DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 2, 2013, Pages

  Cadet, Jean ^a,b   Richard Wagner, J ^b  

^a CEA GRENOBLE   (France)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CHEMISTRY; DNA ADDUCT; DNA DAMAGE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; OXIDATION REDUCTION REACTION; ULTRAVIOLET RADIATION;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA ADDUCTS; DNA DAMAGE; MASS SPECTROMETRY; NUCLEOTIDES; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; ULTRAVIOLET RAYS;

EID: 84875185107     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a012559     Document Type: Article

References (131)

1. Aida M, Nishimura S. 1987. An ab initio molecular orbital study on the characteristics of 8-hydroxyguanine. Mut Res Lett 192: 83-89.
2. Asahi T, Kondo H, Masuda M, Nishino H, Aratani Y, Naito Y, Yoshikawa T, Hisaka S, Kato Y, Osawa T. 2010. Chemical and immunochemical detection of 8-halogenated deoxyguanosines at early stage inflammation. J Biol Chem 285: 9282-9291.
3. Asgatay S, Martinez A, Coantic-Castex S, Harakat D, Philippe C, Douki T, Clivio P. 2010. UV-induced TA photoproducts: Formation and hydrolysis in double-stranded DNA. J Am Chem Soc 132: 10260-10261.
4. Azqueta A, Shaposhnikov S, Collins AR. 2009. DNA oxidation: Investigating its key role in mutagenesis with the comet assay. Mutat Res 674: 101-108.
5. Badouard C, Masuda M, Nishino H, Cadet J, Favier A, Ravanat JL. 2005. Detection of chlorinated DNA and RNA nucleosides by HPLC coupled to tandem mass spectrometry as potential biomarkers of inflammation. J Chromatogr B 827: 26-31.
6. Banyasz A, Vayá I, Changenet-Barret P, Gustavsson T, Douki T, Markovitsi D. 2011. Base pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA. J Am Chem Soc 133: 5163-5165.
7. Bellon S, Gasparutto D, Saint-Pierre C, Cadet J. 2006. Guanine-thymine intrastrand cross-linked lesion containing oligonucleotides: From chemical synthesis to in vitro enzymatic replication. Org Biomol Chem 4: 3831-3837.
8. 0,8-cyclonucleosides in isolated and cellular DNA: High stereospecificity and modulating effect of oxygen. Org Biomol Chem 8: 3211-3219.
9. † radicals induce an unexpected high proportion of tandem base lesions refractory to repair by DNA glycosylases. Proc Natl Acad Sci 107: 5528-5533.
10. Bhattacharjee S, Deterding LJ, Chatterjee S, Jiang J, Ehrenshaft M, Lardinois O, Ramirez DC, Tomer KB, Mason RP. 2011. Site-specific radical formation in DNA induced by Cu(II)-H2O2 oxidizing system, using ESR, immuno-spin trapping, LC-MS, and MS/MS. Free Radic Biol Med 50: 1536-1545.
11. Bhattacharjee S, Chatterjee S, Jiang J, Sinha BK, Mason RP. 2012. Detection and imaging of the free radical DNA in cells: Site-specific radical formation induced by Fenton chemistry and its repair in cellular DNA as seen by electron spin resonance, immuno-spin trapping and confocal microscopy. Nucleic Acids Res 40: 5477-5486.
12. 0-deoxycytidine and stable methyl group oxidation products. J Am Chem Soc 118: 11406-11411.
13. Bourdat AG, Douki T, Frelon S, Gasparutto D, Cadet J. 2000. Tandem base lesions are generated by hydroxyl radical within isolated DNA in aerated aqueous solution. J Am Chem Soc 122: 4549-4556.
14. Box HC, Budzinski EE, Freund HG, Evans MS, Patrzyc HB, Wallace JC, MacCubbin AE. 1993. Vicinal lesions in Xirradiated DNA? Int J Radiat Biol 64: 261-263.
15. Brem R, Karran P. 2012. Multiple forms of DNA damage caused by UVA photoactivation of DNA 6-thioguanine. Photochem Photobiol 88: 5-13.
16. Brem R, Daehn I, Karran P. 2011. Efficient DNA interstrand crosslinking by 6-thioguanine and UVA radiation. DNA Repair 10: 869-876.
17. Burrows CJ. 2009. Surviving an oxygen atmosphere: DNA damage and repair. ACS Symp Ser Am Chem Soc 2009: 145-156.
18. Cadet J, Douki T. 2011. Oxidatively generated damage to DNA by UVA radiation in cells and human skin. J Invest Dermat 131: 1005-1007.
19. 0-deoxyguanosine. J Am Chem Soc 116: 7403-7404.
20. Cadet J, Douki T, Ravanat JL. 2008. Oxidatively generated damage to the guanine moiety of DNA: Mechanistic aspects and formation in cells. Acc Chem Res 41: 1075-1083.
21. Cadet J, Douki T, Ravanat JL, Di Mascio P. 2009. Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochem Photobiol Sci 8: 903-911.
22. Cadet J, Douki T, Ravanat JL. 2010. Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49: 9-21.
23. Cadet J, Douki T, Ravanat JL. 2011. Measurement of oxidatively generated base damage in cellular DNA. Mutat Res 711: 3-12.
24. Cadet J, Douki T, Ravanat JL, Wagner JR. 2012. Measurement of oxidatively generated base damage to nucleic acids in cells: facts and artifacts. Bioanal Rev 4: 55-74.
25. Cadet J, Douki T, Gasparutto D, Ravanat JL, Wagner JR. 2012. Oxidatively generated nucleobase modifications in isolated and cellular DNA (ed. Chatgilialoglu C, Studer A), pp. 1319-1344. John Wiley & Sons, Chichester, UK.
26. Cadet J, Mouret S, Ravanat JL, Douki T. 2012c. Photo-induced damage to cellular DNA: Direct and photosensitized reactions. Photochem Photobiol 88: 1048-1065.
27. Cadet J, Loft S, Olinski R, Evans MD, Bialkowski K, Wagner JR, Dedon PC, Møller P, Greenberg MM, Cooke MS. 2012. Biologically relevant oxidants and terminology, classification and nomenclature of oxidatively generated damage to nucleobases and 2-deoxyribose in nucleic acids. Free Radic Res 46: 367-381.
28. Cadet J, Ravanat JL, Tavernaporro M, Menoni H, Angelov D. 2012. Oxidatively generated complex DNA damage: Tandem and clustered lesions. Cancer Lett 327: 5-15.
29. †. Chem A Eur J 6: 475-484.
30. Cao H, Jiang Y, Wang Y. 2009. Kinetics of deamination and Cu(II)/H2O2/Ascorbate-induced formation of 5-methylcytosine glycol at CpG sites in duplex DNA. Nucleic Acids Res 37: 6635-6643.
31. 0-deoxyguanosine. Chem Res Toxicol 24: 2200-2206.
32. 0,8cyclonucleoside lesions: Chemistry and biology. Chem Soc Rev 40: 1368-1382.
33. 0-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides. Chem Res Toxicol 3: 445-452.
34. Cooke MS, Olinski R, Loft S.2008. Measurement and meaning of oxidatively modified DNA lesions in urine. Cancer Epidemiol Biomark Prev 17: 3-14.
35. Cooke MS, Loft S, Olinski R, Evans MD, Bialkowski K, Wagner JR, Dedon PC, Møller P, Greenberg MM, Cadet J. 2010. Recommendations for standardized description of and nomenclature concerning oxidatively damaged nucleobases in DNA. Chem Res Toxicol 23: 705-707.
36. Courdavault S, Baudouin C, Sauvaigo S, Mouret S, Candéias S, Charveron M, Favier A, Cadet J, Douki T. 2004. Unrepaired cyclobutane pyrimidine dimers do not prevent proliferation of UV-B-irradiated cultured human fibroblasts. Photochem Photobiol 79: 145-151.
37. Courdavault S, Baudouin C, Charveron M, Canguilhem B, Favier A, Cadet J, Douki T. 2005. Repairof the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations. DNA Repair 4: 836-844.
38. 0-deoxyguanosine. Chem Res Toxicol 2: 416-422.
39. Davies RJH, Malone JF, Gan Y, Cardin CJ, Lee MPH, Neidle S. 2007. High-resolution crystal structure of the intramolecular d(TpA) thymine-adenine photoadduct and its mechanistic implications. Nucleic Acids Res 35: 1048-1053.
40. Dedon PC. 2008. The chemical toxicology of 2-deoxyribose oxidation in DNA. Chem Res Toxicol 21: 206-219.
41. D'Errico M, Parlanti E, Teson M, De Jesus BMB, Degan P, Calcagnile A, Jaruga P, Bjørås M, Crescenzi M, Pedrini AM, et al. 2006. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J 25: 4305-4315.
42. Derrico M, Parlanti E, Teson M, Degan P, Lemma T, Calcagnile A, Iavarone I, Jaruga P, Ropolo M, Pedrini AM, et al. 2007. The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 26: 4336-4343.
43. Ding S, Kropachev K, Cai Y, Kolbanovskiy M, Durandina SA, Liu Z, Shafirovich V, Broyde S, Geacintov NE. 2012. Structural, energetic and dynamic properties of guanine(C8)-thymine(N3) cross-links in DNA provide insights on susceptibility to nucleotide excision repair. Nucleic Acids Res 40: 2506-2517.
44. Douki T, 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.
45. Douki T, Perdiz D, Gróf P, Kuluncsics Z, Moustacchi E, Cadet J, Sage E. 1999. Oxidation of guanine in cellular DNA by solar UV radiation: Biological role. Photochem Photobiol 70: 184-190.
46. Douki T, Court M, Sauvaigo S, Odin F, Cadet J. 2000. Formation of the main UV-induced thymine dimeric lesions within isolated and cellular DNA as measured by high performance liquid chromatography-tandem mass spectrometry. J Biol Chem 275: 11678-11685.
47. Douki T, Angelov D, Cadet J. 2001. UV laser photolysis of DNA: Effect of duplex stability on charge-transfer efficiency. J Am Chem Soc 123: 11360-11366.
48. Douki T, Rivière J, Cadet J. 2002. DNA tandem lesions containing 8-oxo-7,8-dihydroguanine and formamido residues arise from intramolecular addition of thymine peroxyl radical to guanine. Chem Res Toxicol 15: 445- 454.
49. 0deoxyuridine hydrates upon exposure of nucleosides to gamma radiation and UVC-irradiation of isolated and cellular DNA. Photochem Photobiol Sci 1: 565-569.
50. Douki T, Reynaud-Angelin A, Cadet J, Sage E. 2003. Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. Biochemistry 42: 9221-9226.
51. Douki T, Ravanat JL, Angelov D, Wagner JR, Cadet J. 2004. Effects of duplex stability on charge transfer efficiency within DNA. Topics Curr Chem 236: 1-25.
52. Douki T, Ravanat JL, Pouget JP, Testard I, Cadet J. 2006. Minor contribution of direct ionization to DNA base damage induced by heavy ions. Int J Radiat Biol 82: 119-127.
53. Frelon S, Douki T, Ravanat JL, Pouget JP, Tornabene C, Cadet J. 2000. High-performance liquid chromatography: Tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem Res Toxicol 13: 1002-1010.
54. 0deoxyadenosine is a minor decomposition product. Free Radical Res 36: 499-508.
55. Gasparutto D, Ravanat JL, Gérot O, Cadet J. 1998. Characterization and chemical stability of photooxidized oligonucleotides that contain 2,2-diamino-4-[(2-deoxy-b-Derythro-pentofuranosyl)amino]-5(2H)-oxazolone. J Am Chem Soc 120: 10283-10286.
56. Gimisis T, Cismaş C. 2006. Isolation, characterization, and independent synthesis of guanine oxidation products. Eur J Org Chem 2006: 1351-1378.
57. Gueranger Q, Kia A, Frith D, Karran P. 2011. Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA. Nucleic Acids Res 39: 5057-5066.
58. Haiser K, Fingerhut BP, Heil K, Glas A, Herzog TT, Pilles BM, Schreier WJ, Zinth W, Devivie-Riedle R, Carell T. 2012. Mechanism of UV-induced formation of Dewar lesions in DNA. Angew Chem Int Ed 51: 408-411.
59. Halliday GM, Cadet J. 2012. It's all about position: The basal layer of human epidermis is particularly susceptible to different types of sunlight-induced DNA damage. J Invest Dermat 132: 265-267.
60. Hawkins CL, Davies MJ. 2001. Hypochlorite-induced damage to nucleosides: Formation of chloramines and nitrogen-centered radicals. Chem Res Toxicol 14: 1071-1081.
61. Hawkins CL, Davies MJ. 2002. Hypochlorite-induced damage to DNA, RNA, and polynucleotides: Formation of chloramines and nitrogen-centered radicals. Chem Res Toxicol 15: 83-92.
62. In SH, Carter KN, Sato K, Greenberg MM. 2007. Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical. J Am Chem Soc 129: 4089-4098.
63. Iqbal K, Jin SG, Pfeifer GP, Szabó PE. 2011. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci 108: 3642-3647.
64. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303.
65. 0-deoxyadenosines in DNA in vivo by liquid chromatography/isotope-dilution tandem mass spectrometry. Biochem Biophys Res Commun 386: 656-660.
66. Jiang Y, Hong H, Cao H, Wang Y. 2007. In vivo formation and invitro replication of a guanine-thymine intrastrand cross-link lesion. Biochemistry 46: 12757-12763.
67. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, Schackert G, Krex D, Lu Q, Pfeifer GP. 2011. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlatewith IDH1 mutations. Cancer Res 71: 7360-7365.
68. Kasai K, Nishimura S. 1983. Hydroxylation of deoxyguanosine by reducing agents in the presence of oxygen. Nucleic Acids Symp Ser 12: 165-167.
69. Kawanishi S, Murata M. 2006. Mechanism of DNA damage induced by bromate differs from general types of oxidative stress. Toxicology 221: 172-178.
70. Kielbassa C, Roza L, Epe B. 1997. Wavelength dependence of oxidative DNA damage induced by UVand visible light. Carcinogenesis 18: 811-816.
71. Kouchakdjian M, Bodepudi V, Shibutani S, Eisenberg M, Johnson F, Grollman AP, Patel DJ. 1991. NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn) dA(anti) †alignment at lesion site. Biochemistry 30: 1403-1412.
72. Kraus TF, Globisch D, Wagner M, Eigenbrod S, Widmann D, Münzel M, Müller M, Pfaffeneder T, Hackner B, Feiden W, et al. 2012. Low values of 5-hydroxymethylcytosine (5hmC), the "sixth base," are associated with anaplasia in human brain tumors. Int J Cancer 131: 1577-1590.
73. Kriaucionis S, Heintz N. 2009. The nuclear DNA base 5hydroxymethylcytosine is present in purkinje neurons and the brain. Science 324: 929-930.
74. 0 -deoxyadenosine N6-aminyl radicals from the photolysis of phenylhydrazone derivatives. Chem Res Toxicol 23: 48-54.
75. Lee YA, Yun BH, Kim SK, Margolin Y, Dedon PC, Geacintov NE, Shafirovich V. 2007. Mechanisms of oxidation of guanine in DNA by carbonate radical anion, a decomposition product of nitrosoperoxycarbonate. Chem A Eur J 13: 4571-4581.
76. Lenton KJ, Therriault H, Fülöp T, Payette H, Wagner JR. 1999. Glutathione and ascorbate are negatively correlated with oxidative DNA damage in human lymphocytes. Carcinogenesis 20: 607-613.
77. Malle E, Furtmüller PG, Sattler W, Obinger C. 2007. Myeloperoxidase: A target for new drug development? Br J Pharmacol 152: 838-854.
78. Masuda M, Suzuki T, Friesen MD, Ravanat JL, Cadet J, Pignatelli B, Nishino H, Ohshima H. 2001. Chlorination of guanosine and other nucleosides byhypochlorous acid and myeloperoxidase of activated human neutrophils: Catalysis by nicotine and trimethylamine. J Biol Chem 276: 40486-40496.
79. Matter B, Malejka-Giganti D, Csallany AS, Tretyakova N. 2006. Quantitative analysis of the oxidative DNA lesion, 2,2-diamino-4-(2-deoxy-b-D-erythro-pentofuranosyl) amino]-5(2H)-oxazolone (oxazolone), in vitro and in vivo by isotope dilution-capillary HPLC-ESI-MS/MS. Nucleic Acids Res 34: 5449-5460.
80. Medinas DB, Cerchiaro G, Trindade DF, Augusto O. 2007. The carbonate radical and related oxidants derived from bicarbonate buffer. IUBMB Life 59: 255-262.
81. Misiaszek R, Crean C, Joffe A, Geacintov NE, Shafirovich V. 2004. Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J Biol Chem 279: 32106-32115.
82. Mori T, Dizdaroglu M. 1994. Ionizing radiation causes greater DNA base damage in radiation-sensitive mutant M10 cells than in parent mouse lymphoma L5178Y cells. Radiat Res 140: 85-90.
83. Mouret S, Baudouin C, Charveron M, Favier A, Cadet J, Douki T. 2006. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc Natl Acad Sci 103: 13765-13770.
84. Mouret S, Charveron M, Favier A, Cadet J, Douki T. 2008. Differential repair of UVB-induced cyclobutane pyrimidine dimers in cultured human skin cells and whole human skin. DNA Repair 7: 704-712.
85. Mouret S, Philippe C, Gracia-Chantegrel J, Banyasz A, Karpati S, Markovitsi D, Douki T. 2010. UVA-induced cyclobutane pyrimidine dimers in DNA: A direct photochemical mechanism? Org Biomol Chem 8: 1706-1711.
86. Mouret S, Leccia MT, Bourrain JL, Douki T, Beani JC. 2011. Individual photosensitivity of human skin and UVA-induced pyrimidine dimers in DNA. J Invest Dermat 131: 1539-1546.
87. Mouret S, Forestier A, Douki T.2012. The specificityofUVAinduced DNA damage in human melanocytes. Photochem Photobiol Sci 11: 155-162.
88. Münzel M, Globisch D, Brückl T, Wagner M, Welzmiller V, Michalakis S, Müller M, Biel M, Carell T. 2010. Quantification of the sixth DNA base hydroxymethylcytosine in the brain. Angew Chem Int Ed 49: 5375-5377.
89. Münzel M, Globisch D, Carell T. 2011. 5-hydroxymethylcytosine, the sixth base of the genome. Angew Chem Int Ed 50: 6460-6468.
90. Neeley WL, Essigmann JM. 2006. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 19: 491-505.
91. Nishimura S. 2011. 8-Hydroxyguanine: A base for discovery. DNA Repair (Amst) 10: 1078-1083.
92. Oda Y, Uesugi S, Ikehara M, Nishimura S, Kawase Y, Ishikawa H, Inoue H, Ohtsuka E. 1991. NMR studies of a DNA containing 8-hydroxydeoxyguanosine. Nucleic Acids Res 19: 1407-1412.
93. Perrier S, Hau J, Gasparutto D, Cadet J, Favier A, Ravanat JL. 2006. Characterization of lysine-guanine cross-links upon one-electron oxidation of a guanine-containing oligonucleotide in the presence of a trilysine peptide. J Am Chem Soc 128: 5703-5710.
94. Pfaffeneder T, Hackner B, Truß M, Münzel M, Müller M, Deiml CA, Hagemeier C, Carell T. 2011. The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew Chem Int Ed 50: 7008-7012.
95. Pfeifer GP, You YH, Besaratinia A. 2005. Mutations induced by ultraviolet light. Mutat Res 571: 19-31.
96. Pouget JP, Frelon S, Ravanat JL, Testard I, Odin F, Cadet J. 2002. Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles. Radiat Res 157: 589-595.
97. Pratviel G, Meunier B. 2006. Guanine oxidation: Oneand two-electron reactions. Chem A Eur J 12: 6018-6030.
98. Ravanat JL, Di Mascio P, Martinez GR, Medeiros MHG, Cadet J. 2000. Singlet oxygen induces oxidation of cellular DNA. J Biol Chem 275: 40601-40604.
99. Ravanat JL, Saint-Pierre C, Di Mascio P, Martinez GR, Medeiros MHG, Cadet J. 2001. Damage to isolated DNA mediated by singlet oxygen. Helv Chim Acta 84: 3702-3709.
100. Ravanat JL, Sauvaigo S, Caillat S, Martinez GR, Medeiros MHG, Di Mascio P, Favier A, Cadet J. 2004. Singlet oxygen-mediated damage to cellular DNA determined by the comet assay associated with DNA repair enzymes. Biol Chem 385: 17-20.
101. Regulus P, Spessotto S, Gateau M, Cadet J, Favier A, Ravanat JL. 2004. Detection of new radiation-induced DNA lesions by liquid chromatography coupled to tandem mass spectrometry. Rapid Commun Mass Spectrom 18: 2223-2228.
102. Regulus P, Duroux B, Bayle PA, Favier A, Cadet J, Ravanat JL. 2007. Oxidation of the sugar moiety of DNA by ionizing radiation or bleomycin could induce the formation of a cluster DNA lesion. Proc Natl Acad Sci 104: 14032-14037.
103. 0-deoxyuridine into isodialuric acid, dialuric acid, and hydantoin products. J Am Chem Soc 126: 6548-6549.
104. Rivière J, Klarskov K, Wagner JR. 2005. Oxidation of 5-hydroxypyrimidine nucleosides to 5-hydroxyhydantoin and its a-hydroxy-ketone isomer. Chem Res Toxicol 18: 1332-1338.
105. Rivière J, Ravanat JL, Wagner JR. 2006. Ascorbate and H2O2 induced oxidative DNA damage inJurkat cells. Free Radic Biol Med 40: 2071-2079.
106. Rizzo JL, Dunn J, Rees A, Rünger TM. 2011. No formation of DNA double-strand breaks and no activation of recombination repair with UVA. J Invest Dermat 131: 1139-1148.
107. Samson-Thibault F, Madugundu GS, Gao S, Cadet J, Wagner JR. 2012. Analysis of cytosine modifications in oxidized DNA by enzymatic digestion and HPLC-MS/ MS. Chem Res Toxicol 25: 1902-1911.
108. 0-oxidized abasic site. J Am Chem Soc 131: 11132-11139.
109. Sczepanski JT, Hiemstra CN, Greenberg MM. 2011. Probing DNA interstrand cross-link formation by an oxidized abasic site using nonnative nucleotides. Bioorg Med Chem 19: 5788-5793.
110. Sheu C, Foote CS. 1993. Endoperoxide formation in a guanosine derivative. J Am Chem Soc 115: 10446-10447.
111. Su DGT, Taylor JSA, Gross ML. 2010. A new photoproduct of 5-methylcytosine and adenine characterized by highperformance liquid chromatography and mass spectrometry. Chem Res Toxicol 23: 474-479.
112. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935.
113. Tewari A, Sarkany RP, Young AR. 2012. UVA1 induces cyclobutane pyrimidine dimers but not 6-4 photoproducts in human skin in vivo. J Invest Dermat 132: 394-400.
114. Trapp C, Reite K, Klungland A, Epe B. 2007. Deficiency of the Cockayne syndrome B (CSB) gene aggravates the genomic instability caused by endogenous oxidative DNA base damage in mice. Oncogene 26: 4044-4048.
115. Tremblay S, Wagner JR. 2008. Dehydration, deamination and enzymatic repair of cytosine glycols from oxidized poly(dG-dC) and poly(dI-dC). Nucleic Acids Res 36: 284-293.
116. 0 -Deoxycytidine glycols, a missing link in the free radical-mediated oxidation of DNA. J Biol Chem 274: 20833-20838.
117. 0-deoxycytidine to four interconverting diastereomersofN1carbamoyl-4,5-dihydroxy-2-oxoimidazolidine nucleosides. J Org Chem 72: 3672-3678.
118. Venkatatesmarlu D, Leszczynski J. 1998. Tautomerism equilibria in 8-oxopuirines: Implication for mutagenesis. J Comput Aided Mol Des 12: 373-382.
119. Vieira AJSC, Steenken S. 1990. Pattern of OH radical reaction with adenine and its nucleosides and nucleotides: Characterization of two typesof isomeric OH adduct and their unimolecular transformation reactions. J Am Chem Soc 112: 6986-6994.
120. von Sonntag C. 2006. Free-radical-induced DNA damage and its repair. Springer-Verlag, Berlin/Heidelberg.
121. Wagner JR, Cadet J. 2010. Oxidation reactions of cytosine DNA components by hydroxyl radical and one-electron oxidants in aerated aqueous solutions. Acc Chem Res 43: 564-571.
122. Wagner JR, Hu CC, Ames BN. 1992. Endogenous oxidative damage of deoxycytidine in DNA. Proc Natl Acad Sci 89: 3380-3384.
123. Wagner JR, van Lier JE, Berger M, Cadet J. 1994. Thymidine hydroperoxides: Structural assignment, conformational features, and thermal decompositioninwater. JAm Chem Soc 116: 2235-2242.
124. 0-deoxycytidine in aerated aqueous solutions. J Am Chem Soc 121: 4101-4110.
125. Wang Y, Taylor JS, Gross ML. 2001. Isolation and mass spectrometric characterization of dimeric adenine photo-products in oligodeoxynucleotides. Chem Res Toxicol 14: 738-745.
126. Wang J, Yuan B, Guerrero C, Bahde R, Gupta S, Wang Y. 2011. Quantification of oxidative DNA lesions in tissues of Long-Evans Cinnamon rats by capillary high-performance liquid chromatography-tandem mass spectrometry coupled with stable isotope-dilution method. Anal Chem 83: 2201-2209.
127. 0-cyclopurines accumulate with aging in a tissue-specific manner. Aging Cell 11: 714-716.
128. Winterbourn CC. 2008. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4: 278-286.
129. Wu H, Zhang Y. 2011. Mechanisms and functions of Tet protein mediated 5-methylcytosine oxidation. Genes Dev 25: 2436-2452.
130. Yun BH, Geacintov NE, Shafirovich V. 2011. Generation of guanine-thymidine cross-links in DNA by peroxynitrite/carbon dioxide. Chem Res Toxicol 24: 1144-1152.
131. Zhang L, Lu X, Lu J, Liang H, Dai Q, Xu GL, Luo C, Jiang H, He C. 2012. Thymine DNA glycosylase specifically recognizes 5-carboxylcytosine-modified DNA. Nat Chem Biol 8: 328-330.