Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover

EMBO Journal

Volumn 25, Issue 12, 2006, Pages 2837-2846

  Robert, Thomas ^a   Dervins, Delphine ^a   Fabre, Francis ^a   Gangloff, Serge ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

Checkpoint; Crossover; Helicase; Mitotic recombination; PCNA

Indexed keywords

CYCLINE; HELICASE; PROTEIN MRC1; PROTEIN SGS1; PROTEIN SRS2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CROSSING OVER; DNA DAMAGE; DNA REPLICATION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HOLLIDAY JUNCTION; MUTATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA DAMAGE; DNA HELICASES; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDONUCLEASES; GENES, FUNGAL; MITOSIS; MODELS, GENETIC; MUTATION; PHOSPHORYLATION; PROLIFERATING CELL NUCLEAR ANTIGEN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 33745541640     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601158     Document Type: Article

References (72)

1. Aylon Y, Kupiec M (2004) New insights into the mechanism of homologous recombination in yeast. Mutat Res 566: 231-248
2. Aylon Y, Liefshitz B, Bitan-Banin G, Kupiec M (2003) Molecular dissection of mitotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol 23: 1403-1417
3. Bailis AM, Arthur L, Rothstein R (1992) Genome rearrangement in top3 mutants of Saccharomyces cerevisiae requires a functional RAD1 excision repair gene. Mol Cell Biol 12: 4988-4993
4. Bartrand AJ, Iyasu D, Brush GS (2004) DNA stimulates Mec1-mediated phosphorylation of replication protein A. J Biol Chem 279: 26762-26767
5. Bashkirov VI, King JS, Bashkirova EV, Schmuckli-Maurer J, Heyer WD (2000) DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints. Mol Cell Biol 20: 4393-4404
6. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ (2003) The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol 23: 3487-3496
7. Baudat F, Nicolas A (1997) Clustering of meiotic double-strand breaks on yeast chromosome III. Proc Natl Acad Sci USA 94: 5213-5218
8. Bennett RJ, Keck JL, Wang JC (1999) Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J Mol Biol 289: 235-248
9. Bennett RJ, Noirot-Gros MF, Wang JC (2000) Interaction between yeast Sgs1 helicase and DNA topoisomerase III. J Biol Chem 275: 26898-26905
10. Boeke J, Lacroute F, Fink G (1984) A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197: 342-346
11. Calzada A, Hodgson B, Kanemaki M, Bueno A, Labib K (2005) Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev 19: 1905-1919
12. Caspari T, Murray JM, Carr AM (2002) Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev 16: 1195-1208
13. de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM (2003) 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: 81-94
14. de los Santos T, Loidl J, Larkin B, Hollingsworth NM (2001) A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics 159: 1511-1525
15. Doe CL, Ahn JS, Dixon J, Whitby MC (2002) Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J Biol Chem 277: 32753-32759
16. Duno M, Thomsen B, Westergaard O, Krejci L, Bendixen C (2000) Genetic analysis of the Saccharomyces cerevisiae Sgs1 helicase defines an essential function for the Sgs1-Top3 complex in the absence of SRS2 or TOP1. Mol Gen Genet 264: 89-97
17. Elliott B, Jasin M (2002) Double-strand breaks and translocations in cancer. Cell Mol Life Sci 59: 373-385
18. Fabre F, Chan A, Heyer WD, Gangloff S (2002) Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc Natl Acad Sci USA 99: 16887-16892
19. Formosa T, Alberts BM (1986) DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell 47: 793-806
20. Frei C, Gasser SM (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
21. Gangloff S, de Massy B, Arthur L, Rothstein R, Fabre F (1999) The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J 18: 1701-1711
22. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398
23. Gangloff S, Soustelle C, Fabre F (2000) Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat Genet 25: 192-194
24. Haghnazari E, Heyer WD (2004) The DNA damage checkpoint pathways exert multiple controls on the efficiency and outcome of the repair of a double-stranded DNA gap. Nucleic Acids Res 32: 4257-4268
25. Heude M, Chanet R, Fabre F (1995) Regulation of the Saccharomyces cerevisiae Srs2 helicase during the mitotic cell cycle, meiosis and after irradiation. Mol Gen Genet 248: 59-68
26. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419: 135-141
27. Interthal H, Heyer WD (2000) MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol Gen Genet 263: 812-827
28. Ira G, Haber JE (2002) Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol Cell Biol 22: 6384-6392
29. Ira G, Malkova A, Liberi G, Foiani M, Haber JE (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411
30. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98: 4569-4574
31. Kaliraman V, Mullen JR, Fricke WM, Bastin-Shanower SA, Brill SJ (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev 15: 2730-2740
32. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, Sugimoto K, Shirahige K (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083
33. Kim RA, Wang JC (1992) Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase. J Biol Chem 267: 17178-17185
34. Klein HL (2001) Spontaneous chromosome loss in Saccharomyces cerevisiae is suppressed by DNA damage checkpoint functions. Genetics 159: 1501-1509
35. Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS, Klein H, Ellenberger T, Sung P (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423: 305-309
36. Kuzminov A (2001) Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci USA 98: 8241-8246
37. Liberi G, Chiolo I, Pellicioli A, Lopes M, Plevani P, Muzi-Falconi M, Foiani M (2000) Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J 19: 5027-5038
38. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, Newlon CS, Foiani M (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561
39. Lu J, Mullen JR, Brill SJ, Kleff S, Romeo AM, Sternglanz R (1996) Human homologues of yeast helicase. Nature 383: 678-679
40. Melo J, Toczyski D (2002) A unified view of the DNA-damage checkpoint. Curr Opin Cell Biol 14: 237-245
41. Miyajima A, Seki M, Onoda F, Shiratori M, Odagiri N, Ohta K, Kikuchi Y, Ohno Y, Enomoto T (2000) Sgs1 helicase activity is required for mitotic but apparently not for meiotic functions. Mol Cell Biol 20: 6399-6409
42. Mullen JR, Kaliraman V, Brill SJ (2000) Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154: 1101-1114
43. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA (2002) Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 36: 617-656
44. Onoda F, Seki M, Miyajima A, Enomoto T (2000) Elevation of sister chromatid exchange in Saccharomyces cerevisiae sgs1 disruptants and the relevance of the disruptants as a system to evaluate mutations in Bloom's syndrome gene. Mutat Res-DNA Repair 459: 203-209
45. Onodera R, Seki M, Ui A, Satoh Y, Miyajima A, Onoda F, Enomoto T (2002) Functional and physical interaction between Sgs1 and Top3 and Sgs1-independent function of Top3 in DNA recombination repair. Genes Genet Syst 77: 11-21
46. Ooi SL, Shoemaker DD, Boeke JD (2003) DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat Genet 35: 277-286
47. Osborn AJ, Elledge SJ (2003) Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 17: 1755-1767
48. Papouli E, Chen S, Davies AA, Huttner D, Krejci L, Sung P, Ulrich HD (2005) Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol Cell 19: 123-133
49. Pâques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404
50. Paull TT, Cortez D, Bowers B, Elledge SJ, Gellert M (2001) Direct DNA binding by Brca1. Proc Natl Acad Sci USA 98: 6086-6091
51. Petes TD, Malone RE, Symington LS (1991) Recombination in yeast. In The Molecular & Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics. (1), Broach JR, Pringle JR, Jones EW (eds) pp 407-521. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
52. Pfander B, Moldovan G-L, Sacher M, Hoege C, Jentsch S (2005) SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436: 428-433
53. Prado F, Aguilera A (2003) Control of cross-over by single-strand DNA resection. Trends Genet 19: 428-431
54. Rockmill B, Fung JC, Branda SS, Roeder GS (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13: 1954-1962
55. Saka Y, Esashi F, Matsusaka T, Mochida S, Yanagida M (1997) Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev 11: 3387-3400
56. Schild D (1995) Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics 140: 115-127
57. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J, Livingston DM (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90: 425-435
58. Sherman F, Hicks J (1991) Micromanipulation and dissection of asci. Methods Enzymol 194: 21-37
59. Sogo JM, Lopes M, Foiani M (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602
60. Spell RM, Jinks-Robertson S (2004) Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae. Methods Mol Biol 262: 3-12
61. Szyjka SJ, Viggiani CJ, Aparicio OM (2005) Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol Cell 19: 691-697
62. Tourrière H, Versini G, Cordón-Preciado V, Alabert C, Pasero P (2005) Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 19: 699-706
63. Ui A, Satoh Y, Onoda F, Miyajima A, Seki M, Enomoto T (2001) The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants. Mol Genet Genomics 265: 837-850
64. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, Arbel-Eden A, Foiani M, Haber JE (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10: 373-385
65. Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423: 309-312
66. Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409-419
67. Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3: 430-440
68. Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J (2000) BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 14: 927-939
69. Willson J, Wilson S, Warr N, Watts FZ (1997) Isolation and characterization of the Schizosaccharomyces pombe rhp9 gene: a gene required for the DNA damage checkpoint but not the replication checkpoint. Nucleic Acids Res 25: 2138-2146
70. Wu L, Hickson ID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874
71. Xu H, Boone C, Klein HL (2004) Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage. Mol Cell Biol 24: 7082-7090
72. Zhao X, Chabes A, Domkin V, Thelander L, Rothstein R (2001) The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage. EMBO J 20: 3544-3553