Translesion and Repair DNA Polymerases: Diverse Structure and Mechanism

Literature Cited

1. 1.  Bessman MJ, Kornberg A, Lehman IR, Simms ES 1956. Enzymic synthesis of deoxyribonucleic acid. Biochim. Biophys. Acta 21:197–98
   [Google Scholar]
2. 2.  Englund PT, Deutscher MP, Jovin TM, Kelly RB, Cozzarelli NR, Kornberg A 1968. Structural and functional properties of Escherichia coli DNA polymerase. Cold Spring Harb. Symp. Quant. Biol. 33:1–9
   [Google Scholar]
3. 3.  Ollis DL, Brick P, Hamlin R, Xuong NG, Steitz TA 1985. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313:762–66
   [Google Scholar]
4. 4.  Lindahl T. 2001. Keynote: past, present, and future aspects of base excision repair. Prog. Nucl. Acid Res. Mol. Biol. 68:xvii–xxx
   [Google Scholar]
5. 5.  Setlow RB. 1966. Cyclobutane-type pyrimidine dimers in polynucleotides. Science 153:379–86
   [Google Scholar]
6. 6.  Witkin EM. 1966. Mutation and the repair of radiation damage in bacteria. Radiat. Res. Suppl 6:30–53
   [Google Scholar]
7. 7.  Boysen G, Hecht SS 2003. Analysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutat. Res. 543:17–30
   [Google Scholar]
8. 8.  Dasari S, Tchounwou PB 2014. Cisplatin in cancer therapy: molecular mechanisms of action. Eur. J. Pharmacol. 740:364–78
   [Google Scholar]
9. 9.  Yang W. 2008. Structure and mechanism for DNA lesion recognition. Cell Res 18:184–97
   [Google Scholar]
10. 10.  Lindahl T, Karran P, Wood RD 1997. DNA excision repair pathways. Curr. Opin. Genet. Dev. 7:158–69
    [Google Scholar]
11. 11.  Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F et al. 2001. The Y-family of DNA polymerases. Mol. Cell 8:7–8
    [Google Scholar]
12. 12.  Yang W, Woodgate R 2007. What a difference a decade makes: insights into translesion DNA synthesis. PNAS 104:15591–98
    [Google Scholar]
13. 13.  Vaisman A, Woodgate R 2017. Translesion DNA polymerases in eukaryotes: What makes them tick?. Crit. Rev. Biochem. Mol. Biol. 52:274–303
    [Google Scholar]
14. 14.  Franco S, Alt FW, Manis JP 2006. Pathways that suppress programmed DNA breaks from progressing to chromosomal breaks and translocations. DNA Repair 5:1030–41
    [Google Scholar]
15. 15.  Ceccaldi R, Rondinelli B, D'Andrea AD 2016. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol 26:52–64
    [Google Scholar]
16. 16.  Lange SS, Tomida J, Boulware KS, Bhetawal S, Wood RD 2016. The polymerase activity of mammalian DNA Pol ζ is specifically required for cell and embryonic viability. PLOS Genet 12:e1005759
    [Google Scholar]
17. 17.  van Schendel R, van Heteren J, Welten R, Tijsterman M 2016. Genomic scars generated by polymerase Theta reveal the versatile mechanism of alternative end-joining. PLOS Genet 12:e1006368
    [Google Scholar]
18. 18.  Wyatt DW, Feng W, Conlin MP, Yousefzadeh MJ, Roberts SA et al. 2016. Essential roles for polymerase θ-mediated end joining in the repair of chromosome breaks. Mol. Cell 63:662–73
    [Google Scholar]
19. 19.  Dudley DD, Chaudhuri J, Bassing CH, Alt FW 2005. Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv. Immunol. 86:43–112
    [Google Scholar]
20. 20.  Zeng X, Winter DB, Kasmer C, Kraemer KH, Lehmann AR, Gearhart PJ 2001. DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immunol. 2:537–41
    [Google Scholar]
21. 21.  Wu WJ, Yang W, Tsai MD 2017. How DNA polymerases catalyse replication and repair with contrasting fidelity. Nat. Rev. Chem. 1:0068
    [Google Scholar]
22. 22.  Wang F, Yang W 2009. Structural insight into translesion synthesis by DNA Pol II. Cell 139:1279–89
    [Google Scholar]
23. 23.  Lee YS, Gao Y, Yang W 2015. How a homolog of high-fidelity replicases conducts mutagenic DNA synthesis. Nat. Struct. Mol. Biol. 22:298–303
    [Google Scholar]
24. 24.  Hübscher U, Spadari S, Villani G, Maga G 2010. DNA Polymerases: Discovery, Characterization and Functions in Cellular DNA Transactions Singapore: World Scientific
25. 25.  Marians KJ. 2018. Lesion bypass and the reactivation of stalled replication forks. Annu. Rev. Biochem. 87:217–38
    [Google Scholar]
26. 26.  Oestergaard VH, Lisby M 2017. Transcription-replication conflicts at chromosomal fragile sites-consequences in M phase and beyond. Chromosoma 126:213–22
    [Google Scholar]
27. 27.  Williams JS, Lujan SA, Kunkel TA 2016. Processing ribonucleotides incorporated during eukaryotic DNA replication. Nat. Rev. Mol. Cell Biol. 17:350–63
    [Google Scholar]
28. 28.  Ito J, Braithwaite DK 1991. Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res 19:4045–57
    [Google Scholar]
29. 29.  Filee J, Forterre P, Sen-Lin T, Laurent J 2002. Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol. 54:763–73
    [Google Scholar]
30. 30.  Nakamura TM, Cech TR 1998. Reversing time: origin of telomerase. Cell 92:587–90
    [Google Scholar]
31. 31.  Rudd SG, Bianchi J, Doherty AJ 2014. PrimPol—A new polymerase on the block. Mol. Cell. Oncol. 1:e960754
    [Google Scholar]
32. 32.  Reha-Krantz LJ. 2010. DNA polymerase proofreading: Multiple roles maintain genome stability. Biochim. Biophys. Acta 1804:1049–63
    [Google Scholar]
33. 33.  Bruck I, Goodman MF, O'Donnell M 2003. The essential C family DnaE polymerase is error-prone and efficient at lesion bypass. J. Biol. Chem. 278:44361–68
    [Google Scholar]
34. 34.  Wood RD, Doublié S 2016. DNA polymerase θ (POLQ), double-strand break repair, and cancer. DNA Repair 44:22–32
    [Google Scholar]
35. 35.  Takata KI, Reh S, Yousefzadeh MJ, Zelazowski MJ, Bhetawal S et al. 2017. Analysis of DNA polymerase ν function in meiotic recombination, immunoglobulin class-switching, and DNA damage tolerance. PLOS Genet 13:e1006818
    [Google Scholar]
36. 36.  Moon AF, Garcia-Diaz M, Batra VK, Beard WA, Bebenek K et al. 2007. The X family portrait: structural insights into biological functions of X family polymerases. DNA Repair 6:1709–25
    [Google Scholar]
37. 37.  Nick McElhinny SA, Havener JM, Garcia-Diaz M, Juárez R, Bebenek K et al. 2005. A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining. Mol. Cell 19:357–66
    [Google Scholar]
38. 38.  Yang W. 2014. An overview of Y-family DNA polymerases and a case study of human DNA polymerase η. Biochemistry 53:2793–803
    [Google Scholar]
39. 39.  Blackburn EH, Greider CW, Szostak JW 2006. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 12:1133–38
    [Google Scholar]
40. 40.  Timinskas K, Balvociute M, Timinskas A, Venclovas C 2014. Comprehensive analysis of DNA polymerase III α subunits and their homologs in bacterial genomes. Nucleic Acids Res 42:1393–413
    [Google Scholar]
41. 41.  Matsui I, Matsui E, Yamasaki K, Yokoyama H 2013. Domain structures and inter-domain interactions defining the holoenzyme architecture of archaeal D-family DNA polymerase. Life 3:375–85
    [Google Scholar]
42. 42.  Yin YW. 2011. Structural insight on processivity, human disease and antiviral drug toxicity. Curr. Opin. Struct. Biol. 21:83–91
    [Google Scholar]
43. 43.  Klinge S, Nunez-Ramirez R, Llorca O, Pellegrini L 2009. 3D architecture of DNA Pol α reveals the functional core of multi-subunit replicative polymerases. EMBO J 28:1978–87
    [Google Scholar]
44. 44.  Baranovskiy AG, Lada AG, Siebler HM, Zhang Y, Pavlov YI, Tahirov TH 2012. DNA polymerase δ and ζ switch by sharing accessory subunits of DNA polymerase δ. J. Biol. Chem. 287:17281–87
    [Google Scholar]
45. 45.  Makarova AV, Stodola JL, Burgers PM 2012. A four-subunit DNA polymerase ζ complex containing Pol δ accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res 40:11618–26
    [Google Scholar]
46. 46.  Johnson RE, Prakash L, Prakash S 2012. Pol31 and Pol32 subunits of yeast DNA polymerase δ are also essential subunits of DNA polymerase ζ. PNAS 109:12455–60
    [Google Scholar]
47. 47.  Lee YS, Gregory MT, Yang W 2014. Human Pol ζ purified with accessory subunits is active in translesion DNA synthesis and complements Pol η in cisplatin bypass. PNAS 111:2954–59
    [Google Scholar]
48. 48.  Yan J, Beattie TR, Rojas AL, Schermerhorn K, Gristwood T et al. 2017. Identification and characterization of a heterotrimeric archaeal DNA polymerase holoenzyme. Nat. Commun. 8:15075
    [Google Scholar]
49. 49.  Jiang J, Chan H, Cash DD, Miracco EJ, Ogorzalek Loo RR et al. 2015. Structure of Tetrahymena telomerase reveals previously unknown subunits, functions, and interactions. Science 350:aab4070
    [Google Scholar]
50. 50.  Yeeles JT, Janska A, Early A, Diffley JF 2017. How the eukaryotic replisome achieves rapid and efficient DNA replication. Mol. Cell 65:105–16
    [Google Scholar]
51. 51.  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
    [Google Scholar]
52. 52.  Rechkoblit O, Gupta YK, Malik R, Rajashankar KR, Johnson RE et al. 2016. Structure and mechanism of human PrimPol, a DNA polymerase with primase activity. Sci. Adv. 2:e1601317
    [Google Scholar]
53. 53.  Li GM. 2008. Mechanisms and functions of DNA mismatch repair. Cell Res 18:85–98
    [Google Scholar]
54. 54.  Patel SS, Wong I, Johnson KA 1991. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30:511–25
    [Google Scholar]
55. 55.  Kati WM, Johnson KA, Jerva LF, Anderson KS 1992. Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267:25988–97
    [Google Scholar]
56. 56.  Fiala KA, Suo Z 2004. Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43:2116–25
    [Google Scholar]
57. 57.  Shah AM, Li SX, Anderson KS, Sweasy JB 2001. Y265H mutator mutant of DNA polymerase β: Proper geometric alignment is critical for fidelity. J. Biol. Chem. 276:10824–31
    [Google Scholar]
58. 58.  Showalter AK, Tsai MD 2002. A reexamination of the nucleotide incorporation fidelity of DNA polymerases. Biochemistry 41:10571–76
    [Google Scholar]
59. 59.  Rothwell PJ, Mitaksov V, Waksman G 2005. Motions of the fingers subdomain of Klentaq1 are fast and not rate limiting: implications for the molecular basis of fidelity in DNA polymerases. Mol. Cell 19:345–55
    [Google Scholar]
60. 60.  Zhang H, Cao W, Zakharova E, Konigsberg W, De La Cruz EM 2007. Fluorescence of 2-aminopurine reveals rapid conformational changes in the RB69 DNA polymerase-primer/template complexes upon binding and incorporation of matched deoxynucleoside triphosphates. Nucleic Acids Res 35:6052–62
    [Google Scholar]
61. 61.  Wong I, Patel SS, Johnson KA 1991. An induced-fit kinetic mechanism for DNA replication fidelity: direct measurement by single-turnover kinetics. Biochemistry 30:526–37
    [Google Scholar]
62. 62.  Pelletier H, Sawaya MR, Kumar A, Wilson SH, Kraut J 1994. Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. Science 264:1891–903
    [Google Scholar]
63. 63.  Doublie S, Sawaya MR, Ellenberger T 1999. An open and closed case for all polymerases. Structure 7:R31–35
    [Google Scholar]
64. 64.  Gao Y, Yang W 2016. Capture of a third Mg²⁺ is essential for catalyzing DNA synthesis. Science 352:1334–37
    [Google Scholar]
65. 65.  Fernandez-Leiro R, Conrad J, Yang JC, Freund SM, Scheres SH, Lamers MH 2017. Self-correcting mismatches during high-fidelity DNA replication. Nat. Struct. Mol. Biol. 24:140–43
    [Google Scholar]
66. 66.  Vandewiele D, Borden A, O'Grady PI, Woodgate R, Lawrence CW 1998. Efficient translesion replication in the absence of Escherichia coli Umu proteins and 3′–5′ exonuclease proofreading function. PNAS 95:15519–24
    [Google Scholar]
67. 67.  Johnson RE, Washington MT, Haracska L, Prakash S, Prakash L 2000. Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406:1015–19
    [Google Scholar]
68. 68.  Livneh Z, Ziv O, Shachar S 2010. Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 9:729–35
    [Google Scholar]
69. 69.  Yang W, Lee YS 2015. A DNA-hairpin model for repeat-addition processivity in telomere synthesis. Nat. Struct. Mol. Biol. 22:844–47
    [Google Scholar]
70. 70.  Fiala KA, Suo Z 2004. Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43:2106–15
    [Google Scholar]
71. 71.  Matsuda T, Bebenek K, Masutani C, Rogozin IB, Hanaoka F, Kunkel TA 2001. Error rate and specificity of human and murine DNA polymerase η. J. Mol. Biol. 312:335–46
    [Google Scholar]
72. 72.  Beard WA, Shock DD, Vande Berg BJ, Wilson SH 2002. Efficiency of correct nucleotide insertion governs DNA polymerase fidelity. J. Biol. Chem. 277:47393–98
    [Google Scholar]
73. 73.  Biertumpfel C, Zhao Y, Kondo Y, Ramon-Maiques S, Gregory M et al. 2010. Structure and mechanism of human DNA polymerase η. Nature 465:1044–48
    [Google Scholar]
74. 74.  Wilson RC, Pata JD 2008. Structural insights into the generation of single-base deletions by the Y family DNA polymerase Dbh. Mol. Cell 29:767–79
    [Google Scholar]
75. 75.  Lone S, Townson SA, Uljon SN, Johnson RE, Brahma A et al. 2007. Human DNA polymerase κ encircles DNA: implications for mismatch extension and lesion bypass. Mol. Cell 25:601–14
    [Google Scholar]
76. 76.  Bauer J, Xing G, Yagi H, Sayer JM, Jerina DM, Ling H 2007. A structural gap in Dpo4 supports mutagenic bypass of a major benzo[α]pyrene dG adduct in DNA through template misalignment. PNAS 104:14905–10
    [Google Scholar]
77. 77.  Liu Y, Yang Y, Tang T-S, Zhang H, Wang Z et al. 2014. Variants of mouse DNA polymerase κ reveal a mechanism of efficient and accurate translesion synthesis past a benzo[α]pyrene dG adduct. PNAS 111:1789–94
    [Google Scholar]
78. 78.  Burgers PMJ, Kunkel TA 2017. Eukaryotic DNA replication fork. Annu. Rev. Biochem. 86:417–38
    [Google Scholar]
79. 79.  Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M et al. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399:700–4
    [Google Scholar]
80. 80.  Johnson RE, Kondratick CM, Prakash S, Prakash L 1999. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263–65
    [Google Scholar]
81. 81.  McCulloch SD, Kokoska RJ, Masutani C, Iwai S, Hanaoka F, Kunkel TA 2004. Preferential cis-syn thymine dimer bypass by DNA polymerase η occurs with biased fidelity. Nature 428:97–100
    [Google Scholar]
82. 82.  Cadet J, Sage E, Douki T 2005. Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res. 571:3–17
    [Google Scholar]
83. 83.  Cleaver JE. 1972. Xeroderma pigmentosum: variants with normal DNA repair and normal sensitivity to ultraviolet light. J. Investig. Dermatol. 58:124–28
    [Google Scholar]
84. 84.  Lehmann AR, Kirk-Bell S, Arlett CF, Paterson MC, Lohman PH et al. 1975. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. PNAS 72:219–23
    [Google Scholar]
85. 85.  Zhao Y, Gregory MT, Biertumpfel C, Hua YJ, Hanaoka F, Yang W 2013. Mechanism of somatic hypermutation at the WA motif by human DNA polymerase η. PNAS 110:8146–51
    [Google Scholar]
86. 86.  Masutani C, Kusumoto R, Iwai S, Hanaoka F 2000. Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J 19:3100–9
    [Google Scholar]
87. 87.  Zhao Y, Biertumpfel C, Gregory MT, Hua YJ, Hanaoka F, Yang W 2012. Structural basis of human DNA polymerase η-mediated chemoresistance to cisplatin. PNAS 109:7269–74
    [Google Scholar]
88. 88.  Shachar S, Ziv O, Avkin S, Adar S, Wittschieben J et al. 2009. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J 28:383–93
    [Google Scholar]
89. 89.  McDonald JP, Frank EG, Plosky BS, Rogozin IB, Masutani C et al. 2003. 129-derived strains of mice are deficient in DNA polymerase ι and have normal immunoglobulin hypermutation. J. Exp. Med. 198:635–43
    [Google Scholar]
90. 90.  Ohkumo T, Kondo Y, Yokoi M, Tsukamoto T, Yamada A et al. 2006. UV-B radiation induces epithelial tumors in mice lacking DNA polymerase η and mesenchymal tumors in mice deficient for DNA polymerase ι. Mol. Cell. Biol. 26:7696–706
    [Google Scholar]
91. 91.  Nair DT, Johnson RE, Prakash S, Prakash L, Aggarwal AK 2004. Replication by human DNA polymerase-ι occurs by Hoogsteen base-pairing. Nature 430:377–80
    [Google Scholar]
92. 92.  Kirouac KN, Ling H 2009. Structural basis of error-prone replication and stalling at a thymine base by human DNA polymerase ι. EMBO J 28:1644–54
    [Google Scholar]
93. 93.  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 14:749–55
    [Google Scholar]
94. 94.  Jain R, Choudhury JR, Buku A, Johnson RE, Prakash L et al. 2017. Mechanism of error-free DNA synthesis across N1-methyl-deoxyadenosine by human DNA polymerase-ι. Sci. Rep. 7:43904
    [Google Scholar]
95. 95.  Kirouac KN, Ling H 2011. Unique active site promotes error-free replication opposite an 8-oxo-guanine lesion by human DNA polymerase iota. PNAS 108:3210–15
    [Google Scholar]
96. 96.  Suzuki N, Ohashi E, Kolbanovskiy A, Geacintov NE, Grollman AP et al. 2002. Translesion synthesis by human DNA polymerase κ on a DNA template containing a single stereoisomer of dG-(+)- or dG-(−)-anti-N²-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene). Biochemistry 41:6100–6
    [Google Scholar]
97. 97.  Rechkoblit O, Zhang Y, Guo D, Wang Z, Amin S et al. 2002. trans-Lesion synthesis past bulky benzo[a]pyrene diol epoxide N²-dG and N⁶-dA lesions catalyzed by DNA bypass polymerases. J. Biol. Chem. 277:30488–94
    [Google Scholar]
98. 98.  Ogi T, Limsirichaikul S, Overmeer RM, Volker M, Takenaka K et al. 2010. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell 37:714–27
    [Google Scholar]
99. 99.  Singer WD, Osimiri LC, Friedberg EC 2013. Increased dietary cholesterol promotes enhanced mutagenesis in DNA polymerase kappa-deficient mice. DNA Repair 12:817–23
    [Google Scholar]
100. 100.  Stancel JN, McDaniel LD, Velasco S, Richardson J, Guo C, Friedberg EC 2009. Polk mutant mice have a spontaneous mutator phenotype. DNA Repair 8:1355–62
     [Google Scholar]
101. 101.  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 439:225–28
     [Google Scholar]
102. 102.  Jha V, Bian C, Xing G, Ling H 2016. Structure and mechanism of error-free replication past the major benzo[a]pyrene adduct by human DNA polymerase κ. Nucleic Acids Res 44:4957–67
     [Google Scholar]
103. 103.  Jha V, Ling H 2017. Structural basis of accurate replication beyond a bulky major benzo[a]pyrene adduct by human DNA polymerase kappa. DNA Repair 49:43–50
     [Google Scholar]
104. 104.  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 28:1058–70
     [Google Scholar]
105. 105.  Nelson JR, Lawrence CW, Hinkle DC 1996. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382:729–31
     [Google Scholar]
106. 106.  Larimer FW, Perry JR, Hardigree AA 1989. The REV1 gene of Saccharomyces cerevisiae: isolation, sequence, and functional analysis. J. Bacteriol. 171:230–37
     [Google Scholar]
107. 107.  Kim N, Mudrak SV, Jinks-Robertson S 2011. The dCMP transferase activity of yeast Rev1 is biologically relevant during the bypass of endogenously generated AP sites. DNA Repair 10:1262–71
     [Google Scholar]
108. 108.  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. 203:319–23
     [Google Scholar]
109. 109.  Lawrence CW, Christensen RB 1978. Ultraviolet-induced reversion of cyc1 alleles in radiation-sensitive strains of yeast. I. rev1 mutant strains. J. Mol. Biol. 122:1–21
     [Google Scholar]
110. 110.  Nair DT, Johnson RE, Prakash L, Prakash S, Aggarwal AK 2005. Rev1 employs a novel mechanism of DNA synthesis using a protein template. Science 309:2219–22
     [Google Scholar]
111. 111.  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
     [Google Scholar]
112. 112.  Nelson JR, Lawrence CW, Hinkle DC 1996. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272:1646–49
     [Google Scholar]
113. 113.  Gibbs PE, McGregor WG, Maher VM, Nisson P, Lawrence CW 1998. A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase ζ. PNAS 95:6876–80
     [Google Scholar]
114. 114.  Gan GN, Wittschieben JP, Wittschieben BO, Wood RD 2008. DNA polymerase zeta (pol ζ) in higher eukaryotes. Cell Res 18:174–83
     [Google Scholar]
115. 115.  Bonner CA, Hays S, McEntee K, Goodman MF 1990. DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli. PNAS 87:7663–67
     [Google Scholar]
116. 116.  Iwasaki H, Ishino Y, Toh H, Nakata A, Shinagawa H 1991. Escherichia coli DNA polymerase II is homologous to alpha-like DNA polymerases. Mol. Gen. Genet. 226:24–33
     [Google Scholar]
117. 117.  Yeiser B, Pepper ED, Goodman MF, Finkel SE 2002. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. PNAS 99:8737–41
     [Google Scholar]
118. 118.  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 19:6259–65
     [Google Scholar]
119. 119.  Becherel OJ, Fuchs RP 2001. Mechanism of DNA polymerase II-mediated frameshift mutagenesis. PNAS 98:8566–71
     [Google Scholar]
120. 120.  Beagan K, Armstrong RL, Witsell A, Roy U, Renedo N et al. 2017. Drosophila DNA polymerase theta utilizes both helicase-like and polymerase domains during microhomology-mediated end joining and interstrand crosslink repair. PLOS Genet 13:e1006813
     [Google Scholar]
121. 121.  Shima N, Hartford SA, Duffy T, Wilson LA, Schimenti KJ, Schimenti JC 2003. Phenotype-based identification of mouse chromosome instability mutants. Genetics 163:1031–40
     [Google Scholar]
122. 122.  Yousefzadeh MJ, Wyatt DW, Takata K, Mu Y, Hensley SC et al. 2014. Mechanism of suppression of chromosomal instability by DNA polymerase POLQ. PLOS Genet 10:e1004654
     [Google Scholar]
123. 123.  Chan SH, Yu AM, McVey M 2010. Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLOS Genet 6:e1001005
     [Google Scholar]
124. 124.  Mateos-Gomez PA, Gong F, Nair N, Miller KM, Lazzerini-Denchi E, Sfeir A 2015. Mammalian polymerase θ promotes alternative NHEJ and suppresses recombination. Nature 518:254–57
     [Google Scholar]
125. 125.  Ceccaldi R, Liu JC, Amunugama R, Hajdu I, Primack B et al. 2015. Homologous-recombination-deficient tumours are dependent on Polθ-mediated repair. Nature 518:258–62
     [Google Scholar]
126. 126.  Zelensky AN, Schimmel J, Kool H, Kanaar R, Tijsterman M 2017. Inactivation of Pol θ and C-NHEJ eliminates off-target integration of exogenous DNA. Nat. Commun. 8:66
     [Google Scholar]
127. 127.  Saito S, Maeda R, Adachi N 2017. Dual loss of human POLQ and LIG4 abolishes random integration. Nat. Commun. 8:16112
     [Google Scholar]
128. 128.  Zahn KE, Averill AM, Aller P, Wood RD, Doublie S 2015. Human DNA polymerase θ grasps the primer terminus to mediate DNA repair. Nat. Struct. Mol. Biol. 22:304–11
     [Google Scholar]
129. 129.  Bollum FJ, Groeniger E, Yoneda M 1964. Polydeoxyadenylic acid. PNAS 51:853–59
     [Google Scholar]
130. 130.  Foa R, Casorati G, Giubellino MC, Basso G, Schiro R et al. 1987. Rearrangements of immunoglobulin and T cell receptor beta and gamma genes are associated with terminal deoxynucleotidyl transferase expression in acute myeloid leukemia. J. Exp. Med. 165:879–90
     [Google Scholar]
131. 131.  Tanabe K, Bohn EW, Wilson SH 1979. Steady-state kinetics of mouse DNA polymerase beta. Biochemistry 18:3401–6
     [Google Scholar]
132. 132.  Uchiyama Y, Takeuchi R, Kodera H, Sakaguchi K 2009. Distribution and roles of X-family DNA polymerases in eukaryotes. Biochimie 91:165–70
     [Google Scholar]
133. 133.  Lecointe F, Shevelev IV, Bailone A, Sommer S, Hübscher U 2004. Involvement of an X family DNA polymerase in double-stranded break repair in the radioresistant organism Deinococcus radiodurans. Mol. Microbiol. 53:1721–30
     [Google Scholar]
134. 134.  Leulliot N, Cladiere L, Lecointe F, Durand D, Hübscher U, van Tilbeurgh H 2009. The family X DNA polymerase from Deinococcus radiodurans adopts a non-standard extended conformation. J. Biol. Chem. 284:11992–99
     [Google Scholar]
135. 135.  Beard WA, Wilson SH 2000. Structural design of a eukaryotic DNA repair polymerase: DNA polymerase β. Mutat. Res. 460:231–44
     [Google Scholar]
136. 136.  Ruiz JF, Dominguez O, Lain de Lera T, Garcia-Diaz M, Bernad A, Blanco L 2001. DNA polymerase mu, a candidate hypermutase?. Philos. Trans. R. Soc. B 356:99–109
     [Google Scholar]
137. 137.  Bertocci B, De Smet A, Berek C, Weill JC, Reynaud CA 2003. Immunoglobulin κ light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu. Immunity 19:203–11
     [Google Scholar]
138. 138.  Bebenek K, Pedersen LC, Kunkel TA 2014. Structure-function studies of DNA polymerase λ. Biochemistry 53:2781–92
     [Google Scholar]
139. 139.  Moon AF, Pryor JM, Ramsden DA, Kunkel TA, Bebenek K, Pedersen LC 2014. Sustained active site rigidity during synthesis by human DNA polymerase μ. Nat. Struct. Mol. Biol. 21:253–60
     [Google Scholar]
140. 140.  Gouge J, Rosario S, Romain F, Poitevin F, Beguin P, Delarue M 2015. Structural basis for a novel mechanism of DNA bridging and alignment in eukaryotic DSB DNA repair. EMBO J 34:1126–42
     [Google Scholar]
141. 141.  Pryor JM, Waters CA, Aza A, Asagoshi K, Strom C et al. 2015. Essential role for polymerase specialization in cellular nonhomologous end joining. PNAS 112:E4537–45
     [Google Scholar]
142. 142.  Moon AF, Gosavi RA, Kunkel TA, Pedersen LC, Bebenek K 2015. Creative template-dependent synthesis by human polymerase mu. PNAS 112:E4530–36
     [Google Scholar]
143. 143.  Boule JB, Rougeon F, Papanicolaou C 2001. Terminal deoxynucleotidyl transferase indiscriminately incorporates ribonucleotides and deoxyribonucleotides. J. Biol. Chem. 276:31388–93
     [Google Scholar]
144. 144.  Nick McElhinny SA, Ramsden DA 2003. Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol. Cell. Biol. 23:2309–15
     [Google Scholar]
145. 145.  Ruiz JF, Juarez R, Garcia-Diaz M, Terrados G, Picher AJ et al. 2003. Lack of sugar discrimination by human Pol μ requires a single glycine residue. Nucleic Acids Res 31:4441–49
     [Google Scholar]
146. 146.  Masuda Y, Kanao R, Kaji K, Ohmori H, Hanaoka F, Masutani C 2015. Different types of interaction between PCNA and PIP boxes contribute to distinct cellular functions of Y-family DNA polymerases. Nucleic Acids Res 43:7898–910
     [Google Scholar]
147. 147.  Choe KN, Moldovan GL 2017. Forging ahead through darkness: PCNA, still the principal conductor at the replication fork. Mol. Cell 65:380–92
     [Google Scholar]
148. 148.  Hedglin M, Pandey B, Benkovic SJ 2016. Characterization of human translesion DNA synthesis across a UV-induced DNA lesion. eLife 5:e19788
     [Google Scholar]
149. 149.  Wimmer U, Ferrari E, Hunziker P, Hübscher U 2008. Control of DNA polymerase λ stability by phosphorylation and ubiquitination during the cell cycle. EMBO Rep 9:1027–33
     [Google Scholar]