RecFOR proteins are essential for Pol V-mediated translesion synthesis and mutagenesis

EMBO Journal

Volumn 25, Issue 24, 2006, Pages 5754-5763

  Fujii, Shingo ^a   Isogawa, Asako ^a   Fuchs, Robert P ^a  

^a CNRS   (France)

Author keywords

Competition between Pol III and Pol V; Induced mutagenesis; Pol V mediated lesion bypass; RecFOR functions

Indexed keywords

BINDING PROTEIN; RECA PROTEIN;

ARTICLE; DNA DAMAGE; ESCHERICHIA COLI; HOMOLOGOUS RECOMBINATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STRUCTURAL GENE;

DNA POLYMERASE III; DNA PRIMERS; DNA, BACTERIAL; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, GENETIC; MUTAGENESIS; MUTATION; PYRIMIDINE DIMERS; REC A RECOMBINASES; ULTRAVIOLET RAYS;

ESCHERICHIA COLI;

EID: 33845709987     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601474     Document Type: Article

References (61)

1. Arenson TA, Tsodikov OV, Cox MM (1999) Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA. J Mol Biol 288: 391-401
2. Bailone A, Sommer S, Knezevic J, Dutreix M, Devoret R (1991) A RecA protein mutant deficient in its interaction with the UmuDC complex. Biochimie 73: 479-484
3. Becherel OJ, Fuchs RP (1999) SOS mutagenesis results from up-regulation of translesion synthesis. J Mol Biol 294: 299-306
4. Becherel OJ, Fuchs RPP, Wagner J (2002) Pivotal role of the β-clamp in translesion DNA synthesis and mutagenesis in E. coli cells. DNA Repair 1: 703-708
5. Bork JM, Cox MM, Inman RB (2001a) RecA protein filaments disassemble in the 5′-3′ direction on single-stranded DNA. J Biol Chem 276: 45740-45743
6. Bork JM, Cox MM, Inman RB (2001b) The RecOR protein's modulate RecA protein function at 5′ ends of single-stranded DNA. EMBO J 20: 7313-7322
7. Chow KH, Courcelle J (2004) RecO acts with RecF and RecR to protect and maintain replication forks blocked by UV-induced DNA damage in Escherichia coli. J Biol Chem 279: 3492-3496
8. Clark AJ, Sandler SJ (1994) Homologous genetic recombination: the pieces begin to fall into place. Crit Rev Microbiol 20: 125-142
9. Courcelle J, Hanawalt PC (2003) RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37: 611-646
10. Dutreix M, Moreau PL, Bailone A, Galibert F, Battista JR, Walker GC, Devoret R (1989) New recA mutations that dissociate the various RecA protein activities in Escherichia coli provide evidence for an additional role for RecA protein in UV mutagenesis. J Bacteriol 171: 2415-2423
11. Ehn M, Nilsson P, Uhlen M, Hober S (2001) Overexpression, rapid isolation, and biochemical characterization of Escherichia coli single-stranded DNA-binding protein. Protein Expr Purif 22: 120-127
12. Frank EG, Gonzalez M, Ennis DG, Levine AS, Woodgate R (1996) In vivo stability of the Umu mutagenesis proteins: a major role for RecA. J Bacteriol 178: 3550-3556
13. Friedberg EC, Lehmann AR, Fuchs RP (2005) Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol Cell 18: 499-505
14. Fuchs RP, Fujii S, Wagner J (2004) Properties and functions of Escherichia coli: Pol IV and Pol V. Adv Protein Chem 69: 229-264
15. Fujii S, Fuchs RP (2004) Defining the position of the switches between replicative and bypass DNA polymerases. EMBO J 23: 4342-4352
16. Fujii S, Gasser V, Fuchs RP (2004) The biochemical requirements of DNA polymerase V-mediated translesion synthesis revisited. J Mol Biol 341: 405-417
17. Gasior SL, Olivares H, Ear U, Hari DM, Weichselbaum R, Bishop DK (2001) Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis. Proc Natl Acad Sci USA 98: 8411-8418
18. Goodman MF (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 71: 17-50
19. Griffin TJT, Kolodner RD (1990) Purification and preliminary characterization of the Escherichia coli K-12 recF protein. J Bacteriol 172: 6291-6299
20. Hegde S, Sandler SJ, Clark AJ, Madiraju MV (1995) recO and recR mutations delay induction of the SOS response in Escherichia coli. Mol Gen Genet 246: 254-258
21. Heller RC, Marians KJ (2006) Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439: 557-562
22. Higuchi K, Katayama T, Iwai S, Hidaka M, Horiuchi T, Maki H (2003) Fate of DNA replication fork encountering a single DNA lesion during oriC plasmid DNA replication in vitro. Genes Cells 8: 437-449
23. Joo C, McKinney SA, Nakamura M, Rasnik I, Myong S, Ha T (2006) Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126: 515-527
24. Karu AE, Belk ED (1982) Induction of E. coli recA protein via recBC and alternate pathways: quantitation by enzyme-linked immunosorbent assay (ELISA). Mol Gen Genet 185: 275-282
25. Kato T, Rothman RH, Clark AJ (1977) Analysis of the role of recombination and repair in mutagenesis of Escherichia coli by UV irradiation. Genetics 87: 1-18
26. Kowalczykowski SC, Clow J, Somani R, Varghese A (1987) Effects of the Escherichia coli SSB protein on the binding of Escherichia coli RecA protein to single-stranded DNA. Demonstration of competitive binding and the lack of a specific protein-protein interaction. J Mol Biol 193: 81-95
27. Kowalczykowski SC, Krupp RA (1987) Effects of Escherichia coli SSB protein on the single-stranded DNA-dependent ATPase activity of Escherichia coli RecA protein. Evidence that SSB protein facilitates the binding of RecA protein to regions of secondary structure within single-stranded DNA. J Mol Biol 193: 97-113
28. Kuzminov A (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63: 751-813, table of contents
29. Langston LD, O'Donnell M (2006) DNA replication: keep moving and don't mind the gap. Mol Cell 23: 155-160
30. Lavery PE, Kowalczykowski SC (1992) Biochemical basis of the constitutive repressor cleavage activity of recA730 protein. A comparison to recA441 and recA803 proteins. J Biol Chem 267: 20648-20658
31. Lehmann AR, Fuchs RP (2006) Gaps and forks in DNA replication: rediscovering old models. DNA Repair (in press)
32. Liu YH, Cheng AJ, Wang TC (1998) Involvement of recF, recO, and recR genes in UV-radiation mutagenesis of Escherichia coli. J Bacteriol 180: 1766-1770
33. Lopes M, Foiani M, Sogo JM (2006) Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 21: 15-27
34. Luisi-DeLuca C, Kolodner R (1994) Purification and characterization of the Escherichia coli RecO protein. Renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein. J Mol Biol 236: 124-138
35. Lusetti SL, Hobbs MD, Stohl EA, Chitteni-Pattu S, Inman RB, Seifert HS, Cox MM (2006) The RecF protein antagonizes RecX function via direct interaction. Mol Cell 21: 41-50
36. Madiraju MV, Templin A, Clark AJ (1988) Properties of a mutant recA-encoded protein reveal a possible role for Escherichia coli recF-encoded protein in genetic recombination. Proc Natl Acad Sci USA 85: 6592-6596
37. Mahdi AA, Lloyd RG (1989) Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair. Mol Gen Genet 216: 503-510
38. McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, West SC (2005) Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20: 783-792
39. McInerney P, O'Donnell M (2004) Functional uncoupling of twin polymerases: mechanism of polymerase dissociation from a lagging-strand block. J Biol Chem 279: 21543-21551
40. Morimatsu K, Kowalczykowski SC (2003) RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol Cell 11: 1337-1347
41. Napolitano R, Janel-Bintz R, Wagner J, Fuchs RP (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J 19: 6259-6265
42. Pages V, Fuchs RP (2003) Uncoupling of leading- and lagging-strand DNA replication during lesion bypass in vivo. Science 300: 1300-1303
43. Pham P, Bertram JG, O'Donnell M, Woodgate R, Goodman MF (2001) A model for SOS-lesion-targeted mutations in Escherichia coli. Nature 409: 366-370
44. Register III JC, Griffith J (1985) The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem 260: 12308-12312
45. Reuven NB, Arad G, Stasiak AZ, Stasiak A, Livneh Z (2001) Lesion bypass by the Escherichia coli DNA polymerase V requires assembly of a RecA nucleoprotein filament. J Biol Chem 276: 5511-5517
46. Rupp WD, Howard-Flanders P (1968) Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J Mol Biol 31: 291-304
47. Sandler SJ, Clark AJ (1994) RecOR suppression of recF mutant phenotypes in Escherichia coli K-12. J Bacteriol 176: 3661-3672
48. Sawitzke JA, Stahl FW (1992) Phage lambda has an analog of Escherichia coli recO, recR and recF genes. Genetics 130: 7-16
49. Schaaper RM, Glickman BW, Loeb LA (1982) Mutagenesis resulting from depurination is an SOS process. Mutat Res 106: 1-9
50. Schlacher K, Cox MM, Woodgate R, Goodman MF (2006) RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature 442: 883-887
51. Schlacher K, Leslie K, Wyman C, Woodgate R, Cox MM, Goodman MF (2005) DNA polymerase V and RecA protein, a minimal mutasome. Mol Cell 17: 561-572
52. Shan Q, Bork JM, Webb BL, Inman RB, Cox MM (1997) RecA protein filaments: end-dependent dissociation from ssDNA and stabilization by RecO and RecR proteins. J Mol Biol 265: 519-540
53. Steinborn G (1978) Uvm mutants of E. coli K12 deficient in UV mutagenesis. 1. Isolation of uvmmutants and their phenotypical characterization in DNA repair and mutagenesis. Mol Gen Genet 165: 87-93
54. Sweasy JB, Witkin EM, Sinha N, Roegner-Maniscalco V (1990) RecA protein of Escherichia coli has a third essential role in SOS mutator activity. J Bacteriol 172: 3030-3036
55. Umezu K, Chi NW, Kolodner RD (1993) Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein. Proc Natl Acad Sci USA 90: 3875-3879
56. Umezu K, Kolodner RD (1994) Protein interactions in genetic recombination in Escherichia coli. Interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein. J Biol Chem 269: 30005-30013
57. Wang TC, Chang HY, Hung JL (1993) Cosuppression of recF, recR and recO mutations by mutant recA alleles in Escherichia coli cells. Mutat Res 294: 157-166
58. Whitby MC, Lloyd RG (1995) Altered SOS induction associated with mutations in recF, recO and recR. Mol Gen Genet 246: 174-179
59. Williams KR, Murphy JB, Chase JW (1984) Characterization of the structural and functional defect in the Escherichia coli single-stranded DNA binding protein encoded by the ssb-1 mutant gene. Expression of the ssb-1 gene under lambda pL regulation. J Biol Chem 259: 11804-11811
60. Wood RD, Stein J (1986) Role of the RecF gene product in UV mutagenesis of lambda phage. Mol Gen Genet 204: 82-84
61. Xu L, Marians KJ (2003) PriA mediates DNA replication pathway choice at recombination intermediates. Mol Cell 11: 817-826