Mechanisms of free radical-induced damage to DNA

References

• Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 4th ed. Oxford: Oxford University Press; 2007.
   Google Scholar
• von Sonntag C. Free-radical-induced DNA damage and its repair. Hiedelberg: Springer; 2006.
   Google Scholar
• Davidson JF, Guo HH, Loeb LA. Endogenous mutagenesis and cancer. Mutat Res 2002;509:17–21.
   PubMed Web of Science ®Google Scholar
• Wallace SS. Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med 2002;33:1–14.
   PubMed Web of Science ®Google Scholar
• Evans MD, Dizdaroglu M, Cooke MS. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 2004;567:1–61.
   PubMed Web of Science ®Google Scholar
• Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. DNA repair and mutagenesis. Washington, D.C.: ASM Press; 2006.
   Google Scholar
• Loeb LA. Human cancers express mutator phenotypes: origin, consequences and targeting. Nature Rev Cancer 2011; 11:450–457.
   PubMed Web of Science ®Google Scholar
• Steenken S, Telo JP, Novais HM, Candeias LP. One-electron-reduction potentials of pyrimidine bases, nucleosides, and nucleotides in aqueous solution. Consequences for DNA redox chemistry. J Am Chem Soc 1992;114:4701–4709.
   Web of Science ®Google Scholar
• Steenken S. Purine bases, nucleosides, and nucleotides: aqueous solution redox chemistry and transformation reactions of their radical cations and e− and OH adducts. Chem Rev 1989;89:503–520.
   Web of Science ®Google Scholar
• Steenken S, Jovanovic SV. How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution. J Am Chem Soc 1997;119:617–618.
   Web of Science ®Google Scholar
• Buxton GV, Greenstock CL, Helman WP, Ross AB. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms, and hydroxyl radicals (•OH/•O2) in aqueous solution. J Phys Chem Ref Data 1988;17:513–886.
   Web of Science ®Google Scholar
• Chatgilialoglu C, D'Angelantonio M, Guerra M, Kaloudis P, Mulazzani QG. A reevaluation of the ambident reactivity of the guanine moiety towards hydroxyl radicals. Angew Chem Int Ed Engl 2009;48:2214–2217.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, D'Angelantonio M, Kciuk G, Bobrowski K. New insights into the reaction paths of hydroxyl radicals with 2′-deoxyguanosine. Chem Res Toxicol 2011;24:2200–2206.
   PubMed Web of Science ®Google Scholar
• O'Neill P. Pulse radiolytic study of the interaction of thiols and ascorbate with OH adducts of dGMP and dG: implications for DNA repair processes. Radiat Res 1983;96:198–210.
   PubMed Web of Science ®Google Scholar
• Mundy CJ, Colvin ME, Quong AA. Irradiated guanine: a Car-Parrinello molecular dynamics study of dehydrogenation in the presence of an OH radical. J Phys Chem 2002;106: 10063–10071.
   Web of Science ®Google Scholar
• Wu Y, Mundy CJ, Colvin ME, Car R. On the mechanisms of OH radical induced DNA-base damage: a comparative quantum chemical and Car-Parrinello molecular dynamics study. J Phys Chem 2004;108:2922–2929.
   Web of Science ®Google Scholar
• 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)•. Chemistry European Journal 2000;6:475–484.
   PubMed Web of Science ®Google Scholar
• Colson A-O, Sevilla MD. Ab initio molecular orbital calculations of radicals formed by H. and OH. addition to DNA bases: electron affinities and ionization potentials. J Phys Chem 1995;99:13033–13037.
   Web of Science ®Google Scholar
• Bonnaccorsi R, Scrocco E, Tomasi J, Pullman A. Ab-initio molecular electrostatic potentials-guanine compared to adenine. Theor Chim Acta 1975;36:339–344.
   Google Scholar
• Solar S, Solar W, Getoff N. Resolved multisite OH-attack on aqueous aniline studied by pulse radiolysis. Radiat Phys Chem 1986;28:229–234.
   Web of Science ®Google Scholar
• Phadatare SD, Sharma KK, Rao BS, Naumov S, Sharma GK. Spectral characterization of guanine C4-OH adduct: a radiation and quantum chemical study. J Phys Chem B 2011;115:13650–13658.
   PubMed Web of Science ®Google Scholar
• Blanksby SJ, Ellison GB. Bond dissociation energies of organic molecules. Acc Chem Res 2003;36:255–263.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Caminal C, Altieri A, Vougioukalakis GC, Mulazzani QG, Gimisis T, . Tautomerism in the guanyl radical. J Am Chem Soc 2006;128:13796–13805.
   PubMed Web of Science ®Google Scholar
• Symons MCR. Apllication of electron spin resonance spectroscopy to the study of the effects of ionising radiation on DNA and DNA complexes. J Chem Soc, Faraday Trans 1987;83:1–11.
   Google Scholar
• 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;31:106–110.
   PubMed Web of Science ®Google Scholar
• Kasai H, Yamaizumi Z, Berger M, Cadet J. Photosensitized formation of 7,8-dihydro-8-oxo-2′-deoxyguanosine (8-hydroxy-2′-deoxyguanosine) in DNA by riboflavin: a non singlet oxygen mediated reaction. J Am Chem Soc 1992;114: 9692–9694.
   Web of Science ®Google Scholar
• Doetsch PW, Zastawny 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.
   PubMed Web of Science ®Google Scholar
• Angelov D, Spassky A, Berger M, Cadet J. High-Intensity UV laser photolysis of DNA and purine 2¢-deoxyribonucleosides: formation of 8-oxopurine damage and oligonucleotide strand cleavage as revealed by HPLC and Gel electrophoresis studies. J Am Chem Soc 1997;119: 11373–11380.
   Web of Science ®Google Scholar
• Spassky A, Angelov D. Influence of the local helical conformation on the guanine modifications generated from one-electron DNA oxidation. Biochemistry 1997;36: 6571–6576.
   PubMed Web of Science ®Google Scholar
• Reynisson J, Steenken S. DFT calculations on the electrophilic reaction with water of the guanine and adenine radical cations. A model for the situation in DNA. Phys Chem Chem Phys 2002;4:527–532.
   Web of Science ®Google Scholar
• Melvin T, Plumb MA, Botchway SW, O'Neill P. Parker AW. 193 nm light induces single strand breakage of DNA predominantly at guanine. Photochem Photobiol 1995;61:584–591.
   PubMed Web of Science ®Google Scholar
• Jortner J, Bixon M, Langenbacher T, Michel-Beyerle ME. Charge transfer and transport in DNA. Proc Natl Acad Sci U S A 1998;95:12759–12765.
   PubMed Web of Science ®Google Scholar
• Nunez ME, Hall DB, Barton JK. Long-range oxidative damage to DNA: effects of distance and sequence. Chem Biol 1999;6:85–97.
   PubMed Web of Science ®Google Scholar
• La Vere T, Becker D, Sevilla MD. Yields of.OH in gamma-irradiated DNA as a function of DNA hydration:hole transfer in competition with.OH formation. Radiat Res 1996;145: 673–680.
   PubMed Web of Science ®Google Scholar
• Swarts SG, Becker D, Sevilla M, Wheeler KT. Radiation-induced DNA damage as a function of hydration.II. Base damage from electron-loss centers. Radiat Res 1996;145: 304–314.
   PubMed Web of Science ®Google Scholar
• Floyd RA, West MS, Eneff KL, Schneider JE. Methylene blue plus light mediates 8-hydroxyguanine formation in DNA. Proc Amer Assoc Cancer Res 1989;30:147.
   Google Scholar
• Schneider JE, Price S, Maidt L, Gutteridge JM, Floyd RA. Methylene blue plus light mediates 8-hydroxy 2′-deoxyguanosine formation in DNA preferentially over strand breakage. Nucleic Acids Res 1990;18:631–635.
   PubMed Web of Science ®Google Scholar
• Yamamoto F, Nishimura S, Kasai H. Photosensitized formation of 8-hydroxydeoxyguanosine in cellular DNA by riboflavin. Biochem Biophys Res Commun 1992;187: 809–813.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, von Sonntag C, Schulte-Frohlinde D. Strand breaks and sugar release by gamma-irradiation of DNA in aqueous solution. J Am Chem Soc 1975;97:2277–2278.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Schulte-Frohlinde D, von Sonntag C. Radiation chemistry of DNA, II. Strand breaks and sugar release by gamma-irradiation of DNA in aqueous solution. The effect of oxygen. Z Naturforsch [C] 1975;30:826–828.
   PubMedGoogle Scholar
• Melvin T, Botchway SW, Parker AW, O'Neill P. Induction of strand breaks in single-stranded polyribonucleotides and DNA by photoionization: one electron oxidized nucleobase radicals as precursors. J Am Chem Soc 1996;118: 10031–10036.
   Web of Science ®Google Scholar
• Cadet J, Berger M, Buchko GW, Joshi PC, Raoul S, Ravanat J-L. 2,2-Diamino-4-[(3,5-di-O-acetyl-2-deoxy-beta-D-erythrosepentofuranosyl) amino]-5-(2H)-oxazolone-A novel and predominant radical oxidation product of 3′,5′-di-O-acetyl-2′-deoxyguanosine. J Am Chem Soc 1994;116:7403–7404.
   Web of Science ®Google Scholar
• Raoul S, Berger M, Buchko GW, Joshi PC, Morin B, Weinfeld M, . H-1, C-13 and N-15 nuclear magnetic resonance analysis and chemical features of the two main radical oxidation products of 2′-deoxyguanosine: oxazolone and imidazolone nucleosides. J Chem Soc Perkin Trans 2 1996;3:371–381.
   Google Scholar
• von Sonntag C. Topics in free radical-mediated DNA damage: purines and damage amplification-superoxic reactions-bleomycin, the incomplete radiomimetic. Int J Radiat Biol 1994;66:485–490.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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)-oxazolon e (oxazolone), in vitro and in vivo by isotope dilution-capillary HPLC-ESI-MS/MS. Nucleic Acids Res 2006;34:5449–5460.
   PubMed Web of Science ®Google Scholar
• Cadet J, Douki T, Ravanat JL. Oxidatively generated damage to the guanine moiety of DNA: mechanistic aspects and formation in cells. Acc Chem Res 2008;41:1075–1083.
   PubMed Web of Science ®Google Scholar
• Llona J, Eriksson LA. Oxidation pathways of adenine and guanine in aqueous solution from first principles electrochemistry. Phys Chem Chem Phys 2004;6:4707–4713.
   Web of Science ®Google Scholar
• Aida M, Nishimura S. An ab initio molecular orbital study on the characteristics of 8-hydroxyguanine. Mutat Res 1987;192:83–89.
   PubMed Web of Science ®Google Scholar
• Culp SJ, Cho BP, Kadlubar FF, Evans FE. Structural and conformational analyses of 8-hydroxy-2′-deoxyguanosine. Chem Res Toxicol 1989;2:416–422.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kasai H, Nishimura S. Hydroxylation of the C-8 position of deoxyguanosine by reducing agents in the presence of oxygen. Nucleic Acids Symp Ser 1983;12:165–167.
   Google Scholar
• Kasai H, Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res 1984;12:2137–2145.
   PubMed Web of Science ®Google Scholar
• Kasai H, Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by polyphenols and aminophenols in the presence of hydrogen peroxide and ferric ion. Gann 1984;75:565–566.
   PubMedGoogle Scholar
• Kasai H, Tanooka H, Nishimura S. Formation of 8-hydroxyguanine residues in DNA by X-irradiation. Gann 1984;75: 1037–1039.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M. Formation of an 8-hydroxyguanine moiety in deoxyribonucleic acid on gamma-irradiation in aqueous solution. Biochemistry 1985;24:4476–4481.
   PubMed Web of Science ®Google Scholar
• Breen AP, Murphy JA. Reactions of oxyl radicals with DNA. Free Radic Biol Med 1995;18:1033–1077.
   PubMed Web of Science ®Google Scholar
• Nishimura S. 8-Hydroxyguanine: a base for discovery. DNA Repair (Amst) 2011;10:1078–1083.
   PubMed Web of Science ®Google Scholar
• Zander R. The distribution space of physically dissolved oxygen in aqueous solutions of organic substances. Z Naturforsch, C: Biosci 1976;31:339–352.
   PubMedGoogle Scholar
• Zander R. Cellular oxygen concentration. Adv Exp Med Biol 1976;75:463–467.
   PubMedGoogle Scholar
• Dizdaroglu M, Kirkali G, Jaruga P. Formamidopyrimidines in DNA: mechanisms of formation, repair, and biological effects. Free Radic Biol Med 2008;45:1610–1621.
   PubMed Web of Science ®Google Scholar
• Boiteux S, Belleney J, Roques BP, Laval J. Two rotameric forms of open ring 7-methylguanine are present in alkylated polynucleotides. Nucleic Acids Res 1984;12:5429–5439.
   PubMed Web of Science ®Google Scholar
• Chetsanga CJ, Makaroff C. Alkaline opening of imidazole ring of 7-methylguanosine. 2. Further studies on reaction mechanisms and products. Chem Biol Interact 1982;41:235–249.
   PubMed Web of Science ®Google Scholar
• Chetsanga CJ, Lindahl T. Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli. Nucleic Acids Res 1979;6:3673–3684.
   PubMed Web of Science ®Google Scholar
• Coste F, Ober M, Carell T, Boiteux S, Zelwer C, Castaing B. Structural basis for the recognition of the FapydG lesion (2,6-diamino-4-hydroxy-5-formamidopyrimidine) by formamidopyrimidine-DNA glycosylase. J Biol Chem 2004;279: 44074–44083.
   PubMed Web of Science ®Google Scholar
• Munk BH, Burrows CJ, Schlegel HB. Exploration of mechanisms for the transformation of 8-hydroxy guanine radical to FAPyG by density functional theory. Chem Res Toxicol 2007;20:432–444.
   PubMed Web of Science ®Google Scholar
• Cysewski P, Olinski R. Theoretical description of the coding potential of diamino-5-formamidopyrimidines. Z Naturforsch [C] 1999;54:239–245.
   PubMed Web of Science ®Google Scholar
• Raoul S, Bardet M, Cadet J. Gamma irradiation of 2′-deoxyadenosine in oxygen-free aqueous solutions: identification and conformational features of formamidopyrimidine nucleoside derivatives. Chem Res Toxicol 1995;8:924–933.
   PubMed Web of Science ®Google Scholar
• Burgdorf LT, Carell T. Synthesis, stability, and conformation of the formamidopyrimidine G DNA lesion. Chem Eur J 2002;8:293–301.
   PubMed Web of Science ®Google Scholar
• Westmore SD, Boyd RJ, Llano J, Lundqvist MJ, Eriksson LA. Hydroxyl radical reactions in biological media. In: Barone V, Bencini A, Fantucci P (eds). Recent advances in density functional methods. Singapore: World Scientific; 2000. pp. 387–415.
   Google Scholar
• Steenken S, Jovanovic SV, Bietti M, Bernhard K. The trap depth (in DNA) of 8-oxo-7,8-dihydro-2′-deoxyguanosine as derived from electron-transfer equilibria in aqeous solution. J Am Chem Soc 2000;122:2373–284.
   Web of Science ®Google Scholar
• Luo W, Muller JG, Rachlin EM, Burrows CJ. Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-Oxo-7,8-dihydroguanosine. Org Lett 2000;2: 613–616.
   PubMed Web of Science ®Google Scholar
• Cadet J, Decarroz C, Wang SY, Midden WR. Mechanisms and products of photosensitized degradation of nucleic acids and related model compounds. Isr J Chem 1983;23:420–429.
   Web of Science ®Google Scholar
• Cadet J, Berger M, Decarroz C, Wagner JR, Van Lier JE, Ginot YM, . Photosensitized reactions of nucleic acids. Biochimie 1986;68:813–834.
   PubMed Web of Science ®Google Scholar
• Buchko GW, Cadet J, Berger M, Ravanat JL. Photooxidation of d(TpG) by phthalocyanines and riboflavin. Isolation and characterization of dinucleoside monophosphas containing the 4R* and 4S* diastereoisomers of 4,8-dihydro-4-hydroxy-8-oxo-2′-deoxy-guanosine. Nucleic Acids Res 1992; 20:4847–4851.
   PubMed Web of Science ®Google Scholar
• Ravanat J-L, Berger M, Benard F, Langlois R, Ouellet R, Van Lier JE, . Phthalocyanine and naphthalocyanine photosensitized oxidation of 2′-deoxyguanosine. Photochem Photobiol 1992;55:809–814.
   Web of Science ®Google Scholar
• 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: 379–388.
   PubMed Web of Science ®Google Scholar
• Luo W, Muller JG, Rachlin EM, Burrows CJ. Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem Res Toxicol 2001;14:927–938.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Burrows CJ, Muller JG, Kornyushyna O, Luo W, Duarte V, Leipold MD, . Structure and potential mutagenicity of new hydantoin products from guanosine and 8-oxo-7,8-dihydroguanine oxidation by transition metals. Environ Health Perspect 2002;110(Suppl 5):713–717.
   PubMedGoogle Scholar
• Adam W, Arnold MA, Grune M, Nau WM, Pischel U, Saha-Moller CR. Spiroiminodihydantoin is a major product in the photooxidation of 2′-deoxyguanosine by the triplet states and oxyl radicals generated from hydroxyacetophenone photolysis and dioxetane thermolysis. Org Lett 2002;4: 537–540.
   PubMed Web of Science ®Google Scholar
• Adam W, Saha-Moller CR, Schonberger A. Photooxidation of 8-oxo-7,8-dihydro-2′-deoxyguanosine by thermally generated triplet-excited ketones from 3-(hydroxymethyl)-3,4,4-trimethyl-1,2-dioxetane and comparison with type I and type II photosensitizers. J Am Chem Soc 1996;118:9 233–9238.
   Web of Science ®Google Scholar
• Luo W, Muller JG, Burrows CJ. The pH-dependent role of superoxide in riboflavin-catalyzed photooxidation of 8-oxo-7,8-dihydroguanosine. Org Lett 2001;3:2801–2804.
   PubMed Web of Science ®Google Scholar
• Adam W, Arnold MA, Nau WM, Pischel U, Saha-Moller CR. A comparative photomechanistic study (spin trapping, EPR spectroscopy, transient kinetics, photoproducts) of nucleoside oxidation (dG and 8-oxodG) by triplet-excited acetophenones and by the radicals generated from alpha-oxy-substituted derivatives through Norrish-type I cleavage. J Am Chem Soc 2002;124:3893–3904.
   PubMed Web of Science ®Google Scholar
• Hickerson RP, Prat F, Muller CE, Foote CS, Burrows CJ. Sequence and stacking dependence of 8-oxoguanine oxidation: comparison of one-electron vs singlet oxygen mechanism. J Am Chem Soc 1999;121:9423–9428.
   Web of Science ®Google Scholar
• Duarte V, Gasparutto D, Yamaguchi LF, Ravanat JL, Martinez GR, Medeiros MHG, . Oxaluric acid as the major product of singlet oxygen-mediated oxidation of 8-oxo-7,8-dihydroguanine in DNA. J Am Chem Soc 2000;122:12622–12628.
   Web of Science ®Google Scholar
• Misiaszek R, Uvaydov Y, Crean C, Geacintov NE, Shafirovich V. Combination reactions of superoxide with 8-Oxo-7,8-dihydroguanine radicals in DNA: kinetics and end products. J Biol Chem 2005;280:6293–6300.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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 2012;25:366–373.
   PubMed Web of Science ®Google Scholar
• Neeley WL, Essigmann JM. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 2006;19:491–505.
   PubMed Web of Science ®Google Scholar
• David SS, O'Shea VL, Kundu S. Base-excision repair of oxidative DNA damage. Nature 2007;447:941–950.
   PubMed Web of Science ®Google Scholar
• ESCODD. 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;23:2129–2133.
   PubMed Web of Science ®Google Scholar
• ESCODD. Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic Biol Med 2003;34:1089–1099.
   PubMed Web of Science ®Google Scholar
• Collins AR, Cadet J, Moller L, Poulsen HE, Vina J. Are we sure we know how to measure 8-oxo-7,8-dihydroguanine in DNA from human cells? Arch Biochem Biophys 2004;423:57–65.
   PubMed Web of Science ®Google Scholar
• Candeias LP, Wolf P, O'Neill P, Steenken S. Reaction of hydrated electrons with guanine nucleosides: fast protonation on carbon of the electron adduct. J Phys Chem 1992;96: 10302–10307.
   Web of Science ®Google Scholar
• D'Angelantonio M, Russo M, Kaloudis P, Mulazzani QG, Wardman P, Guerra M, . Reaction of hydrated electrons with guanine derivatives: tautomerism of intermediate species. J Phys Chem B 2009;113:2170–2176.
   PubMed Web of Science ®Google Scholar
• Vieira AJSC, Steenken S. Pattern of OH radical reactions with N6,N6-dimethyladenosine. Production of three isomeric OH adducts and their dehydration and ring-opening reactions. J Amer Chem Soc 1987;109:7441–7448.
   Web of Science ®Google Scholar
• Vieira AJSC, Steenken S. Pattern of OH radical reaction with adenine and its nucleosides and nucleotides. Characterization of two types of isomeric OH adduct and their unimolecular transformation reactions. J Am Chem Soc 1990;112:6986–6994.
   Web of Science ®Google Scholar
• Nackerdien Z, Kasprzak KS, Rao G, Halliwell B, Dizdaroglu M. Nickel(II)- and cobalt(II)-dependent damage by hydrogen peroxide to the DNA bases in isolated chromatin. Cancer Res 1991;51:5837–5842.
   PubMed Web of Science ®Google Scholar
• Kasprzak KS, Diwan BA, Rice JM, Misra M, Riggs CW, Olinski R, . Nickel(II)-mediated oxidative DNA base damage in renal and hepatic chromatin of pregnant rats and their fetuses. Possible relevance to carcinogenesis. Chem Res Toxicol 1992;5:809–815.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M. Oxidative damage to DNA in mammalian chromatin. Mutat Res 1992;275:331–342.
   PubMed Web of Science ®Google Scholar
• Hissung A, von Sonntag C, Veltwisch D, Asmus KD. The reactions of the 2′-deoxyadenosine electron adduct in aqueous solution. The effects of the radiosensitizer p-nitroacetophenone. A pulse spectroscopic and pulse conductometric study. Int J Radiat Biol Relat Stud Phys Chem Med 1981;39:63–71.
   PubMed Web of Science ®Google Scholar
• Visscher KJ, Spoelder HJ, Loman H, Hummel A, Hom ML. Kinetics and mechanism of electron transfer between purines and pyrimidines, their dinucleotides and polynucleotides after reaction with hydrated electrons; a pulse radiolysis study. Int J Radiat Biol 1988;54:787–802.
   PubMed Web of Science ®Google Scholar
• Candeias LP, Steenken S. Electron adducts of adenine nucleosides and nucleotides in aqueous solution: protonation at two carbon sites (C2 and C8) and intra- and intermolecular catalysis by phosphate. J Phys Chem 1992;96: 937–944.
   Web of Science ®Google Scholar
• Fujita S, Steenken S. Pattern of OH radical addition to uracil and methyl- and carboxyl-substituted uracils. Electron transfer of OH adducts with N,N,N′,N′-tetramethyl-p-phenylenediamine and tetranitromethane. J Am Chem Soc 1981;103: 2540–2545.
   Web of Science ®Google Scholar
• Al-Sheikly, von Sonntag C. γ−Radiolysis of 1,3-dimethyluracil in N2O-saturated aqueous solution. Zeitschrift für Naturforschung 1983;38b:1622–1629.
   Google Scholar
• Lemaire DG, Bothe E, Schulte-Frohlinde D. Yields of radiation-induced main chain scission of poly U in aqueous solution: strand break formation via base radicals. Int J Radiat Biol Relat Stud Phys Chem Med 1984;45:351–358.
   PubMed Web of Science ®Google Scholar
• Karam LR, Dizdaroglu M, Simic MG. Intramolecular H atom abstraction from the sugar moiety by thymine radicals in oligo- and polydeoxynucleotides. Radiat Res 1988;116: 210–216.
   PubMed Web of Science ®Google Scholar
• Willson RL. The reaction of oxygen with radiation-induced free radicals in DNA and related compounds. Int J Radiat Biol Relat Stud Phys Chem Med 1970;17:349–358.
   PubMed Web of Science ®Google Scholar
• Teoule R. Radiation-induced DNA damage and its repair. Int J Radiat Biol 1987;51:573–589.
   Web of Science ®Google Scholar
• Kasai H, Iida A, Yamaizumi Z, Nishimura S, Tanooka H. 5-Formyldeoxyuridine: a new type of DNA damage induced by ionizing radiation and its mutagenicity to salmonella strain TA102. Mutat Res 1990;243:249–253.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Das S, Deeble DJ, von SC. Site of H atom attack on uracil and its derivatives in aqueous solution. Z Naturforsch 1985;40C:292–294.
   Google Scholar
• Furlong EA, Jorgensen TJ, Henner WD. Production of dihydrothymidine stereoisomers in DNA by γ-irradiation. Biochemistry 1986;25:4344–4349.
   PubMed Web of Science ®Google Scholar
• Michaels HB, Hunt JW. Reactions of the hydroxyl radical with polynucleotides. Radiat Res 1973;56:57–70.
   PubMed Web of Science ®Google Scholar
• Hazra DK, Steenken S. Pattern of OH radical addition to cytosine and 1-, 3-, 5-, and 6-substituted cytosines. Electron tranfer and dehydration reactions of OH adducts. J Am Chem Soc 1983;105:4380–436.
   Web of Science ®Google Scholar
• Simic M, Hayon E. A model of radiation sensitization by quinones. Int J Radiat Biol Relat Stud Phys Chem Med 1972;22:507–511.
   PubMed Web of Science ®Google Scholar
• Rao PS, Hayon E. One-electron redox reactions of free radicals in solution. Rate of electron transfer processes to quinones. Biochim Biophys Acta 1973;292:516–533.
   PubMedGoogle Scholar
• Dizdaroglu M, Holwitt E, Hagan MP, Blakely WF. Formation of cytosine glycol and 5,6-dihydroxycytosine in deoxyribonucleic acid on treatment with osmium tetroxide. Biochem J 1986;235:531–536.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Laval J, Boiteux S. Substrate specificity of Escherischia coli endonuclease III: excision of thymine- and cytosine-derived lesions in DNA produced by ionizing radiation-generated free radicals. Biochemistry 1993;32: 12105–12111.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Bauche C, Rodriguez H, Laval J. Novel substrates of Escherichia coli Nth protein and its kinetics for excision of modified bases from DNA damaged by free radicals. Biochemistry 2000;39:5586–5592.
   PubMed Web of Science ®Google Scholar
• Wagner JR. Analysis of oxidative cytosine products in DNA exposed to ionizing radiation. J Chim Phys 1994;91: 1280–1286.
   Google Scholar
• Behrend R, Roosen O. Synthese der Harnsäure. Justus Liebigs Ann Chem 1889;251:235–256.
   Google Scholar
• Richardson GM. The autoxidation of dialuric acid. Biochem J 1932;26:1959–1977.
   PubMedGoogle Scholar
• Dizdaroglu M. Quantitative determination of oxidative base damage in DNA by stable isotope-dilution mass spectrometry. FEBS Lett 1993;315:1–6.
   PubMed Web of Science ®Google Scholar
• Wagner JR, Blount BC, Weinfeld M. Excision of oxidative cytosine modifications from gamma-irradiated DNA by Escherichia coli endonuclease III and human whole-cell extracts. Anal Biochem 1996;233:76–86.
   PubMed Web of Science ®Google Scholar
• Hissung A, von SC. The reaction of solvated electrons with cytosine, 5-methyl cytosine and 2′-deoxycytidine in squeous solution. The reaction of the electron adduct intermediates with water, p-nitroacetophenone and oxygen. A pulse spectroscopic and pulse conductometric study. Int J Radiat Biol Relat Stud Phys Chem Med 1979;35:449–458.
   PubMedGoogle Scholar
• Dizdaroglu M, Jaruga P, Birincioglu M, Rodriguez H. Free radical-induced damage to DNA: mechanisms and measurement. Free Radic Biol Med 2002;32:1102–1115.
   PubMed Web of Science ®Google Scholar
• Cadet J, Douki T, Ravanat JL. Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 2010;49:9–21.
   PubMed Web of Science ®Google Scholar
• Deeble DJ, Schulz D, von SC. Reactions of OH radicals with poly(U) in deoxygenated solutions: sites of OH radical attack and the kinetics of base release. Int J Radiat Biol Relat Stud Phys Chem Med 1986;49:915–926.
   PubMed Web of Science ®Google Scholar
• Deeble DJ, von SC. Gamma-radiolysis of poly(U) in aqueous solution. The role of primary sugar and base radicals in the release of undamaged uracil. Int J Radiat Biol Relat Stud Phys Chem Med 1984;46:247–260.
   PubMed Web of Science ®Google Scholar
• Deeble DJ, von SC. Radiolysis of poly(U) in oxygenated solution. Int J Radiat Biol Relat Stud Phys Chem Med 1986;49:927–936.
   PubMed Web of Science ®Google Scholar
• Lemaire DG, Bothe E, Schulte-Frohlinde D. Hydroxyl radical-induced strand break formation of poly(U) in anoxic solution. Effect of dithiothreitol and tetranitromethane. Int J Radiat Biol Relat Stud Phys Chem Med 1987;51:319–330.
   PubMed Web of Science ®Google Scholar
• Hildenbrand K, Schulte-Frohlinde D. E.s.r. studies on the mechanism of hydroxyl radical-induced strand breakage of polyuridylic acid. Int J Radiat Biol 1989;55:725–738.
   PubMed Web of Science ®Google Scholar
• Jones GD, O'Neill P. Kinetics of radiation-induced strand break formation in single-stranded pyrimidine polynucleotides in the presence and absence of oxygen; a time-resolved light-scattering study. Int J Radiat Biol 1991;59:1127–1145.
   PubMed Web of Science ®Google Scholar
• Hildenbrand K, Mirtsch S, Schulte-Frohlinde D. 1H NMR studies of gamma-irradiated polynucleotides and DNA in N2O-saturated aqueous solutions: release of undamaged and modified bases. Radiat Res 1993;134:283–294.
   PubMed Web of Science ®Google Scholar
• Pardo L, Banfelder JR, Osman R. Theoretical studies of the kinetics, thermochemistry, and mechanism of H-abstraction from methanol and ethanol. J Am Chem Soc 1992;114: 2382–2390.
   Web of Science ®Google Scholar
• Miaskiewicz K, Osman R. Theoretical study on the deoxyribose radicals formed by hydrogen abstraction. J Am Chem Soc 1994;116:232–238.
   Web of Science ®Google Scholar
• Sy D, Savoye C, Begusova M, Michalik V, Charlier M, Spotheim-Maurizot M. Sequence-dependent variations of DNA structure modulate radiation-induced strand breakage. Int J Radiat Biol 1997;72:147–155.
   PubMed Web of Science ®Google Scholar
• Begusova M, Spotheim-Maurizot M, Sy D, Michalik V, Charlier M. RADACK, a stochastic simulation of hydroxyl radical attack to DNA. J Biomol Struct Dyn 2001;19:141–158.
   PubMed Web of Science ®Google Scholar
• Toure P, Villena F, Melikyan GG. Thymidine 3′,5′-diphosphoric acid derived cations and radicals: ab initio study. Org Lett 2002;4:3989–3992.
   PubMed Web of Science ®Google Scholar
• Balasubramanian B, Pogozelski WK, Tullius TD. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc Natl Acad Sci USA 1998;95:9738–9743.
   PubMed Web of Science ®Google Scholar
• Pogozelski WK, Tullius TD. Oxidative strand scission of nucleic acids: routes initiated by hydrogen abstraction from the sugar moiety. Chem Rev 1998;98:1089–1108.
   PubMed Web of Science ®Google Scholar
• Stelter L, von SC, Schulte-Frohlinde D. Letter: radiation chemistry of DNA-model compounds. V. Phosphate elimination from ribose-5-phosphate after OH radical attack at C-4. Int J Radiat Biol Relat Stud Phys Chem Med 1974;25:515–519.
   PubMed Web of Science ®Google Scholar
• Stelter L, von Sonntag C, Schulte-Frohlinde D. Phosphate ester cleavage in ribose-5-phosphate induced by OH radicals in deoxygenated aqueous solution. The effect of Fe(II) and Fe(III) ions. Int J Radiat Biol Relat Stud Phys Chem Med 1976;29:255–269.
   PubMed Web of Science ®Google Scholar
• Behrens G, Koltzenburg G, Ritter A, Schulte-Frohlinde D. The influence of protonation or alkylation of the phosphate group on the e.s.r. spectra and on the rate of phosphate elimination from 2-methoxyethyl phosphate 2-yl radicals. Int J Radiat Biol Relat Stud Phys Chem Med 1978;33:163–171.
   PubMed Web of Science ®Google Scholar
• Behrens G, Koltzenburg G, Schulte-Frohlinde D. Model reactions for the degradation of DNA-4′ radicals in aqueous solution. Fast hydrolysis of α-alkoxyalkyl radicals with a leaving group in β-position followed by radical rearrangement and elimination reactions. Zeitschrift fuer Naturforschung 1982;37c:1205–1227.
   Google Scholar
• Beesk F, Dizdaroglu M, Schulte-Frohlinde D, von Sonntag C. Radiation-induced DNA strand breaks in deoxygenated aqueous solutions. The formation of altered sugars as end groups. Int J Radiat Biol Relat Stud Phys Chem Med 1979;36:565–576.
   PubMed Web of Science ®Google Scholar
• Henner WD, Rodriguez LO, Hecht SM, Haseltine WA. Gamma-Ray induced deoxyribonucleic acid strand breaks. 3′ Glycolate termini. J Biol Chem 1983;258:711–713.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Schulte-Frohlinde D, von Sonntag C. Isolation of 2-deoxy-D-erythro-pentonic acid from an alkali labile site in gamma-irradiated DNA. Int J Radiat Biol 1977;32:481–483.
   Web of Science ®Google Scholar
• Dizdaroglu M, Schulte-Frohlinde D, von Sonntag C. Radiolysis of DNA in oxygenated aqueous solution. Structure of an alkali labile site. Z Naturforsch 1977;32c:1021–1022.
   Google Scholar
• Keck K. Bildung von Cyclonucleotiden bei Betrahlung wässriger Lösungen von Purinnucleotiden. Z Naturforsch B 1968;23:1034–1043.
   PubMedGoogle Scholar
• Pullman B, Pullman A. Submolecular structure of the nucleic acids. Nature 1961;189:725–727.
   PubMed Web of Science ®Google Scholar
• Raleigh JA, Kremers W, Whitehouse R. Radiation chemistry of nucleotides: 8,5′-cyclonucleotide formation and phosphate release initiated by hydroxyl radical attack on adenosine monophosphates. Radiat Res 1976;65:414–422.
   PubMed Web of Science ®Google Scholar
• Mariaggi N, Cadet J, Téoule R. Cyclysation radicalaire de la desoxy-2′-adenosine en solution aqueous, sous l'effet du rayonnement gamma. Tetrahedron 1976;32:2385–2387.
   Web of Science ®Google Scholar
• Raleigh JA, Blackburn BJ. Substrate conformation in 5′-AMP-utilizing enzymes: 8,5′-cycloadenosine 5′-monophosphate. Biochem Biophys Res Commun 1978;83: 1061–1066.
   PubMed Web of Science ®Google Scholar
• Haromy TP, Raleigh J, Sundaralingam M. Enzyme-bound conformations of nucleotide substrates. X-ray structure and absolute configuration of 8,5′-cycloadenosine monohydrate. Biochemistry 1980;19:1718–1722.
   PubMed Web of Science ®Google Scholar
• Fuciarelli AF, Miller GG, Raleigh JA. An immunochemical probe for 8,5′-cycloadenosine-5′-monophosphate and its deoxy analog in irradiated nucleic acids. Radiat Res 1985;104:272–283.
   PubMed Web of Science ®Google Scholar
• Raleigh JA, Fuciarelli AF. Distribution of damage in irradiated 5′-AMP: 8,5′-cyclo-AMP, 8-hydroxy-AMP, and adenine release. Radiat Res 1985;102:165–175.
   Web of Science ®Google Scholar
• Fuciarelli AF, Shum FY, Raleigh JA. Stereoselective intramolecular cyclization in irradiated nucleic acids: R- and S-8,5′-cycloadenosine in polyadenylic acid. Biochem Biophys Res Commun 1986;134:883–887.
   PubMed Web of Science ®Google Scholar
• Alexander AJ, Kebarle P, Fuciarelli AF, Raleigh JA. Characterization of radiation-induced damage to polyadenylic acid using high-performance liquid chromatography/tandem mass spectrometry. Anal Chem 1987;59:2484–2491.
   PubMed Web of Science ®Google Scholar
• Fuciarelli AF, Shum FY, Raleigh JA. Intramolecular cyclization in irradiated nucleic acids: correlation between high-performance liquid chromatography and an immunochemical assay for 8,5′-cycloadenosine in irradiated poly(A). Radiat Res 1987;110:35–44
   PubMed Web of Science ®Google Scholar
• Fuciarelli AF, Mele FG, Raleigh JA. Interaction of nitroaromatic radiosensitizers with irradiated polyadenylic acid as measured by an indirect immunochemical assay with specificity for the 8,5′-cycloadenosine moiety. Int J Radiat Biol Relat Stud Phys Chem Med 1987;51:629–639.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M. Free-radical-induced formation of an 8,5′-cyclo-2′-deoxyguanosine moiety in deoxyribonucleic acid. Biochem J 1986;238:247–254.
   PubMed Web of Science ®Google Scholar
• Dirksen ML, Blakely WF, Holwitt E, Dizdaroglu M. Effect of DNA conformation on the hydroxyl radical-Induced formation of 8,5′-cyclopurine-2′-deoxyribonucleoside residues in DNA. Int J Radiat Biol 1988;54:195–204.
   PubMed Web of Science ®Google Scholar
• Birincioglu M, Jaruga P, Chowdhury G, Rodriguez H, Dizdaroglu M, Gates KS. DNA base damage by the antitumor agent 3-amino-1,2,4-benzotriazine 1,4-dioxide (tirapazamine). J Am Chem Soc 2003;125:11607–11615.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Dirksen ML, Jiang HX, Robbins JH. Ionizing-radiation-induced damage in the DNA of cultured human cells. Identification of 8,5′-cyclo-2′-deoxyguanosine. Biochem J 1987;241:929–932.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Guerra M, Mulazzani QG. Model studies of DNA C5′ radicals. Selective generation and reactivity of 2′-deoxyadenosin-5′-yl radical. J Am Chem Soc 2003;125: 3839–3848.
   PubMed Web of Science ®Google Scholar
• Manetto A, Georganakis D, Leondiadis L, Gimisis T, Mayer P, Carell T, . Independent generation of C5′-nucleosidyl radicals in thymidine and 2′-deoxyguanosine. J Org Chem 2007;72:3659–3666.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Ferreri C, Terzidis MA. Purine 5′, 8-cyclonucleoside lesions: chemistry and biology. Chem Soc Rev 2011;40:1368–1382.
   PubMed Web of Science ®Google Scholar
• Fuciarelli AF, Koch CJ, Raleigh JA. Oxygen dependence of product formation in irradiated adenosine 5′-monophosphate. Radiat Res 1988;113:447–457.
   PubMed Web of Science ®Google Scholar
• Boussicault F, Kaloudis P, Caminal C, Mulazzani QG, Chatgilialoglu C. The fate of C5’ radicals of purine nucleosides under oxidative conditions. J Am Chem Soc 2008;130: 8377–8385.
   PubMed Web of Science ®Google Scholar
• Belmadoui N, Boussicault F, Guerra M, Ravanat JL, 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.
   PubMed Web of Science ®Google Scholar
• Meister A, Anderson ME. Glutathione. Annu Rev Biochem 1983;52:711–760.
   PubMed Web of Science ®Google Scholar
• Hampton A, Harper PJ, Sasaki T. Substrate properties of cycloadenosines with adenosine aminohydrolase as evidence for the conformation of enzyme-bound adenosine. Biochemistry 1972;11:4736–4739.
   PubMed Web of Science ®Google Scholar
• Birnbaum GI, Cygler M, Dudycz L, Stolarski R, Shugar D. Comparison of solid state and solution conformations of R and S epimers of 8,5′-cycloadenosine and their relevance to some enzymatic reactions. Biochemistry 1981;20: 3294–3301.
   PubMed Web of Science ®Google Scholar
• Schroder E, Budzinski EE, Wallace JC, Zimbrick JD, Box HC. Radiation chemistry of d(ApCpGpT). Int J Radiat Biol 1995;68:509–523.
   PubMed Web of Science ®Google Scholar
• Miaskiewicz K, Miller JH, Fuciarelli AF. Theoretical analysis of DNA intrastrand cross linking by formation of 8,5′-cyclodeoxyadenosine. Nucleic Acids Res 1995;23:515–521.
   PubMed Web of Science ®Google Scholar
• Flyunt R, Bazzanini R, Chatgilialoglu C, Mulazzani QG. Fate of the 2′-deoxyadenosyl-5′-radical under anaerobic conditions. J Am Chem Soc 2000;122:4225–4226.
   Web of Science ®Google Scholar
• Dizdaroglu M, Jaruga P, Rodriguez H. Identification and quantification of 8,5′-cyclo-2′-deoxyadenosine in DNA by liquid chromatography/mass spectrometry. Free Radic Biol Med 2001;30:774–784.
   PubMed Web of Science ®Google Scholar
• 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: 3703–3711.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Duca M, Ferreri C, Guerra M, Ioele M, Mulazzani QG, . Selective generation and reactivity of 5′-adenosinyl and 2′-adenosinyl radicals. Chemistry 2004;10: 1249–1255.
   PubMed Web of Science ®Google Scholar
• Navacchia ML, Chatgilialoglu C, Montevecchi PC. C5′-adenosinyl radical cyclization. A stereochemical investigation. J Org Chem 2006;71:4445–4452.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Bazzanini R, Jimenez LB, Miranda MA. (5′S)- and (5′R)-5′,8-cyclo-2′-deoxyguanosine: mechanistic insights on the 2′-deoxyguanosin-5′-yl radical cyclization. Chem Res Toxicol 2007;20:1820–1824.
   PubMed Web of Science ®Google Scholar
• Karwowski BT, Gaillard J, Grand A, Cadet J. Effect of (5′S)-5′,8-cyclo-2′-deoxyadenosine on the conformation of di and trinucleotides. A NMR and DFT study. Org Biomol Chem 2008;6:3408–3413.
   PubMed Web of Science ®Google Scholar
• Jaruga P, Theruvathu J, Dizdaroglu M, Brooks PJ. Complete release of (5′S)-8,5′-cyclo-2′-deoxyadenosine from dinucleotides, oligodeoxynucleotides and DNA, and direct comparison of its levels in cellular DNA with other oxidatively induced DNA lesions. Nucleic Acids Res 2005; 32:e87.
   Web of Science ®Google Scholar
• Egler RA, Fernandes E, Rothermund K, Sereika S, de Souza-Pinto N, Jaruga P, . Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1. Oncogene 2005;24:8038–8050.
   PubMed Web of Science ®Google Scholar
• Malins DC, Anderson KM, Stegeman JJ, Jaruga P, Green VM, Gilman NK, . Biomarkers signal contaminant effects on the organs of English sole (Parophrys vetulus) from Puget Sound. Environ Health Perspect 2006;114:823–829.
   PubMed Web of Science ®Google Scholar
• Anderson KM, Jaruga P, Ramsey CR, Gilman NK, Green VM, Rostad SW, . Structural alterations in breast stromal and epithelial DNA: the influence of 8,5′-cyclo-2′-deoxyadenosine. Cell Cycle 2006;5:1240–1244.
   PubMed Web of Science ®Google Scholar
• D'Errico M, Parlanti E, Teson M, 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.
   PubMed Web of Science ®Google Scholar
• Nyaga SG, Jaruga P, Lohani A, Dizdaroglu M, Evans MK. Accumulation of oxidatively induced DNA damage in human breast cancer cell lines following treatment with hydrogen peroxide. Cell Cycle 2007;6:1472–1478.
   PubMed Web of Science ®Google Scholar
• Rodriguez H, Jaruga P, Leber D, Nyaga SG, Evans MK, Dizdaroglu M. Lymphoblasts of women with BRCA1 mutations are deficient in cellular repair of 8,5′-Cyclopurine-2′-deoxynucleosides and 8-hydroxy-2′-deoxyguanosine. Biochemistry 2007;46:2488–2496.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kirkali G, Tunca M, Genc S, Jaruga P, Dizdaroglu M. Oxidative DNA damage in polymorphonuclear leukocytes of patients with familial Mediterranean fever. Free Radic Biol Med 2008;44:386–393.
   PubMed Web of Science ®Google Scholar
• Gokce G, Ozsarlak-Sozer G, Oktay G, Kirkali G, Jaruga P, Dizdaroglu M, . Glutathione depletion by buthionine sulfoximine induces oxidative damage to DNA in organs of rabbits in vivo. Biochemistry 2009;48:4980–4987.
   PubMed Web of Science ®Google Scholar
• Kirkali G, de Souza-Pinto NC, Jaruga P, Bohr VA, Dizdaroglu M. Accumulation of (5′S)-8,5′-cyclo-2′-deoxyadenosine in organs of Cockayne syndrome complementation group B gene knockout mice. DNA Repair (Amst) 2009;8:274–278.
   PubMed Web of Science ®Google Scholar
• Jaruga P, Xiao Y, Nelson BC, Dizdaroglu M. Measurement of (5′R)- and (5′S)-8,5′-cyclo-2′-deoxyadenosines in DNA in vivo by liquid chromatography/isotope-dilution tandem mass spectrometry. Biochem Biophys Res Commun 2009;386:656–660.
   PubMed Web of Science ®Google Scholar
• Jaruga P, Xiao Y, Vartanian V, Lloyd RS, Dizdaroglu M. Evidence for the involvement of DNA repair enzyme NEIL1 in nucleotide excision repair of (5′R)- and (5′S)-8,5′-cyclo-2′-deoxyadenosines. Biochemistry 2010;49:1053–1055.
   PubMed Web of Science ®Google Scholar
• Jaruga P, Dizdaroglu M. Identification and quantification of (5′R)- and (5′S)-8,5′-cyclo-2′-deoxyadenosines in human urine as putative biomarkers of oxidatively induced damage to DNA. Biochem Biophys Res Commun 2010;397:48–52.
   PubMed Web of Science ®Google Scholar
• Wang J, Yuan B, Guerrero C, Bahde R, Gupta S, Wang Y. 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 2011;83: 2201–2209.
   PubMed Web of Science ®Google Scholar
• Kirkali G, Keles D, Canda AE, Terzi C, Reddy PT, Jaruga P, . Evidence for upregulated repair of oxidatively induced DNA damage in human colorectal cancer. DNA Repair 2011;10:1114–1120.
   PubMed Web of Science ®Google Scholar
• Jaruga P, Dizdaroglu M. 8,5′-Cyclopurine-2′-deoxynucleosides in DNA: mechanisms of formation, measurement, repair and biological effects. DNA Repair (Amst) 2008;7: 1413–1425.
   PubMed Web of Science ®Google Scholar
• Shaw AA, Cadet J. Formation of cyclopyrimidines via the direct effects of gamma radiation of pyrimidine nucleosides. Int J Radiat Biol 1988;54:987–997.
   PubMed Web of Science ®Google Scholar
• Wagner JR, Decarroz C, Berger M, Cadet J. Hydroxyl- radical-induced decomposition of 2′-deoxycytidine in aerated aqueous solutions. J Am Chem Soc 1999;121:4101– 4110.
   Web of Science ®Google Scholar
• Box HC, Budzinski EE, Freund HG, Evans MS, Patrzyc HB, Wallace JC, . Vicinal lesions in X-irradiated DNA? Int J Radiat Biol 1993;64:261–263.
   PubMed Web of Science ®Google Scholar
• Budzinski EE, MacCubbin AE, Freund HG, Wallace JC, Box HC. Characterization of the products of dinucleoside monophosphates d(GpN) irradiated in aqueous solutions. Radiat Res 1993;136:171–177.
   PubMed Web of Science ®Google Scholar
• Budzinski EE, Dawidzik JD, Wallace JC, Freund HG, Box HC. The radiation chemistry of d(CpGpTpA) in the presence of oxygen. Radiat Res 1995;142:107–109.
   PubMed Web of Science ®Google Scholar
• Box HC, Freund HG, Budzinski EE, Wallace JC, MacCubbin AE. Free radical-induced double base lesions. Radiat Res 1995;141:91–94.
   PubMed Web of Science ®Google Scholar
• Box HC, Budzinski EE, Dawidzik JB, Gobey JS, Freund HG. Free radical-induced tandem base damage in DNA oligomers. Free Radic Biol Med 1997;23:1021–1030.
   PubMed Web of Science ®Google Scholar
• Box HC, Patrzyc HB, Dawidzik JB, Wallace JC, Freund HG, Iijima H, . Double base lesions in DNA X-irradiated in the presence or absence of oxygen. Radiat Res 2000;153: 442–446.
   PubMed Web of Science ®Google Scholar
• MacCubbin AE, Iijima H, Ersing N, Dawidzik JB, Patrzyc HB, . Double-base lesions are produced in DNA by free radicals. Arch Biochem Biophys 2000;375:119–123.
   PubMed Web of Science ®Google Scholar
• Patrzyc HB, Dawidzik JB, Budzinski EE, Iijima H, Box HC. Double lesions are produced in DNA oligomer by ionizing radiation and by metal-catalyzed H2O2 reactions. Radiat Res 2001;155:634–636.
   PubMed Web of Science ®Google Scholar
• Bourdat A-G, Douki T, Frelon S, Gasparutto D, Cadet J. Tandem base lesions are generated by hydroxyl radical within isolated DNA in aerated aqueous solution. J Am Chem Soc 2000;122:4549–4566.
   Web of Science ®Google Scholar
• Douki T, Riviere J, Cadet J. 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 2002;15:445–454.
   PubMed Web of Science ®Google Scholar
• Cadet J, Bellon S, Berger M, Bourdat AG, Douki T, Duarte V, . Recent aspects of oxidative DNA damage: guanine lesions, measurement and substrate specificity of DNA repair glycosylases. Biol Chem 2002;383:933–943.
   PubMed Web of Science ®Google Scholar
• Box HC, Budzinski EE, Dawidzik JD, Wallace JC, Evans MS, Gobey JS. Radiation-induced formation of a crosslink between base moieties of deoxyguanosine and thymidine in deoxygenated solutions of d(CpGpTpA). Radiat Res 1996;145:641–643.
   PubMed Web of Science ®Google Scholar
• Box HC, Budzinski EE, Dawidzik JB, Wallace JC, Iijima H. Tandem lesions and other products in X-irradiated DNA oligomers. Radiat Res 1998;149:433–439.
   PubMed Web of Science ®Google Scholar
• Romieu A, Bellon S, Gasparutto D, Cadet J. Synthesis and UV photolysis of oligodeoxynucleotides that contain 5-(phenylthiomethyl)-2′-deoxyuridine: a specific photolabile precursor of 5-(2′-deoxyuridilyl)methyl radical. Org Lett 2000;2:1085–1088.
   PubMed Web of Science ®Google Scholar
• Bellon S, Ravanat JL, 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.
   PubMed Web of Science ®Google Scholar
• Hong H, Cao H, Wang Y, Wang Y. Identification and quantification of a guanine-thymine intrastrand cross-link lesion induced by Cu(II)/H2O2/ascorbate. Chem Res Toxicol 2006;19:614–621.
   PubMed Web of Science ®Google Scholar
• Bellon S, Gasparutto D, Saint-Pierre C, Cadet J. Guanine-thymine intrastrand cross-linked lesion containing oligonucleotides: from chemical synthesis to in vitro enzymatic replication. Org Biomol Chem 2006;4:3831–3837.
   PubMed Web of Science ®Google Scholar
• Labet V, Morell C, Grand A, Cadet J, Cimino P, Barone V. Formation of cross-linked adducts between guanine and thymine mediated by hydroxyl radical and one-electron oxidation: a theoretical study. Org Biomol Chem 2008;6:3300–3305.
   PubMed Web of Science ®Google Scholar
• Wang Y. Bulky DNA lesions induced by reactive oxygen species. Chem Res Toxicol 2008;21:276–281.
   PubMed Web of Science ®Google Scholar
• Xerri B, Morell C, Grand A, Cadet J, Cimino P, Barone V. Radiation-induced formation of DNA intrastrand crosslinks between thymine and adenine bases: a theoretical approach. Org Biomol Chem 2006;4:3986–3992.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wang Y. Independent generation of 5-(2′-deoxycytidyl)methyl radical and the formation of a novel crosslink lesion between 5-methylcytosine and guanine. J Am Chem Soc 2003;125:12795–12802.
   PubMed Web of Science ®Google Scholar
• Zang Q, Wang Y. Generation of 5-(2′-deoxycytidyl)methyl radical and the formation of intrastrand cross-link lesions in oligodeoxyribonucleosides. Nucleic Acids Res 2005;33: 1593–1603.
   PubMed Web of Science ®Google Scholar
• Cao H, Wang Y. Quantification of oxidative single-base and intrastrand cross-link lesions in unmethylated and CpG-methylated DNA induced by Fenton-type reagents. Nucleic Acids Res 2007;35:4833–4844.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hong H, Cao H, Wang Y. Formation and genotoxicity of a guanine-cytosine intrastrand cross-link lesion in vivo. Nucleic Acids Res 2007;35:7118–7127.
   PubMed Web of Science ®Google Scholar
• Hong IS, Greenberg MM. Efficient DNA interstrand cross-link formation from a nucleotide radical. J Am Chem Soc 2005;127:3692–3693.
   PubMed Web of Science ®Google Scholar
• Hong IS, Ding H, Greenberg MM. Oxygen independent DNA interstrand cross-link formation by a nucleotide radical. J Am Chem Soc 2006;128:485–491.
   PubMed Web of Science ®Google Scholar
• Ding H, Greenberg MM. Gamma-radiolysis and hydroxyl radical produce interstrand cross-links in DNA involving thymidine. Chem Res Toxicol 2007;20:1623–1628.
   PubMed Web of Science ®Google Scholar
• Dink H, Majumdar A, Tolman JR, Greenberg MM. Multinuclear NMR and kinetic analysis of DNA interstrand cross-link formation. J Am Chem Soc 2008;130:17981–17987.
   PubMed Web of Science ®Google Scholar
• Ward JF. Some biochemical consequences of the spatial distribution of ionizing radiation-produced free radicals. Radiat Res 1981;86:185–195.
   PubMed Web of Science ®Google Scholar
• Ward JF. Biochemistry of DNA lesions. Radiat Res Suppl 1985;8:S103–S111.
   PubMedGoogle Scholar
• Goodhead DT. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol 1994;65:7–17.
   PubMed Web of Science ®Google Scholar
• Ward JF. The complexity of DNA damage: relevance to biological consequences. Int J Radiat Biol 1994;66:427–432.
   PubMed Web of Science ®Google Scholar
• Sutherland BM, Bennett PV, Sidorkina O, Laval J. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc Natl Acad Sci USA 2000;97:103–108.
   PubMed Web of Science ®Google Scholar
• David-Cordonnier MH, Laval J, O'Neill P. Clustered DNA damage, influence on damage excision by XRS5 nuclear extracts and Escherichia coli Nth and Fpg proteins. J Biol Chem 2000;275:11865–11873.
   PubMed Web of Science ®Google Scholar
• Blaisdell JO, Harrison L, Wallace SS. Base excision repair processing of radiation-induced clustered DNA lesions. Radiat Prot Dosimetry 2001;97:25–31.
   PubMed Web of Science ®Google Scholar
• Sutherland BM, Bennett PV, Sutherland JC, Laval J. Clustered DNA damages induced by x rays in human cells. Radiat Res 2002;157:611–616.
   PubMed Web of Science ®Google Scholar
• Regulus P, Duroux B, Bayle PA, Favier A, Cadet J, Ravanat JL. 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 U S A 2007;104: 14032–14037.
   PubMed Web of Science ®Google Scholar
• Georgakilas AG. Processing of DNA damage clusters in human cells: current status of knowledge. Mol Biosyst 2008; 4:30–35.
   PubMed Web of Science ®Google Scholar
• Eccles LJ, O'Neill P, Lomax ME. Delayed repair of radiation induced clustered DNA damage: friend or foe? Mutat Res 2011;711:134–141.
   PubMed Web of Science ®Google Scholar
• Kryston TB, Georgiev AB, Pissis P, Georgakilas AG. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 2011;711:193–201.
   PubMed Web of Science ®Google Scholar
• Sage E, Harrison L. Clustered DNA lesion repair in eukaryotes: relevance to mutagenesis and cell survival. Mutat Res 2011;711:123–133.
   PubMed Web of Science ®Google Scholar
• Sutherland BM, Bennett PV, Cintron NS, Guida P, Laval J. Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs. Free Radic Biol Med 2003;35:495–503.
   PubMed Web of Science ®Google Scholar
• Bennett PV, Cintron NS, Gros L, Laval J, Sutherland BM. Are endogenous clustered DNA damages induced in human cells? Free Radic Biol Med 2004;37:488–499.
   PubMed Web of Science ®Google Scholar
• Fornace AJ Jr, Little JB. DNA-protein cross-linking by chemical carcinogens in mammalian cells. Cancer Res 1979;39:704–710.
   Google Scholar
• Yamamoto O.Ionizing radiation-induced DNA-protein cross-linking. In: Smith KC, ed. Aging, Carcinogenesis, and Radiation Biology. New York: Plenum Press; 1976. p. 165–192.
   Google Scholar
• Cress AE, Bowden GT. Covalent DNA-protein cross-linking occurs after hyperthermia and radiation. Radiat Res 1983;95:610–618.
   PubMed Web of Science ®Google Scholar
• Lesko SA, Drocourt JL, Yang SU. Deoxyribonucleic acid-protein and deoxyribonucleic acid interstrand cross-links induced in isolated chromatin byhydrogen peroxide and ferrous ethylenediaminetetraacetate chelates. Biochemistry 1982;21:5010–5015.
   PubMed Web of Science ®Google Scholar
• Mee LK, Adelstein SJ. Predominance of core histones in formation of DNA-protein cross-links in g-irradiated chromatin. Proc Natl Acad Sci (U S A) 1981;78:2194–2198.
   PubMed Web of Science ®Google Scholar
• Oleinick NL, Chiu S, Ramakrishnan N, Xue L. The formation, identification, and significance of DNA-protein cross-links in mammalian cells. Brit J Cancer 1987;55(Suppl VIII):135–140.
   PubMedGoogle Scholar
• Mee LK, Adelstein SJ. Radiolysis of chromatin extracted from cultured mammalian cells: formation of DNA-protein cross links. Int J Radiat Biol 1979;36:359–366.
   Web of Science ®Google Scholar
• Dizdaroglu M. The use of capillary gas chromatography-mass spectrometry for identification of radiation-induced DNA base damage and DNA base-amino acid crosslinks. J Chromatogr 1984;295:103–121.
   PubMed Web of Science ®Google Scholar
• Simic MG, Dizdaroglu M. Formation of radiation-induced crosslinks between thymine and tyrosine: possible model for crosslinking of DNA and proteins by ionizing radiation. Biochemistry 1985;24:233–236.
   PubMed Web of Science ®Google Scholar
• Margolis S, Coxon B, Gajewski E, Dizdaroglu M. Structure of a hydroxyl radical induced cross-link of thymine and tyrosine. Biochemistry 1988;27:6353–6359.
   PubMed Web of Science ®Google Scholar
• Lipton MSW, Fuciarelli AF, Springer DL, Edmonds CG. Characterization of radiation-induced thymine-tyrosine crosslinks by electrospray ionization mass spectrometry. Radiat Res 1996;145:681–686.
   PubMed Web of Science ®Google Scholar
• Lipton MS, Fuciarelli AL, Springer DL, Hofstadler SA, Edmonds CG. Analysis of radiation induced nucleobase-peptide crosslinks by electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 1997;11: 1673–1676.
   PubMedGoogle Scholar
• Carlton TS, Ingelse BA, Black DS, Craig DC, Mason KE, Duncan MW. A covalent thymine-tyrosine adduct involved in DNA-protein crosslinks: synthesis, characterization and quantification. Free Radic Biol Med 1999;27:254–261.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Gajewski E, Reddy P, Margolis SA. Structure of a hydroxyl radical induced DNA-protein cross-link involving thymine and tyrosine in nucleohistone. Biochemistry 1989;28:3625–3628.
   PubMed Web of Science ®Google Scholar
• Land EJ, Ebert M. Pulse radiolysis studies of aqueous phenol. Water elimination from dihydroxycyclohexadienyl radicals to form phenoxyl. Trans Farad Soc 1967;63: 1181–1190.
   Google Scholar
• Wagenknecht HA, Stemp ED, Barton JK. DNA-Bound peptide radicals generated through DNA-mediated electron transport. Biochemistry 2001;39:5483–5491.
   Web of Science ®Google Scholar
• Bjorklund CC, Davis WB. Stable DNA-protein cross-links are products of DNA charge transport in a nucleosome core particle. Biochemistry 2007;46:10745–10755.
   PubMed Web of Science ®Google Scholar
• Hendry LB, Bransome ED Jr, Hutson MS, Campbell LK. First approximation of a stereochemical rationale for the genetic code based on the topography and physicochemical properties of “cavities” constructed from models of DNA. Proc Natl Acad Sci U S A 1981;78:7440–7444.
   PubMed Web of Science ®Google Scholar
• Nackerdien Z, Rao G, Cacciuttolo MA, Gajewski E, Dizdaroglu M. Chemical nature of DNA-protein cross-links produced in mammalian chromatin by hydrogen peroxide in the presence of Iron or copper Ions. Biochemistry 1991;30: 4873–4879.
   PubMed Web of Science ®Google Scholar
• Samuni A, Aronovich J, Godinger D, Chevion M, Czapski G. On the toxicity of vitamin C and metal ions. A site-specific Fenton mechanism. Eur J Biochem 1983;137:119–124.
   PubMedGoogle Scholar
• Ward JF, Blakely WF, Joner EI. Mammalian cells are not killed by DNA single-strand breaks caused by hydroxyl radicals from hydrogen peroxide. Radiat Res 1985;103:383–392.
   PubMed Web of Science ®Google Scholar
• Goldstein S, Czapski G. The role and mechanism of metal ions and their complexes in enhancing damage in biological systems or in protecting these systems from the toxicity of O2-. J Free Rad Biol Med 1986;2:3–11.
   PubMedGoogle Scholar
• Gajewski E, Fuciarelli A, Dizdaroglu M. Structure of hydroxyl radical-induced DNA-protein crosslinks in calf thymus nucleohistone in vitro. Int J Radiat Biol 1988;54: 445–459.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M, Gajewski E. Structure and mechanism of hydroxyl radical-induced formation of a DNA-protein cross-link involving thymine and lysine in nucleohistone. Cancer Res 1989;49:3463–3467.
   PubMed Web of Science ®Google Scholar
• Gajewski E, Dizdaroglu M. Hydroxyl radical-induced cross-linking of cytosine and tyrosine in nucleohistone. Biochemistry 1990;29:977–980.
   PubMed Web of Science ®Google Scholar
• Morimoto S, Hatta H, Fujita S, Matsuyama T, Ueno T, Nishimoto S. Hydroxyl radical-induced cross-linking of thymine and lysine:identification of the primary structure and mechanism. Bioorg Med Chem Lett 1998;8:865–870.
   PubMed Web of Science ®Google Scholar
• Ban F, Lundqvist MJ, Boyd RJ, Eriksson LA. Theoretical studies of the cross-linking mechanisms between cytosine and tyrosine. J Am Chem Soc 2002;124:2753–2761.
   PubMed Web of Science ®Google Scholar
• Olinski R, Nackerdien Z, Dizdaroglu M. DNA-protein cross-linking between thymine and tyrosine in chromatin of gamma-irradiated or H2O2-treated cultured human cells. Archiv Biochem Biophys 1992;297:139–143.
   PubMed Web of Science ®Google Scholar
• Altman SA, Zastawny TH, Randers-Eichhorn L, Cacciuttolo MA, Akman SA, Dizdaroglu M, . Formation of DNA-protein cross-links in cultured mammalian cells upon treatment with iron ions. Free Radic Biol Med 1995;19: 897–902.
   PubMed Web of Science ®Google Scholar
• Toyokuni S, Mori T, Hiai H, Dizdaroglu M. Treatment of Wistar rats with a renal carcinogen, ferric nitrilotriacetate, causes DNA-protein cross-linking between thymine and tyrosine in their renal chromatin. Int J Cancer 1995;62: 309–313.
   PubMed Web of Science ®Google Scholar