Yeast Rad52 and Rad51 Recombination Proteins Define a Second Pathway of DNA Damage Assessment in Response to a Single Double-Strand Break

Molecular and Cellular Biology

Volumn 23, Issue 23, 2003, Pages 8913-8923

  Lee, Sang Eun ^a,c   Pellicioli, Achille ^b   Vaze, Moreshwar B ^a,d   Sugawara, Neal ^a   Malkova, Anna ^a   Foiani, Marco ^b   Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d Cyclis Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; RAD51 PROTEIN; RAD52 PROTEIN; RECOMBINANT PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; GENE DELETION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES; YEAST;

BASE SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; EPISTASIS, GENETIC; GENES, FUNGAL; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0242468917     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.23.8913-8923.2003     Document Type: Article

References (58)

1. Allen, J. B., Z. Zhou, W. Siede, E. C. Friedberg, and S. J. Elledge. 1994. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA dam age-induced transcription in yeast. Genes Dev. 8:2401-2415.
2. Bai, Y., and L. S. Symington. 1996. A RAD52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 10:2025-2037.
3. Cohen, Y., M. Dardalhon, and D. Averbeck. 2002. Homologous recombination is essential for RAD51 up-regulation in Saccharomyces cerevisiae following DNA crosslinking damage. Nucleic Acids Res. 30:1224-1232.
4. de la Torre-Ruiz, M., and N. F. Lowndes. 2000. The Saccharomyces cerevisiae DNA damage checkpoint is required for efficient repair of double strand breaks by non-homologous end joining. FEBS Lett. 467:311-315.
5. de la Torre-Ruiz, M. A., C. M. Green, and N. F. Lowndes. 1998. RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J. 17:2687-2698.
6. Dresser, M. E., D. J. Ewing, M. N. Conrad, A. M. Dominguez, R. Barstead, H. Jiang, and T. Kodadek. 1997. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147:533-544.
7. Elledge, S. J. 1996. Cell cycle checkpoints: preventing an identity crisis. Science 274:1664-1672.
8. Evans, E., N. Sugawara, J. E. Haber, and E. Alani. 2000. The Saccharomyces cerevisiae Msh2 mismatch repair protein localizes to recombination intermediates in vivo. Mol. Cell 5:789-799.
9. Firmenich, A. A., A. M. Elias, and P. Berg. 1995. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Mol. Cell. Biol. 15:1620-1631.
10. Garvik, B., M. Carson, and L. Hartwell. 1995. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15:6128-6138.
11. Gasior, S. L., A. K. Wong, Y. Kora, A. Shinohara, and D. K. Bishop. 1998. Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes Dev. 12:2208-2221.
12. Gilbert, C. S., C. M. Green, and N. F. Lowndes. 2001. Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8:129-136.
13. Hays, S. L., A. A. Firmenich, and P. Berg. 1995. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92:6925-6929.
14. Hays, S. L., A. A. Firmenich, P. Massey, R. Banerjee, and P. Berg. 1998. Studies of the interaction between Rad52 protein and the yeast single-stranded DNA binding protein RPA. Mol. Cell. Biol. 18:4400-4406.
15. Ira, G., and J. E. Haber. 2002. Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol. Cell. Biol. 22:6384-6392.
16. Jaskelioff, M., S. Van Komen, J. E. Krebs, P. Sung, and C. L. Peterson. 2003. Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J. Biol. Chem. 278:9212-9218.
17. Kantake, N., T. Sugiyama, R. D. Kolodner, and S. C. Kowalczykowski. 2003. The recombination-deficient mutant RPA (rfa1-t11) is displaced slowly from single-stranded DNA by Rad51 protein. J. Biol. Chem. 278:23410-23417.
18. Kolodner, R. D., C. D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552-557.
19. Kondo, T., K. Matsumoto, and K. Sugimoto. 1999. Role of a complex containing Rad17, Mec3, and Ddc1 in the yeast DNA damage checkpoint pathway. Mol. Cell. Biol. 19:1136-1143.
20. Kondo, T., T. Wakayama, T. Naiki, K. Matsumoto, and K. Sugimoto. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294:867-870.
21. Krejci, L., J. Damborsky, B. Thomsen, M. Duno, and C. Bendixen. 2001. Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell. Biol. 21:966-976.
22. Krejci, L., B. Song, W. Bussen, R. Rothstein, U. H. Mortensen, and P. Sung. 2002. Interaction with Rad51 is indispensable for recombination mediator function of Rad52. J. Biol. Chem. 277:40132-40141.
23. Krejci, L., S. Van Komen, Y. Li, J. Villemain, M. S. Reddy, H. Klein, T. Ellenberger, and P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305-309.
24. Lee, S. E., J. K. Moore, A. Holmes, K. Umezu, R. Kolodner, and J. E. Haber. 1998. Saccharomyces Ku70, Mre11/Rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399-409.
25. Lee, S. E., A. Pellicioli, A. Malkova, M. Foiani, and J. E. Haber. 2001. The Saccharomyces recombination protein Tidlp is required for adaptation from G2/M arrest induced by a double-strand break. Curr. Biol. 11:1053-1057.
26. Leroy, C., S. E. Lee, M. B. Vaze, F. Ochsenbein, R. Guerois, J. E. Haber, and M. C. Marsolier-Kergoat. 2003. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11:827-835. (Erratum, 11:1119.)
27. Lowndes, N. F., and J. R. Murguia. 2000. Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10:17-25.
28. Melo, J. A., J. Cohen, and D. P. Toczyski. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15:2809-2821.
29. Morgan, E. A., N. Shah, and L. S. Symington. 2002. The requirement for ATP hydrolysis by Saccharomyces cerevisiae Rad51 is bypassed by mating-type heterozygosity or RAD54 in high copy. Mol. Cell. Biol. 22:6336-6343.
30. New, J. H., and S. C. Kowalczykowski. 2002. Rad52 protein has a second stimulatory role in DNA strand exchange that complements replication protein-a function. J. Biol. Chem. 277:26171-26176.
31. New, J. H., T. Sugiyama, E. Zaitseva, and S. C. Kowalczykowski. 1998. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391:407-410.
32. Nigg, E. A. 1998. Polo-like kinases: positive regulators of cell division from start to finish. Curr. Opin. Cell Biol. 10:776-783.
33. Paulovich, A. G., and L. H. Hartwell. 1995. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82:841-847.
34. Pellicioli, A., S. E. Lee, C. Lucca, M. Foiani, and J. E. Haber. 2001. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from G2/M arrest. Mol. Cell 7:293-300.
35. Petukhova, G., P. Sung, and H. Klein. 2000. Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. Genes Dev. 14:2206-2215.
36. Rhind, N., and P. Russell. 1998. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10:749-758.
37. Rouse, J., and S. P. Jackson. 2002. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell 9:857-869.
38. Sanchez, Y., J. Bachant, H. Wang, F. Hu, D. Liu, M. Tetzlaff, and S. J. Elledge. 1999. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286:1166-1171.
39. Sanchez, Y., B. A. Desany, W. J. Jones, Q. Liu, B. Wang, and S. J. Elledge. 1996. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271:357-360.
40. Sandell, L. L., and V. A. Zakian. 1993. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75:729-739.
41. Shinohara, A., and T. Ogawa. 1998. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391:404-407.
42. Signon, L., A. Malkova, M. Naylor, and J. E. Haber. 2001. Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21:2048-2056.
43. Smith, J., and R. Rothstein. 1995. A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfal stimulates a RAD52-independent pathway for direct-repeat recombination. Mol. Cell. Biol. 15:1632-1641.
44. Sugawara, N., E. L. Ivanov, L. J. Fishman, B. L. Ray, X. Wu, and J. E. Haber. 1995. DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature 373:84-86.
45. Sugawara, N., X. Wang, and J. E. Haber. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209-219.
46. Sugiyama, T., and S. C. Kowalczykowski. 2002. Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 277:31663-31672.
47. Sung, P. 1997. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272:28194-28197.
48. Sung, P., and S. A. Stratton. 1996. Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271:27983-27986.
49. Toczyski, D. P., D. J. Galgoczy, and L. H. Hartwell. 1997. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90:1097-1106.
50. Umezu, K., N. Sugawara, C. Chen, J. E. Haber, and R. D. Kolodner. 1998. Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics 148:989-1005.
51. Van Dyck, E., A. Z. Stasiak, A. Stasiak, and S. C. West. 1999. Binding of double-strand breaks in DNA by human Rad52 protein. Nature 398:728-731.
52. Van Komen, S., G. Petukhova, S. Sigurdsson, S. Stratton, and P. Sung. 2000. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 6:563-572.
53. Vaze, M., A. Pellicioli, S. Lee, G. Ira, G. Liberi, A. Arbel-Eden, M. Foiani, and J. Haber. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell 10:373-385.
54. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 belicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-312.
55. Weinert, T. 1998. DNA damage checkpoints update: getting molecular. Curr. Opin. Genet. Dev. 8:185-193.
56. White, C. I., and J. E. Haber. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663-673.
57. Wu, X., and J. E. Haber. 1996. A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell 87:277-285.
58. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.