Oxidatively generated DNA lesions as potential biomarkers of in vivo oxidative stress

Current Molecular Medicine

Volumn 12, Issue 6, 2012, Pages 655-671

  Ravanat, J L ^a   Cadet, J ^a,b   Douki, T ^a  

^a CEA GRENOBLE   (France)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Biomarkers; DNA chemistry; DNA damage; DNA repair; Oxidative stress; Tandem mass spectrometry

Indexed keywords

2 DEOXYRIBOSE; ADENINE; BIOLOGICAL MARKER; CATION; CYTOSINE; GUANINE; HYDROXYL RADICAL; OXYGEN; THYMIDINE; THYMINE;

ARTICLE; CELL LEVEL; CHEMICAL STRUCTURE; COMET ASSAY; DECOMPOSITION; DNA CROSS LINKING; DNA DAMAGE; DNA DETERMINATION; DNA MODIFICATION; ELECTROCHEMICAL ANALYSIS; ELECTRON; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDRATION; INTERMETHOD COMPARISON; IONIZING RADIATION; MASS SPECTROMETRY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PROTON TRANSPORT; RADIATION EXPOSURE;

ANIMALS; DNA DAMAGE; GENETIC MARKERS; HUMANS; HYDROXYL RADICAL; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PYRIMIDINE DIMERS; REACTIVE OXYGEN SPECIES;

EID: 84862527681     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412800792651     Document Type: Article

References (190)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362: 709-15.
2. Martinez MC, Andriantsitohaina R. Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid Redox Signal 2009; 11: 669-702.
3. Beckman KB, Ames BN. Oxidative decay of DNA. J Biol Chem 1997; 272: 19633-6.
4. Halliwell B, Gutteridge MC. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 1984; 219: 1-14.
5. Friedberg EC. DNA damage and repair. Nature 2003; 421: 436-40.
6. ESCODD. Comparison of different methods of measuring 8- oxoguanine as a marker of oxidative DNA damage. ESCODD (European Standards Committee on Oxidative DNA Damage). Free Radic Res 2000; 32: 333-41.
7. ESCODD. Inter-laboratory validation of procedures for measuring 8-oxo-7,8-dihydroguanine/8-oxo-7,8-dihydrodeoxyguanosine in DNA. Free Radic Res 2002; 36: 239-45.
8. ESCODD. Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic Biol Med 2003; 34: 1089-99.
9. ESCOOD. Comparative analysis of baseline 8-oxo-7,8- dihydroguanine in mammalian cell DNA by different methods in different laboratories: an approach to consensus. Carcinogenesis 2002; 23: 2129-33.
10. Lunec J. ESCODD: European Standards Committee on Oxidative DNA Damage. Free Radic Res 1998; 29: 601-8.
11. Cadet J, Douki T, Ravanat J-L. Oxidatively generated damage to the guanine moiety of DNA: mechanistic aspects and formation in cells. Acc Chem Res 2008; 41: 1075-83.
12. Cadet J, Douki T, Ravanat J-L. Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 2010; 49: 9-21.
13. Guetens G, De Boeck G, Highley M, et al. Oxidative DNA damage: biological significance and methods of analysis. Crit Rev Clin Lab Sci 2002; 39: 331-457.
14. Sekiguchi M, Tsuzuki T. Oxidative nucleotide damage: consequences and prevention. Oncogene 2002; 21: 8895-904.
15. Hiraku Y. Formation of 8-nitroguanine, a nitrative DNA lesion, in inflammation-related carcinogenesis and its significance. Environ Health Prev Med 2010; 15(2): 63-72.
16. Delaney S, Delaney JC, Essigmann JM. Chemical-biological fingerprinting: probing the properties of DNA lesions formed by peroxynitrite. Chem Res Toxicol 2007; 20: 1718-29.
17. Niles JC, Wishnok JS, Tannenbaum SR. Peroxynitriteinduced oxidation and nitration products of guanine and 8- oxoguanine: structures and mechanisms of product formation. Nitric Oxide 2006; 14: 109-21.
18. Ohnishi S, Murata M, Kawanishi S. DNA damage induced by hypochlorite and hypobromite with reference to inflammationassociated carcinogenesis. Cancer Lett 2002; 178: 37-42.
19. Ito K, Inoue S, Hiraku Y, Kawanishi S. Mechanism of sitespecific DNA damage induced by ozone. Mutat Res 2005; 585: 60-70.
20. Wagner JR, Cadet J, Fisher GJ. Photooxidation of thymine sensitized by 2-methyl-1,4-naphthoquinone: analysis of products including three novel photodimers. Photochem Photobiol 1984; 40: 589-97.
21. Wagner JR, Berger M, Cadet J, van Lier JE. Analysis of thymidine hydroperoxides by post-column reaction high performance liquid chromatography. J Chromatogr 1990; 504: 191-6.
22. Cadet J, Delatour T, Douki T, et al. Hydroxyl radicals and DNA base damage. Mutat Res 1999; 424: 9-21.
23. Wagner JR, Decarroz C, Berger M, Cadet J. Hydroxylradical- induced decomposition of 2'-deoxycytidine in aerated aqueous solutions. J Am Chem Soc 1999; 121: 4101-10.
24. Tremblay S, Douki T, Cadet J, Wagner JR. 2'-Deoxycytidine glycols, a missing link in the free radical-mediated oxidation of DNA. J Biol Chem 1999; 274: 20833-8.
25. Steenken S. Purine bases, nucleosides and nucleotides: aqueous solution redox chemistry and transformation reactions of their radical cation and e- and OH adducts. Chem Rev 1989; 89: 503-20.
26. Candeias LP, Steenken S. Reaction of HO* with guanine derivatives in aqueous solution: formation of two different redox-active OH-adduct radicals and their unimolecular transformation reactions. Properties of G(-H)*. Chem Eur J 2000; 6: 475-84.
27. Cadet J, Berger M, Buchko GW, et al. 2,2-Diamino-4-[(3,5-di- O-acetyl-2-deoxy-ß-D-erythro-pentofuranosyl)amino]-5-(2H)- oxazolone: a novel and predominant radical oxidation product of 3',5'-di-O-acetyl-2'-deoxyguanosine. J Am Chem Soc 1994; 116: 7403-4.
28. Hall DB, Holmlin RE, Barton JK. Oxidative DNA damage through long-range electron transfer. Nature 1996; 382: 731-5.
29. Nunez ME, Holmquist GP, Barton JK. Evidence for DNA charge transport in the nucleus. Biochemistry 2001; 40: 12465-71.
30. Nunez ME, Rajski SR, Barton JK. Damage to DNA by longrange charge transport. Methods Enzymol 2000; 319: 165-88.
31. Giese B, Amaudrut J, Kohler AK, et al. Direct observation of hole transfer through DNA by hopping between adenine bases and by tunnelling. Nature 2001; 412: 318-20.
32. Wan C, Fiebig T, Schiemann O, et al. Femtosecond direct observation of charge transfer between bases in DNA. Proc Natl Acad Sci USA 2000; 97: 14052-5.
33. Douki T, Ravanat J-L, Angelov D, et al. Effects of duplex stability on charge-transfer efficiency within DNA. Top Curr Chem 2004; 236: 1-25.
34. Ravanat J-L, Saint-Pierre C, Cadet J. One-electron oxidation of the guanine moiety of 2'-deoxyguanosine: influence of 8- oxo-7,8-dihydro-2'-deoxyguanosine. J Am Chem Soc 2003; 125: 2030-1.
35. Kuttappan-Nair V, Samson-Thibault F, Wagner JR. Generation of 2'-deoxyadenosine N6-aminyl radicals from the photolysis of phenylhydrazone derivatives. Chem Res Toxicol 2010; 23: 48-54.
36. Wang Y. Bulky DNA lesions induced by reactive oxygen species. Chem Res Toxicol 2008; 21: 276-81.
37. Barker S, Weinfeld M, Murray D. DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat Res 2005; 589: 111-35.
38. Cadet J, Douki T, Ravanat J-L. One-electron oxidation of DNA and inflammation processes. Nat Chem Biol 2006; 2: 348-9.
39. Buchko GW, Cadet J, Ravanat J-L, Labataille P. Isolation and characterization of a new product produced by ionizing irradiation and type I photosensitization of 2'-deoxyguanosine in oxygen-saturated aqueous solution: (2S)-2,5'-anhydro-1- (2-deoxy-α-D-erythro-pentofuranosyl)-5-guanidinylidene-2- hydroxy-4-oxoimidazolidine. Int J Radiat Biol 1993; 63: 669-76.
40. Morin B, Cadet J. Type I benzophenone-mediated nucleophilic reaction of 5'-amino-2',5'-dideoxyguanosine. A model system for the investigation of photosensitized formation of DNA-protein cross-links. Chem Res Toxicol 1995; 8: 792-9.
41. Morin B, Cadet J. Chemical aspect of the benzophenonephotosensitized formation of two lysine-2'-deoxyguanosine cross-links. J Am Chem Soc 1995; 117: 12408-15.
42. Perrier S, Hau J, Gasparutto D, et al. 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 2006; 128: 5703-10.
43. Box HC, Budzinski EE, Dawidzik JB, et al. Free radicalinduced tandem base damage in DNA oligomers. Free Radic Biol Med 1997; 23: 1021-30.
44. Box HC, Budzinski EE, Dawidzik JB, et al. Tandem lesions and other products in X-irradiated DNA oligomers. Radiat Res 1998; 149: 433-9.
45. Box HC, Dawidzik JB, Budzinski EE. Free radical-induced double lesions in DNA. Free Radic Biol Med 2001; 31:856-68.
46. Bellon S, Gasparutto D, Romieu A, Cadet J. 5- (phenylthiomethyl)-2'-deoxyuridine as an efficient photoreactive precursor to generate single and multiple lesions within DNA fragments. Nucleosides Nucleotides Nucleic Acids 2001; 20: 967-71.
47. Bellon S, Ravanat J-L, Gasparutto D, Cadet J. Cross-linked thymine-purine base tandem lesions: Synthesis, characterization, and measurement in gamma-Irradiated isolated DNA. Chem Res Toxicol 2002; 15: 598-606.
48. Hong H, Cao H, Wang Y. Formation and genotoxicity of a guanine-cytosine intrastrand cross-link lesion in vivo. Nucleic Acids Res 2007; 35: 7118-27.
49. Bourdat AG, Gasparutto D, Cadet J. Synthesis and enzymatic processing of oligodeoxynucleotides containing tandem base damage. Nucleic Acids Res 1999; 27: 1015-24.
50. Bourdat A-G, Douki T, Frelon S, et al. Tandem base lesions are generated by hydroxyl radical within isolated DNA in aerated aqueous solution. J Am Chem Soc 2000; 122: 4549-56.
51. Bergeron F, Auvré F, Radicella JP, Ravanat J-L. HO° radicals induce an unexpected high proportion of tandem base lesions refractory to repair by DNA glycosylases. Proc Natl Acad Sci USA 2010; 107: 5528-33.
52. Hong IS, Carter KN, Greenberg MM. Evidence for glycosidic bond rotation in a nucleobase peroxyl radical and its effect on tandem lesion formation. J Org Chem 2004; 69: 6974-8.
53. Hong IS, Carter KN, Sato K, Greenberg MM. Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical. J Am Chem Soc 2007; 129: 4089-98.
54. Pogozelski WK, Tullius TD. Oxidative strand scission of nucleic acids: routes initiated by hydrogen abstraction from the sugar moiety. Chem Rev 1998; 98: 1089-108.
55. Chatgilialoglu C, Ferreri C, Terzidis MA. Purine 5',8- cyclonucleoside lesions: chemistry and biology. Chem Soc Rev 2011; 40: 1368-82.
56. Belmadoui N, Boussicault F, Guerra M, et al. Radiationinduced formation of purine 5',8-cyclonucleosides in isolated and cellular DNA: high stereospecificity and modulating effect of oxygen. Org Biomol Chem 2010; 8: 3311-219.
57. Regulus P, Spessotto S, Gateau M, et al. Detection of new radiation-induced DNA lesions by liquid chromatography coupled to tandem mass spectrometry. Rapid Commun Mass Spectrom 2004; 18: 2223-8.
58. Regulus P, Duroux B, Bayle P-A, et al. 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 USA 2007; 104: 14032-7.
59. Sczepanski JT, Jacobs AC, Greenberg MM. Self-promoted DNA interstrand cross-link formation by an abasic site. J Am Chem Soc 2008; 130: 9646-7.
60. Sczepanski JT, Jacobs AC, Van Houten B, Greenberg MM. Double-strand break formation during nucleotide excision repair of a DNA interstrand cross-link. Biochemistry 2009; 48: 7565-7.
61. Sczepanski JT, Wong RS, McKnight JN, et al. Rapid DNAprotein cross-linking and strand scission by an abasic site in a nucleosome core particle. Proc Natl Acad Sci USA 2010; 107: 22475-80.
62. Rentel C, Wang X, Batt M, et al. Formation of modified cytosine residues in the presence of depurinated DNA. J Org Chem 2005; 70: 7841-5.
63. Cadet J, Douki T, Pouget J-P, Ravanat J-L. Singlet oxygen DNA damage products: Formation and measurement. Methods Enzymol 2000; 319: 143-53.
64. Cadet J, Ravanat J-L, Buchko GW, et al. Singlet oxygen DNA damage: chromatographic and mass spectrometry analysis of damage products. Methods Enzymol 1994; 234: 79-88.
65. Ravanat J-L, Cadet J. Reaction of singlet oxygen with 2'- deoxyguanosine and DNA. Isolation and characterization of the main oxidation products. Chem Res Toxicol 1995; 8: 379-88.
66. Martinez GR, Ravanat J-L, Cadet J, et al. Spiroiminodihydantoin nucleoside formation from 2'-deoxyguanosine oxidation by [(18)O-labeled] singlet molecular oxygen in aqueous solution. J Mass Spectrom 2007; 42: 1326-32.
67. Ravanat J-L, Saint-Pierre C, Di Mascio P, et al. Damage to isolated DNA mediated by singlet oxygen. Helv Chim Acta 2001; 84: 3702-9.
68. Ravanat J-L, Martinez GR, Medeiro MHG, et al. Mechanistic aspects of the oxidation of DNA constituents mediated by singlet molecular oxygen. Arch Biochem Biophys 2004; 423: 23-30.
69. Martinez GR, Medeiros MHG, Ravanat J-L, et al.[180]- labeled singlet oxygen as a tool for mechanistic studies of 8- oxo-7,8-dihydroguanine oxidative damage: detection of spiroiminodihydantoin, imidazolone and oxazolone derivatives. Biol Chem 2002; 383: 607-17.
70. Duarte V, Gasparutto D, Yamaguchi L, et al. Oxaluric acid as the major product of singlet oxygen mediated oxidation of 8- oxo-7,8-dihydro-2'-deoxyguanosine in DNA. J Am Chem Soc 2000; 122: 12622-8.
71. Ravanat J-L, Martinez GR, Medeiros MGH, et al. Singlet oxygen oxidation of 2'-deoxyguanosine. Formation and mechanistic insights. Tetrahedron 2006; 62: 10709-10715.
72. Martinez GR, Ravanat J-L, Medeiros MHG, et al. Synthesis of a naphthalene endoperoxide as a source of 18O-labeled singlet oxygen for mechanistic studies. J Am Chem Soc 2000; 122: 10212-3.
73. Ravanat J-L, Di Mascio P, Martinez GR, et al. Singlet oxygen induces oxidation of cellular DNA. J Biol Chem 2000; 275: 40601-4.
74. Ravanat J-L, Sauvaigo S, Caillat S, et al. Singlet oxygenmediated damage to cellular DNA as determined by the comet assay associated with DNA repair enzymes. Biol Chem 2004; 385: 17-20.
75. Cadet J, Douki T, Ravanat J-L. Measurement of oxidatively generated base damage in cellular DNA. Mutat Res 2011; 711: 3-12.
76. Collins AR, Dobson VL, Dusinska M, et al. The comet assay: what can it really tell us? Mutat Res 1997; 375: 183-93.
77. Collins AR, Dusinska M. Oxidation of cellular DNA measured with the comet assay. Methods Mol Biol 2002; 186: 147-59.
78. Collins AR, Dusinska M, Gedik CM, Stetina R. Oxidative damage to DNA: Do we have reliable biomarker? Environ. Health Perspect. 1996; 104: 465-9.
79. Floyd RA, Watson JJ, Wong PK, et al. Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanism of formation. Free Radic Res Commun 1986; 1: 163-72.
80. Kasai H, Tanooka H, Nishimura S. Formation of 8- hydroxyguanine residues in DNA by X-irradiation. Gann 1984; 75: 1037-9.
81. Berger M, Anselmino C, Mouret J-F, Cadet J. High performance liquid chromatography-electrochemical assay for monitoring the formation of 8-oxo-7,8-dihydroadenine and its related 2'-deoxyribonucleoside. J Liquid Chromatogr 1990; 13: 929-32.
82. Wagner R, Decarroz C, Berger M, Cadet J. Ionizing radiation induced decomposition of 2'-deoxycytidine in aerated solutions. J Am Chem Soc 1999; 121: 4101-10.
83. Dizdaroglu M. The use of capillary gas chromatographymass spectrometry for identification of radiation-induced DNA base damage and DNA base-amino acid cross-links. J Chromatogr 1984; 295: 103-21.
84. Ravanat J-L, Gremaud E, Markovic J, Turesky RJ. Detection of 8-oxoguanine in cellular DNA using 2,6-diamino-8- oxopurine as an internal standard for HPLC-EC detection. Anal Biochem 1998; 260: 30-7.
85. Fuciarelli AF, Wegher BJ, Gajewski E, et al. Quantitative measurement of radiation-induced base products in DNA using gas chromatography-Mass sprectrometry. Radiat Res 1989; 119: 219-31.
86. Halliwell B, Dizdaroglu M. Commentary. The measurement of oxidative damage to DNA by HPLC and GC/MS techniques. Free Radic Res Commun 1992; 16: 75-87.
87. Ravanat J-L, Turesky RJ, Gremaud E, et al. Determination of 8-oxoguanine in DNA by gas chromatography-mass spectrometry and HPLC-electrochemical detection. Overestimation of the background level of the oxidized base by the gas chromatography-mass spectrometry assay. Chem Res Toxicol 1995; 8: 1039-45.
88. Hamberg M, Zhang L-Y. Quantitative determination of 8- hydroxyguanine and guanine by isotope dilution mass spectrometry. Anal Biochem 1995; 229: 336-44.
89. Douki T, Delatour T, Bianchini F, Cadet J. Observation and prevention of an artifactual formation of oxidized DNA bases and nucleosides in the GC-EIMS method. Carcinogenesis 1996; 17: 347-53.
90. Ravanat J-L, Remaud G, Cadet J. Measurement of the main photooxidation products of 2'-deoxyguanosine using chromatographic methods coupled to mass spectrometry. Arch. Biochem Biophys 2000; 374: 118-27.
91. Dizdaroglu M. Quantitative determination of oxidative base damage in DNA by stable isotope-dilution mass spectrometry. FEBS Lett 1993; 315: 1-6.
92. Rodriguez H, Jurado J, Laval J, Dizdaroglu M. Comparison of the levels of 8-hydroxyguanine in DNA as measured by gas chromatography mass spectrometry following hydrolysis of DNA by Escherichia coli Fpg protein or formic acid. Nucleic Acids Res 2000; 28: E75.
93. Poulsen HE, Weimann A, Salonen JT, et al. Does vitamin C have a pro-oxidant effect? Nature 1998; 395: 231-2.
94. Podmore ID, Griffiths HR, Herbert KE, et al. Vitamin C exhibits pro-oxidant properties. Nature 1998; 392: 559.
95. Berger M, Cadet J, Berube R, et al. Reversed-phase highperformance liquid chromatography-thermospray mass spectrometry of radiation-induced decomposition of thymine and thymidine. J Chromatogr 1992; 593: 133-8.
96. Ravanat J-L, Duretz B, Guiller A, et al. Isotope dilution highperformance liquid chromatography-electrospray tandem mass spectrometry assay for the measurement of 8-oxo-7,8- dihydro-2'-deoxyguanosine in biological samples. J Chromatogr B 1998; 715: 349-56.
97. Griffiths WJ, Jonsson AP, Liu S, et al. Electrospray and tandem mass spectrometry in biochemistry. Biochem J 2001; 355: 545-61.
98. Frelon S, Douki T, Ravanat J-L, et al. High performance liquid chromatography - tandem mass spectrometry for the measurement of radiation-induced base damage to isolated and cellular DNA. Chem Res Toxicol 2000; 13: 1002-10.
99. Matter B, Malejka-Giganti D, Csallany AS, Tretyakova N. Quantitative analysis of the oxidative DNA lesion, 2,2- diamino-4-(2-deoxy-beta-D-erythro-pentofuranosyl)amino]- 5(2H)-oxazolone (oxazolone), in vitro and in vivo by isotope dilution-capillary HPLC-ESI-MS/MS. Nucleic Acids Res 2006; 34: 5449-60.
100. Wang J, Yuan B, Guerrero C, et al. Quantification of oxidative DNA lesions in tissues of long-Evans Cinnamon rats by capillary high-performance liquid chromatographytandem mass spectrometry coupled with stable isotopedilution method. Anal Chem 2011; 83: 2201-9.
101. Boysen G, Collins LB, Liao S, et al. Analysis of 8-oxo-7,8- dihydro-2'-deoxyguanosine by ultra high pressure liquid chromatography-heat assisted electrospray ionizationtandem mass spectrometry. J Chromatogr B 2010; 878: 375-80.
102. Legido-Quigley C, Smith NW, Mallet D. Quantification of the sensitivity increase of a micro-high-performance liquid chromatography-electrospray ionization mass spectrometry system with decreasing column diameter. J Chromatogr A 2002; 976: 11-8.
103. Cadet J, Douki T, Frelon S, et al. Assessment of oxidative base damage to isolated and cellular DNA by HPLC-MS/MS measurement. Free Radic Biol Med 2002; 33: 441-9.
104. Badouard C, Masuda M, Nishino H, et al. Detection of chlorinated DNA and RNA nucleosides by HPLC coupled to tandem mass spectrometry as potential biomarkers of inflammation. J Chromatogr B 2005; 827: 26-31.
105. Masuda M, Suzuki T, Friesen MD, et al. Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils. J Biol Chem 2001; 276: 40486-96.
106. Douki T, Court M, Cadet J. Electrospray-mass spectrometry characterization and measurement of far- UV-induced thymine photoproducts. J Photochem Photobiol B Biol 2000; 54: 145-54.
107. Douki T, Court M, Sauvaigo S, et al. 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 2000; 275: 11678-85.
108. Koc H, Swenberg JA. Applications of mass spectrometry for quantitation of DNA adducts. J Chromatogr B 2002; 778: 323-43.
109. Bessette EE, Spivack SD, Goodenough AK, et al. Identification of carcinogen DNA adducts in human saliva by linear quadrupole ion trap/multistage tandem mass spectrometry. Chem Res Toxicol 2010; 23: 1234-44.
110. Marie C, Maitre A, Douki T, et al. Influence of the metabolic properties of human cells on the kinetic of formation of the major benzo[a]pyrene DNA adducts. J Appl Toxicol 2007; I28: 579-90.
111. Singh R, Farmer PB. Liquid chromatography-electrospray ionization-mass spectrometry: the future of DNA adduct detection. Carcinogenesis 2006; 27: 178-96.
112. Douki T, Odin F, Caillat S, et al. Predominance of the 1,N2- propano 2'-deoxyguanosine adduct among 4-hydroxy-2- nonenal-induced DNA lesions. Free Radic Biol Med 2004; 37: 62-70.
113. Jajoo HK, Burcham PC, Goda Y, et al. A thermospray liquid chromatography/mass spectrometry method for analysis of human urine for the major malondialdehyde-guanine adduct. Chem Res Toxicol 1992; 5: 870-5.
114. Pollack M, Oe T, Lee SH, et al. Characterization of 2'- deoxycytidine adducts derived from 4-oxo-2-nonenal, a novel lipid peroxidation product. Chem Res Toxicol 2003; 16: 893-900.
115. Maurel V, Ravanat J-L, Gambarelli S. Detection of reactive free radicals derived from nucleosides by liquid chromatography coupled to tandem mass spectrometry of DMPO spin trapping adducts. Rapid Commun. Mass Spectrom 2006; 20: 2235-42.
116. Hofer T, Moller L. Optimization of the workup procedure for the analysis of 8-oxo-7,8- dihydro-2'-deoxyguanosine with electrochemical detection. Chem Res Toxicol 2002; 15: 426-32.
117. Cadet J, Douki T, Ravanat J-L. Artifacts associated with the measurement of oxidized DNA bases. Environ Health Perspect 1997; 105: 1033-9.
118. Huang X, Powell J, Mooney LA, et al. Importance of complete DNA digestion in minimizing variability of 8-oxo-dG analyses. Free Radic Biol Med 2001; 31: 1341-51.
119. Douki T, Martini R, Ravanat J-L, et al. Measurement of 2,6- diamino-4-hydroxy-5-formamidopyrimidine and 8-oxo-7,8- dihydroguanine in isolated DNA exposed to gamma radiation in aqueous solution. Carcinogenesis 1997; 18: 2385-91.
120. Falcone JM, Box HC. Selective hydrolysis of damaged DNA by nuclease P1. Biochim. Biophys. Acta 1997; 1337: 267-75.
121. Jaruga P, Birincioglu M, Rodriguez H, Dizdaroglu M. Mass spectrometric assays for the tandem lesion 8,5'-cyclo-2'- deoxyguanosine in mammalian DNA. Biochemistry 2002; 41: 3703-11.
122. Ravanat J-L, Douki T, Duez P, et al. Cellular background level of 8-oxo-7,8-dihydro-2'-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis 2002; 23: 1911-8.
123. Adachi S, Zeisig M, Möller L. Improvements in the analytical method for 8-hydroxydeoxyguanosine in nuclear DNA. Carcinogenesis 1995; 16: 253-8.
124. Singh R, McEwan M, Lamb JH, et al. An improved liquid chromatography/tandem mass spectrometry method for the determination of 8-oxo-7,8-dihydro-2'-deoxyguanosine in DNA samples using immunoaffinity column purification. Rapid Commun Mass Spectrom 2003; 17: 126-34.
125. Badouard C, Menezo Y, Panteix G, et al. Determination of new types of DNA lesions in human sperm. Zygote 2008; 16: 9-13.
126. Mamer OA. Stable isotope dilution techniques. J Chromatogr B 1996; 682:182-183.
127. Randerath K, Reddy MV, Gupta RC. 32P-labeling test for DNA damage. Proc Natl Acad Sci USA 1981; 78: 6126-9.
128. Maccubin A, Budzinski EE, Patrzyc HB, et al. 32Ppostlabeling assay for free radical-induced DNA damage: the formamido remnant of thymine. Free Rad Res Comms 1992; 18: 17-28.
129. Devanaboyina U-S, Gupta SP. Sensitive detection of 8- hydroxy-2'-deoxyguanosine in DNA by 32P-postlabeling assay and the basal levels in rat tissues. Carcinogenesis 1996; 17: 917-24.
130. Zeisig M, Hofer T, Cadet J, Moller L. 32P-postlabeling highperformance liquid chromatography (32P-HPLC) adapted for analysis of 8-hydroxy-2'-deoxyguanosine. Carcinogenesis 1999; 20: 1241-5.
131. Moller L, Hofer T. [32P]ATP mediates formation of 8-hydroxy- 2'-deoxyguanosine from 2'-deoxyguanosine, a possible problem in the 32P-poslabling assay. Carcinogenesis 1997; 18: 2415-9.
132. Cadet J, Bianchini F, Girault I, et al. Measurement of oxidative base damage to DNA: HPLC/32P-postlabelling, immunological and non invasive assays. In: DNA & Free Radicals: Techniques, mechanisms and applications. Halliwell B, Aruoma OI (Eds). London: OICA International; 1998. pp. 285-300.
133. Mouret J-F, Polverelli M, Sarrazin F, Cadet J. Ionic and radical oxidations of DNA by hydrogen peroxide. Chem Biol Interac 1991; 77: 187-201.
134. Toyokuni S, Tanaka T, Hatton Y, et al. Quantitative immunohistochemical determination of 8-hydroxy-2'- deoxyguanosine by a monoclonal antibody N45.1: Its application to ferric nitrilotriacetate-induced renal carcinogenesis model. Lab Investig 1997; 76: 365-74.
135. Breton J, Sichel F, Bianchini F, Prevost V. Measurement of 8-hydroxy-2'-deoxyguanosine by a commercial available ELISA test: Comparison with HPLC/Electrochemical detection in calf thymus DNA and determination in human serum. Anal Lett 2003; 36: 123-34.
136. Collins AR, Duthie SJ, Dobson VL. Direct enzymic detection of endogenous oxidative base damage in human lymphocyte DNA. Carcinogenesis 1993; 14: 1733-5.
137. Mc Kelvey-Martin VJ, Green MHL, Pool-Zobel BL, et al. The single cell gel electrophoresis assay (comet assay): A Europeen review. Mutat Res 1993; 288: 47-63.
138. Tice RR. The single cell gel/comet assay: a microgel electrophoretic technique for the detection of DNA damage and repair in individual cells. In: Environmental Mutagenesis. Phillips DH, Venitt S (Eds). Oxford: BIOS Scientific Publishers; 1996.
139. Pflaum M, Epe B. Measuring oxidative DNA damage by alkaline elution. In: Measuring in vivo oxidative damage: a practical course. J. Lunec, Griffiths HR (Eds). Chischester: John Wiley & Sons, LTD; 2000. pp. 95-104.
140. Swenberg JA, Petzold GL, Harbach PR. In vitro DNA damage/alkaline elution assay for predicting carcinogenic potential. Biochem. Biophys. Res Commun 1976; 72: 732-8.
141. Hartwig A, Dally H, Schlepegrell R. Sensitive analysis of oxidative DNA damage in mammalian cells: use of the bacterial Fpg protein in combination with alkaline unwinding. Toxicol Lett 1996; 88: 85-90.
142. Epe B, Hegler J. Oxidative DNA damage: Endonuclease fingerprinting. Methods Enzymol 1994; 234: 122-31.
143. Collins AR. Measurement of oxidative DNA damage using the comet assay. In: Measuring in vivo oxidative damage: A practical course. Lunec J, Griffiths HR (Editors). Chichester: John Wiley & Sons, LTD; 2000. pp. 83-94.
144. Boiteux S, Gajewski E, Laval J, Dizdaroglu M. Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): Excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 1992; 31: 106-10.
145. Ravanat J-L, Berger M, Boiteux S, et al. Excision of 7,8- dihydro-8-oxoguanine from DNA by the Fpg protein. J Chim Phys 1993; 90: 871-9.
146. Girard P-M, Guibourt N, Boiteux S. The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res 1997; 25: 3204-11.
147. Radicella JP, Dherin C, Desmaze C, et al. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1997; 94: 8010-5.
148. Smith CC, O'Donovan MR, Martin EA. hOGG1 recognizes oxidative damage using the comet assay with greater specificity than FPG or ENDOIII. Mutagenesis 2006; 21: 185-90.
149. Griffiths HR, Möller L, Bartosz G, et al. Biomarkers Mol Aspects Med 2002; 23: 101-208.
150. Riis B, ESCODD. Comparison of results from different laboratories in measuring 8-oxo-2'-deoxyguanosine in synthetic oligonucleotides. Free Rad Res 2002; 36: 649-59.
151. Shimoi K, Kasai H, Yokota N, et al. Comparison between high-performance liquid chromatography and enzyme- linked immunosorbent assay for the determination of 8-hydroxy-2'- deoxyguanosine in human urine. Cancer Epidemiol Biomarkers Prev 2002; 11: 767-70.
152. Shigenaga MK, Gimeno CJ, Ames BN. Urinary 8-hydroxy-2'- deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc Natl Acad Sci USA 1989; 86: 9697-701.
153. Bogdanov MB, Beal MF, McCabe DR, et al. A carbon column-based liquid chromatography electrochemical approach to routine 8-hydroxy-2'-deoxyguanosine measurements in urine and other biologic matrices: a oneyear evaluation of methods. Free Radic Biol Med 1999; 27: 647-66.
154. Bianchini F, Donato F, Faure H, et al. Urinary excretion of 5- (hydroxymethyl)uracil in healthy volunters: effect of active and passive tobacco-smoke. Int J Cancer 1998; 77: 40-6.
155. Faure H, Mousseau M, Cadet J, et al. Urine 8-oxo-7,8- dihydro-2-deoxyguanosine vs. 5-(hydroxymethyl) uracil as DNA oxidation marker in adriamycin-treated patients. Free Radic Res 1998; 28: 377-82.
156. Ravanat J-L, Guicherd P, Tuce Z, Cadet J. Simultaneous determination of five oxidative DNA lesions in human urine. Chem Res Toxicol 1999; 12: 802-8.
157. Weimann A, Belling D, Poulsen HE. Measurement of 8-oxo- 2'-deoxyguanosine and 8-oxo-2'-deoxyadenosine in DNA and human urine by high performance liquid chromatography-electrospray tandem mass spectrometry. Free Radic Biol Med 2001; 30: 757-64.
158. Weimann A, Belling D, Poulsen HE. Quantification of 8-oxoguanine and guanine as the nucleobase, nucleoside and deoxynucleoside forms in human urine by high-performance liquid chromatography-electrospray tandem mass spectrometry. Nucleic Acids Res 2002; 30: E7.
159. Cooke MS, Lunec J, Evans MD. Progress in the analysis of urinary oxidative DNA damage. Free Radic Biol Med 2002; 33: 1601-14.
160. Loft S, Fischer-Nielsen A, Jeding IB, et al. 8- Hydroxydeoxyguanosine as a urinary biomarker of oxidative DNA damage. J Toxicol Environ Health 1995; 40: 391-404.
161. Gackowski D, Rozalski R, Roszkowski K, et al. 8-Oxo-7,8- dihydroguanine and 8-oxo-7,8-dihydro-2'-deoxyguanosine levels in human urine do not depend on diet. Free Radic Res 2001; 35: 825-32.
162. Cooke MS, Evans MD, Dove R, et al. DNA repair is responsible for the presence of oxidatively damaged DNA lesions in urine. Mutat Res 2005; 574: 58-66.
163. Evans MD, Saparbaev M, Cooke MS. DNA repair and the origins of urinary oxidized 2'-deoxyribonucleosides. Mutagenesis 2010; 25: 433-42.
164. Pouget J-P, Frelon S, Ravanat J-L, et al. Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles. Radiat Res 2002; 157: 589-95.
165. Pouget J-P, Ravanat J-L, Douki T, et al. Measurement of DNA base damage in cells exposed to low doses of gamma radiation: comparison between the HPLC-EC and the comet assays. Int J Radiat Biol 1999; 75: 51-8.
166. Sauvaigo S, Petec-Calin C, Caillat S, et al. Comet assay coupled to repair enzymes for the detection of oxidative damage to DNA induced by low doses of gamma-radiation: use of YOYO-1, low-background slides, and optimized electrophoresis conditions. Anal Biochem 2002; 303: 107-9.
167. Rothkamm K, Horn S. Gamma-H2AX as protein biomarker for radiation exposure. Ann Ist Super Sanita 2009; 45: 265-71.
168. de Feraudy S, Revet I, Bezrookove V, et al. A minority of foci or pan-nuclear apoptotic staining of gamma H2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci USA 2011; 107: 6870-5.
169. Lobrich M, Shibata A, Beucher A, et al. gamma H2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010; 9: 662-9.
170. Sutherland BM, Bennett PV, Sidorkina O, Laval J. Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks. Biochemistry 2000; 39: 8026-31.
171. Sutherland BM, Bennett PV, Cintron NS, et al. Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs. Free Radic Biol Med 2003; 35: 495-503.
172. Georgakilas AG, Holt SM, Hair JM, Loftin CW. Measurement of oxidatively-induced clustered DNA lesions using a novel adaptation of single cell gel electrophoresis (comet assay). Curr Protoc Cell Biol 2011; Chapter 6: Unit 6 11.
173. Hada M, Georgakilas AG. Formation of clustered DNA damage after high-LET irradiation: a review. J Radiat Res (Tokyo) 2008; 49: 203-10.
174. Boucher D, Testard I, Averbeck D. Low levels of clustered oxidative DNA damage induced at low and high LET irradiation in mammalian cells. Radiat Environ Biophys 2006; 45: 267-76.
175. David-Cordonnier MH, Boiteux S, O'Neill P. Excision of 8- oxoguanine within clustered damage by the yeast OGG1 protein. Nucleic Acids Res 2001; 29: 1107-13.
176. Eot-Houllier G, Gonera M, Gasparutto D, et al. Interplay between DNA N-glycosylases/AP lyases at multiply damaged sites and biological consequences. Nucleic Acids Res 2007; 35: 3355-66.
177. Malyarchuk S, Brame KL, Youngblood R, et al. Two clustered 8-oxo-7,8-dihydroguanine (8-oxodG) lesions increase the point mutation frequency of 8-oxodG, but do not result in double strand breaks or deletions in Escherichia coli. Nucleic Acids Res 2004; 32: 5721-31.
178. Muller JG, Duarte V, Hickerson RP, Burrows CJ. Gel electrophoretic detection of 7,8-dihydro-8-oxoguanine and 7, 8-dihydro-8-oxoadenine via oxidation by Ir (IV). Nucleic Acids Res 1998; 26: 2247-9.
179. Collins AR, Oscoz AA, Brunborg G, et al. The comet assay: topical issues. Mutagenesis 2008; 23: 143-151.
180. Kryston TB, Georgiev AB, Pissis P, Georgakilas AG. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 2011; 711: 193-201.
181. Martin OA, Redon CE, Nakamura AJ, et al. Systemic DNA damage related to cancer. Cancer Res 2011; 71: 3437-41.
182. Redon CE, Dickey JS, Nakamura AJ, et al. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc Natl Acad Sci USA 2010; 107: 17992-7.
183. Teng Y, Bennett M, Evans KE, et al. A novel method for the genome-wide high resolution analysis of DNA damage. Nucleic Acids Res 2010; 39: e10.
184. Klungland A, Rosewell I, Hollenbach S, et al. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci USA 1999; 96: 13300-5.
185. Sauvaigo S, Caillat S, Odin F, et al. Effect of aging on DNA excision/synthesis repair capacities of human skin fibroblasts. J Invest Dermatol 2011; 130: 1739-41.
186. Bravard A, Vacher M, Moritz E, et al. Oxidation status of human OGG1-S326C polymorphic variant determines cellular DNA repair capacity. Cancer Res 2009; 69: 3642-9.
187. Sauvaigo S, Guerniou V, Rapin D, et al. An oligonucleotide microarray for the monitoring of repair enzyme activitasy toward different DNA base damage. Anal Biochem 2004; 333: 182-92.
188. Jaruga P, Dizdaroglu M. 8,5'-Cyclopurine-2'- deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst) 2008; 7: 1413-25.
189. Kanaly RA, Hanaoka T, Sugimura H, et al. Development of the adductome approach to detect DNA damage in humans. Antioxid Redox Signal 2006; 8: 993-1001.
190. Farmer PB, Brown K, Tompkins E, et al. DNA adducts: Mass spectrometry methods and future prospects. Toxicol Appl Pharmacol 2005; 207: 293-301.