Translesion DNA polymerases

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 10, 2013, Pages

  Goodman, Myron F ^a   Woodgate, Roger ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE;

ARCHAEON; BIOLOGICAL MODEL; CHEMISTRY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ESCHERICHIA COLI; GENETICS; HUMAN; MUTAGENESIS; PHYSIOLOGY; REVIEW; SACCHAROMYCES CEREVISIAE;

ARCHAEA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; HUMANS; MODELS, GENETIC; MUTAGENESIS; SACCHAROMYCES CEREVISIAE;

EID: 84875992884     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a010363     Document Type: Article

References (173)

1. Anderson WF, Prince DB, Yu H, McEntee K, Goodman MF. 1994. Crystallization of DNA polymerase II from Escher-ichia coli. J Mol Biol 238: 120-122.
2. Baranovskiy AG, Lada AG, Siebler HM, Zhang Y, Pavlov YI, Tahirov TH. 2012. DNA polymerase d and z switch by sharing accessory subunits of DNA polymerase d. J Biol Chem 287: 17281-17287.
3. Beaber JW, Hochhut B, Waldor MK. 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427: 72-74.
4. Bebenek K, Kunkel TA. 2004. Functions of DNA polymerases. Adv Protein Chem 69: 137-165.
5. Becherel OJ, Fuchs RP, Wagner J. 2002. Pivotal role of the β-clamp in translesion DNA synthesis and mutagenesis in E. coli cells. DNA Repair 1: 703-708.
6. Bemark M, Khamlichi AA, Davies SL, Neuberger MS. 2000. Disruption of mouse polymerase ζ (Rev3) leads to embryonic lethality and impairs blastocyst development in vitro. Curr Biol 10: 1213-1216.
7. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, Coull B, Kannouche P, Wider G, Peter M, Lehmann AR, et al. 2005. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310: 1821-1824.
8. Bienko M, Green CM, Sabbioneda S, Crosetto N, Matic I, Hibbert RG, Begovic T, Niimi A, Mann M, Lehmann AR, et al. 2010. Regulation of translesion synthesis DNA polymerase η by monoubiquitination. Mol Cell 37: 396-407.
9. Biertümpfel C, Zhao Y, Kondo Y, Ramon-Maiques S, Gregory M, Lee JY, Masutani C, Lehmann AR, Hanaoka F, Yang W. 2010. Structure and mechanism of human DNA polymerase η. Nature 465: 1044-1048.
10. Bomar MG, Pai MT, Tzeng SR, Li SS, Zhou P. 2007. Structure of the ubiquitin-binding zinc finger domain of human DNAY-polymerase T). EMBO Rep 8: 247-251.
11. Bomar MG, D'Souza S, Bienko M, Dikic I, Walker GC, Zhou P. 2010. Unconventional ubiquitin recognition by the ubiquitin-binding motif within the Y family DNA polymerases ι and Rev1. Mol Cell 37: 408-417.
12. Bonner CA, Randall SK, Rayssiguier C, Radman M, Eritja R, Kaplan BE, McEntee K, Goodman MF. 1988. Purification and characterization of an inducible Escherichia coli DNA polymerase capable of insertion and bypass at abasic lesions in DNA. J Biol Chem 263: 18946-18952.
13. Bonner CA, Hays S, McEntee K, Goodman MF. 1990. DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli. Proc Natl Acad Sci 87: 7663-7667.
14. - recombination by the mutagenesis complex UmuD'C. J Mol Biol 270: 201-211.
15. Boudsocq F, Iwai S, Hanaoka F, Woodgate R. 2001. Sulfolo-bus solfataricus P2 DNA polymerase IV (Dpo4): An ar-chaeal DNA polymerase with lesion-bypass properties akin to eukaryotic polη. Nucleic Acids Res 29: 4607-4616.
16. Boudsocq F, Kokoska RJ, Plosky BS, Vaisman A, Ling H, Kunkel TA, Yang W, Woodgate R. 2004. Investigating the role of the little finger domain of Y-family DNA polymerases in low-fidelity synthesis and translesion replication. J Biol Chem 279: 32932-32940.
17. Bridges BA, Woodgate R. 1984. Mutagenic repair in Escherichia coli, X. The umuC gene product may be required for replication past pyrimidine dimers but not for the coding error in UV mutagenesis. Mol Gen Genet 196: 364-366.
18. Bridges BA, Woodgate R. 1985a. Mutagenic repair in Escherichia coli: Products of the recA gene and of the umuD and umuC genes act at different steps in UV-induced mutagenesis. Proc Natl Acad Sci 82: 4193-4197.
19. Bridges BA, Woodgate R. 1985b. The two-step model of bacterial UV mutagenesis. Mutat Res 150: 133-139.
20. Brotcorne-Lannoye A, Maenhaut-Michel G. 1986. Role of RecA protein in untargeted UV mutagenesis of bacteriophage X: Evidence for the requirement for the dinB gene. Proc Natl Acad Sci 83: 3904-3908.
21. Bruck I, Woodgate R, McEntee K, Goodman MF. 1996. Purification of a soluble UmuD'C complex from Escherichia coli: Cooperative binding of UmuD'C to single-stranded DNA. J Biol Chem 271: 10767-10774.
22. Bull HJ, Lombardo MJ, Rosenberg SM. 2001. Stationary-phase mutation in the bacterial chromosome: Recombination protein and DNA polymerase IV dependence. Proc Natl Acad Sci 98: 8334-8341.
23. Burckhardt SE, Woodgate R, Scheuermann RH, Echols H. 1988. UmuD mutagenesis protein of Escherichia coli: Overproduction, purification and cleavage by RecA. Proc Natl Acad Sci 85: 1811-1815.
24. Chen L, Brugger K, Skovgaard M, Redder P, She Q, Torarinsson E, Greve B, Awayez M, Zibat A, Klenk HP, et al. 2005. The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187: 4992-4999.
25. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC. 2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41-64.
26. Dalrymple BP, Kongsuwan K, Wijffels G, Dixon NE, Jennings PA. 2001. A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc Natl Acad Sci 98: 11627-11632.
27. De Lucia P, Cairns J. 1969. Isolation of an E. coli strain with a mutation affecting DNA polymerase. Nature 224: 1164-1166.
28. Dumstorf CA, Clark AB, Lin Q, Kissling GE, Yuan T, Kucherlapati R, McGregor WG, Kunkel TA. 2006. Participation of mouse DNA polymerase ι in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc Natl Acad Sci 103: 18083-18088.
29. 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 Escher-ichia coli provide evidence foran additional role for RecA protein in UV mutagenesis. J Bacteriol 171: 2415-2423.
30. Echols H, Goodman MF. 1990. Mutation induced by DNA damage: A many protein affair. Mutat Res 236: 301-311.
31. Echols H, Goodman MF. 1991. Fidelity mechanisms inDNA replication. Annu Rev Biochem 60: 477-511.
32. Esposito G, Godindagger I, Klein U, Yaspo M, Cumano A, Rajewsky K. 2000. Disruption of the Rev3l-encoded catalytic subunit of polymerase ζ in mice results in early embryonic lethality. Curr Biol 10: 1221-1224.
33. Fernández De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, Ohmori H, Woodgate R. 2000. Identification of additional genes belonging to the LexA-regulon in Escherichia coli. Mol Microbiol 35: 1560-1572.
34. Foster PL, Gudmundsson G, Trimarchi JM, Cai H, Goodman MF. 1995. Proofreading-defective DNA poly-merase II increases adaptive mutation in Escherichia coli. Proc Natl Acad Sci 92: 7951-7955.
35. Frank EG, Ennis DG, Gonzalez M, Levine AS, Woodgate R. 1996. Regulation of SOS mutagenesis by proteolysis. Proc Natl Acad Sci 93: 10291-10296.
36. Friedberg EC, Walker GC, Siede W, Wood R, Schultz RA, Ellenberger T. 2006. DNA repair and mutagenesis. ASM Press, Washington, DC.
37. Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, Hastings PJ. 2010. Separate DNA Pol II-and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J Bacteriol 192: 4694-4700.
38. Fuchs RP, Fujii S. 2007. Translesion synthesis in Escherichia coli: Lessons from the NarI mutation hot spot. DNA Repair 6: 1032-1041.
39. Furukohri A, Goodman MF, Maki H. 2008. A dynamic po-lymerase exchange with Escherichia coli DNA polymerase IV replacing DNA polymerase III on the sliding clamp. J Biol Chem 283: 11260-11269.
40. Gefter ML, Hirota Y, Kornberg T, Wechsler JA, Barnoux C. 1971. Analysis of DNA polymerases II and III in mutants of Escherichia coli thermosensitive for DNA synthesis. Proc Natl Acad Sci 68: 3150-3153.
41. Gerlach VL, Aravind L, Gotway G, Schultz RA, Koonin EV, Friedberg EC. 1999. Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily. Proc Natl Acad Sci 96: 11922-11927.
42. Gerlach VL, Feaver WJ, Fischhaber PL, Friedberg EC. 2001. Purification and characterization of polκ, a DNA poly-merase encoded by the human DINB1 gene. J Biol Chem 276: 92-98.
43. Godoy VG, Jarosz DF, Simon SM, Abyzov A, Ilyin V, Walker GC. 2007. UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB. Mol Cell 28: 1058-1070.
44. Gonzalez M, Frank EG, Levine AS, Woodgate R. 1998. Lon-mediated proteolysis of the Escherichia coli UmuD mutagenesis protein: In vitro degradation and identification of residues required for proteolysis. Genes Dev 12: 3889-3899.
45. Gonzalez M, Rasulova F, Maurizi MR, Woodgate R. 2000. Subunit-specific degradation of the UmuD/D' hetero-dimer by the ClpXP protease: The role of trans recognition in UmuD' stability. EMBO J 19: 5251-5258.
46. Goodman MF. 2002. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 71: 17-50.
47. Guo C, Fischhaber PL, Luk-Paszyc MJ, Masuda Y, Zhou J, Kamiya K, Kisker C, Friedberg EC. 2003. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J 22: 6621-6630.
48. Guo C, Tang TS, Bienko M, Parker JL, Bielen AB, Sonoda E, Takeda S, Ulrich HD, Dikic I, Friedberg EC. 2006. Ubiq-uitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol Cell Biol 26: 8892-8900.
49. Hishiki A, Hashimoto H, Hanafusa T, Kamei K, Ohashi E, Shimizu T, Ohmori H, Sato M. 2009. Structural basis for novel interactions between human translesion synthesis polymerases and proliferating cell nuclear antigen. J Biol Chem 284: 10552-10560.
50. 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.
51. Hogg M, Seki M, Wood RD, Doublie S, Wallace SS. 2011. Lesion bypass activity of DNA polymerase u (POLQ) is an intrinsic property of the Pol domain and depends on unique sequence inserts. J Mol Biol 405: 642-652.
52. Indiani C, McInerney P, Georgescu R, Goodman MF, O'Donnell M. 2005. A sliding-clamp toolbelt binds high- and low-fidelity DNA polymerases simultaneously. Mol Cell 19: 805-815.
53. Indiani C, Langston LD, Yurieva O, Goodman MF, O'Donnell M. 2009. Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc Natl Acad Sci 106: 6031-6038.
54. Iwasaki H, Nakata A, Walker GC, Shinagawa H. 1990. The Escherichia coli polB gene, which encodes DNA polymer-ase II, is regulated by the SOS system. J Bacteriol 172: 6268-6273.
55. Jansen JG, Langerak P, Tsaalbi-Shtylik A, van den Berk P, Jacobs H, de Wind N. 2006. Strand-biased defect in C/G transversions in hypermutating immunoglobulin genes in Rev1-deficient mice. J Exp Med 203: 319-323.
56. Jarosz DF, Godoy VG, Delaney JC, Essigmann JM, Walker GC. 2006. A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439: 225-228.
57. 02C-RecA-ATP. Nature 460: 359-363.
58. Johnson A, O'Donnell M. 2005. Cellular DNA replicases: Components and dynamics at the replication fork. Annu Rev Biochem 74: 283-315.
59. Johnson RE, Kondratick CM, Prakash S, Prakash L. 1999a. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285: 263-265.
60. Johnson RE, Prakash S, Prakash L. 1999b. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, polh. Science 283: 1001-1004.
61. Johnson RE, Washington MT, Haracska L, Prakash S, Prakash L. 2000a. Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406: 1015-1019.
62. Johnson RE, Washington MT, Prakash S, Prakash L. 2000b. Fidelity of human DNA polymerase η. J Biol Chem 275: 7447-7450.
63. Johnson RE, Prakash L, Prakash S. 2012. Pol 31 and Pol 32 subunits of yeast DNA polymerase δ are also essential subunits of DNA polymerase ζ. Proc Natl Acad Sci 109: 12455-12460.
64. Jung YS, Liu G, Chen X. 2010. Pirh2 E3 ubiquitin ligase targets DNA polymerase η for 20S proteasomal degradation. Mol Cell Biol 30: 1041-1048.
65. Jung YS, Hakem A, Hakem R, Chen X. 2011. Pirh2 E3 ubiq-uitin ligase monoubiquitinates DNA polymerase h to suppress translesion DNA synthesis. Mol Cell Biol 19: 3997-4006.
66. Karata K, Vaisman A, Goodman MF, Woodgate R. 2012. Simple and efficient purification of E. coli DNA polymer-ase V: Cofactor requirements for optimal activity and processivity in vitro. DNA Repair 11: 431-440.
67. Kato T, Shinoura Y. 1977. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet 156: 121-131.
68. Kawamoto T, Araki K, Sonoda E, Yamashita YM, Harada K, Kikuchi K, Masutani C, Hanaoka F, Nozaki K, Hashimoto N, et al. 2005. Dual roles for DNA polymerase h in homologous DNA recombination and translesion DNA synthesis. Mol Cell 20: 793-799.
69. Kenyon CJ, Walker GC. 1980. DNA-damaging agents stimulate gene expression at specific loci in Escherichia coli. Proc Natl Acad Sci 77: 2819-2823.
70. Kim SR, Maenhaut-Michel G, Yamada M, Yamamoto Y, Matsui K, Sofuni T, Nohmi T, Ohmori H. 1997. 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 94: 13792-13797.
71. Kirouac KN, Ling H. 2009. Structural basis of error-prone replication and stalling at athymine base by human DNA polymerase ι. EMBO J 28: 1644-1654.
72. Knippers R. 1970. DNA polymerase II. Nature 228: 1050-1053.
73. Kulaeva OI, Wootton JC, Levine AS, Woodgate R. 1995. Characterization of the umu-complementing operon from R391. J Bacteriol 177: 2737-2743.
74. Kulaeva OI, Koonin EV, McDonald JP, Randall SK, Rabi-novich N, Connaughton JF, Levine AS, Woodgate R. 1996. Identification of a DinB/UmuC homolog in the archeon Sulfolobus solfataricus. Mutat Res 357: 245-253.
75. Kumari A, Minko IG, Harbut MB, Finkel SE, Goodman MF, Lloyd RS. 2008. Replication bypass of interstrand crosslink intermediates by Escherichia coli DNA polymerase IV. J Biol Chem 283: 27433-27437.
76. Kuzminov A. 1999. Recombinational repairofDNA damage in Escherichia coli and bacteriophage l. Microbiol Mol Biol Rev 63: 751-813.
77. Lange SS, Takata K, Wood RD. 2011. DNA polymerases and cancer. Nat Rev Cancer 11: 96-110.
78. Lawrence CW, Hinkle DC. 1996. DNA polymerase ζ and the control of DNA damage induced mutagenesis in eukary-otes. In Cancer surveys: Genetic instability in cancer (ed. Lindahl T), pp. 21-31. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
79. Lemontt JF. 1971. Mutants of yeast defective in mutation induced by ultraviolet light. Genetics 68: 21-33.
80. Lewis LK, Harlow GR, Gregg-Jolly LA, Mount DW. 1994. Identification of high affinity binding sites for LexA which define new DNA damage-inducible genes in Es-cherichia coli. J Mol Biol 241: 507-523.
81. Lia G, Michel B, Allemand JF. 2012. Polymerase exchange during Okazaki fragment synthesis observed in living cells. Science 335: 328-331.
82. Ling H, Boudsocq F, Woodgate R, Yang W. 2001. Crystal structure of a Y-family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication. Cell 107: 91-102.
83. Ling H, Boudsocq F, Plosky BS, Woodgate R, Yang W. 2003. Replication of a cis-syn thymine dimer at atomic resolution. Nature 424: 1083-1087.
84. Ling H, Boudsocq F, Woodgate R, Yang W. 2004a. Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts. Mol Cell 13: 751-762.
85. Ling H, Sayer JM, Plosky BS, Yagi H, Boudsocq F, Woodgate R, Jerina DM, Yang W. 2004b. Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase. Proc Natl Acad Sci 101: 2265-2269.
86. Little JW, Edmiston SH, Pacelli LZ, Mount DW. 1980. Cleavage of the Escherichia coli lexA protein by the recA protease. Proc Natl Acad Sci 77: 3225-3229.
87. Maga G, Villani G, Crespan E, Wimmer U, Ferrari E, Bertocci B, Hubscher U. 2007. 8-Oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447: 606-608.
88. Makarova AV, Stodola JL, Burgers PM. 2012. A four-subunit DNA polymerase z complex containing Pol d accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res doi: 10.1093/nar/gks948.
89. Masutani C, Araki M, Yamada A, Kusumoto R, Nogimori T, Maekawa T, Iwai S, Hanaoka F. 1999a. Xeroderma pig-mentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J 18: 3491-3501.
90. Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, Yuasa M, Araki M, Iwai S, Takio K, Hanaoka F.1999b. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase h. Nature 399: 700-704.
91. Matsuda T, Bebenek K, Masutani C, Rogozin IB, Hanaoka F, Kunkel TA. 2001. Error rate and specificity of human and murine DNA polymerase h. J Mol Biol 312: 335-346.
92. McCann JC, Springarn NE, Kobari J, Ames BN. 1975. Detection of carcinogens as mutagens: Bacterial tester strains with R factor plasmids. Proc Natl Acad Sci 72: 979-983.
93. McDonald JP, Levine AS, Woodgate R. 1997. The Saccharo-myces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147: 1557-1568.
94. McDonald JP, Rapic-Otrin V, Epstein JA, Broughton BC, Wang X, Lehmann AR, Wolgemuth DJ, Woodgate R. 1999. Novel human and mouse homologs of Saccharo-myces cerevisiae DNA polymeraseh. Genomics 60:20-30.
95. McDonald JP, Frank EG, Plosky BS, Rogozin IB, Masutani C, Hanaoka F, Woodgate R, Gearhart PJ. 2003. Identification of a nonsense mutation in DNA polymerase i from 129-derived strains of mice and its effect on somatic hy-permutation. J Exp Med 198: 635-643.
96. McDonald JP, Hall A, Gasparutto D, Cadet J, Ballantyne J, Woodgate R. 2006. Novel thermostable Y-family poly-merases: Applications for the PCR amplification of damaged or ancient DNAs. Nucleic Acids Res 34: 1102-1111.
97. McHenry CS. 2011. DNA replicases from a bacterial perspective. Annu Rev Biochem 80: 403-436.
98. McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, West SC. 2005. Human DNA polymerase h promotes DNA synthesis from strand invasion intermediates (D-loops) of homologous recombination. Mol Cell 20: 783-792.
99. 0B from the IncJ conjugative transposon, R391. Mol Micro-biol 63: 797-810.
100. Nair DT, Johnson RE, Prakash S, Prakash L, Aggarwal AK. 2004. Replication by human DNA polymerase ι occurs by Hoogsteen base-pairing. Nature 430: 377-380.
101. Nair DT, Johnson RE, Prakash L, Prakash S, Aggarwal AK. 2005. Rev1 employsa novel mechanism of DNA synthesis using a protein template. Science 309: 2219-2222.
102. Nair DT, Johnson RE, Prakash L, Prakash S, Aggarwal AK. 2006. An incoming nucleotide imposes an anti to syn conformational change on the templating purine in the human DNA polymerase-ι active site. Structure 14: 749-755.
103. 0 mediate tethering and substrate processingbythe ClpXP protease. Proc Natl Acad Sci 100: 13219-13224.
104. Nelson JR, Lawrence CW, Hinkle DC. 1996a. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382: 729-731.
105. Nelson JR, Lawrence CW, Hinkle DC. 1996b. Thymine-thymine dimer bypass by yeast DNA polymerase z. Science 272: 1646-1649.
106. Nohmi T, Battista JR, Dodson LA, Walker GC. 1988. RecA-mediated cleavage activates UmuD for mutagenesis: Mechanistic relationship between transcriptional dere-pression and posttranslational activation. Proc Natl Acad Sci 85: 1816-1820.
107. Ogi T, Kato TJ, Kato T, Ohmori H. 1999. Mutation enhancement by DINB1, a mammalian homologue of the Escher-ichia coli mutagenesis protein DinB. Genes Cells 4: 607-618.
108. Ogi T, Shinkai Y, Tanaka K, Ohmori H. 2002. Polk protects mammalian cells against the lethal and mutagenic effects of polycyclic hydrocarbons. Proc Natl Acad Sci 99: 15548-15553.
109. Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K, Cloney R, Nakazawa Y, Niimi A, Miki Y, Jaspers NG, et al. 2010. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol Cell 37: 714-727.
110. Ohashi E, Ogi T, Kusumoto R, Iwai S, Masutani C, Hanaoka F, Ohmori H. 2000. Error-prone bypass of certain DNA lesions by the human DNA polymerase k. Genes Dev 14: 1589-1594.
111. Ohashi E, Murakumo Y, Kanjo N, Akagi J, Masutani C, Hanaoka F, Ohmori H. 2004. Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9: 523-531.
112. Ohkumo T, Kondo Y, Yokoi M, Tsukamoto T, Yamada A, Sugimoto T, Kanao R, Higashi Y, Kondoh H, Tatematsu M, et al. 2006. UV-B radiation induces epithelial tumors in mice lacking DNA polymerase h and mes-enchymal tumors in mice deficient for DNA polymerase i. Mol Cell Biol 26: 7696-7706.
113. Ohmori H, Hatada E, Qiao Y, Tsuji M, Fukuda R. 1995. dinP, a new gene in Escherichia coli, whose product shows similarities to UmuC and its homologues. Mutat Res 347: 1-7.
114. Ohmori H, Friedberg EC, Fuchs RPP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, et al. 2001. The Y-family of DNA polymerases. Mol Cell 8: 7-8.
115. Pata JD. 2010. Structural diversity of the Y-family DNA polymerases. Biochim Biophys Acta 1804: 1124-1135.
116. Patel M, Jiang Q, Woodgate R, Cox MM, Goodman MF. 2010. A new model for SOS-induced mutagenesis: How RecA protein activates DNA polymerase V. Crit Rev Bio-chem Mol Biol 45: 171-184.
117. Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, Scharff MD. 2008. The biochemistry of somatic hypermutation. Annu Rev Immunol 26: 481-511.
118. Perry KL, Walker GC. 1982. Identification of plasmid (pKM101) coded proteins involved in mutagenesis and UV resistance. Nature 300: 278-281.
119. Petruska J, Goodman MF. 1995. Enthalpy-entropy compensation in DNA melting thermodynamics. J Biol Chem 270: 746-750.
120. Petruska J, Sowers LC, Goodman MF. 1986. Comparison of nucleotide interactions in water, proteins, and vacuum: Model for DNA polymerase fidelity. Proc Natl Acad Sci 83: 1559-1562.
121. Pham P, Bertram JG, O'Donnell M, Woodgate R, Goodman MF. 2001. A model for SOS-lesion targeted mutations in E. coli involving pol V, RecA, SSB and b sliding clamp. Nature 409: 366-370.
122. Plosky BS, Vidal A, Fernández De Henestrosa AR, McLenigan MP, McDonald JP, Mead S, Woodgate R. 2006. Controlling the subcellular localizationof DNA polymer-ases i and h via interactions with ubiquitin. EMBO J 25: 2847-2855.
123. Qiu Z, Goodman MF. 1997. The Escherichia coli polB locus is identical to dinA, the structural gene for DNA polymer-ase II. Characterization of Pol II purified from a polB mutant. J Biol Chem 272: 8611-8617.
124. Radman M. 1974. Phenomenology of an inducible muta-genic DNA repair pathway in Escherichia coli: SOS repair hypothesis. In Molecular and environmental aspects of mutagenesis (ed. Prakash L, et al.), pp. 128-142. Charles C. Thomas, Springfield, IL.
125. Rajagopalan M, Lu C, Woodgate R, O'Donnell M, Goodman MF, Echols H. 1992. Activity of the purified mutagenesis proteins UmuC, UmuD' and RecA in repli-cative bypass of an abasic DNA lesion by DNA polymer-ase III. Proc Natl Acad Sci 89: 10777-10781.
126. Rangarajan S, Gudmundsson G, Qiu Z, Foster PL, Goodman MF. 1997. Escherichia coli DNA polymerase II catalyzes chromosomal and episomal DNA synthesis in vivo. Proc Natl Acad Sci 94: 946-951.
127. 0, RecA, and SSB and is specialized for translesion replication. J Biol Chem 274: 31763-31766.
128. Reyes-Lamothe R, Sherratt DJ, Leake MC. 2010. Stoichiom-etry and architecture of active DNA replication machinery in Escherichia coli. Science 328: 498-501.
129. Rogozin IB, Pavlov YI, Bebenek K, Matsuda T, Kunkel TA. 2001. Somatic mutation hotspots correlate with DNA polymerase h error spectrum. Nat Immunol 2: 530-536.
130. Roush AA, Suarez M, Friedberg EC, Radman M, Siede W. 1998. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol Gen Genet 257: 686-692.
131. Sale JE, Lehmann AR, Woodgate R. 2012. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13: 141-152.
132. Schenten D, Gerlach VL, Guo C, Velasco-Miguel S, Hladik CL, White CL, Friedberg EC, Rajewsky K, Esposito G. 2002. DNA polymerase κ deficiency does not affect somatic hypermutation in mice. EurJ Immunol 32: 3152-3160.
133. Schlacher K, Goodman MF. 2007. Lessons from 50 years of SOS DNA-damage-induced mutagenesis. Nat Rev Mol Cell Biol 8: 587-594.
134. 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.
135. Seki M, Wood RD. 2008. DNA polymerase θ (POLQ) can extend from mismatches and from bases opposite a (6-4) photoproduct. DNA Repair 7: 119-127.
136. She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC, Clausen IG, Curtis BA, De Moors A, et al. 2001. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci 98: 7835-7840.
137. Shinagawa H, Iwasaki H, Kato T, Nakata A. 1988. RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci 85: 1806-1810.
138. Shtygasheva AA, Belousova EA, Rechkunova NI, Lebedeva NA, Lavrik OI. 2008. DNA polymerases β and γ as potential participants of TLS during genomic DNA replication on the lagging strand. Biochemistry (Mosc) 73: 1207-1213.
139. Silvian LF, Toth EA, Pham P, Goodman MF, Ellenberger T. 2001. Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat Struct Biol 8: 984-989.
140. Skoneczna A, McIntyre J, Skoneczny M, Policinska Z, Sled-ziewska-Gojska E. 2007. Polymerase h is a short-lived, proteasomally degraded protein that is temporarily stabilized following UV irradiation in Saccharomyces cerevi-siae. J Mol Biol 366: 1074-1086.
141. 0C protein complex in Escherichia coli switches repair from homologous recombination to SOS muta-genesis. Mol Microbiol 10: 963-971.
142. Steinborn G. 1978. Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol Gen Genet 165: 87-93.
143. Swan MK, Johnson RE, Prakash L, Prakash S, Aggarwal AK. 2009. Structure of the human Rev1-DNA-dNTP ternary complex. J Mol Biol 390: 699-709.
144. 02-C mutagenic complex and RecA. Proc Natl Acad Sci 95: 9755-9760.
145. 02C is an error-prone DNA polymerase, Escherichia coli, DNA pol V. Proc Natl Acad Sci 96: 8919-8924.
146. Tissier A, McDonald JP, Frank EG, Woodgate R. 2000. Poli, a remarkably error-prone human DNA polymerase. Genes Dev 14: 1642-1650.
147. Tissier A, Kannouche P, Reck MP, Lehmann AR, Fuchs RP, Cordonnier A. 2004. Co-localization in replication foci and interaction of human Y-family members, DNA polymerase polh and REVl protein. DNA Repair 3: 1503-1514.
148. Tompkins JD, Nelson JL, Hazel JC, Leugers SL, Stumpf JD, Foster PL. 2003. Error-prone polymerase, DNA polymer-ase IV, is responsible for transient hypermutation during adaptive mutation in Escherichia coli. J Bacteriol 185: 3469-3472.
149. Trincao J, Johnson RE, Escalante CR, Prakash S, Prakash L, Aggarwal AK. 2001. Structure of the catalytic core of S. cerevisiae DNA polymerase h. Implications for trans-lesion DNA synthesis. Mol Cell 8: 417-426.
150. Vaisman A, McDonald JP, Woodgate R. 2012. Translesion DNA synthesis. In EcoSal-Escherichia coli and Salmonella: Cellular and molecular biology (ed. Böck A, Curtiss R III, Kaper JB, Karp PD, Neidhardt FC, Slauch JM, Squires CL). ASM Press, Washington, DC.
151. Villani G, Hubscher U, Gironis N, Parkkinen S, Pospiech H, Shevelev I, Di Cicco G, Markkanen E, Syvaoja JE, Tanguy Le Gac N. 2011. In vitro gap-directed translesion DNA synthesis of an abasic site involving human DNA poly-merases1, l, and b. J Biol Chem 286: 32094-32104.
152. Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, Fuchs RPP, Nohmi T. 1999. The dinB gene encodes a novel Escher-ichia coli DNA polymerase, DNA Pol IV, involved in mu-tagenesis. Mol Cell 4: 281-286.
153. Wagner J, Fujii S, Gruz P, Nohmi T, Fuchs RP. 2001. The b clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep 1: 484-488.
154. Walker GC. 1984. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Micro-biol Rev 48: 60-93.
155. Wang F, Yang W. 2009. Structural insight into translesion synthesis by DNA Pol II. Cell 139: 1279-1289.
156. Warbrick E. 1998. PCNA binding through a conserved motif. Bioessays 20: 195-199.
157. Warbrick E. 2000. The puzzle of PCNA's many partners. Bioessays 22: 997-1006.
158. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. 2009. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Molec Biol Rev 73: 134-154.
159. Watson JD, Crick FH. 1953. Molecular structure of nucleic acids; A structure for deoxyribose nucleic acid. Nature 171: 737-738.
160. Weigle JJ. 1953. Induction of mutation in a bacterial virus. Proc Natl Acad Sci 39: 628-636.
161. Wilson RC, Pata JD. 2008. Structural insights into the generation of single-base deletions by the Y family DNA polymerase Dbh. Mol Cell 29: 767-779.
162. Witkin EM. 1967. The radiation sensitivity of Escherichia coli B: A hypothesis relating filament formation and pro-phage induction. Proc Natl Acad Sci 57: 1275-1279.
163. Witkin EM. 1976. Ultraviolet mutagenesis and inducible DNA repair inEscherichia coli. Bacteriol Rev 40: 869-907.
164. Wittschieben J, Shivji MK, Lalani E, Jacobs MA, Marini F, Gearhart PJ, Rosewell I, Stamp G, Wood RD. 2000. Disruption of the developmentally regulated REV3L gene causes embryonic lethality. Curr Biol 10: 1217-1220.
165. Wittschieben JP, Reshmi SC, Gollin SM, Wood RD. 2006. Loss of DNA polymerase z causes chromosomal instability in mammalian cells. Cancer Res 66: 134-142.
166. 0. Proc Natl Acad Sci 86: 7301-7305.
167. Yamanaka K, Minko IG, Takata K, Kolbanovskiy A, Kozekov ID, Wood RD, Rizzo CJ, Lloyd RS. 2010. Novel enzymatic function of DNA polymerasenin trans-lesion DNA synthesis past major groove DNA-peptide and DNA-DNA cross-links. Chem Res Toxicol 23: 689-695.
168. Yang W, Woodgate R. 2007. What a difference a decade makes: Insights into translesion DNA synthesis. Proc Natl Acad Sci 104: 15591-15598.
169. Yeiser B, Pepper ED, Goodman MF, Finkel SE. 2002. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. Proc Natl Acad Sci 99: 8737-8741.
170. Zeng X, Winter DB, Kasmer C, Kraemer KH, Lehmann AR, Gearhart PJ. 2001. DNA polymerase h is an A-Tmutator in somatic hypermutation of immunoglobulin variable genes. Nat Immunol 2: 537-541.
171. Zhang Y, Yuan F, Wu X, Wang Z. 2000. Preferential incorporation of G opposite template T by the low-fidelity human DNA polymerase i. Mol Cell Biol 20: 7099-7108.
172. Zhang Y, Yuan F, Wu X, Taylor J-S, Wang Z. 2001. Response of human DNA polymerase i to DNA lesions. Nucleic Acids Res 29: 928-935.
173. Zhou B, Pata JD, Steitz TA. 2001. Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain. Mol Cell 8: 427-437.