickson, I.D. 2008. RecQ helicases: Guardian angels of the DNA replication fork. Chromosoma 117: 219-233.
3. Bachrati, C.Z., Borts, R.H., and Hickson, I.D. 2006. Mobile D- loops are a preferred substrate for the Bloom's syndrome helicase. Nucleic Acids Res. 34: 2269-2279.
4. Banerjee, S., Smith, S., Oum, J.H., Liaw, H.J., Hwang, J.Y., Sikdar, N.,Motegi, A.,Lee, S.E., andMyung,K. 2008. Mphlppromotes gross chromosomal rearrangement through partial inhibition of homologous recombination. J. Cell Biol. 181: 1083-1093.
5. Bjergbaek, L., Cobb, J.A., Tsai-Pflugfelder, M., and Gasser, S.M. 2005. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24: 405-417.
6. Bosco, G. and Haber, J.E. 1998. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150: 1037-1047.
7. Branzei, D. and Foiani, M. 2007a. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst.) 6: 994-1003.
8. Branzei, D. and Foiani, M. 2007b. RecQ helicases queuing with Srs2 to disrupt Rad51 filaments and suppress recombination. Genes & Dev. 21: 3019-3026.
9. Burgers, P.M. and Gerik, K.J. 1998. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase δ. J. Biol. Chem. 273: 19756-19762.
10. Clerici, M., Mantiero, D., Lucchini, G., and Longhese, M.P. 2005. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280: 38631-38638.
11. Connolly, B., White, C.I., and Haber, J.E. 1988. Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 8: 2342-2349.
12. Davis, A.P. and Symington, L.S. 2004. RAD51-dependent break- induced replication in yeast. Mol. Cell. Biol. 24: 2344-2351.
13. Fishman-Lobell, J., Rudin, N., and Haber, J.E. 1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12: 1292-1303.
14. Frei, C. and Gasser, S.M. 2000. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes & Dev. 14: 81-96.
15. Gerik, K.J., Li, X., Pautz, A., and Burgers, P.M. 1998. Characterization of the two small subunits of Saccharomyces cerevi- siae DNA polymerase δ. J. Biol. Chem. 273: 19747-19755.
16. Gravel, S., Chapman, J.R., Magill, C., and Jackson, S.P. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes & Dev. 22: 2767-2772.
17. Haber, J.E. 1999. DNA recombination: The replication connection. Trends Biochem. Sci. 24: 271-275.
18. Holmes, A.M. and Haber, J.E. 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96: 415-424.
19. Ira, G. and Haber, J.E. 2002. Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol. Cell. Biol. 22: 6384-6392.
20. Ira, G., Malkova, A., Liberi, G., Foiani, M., and Haber, J.E. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411.
21. Ira, G., Satory, D., and Haber, J.E. 2006. Conservative inheritance of newly synthesized DNA in double-strand break- induced gene conversion. Mol. Cell. Biol. 26: 9424-9429.
22. Ivanov, E.L., Sugawara, N., Fishman-Lobell, J., and Haber, J.E. 1996. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 142: 693-704.
23. Johnson-Schlitz, D.M. and Engels, W.R. 2006. The effect of gap length on double-strand break repair in Drosophila. Genetics 173: 2033-2038.
24. Kang, L.E. and Symington, L.S. 2000. Aberrant double-strand break repair in rad51 mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 9162-9172.
25. Kaye, J.A., Melo, J.A., Cheung, S.K., Vaze, M.B., Haber, J.E., and Toczyski, D.P. 2004. DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr. Biol. 14: 2096-2106.
26. Keogh, M.C., Kim, J.A., Downey, M., Fillingham, J., Chowdhury, D., Harrison, J.C., Onishi, M., Datta, N., Galicia, S., Emili, A., et al. 2006. A phosphatase complex that dephosphory- lates γH2AX regulates DNA damage checkpoint recovery. Nature 439: 497-501.
27. Kraus, E., Leung, W.Y., and Haber, J.E. 2001. Break-induced replication: A review and an example in budding yeast. Proc. Natl. Acad. Sci. 98: 8255-8262.
28. Krishna, S., Wagener, B.M., Liu, H.P., Lo, Y.C., Sterk, R., Petrini,J.H., and Nickoloff, J.A. 2007. Mre11 and Ku regulation of double-strand break repair by gene conversion and break- induced replication. DNA Repair (Amst.) 6: 797-808.
29. Krogh, B.O. and Symington, L.S. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38: 233-271.
30. Le, S., Moore, J.K., Haber, J.E., and Greider, C.W. 1999. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres inthe absence oftelomerase. Genetics 152: 143-152.
31. Lo, Y.C., Paffett, K.S., Amit, O., Clikeman, J.A., Sterk, R., Brenneman, M.A., and Nickoloff, J.A. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 26: 4086-4094.
32. Lobachev, K., Vitriol, E., Stemple, J., Resnick, M.A., and Bloom, K. 2004. Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr. Biol. 14: 2107-2112.
33. Lundblad, V. and Blackburn, E.H. 1993. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73: 347-360.
34. Lydeard, J.R., Jain, S., Yamaguchi, M., and Haber, J.E. 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823.
35. Malkova, A., Ivanov, E.L., and Haber, J.E. 1996. Double-strand break repair in the absence of RAD51 in yeast: A possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. 93: 7131-7136.
36. Malkova, A., Signon, L., Schaefer, C.B., Naylor, M.L., Theis, J.F., Newlon, C.S., and Haber, J.E. 2001. RAD51-independent break-induced replication to repair a broken chromosome depends on a distant enhancer site. Genes & Dev. 15: 1055-1060.
37. Malkova, A., Naylor, M.L., Yamaguchi, M., Ira, G., and Haber, J.E. 2005. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51- mediated gene conversion. Mol. Cell. Biol. 25: 933-944.
38. McDonald, J.P. and Rothstein, R. 1994. Unrepaired heteroduplex DNA in Saccharomyces cerevisiae is decreased in RAD1 RAD52-independent recombination. Genetics 137: 393-405.
39. McEachern, M.J. and Haber, J.E. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75: 111-135.
40. McVey, M., Larocque, J.R., Adams, M.D., and Sekelsky, J.J. 2004. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl. Acad. Sci. 101: 15694-15699.
41. Mimitou, E.P. and Symington, L.S. 2008. Sae2, Exol and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774.
42. Morrow, D.M., Connelly, C., and Hieter, P. 1997. ''Break copy'' duplication: A model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147: 371-382.
43. Mullen, J.R., Kaliraman, V., and Brill, S.J. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154: 1101-1114.
44. Nickoloff, J.A. and Haber, J.E. 2001. Mating-type control of DNA repair and recombination in Saccharomyces cerevisiae.ln DNA damage and repair: Advances from phage to humans, Vol. 3 (eds. J.A. Nickoloff and M.F. Hoekstra), pp. 107-124. Humana Press, Totowa, NJ.
45. Oh, S.D., Lao, J.P., Hwang, P.Y., Taylor, A.F., Smith, G.R., and Hunter, N. 2007. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
46. Paques, F. and Haber, J.E. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
47. Sikorski, R.S. and Hieter, P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
48. Smith, C.E., Llorente, B., and Symington, L.S. 2007. Template switching during break-induced replication. Nature 447: 102-105.
49. Sugawara, N. and Haber, J.E. 1992. Characterization of double-strand break-induced recombination: Homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12: 563-575.
50. Sugawara, N., Ira, G., and Haber, J.E. 2000. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol. 20: 5300-5309.
51. Sugawara, N., Wang, X., and Haber, J.E. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12: 209-219.
52. Teng, S.C., Chang, J., McCowan, B., and Zakian, V.A. 2000. Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell 6: 947-952.
53. VanHulle, K., Lemoine, F.J., Narayanan, V., Downing, B., Hull, K., McCullough, C., Bellinger, M., Lobachev, K., Petes, T.D., and Malkova, A. 2007. Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol. Cell. Biol. 27: 2601-2614.
54. Vaze, M.B., Pellicioli, A., Lee, S.E., Ira, G., Liberi, G., Arbel-Eden, A., Foiani, M., and Haber, J.E. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10: 373-385.
55. Voelkel-Meiman, K. and Roeder, G.S. 1990. Gene conversion tracts stimulated by HOT1-promoted transcription are long and continuous. Genetics 126: 851-867.
56. Wang, X., Ira, G., Tercero, J.A., Holmes, A.M., Diffley, J.F., and Haber, J.E. 2004. Role of DNA replication proteins in double- strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 24: 6891-6899.
57. White, C.I. and Haber, J.E. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9: 663-673.
58. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E., and Ira, G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994.