The Srs2 Helicase Activity Is Stimulated by Rad51 Filaments on dsDNA: Implications for Crossover Incidence during Mitotic Recombination

Molecular Cell

Volumn 29, Issue 2, 2008, Pages 243-254

  Dupaigne, Pauline ^b   Le Breton, Cyrille ^a   Fabre, Francis ^a   Gangloff, Serge ^a   Le Cam, Eric ^b   Veaute, Xavier ^a  

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

^b CNRS   (France)

Author keywords

DNA

Indexed keywords

DOUBLE STRANDED DNA; HELICASE; NUCLEOPROTEIN; RAD51 PROTEIN;

ARTICLE; DNA STRUCTURE; ENZYME ACTIVITY; GENE TRANSLOCATION; MITOTIC RECOMBINATION; NUCLEOTIDE SEQUENCE;

SACCHAROMYCES CEREVISIAE;

EID: 38649130654     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.11.033     Document Type: Article

References (55)

1. Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., and Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 17 (1989) 7211-7219
2. Aboussekhra A., Chanet R., Adjiri A., and Fabre F. Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol. Cell. Biol. 12 (1992) 3224-3234
3. Adams M.D., McVey M., and Sekelsky J.J. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299 (2003) 265-267
4. Aguilera A., and Klein H.L. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119 (1988) 779-790
5. Beloin C., Jeusset J., Revet B., Mirambeau G., Le Hegarat F., and Le Cam E. Contribution of DNA conformation and topology in right-handed DNA wrapping by the Bacillus subtilis LrpC protein. J. Biol. Chem. 278 (2003) 5333-5342
6. Benson F.E., and West S.C. Substrate specificity of the Escherichia coli RuvC protein. Resolution of three- and four-stranded recombination intermediates. J. Biol. Chem. 269 (1994) 5195-5201
7. Brendza K.M., Cheng W., Fischer C.J., Chesnik M.A., Niedziela-Majka A., and Lohman T.M. Autoinhibition of Escherichia coli Rep monomer helicase activity by its 2B subdomain. Proc. Natl. Acad. Sci. USA 102 (2005) 10076-10081
8. Bugreev D.V., Mazina O.M., and Mazin A.V. Rad54 protein promotes branch migration of Holliday junctions. Nature 442 (2006) 590-593
9. Bugreev D.V., Hanaoka F., and Mazin A.V. Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 14 (2007) 746-753
10. Byrd A.K., and Raney K.D. Protein displacement by an assembly of helicase molecules aligned along single-stranded DNA. Nat. Struct. Mol. Biol. 11 (2004) 531-538
11. Chanet R., Heude M., Adjiri A., Maloisel L., and Fabre F. Semidominant mutations in the yeast Rad51 protein and their relationships with the Srs2 helicase. Mol. Cell. Biol. 16 (1996) 4782-4789
12. Dessinges M.N., Lionnet T., Xi X.G., Bensimon D., and Croquette V. Single-molecule assay reveals strand switching and enhanced processivity of UvrD. Proc. Natl. Acad. Sci. USA 101 (2004) 6439-6444
13. Dubochet J., Ducommun M., Zollinger M., and Kellenberger E. A new preparation method for dark-field electron microscopy of biomacromolecules. J. Ultrastruct. Res. 35 (1971) 147-167
14. Fabre F. Induced intragenic recombination in yeast can occur during the G1 mitotic phase. Nature 272 (1978) 795-798
15. Fabre F. Mitotic recombination and repair in relation to the cell cycle in yeast. In: Von Wettstein A.S., Kielland-Brandt M., and Friis J. (Eds). Molecular Genetics in Yeast, D (1981), Munksgaard, Copenhagen, Denmark 399-406
16. Fabre F., Chan A., Heyer W.D., and Gangloff S. 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 (2002) 16887-16892
17. Fischer C.J., Maluf N.K., and Lohman T.M. Mechanism of ATP-dependent translocation of E. coli UvrD monomers along single-stranded DNA. J. Mol. Biol. 344 (2004) 1287-1309
18. Gangloff S., Soustelle C., and Fabre F. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25 (2000) 192-194
19. Harmon F.G., and Kowalczykowski S.C. Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J. Biol. Chem. 276 (2001) 232-243
20. Heude M., Chanet R., and Fabre F. Regulation of the Saccharomyces cerevisiae Srs2 helicase during the mitotic cell cycle, meiosis and after irradiation. Mol. Gen. Genet. 248 (1995) 59-68
21. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
22. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
23. Kantake N., Sugiyama T., Kolodner R.D., and Kowalczykowski S.C. The recombination-deficient mutant RPA (rfa1-t11) is displaced slowly from single-stranded DNA by Rad51 protein. J. Biol. Chem. 278 (2003) 23410-23417
24. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
25. Krogh B.O., and Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38 (2004) 233-271
26. Lawrence C.W., and Christensen R.B. Metabolic suppressors of trimethoprim and ultraviolet light sensitivities of Saccharomyces cerevisiae rad6 mutants. J. Bacteriol. 139 (1979) 866-876
27. Lee J.Y., and Yang W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127 (2006) 1349-1360
28. Lettier G., Feng Q., de Mayolo A.A., Erdeniz N., Reid R.J., Lisby M., Mortensen U.H., and Rothstein R. The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet. 2 (2006) e194 10.1371/journal.pgen.0020194
29. Matson S.W., and George J.W. DNA helicase II of Escherichia coli. Characterization of the single-stranded DNA-dependent NTPase and helicase activities. J. Biol. Chem. 262 (1987) 2066-2076
30. Mazin A.V., Bornarth C.J., Solinger J.A., Heyer W.D., and Kowalczykowski S.C. Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell 6 (2000) 583-592
31. Mazin A.V., Zaitseva E., Sung P., and Kowalczykowski S.C. Tailed duplex DNA is the preferred substrate for Rad51 protein-mediated homologous pairing. EMBO J. 19 (2000) 1148-1156
32. McVey M., Larocque J.R., Adams M.D., and Sekelsky J.J. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl. Acad. Sci. USA 101 (2004) 15694-15699
33. Morris P.D., and Raney K.D. DNA helicases displace streptavidin from biotin-labeled oligonucleotides. Biochemistry 38 (1999) 5164-5171
34. Nakagawa T., Flores-Rozas H., and Kolodner R.D. The MER3 helicase involved in meiotic crossing over is stimulated by single-stranded DNA-binding proteins and unwinds DNA in the 3′ to 5′ direction. J. Biol. Chem. 276 (2001) 31487-31493
35. Nickoloff J.A., Sweetser D.B., Clikeman J.A., Khalsa G.J., and Wheeler S.L. Multiple heterologies increase mitotic double-strand break-induced allelic gene conversion tract lengths in yeast. Genetics 153 (1999) 665-679
36. Niedziela-Majka A., Chesnik M.A., Tomko E.J., and Lohman T.M. Bacillus stearothermophilus PcrA monomer is a single-stranded DNA translocase but not a processive helicase in vitro. J. Biol. Chem. 282 (2007) 27076-27085
37. Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., and Ulrich H.D. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19 (2005) 123-133
38. Pâques F., and Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63 (1999) 349-404
39. Petukhova G., Stratton S., and Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393 (1998) 91-94
40. Pfander B., Moldovan G.L., Sacher M., Hoege C., and Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005) 428-433
41. Raynard S., Bussen W., and Sung P. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J. Biol. Chem. 281 (2006) 13861-13864
42. Robert T., Dervins D., Fabre F., and Gangloff S. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25 (2006) 2837-2846
43. Rong L., and Klein H.L. Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268 (1993) 1252-1259
44. Schild D. 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 (1995) 115-127
45. Solinger J.A., Kiianitsa K., and Heyer W.D. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell 10 (2002) 1175-1188
46. Soultanas P., Dillingham M.S., Wiley P., Webb M.R., and Wigley D.B. Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism. EMBO J. 19 (2000) 3799-3810
47. Sugiyama T., Zaitseva E.M., and Kowalczykowski S.C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272 (1997) 7940-7945
48. Van Komen S., Petukhova G., Sigurdsson S., Stratton S., and Sung P. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 6 (2000) 563-572
49. Van Komen S., Reddy M.S., Krejci L., Klein H., and Sung P. ATPase and DNA helicase activities of the Saccharomyces cerevisiae anti-recombinase Srs2. J. Biol. Chem. 278 (2003) 44331-44337
50. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., and Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003) 309-312
51. Veaute X., Delmas S., Selva M., Jeusset J., Le Cam E., Matic I., Fabre F., and Petit M.A. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 24 (2005) 180-189
52. Wang X., and Haber J.E. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2 (2004) E21 10.1371/journal.pbio.0020021
53. Wu L., and Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426 (2003) 870-874
54. Wu L., Bachrati C.Z., Ou J., Xu C., Yin J., Chang M., Wang W., Li L., Brown G.W., and Hickson I.D. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. USA 103 (2006) 4068-4073
55. Zaitseva E.M., Zaitsev E.N., and Kowalczykowski S.C. The DNA binding properties of Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 274 (1999) 2907-2915