UmuD and RecA Directly Modulate the Mutagenic Potential of the Y Family DNA Polymerase DinB

Molecular Cell

Volumn 28, Issue 6, 2007, Pages 1058-1070

  Godoy, Veronica G ^a,b   Jarosz, Daniel F ^a   Simon, Sharotka M ^a   Abyzov, Alexej ^b   Ilyin, Valentin ^b   Walker, Graham C ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

DNA; MICROBIO

Indexed keywords

BACTERIAL PROTEIN; DNA POLYMERASE; GENE PRODUCT; PROTEIN DINB; PROTEIN UMUD; RECA PROTEIN; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; DNA DAMAGE; EUKARYOTE; FRAMESHIFT MUTATION; NONHUMAN; ORTHOLOGY; PHENOTYPE; PROTEIN FAMILY; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; BINDING SITES; BLOTTING, FAR-WESTERN; DNA POLYMERASE BETA; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REC A RECOMBINASES; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA;

EID: 37349132340     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.10.025     Document Type: Article

References (66)

1. Afonnikov D.A., and Kolchanov N.A. CRASP: a program for analysis of coordinated substitutions in multiple alignments of protein sequences. Nucleic Acids Res. 32 (2004) W64-W68
2. Bailone A., Sommer S., Knezevic J., Dutreix M., and Devoret R. A RecA protein mutant deficient in its interaction with the UmuDC complex. Biochimie 73 (1991) 479-484
3. Battista J.R., Ohta T., Nohmi T., Sun W., and Walker G.C. Dominant negative umuD mutations decreasing RecA-mediated cleavage suggest roles for intact UmuD in modulation of SOS mutagenesis. Proc. Natl. Acad. Sci. USA 87 (1990) 7190-7194
4. Bavoux C., Leopoldino A.M., Bergoglio V., O-Wang J., Ogi T., Bieth A., Judde J.G., Pena S.D., Poupon M.F., Helleday T., et al. Up-regulation of the error-prone DNA polymerase kappa promotes pleiotropic genetic alterations and tumorigenesis. Cancer Res. 65 (2005) 325-330
5. Becherel O.J., Fuchs R.P., and Wagner J. Pivotal role of the beta-clamp in translesion DNA synthesis and mutagenesis in E. coli cells. DNA Repair (Amst.) 1 (2002) 703-708
6. Bergoglio V., Bavoux C., Verbiest V., Hoffmann J.S., and Cazaux C. Localisation of human DNA polymerase kappa to replication foci. J. Cell Sci. 115 (2002) 4413-4418
7. Beuning P.J., Sawicka D., Barsky D., and Walker G.C. Two processivity clamp interactions differentially alter the dual activities of UmuC. Mol. Microbiol. 59 (2006) 460-474
8. Beuning P.J., Simon S.M., Godoy V.G., Jarosz D.F., and Walker G.C. Characterization of Escherichia coli translesion synthesis polymerases and their accessory factors. Methods Enzymol. 408 (2006) 318-340
9. Beuning P.J., Simon S.M., Zemla A., Barsky D., and Walker G.C. A non-cleavable UmuD variant that acts as a UmuD′ mimic. J. Biol. Chem. 281 (2006) 9633-9640
10. Brotcorne-Lannoye A., and Maenhaut-Michel G. Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene. Proc. Natl. Acad. Sci. USA 83 (1986) 3904-3908
11. Bunting K.A., Roe S.M., and Pearl L.H. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp. EMBO J. 22 (2003) 5883-5892
12. Burckhardt S.E., Woodgate R., Scheuermann R.H., and Echols H. UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc. Natl. Acad. Sci. USA 85 (1988) 1811-1815
13. Cairns J., and Foster P.L. Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128 (1991) 695-701
14. Chen B.P., and Hai T. Expression vectors for affinity purification and radiolabeling of proteins using Escherichia coli as host. Gene 139 (1994) 73-75
15. Dalrymple B.P., Kongsuwan K., Wijffels G., Dixon N.E., and Jennings P.A. A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc. Natl. Acad. Sci. USA 98 (2001) 11627-11632
16. Donnelly C.E., and Walker G.C. groE mutants of Escherichia coli are defective in umuDC-dependent UV mutagenesis. J. Bacteriol. 171 (1989) 6117-6125
17. Elledge S.J., and Walker G.C. Proteins required for ultraviolet light and chemical mutagenesis. Identification of the products of the umuC locus of Escherichia coli. J. Mol. Biol. 164 (1983) 175-192
18. Foster P.L. Methods for determining spontaneous mutation rates. Methods Enzymol. 409 (2006) 195-213
19. Frampton J., Irmisch A., Green C.M., Neiss A., Trickey M., Ulrich H.D., Furuya K., Watts F.Z., Carr A.M., and Lehmann A.R. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell 17 (2006) 2976-2985
20. Frank R. The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports-principles and applications. J. Immunol. Methods 267 (2002) 13-26
21. Frank E.G., Hauser J., Levine A.S., and Woodgate R. Targeting of the UmuD, UmuD′, and MucA′ mutagenesis proteins to DNA by RecA protein. Proc. Natl. Acad. Sci. USA 90 (1993) 8169-8173
22. Friedberg E.C., Wagner R., and Radman M. Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296 (2002) 1627-1630
23. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis, Second Edition (2006), ASM Press, Washington, DC
24. Fuchs R.P., Fujii S., and Wagner J. Properties and functions of Escherichia coli: Pol IV and Pol V. Adv. Protein Chem. 69 (2004) 229-264
25. Fujii S., Isogawa A., and Fuchs R.P. RecFOR proteins are essential for Pol V-mediated translesion synthesis and mutagenesis. EMBO J. 25 (2006) 5754-5763
26. Godoy V.G., Gizatullin F.S., and Fox M.S. Some features of the mutability of bacteria during nonlethal selection. Genetics 154 (2000) 49-59
27. Goodman M.F. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71 (2002) 17-50
28. Grudniak A.M., Kuc M., and Wolska K.I. Role of Escherichia coli DnaK and DnaJ chaperones in spontaneous and induced mutagenesis and their effect on UmuC stability. FEMS Microbiol. Lett. 242 (2005) 361-366
29. Jarosz D.F., Godoy V.G., Delaney J.C., Essigmann J.M., and Walker G.C. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439 (2006) 225-228
30. Jarosz D.F., Beuning P.J., Cohen S.E., and Walker G.C. Y-family DNA polymerases in Escherichia coli. Trends Microbiol. 15 (2007) 70-77
31. Kato T., and Shinoura Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol. Gen. Genet. 156 (1977) 121-131
32. Kenyon C.J., and Walker G.C. DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli. Proc. Natl. Acad. Sci. USA 77 (1980) 2819-2823
33. Kim S.R., Maenhaut-Michel G., Yamada M., Yamamoto Y., Matsui K., Sofuni T., Nohmi T., and Ohmori H. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc. Natl. Acad. Sci. USA 94 (1997) 13792-13797
34. Kim S.R., Matsui K., Yamada M., Gruz P., and Nohmi T. Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol. Genet. Genomics 266 (2001) 207-215
35. Kobayashi S., Valentine M.R., Pham P., O'Donnell M., and Goodman M.F. Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment. J. Biol. Chem. 277 (2002) 34198-34207
36. Konola J.T., Nastri H.G., Logan K.M., and Knight K.L. Mutations at Pro67 in the RecA protein P-loop motif differentially modify coprotease function and separate coprotease from recombination activities. J. Biol. Chem. 270 (1995) 8411-8419
37. Layton J.C., and Foster P.L. Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol. Microbiol. 50 (2003) 549-561
38. Layton J.C., and Foster P.L. Error-prone DNA polymerase IV is regulated by the heat shock chaperone GroE in Escherichia coli. J. Bacteriol. 187 (2005) 449-457
39. Lee M.H., and Walker G.C. Interactions of Escherichia coli UmuD with activated RecA analyzed by cross-linking UmuD monocysteine derivatives. J. Bacteriol. 178 (1996) 7285-7294
40. Lenne-Samuel N., Wagner J., Etienne H., and Fuchs R.P. The processivity factor beta controls DNA polymerase IV traffic during spontaneous mutagenesis and translesion synthesis in vivo. EMBO Rep. 3 (2002) 45-49
41. Ling H., Boudsocq F., Woodgate R., and Yang W. Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell 107 (2001) 91-102
42. Lone S., Townson S.A., Uljon S.N., Johnson R.E., Brahma A., Nair D.T., Prakash S., Prakash L., and Aggarwal A.K. Human DNA polymerase κ encircles DNA: implications for mismatch extension and lesion bypass. Mol. Cell 25 (2007) 601-614
43. McGrew D.A., and Knight K.L. Molecular design and functional organization of the RecA protein. Crit. Rev. Biochem. Mol. Biol. 38 (2003) 385-432
44. McKenzie G.J., Lee P.L., Lombardo M.J., Hastings P.J., and Rosenberg S.M. SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol. Cell 7 (2001) 571-579
45. Niehbuhr K., and Wehland J. Screening of antibody epitopes and regions of protein-protein interaction sites using SPOT peptides. In: Lefkovits I. (Ed). Immunology Methods Manual: The Comprehensive Sourcebook of Techniques (1997), Academic Press, San Diego, CA
46. Nohmi T. Environmental stress and lesion-bypass DNA polymerases. Annu. Rev. Microbiol. 60 (2006) 231-253
47. Nohmi T., Battista J.R., Dodson L.A., and Walker G.C. RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc. Natl. Acad. Sci. USA 85 (1988) 1816-1820
48. Ogi T., Kannouche P., and Lehmann A.R. Localisation of human Y-family DNA polymerase kappa: relationship to PCNA foci. J. Cell Sci. 118 (2005) 129-136
49. Ohmori H., Friedberg E.C., Fuchs R.P., Goodman M.F., Hanaoka F., Hinkle D., Kunkel T.A., Lawrence C.W., Livneh Z., Nohmi T., et al. The Y-family of DNA polymerases. Mol. Cell 8 (2001) 7-8
50. Potapova O., Grindley N.D., and Joyce C.M. The mutational specificity of the Dbh lesion bypass polymerase and its implications. J. Biol. Chem. 277 (2002) 28157-28166
51. Reuven N.B., Arad G., Maor-Shoshani A., and Livneh Z. The mutagenesis protein UmuC is a DNA polymerase activated by UmuD′, RecA, and SSB and is specialized for translesion replication. J. Biol. Chem. 274 (1999) 31763-31766
52. Salles B., and Paoletti C. Control of UV induction of RecA protein. Proc. Natl. Acad. Sci. USA 80 (1983) 65-69
53. Schlacher K., Leslie K., Wyman C., Woodgate R., Cox M.M., and Goodman M.F. DNA polymerase V and RecA protein, a minimal mutasome. Mol. Cell 17 (2005) 561-572
54. Schlacher K., Cox M.M., Woodgate R., and Goodman M.F. RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature 442 (2006) 883-887
55. Silvian L.F., Toth E.A., Pham P., Goodman M.F., and Ellenberger T. Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat. Struct. Biol. 8 (2001) 984-989
56. Simon S.M., Sousa F., Mohana-Borges R.S., and Walker G.C. Regulation of E. coli Mutagenesis by Dimeric Intrinsically Disordered umuD Gene Products. Proc. Natl. Acad. Sci. USA (2007) in press
57. Story R.M., Weber I.T., and Steitz T.A. The structure of the E. coli RecA protein monomer and polymer. Nature 355 (1992) 318-325
58. Sutton M.D., and Walker G.C. Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination. Proc. Natl. Acad. Sci. USA 98 (2001) 8342-8349
59. Sutton M.D., and Walker G.C. umuDC-mediated cold sensitivity is a manifestation of functions of the UmuD(2)C complex involved in a DNA damage checkpoint control. J. Bacteriol. 183 (2001) 1215-1224
60. Sutton M.D., Opperman T., and Walker G.C. The Escherichia coli SOS mutagenesis proteins UmuD and UmuD′ interact physically with the replicative DNA polymerase. Proc. Natl. Acad. Sci. USA 96 (1999) 12373-12378
61. Sutton M.D., Farrow M.F., Burton B.M., and Walker G.C. Genetic interactions between the Escherichia coli umuDC gene products and the beta processivity clamp of the replicative DNA polymerase. J. Bacteriol. 183 (2001) 2897-2909
62. 2 protein. DNA Repair (Amst.) 1 (2002) 77-93
63. Tang M., Shen X., Frank E.G., O'Donnell M., Woodgate R., and Goodman M.F. UmuD′(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl. Acad. Sci. USA 96 (1999) 8919-8924
64. Tompkins J.D., Nelson J.L., Hazel J.C., Leugers S.L., Stumpf J.D., and Foster P.L. Error-prone polymerase, DNA polymerase IV, is responsible for transient hypermutation during adaptive mutation in Escherichia coli. J. Bacteriol. 185 (2003) 3469-3472
65. Wagner J., Gruz P., Kim S.R., Yamada M., Matsui K., Fuchs R.P., and Nohmi T. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4 (1999) 281-286
66. Woodgate R., and Ennis D.G. Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol. Gen. Genet. 229 (1991) 10-16