Impact of Chemical Adducts on Translesion Synthesis in Replicative and Bypass DNA Polymerases: From Structure to Function

The Chemical Biology of DNA Damage

Volumn , Issue , 2010, Pages 299-330

  Eoff, Robert L ^a   Egli, Martin ^a   Guengerich, Peter ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bypass polymerase; Cyclobutane pyrimidine dimer; DNA adduct; Polycyclic aromatic hydrocarbon; Replicative polymerase; Translesion synthesis; UV photoproduct

Indexed keywords

EID: 77956547549     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527630110.ch13     Document Type: Chapter

References (215)

1. Ito, J. and Braithwaite, D.K. (1991) Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res., 19, 4045-4057.
2. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., Kunkel, T.A., Lawrence, C.W., et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
3. Bessman, M.J., Lehman, I.R., Simms, E.S., and Kornberg, A. (1958) Enzymatic synthesis of deoxyribonucleic acid. II. General properties of the reaction. J. Biol. Chem., 233, 171-177.
4. Lehman, I.R., Bessman, M.J., Simms, E.S., and Kornberg, A. (1958) Enzymatic synthesis of deoxyribonucleic acid. I. Preparation of substrates and partial purification of an enzyme from Escherichia coli. J. Biol. Chem., 233, 163-170.
5. Burgers, P.M. (1998) Eukaryotic DNA polymerases in DNA replication and DNA repair. Chromosoma, 107, 218-227.
6. Friedberg, E.C., Fischhaber, P.L., and Kisker, C. (2001) Error-prone DNA polymerases: novel structures and the benefits of infidelity. Cell, 107, 9-12.
7. Friedberg, E.C., Lehmann, A.R., and Fuchs, R.P. (2005) Trading places: how do DNA polymerases switch during translesion DNA synthesis? Mol. Cell, 18, 499-505.
8. Guengerich, F.P. (2006) Interactions of carcinogen-bound DNA with individual DNA polymerases. Chem. Rev., 106, 420-452.
9. Johnson, K.A. (1993) Conformational coupling in DNA polymerase fidelity. Annu. Rev. Biochem., 62, 685-713.
10. Joyce, C.M. and Benkovic, S.J. (2004) DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry, 43, 14317-14324.
11. Kunkel, T.A. (2004) DNA replication fidelity. J. Biol. Chem., 279, 16895-16898.
12. Lehman, I.R. and Richardson, C.C. (1964) The deoxyribonucleases of Escherichia coli. IV. An exonuclease activity present in purified preparations of deoxyribonucleic acid polymerase. J. Biol. Chem., 239, 233-241.
13. Livingston, D.M. and Richardson, C.C. (1975) Deoxyribonucleic acid polymerase III of Escherichia coli. Characterization of associated exonuclease activities. J. Biol. Chem., 250, 470-478.
14. Maki, H. and Kornberg, A. (1987) Proofreading by DNA polymerase III of Escherichia coli depends on cooperative interaction of the polymerase and exonuclease subunits. Proc. Natl. Acad. Sci. USA, 84, 4389-4392.
15. Richardson, C.C. and Kornberg, A.A. (1964) Deoxyribonucleic acid phosphatase-exonuclease from Escherichia coli. I. Purification of the enzyme and characterization of the phosphatase activity. J. Biol. Chem., 239, 242-250.
16. Richardson, C.C., Lehman, I.R., and Kornberg, A.A. (1964) Deoxyribonucleic acid phosphatase-exonuclease from Escherichia coli. II. Characterization of the exonuclease activity. J. Biol. Chem., 239, 251-258.
17. Tabor, S. and Richardson, C.C. (1989) Selective inactivation of the exonuclease activity of bacteriophage T7 DNA polymerase by in vitro mutagenesis. J. Biol. Chem., 264, 6447-6458.
18. Bedinger, P. and Alberts, B.M. (1983) The 3 ′-5 ′ proofreading exonuclease of bacteriophage T4 DNA polymerase is stimulated by other T4 DNA replication proteins. J. Biol. Chem., 258, 9649-9656.
19. Capson, T.L., Peliska, J.A., Kaboord, B.F., Frey, M.W., Lively, C., Dahlberg, M., and Benkovic, S.J. (1992) Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry, 31, 10984-10994.
20. Venkatesan, M. and Nossal, N.G. (1982) Bacteriophage T4 gene 44/62 and gene 45 polymerase accessory proteins stimulate hydrolysis of duplex DNA by T4 DNA polymerase. J. Biol. Chem., 257, 12435-12443.
21. Irimia, A., Zang, H., Loukachevitch, L.V., Eoff, R.L., Guengerich, F.P., and Egli, M. (2006) Calcium is a cofactor of polymerization but inhibits pyrophosphorolysis by the Sulfolobus solfataricus DNA polymerase Dpo4. Biochemistry, 45, 5949-5956.
22. Vaisman, A., Ling, H., Woodgate, R., and Yang, W. (2005) Fidelity of Dpo4: effect of metal ions, nucleotide selection and pyrophosphorolysis. EMBO J., 24, 2957-2967.
23. Prasad, R., Beard, W.A., Strauss, P.R., and Wilson, S.H. (1998) Human DNA polymerase β deoxyribose phosphate lyase. Substrate specificity and catalytic mechanism. J. Biol. Chem., 273, 15263-15270.
24. SantaLucia, J., Jr. (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl. Acad. Sci. USA, 95, 1460-1465.
25. Blattner, F.R., Plunkett, G., 3rd, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science, 277, 1453-1474.
26. Kelman, Z. and O'Donnell, M. (1995) DNA polymerase III holoenzyme: structure and function of a chromosomal replicating machine. Annu. Rev. Biochem., 64, 171-200.
27. McHenry, C.S. (1988) DNA polymerase III holoenzyme of Escherichia coli. Annu. Rev. Biochem., 57, 519-550.
28. Goodman, M.F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem., 71, 17-50.
29. She, Q., Singh, R.K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M.J., Chan-Weiher, C.C., Clausen, I.G., et al. (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc. Natl. Acad. Sci. USA, 98, 7835-7840.
30. Loeb, L.A. and Monnat, R.J., Jr. (2008) DNA polymerases and human disease. Nat. Rev. Genet., 9, 594-604.
31. Steitz, T.A. (1999) DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem., 274, 17395-17398.
32. Yang, W. and Woodgate, R. (2007) What a difference a decade makes: insights into translesion DNA synthesis. P roc. Natl. Acad. Sci. USA, 104, 15591-15598.
33. Patel, P.H. and Loeb, L.A. (2001) Getting a grip on how DNA polymerases function. Nat. Struct. Biol., 8, 656-659.
34. Steitz, T.A. (1998) A mechanism for all polymerases. Nature, 391, 231-232.
35. von Hippel, P.H., Fairfield, F.R., and Dolejsi, M.K. (1994) On the processivity of polymerases. Ann. NY Acad. Sci., 726, 118-131.
36. Seki, M., Marini, F., and Wood, R.D. (2003) POLQ (Pol θ), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res., 31, 6117-6126.
37. Patel, S.S., Wong, I., and Johnson, K.A. (1991) Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry, 30, 511-525.
38. Doublie, S., Sawaya, M.R., and Ellenberger, T. (1999) An open and closed case for all polymerases. Structure, 7, R31-R35.
39. Doublié, S., Tabor, S., Long, A.M., Richardson, C.C., and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature, 391, 251-258.
40. Tsai, Y.C. and Johnson, K.A. (2006) A new paradigm for DNA polymerase specificity. Biochemistry, 45, 9675-9687.
41. Lin, P., Pedersen, L.C., Batra, V.K., Beard, W.A., Wilson, S.H., and Pedersen, L.G. (2006) Energy analysis of chemistry for correct insertion by DNA polymerase β. Proc. Natl. Acad. Sci. USA, 103, 13294-13299.
42. Wang, L., Yu, X., Hu, P., Broyde, S., and Zhang, Y. (2007) A water-mediated and substrate-assisted catalytic mechanism for Sulfolobus solfataricus DNA polymerase IV. J. Am. Chem. Soc., 129, 4731-4737.
43. Zang, H., Goodenough, A.K., Choi, J.Y., Irimia, A., Loukachevitch, L.V., Kozekov, I.D., Angel, K.C., Rizzo, C.J., et al. (2005) DNA adduct bypass polymerization by Sulfolobus solfataricus DNA polymerase Dpo4: analysis and crystal structures of multiple base pair substitution and frameshift products with the adduct 1, N 2-ethenoguanine. J. Biol. Chem., 280, 29750-29764.
44. Lindahl, T. and Andersson, A. (1972) Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry, 11, 3618-3623.
45. Nakamura, J., Walker, V.E., Upton, P.B., Chiang, S.Y., Kow, Y.W., and Swenberg, J.A. (1998) Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions. Cancer Res., 58, 222-225.
46. Loeb, L.A. and Preston, B.D. (1986) Mutagenesis by apurinic/apyrimidinic sites. Annu. Rev. Genet., 20, 201-230.
47. Xue, L. and Greenberg, M.M. (2007) Use of fluorescence sensors to determine that 2-deoxyribonolactone is the major alkali-labile deoxyribose lesion produced in oxidatively damaged DNA. Angew. Chem. Int. Ed., 46, 561-564.
48. Kokoska, R.J., McCulloch, S.D., and Kunkel, T.A. (2003) The efficiency and specificity of apurinic/apyrimidinic site bypass by human DNA polymerase η and Sulfolobus solfataricus Dpo4. J. Biol. Chem., 278, 50537-50545.
49. Paz-Elizur, T., Takeshita, M., Goodman, M., O'Donnell, M., and Livneh, Z. (1996) Mechanism of translesion DNA synthesis by DNA polymerase II. Comparison to DNA polymerases I and III core. J. Biol. Chem., 271, 24662-24669.
50. Randall, S.K., Eritja, R., Kaplan, B.E., Petruska, J., and Goodman, M.F. (1987) Nucleotide insertion kinetics opposite abasic lesions in DNA. J. Biol. Chem., 262, 6864-6870.
51. Shibutani, S., Takeshita, M., and Grollman, A.P. (1997) Translesional synthesis on DNA templates containing a single abasic site. A mechanistic study of the " A rule ". J. Biol. Chem., 272, 13916-13922.
52. Tang, M., Pham, P., Shen, X., Taylor, J.S., O'Donnell, M., Woodgate, R., and Goodman, M.F. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature, 404, 1014-1018.
53. Gibbs, P.E., McDonald, J., Woodgate, R., and Lawrence, C.W. (2005) The relative roles in vivo of Saccharomyces cerevisiae Pol η, Pol ζ, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics, 169, 575-582.
54. Haracska, L., Unk, I., Johnson, R.E., Johansson, E., Burgers, P.M., Prakash, S., and Prakash, L. (2001) Roles of yeast DNA polymerases δ and ζ and of Rev1 in the bypass of abasic sites. Genes Dev., 15, 945-954.
55. Mozzherin, D.J., Shibutani, S., Tan, C.K., Downey, K.M., and Fisher, P.A. (1997) Proliferating cell nuclear antigen promotes DNA synthesis past template lesions by mammalian DNA polymerase δ. Proc. Natl. Acad. Sci. USA, 94, 6126-6131.
56. Avkin, S., Adar, S., Blander, G., and Livneh, Z. (2002) Quantitative measurement of translesion replication in human cells: evidence for bypass of abasic sites by a replicative DNA polymerase. P roc. Natl. Acad. Sci. USA, 99, 3764-3769.
57. Haracska, L., Washington, M.T., Prakash, S., and Prakash, L. (2001) Inefficient bypass of an abasic site by DNA polymerase η. J. Biol. Chem., 276, 6861-6866.
58. Haracska, L., Prakash, L., and Prakash, S. (2002) Role of human DNA polymerase κ as an extender in translesion synthesis. Proc. Natl. Acad. Sci. USA, 99, 16000-16005.
59. Wolfle, W.T., Washington, M.T., Prakash, L., and Prakash, S. (2003) Human DNA polymerase κ uses template-primer misalignment as a novel means for extending mispaired termini and for generating single-base deletions. G enes Dev., 17, 2191-2199.
60. Otsuka, C., Loakes, D., and Negishi, K. (2002) The role of deoxycytidyl transferase activity of yeast Rev1 protein in the bypass of abasic sites. Nucleic Acids Res. Suppl., 2, 87-88.
61. Zhao, B., Xie, Z., Shen, H., and Wang, Z. (2004) Role of DNA polymerase η in the bypass of abasic sites in yeast cells. Nucleic Acids Res., 32, 3984-3994.
62. Greer, S. and Zamenhof, S. (1962) Studies on depurination of DNA by heat. J. Mol. Biol., 4, 123-141.
63. Suzuki, T., Ohsumi, S., and Makino, K. (1994) Mechanistic studies on depurination and apurinic site chain breakage in oligodeoxyribonucleotides. Nucleic Acids Res., 22, 4997-5003.
64. Hogg, M., Wallace, S.S., and Doublie, S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site. EMBO J., 23, 1483-1493.
65. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2004) Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts. Mol. Cell, 13, 751-762.
66. Zahn, K.E., Belrhali, H., Wallace, S.S., and Doublié, S. (2007) Caught bending the A-rule: crystal structures of translesion DNA synthesis with a non-natural nucleotide. Biochemistry, 46, 10551-10561.
67. Fiala, K.A., Hypes, C.D., and Suo, Z. (2007) Mechanism of abasic lesion bypass catalyzed by a Y-family DNA polymerase. J. Biol. Chem., 282, 8188-8198.
68. Fiala, K.A. and Suo, Z. (2007) Sloppy bypass of an abasic lesion catalyzed by a Y-family DNA polymerase. J. Biol. Chem., 282, 8199-8206.
69. Reineks, E.Z. and Berdis, A.J. (2004) Evaluating the contribution of base stacking during translesion DNA replication. B iochemistry, 43, 393-404.
70. Ames, B.N. (1982) Mutagens, carcinogens, and anti-carcinogens. Basic Life Sci., 21, 499-508.
71. Fraga, C.G., Shigenaga, M.K., Park, J.W., Degan, P., and Ames, B.N. (1990) Oxidative damage to DNA during aging: 8-hydroxy-2 ′-deoxyguanosine in rat organ DNA and urine. Proc. Natl. Acad. Sci. USA, 87, 4533-4537.
72. Marnett, L.J. (2000) Oxyradicals and DNA damage. Carcinogenesis, 21, 361-370.
73. Marnett, L.J. (2002) Oxy radicals, lipid peroxidation and DNA damage. Toxicology, 181-182, 219-222.
74. Ames, B.N. (1983) Dietary carcinogens and anticarcinogens. Oxygen radicals and degenerative diseases. Science, 221, 1256-1264.
75. Valko, M., Morris, H., and Cronin, M.T. (2005) Metals, toxicity and oxidative stress. Curr. Med. Chem., 12, 1161-1208.
76. Wallace, K.B. and Starkov, A.A. (2000) Mitochondrial targets of drug toxicity. Annu. Rev. Pharmacol. Toxicol., 40, 353-388.
77. MacMicking, J., Xie, Q.W., and Nathan, C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol., 15, 323-350.
78. Nathan, C. and Shiloh, M.U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA, 97, 8841-8848.
79. Aruoma, O.I., Halliwell, B., and Dizdaroglu, M. (1989) Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J. Biol. Chem., 264, 13024-13028.
80. Aruoma, O.I., Halliwell, B., Gajewski, E., and Dizdaroglu, M. (1989) Damage to the bases in DNA induced by hydrogen peroxide and ferric ion chelates. J. Biol. Chem., 264, 20509-20512.
81. Demple, B. and Harrison, L. (1994) Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem., 63, 915-948.
82. Brieba, L.G., Eichman, B.F., Kokoska, R.J., Doublié, S., Kunkel, T.A., and Ellenberger, T. (2004) Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J., 23, 3452-3461.
83. Einolf, H.J. and Guengerich, F.P. (2001) Fidelity of nucleotide insertion at 8-oxo-7,8-dihydroguanine by mammalian DNA polymerase δ. Steady-state and pre-steady-state kinetic analysis. J. Biol. Chem., 276, 3764-3771.
84. Eoff, R.L., Irimia, A., Angel, K.C., Egli, M., and Guengerich, F.P. (2007) Hydrogen bonding of 7,8-dihydro-8-oxodeoxyguanosine with a charged residue in the little finger domain determines miscoding events in Sulfolobus solfataricus DNA polymerase Dpo4. J. Biol. Chem., 282, 19831-19843.
85. Furge, L.L. and Guengerich, F.P. (1997) Analysis of nucleotide insertion and extension at 8-oxo-7,8-dihydroguanine by replicative T7 polymerase exo-and human immunodeficiency virus-1 reverse transcriptase using steady-state and pre-steady-state kinetics. Biochemistry, 36, 6475-6487.
86. Furge, L.L. and Guengerich, F.P. (1998) Pre-steady-state kinetics of nucleotide insertion following 8-oxo-7,8-dihydroguanine base pair mismatches by bacteriophage T7 DNA polymerase exo-. Biochemistry, 37, 3567-3574.
87. Haracska, L., Prakash, S., and Prakash, L. (2003) Yeast DNA polymerase ζ is an efficient extender of primer ends opposite from 7,8-dihydro-8-oxoguanine and O 6-methylguanine. Mol. Cell. Biol., 23, 1453-1459.
88. Haracska, L., Yu, S.L., Johnson, R.E., Prakash, L., and Prakash, S. (2000) Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase η. Nat. Genet., 25, 458-461.
89. Shibutani, S., Takeshita, M., and Grollman, A.P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature, 349, 431-434.
90. Zang, H., Irimia, A., Choi, J.Y., Angel, K.C., Loukachevitch, L.V., Egli, M., and Guengerich, F.P. (2006) Efficient and high fidelity incorporation of dCTP opposite 7,8-dihydro-8-oxodeoxyguanosine by Sulfolobus solfataricus DNA polymerase Dpo4. J. Biol. Chem., 281, 2358-2372.
91. Einolf, H.J., Schnetz-Boutaud, N., and Guengerich, F.P. (1998) Steady-state and pre-steady-state kinetic analysis of 8-oxo-7,8-dihydroguanosine triphosphate incorporation and extension by replicative and repair DNA polymerases. Biochemistry, 37, 13300-13312.
92. Lowe, L.G. and Guengerich, F.P. (1996) Steady-state and pre-steady-state kinetic analysis of dNTP insertion opposite 8-oxo-7,8-dihydroguanine by Escherichia coli polymerases I exo-and II exo-. Biochemistry, 35, 9840-9849.
93. Carlson, K.D. and Washington, M.T. (2005) Mechanism of efficient and accurate nucleotide incorporation opposite 7,8-dihydro-8-oxoguanine by Saccharomyces cerevisiae DNA polymerase η. Mol. Cell. Biol., 25, 2169-2176.
94. Efrati, E., Tocco, G., Eritja, R., Wilson, S.H., and Goodman, M.F. (1997) Abasic translesion synthesis by DNA polymerase β violates the " A-rule ". Novel types of nucleotide incorporation by human DNA polymerase β at an abasic lesion in different sequence contexts. J. Biol. Chem., 272, 2559-2569.
95. Pinz, K.G., Shibutani, S., and Bogenhagen, D.F. (1995) Action of mitochondrial DNA polymerase γ at sites of base loss or oxidative damage. J. Biol. Chem., 270, 9202-9206.
96. Hsu, G.W., Ober, M., Carell, T., and Beese, L.S. (2004) Error-prone replication of oxidatively damaged DNA by a high-fidelity DNA polymerase. Nature, 431, 217-221.
97. McAuley-Hecht, K.E., Leonard, G.A., Gibson, N.J., Thomson, J.B., Watson, W.P., Hunter, W.N., and Brown, T.(1994) Crystal structure of a DNA duplex containing 8-hydroxydeoxyguanine-adenine base pairs. Biochemistry, 33, 10266-10270.
98. Freisinger, E., Grollman, A.P., Miller, H., and Kisker, C. (2004) Lesion (in) tolerance reveals insights into DNA replication fidelity. EMBO J., 23, 1494-1505.
99. Rechkoblit, O., Malinina, L., Cheng, Y., Kuryavyi, V., Broyde, S., Geacintov, N.E., and Patel, D.J. (2006) Stepwise translocation of Dpo4 polymerase during error-free bypass of an oxoG lesion. PLoS Biol., 4, e11.
100. Lee, D.H. and Pfeifer, G.P. (2008) Translesion synthesis of 7,8-dihydro-8-oxo-2 ′-deoxyguanosine by DNA polymerase η in vivo. Mutat. Res., 641, 19-26.
101. Patro, J.N., Wiederholt, C.J., Jiang, Y.L., Delaney, J.C., Essigmann, J.M., and Greenberg, M.M. (2007) Studies on the replication of the ring opened formamidopyrimidine, Fapy · dG in Escherichia coli. Biochemistry, 46, 10202-10212.
102. Kalam, M.A., Haraguchi, K., Chandani, S., Loechler, E.L., Moriya, M., Greenberg, M.M., and Basu, A.K. (2006) Genetic effects of oxidative DNA damages: comparative mutagenesis of the imidazole ring-opened formamidopyrimidines (Fapy lesions) and 8-oxo-purines in simian kidney cells. Nucleic Acids Res., 34, 2305-2315.
103. Cathcart, R., Schwiers, E., Saul, R.L., and Ames, B.N. (1984) Thymine glycol and thymidine glycol in human and rat urine: a possible assay for oxidative DNA damage. Proc. Natl. Acad. Sci. USA, 81, 5633-5637.
104. Flippen, J.L. (1973) Crystal and molecular structures of reaction products from γ-irradiation of thymine and cytosine. cis-Thymine glycol and trans-1-cabamoylimidazolidone-4,5-diol. Acta Crystallogr. B, 29, 1756-1762.
105. Clark, J.M. and Beardsley, G.P. (1987) Functional effects of cis-thymine glycol lesions on DNA synthesis in vitro. Biochemistry, 26, 5398-5403.
106. Johnson, R.E., Yu, S.L., Prakash, S., and Prakash, L. (2003) Yeast DNA polymerase ζ is essential for error-free replication past thymine glycol. Genes Dev., 17, 77-87.
107. Kusumoto, R., Masutani, C., Iwai, S., and Hanaoka, F. (2002) Translesion synthesis by human DNA polymerase η across thymine glycol lesions. Biochemistry, 41, 6090-6099.
108. Fischhaber, P.L., Gerlach, V.L., Feaver, W.J., Hatahet, Z., Wallace, S.S., and Friedberg, E.C. (2002) Human DNA polymerase κ bypasses and extends beyond thymine glycols during translesion synthesis in vitro, preferentially incorporating correct nucleotides. J. Biol. Chem., 277, 37604-37611.
109. Aller, P., Rould, M.A., Hogg, M., Wallace, S.S., and Doublié, S. (2007) A structural rationale for stalling of a replicative DNA polymerase at the most common oxidative thymine lesion, thymine glycol. Proc. Natl. Acad. Sci. USA, 104, 814-818.
110. Kung, H.C. and Bolton, P.H. (1997) Structure of a duplex DNA containing a thymine glycol residue in solution. J. Biol. Chem., 272, 9227-9236.
111. Clark, J.M. and Beardsley, G.P. (1989) Template length, sequence context, and 3 ′-5 ′ exonuclease activity modulate replicative bypass of thymine glycol lesions in vitro. Biochemistry, 28, 775-779.
112. Hayes, R.C. and LeClerc, J.E. (1986) Sequence dependence for bypass of thymine glycols in DNA by DNA polymerase I. Nucleic Acids Res., 14, 1045-1061.
113. Akasaka, S. and Guengerich, F.P. (1999) Mutagenicity of site-specifically located 1, N 2-ethenoguanine in Chinese hamster ovary cell chromosomal DNA. Chem. Res. Toxicol., 12, 501-507.
114. Guengerich, F.P., Langouet, S., Mican, A.N., Akasaka, S., Muller, M., and Persmark, M. (1999) Formation of etheno adducts and their effects on DNA polymerases. IARC Sci. Publ., 150, 137-145.
115. Moriya, M., Zhang, W., Johnson, F., and Grollman, A.P. (1994) Mutagenic potency of exocyclic DNA adducts: marked differences between Escherichia coli and simian kidney cells. Proc. Natl. Acad. Sci. USA, 91, 11899-11903.
116. Pandya, G.A. and Moriya, M. (1996) 1, N 6-ethenodeoxyadenosine, a DNA adduct highly mutagenic in mammalian cells. Biochemistry, 35, 11487-11492.
117. Choi, J.Y., Zang, H., Angel, K.C., Kozekov, I.D., Goodenough, A.K., Rizzo, C.J., and Guengerich, F.P. (2006) Translesion synthesis across 1, N 2-ethenoguanine by human DNA polymerases. Chem. Res. Toxicol., 19, 879-886.
118. Langouet, S., Mican, A.N., Muller, M., Fink, S.P., Marnett, L.J., Muhle, S.A., and Guengerich, F.P. (1998) Misincorporation of nucleotides opposite five-membered exocyclic ring guanine derivatives by Escherichia coli polymerases in vitro and in vivo : 1, N 2-ethenoguanine, 5,6,7,9-tetrahydro-9-oxoimidazo[1,2-a ] purine, and 5,6,7,9-tetrahydro-7-hydroxy-9-oxoimidazo[1,2-a ]purine. Biochemistry, 37, 5184-5193.
119. Wolfle, W.T., Johnson, R.E., Minko, I.G., Lloyd, R.S., Prakash, S., and Prakash, L. (2005) Human DNA polymerase ι promotes replication through a ring-closed minor-groove adduct that adopts a syn conformation in DNA. Mol. Cell Biol., 25, 8748-8754.
120. Shanmugam, G., Goodenough, A.K., Kozekov, I.D., Guengerich, F.P., Rizzo, C.J., and Stone, M.P. (2007) Structure of the 1, N 2-etheno-2 ′-deoxyguanosine adduct in duplex DNA at pH 8.6. Chem. Res. Toxicol., 20, 1601-1611.
121. Shanmugam, G., Kozekov, I.D., Guengerich, F.P., Rizzo, C.J., and Stone, M.P. (2008) Structure of the 1, N 2-ethenodeoxyguanosine adduct opposite cytosine in duplex DNA: Hoogsteen base pairing at pH 5.2. Chem. Res. Toxicol., 21, 1795-1805.
122. Stone, M.P., Cho, Y.J., Huang, H., Kim, H.Y., Kozekov, I.D., Kozekova, A., Wang, H., Minko, I.G., et al. (2008) Interstrand DNA cross-links induced by α, β-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc. Chem. Res., 41, 793-804.
123. Mao, H., Schnetz-Boutaud, N.C., Weisenseel, J.P., Marnett, L.J., and Stone, M.P. (1999) Duplex DNA catalyzes the chemical rearrangement of a malondialdehyde deoxyguanosine adduct. Proc. Natl. Acad. Sci. USA, 96, 6615-6620.
124. Guengerich, F.P., Persmark, M., and Humphreys, W.G. (1993) Formation of 1, N 2-and N 2,3-ethenoguanine from 2-halooxiranes: isotopic labeling studies and isolation of a hemiaminal derivative of N 2-(2-oxoethyl)guanine. Chem. Res. Toxicol., 6, 635-648.
125. de los Santos, C., Zaliznyak, T., and Johnson, F. (2001) NMR characterization of a DNA duplex containing the major acrolein-derived deoxyguanosine adduct γ-OH-1,-N 2-propano-2 ′-deoxyguanosine. J. Biol. Chem., 276, 9077-9082.
126. Minko, I.G., Washington, M.T., Kanuri, M., Prakash, L., Prakash, S., and Lloyd, R.S. (2003) Translesion synthesis past acrolein-derived DNA adduct, γ-hydroxypropanodeoxyguanosine, by yeast and human DNA polymerase η. J. Biol. Chem., 278, 784-790.
127. Nair, D.T., Johnson, R.E., Prakash, L., Prakash, S., and Aggarwal, A.K. (2008) Protein-template-directed synthesis across an acrolein-derived DNA adduct by yeast Rev1 DNA polymerase. Structure, 16, 239-245.
128. Washington, M.T., Minko, I.G., Johnson, R.E., Wolfle, W.T., Harris, T.M., Lloyd, R.S., Prakash, S., and Prakash, L. (2004) Efficient and error-free replication past a minor-groove DNA adduct by the sequential action of human DNA polymerases ι and κ. Mol. Cell. Biol., 24, 5687-5693.
129. Wang, Y., Musser, S.K., Saleh, S., Marnett, L.J., Egli, M., and Stone, M.P. (2008) Insertion of dNTPs opposite the 1, N 2-propanodeoxyguanosine adduct by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry, 47, 7322-7334.
130. Basu, A.K., Niedernhofer, L.J., and Essigmann, J.M. (1987) Deoxyhexanucleotide containing a vinyl chloride induced DNA lesion, 1, N 6-ethenoadenine: synthesis, physical characterization, and incorporation into a duplex bacteriophage M13 genome as part of an amber codon. Biochemistry, 26, 5626-5635.
131. Basu, A.K., Wood, M.L., Niedernhofer, L.J., Ramos, L.A., and Essigmann, J.M. (1993) Mutagenic and genotoxic effects of three vinyl chloride-induced DNA lesions: 1, N 6-ethenoadenine, 3, N 4-ethenocytosine, and 4-amino-5-(imidazol-2-yl) imidazole. B iochemistry, 32, 12793-12801.
132. Müller, M., Belas, F.J., Blair, I.A., and Guengerich, F.P. (1997) Analysis of 1, N 2-ethenoguanine and 5,6,7,9-tetrahydro-7-hydroxy-9-oxoimidazo[1,2-α ]purine in DNA treated with 2-chlorooxirane by high performance liquid chromatography/electrospray mass spectrometry and comparison of amounts to other DNA adducts. Chem. Res. Toxicol., 10, 242-247.
133. Cheng, K.C., Preston, B.D., Cahill, D.S., Dosanjh, M.K., Singer, B., and Loeb, L.A. (1991) The vinyl chloride DNA derivative N 2,3-ethenoguanine produces G → A transitions in Escherichia coli. Proc. Natl. Acad. Sci. USA, 88, 9974-9978.
134. Kusmierek, J.T., Folkman, W., and Singer, B. (1989) Synthesis of N 2,3-ethenodeoxyguanosine, N 2,3-ethenodeoxyguanosine 5 ′-phosphate, and N 2,3-ethenodeoxyguanosine 5 ′-triphosphate. Stability of the glycosyl bond in the monomer and in poly(dG, epsilon dG-dC). Chem. Res. Toxicol., 2, 230-233.
135. Lawley, P.D. (1984) Carcinogenesis by alkylating agents, in Chemical Carcinogens, 2nd edn (ed. C.E. Searle), ACS Monograph 182, American Chemical Society, Washington, DC, pp. 325-484.
136. Loveless, A. (1969) Possible relevance of O 6 alkylation of deoxyguanosine to the mutagenicity and carcinogenicity of nitrosamines and nitrosamides. Nature, 223, 206-207.
137. Singer, B. and Kusmierek, J.T. (1982) Chemical mutagenesis. Annu. Rev. Biochem., 51, 655-693.
138. Lawley, P.D. and Brookes, P. (1961) Acidic dissociation of 7 : 9-dialkylguanines and its possible relation to mutagenic properties of alkylating agents. Nature, 192, 1081-1082.
139. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Shultz, R.A., and Ellenberger, T. (2006) DNA Repair and Mutagenesis, 2nd edn, ASM Press, Washington, DC.
140. Margison, G.P., Santibanez Koref, M.F., and Povey, A.C. (2002) Mechanisms of carcinogenicity/chemotherapy by O 6-methylguanine. Mutagenesis, 17, 483-487.
141. Wyatt, M.D. and Pittman, D.L. (2006) Methylating agents and DNA repair responses: methylated bases and sources of strand breaks. Chem. Res. Toxicol., 19, 1580-1594.
142. Grafstrom, R.C., Pegg, A.E., Trump, B.F., and Harris, C.C. (1984) O 6-alkylguanine-DNA alkyltransferase activity in normal human tissues and cells. Cancer Res., 44, 2855-2857.
143. Pegg, A.E., Roberfroid, M., von Bahr, C., Foote, R.S., Mitra, S., Bresil, H., Likhachev, A., and Montesano, R. (1982) Removal of O 6-methylguanine from DNA by human liver fractions. Proc. Natl. Acad. Sci. USA, 79, 5162-5165.
144. Pegg, A.E., Scicchitano, D., Morimoto, K., and Dolan, M.E. (1987) Specificity of O 6-alkylguanine-DNA alkyltransferase. IARC Sci. Publ., 84, 30-34.
145. Shen, L., Kondo, Y., Rosner, G.L., Xiao, L., Hernandez, N.S., Vilaythong, J., Houlihan, P.S., Krouse, R.S., et al. (2005) MGMT promoter methylation and field defect in sporadic colorectal cancer. J. Natl. Cancer Inst., 97, 1330-1338.
146. Essigmann, J.M., Loechler, E.L., and Green, C.L. (1986) Mutagenesis and repair of O 6-substituted guanines. IARC Sci. Publ., 70, 393-399.
147. Essigmann, J.M., Loechler, E.L., and Green, C.L. (1986) Genetic toxicology of O 6 methylguanine. Prog. Clin. Biol. Res., 209A, 433-440.
148. Loechler, E.L., Green, C.L., and Essigmann, J.M. (1984) In vivo mutagenesis by O 6-methylguanine built into a unique site in a viral genome. Proc. Natl. Acad. Sci. USA, 81, 6271-6275.
149. Choi, J.Y., Chowdhury, G., Zang, H., Angel, K.C., Vu, C.C., Peterson, L.A., and Guengerich, F.P. (2006) Translesion synthesis across O 6-alkylguanine DNA adducts by recombinant human DNA polymerases. J. Biol. Chem., 281, 38244-38256.
150. Eoff, R.L., Irimia, A., Egli, M., and Guengerich, F.P. (2007) Sulfolobus solfataricus DNA polymerase Dpo4 is partially inhibited by " wobble " pairing between O 6-methylguanine and cytosine, but accurate bypass is preferred. J. Biol. Chem., 282, 1456-1467.
151. Woodside, A.M. and Guengerich, F.P. (2002) Effect of the O 6 substituent on misincorporation kinetics catalyzed by DNA polymerases at O 6-methylguanine and O 6-benzylguanine. Biochemistry, 41, 1027-1038.
152. Woodside, A.M. and Guengerich, F.P. (2002) Misincorporation and stalling at O 6-methylguanine and O 6-benzylguanine: evidence for inactive polymerase complexes. Biochemistry, 41, 1039-1050.
153. Ginell, S.L., Kuzmich, S., Jones, R.A., and Berman, H.M. (1990) Crystal and molecular structure of a DNA duplex containing the carcinogenic lesion O 6-methylguanine. Biochemistry, 29, 10461-10465.
154. Patel, D.J., Shapiro, L., Kozlowski, S.A., Gaffney, B.L., and Jones, R.A. (1986) Structural studies of the O 6 MeG · C interaction in the d(C-G-C-G-A-A-T-T-C-O 6 MeG-C-G) duplex. Biochemistry, 25, 1027-1036.
155. Patel, D.J., Shapiro, L., Kozlowski, S.A., Gaffney, B.L., and Jones, R.A. (1986) Structural studies of the O 6 MeG · T interaction in the d(C-G-T-G-A-A-T-T-C-O 6 MeG-C-G) duplex. Biochemistry, 25, 1036-1042.
156. Sriram, M., van der Marel, G.A., Roelen, H.L., van Boom, J.H., and Wang, A.H. (1992) Structural consequences of a carcinogenic alkylation lesion on DNA: effect of O 6-ethylguanine on the molecular structure of the d(CGC[e6G]AATTCGCG)-netropsin complex. B iochemistry, 31, 11823-11834.
157. Gaffney, B.L. and Jones, R.A. (1989) Thermodynamic comparison of the base pairs formed by the carcinogenic lesion O 6-methylguanine with reference both to Watson-Crick pairs and to mismatched pairs. Biochemistry, 28, 5881-5889.
158. Warren, J.J., Forsberg, L.J., and Beese, L.S. (2006) The structural basis for the mutagenicity of O 6-methyl-guanine lesions. Proc. Natl. Acad. Sci. USA, 103, 19701-19706.
159. Eoff, R.L., Angel, K.C., Egli, M., and Guengerich, F.P. (2007) Molecular basis of selectivity of nucleoside triphosphate incorporation opposite O 6-benzylguanine by Sulfolobus solfataricus DNA polymerase Dpo4: steady-state and pre-steady-state kinetics and X-ray crystallography of correct and incorrect pairing. J. Biol. Chem., 282, 13573-13584.
160. Phillips, D.H. (1983) Fifty years of benzo[ a ]pyrene. Nature, 303, 468-472.
161. Cosman, M., de los Santos, C., Fiala, R., Hingerty, B.E., Singh, S.B., Ibanez, V., Margulis, L.A., Live, D., et al. (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[ a ]pyrene diol epoxide and DNA. Proc. Natl. Acad. Sci. USA, 89, 1914-1918.
162. Graslund, A. and Jernstrom, B. (1989) DNA-carcinogen interaction: covalent DNA-adducts of benzo[ a ]pyrene 7,8-dihydrodiol 9,10-epoxides studied by biochemical and biophysical techniques. Q. Rev. Biophys., 22, 1-37.
163. Alekseyev, Y.O., Dzantiev, L., and Romano, L.J. (2001) Effects of benzo[ a ] pyrene DNA adducts on Escherichia coli DNA polymerase I (Klenow fragment) primer-template interactions: evidence for inhibition of the catalytically active ternary complex formation. Biochemistry, 40, 2282-2290.
164. Alekseyev, Y.O. and Romano, L.J. (2000) In vitro replication of primer-templates containing benzo[ a ]pyrene adducts by exonuclease-deficient Escherichia coli DNA polymerase I (Klenow fragment): effect of sequence context on lesion bypass. Biochemistry, 39, 10431-10438.
165. Alekseyev, Y.O. and Romano, L.J. (2002) Effects of benzo[ a ]pyrene adduct stereochemistry on downstream DNA replication in vitro : evidence for different adduct conformations within the active site of DNA polymerase I (Klenow fragment). Biochemistry, 41, 4467-4479.
166. Hruszkewycz, A.M., Canella, K.A., Peltonen, K., Kotrappa, L., and Dipple, A. (1992) DNA polymerase action on benzo[ a ]pyrene-DNA adducts. Carcinogenesis, 13, 2347-2352.
167. Hsu, G.W., Huang, X., Luneva, N.P., Geacintov, N.E., and Beese, L.S. (2005) Structure of a high fidelity DNA polymerase bound to a benzo[ a ]pyrene adduct that blocks replication. J. Biol. Chem., 280, 3764-3770.
168. Rechkoblit, O., Zhang, Y., Guo, D., Wang, Z., Amin, S., Krzeminsky, J., Louneva, N., and Geacintov, N.E. (2002) trans-Lesion synthesis past bulky benzo[ a ]pyrene diol epoxide N 2-dG and N 6-dA lesions catalyzed by DNA bypass polymerases. J. Biol. Chem., 277, 30488-30494.
169. Shibutani, S., Margulis, L.A., Geacintov, N.E., and Grollman, A.P. (1993) Translesional synthesis on a DNA template containing a single stereoisomer of dG-(+)-or dG-(-)-anti-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[ a ]pyrene). Biochemistry, 32, 7531-7541.
170. Feng, B., Gorin, A., Hingerty, B.E., Geacintov, N.E., Broyde, S., and Patel, D.J. (1997) Structural alignment of the (+)-trans-anti-benzo[ a ]pyrene-dG adduct positioned opposite dC at a DNA template-primer junction. B iochemistry, 36, 13769-13779.
171. Bauer, J., Xing, G., Yagi, H., Sayer, J.M., Jerina, D.M., and Ling, H. (2007) 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.
172. Ling, H., Sayer, J.M., Plosky, B.S., Yagi, H., Boudsocq, F., Woodgate, R., Jerina, D.M., and Yang, W. (2004) Crystal structure of a benzo[ a ]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase. Proc. Natl. Acad. Sci. USA, 101, 2265-2269.
173. Ogi, T., Shinkai, Y., Tanaka, K., and Ohmori, H. (2002) Pol κ protects mammalian cells against the lethal and mutagenic effects of benzo[ a ]pyrene. Proc. Natl. Acad. Sci. USA, 99, 15548-15553.
174. Suzuki, N., Ohashi, E., Kolbanovskiy, A., Geacintov, N.E., Grollman, A.P., Ohmori, H., and Shibutani, S. (2002) Translesion synthesis by human DNA polymerase κ on a DNA template containing a single stereoisomer of dG-(+)-or dG-(-)-anti-N 2-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[ a ]pyrene). Biochemistry, 41, 6100-6106.
175. Choi, J.Y., Angel, K.C., and Guengerich, F.P. (2006) Translesion synthesis across bulky N 2-alkyl guanine DNA adducts by human DNA polymerase κ. J. Biol. Chem., 281, 21062-21072.
176. Choi, J.Y. and Guengerich, F.P. (2004) Analysis of the effect of bulk at N 2-alkylguanine DNA adducts on catalytic efficiency and fidelity of the processive DNA polymerases bacteriophage T7 exonuclease-and HIV-1 reverse transcriptase. J. Biol. Chem., 279, 19217-19229.
177. Choi, J.Y. and Guengerich, F.P. (2005) Adduct size limits efficient and error-free bypass across bulky N 2-guanine DNA lesions by human DNA polymerase η. J. Mol. Biol., 352, 72-90.
178. Choi, J.Y. and Guengerich, F.P. (2006) Kinetic evidence for inefficient and error-prone bypass across bulky N 2-guanine DNA adducts by human DNA polymerase ι. J. Biol. Chem., 281, 12315-12324.
179. Choi, J.Y. and Guengerich, F.P. (2008) Kinetic analysis of translesion synthesis opposite bulky N 2-and O 6-alkylguanine DNA adducts by human DNA polymerase REV1. J. Biol. Chem., 283, 23645-23655.
180. Zang, H., Harris, T.M., and Guengerich, F.P. (2005) Kinetics of nucleotide incorporation opposite DNA bulky guanine N2 adducts by processive bacteriophage T7 DNA polymerase (exonuclease-) and HIV-1 reverse transcriptase. J. Biol. Chem., 280, 1165-1178.
181. Cross, A.J., Pollock, J.R., and Bingham, S.A. (2002) Red meat and colorectal cancer risk: the effect of dietary iron and haem on endogenous N-nitrosation. IARC Sci. Publ., 156, 205-206.
182. Cross, A.J. and Sinha, R. (2004) Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ. Mol. Mutagen., 44, 44-55.
183. Sinha, R., Peters, U., Cross, A.J., Kulldorff, M., Weissfeld, J.L., Pinsky, P.F., Rothman, N., and Hayes, R.B. (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res., 65, 8034-8041.
184. Lemee, F., Bavoux, C., Pillaire, M.J., Bieth, A., Machado, C.R., Pena, S.D., Guimbaud, R., Selves, J., et al. (2007) Characterization of promoter regulatory elements involved in downexpression of the DNA polymerase κ in colorectal cancer. Oncogene, 26, 3387-3394.
185. Mouret, S., Baudouin, C., Charveron, M., Favier, A., Cadet, J., and Douki, T. (2006) Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl. Acad. Sci. USA, 103, 13765-13770.
186. Douki, T. and Cadet, J. (2001) Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions. Biochemistry, 40, 2495-2501.
187. Washington, M.T., Prakash, L., and Prakash, S. (2003) Mechanism of nucleotide incorporation opposite a thymine-thymine dimer by yeast DNA polymerase η. Proc. Natl. Acad. Sci. USA, 100, 12093-12098.
188. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., et al. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature, 399, 700-704.
189. Lehmann, A.R., Kirk-Bell, S., Arlett, C.F., Paterson, M.C., Lohman, P.H., de Weerd-Kastelein, E.A., and Bootsma, D. (1975) 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.
190. Limoli, C.L., Giedzinski, E., Bonner, W.M., and Cleaver, J.E. (2002) UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, γ-H2AX formation, and Mre11 relocalization. Proc. Natl. Acad. Sci. USA, 99, 233-238.
191. Lin, Q., Clark, A.B., McCulloch, S.D., Yuan, T., Bronson, R.T., Kunkel, T.A., and Kucherlapati, R. (2006) Increased susceptibility to UV-induced skin carcinogenesis in polymerase η-deficient mice. Cancer Res., 66, 87-94.
192. Maher, V.M., Ouellette, L.M., Curren, R.D., and McCormick, J.J. (1976) Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells. Nature, 261, 593-595.
193. Misra, R.R. and Vos, J.M. (1993) Defective replication of psoralen adducts detected at the gene-specific level in xeroderma pigmentosum variant cells. Mol. Cell. Biol., 13, 1002-1012.
194. Wang, Y.C., Maher, V.M., and McCormick, J.J. (1991) Xeroderma pigmentosum variant cells are less likely than normal cells to incorporate dAMP opposite photoproducts during replication of UV-irradiated plasmids. Proc. Natl. Acad. Sci. USA, 88, 7810-7814.
195. Waters, H.L., Seetharam, S., Seidman, M.M., and Kraemer, K.H. (1993) Ultraviolet hypermutability of a shuttle vector propagated in xeroderma pigmentosum variant cells. J. Invest. Dermatol., 101, 744-748.
196. Dumstorf, C.A., Clark, A.B., Lin, Q., Kissling, G.E., Yuan, T., Kucherlapati, R., McGregor, W.G., and Kunkel, T.A. (2006) Participation of mouse DNA polymerase ι in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc. Natl. Acad. Sci. USA, 103, 18083-18088.
197. Ling, H., Boudsocq, F., Plosky, B.S., Woodgate, R., and Yang, W. (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature, 424, 1083-1087.
198. Li, Y., Dutta, S., Doublié, S., Bdour, H.M., Taylor, J.S., and Ellenberger, T. (2004) Nucleotide insertion opposite a cis-syn thymine dimer by a replicative DNA polymerase from bacteriophage T7. Nat. Struct. Mol. Biol., 11, 784-790.
199. Taylor, J.S., Garrett, D.S., and Cohrs, M.P. (1988) Solution-state structure of the Dewar pyrimidinone photoproduct of thymidylyl-(3 ′ → 5 ′)-thymidine. Biochemistry, 27, 7206-7215.
200. Johnson, R.E., Haracska, L., Prakash, S., and Prakash, L. (2001) Role of DNA polymerase ζ in the bypass of a (6-4) TT photoproduct. Mol. Cell Biol., 21, 3558-3563.
201. Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S., and Prakash, L. (2000) Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature, 406, 1015-1019.
202. Minko, I.G., Harbut, M.B., Kozekov, I.D., Kozekova, A., Jakobs, P.M., Olson, S.B., Moses, R.E., Harris, T.M., et al. (2008) Role for DNA polymerase κ in the processing of N 2-N 2-guanine interstrand cross-links. J. Biol. Chem., 283, 17075-17082.
203. Kumari, A., Minko, I.G., Harbut, M.B., Finkel, S.E., Goodman, M.F., and Lloyd, R.S. (2008) Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J. Biol. Chem., 283, 27433-27437.
204. Cole, R.S. (1973) Repair of DNA containing interstrand crosslinks in Escherichia coli : sequential excision and recombination. Proc. Natl. Acad. Sci. USA, 70, 1064-1068.
205. van Houten, B. (1990) Nucleotide excision repair in Escherichia coli. Microbiol. Rev., 54, 18-51.
206. Marini, F., Kim, N., Schuffert, A., and Wood, R.D. (2003) POLN, a nuclear PolA family DNA polymerase homologous to the DNA cross-link sensitivity protein Mus308. J. Biol. Chem., 278, 32014-32019.
207. Marini, F. and Wood, R.D. (2002) A human DNA helicase homologous to the DNA cross-link sensitivity protein Mus308. J. Biol. Chem., 277, 8716-8723.
208. Boyd, J.B., Sakaguchi, K., and Harris, P.V. (1990) Mus308 mutants of Drosophila exhibit hypersensitivity to DNA cross-linking agents and are defective in a deoxyribonuclease. Genetics, 125, 813-819.
209. Zan, H., Shima, N., Xu, Z., Al-Qahtani, A., Evinger Iii, A.J., Zhong, Y., Schimenti, J.C., and Casali, P. (2005) The translesion DNA polymerase θ plays a dominant role in immunoglobulin gene somatic hypermutation. EMBO J., 24, 3757-3769.
210. Alt, A., Lammens, K., Chiocchini, C., Lammens, A., Pieck, J.C., Kuch, D., Hopfner, K.P., and Carell, T. (2007) Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase η. Science, 318, 967-970.
211. Bruning, J.B. and Shamoo, Y. (2004) Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-δ p66 subunit and flap endonuclease-1. Structure, 12, 2209-2219.
212. Bunting, K.A., Roe, S.M., and Pearl, L.H. (2003) Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the β-clamp. EMBO J., 22, 5883-5892.
213. Shamoo, Y. and Steitz, T.A. (1999) Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell, 99, 155-166.
214. Eoff, R.L., Stafford, J.B., Szekely, J., Rizzo, C.J., Egli, M., Guengerich, F.P., and Marnett, L.J. (2009) Structural and functional analysis of Sulfolobus solfataricus Y-family DNA polymerase Dpo4-catalyzed bypass of the malondialdehyde-deoxyguanosine adduct. Biochemistry, 48, 7079-7088.
215. Stafford, J.B., Eoff, R.L., Kozekova, A., Rizzo, C.J., Guengerich, F.P., and Marnett, L.J. (2009) Translesion DNA synthesis by human DNA polymerase η on templates containing a pyrimidopurinone deoxyguanosine adduct, 3-(2 ′-deoxy-β-D-erythro-pentofuranosyl) pyrimido-[1,2-a ]purin-10(3 H) one. Biochemistry, 48, 471-480.