Y-family DNA polymerases and their role in tolerance of cellular DNA damage

Nature Reviews Molecular Cell Biology

Volumn 13, Issue 3, 2012, Pages 141-152

  Sale, Julian E ^a   Lehmann, Alan R ^b   Woodgate, Roger ^c  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; DNA POLYMERASE; UNCLASSIFIED DRUG; Y FAMILY DNA POLYMERASE;

DNA DAMAGE; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRUCTURE ANALYSIS;

ANIMALS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMANS; MUTAGENESIS; NUCLEOTIDYLTRANSFERASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84857411787     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3289     Document Type: Review

References (133)

1. Ohmori, H. et al. The Y-family of DNA polymerases. Mol. Cell 8, 7-8 (2001). (Pubitemid 32772900)
2. Rupp, W. D. & Howard-Flanders, P. Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J. Mol. Biol. 31, 291-304 (1968).
3. Radman, M. in Molecular and Environmental Aspects of Mutagenesis (eds Prakash, L., Sherman, F., Miller, M. W., Lawrence, C. W. & Tabor, H. W.) 128-142 (Charles, C. Thomas, Springfield, Illinois, 1974).
4. Lemontt, J. F. Mutants of yeast defective in mutation induced by ultraviolet light. Genetics 68, 21-33 (1971).
5. Kato, T. & Shinoura, Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol. Gen. Genet. 156, 121-131 (1977). (Pubitemid 8217165)
6. Steinborn, G. 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 (1978). (Pubitemid 9021075)
7. Lehmann, A. R. et al. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl Acad. Sci. USA 72, 219-223 (1975).
8. Nelson, J. R., Lawrence, C. W. & Hinkle, D. C. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382, 729-731 (1996). (Pubitemid 26282181)
9. Nelson, J. R., Lawrence, C. W. & Hinkle, D. C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272, 1646-1649 (1996). (Pubitemid 26200022)
10. Johnson, R. E., Prakash, S. & Prakash, L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη. Science 283, 1001-1004 (1999).
11. Masutani, C. et al. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399, 700-704 (1999). (Pubitemid 29289067)
12. Johnson, R. E., Kondratick, C. M., Prakash, S. & Prakash, L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285, 263-265 (1999). (Pubitemid 29330001)
13. Wagner, J. et al. The dinB gene encodes a novel, E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4, 281-286 (1999). (Pubitemid 29456897)
14. Reuven, N. B., Arad, G., Maor-Shoshani, A. & 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, 31763-31766 (1999).
15. Tang, M. et al. UmuD′2C is an error-prone DNA polymerase, Escherichia coli pol V. Proc. Natl Acad. Sci. USA 96, 8919-8924 (1999).
16. McDonald, J. P., Levine, A. S. & Woodgate, R. The Saccharomyces 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 (1997).
17. Tissier, A., McDonald, J. P., Frank, E. G. & Woodgate, R. polι, a remarkably error-prone human DNA polymerase. Genes Dev. 14, 1642-1650 (2000). (Pubitemid 30460913)
18. Johnson, R. E., Washington, M. T., Haracska, L., Prakash, S. & Prakash, L. Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406, 1015-1019 (2000).
19. Zhang, Y., Yuan, F., Wu, X. & Wang, Z. Preferential incorporation of G opposite template T by the low-fidelity human DNA polymerase ι. Mol. Cell. Biol. 20, 7099-7108 (2000).
20. Ogi, T., Kato, T. Jr, Kato, T. & Ohmori, H. Mutation enhancement by DINB1, a mammalian homologue of the Escherichia coli mutagenesis protein dinB. Genes Cells 4, 607-618 (1999). (Pubitemid 30043542)
21. Gerlach, V. L. et al. Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily. Proc. Natl Acad. Sci. USA 96, 11922-11927 (1999). (Pubitemid 29502834)
22. Ohashi, E. et al. Error-prone bypass of certain DNA lesions by the human DNA polymerase κ. Genes Dev. 14, 1589-1594 (2000). (Pubitemid 30460908)
23. Zhang, Y. et al. Error-free and error-prone lesion bypass by human DNA polymerase κ in vitro. Nucleic Acids Res. 28, 4138-4146 (2000).
24. Woodgate, R. Evolution of the two-step model for UV-mutagenesis. Mutat. Res. 485, 83-92 (2001). (Pubitemid 32112784)
25. Shachar, S. et al. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J. 28, 383-393 (2009).
26. Woodgate, R. A plethora of lesion-replicating DNA polymerases. Genes Dev. 13, 2191-2195 (1999). (Pubitemid 29426724)
27. Beard, W. A., Shock, D. D., Vande Berg, B. J. & Wilson, S. H. Efficiency of correct nucleotide insertion governs DNA polymerase fidelity. J. Biol. Chem. 277, 47393-47398 (2002). (Pubitemid 36159254)
28. Ollis, D. L., Brick, P., Hamlin, R., Xuong, N. G. & Steitz, T. A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313, 762-766 (1985). (Pubitemid 15130824)
29. Doublie, S., Tabor, S., Long, A. M., Richardson, C. C. & Ellenberger, T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391, 251-258 (1998). (Pubitemid 28099004)
30. Yang, W. & Woodgate, R. What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl Acad. Sci. USA 104, 15591-15598 (2007). (Pubitemid 350035345)
31. Boudsocq, F. et al. 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 (2004). (Pubitemid 39014753)
32. Adar, S. & Livneh, Z. Translesion DNA synthesis across non-DNA segments in cultured human cells. DNA Repair 5, 479-490 (2006).
33. Ling, H., Boudsocq, F., Woodgate, R. & Yang, W. Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell 107, 91-102 (2001). (Pubitemid 32972040)
34. Ling, H., Boudsocq, F., Woodgate, R. & Yang, W. Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts. Mol. Cell 13, 751-762 (2004). (Pubitemid 38368130)
35. Kim, S. R. et al. 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, 13792-13797 (1997).
36. Ohashi, E. et al. Fidelity and processivity of DNA synthesis by DNA polymerase κ, the product of the human DINB1 gene. J. Biol. Chem. 275, 39786-39684 (2000).
37. Bauer, J. et al. A structural gap in Dpo4 supports mutagenic bypass of a major benzo[a]pyrene dG adduct in DNA through template misalignment. Proc. Natl Acad. Sci. USA 104, 14905-14910 (2007). (Pubitemid 47619566)
38. Ogi, T., Shinkai, Y., Tanaka, K. & Ohmori, H. Polκ protects mammalian cells against the lethal and mutagenic effects of polycyclic hydrocarbons. Proc. Natl Acad. Sci. USA 99, 15548-15553 (2002). (Pubitemid 35403971)
39. Wang, Y. et al. Evidence that in xeroderma pigmentosum variant cells, which lack DNA polymerase ε, DNA polymerase ι causes the very high frequency and unique spectrum of UV-induced mutations. Cancer Res. 67, 3018-3026 (2007). (Pubitemid 46724838)
40. Ziv, O., Geacintov, N., Nakajima, S., Yasui, A. & Livneh, Z. DNA polymerase ζ cooperates with polymerases κ and ι in translesion DNA synthesis across pyrimidine photodimers in cells from XPV patients. Proc. Natl Acad. Sci. USA 29 Jun 2009 (doi:10.1073/pnas.0812548106).
41. Silverstein, T. D. et al. Structural basis for the suppression of skin cancers by DNA polymerase η. Nature 465, 1039-1043 (2010).
42. Biertimpfel, C. et al. Structure and mechanism of human DNA polymerase η. Nature 465, 1044-1048 (2010).
43. Nair, D. T., Johnson, R. E., Prakash, S., Prakash, L. & Aggarwal, A. K. Replication by human DNA polymerase ι occurs by Hoogsteen base-pairing. Nature 430, 377-380 (2004). (Pubitemid 38937748)
44. Kirouac, K. N. & Ling, H. Structural basis of error-prone replication and stalling at a thymine base by human DNA polymerase ι. EMBO J. 28, 1644-1654 (2009).
45. Vaisman, A. & Woodgate, R. Unique misinsertion specificity of polι may decrease the mutagenic potential of deaminated cytosines. EMBO J. 20, 6520-6529 (2001). (Pubitemid 33078724)
46. Kirouac, K. N. & Ling, H. Unique active site promotes error-free replication opposite an 8-oxo-guanine lesion by human DNA polymerase ι. Proc. Natl Acad. Sci. USA 108, 3210-3215 (2011).
47. Petta, T. B. et al. Human DNA polymerase ι protects cells against oxidative stress. EMBO J. 27, 2883-2895 (2008).
48. Haracska, L., Prakash, S. & Prakash, L. Yeast Rev1 protein is a G template-specific DNA polymerase. J. Biol. Chem. 277, 15546-15551 (2002). (Pubitemid 34967822)
49. Zhang, Y. et al. Response of human REV1 to different DNA damage: preferential dCMP insertion opposite the lesion. Nucleic Acids Res. 30, 1630-1638 (2002). (Pubitemid 34679738)
50. Washington, M. T. et al. Efficient and error-free replication past a minor-groove N2-guanine adduct by the sequential action of yeast Rev1 and DNA polymerase ζ. Mol. Cell. Biol. 24, 6900-6906 (2004). (Pubitemid 39014419)
51. Ross, A. L., Simpson, L. J. & Sale, J. E. Vertebrate DNA damage tolerance requires the C-terminus but not BRCT or transferase domains of REV1. Nucleic Acids Res. 33, 1280-1289 (2005). (Pubitemid 41439921)
52. Masuda, K. et al. A critical role for REV1 in regulating the induction of C:G. transitions and A:T mutations during Ig gene hypermutation. J. Immunol. 183, 1846-1850 (2009).
53. Wiltrout, M. E. & Walker, G. C. The DNA polymerase activity of Saccharomyces cerevisiae Rev1 is biologically significant. Genetics 187, 21-35 (2011).
54. Ross, A. L. & Sale, J. E. The catalytic activity of REV1 is employed during immunoglobulin gene diversification in DT40. Mol. Immunol. 43, 1587-1594 (2006).
55. Jansen, J. G. et al. Strand-biased defect in C/G. transversions in hypermutating immunoglobulin genes in Rev1-deficient mice. J. Exp. Med. 203, 319-323 (2006). (Pubitemid 43290841)
56. Kim, N., Mudrak, S. V. & Jinks-Robertson, S. The dCMP transferase activity of yeast Rev1 is biologically relevant during the bypass of endogenously generated AP sites. DNA Repair 10, 1262-1271 (2011).
57. Nair, D. T., Johnson, R. E., Prakash, L., Prakash, S. & Aggarwal, A. K. Rev1 employs a novel mechanism of DNA synthesis using a protein template. Science 309, 2219-2222 (2005). (Pubitemid 41396072)
58. Friedberg, E. C., Walker, G. C. & Siede, W. DNA Repair and Mutagenesis Ch. 14-15 (Am. Soc. for Microbiology, Washington, DC, 1995).
59. Frank, E. G., Ennis, D. G., Gonzalez, M., Levine, A. S. & Woodgate, R. Regulation of SOS mutagenesis by proteolysis. Proc. Natl Acad. Sci. USA 93, 10291-10296 (1996). (Pubitemid 26314615)
60. Nohmi, T., Battista, J. R., Dodson, L. A. & Walker, G. C. RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc. Natl Acad. Sci. USA 85, 1816-1820 (1988). (Pubitemid 24315773)
61. Waters, L. S. & Walker, G. C. The critical mutagenic translesion DNA polymerase Rev1 is highly expressed during G2/M phase rather than S phase. Proc. Natl Acad. Sci. USA 103, 8971-8976 (2006). (Pubitemid 43902518)
62. Wiltrout, M. E. & Walker, G. C. Proteasomal regulation of the mutagenic translesion DNA polymerase, Saccharomyces cerevisiae Rev1. DNA Repair 10, 169-175 (2011).
63. Bravo, R. & Macdonald-Bravo, H. Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J. Cell Biol. 105, 1549-1554 (1987). (Pubitemid 18023377)
64. Kannouche, P. et al. Domain structure, localization and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells. Genes Dev. 15, 158-172 (2001). (Pubitemid 32107662)
65. Gueranger, Q. et al. Role of DNA polymerases η, ι and ζ in UV resistance and UV-induced mutagenesis in a human cell line. DNA Repair 7, 1551-1562 (2008).
66. Naryzhny, S. N. Proliferating cell nuclear antigen: a proteomics view. Cell. Mol. Life Sci. 65, 3789-3808 (2008).
67. Moldovan, G. L., Pfander, B. & Jentsch, S. PCNA, the maestro of the replication fork. Cell 129, 665-679 (2007).
68. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. & Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141 (2002). (Pubitemid 35025438)
69. Stelter, P. & Ulrich, H. D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188-191 (2003). (Pubitemid 37150898)
70. Haracska, L., Torres-Ramos, C., Johnson, R., Prakash, S. & Prakash, L. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4267-4274 (2004). (Pubitemid 41070998)
71. Kannouche, P. L., Wing, J. & Lehmann, A. R. Interaction of human DNA polymerase η with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491-500 (2004). (Pubitemid 38648802)
72. Terai, K., Abbas, T., Jazaeri, A. A. & Dutta, A. CRL4(Cdt2) E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis. Mol. Cell 37, 143-149 (2010).
73. Zhang, S. et al. PCNA is ubiquitinated by RNF8. Cell Cycle 7, 3399-3404 (2008).
74. Davies, A. A., Huttner, D., Daigaku, Y., Chen, S. & Ulrich, H. D. Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein A. Mol. Cell 29, 625-636 (2008). (Pubitemid 351374681)
75. Bienko, M. et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310, 1821-1824 (2005). (Pubitemid 41814383)
76. Plosky, B. et al. Controlling the subcellular localization of DNA polymerases ι and η via interactions with ubiquitin. EMBO J. 25, 2847-2855 (2006). (Pubitemid 43980391)
77. Bomar, M. G. et al. Unconventional ubiquitin recognition by the ubiquitin-binding motif within the Y family DNA polymerases iota and Rev1. Mol. Cell 37, 408-417 (2010).
78. Sabbioneda, S. et al. Effect of proliferating cell nuclear antigen ubiquitination and chromatin structure on the dynamic properties of the Y-family DNA polymerases. Mol. Biol. Cell 19, 5193-5202 (2008).
79. Arakawa, H. et al. A role for PCNA ubiquitination in immunoglobulin hypermutation. PLoS Biol. 4, e366 (2006).
80. Langerak, P., Nygren, A. O., Krijger, P. H., van den Berk, P. C. & Jacobs, H. A/T mutagenesis in hypermutated immunoglobulin genes strongly depends on PCNAK164 modification. J. Exp. Med. 204, 1989-1998 (2007). (Pubitemid 47236332)
81. Sz̈ts, D., Marcus, A. P., Himoto, M., Iwai, S. & Sale, J. E. REV1 restrains DNA polymerase ζ to ensure frame fidelity during translesion synthesis of UV photoproducts in vivo. Nucleic Acids Res. 36, 6767-6780 (2008).
82. Hendel, A. et al. PCNA ubiquitination is important, but not essential for translesion DNA synthesis in mammalian cells. PLoS Genet. 7, e1002262 (2011).
83. Edmunds, C. E., Simpson, L. J. & Sale, J. E. PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol. Cell 30, 519-529 (2008). (Pubitemid 351672376)
84. Guo, C. et al. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 22, 6621-6630 (2003). (Pubitemid 38009608)
85. Ohashi, E. et al. Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9, 523-531 (2004). (Pubitemid 38877782)
86. Tissier, A. et al. Co-localization in replication foci and interaction of human Y-family members, DNA polymerase polη and REVl protein. DNA Repair 3, 1503-1514 (2004). (Pubitemid 39221748)
87. Murakumo, Y. et al. Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J. Biol. Chem. 276, 35644-35651 (2001).
88. Guo, C. et al. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 23, 265-271 (2006). (Pubitemid 44081878)
89. de Groote, F. H. et al. The Rev1 translesion synthesis polymerase has multiple distinct DNA binding modes. DNA Repair 10, 915-925 (2011).
90. Wood, A., Garg, P. & Burgers, P. M. A Ubiquitin-binding motif in the translesion DNA polymerase rev1 mediates its essential functional interaction with ubiquitinated PCNA in response to DNA damage. J. Biol. Chem. 282, 20256-20263 (2007). (Pubitemid 47099980)
91. Guo, C. et al. Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell. Biol. 26, 8892-8900 (2006). (Pubitemid 44851947)
92. Acharya, N., Haracska, L., Prakash, S. & Prakash, L. Complex formation of yeast Rev1 with DNA polymerase η. Mol. Cell. Biol. 27, 8401-8408 (2007). (Pubitemid 350234250)
93. D'Souza, S., Waters, L. & Walker, G. Novel conserved motifs in Rev1 C-terminus are required for mutagenic DNA damage tolerance. DNA Repair 7, 1455-1470 (2008).
94. Sabbioneda, S., Bortolomai, I., Giannattasio, M., Plevani, P. & Muzi-Falconi, M. Yeast Rev1 is cell cycle regulated, phosphorylated in response to DNA damage and its binding to chromosomes is dependent upon MEC1. DNA Repair 6, 121-127 (2007). (Pubitemid 46014549)
95. Bienko, M. et al. Regulation of translesion synthesis DNA polymerase ε by monoubiquitination. Mol. Cell 37, 396-407 (2010).
96. Pages, V., Santa Maria, S. R., Prakash, L. & Prakash, S. Role of DNA damage-induced replication checkpoint in promoting lesion bypass by translesion synthesis in yeast. Genes Dev. 23, 1438-1449 (2009).
97. Goehler, T., Sabbioneda, S., Green, C. M. & Lehmann, A. R. ATR-mediated phosphorylation of DNA polymerase η is needed for efficient recovery from UV damage. J. Cell Biol. 192, 219-227 (2011).
98. Jung, Y. S., Hakem, A., Hakem, R. & Chen, X. Pirh2 E3 ubiquitin ligase monoubiquitinates DNA polymerase η to suppress translesion DNA synthesis. Mol. Cell. Biol. 31, 3997-4006 (2011).
99. Huang, M., de Calignon, A., Nicolas, A. & Galibert, F. POL32, a subunit of the Saccharomyces cerevisiae DNA polymerase δ, defines a link between DNA replication and the mutagenic bypass repair pathway. Curr. Genet. 38, 178-187 (2000).
100. Kai, M. & Wang, T. S. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 17, 64-76 (2003). (Pubitemid 36062509)
101. Sabbioneda, S. et al. The 9-1-1 checkpoint clamp physically interacts with polζ and is partially required for spontaneous polζ-dependent mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280, 38657-38665 (2005). (Pubitemid 43853768)
102. Acharya, N., Johnson, R., Pages, V., Prakash, L. & Prakash, S. Yeast Rev1 protein promotes complex formation of DNA polymerase ζ with Pol32 subunit of DNA polymerase δ. Proc. Natl Acad. Sci. USA 106, 9631-9636 (2009).
103. Tissier, A. et al. Crosstalk between replicative and translesional DNA polymerases: PDIP38 interacts directly with Polε. DNA Repair 9, 922-928 (2010).
104. Huang, T. T. et al. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nature Cell Biol. 8, 341-347 (2006).
105. Goehler, T., Munoz, I. M., Rouse, J. & Blow, J. J. PTIP/Swift is required for efficient PCNA ubiquitination in response to DNA damage. DNA Repair 7, 775-787 (2008).
106. Yang, X. H., Shiotani, B., Classon, M. & Zou, L. Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev. 22, 1147-1152 (2008). (Pubitemid 351656574)
107. Terai, K., Abbas, T., Jazaeri, A. A. & Dutta, A. CRL4(Cdt2) E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis. Mol. Cell 37, 143-149 (2010).
108. Lehmann, A. R. Postreplication repair of DNA in ultraviolet-irradiated mammalian cells. J. Mol. Biol. 66, 319-337 (1972).
109. Lopes, M., Foiani, M. & Sogo, J. M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21, 15-27 (2006). (Pubitemid 43017845)
110. Daigaku, Y., Davies, A. A. & Ulrich, H. D. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 465, 951-955 (2010).
111. Karras, G. I. & Jentsch, S. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141, 255-267 (2010).
112. Diamant, N. et al. DNA damage bypass operates in the S and G2 phases of the cell cycle and exhibits differential mutagenicity. Nucleic Acids Res. 40, 170-180 (2012).
113. Di Noia, J. M. & Neuberger, M. S. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76, 1-22 (2007).
114. Sale, J. E. et al. Timing matters: error-prone gap filling and translesion synthesis in immunoglobulin gene hypermutation. Phil. Trans. R. Soc. B. 364, 595-603 (2009).
115. Zeng, X. et al. DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nature Immunol. 2, 537-541 (2001). (Pubitemid 33705856)
116. Delbos, F., Aoufouchi, S., Faili, A., Weill, J. C. & Reynaud, C. A. DNA polymerase η is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 204, 17-23 (2007). (Pubitemid 46148751)
117. Zlatanou, A. et al. The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and pol η in response to oxidative DNA damage in human cells. Mol. Cell 43, 649-662 (2011).
118. Ogi, T. et al. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell 37, 714-727 (2010).
119. Sarkies, P., Reams, C., Simpson, L. J. & Sale, J. E. Epigenetic instability due to defective replication of structured DNA. Mol. Cell 40, 703-713 (2010).
120. Sarkies, P. et al. FANCJ coordinates two pathways that maintain epigenetic stability at G-quadruplex DNA. Nucleic Acids Res. 22 Oct 2011 (doi:10.1093/nar/gkr868).
121. Betous, R. et al. Role of TLS DNA polymerases η and κ in processing naturally occurring structured DNA in human cells. Mol. Carcinog. 48, 369-378 (2009).
122. Rey, L. et al. Human DNA polymerase η is required for common fragile site stability during unperturbed DNA replication. Mol. Cell. Biol. 29, 3344-3354 (2009).
123. Kawamoto, T. et al. Dual roles for DNA polymerase η in homologous DNA recombination and translesion DNA synthesis. Mol. Cell 20, 793-799 (2005). (Pubitemid 41740700)
124. McIlwraith, M. J. et al. Human DNA polymerase η promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol. Cell 20, 783-792 (2005).
125. Bomar, M. G., Pai, M. T., Tzeng, S. R., Li, S. S. & Zhou, P. Structure of the ubiquitin-binding zinc finger domain of human DNA Y-polymerase η. EMBO Rep. 8, 247-251 (2007). (Pubitemid 46344589)
126. Burschowsky, D. et al. Structural analysis of the conserved ubiquitin-binding motifs (UBMs) of the translesion polymerase ι in complex with ubiquitin. J. Biol. Chem. 286, 1364-1373 (2011).
127. Huang, B., Bates, M. & Zhuang, X. Super-resolution fluorescence microscopy. Ann. Rev. Biochem. 78, 993-1016 (2009).
128. Luedeke, M. et al. Predisposition for TMPRSS2-ERG fusion in prostate cancer by variants in DNA repair genes. Cancer Epidemiol. Biomarkers Prev. 18, 3030-3035 (2009).
129. Doles, J. et al. Suppression of Rev3, the catalytic subunit of Polζ, sensitizes drug-resistant lung tumors to chemotherapy. Proc. Natl Acad. Sci. USA 107, 20786-20791 (2010).
130. Xie, K., Doles, J., Hemann, M. T. & Walker, G. C. Error-prone translesion synthesis mediates acquired chemoresistance. Proc. Natl Acad. Sci. USA 107, 20792-20797 (2010).
131. Bridges, B. A. & Woodgate, R. The two-step model of bacterial UV mutagenesis. Mutat. Res. 150, 133-139 (1985). (Pubitemid 15226341)
132. Wang, M. et al. Insights into base selectivity from the 1.8 ? resolution structure of an RB69 DNA polymerase ternary complex. Biochemistry 50, 581-590 (2011).
133. Jiang, Q., Karata, K., Woodgate, R., Cox, M. M. & Goodman, M. F. The active form of DNA polymerase V is UmuD′2C-RecA-ATP. Nature 460, 359-363 (2009).