Thymidine glycol: The effect on DNA molecular structure and enzymatic processing

Biochimie

Volumn 95, Issue 2, 2013, Pages 134-147

  Dolinnaya, Nina G ^a   Kubareva, Elena A ^a   Romanova, Elena A ^a   Trikin, Roman M ^a   Oretskaya, Tatiana S ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Alteration in DNA structure; Oxidative DNA damage; Tandem (clustered) lesions; Thymine glycol repair; Translesion synthesis

Indexed keywords

5,6 DIHYDRO 5,6 DIHYDROXYTHYMIDINE; DNA POLYMERASE; DOUBLE STRANDED DNA;

CHIRALITY; CRYSTAL STRUCTURE; DNA DAMAGE; DNA HELIX; DNA REPAIR; DNA STRUCTURE; DNA TEMPLATE; DOWN REGULATION; EPIMERIZATION; EXCISION REPAIR; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MODEL; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; REVIEW; STEREOCHEMISTRY; STEREOISOMERISM;

BASE PAIRING; DNA; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; ENDONUCLEASES; ESCHERICHIA COLI; HUMANS; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES; PROTEIN BIOSYNTHESIS; STEREOISOMERISM; THYMIDINE; TRANSCRIPTION, GENETIC;

EID: 84872786815     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.09.008     Document Type: Review

References (129)

1. R. Adelman, R.L. Saul, and B.N. Ames Oxidative damage to DNA: relation to species metabolic rate and life span Proc. Natl. Acad. Sci. U.S.A. 85 1988 2706 2708
2. K. Frenkel, M.S. Goldstein, and G.W. Teebor Identification of the cis-thymine glycol moiety in chemically oxidized and gamma-irradiated deoxyribonucleic acid by high-pressure liquid chromatography analysis Biochemistry 20 1981 7566 7571
3. G. Teebor, A. Cummings, K. Frenkel, A. Shaw, L. Voituriez, and J. Cadet Quantitative measurement of the diastereoisomers of cis thymidine glycol in gamma-irradiated DNA Free Radic. Res. Commun. 2 1987 303 309
4. S.S. Wallace Biological consequences of free radical-damaged DNA bases Free Radic. Biol. Med. 33 2002 1 14
5. S. Zuo, R.J. Boorstein, and G.W. Teebor Oxidative damage to 5-methylcytosine in DNA Nucleic Acids Res. 23 1995 3239 3243
6. G.P. Pfeifer p53 mutational spectra and the role of methylated CpG sequences Mutat. Res. 450 2000 155 166
7. R. Cathcart, E. Schwiers, R.L. Saul, and B.N. Ames Thymine glycol and thymidine glycol in human and rat urine: a possible assay for oxidative DNA damage Proc. Natl. Acad. Sci. U.S.A. 81 1984 5633 5637
8. M.J. Lustig, J. Cadet, R.J. Boorstein, and G.W. Teebor Synthesis of the diastereomers of thymidine glycol, determination of concentrations and rates of interconversion of their cistrans epimers at equilibrium and demonstration of differential alkali lability within DNA Nucleic Acids Res. 20 1992 4839 4845
9. A.K. Basu, E.L. Loechler, S.A. Leadon, and J.M. Essigmann Genetic effects of thymine glycol: site-specific mutagenesis and molecular modeling studies Proc. Natl. Acad. Sci. U.S.A. 86 1989 7677 7681
10. H. Ide, Y.W. Kow, and S.S. Wallace Thymine glycols and urea residues in M13 DNA constitute replicative blocks in vitro Nucleic Acids Res. 13 1985 8035 8052
11. J.M. Clark, and G.P. Beardsley Functional effects of cis-thymine glycol lesions on DNA synthesis in vitro Biochemistry 26 1987 5398 5403
12. S. Rabkin, and B. Strauss A role for DNA polymerase in the specificity of nucleotide incorporation opposite N-acetyl-2-aminofluorene adducts J. Mol. Biol. 178 1984 569 594
13. Z. Hatahet, A.A. Purmal, and S.S. Wallace A novel method for site specific introduction of single model oxidative DNA lesion into oligodeoxyribonucleotides Nucleic Acids Res. 21 1993 1563 1568
14. K. Frenkel, M.S. Goldstein, N.J. Duker, and G.W. Teebor Identification of the cis-thymine glycol moiety in oxidized deoxyribonucleic acid Biochemistry 20 1981 750 754
15. R.C. Hayes, and J.E. LeClerc Sequence dependence for bypass of thymine glycols in DNA by DNA polymerase I Nucleic Acids Res. 14 1986 1045 1061
16. J.M. Clark, and G.P. Beardsley Thymine glycol lesions terminate chain elongation by DNA polymerase I in vitro Nucleic Acids Res. 14 1986 737 749
17. G.L. Dianov, T. Thybo, I.I. Dianova, L.J. Lipinski, and V.A. Bohr Single nucleotide patch base excision repair is the major pathway for removal of thymine glycol from DNA in human cell extracts J. Biol. Chem. 275 2000 11809 11813
18. J.Y. Kao, I. Goljer, T.A. Phan, and P.H. Bolton Characterization of the effects of a thymine glycol residue on the structure, dynamics and stability of duplex DNA by NMR J. Biol. Chem. 268 1993 17787 17793
19. H.C. Kung, and P.H. Bolton Structure of a duplex DNA containing a thymine glycol residue in solution J. Biol. Chem. 272 1997 9227 9236
20. H. Ide, R.J. Melamede, and S.S. Wallace Synthesis of dihydrothymidine and thymidine glycol 5′-triphosphates and their ability to serve as substrates for Escherichia coli DNA polymerase I Biochemistry 26 1987 964 969
21. H. Ide, and S.S. Wallace Dihydrothymidine and thymidine glycol triphosphates as substrates for DNA polymerases: differential recognition of thymine C5-C6 bond saturation and sequence specificity of incorporation Nucleic Acids Res. 16 1988 11339 11354
22. A.A. Purmal, J.P. Bond, B.A. Lyons, Y.W. Kow, and S.S. Wallace Uracil glycol deoxynucleoside triphosphate is a better substrate for DNA polymerase I Klenow Fragment than thymine glycol deoxynucleoside triphosphate Biochemistry 37 1998 330 338
23. S. Tornaletti, L.S. Maeda, D.R. Lloyd, D. Reines, and P.C. Hanawalt Effect of thymine glycol on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II J. Biol. Chem. 276 2001 45367 45371
24. H. Miller, A.S. Fernandes, E. Zaika, M.M. McTigue, M.C. Torres, M. Wente, C.R. Iden, and A.P. Grollman Stereoselective excision of thymine glycol from oxidatively damaged DNA Nucleic Acids Res. 32 2004 338 345
25. Y. Wang HPLC isolation and mass spectrometric characterization of two isomers of thymine glycols in oligodeoxynucleotides Chem. Res. Toxicol. 15 2002 671 676
26. M.M. McTigue, R.A. Rieger, T.A. Rosenquist, C.R. Iden, and C.R. De Los Santos Stereoselective excision of thymine glycol lesions by mammalian cell extracts DNA Repair (Amst) 3 2004 313 322
27. Y. Vaishnav, E. Holwitt, C. Swenberg, H.-C. Lee, and L.-S. Kan Synthesis and characterization of stereoisomers of 5,6-dihydro-5,6-dihydroxythymidine J. Biomol. Struct. Dyn. 8 1991 935 951
28. S. Iwai Synthesis and thermodynamic studies of oligonucleotides containing the two isomers of thymine glycol Chem. Eur. J. 7 2001 4343 4351
29. S. Iwai Synthesis of a thymine glycol building block and its incorporation into oligonucleotides Nucleic Acids Symp. Ser. 44 2000 121 122
30. S. Iwai Synthesis of thymine glycol containing oligonucleotides from a building block with the oxidized base Angew. Chem. Int. Ed. 39 2000 3874 3876
31. Y. Doi, K. Hitomi, J.A. Tainer, and S. Iwai Synthesis of oligonucleotides containing 2′-fluorinated thymidine glycol as mechanism-based inhibitors of endonuclease III Nucleic Acids Symp. Ser. (Oxf.) 49 2005 195 196
32. T. Shimizu, K. Manabe, S. Yoshikawa, Y. Kawasaki, and S. Iwai Preferential formation of (5S, 6R)-thymine glycol for oligodeoxyribonucleotide synthesis and analysis of drug binding to thymine glycol-containing DNA Nucleic Acids Res. 34 2006 313 321
33. Y. Doi, A. Katafuchi, Y. Fujiwara, K. Hitomi, J.A. Tainer, H. Ide, and S. Iwai Synthesis and characterization of oligonucleotides containing 2′-fluorinated thymidine glycol as inhibitors of the endonuclease III reaction Nucleic Acids Res. 34 2006 1540 1551
34. K.B. Sharpless, W. Amberg, Y.L. Bennani, G.A. Crispino, J. Hartung, K.S. Jeong, H.L. Kwong, K. Morikawa, Z.M. Wang, D. Xu, and X.L. Zhang The osmium-catalyzed asymmetric dihydroxylation (AD): a new ligand class and a process improvement J. Org. Chem. 57 1992 2768 2771
35. W. Guschlbauer, and K. Jankowski Nucleoside conformation is determined by the electronegativity of the sugar substituent Nucleic Acids Res. 8 1980 1421 1433
36. P. Aller, M.A. Rould, M. Hogg, S.S. Wallace, and S. Doublié A structural rationale for stalling of a replicative DNA polymerase at the most common oxidative thymine lesion, thymine glycol Proc. Natl. Acad. Sci. U.S.A. 104 2007 814 818
37. J.M. Clark, N. Pattabiraman, W. Jarvis, and G.P. Beardsley Modeling and molecular mechanical studies of the cis-thymine glycol radiation damage lesion in DNA Biochemistry 26 1987 5404 5409
38. K. Miaskiewicz, J. Miller, R. Ornstein, and R. Osman Molecular dynamics simulations of the effects of ring-saturated thymine lesions on DNA structure Biopolymers 35 1995 113 124
39. J. Evans, M. Maccabee, Z. Hatahet, J. Courcelle, R. Bockrath, H. Ide, and S. Wallace Thymine ring saturation and fragmentation products: lesion bypass, misinsertion and implications for mutagenesis Mutat. Res. 299 1993 147 156
40. J.M. Clark, and G.P. Beardsley Template length, sequence context, and 3′-5′ exonuclease activity modulate replicative bypass of thymine glycol lesions in vitro Biochemistry 28 1989 775 779
41. P. Aller, S. Duclos, S.S. Wallace, and S. Doublié A crystallographic study of the role of sequence context in thymine glycol bypass by a replicative DNA polymerase serendipitously sheds light on the exonuclease complex J. Mol. Biol. 412 2011 22 34
42. K.L. Brown, T. Adams, V.P. Jasti, A.K. Basu, and M.P. Stone Interconversion of the cis-5R,6S- and trans-5R,6R-thymine glycol lesions in duplex DNA J. Am. Chem. Soc. 130 2008 11701 11710
43. K.L. Brown, A.K. Basu, and M.P. Stone The cis-(5R,6S)-thymine glycol lesion occupies the wobble position when mismatched with deoxyguanosine in DNA Biochemistry 48 2009 9722 9733
44. K.L. Brown, M. Roginskaya, Y. Zou, A. Altamirano, A.K. Basu, and M.P. Stone Binding of the human nucleotide excision repair proteins XPA and XPC/HR23B to the 5R-thymine glycol lesion and structure of the cis-(5R,6S) thymine glycol epimer in the 5′-GTgG-3′ sequence: destabilization of two base pairs at the lesion site Nucleic Acids Res. 38 2010 428 440
45. K.L. Brown, M. Roginskaya, Y. Zou, A. Altamirano, A.K. Basu, and M.P. Stone Structural consequences of Epimerization of thymine glycol lesions in duplex DNA: implications for DNA repair M.P. Stone, Structural Biology of DNA Damage and Repair ACS Symposium series vol. 1041 2010 Am. Chem. Soc. Washington, DC 11 28
46. M.T. Ocampo-Hafalla, A. Altamirano, A.K. Basu, M.K. Chan, J.E. Ocampo, A. Cummings Jr., R.J. Boorstein, R.P. Cunningham, and G.W. Teebor Repair of thymine glycol by hNth1 and hNeil1 is modulated by base pairing and cis-trans epimerization DNA Repair 5 2006 444 454
47. M. Haranczyk, G. Lupica, I. Dabkowska, and M. Gutowski Cylindrical projection of electrostatic potential and image analysis tools for damaged DNA: the substitution of thymine with thymine glycol J. Phys. Chem. B 112 2008 2198 2206
48. S. Ikeda, T. Biswas, R. Roy, T. Izumi, I. Boldogh, A. Kurosky, A. Sarker, S. Seki, and S. Mitra Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue J. Biol. Chem. 273 1998 21585 21593
49. A. Katafuchi, T. Nakano, A. Masaoka, H. Terato, S. Iwai, F. Hanaoka, and H. Ide Differential specificity of human and Escherichia coli endonuclease III and VIII homologues for oxidative base lesions J. Biol. Chem. 279 2004 14464 14471
50. M. Dizdaroglu, J. Laval, and S. Boiteux Substrate specificity of the Escherichia coli endonuclease III: excision of thymine- and cytosine-derived lesions in DNA produced by radiation-generated free radicals Biochemistry 32 1993 12105 12111
51. M.F. Laspia, and S.S. Wallace Excision repair of thymine glycols, urea residues, and apurinic sites in Escherichia coli J. Bacteriol. 170 1988 3359 3366
52. Z. Hatahet, Y.W. Kow, A.A. Purmal, R.P. Cunningham, and S.S. Wallace New substrates for old enzymes. 5-Hydroxy-2′-deoxycytidine and 5-hydroxy-2′-deoxyuridine are substrates for Escherichia coli endonuclease III and formamidopyrimidine DNA N-glycosylase, while 5-hydroxy-2′- deoxyuridine is a substrate for uracil DNA N-glycosylase J. Biol. Chem. 269 1994 18814 18820
53. M.L. Dodson, R.D. Schrock, and R.S. Lloyd Evidence for an imino intermediate in the T4 endonuclease V reaction Biochemistry 32 1993 8284 8290
54. J.C. Fromme, and G.L. Verdine Structure of a trapped endonuclease III-DNA covalent intermediate EMBO J. 22 2003 3461 3471
55. D. Jiang, Z. Hatahet, J.O. Blaisdell, and R.J. Melamede S.S. Wallace, Escherichia coli endonuclease VIII: Cloning, sequencing and overexpression of the nei structural gene and characterization of nei and nei nth mutants J. Bacteriol. 179 1997 3773 3782
56. Y. Saito, F. Uraki, S. Nakajima, A. Asaeda, K. Ono, K. Kubo, and K. Yamamoto Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12 J. Bacteriol. 179 1997 3783 3785
57. R.J. Melamede, Z. Hatahet, Y.W. Kow, H. Ide, and S.S. Wallace Isolation and characterization of endonuclease VIII from Escherichia coli Biochemistry 33 1994 1255 1264
58. I. Alseth, L. Eide, M. Pirovano, T. Rognes, E. Seeberg, and M. Bjoras The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast Mol. Biol. Cell. 19 1999 3779 3787
59. L. Eide, M. Bjoras, M. Pirovano, I. Alseth, K.G. Berdal, and E. Seeberg Base excision of oxidative purine and pyrimidine DNA damage in Saccharomyces cerevisiae by a DNA glycosylase with sequence similarity to endonuclease III from Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 93 1996 10735 10740
60. S. Senturker, P. Auffret van der Kemp, H.J. You, P.W. Doetsch, M. Dizdaroglu, and S. Boiteux Substrate specificities of the ntg1 and ntg2 proteins of Saccharomyces cerevisiae for oxidized DNA bases are not identical Nucleic Acids Res. 26 1998 5270 5276
61. V. Bandaru, S. Sunkara, S.S. Wallace, and J.P. Bond A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII DNA Repair (Amst.) 1 2002 517 529
62. T.K. Hazra, T. Izumi, I. Boldogh, B. Imhoff, Y.W. Kow, P. Jaruga, M. Dizdaroglu, and S. Mitra Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA Proc. Natl. Acad. Sci. U.S.A. 99 2002 3523 3528
63. M. Takao, S. Kanno, T. Shiromoto, R. Hasegawa, H. Ide, S. Ikeda, A.H. Sarker, S. Seki, J.Z. Xing, X.C. Le, M. Weinfeld, K. Kobayashi, J. Miyazaki, M. Miijtjens, J.H. Hoeijmakers, G. van der Horst, and A. Yasui Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse nth1 gene encoding an endonuclease III homolog for repair of thymine glycol EMBO J. 21 2002 3486 3493
64. M. Takao, S. Kanno, K. Kobayashi, Q.M. Zhang, S. Yonei, G.T. van der Horst, and A. Yasui A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue J. Biol. Chem. 277 2002 42205 42213
65. M.T. Ocampo, W. Chaung, D.R. Marenstein, M.K. Chan, A. Altamirano, A.K. Basu, R.J. Boorstein, R.P. Cunningham, and G.W. Teebor Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity Mol. Biol. Cell. 22 2002 6111 6121
66. T.A. Rosenquist, E. Zaika, A.S. Fernandes, D.O. Zharkov, H. Miller, and A.P. Grollman The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death DNA Repair 2 2003 581 591
67. R. Yamamoto, M. Akiyama, H. Ide, K. Yamamoto, S. Matsuyama, and K. Kubo A novel monofunctional DNA glycosylase activity against thymine glycol in mouse cell nuclei Radiat. Res. 49 2008 249 259
68. I.D. Odell, K. Newick, N.H. Heintz, S.S. Wallace, and D.S. Pederson Non-specific DNA binding interferes with the efficient excision of oxidative lesions from chromatin by the human glycosylase, NEIL1 DNA Repair 9 2010 134 143
69. M. Goto, K. Shinmura, H. Igarashi, M. Kobayashi, H. Konno, H. Yamada, M. Iwaizumi, S. Kageyama, T. Tsuneyoshi, S. Tsugane, and H. Sugimura Altered expression of the human base excision repair gene NTH1 in gastric cancer Carcinogenesis 30 2009 1345 1352
70. K. Imamura, A. Averill, S.S. Wallace, and S. Doublié Structural characterization of viral ortholog of human DNA glycosylase NEIL1 bound to thymine glycol or 5-hydroxyuracil-containing DNA J. Biol. Chem. 287 2012 4288 4298
71. A.A. Purmal, G.W. Lampman, J.P. Bond, Z. Hatahet, and S.S. Wallace Enzymatic processing of uracil glycol, a major oxidative product of DNA cytosine J. Biol. Chem. 273 1998 10026 10035
72. M. Jaciuk, E. Nowak, K. Skowronek, A. Tańska, and M. Nowotny Structure of UvrA nucleotide excision repair protein in complex with modified DNA Nat. Struct. Mol. Biol. 18 2011 191 197
73. Z. Yang, M. Roginskaya, L.C. Colis, A.K. Basu, S.M. Shell, Y. Liu, P.R. Musich, C.M. Harris, T.M. Harris, and Y. Zou Specific and efficient binding of xeroderma pigmentosum complementation group A to double-strand/single-strand DNA junctions with 3′- and/or 5′-ssDNA branches Biochemistry 45 2006 15921 15930
74. J.J. Lin, and A. Sancar A new mechanism for repairing oxidative damage to DNA: (A)BC exenuclease removes AP sites and thymine glycols from DNA Biochemistry 28 1989 7979 7984
75. Y.W. Kow, S.S. Wallace, and B. Van Houten UvrABC nuclease complex repairs thymine glycol, an oxidative DNA base damage Mutat. Res. 235 1990 147 156
76. K. Miaskiewicz, J. Miller, and R. Osman Ab initio theoretical study of the structures of thymine glycol and dihydrothymine Int. J. Radiat. Biol. 63 1993 677 686
77. F. Le Page, E.E. Kwoh, A. Avrutskaya, A. Gentil, S.A. Leadon, A. Sarasin, and P.K. Cooper Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome Cell (Cambridge, MA, U.S.) 101 2000 159 171
78. P.C. Hanawalt Transcription-coupled repair and human disease Science (Washington, DC, U.S.) 266 1994 1957 1958
79. S. Tornaletti, and P.C. Hanawalt Effect of DNA lesions on transcription elongation Biochimie 81 1999 139 146
80. I. Mellon, V.A. Bohr, C.A. Smith, and P.C. Hanawalt Preferential DNA repair of an active gene in human cells Proc. Natl. Acad. Sci. U.S.A. 83 1986 8878 8882
81. H. Dou, S. Mitra, and T.K. Hazra Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2 J. Biol. Chem. 278 2003 49679 49684
82. D. Banerjee, S.M. Mandal, A. Das, M.L. Hegde, S. Das, K.K. Bhakat, I. Boldogh, P.S. Sarkar, S. Mitra, and T.K. Hazra Preferential repair of oxidized base damage in the transcribed genes of mammalian cells J. Biol. Chem. 286 2011 6006 6016
83. H. Ide, Y. Kimura, A. Murakami, S.S. Wallace, and K. Makino Effects of base damages on DNA replication Nucleic Acids Symp. Ser. 25 1991 161 162
84. J.M. McNulty, B. Jerkovic, P.H. Bolton, and A.K. Basu Replication inhibition and miscoding properties of DNA templates containing a site-specific cis-thymine glycol or urea residue Chem. Res. Toxicol. 11 1998 666 673
85. L.A. Loeb, and R.A. Zakour Relationship between mutagenesis and carcinogenesis T.G. Spiro, Nucleic Acid-Metal Ion Interactions vol. I 1980 John Wiley New York 115 144
86. A.A. Purmal, Y.W. Kow, and S.S. Wallace Major oxidative products of cytosine, 5-hydroxycytosine and 5-hydroxyuracil, exhibit sequence context-dependent mispairing in vitro Nucleic Acids Res. 22 1994 72 78
87. M.F. Goodman Error-prone repair DNA polymerases in prokaryotes and eukaryotes Annu. Rev. Biochem. 71 2002 17 50
88. H. Ohmori, E.C. Friedberg, R.P. Fuchs, M.F. Goodman, F. Hanaoka, D. Hinkle, T.A. Kunkel, C.W. Lawrence, Z. Livneh, T. Nohmi, L. Prakash, S. Prakash, T. Todo, G.C. Walker, Z. Wang, and R. Woodgate The Y-family of DNA polymerases Mol. Cell. 8 2001 7 8
89. P.L. Fischhaber, V.L. Gerlach, W.J. Feaver, Z. Hatahet, S.S. Wallace, and E.C. Friedberg Human DNA polymerase κ bypasses and extends beyond thymine glycols during translesion synthesis in vitro, preferentially incorporating correct nucleotides J. Biol. Chem. 277 2002 37604 37611
90. E.C. Friedberg, R. Wagner, and M. Radman Specialized DNA polymerases, cellular survival, and the genesis of mutations Science (Washington, DC, U.S.) 296 2002 1627 1630
91. U. Hübscher, and G. Maga DNA replication and repair bypass machines Curr. Opin. Chem. Biol. 15 2011 627 635
92. L.A. Loeb, and R.J. Monnat Jr. DNA polymerases and human disease Nat. Rev. Genet. 9 2008 594 604
93. A. Alt, K. Lammens, C. Chiocchini, A. Lammens, J.C. Pieck, D. Kuch, K.P. Hopfner, and T. Carell Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase eta Science (Washington, DC, U.S.) 318 2007 967 970
94. A. Ummat, T.D. Silverstein, R. Jain, A. Buku, R.E. Johnson, L. Prakash, S. Prakash, and A.K. Aggarwal Human DNA polymerase η is pre-aligned for dNTP binding and catalysis J. Mol. Biol. 415 2012 627 634
95. R. Kusumoto, C. Masutani, S. Iwai, and F. Hanaoka Translesion synthesis by human DNA polymerase η across thymine glycol lesions Biochemistry 41 2002 6090 6099
96. V.L. Gerlach, L. Aravind, G. Gotway, R.A. Schultz, E.V. Koonin, and E.C. Friedberg Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily Proc. Natl. Acad. Sci. U.S.A. 96 1999 11922 11927
97. N. Niimi, A. Sassa, A. Katafuchi, P. Gruz, H. Fujimoto, R.R. Bonala, F. Johnson, T. Ohta, and T. Nohmi The steric gate amino acid tyrosine 112 is required for efficient mismatched-primer extension by human DNA polymerase kappa Biochemistry 48 2009 4239 4246
98. S. Lone, S.A. Townson, S.N. Uljon, R.E. Johnson, A. Brahma, D.T. Nair, S. Prakash, L. Prakash, and A.K. Aggarwal Human DNA polymerase kappa encirclies DNA; implications for mismatch extension and lesion bypass Mol. Cell. 25 2007 601 614
99. D.T. Nair, R.E. Johnson, L. Prakash, S. Prakash, and A.K. Aggarwal Rev1 employs a novel mechanism of DNA synthesis using a protein template Science (Washington, DC, U.S.) 309 2005 2219 2222
100. J.-Y. Choi, S. Lim, E.-J. Kim, A. Jo, and F.P. Guengerich Translesion synthesis across abasic lesions by human B-family and Y-family DNA polymerases α, δ, η, ι, κ, and REV1 J. Mol. Biol. 404 2010 34 44
101. S. Prakash, R.E. Johnson, and L. Prakash Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function Annu. Rev. Biochem. 74 2005 317 353
102. L. Maddukuri, R.L. Eoff, J.-Y. Choi, C.J. Rizzo, F.P. Guengerich, and L.J. Marnett In vitro bypass of the major malondialdehyde- and base propenal-derived DNA adduct by human Y-family DNA polymerases k, l, and Rev1 Biochemistry 49 2010 8415 8424
103. R.E. Johnson, S.-L. Yu, S. Prakash, and L. Prakash Yeast DNA polymerase zeta (ζ) is essential for error-free replication past thymine glycol Genes Dev. 17 2003 77 87
104. J.-H. Yoon, G. Bhatia, S. Prakash, and L. Prakash Error-free replicative bypass of thymine glycol by the combined action of DNA polymerases κ and ζ in human cells Proc. Natl. Acad. Sci. U.S.A. 107 2010 14116 14121
105. K. Takata, T. Shimizu, S. Iwai, and R.D. Wood Human DNA polymerase N (POLN) is a low fidelity enzyme capable of error-free bypass of 5S-thymine glycol J. Biol. Chem. 281 2006 23445 23455
106. K. Takata, M.E. Arana, M. Seki, T.A. Kunkel, and R.D. Wood Evolutionary conservation of residues in vertebrate DNA polymerase N conferring low fidelity and bypass activity Nucleic Acids Res. 38 2010 3233 3244
107. E.A. Belousova, G. Maga, F. Yang, E.A. Kubareva, E.A. Romanova, N.A. Lebedeva, T.S. Oretskaya, and O.I. Lavrik DNA polymerases beta and lyambda bypass thymine glycol in gapped DNA structures Biochemistry 49 2010 4695 4704
108. R.W. Sobol, J.K. Horton, R. Kühn, H. Gu, R.K. Singhal, R. Prasad, K. Rajewsky, and S.H. Wilson Requirement of mammalian DNA polymerase-beta in base-excision repair Nature (London, U.K.) 379 1996 183 186
109. R.K. Singhal, and S.H. Wilson Short gap-filling synthesis by DNA polymerase beta is processive J. Biol. Chem. 268 1993 15906 15911
110. N.A. Lebedeva, N.I. Rechkunova, S.V. Dezhurov, S.N. Khodyreva, A. Favre, L. Blanco, and O.I. Lavrik Comparison of functional properties of mammalian DNA polymerase λ and DNA polymerase β in reactions of DNA syntesis related to DNA repair Biochim. Biophys. Acta 1751 2005 150 158
111. M. Garcia-Diaz, O. Dominguez, L.A. López-Fernández, L.T. de Lera, M.L. Saniger, J.F. Ruiz, M. Parraga, M.J. Garcia-Ortiz, T. Kirchhoff, J. del Mazo, A. Bernad, and L. Blanco DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis J. Mol. Biol. 301 2000 851 867
112. K. Ramadan, I.V. Shevelev, G. Maga, and U. Hübscher DNA polymerase lambda from calf thymus preferentially replicates damaged DNA J. Biol. Chem. 277 2002 18454 18458
113. M. Garcia-Diaz, K. Bebenek, A.A. Larrea, J.M. Havener, L. Perera, J.M. Krahn, L.C. Pedersen, D.A. Ramsden, and T.A. Kunkel Template strand scrunching during DNA gap repair synthesis by human polymerase lambda Nat. Struct. Mol. Biol. 16 2009 967 972
114. H. Maki, and M. Sekiguchi MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis Nature (London, U.K.) 355 1992 273 275
115. L.J. Ferrin, and A.S. Mildvan Nuclear Overhauser effect studies of the conformations and binding site environments of deoxynucleoside triphosphate substrates bound to DNA polymerase I and its large fragment Biochemistry 24 1985 6904 6913
116. J. Miller, K. Miaskiewicz, and R. Osman Structure-function studies of DNA damage using ab initio quantum mechanics and molecular dynamics simulation Ann. NY Acad. Sci. 726 1994 71 91
117. J.R. Wagner, C.-C. Hu, and B.N. Ames Endogenous oxidative damage of deoxycytidine in DNA Proc. Natl. Acad. Sci. U.S.A. 89 1992 3380 3384
118. M. Shimizu, P. Gruz, H. Kamiya, C. Masutani, Y. Xu, Y. Usui, H. Sugiyama, H. Harashima, F. Hanaoka, and T. Nohmi Efficient and erroneous incorporation of oxidized DNA precursors by human DNA polymerase eta Biochemistry 46 2007 5515 5522
119. A. Katafuchi, A. Sassa, N. Niimi, P. Grúz, H. Fujimoto, C. Masutani, F. Hanaoka, T. Ohta, and T. Nohmi Critical amino acids in human DNA polymerases η and κ involved in erroneous incorporation of oxidized nucleotides Nucleic Acids Res. 38 2010 859 867
120. J.O. Blaisdell, and S.S. Wallace Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 98 2001 7426 7430
121. Y. Jiang, Y. Wang, and Y. Wang In vitro replication and repair studies of tandem lesions containing neighbouring thymidine glycol and 8-oxo-7,8-dihydro-2′-deoxyguanosine Chem. Res. Toxicol. 22 2009 574 583
122. H. Huang, S. Imoto, and M.M. Greenberg The mutagenicity of thymidine glycol in Escherichia coli is increased when it is part of a tandem lesion Biochemistry 48 2009 7833 7841
123. I.S. Hong, K.N. Carter, K. Sato, and M.M. Greenberg Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical J. Am. Chem. Soc. 129 2007 4089 4098
124. S. Imoto, L.A. Bransfield, D.L. Croteau, B. Van Houten, and M.M. Greenberg DNA tandem lesion repair by strand displacement synthesis and nucleotide excision repair Biochemistry 47 2008 4306 4316
125. K.C. Cheng, D.S. Cahill, H. Kasai, S. Nishimura, and L.A. Loeb 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions J. Biol. Chem. 267 1992 166 172
126. B. Yuan, Y. Jiang, Y. Wang, and Y. Wang Efficient formation of the tandem thymine glycol/8-oxo-7,8-dihydroguanine lesion in isolated DNA and the mutagenic and cytotoxic properties of the tandem lesions in Escherichia coli cells Chem. Res. Toxicol. 23 2010 11 19
127. Y. Wang, and Y. Wang Synthesis and thermodynamic studies of oligodeoxyribonucleotides containing tandem lesions of thymidine glycol and 8-oxo-2′-deoxyguanosine Chem. Res. Toxicol. 19 2006 837 843
128. 2/ascorbate-induced formation of 5-methylcytosine glycol at CpG sites in duplex DNA Nucleic Acids Res. 37 2009 6635 6643
129. S. Bellon, N. Shikazono, S. Cunniffe, M. Lomax, and P. O'Neill Processing of thymine glycol in a clustered DNA damage site: mutagenic or cytotoxic Nucleic Acids Res. 37 2009 4430 4440