973
Views
109
CrossRef citations to date
0
Altmetric
Review Article

Biologically relevant oxidants and terminology, classification and nomenclature of oxidatively generated damage to nucleobases and 2-deoxyribose in nucleic acids

, , , , , , , , & show all
Pages 367-381 | Received 31 Dec 2011, Accepted 17 Jan 2012, Published online: 22 Feb 2012

References

  • Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417:1–13.
  • Morgan MJ, Liu ZG. Crosstalk of reactive oxygen species and NF-kB signalling. Cell Res 2011;21:103–115.
  • D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007;8:13–24.
  • Hanukoglu I. Antioxidant protective mechanism against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev 2006;38:171–196.
  • Powers SK, Jackson MJ. Exercise-induced oxidative stress; cellular mechanisms and impact on muscle force production. Physiol Rev 2008;88:1245–1276.
  • Lonkar P, Dedon PC. Reactive species and DNA damage in chronic inflammation: reconciling chemical mechanisms and biological fates. Int J Cancer 2011;128:1999–2009.
  • Roberts RA, Laskin DL, Smith CV, Robertson FM, Allen EMG, Doom JA, . Nitrative and oxidative stress in toxicology and disease. Toxicol Sci 2009;112:4–16.
  • Bertram C, Hass R. Cellular responses to reactive oxygen species-induced DNA damage and aging. Biol Chem 2008; 389:211–220.
  • Wells PG, McCallum GP, Lam KC, Henderson JT, Ondovcik SL. Oxidative DNA damage and repair in teratogenesis and neurodevelopmental deficits. Birth Defects Res C Embryo Today 2010;90:103–109.
  • Pratviel G, Meunier B. Guanine oxidation: one- and two-electron reactions. Chemistry 2006;12:6018–6030.
  • von Sonntag CV. Free-Radical-Induced DNA Damage and Its Repair. Berlin Heidelberg: Springer-Verlag, 2006.
  • 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;41:1075–1083.
  • Burrows CJ. Surviving an oxygen atmosphere: DNA damage and repair. ACS Symp Ser Am Chem Soc 2009;2009:145–56.
  • Cadet J, Douki T, Ravanat J-L, Di Mascio P. Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochem Photobiol Sci 2009;8: 903–911.
  • Cadet J, Douki T, Ravanat J-L. Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 2010; 49:9–21.
  • Wagner JR, Cadet J. Oxidation reactions of cytosine DNA components by hydroxyl radical and one-electron oxidants in aerated aqueous solutions. Acc Chem Res 2010;43: 564–571.
  • Dedon PC. The chemical toxicology of 2-deoxyribose oxidation in DNA. Chem Res Toxicol 2008;21:206–219.
  • Cadet J, Douki T, Ravanat J-L. Measurement of oxidatively generated base damage in cellular DNA. Mutat Res 2011;711:3–12.
  • Cooke MS, Olinski R, Loft S, European Standards Committee on Urinary (DNA) Lesion Analysis. Measurement and meaning of oxidatively modified DNA lesions in urine. Cancer Epidemiol Biomarkers Prev 2008;17:3–14.
  • Loft S, Svoboda P, Kawai K, Kasai H, Sørensen M, Tiønneland A, . Association between 8-oxo-7, 8-dihydroguanine excretion and risk of lung cancer in a prospective study. Free Radic Biol Med 2012;52:167–172.
  • Maynard S, Schuman SH, Harboe C, de Souza-Pinto NC, Bohr VA. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2010;30:2–10.
  • Svilar D, Goellner EM, Almeida KH, Sobol RW. Base excision repair and lesion-dependent subpathways for repair of oxidative base damage. Antioxid Redox Signal 2011; 14:2491–2507.
  • Pascuccci B, D'Errico, Parlanti E, Giovannini S, Dogliotti E. Role of nucleotide excision repair proteins in oxidative DNA damage repair: an updating. Biochemistry (Mosc) 2011;76:4–15.
  • Sage E, Harrison L. Clustered DNA lesion repair in eukaryotes: relevance to mutagenesis and cell survival. Mutat Res 2011;711:123–133.
  • Delaney JC, Essigmann JM. Biological properties of single chemical-DNA adducts: a twenty year perspective. Chem Res Toxicol 2008;21:232–252.
  • Kamiya H. Mutagenicity of oxidized DNA precursors in living cells; Roles of nucleotide pool sanitization and DNA repair enzymes, and translesion synthesis polymerases. Mutat Res 2010;703:32–36.
  • Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Ischiropoulos H. , Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 2012:52;1–6.
  • Cooke MS, Loft S, Olinski R, Evans MD, Bialkowski K, Wagner JR, . Recommendations for standardized of and nomenclature concerning oxidatively damaged nucleobases in DNA. Chem Res Toxicol 2010;23:705–707.
  • Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008;4: 278–286.
  • Bielski BHJ, Cabelli DE, Arudi RL, Ross AB. Reactivity of HO2/O2•- in aqueous solutions. J Phys Chem Ref Data 1985;14:1041–1100.
  • Wagner JR, van Lier JE, Johnston LJ. Quinone sensitized electron transfer photooxidation of nucleic acids: chemistry of thymine and thymidine radical cations in aqueous solution. Photochem Photobiol 1990;52:333–343.
  • Wagner JR, van Lier JE, Berger M, Cadet J. Thymidine hydroperoxides: structural assignment, conformational features, and thermal decomposition in water. J Am Chem Soc 1994;116:2235–2242.
  • Misiaszek R, Crean C, Joffe A, Geacintov NE, Shafirovich V. Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J Biol Chem 2004;279:32106–32115.
  • Winterbourn CC, Kettle AJ. Radical-radical reactions of superoxide: a potential route to toxicity. Biochem Biophys Res Commun 2003;305:729–736.
  • Chatgilialoglu C, D'Angelantonio M, Kciuk G, Bobrowski K. New insights into the reaction paths of hydroxyl radical with 2′-deoxyguanosine. Chem Res Toxicol 2011;24: 2200–2206.
  • Douki T, Rivière J, Cadet J. DNA tandem lesions containing 8-oxo-7,8-dihydroguanine and formamido residues arise from intermolecular addition of thymine peroxyl radical to guanine. Chem Res Toxicol 2002;15:445–454.
  • Hong S, 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; 129:4089–4098.
  • Bergeron F, Auvré F, Radicella JP, Ravanat J-L. HO● radicals induced an unexpected high proportion of tandem base lesions refractory to repair by DNA glycosylases. Proc Natl Acad Sci USA 2010;107:5528–5533.
  • Cadet J, Berger M, Douki T, Ravanat J-L. Oxidative damage to DNA: formation, measurement and biological significance. Rev Biochem Physiol 1997;131:2–87.
  • Sandermann H. Ecotoxicology of ozone: bioactivation of extracellular ascorbate. Biochem Biophys Res Commun 2008;366:271–274.
  • Roberts RA, Laskin DL, Smith CV, Robertson FM, Allen EMG, Doorn JA, . Nitrative and oxidative stress in toxicology and disease. Toxicol Sci 2009;112:4–16.
  • Wentworth P, Nieva J, Takeuchi C, Gaive R, Wentworth AD, Dilley RB, . Evidence for ozone formation in human atherosclerotic arteries. Science 2003;302: 1053–1056.
  • Sies H. Ozone in arteriosclerotic plaques: searching for the “Smoking gun”. Angew Chem Int Ed 2004;43: 3514–3515.
  • Smith LL. Oxygen, oxysterols, ouabain, and ozone: a cautionary tale. Free Radic Biol Med 2004;37:318–324.
  • Russell GA. Deuterium-isotope effects in the autoxidation of aralkylhydrocarbons. J Am Chem Soc 1957;79:3871–3877.
  • Cadet J, Ravanat J-L, Martinez GR, Medeiros MHG, Di Mascio P. Singlet oxygen oxidation of isolated and cellular DNA: product formation and mechanistic insights. Photochem Photobiol 2006;82:1219–1225.
  • Miyamoto S, Martinez GR, Rettri D, Augusto O, Medeiros MHG, Di Mascio P. Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet oxygen. Proc Natl Acad Sci 2006; 103:293–298.
  • Malle E, Furtmüller PG, Sattler W, Obinger C. Myeloperoxidase: a target for new drug development? Br J Pharmacol 2007;152:838–854.
  • Masuda M, Suzuki T, Friesen MD, Ravanat J-L, Cadet J, Pignatelli B, . Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils. J Biol Chem 2001;276: 40486–40496.
  • Asahi T, Kondo H, Masuda M, Nishino H, Aratani Y, Naito Y, . Chemical and immunological detection of 8-halogenated deoxyguanosines at early inflammation. J Biol Chem 2010;285:9282–9291.
  • Stanley NR, Pattison DL, Hawkins CL. Ability for hypochlorous acid and N-chloramines to chlorinate DNA and its constituents. Chem Res Toxicol 2010;23:1293–1302.
  • Spencer JP, Whiteman M, Jenner A, Halliwell B. Nitrite-induced deamination and hypochlorite-induced oxidation of DNA in intact human respiratory tract epithelial cells. Free Radic Biol Med 2000;28:1039–1050.
  • Ferrer-Sueta G, Radi R. Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 2009;4: 161–177.
  • Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990;87:1620–1624.
  • Koppenol WH. The basic chemistry of nitrogen monoxide and peroxynitrite. Free Radic Biol Med 1998;25:385–391.
  • Dedon PC, Tannenbaum SR. Reactive nitrogen species in the chemical biology of inflammation. Arch Biochem Biophys 2004;423:12–22.
  • Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, . Free radical biology and medicine: it's a gas, man! Am J Physiol Regul Integr Comp Physiol 2006;291:R491–R511.
  • Denicola A, Freeman BA, Trujillo M, Radi R. Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations. Arch Biochem Biophys 1996;333:49–58.
  • Medinas DB, Cerchiaro G, Trindade DF, Augusto O. The carbonate radical and related oxidantsderived from bicarbonate buffer. IUBMB Life 2007;59:255–262.
  • Cadet J, Douki T, Ravanat J-L. One-electron oxidation of DNA and inflammation processes. Nat Chem Biol 2006;2:348–349.
  • Lee YA, Yun BH, Him SH, Margolin Y, Dedon PC. Geacintov NE, Mechanisms of oxidation of guanine in DNA by carbonate radical anion, a decomposition product of nitrosoperoxycarbonate. Chemistry 2007;13: 4571–4581.
  • Niles JC, Wishnok JS, Tannenbaum SR. Peroxynitrite- induced oxidation and nitration products of guanine and 8-oxoguanine: structures and mechanisms of product formation. Nitric Oxide 2006;14:109–121.
  • Yun BH, Geacintov NE, Shafirovich V. Generation of guanine-thymidine cross-links in DNA by peroxynitrite/carbon dioxide. Chem Res Toxicol 2011;24:1144–1152.
  • Kawanishi S, Hiraku Y. Oxidative and nitrative DNA damage as biomarker for carcinogenesis with special reference to inflammation. Antioxd Redox Signal 2006;8: 1047–1058.
  • Hiraku Y. Formation of 8-nitroguanine, a nitrative DNA lesion, in inflammation-related carcinogenesis and its significance. Environ Health Prev Med 2010;15:63–72.
  • Hiraku Y, Kawanishi S, Ichinose T, Murata M. The role of iNOS-mediated DNA damage in infection- and asbestos-induced carcinogenesis. Ann NY Acad Sci 2010;1203: 15–22.
  • Crespo-Hernández CE, Close DM, Gorb L, Leszczynski J. Determination of redox potentials for the Watson-Crick base pairs, DNA nucleosides, and relevant nucleosides analogues. J Phys Chem B 2007;111:5386–5395.
  • Kawanishi S, Murata M. Mechanism of DNA damage induced by bromate differs from general types of oxidative stress. Toxicology 2006;221:172–178.
  • Ballmaier D, Epe B. DNA damage by bromate: mechanism and consequences. Toxicology 2006;221:166–171.
  • Mangal D, Vudathala D, Park J-H, Lee S-H, Penning TM, Blair IA, . Analysis of 7,8-dihydro-8-oxo-2′-deoxyguanosine in cellular DNA during oxidative stress. Chem Res Toxicol 2009;22:788–797.
  • Attard, NR, Karran P. UVA photosensitization of thiopurines and skin cancer in organ transplant recipients. Photochem Photobiol Sci 2011;11:62–68.
  • Brem R, Karran P. Multiple forms of DNA damage caused by UVA photoactivation of DNA 6-thioguanine. Photochem Photobiol 2012;88:5–13.
  • Douki T, Ravanat J-L, Angelov D, Wagner JR, Cadet J. Effects of duplex stability on charge-transfer efficiency within DNA. Top Curr Chem 2004;236:1–25.
  • Douki T, Ravanat J-L, Pouget JP, Testard I, Cadet J. Minor contribution of direct ionization to DNA base damage induced by heavy ions. Int J Radiat Biol 2006;82:119–127.
  • Wagenknecht HA. Electron transfer processes in DNA: mechanisms, biological relevance and applications in DNA analytics. Nat Prod Rep 2006;23:973–1006.
  • Kanvah S, Joseph J, Schuster GB, Barnett RN. Cleveland CL, Landman U, Oxidation of DNA: damage to nucleobases. Acc Chem Res 2010;43:280–287.
  • Taliliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, . Conversion of 5-methylcytosine to 5- hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009;324:930–935.
  • Iqbal K, Jin S-G, Szabo PE. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 2011;108: 3642–3647.
  • Pfaffeneder T, Hackner B, Truβ M, Münzel M, Müller M, Deiml CA, . The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew Chem Int Ed 2011; 50:7008–7012.
  • Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, . Tet proteins can convert 5-methylcytosine to 5- formylcytosine and 5-carboxylcytosine. Science 2011;333: 1300–1303.
  • He Y-F, Li B-Z, Li Z, Liu P, Wang Y, Tang Q, . Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011;333: 1303–1307.
  • Greenberg MM. The formamidopyrimidines: purine lesions formed in competition with 8-oxopurines from oxidative stress. Acc Chem Res doi:10.1021/ar2002182.
  • Berger M, Cadet J. Isolation and characterization of the radiation-induced degradation products of 2′-deoxyguanosine in oxygen-free solutions. Z Naturforsch 1985;40b: 1519–1531.
  • Raoul S, Bardet M, Cadet J. Gamma irradiation of 2′-deoxyadenosine in oxygen-aqueous solutions. Identification and conformational features of formamidopyrimidine nucleoside derivatives. Chem Res Toxicol 1995;8:924–933.
  • Greenberg MM, Hantosi Z, Wiederholt CJ, Rithner CD. Studies on N4-(2-deoxy-D-pentofuranosyl)-4,6-diamino-5-formamidopyrimidine (Fapy•dA) and N6-(2-deoxy-D-pentofuranosyl)-6-diamino-5-formamido-4-hydroxypyrimidine (Fapy•dG). Biochemistry 2001;40:15856–15861.
  • Povirk LF. DNA damage and mutagenic by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enedynes. Mutat Res 1996;355:71–89.
  • Guan L, Greenberg MM. DNA interstrand cross-link formation by the 1,4-dioxobutane abasic site. J Am Chem Soc 2009;131:15225–15231.
  • Bellon S, Ravanat J-L, Gasparutto D, Cadet J. Cross-linked thymine-purine base tandem lesions: synthesis, characterization, and measurement in gamma-irradiated DNA. Chem Res Toxicol 2002;15:598–606.
  • Wang Y. Bulky DNA lesions induced by reactive oxygen species. Chem Res Toxicol 2008;21:276–281.
  • Jiang Y, Hong H, Cao H, Wang Y. In vivo formation and in vitro replication of a guanine-thymine intrastrand cross-link lesion. Biochemistry 2007;46:12757–12763.
  • Hong H, Cao H, Wang Y. Formation and genotoxicity of a guanine-cytosine intrastrand cross-link lesion in vivo. Nucleic Acids Res2007;35:7118–7127.
  • Box HC, Budzinski EE, Freund HG, Evans MS, Patrzyc HB, Wallace JC, . Vicinal lesions in X-irradiated DNA? Int J Radiat Biol1993;64:261–263.
  • Dizdaroglu M, Jaruga P, Rodriguez H. Identification and quantification of 8,5′-cyclo-2′-deoxyguanosine in DNA by liquid chromatography/mass spectrometry. Free Radic Biol Med 2001;30:777–784.
  • Chatgilialoglu C, Ferreri C, Terzidis MA. Purine 5′, 8-cyclonucleoside lesions: chemistry and biology. Chem Soc Rev 2011;40:1368–1382.
  • Belmadoui N, Boussicault F, Guerra M, Ravanat J-L, Chatgilialoglu C, Cadet J. Radiation-induced formation of purine 5′,8-cyclonucleosides in isolated and cellular DNA: high stereospecificity and modulating effect of oxygen. Org Biomol Chem 2010;8:3211–3219.
  • D'Errico M, Parlanti E, Teson M, Bernades de Jesus BM, Degan P, Calcagnile A, . New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J 2006;25:4305–4315.
  • D'Errico M, Parlanti E, Teson M, Degan P, Lemma T, Calcagnile A, . The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 2007;26: 4336–4343.
  • Sczepanski, JT, Jacobs AC, Majumdar A, Greenberg MM. Scope and mechanism of interstrand cross-link formation by the C4′-oxidized abasic site. J Am Chem Soc 2009; 131:11132–11139.
  • Sczepanski JT, Hiemstra CN, Greenberg MM. Probing DNA interstrand cross-link formation by an oxidized abasic site using nonnative nucleotides. Biorg Med Chem 2011;19:5788–5793.
  • Regulus P, Duroux B, Bayle PA, Favier A, Cadet J, Ravanat J-L. 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: 14032–14037.
  • Gueranger Q, Kia A, Frith D, Karran P. Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA. Nucleic Acids Res 2011; 39:5057–5060.
  • Peng X, Ghosh AK, Van Houten B, Greenberg MM. Nucleotide excision repair of a DNA interstrand cross-link produces single- and double-strand breaks. Biochemistry 2010;12:11–19.
  • Perrier S, Hau J, Gasparutto D, Cadet J, Favier A, Ravanat J-L. 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;128:5703–5710.
  • Xu X, Muller JG, Ye Y, Burrows CJ. DNA-protein cross-links between guanine and lysine depend on the mechanism of oxidation for formation of C5 vs C8 guanosine adducts. J Am Chem Soc 2008;130:703–709.
  • Brem R, Daehn I, Karran P. Efficient DNA interstrand crosslinking by 6-thioguanine and UVA radiation. DNA Repair (Amst) 2011;10:869–876.
  • Marnett LJ. Oxy radicals, lipid peroxidation and DNA damage. Toxicology 2000;181–182:219–222.
  • Jacobs AT, Marnett LJ. Systems analysis of protein modification and cellular responses induced by electrophile stress. Acc Chem Res 2010; 18:673–683.
  • Medeiros MH. Exocyclic DNA adducts as biomarkers of lipid oxidation and predictors of disease. Challenges in developing sensitive and specific methods for clinical studies. Chem Res Toxicol 2009;22:419–425.
  • Nair U, Bartsch H, Nair J. Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. Free Radic Biol Med 2007;43:1009–1120.
  • Chan SW, Dedon PC. The biological and metabolic fates of endogenous DNA damage products. J Nucleic Acids 2010;2010:929047.
  • Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A. DNA damage induced by endogenous aldehydes: current stage of knowledge. Mutat Res 2011;711:13–27.
  • Nair J, Nair UJ, Sun X, Wang Y, Arab K, Bartsch H, . Quantifying etheno-DNA adducts in human tissues, white blood cells, and urine by ultrasensitive 32P-postlabeling and immunohistochemistry. Methods Mol Biol 2011; 682:189–205.
  • Karlsson HL. The comet assay in nanotoxicology. Anal Bioanal Chem 2010;398:651–666.
  • Azqueta A, Gutzkow KB, Brunborg G, Collins AR. Towards a more reliable comet assay: optimizing agarose concentration, unwinding time and electrophoresis conditions. Mutat Res 2011;724:41–45.
  • Pfaum M, Will O, Epe B. Determination of steady-state levels of oxidative base modifications in mammalian cells by means of repair enzymes. Carcinogenesis 1997;18: 2225–2231.
  • Kino K, Saito I. Product analysis of GG-specific photooxidation DNA via electron transfer: 2-aminoimidazolone as a major guanine oxidation product. J Am Chem Soc 1998; 120:7373–7374.
  • Gasparutto D, Ravanat J-L, Gérot O, Cadet J. Characterization and chemical stability of photooxidized oligonucleotides thatcontain 2,2-diamino-4-[(2-deoxy-β-D- erythro-pentofuranosyl)-amino]-5(2H)-oxazolone. J Am Chem Soc 1998;120:10283–10286.
  • Ghosh A, Joy A, Schuster GB, Douki T, Cadet J. Selective one-electron oxidation of duplex DNA oligomers: reaction at thymines. Org Biomol Chem 2008;6:916–928.
  • Haraguchi K, Delaney MO, Wiederholt CJ, Sambandon A, Hantosi Z, Greenberg MM, . Synthesis and characterization of oligodeoxynucleotides containing formamidopyrimidine lesions and nonhydrolyzable analogues. J Am Chem Soc 2002;124:3263–3269.
  • Delaney S, Delaney JC, Essigmann JM. Chemical- biology fingerprint: probing the properties of DNA lesions formed by peroxynitrite. Chem Res Toxicol 2007;20: 1718–1729.
  • Berthod T, Pétillot Y, Guy A, Cadet J, Forest E, Molko D. Synthesis and mass spectrometry analysis of oligonucleotides bearing 5-formyl-2′-deoxyuridine in their structure. Nucleosides Nucleotides. 1996;15:1287–1305.
  • Collins AR. The use of bacterial repair endonucleases in the comet assay. Methods Mol Biol 2011;691:137–147.
  • David SS, Williams SD. Chemistry of glycosylases and endonucleases involved in base-excision repair. Chem Rev 1998:98:1221–1261.
  • 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: 185–190.
  • Jensen A, Løhr M, Eriksen L, Grønbæk M, Dorry E, Loft S, . Influence of the OGG1 Ser326Cys polymorphism on oxidatively damaged DNA and repair activity. Free Radic Biol Med 2012;52:118–125.
  • Gedick CM, Collins A; ESCODD (European Standards Committee on Oxidative DNA Damage). Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB J 2005;19:82–84.
  • Goodhead DT. Energy deposition stochastics and track structure: what about the target? Radiat Prot Dosimetry 2006;122:3–15.
  • Nikjoo H, Girard P. A model of the cell nucleus for DNA damage calculations. Int J Radiat Biol 2012;88:87–97.
  • Olive PL, Banáth JP. The comet assay: a method to measure DNA damage in individual cells. Nat Protocol 2006; 1:23–29.
  • Bonner WM, Redon CE, Dickey JS Nakamura AJ, Sedelnikova OA Solier S. GammaH2AX and cancer. Nat Rev Cancer 2008;8:957–1967.
  • Ivashkevich AN, Martin OA, Smith AJ, Redon CE, Bonner WM, Lobachevsky PN. γH2AX as a measure of DNA damage: a computational approach to automatic analysis. Mutat Res 2011;711:49–160.
  • Olive PL. Endogenous DNA breaks: gamma H2AX and the role of telomeres. Aging (Albany NY) 2009:1;154–156.
  • Cleaver JE. γH2AX biomarker of damage or functional participant in DNA repair “all that glitters is not gold”. Photochem Photobiol 2011;87:1230–1239.
  • Hada M, Georgalikas. Formation of clustered DNA damage after high-LET irradiation: a review. J Radiat Res 2008;49: 203–210.
  • Kryston TB, Georgiev AB Pissis P, Georgakilas AG. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 2011;711:193–211.
  • Sutherland BM, Bennett PV, Sutherland JC, Laval J. Clustered DNA damages induced by X-rays in human cells. Radiat Res 2002;157:611–616.
  • Holt SM, Georgakilas AG. Detection of complex DNA damage in gamma-irradiated acute lymphoblastic Pre-b NALM-6 cells. Radiat Res 2007;168:527–534.
  • Hickerson RP, Part F, Muller JG, Foote CS, Burrows CJ. Sequence and stacking dependence of 8-oxoguanine oxidation: comparison of one-electron vs singlet oxygen mechanisms. J Am Chem Soc 1999;121:9423–9428.
  • Luo W, Muller JG, Rachlin EM, Burrows CJ. Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-oxo-7,8-dihydroguanosine; Chem Lett 2000; 2:613–616.
  • Niles JC, Wishnok JS, Tannenbaum SR. Spiroiminodihydantoin is the major product of the 8-oxo-7,8-dihydroguanosine reaction with peroxynitrite in the presence of thiols and guanosine photooxidation by methylene blue. Org Lett 2001;3:963–966.
  • Lim KS, Taghizadeh K, Wishnok JS, Babu IR, Shafirovich V, Geacintov NE, . Sequence-dependent variation in the reactivity of 8-oxo-7,8-dihydro-2′-deoxyguanosine toward oxidation. Chem Res Toxicol doi: 10.1021/tx 200422g.
  • Hailer MK, Slade PG, Martin BD, Sugden KD. Nei deficient Escherichia coli are sensitive to chromate and accumulate the oxidized guanine lesion spiroiminodihydantoin. Chem Res Toxicol 2005;18:1378–1383.
  • Kanvah S, Schuster GB. The sacrificial role of easily oxidizable sites in the protection of DNA from damage. Nucleic Acids Res 2005;33:5133–5138.
  • Frelon S, Douki T, Cadet J. Radical oxidation of the adenine moiety of nucleoside and DNA: 2-hydroxy-2′-deoxyadenosine is a minor decomposition product. Free Radic Res. 2002; 36:499–508.
  • Doetsch PW, Zasatawny TH, Martin AM, Dizdaroglu M. Monomeric base damage products from adenine, guanine and thymine induced by exposure of DNA to ultraviolet radiation. Biochemistry 1995;34:737–742.
  • Cadet J, Douki T, Sage E. Ultraviolet radiation-mediated damage to cellular DNA. Mutat Res 2005;571:3–17.
  • Panico R, Powell WH, Richer J-C (eds). A Guide to IUPAC Nomenclature of Organic Compounds, recommendations 1993. Oxford:Blackwell Scientific Publications; 1993.
  • Culp SJ, Cho BP, Kadlubar FF, Evans FE. Structural and conformational analyses of 8-hydroxy-2′-deoxyguanosine. Chem Res Toxicol 1989;2:416–422.
  • Oda Y, Uesugi S, Ikehara M, Nishimura S, Kawase Y, Ishikawa H, . NMR studies of a DNA containing 8-hydroxydeoxyguanosine. Nucleic Acids Res 1991;19: 1407–1412.
  • Kouchakdjian M, Bodepudi V, Shibutani S, Eisenberg M, Johnson F, Grollman AP,. 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 1991;30:1403–1412.
  • Cho BP, Kadlubar FF, Culp SJ, Evans FE. 15N nuclear magnetic resonance studies on the tautomerism of 8-hydroxy-2′-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides. Chem Res Toxicol 1990;3:445–452.
  • Aida M, Nishimura S. An ab initio molecular orbital study on the characteristics of 8-hydroxyguanine. Mutat Res 1987;192:83–89.
  • Venkatesmarlu D, Leszczynski J. Tautomerism equilibria in 8-oxopurines: implication for mutagenesis. J. Comput Aided Mol Des1998;12:373–382.
  • Jang YH, Goddard WA 3rd, Noyes KT, Sowers LC, Hwang S, Chung DS. First principles calculations of the tautomers and pK(a) values of 8-oxoguanine: implications for mutagenicity and repair. Chem Res Toxicol 2002;15: 1023–1035.
  • Niedernhofer LJ, Riley M, Schnetz-Boutaud N, Sanduwaran G, Chaudhary AK, Reddy GR, . Temperature- dependent formation of a conjugate between tris(hydroxymethyl)aminomethane buffer and the malondialdehyde-DNA adduct pyrimidopurinone. Chem Res Toxicol 1997;10: 556–561.
  • Schnetz-Boutaud NC, Saleh S, Marnett LJ, Stone MP. The exocyclic 1,N2-deoxyguanosine pyrimidopurinone M1G is a chemically stable DNA adduct when placed opposite a two-base deletion in the (CpG)3 frameshift hotspot of the Salmonella typhimurium hisD3052 gene. Biochemistry 2001;40:15638–15649.
  • Radi R. Peroxynitrite and reactive nitrogen species: the contribution of ABB intwo decades of research. Arch Biochem Biophys 2009;484:111–113.
  • Griffiths HR, Moller L, Bartosz G, Bast A, Bertoni-Freddari C, Collins A, . Biomarkers. Mol Aspects Med 2002; 23:101–208.
  • H. Kasai, S. Nishimura. Hydroxylation of the C-8 position of deoxyguanosine by reducing agents in the presence of oxygen. Nucleic Acids Symp Ser 1983;No. 12:165–167.
  • Nishimura S. 8-Hydroxyguanine: a base for discovery. DNA Repair (Amst) 2011;10:1078–1083.
  • Dizdaroglu M. Application of capillary gas chromatography-mass spectrometry to chemical characterization of radiation-induced base damage of DNA: implications for assessing DNA repair processes. Anal Biochem 1985;144: 593–603.
  • Floyd RA, Watson JJ, Wong PK, Altmiller DH, Rickard RC. Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanisms of formation. Free Radic Res Commun 1986;1:163–172.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.