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

Abstract A broad scientific community is involved in investigations aimed at delineating the mechanisms of formation and cellular processing of oxidatively generated damage to nucleic acids. Perhaps as a consequence of this breadth of research expertise, there are nomenclature problems for several of the oxidized bases including 8-oxo-7,8-dihydroguanine (8-oxoGua), a ubiquitous marker of almost every type of oxidative stress in cells. Efforts to standardize the nomenclature and abbreviations of the main DNA degradation products that arise from oxidative pathways are reported. Information is also provided on the main oxidative radicals, non-radical oxygen species, one-electron agents and enzymes involved in DNA degradation pathways as well in their targets and reactivity. A brief classification of oxidatively generated damage to DNA that may involve single modifications, tandem base modifications, intrastrand and interstrand cross-links together with DNA-protein cross-links and base adducts arising from the addition of lipid peroxides breakdown products is also included.

[1]  Evelyne Sage,et al.  Clustered DNA lesion repair in eukaryotes: relevance to mutagenesis and cell survival. , 2011, Mutation research.

[2]  In Seok Hong,et al.  Characterization and mechanism of formation of tandem lesions in DNA by a nucleobase peroxyl radical. , 2007, Journal of the American Chemical Society.

[3]  Yuji Naito,et al.  Chemical and Immunochemical Detection of 8-Halogenated Deoxyguanosines at Early Stage Inflammation* , 2010, The Journal of Biological Chemistry.

[4]  Y. Hiraku,et al.  Formation of 8-nitroguanine, a nitrative DNA lesion, in inflammation-related carcinogenesis and its significance , 2010, Environmental health and preventive medicine.

[5]  Hooshang Nikjoo,et al.  A model of the cell nucleus for DNA damage calculations , 2012, International journal of radiation biology.

[6]  Israel Hanukoglu,et al.  Antioxidant Protective Mechanisms against Reactive Oxygen Species (ROS) Generated by Mitochondrial P450 Systems in Steroidogenic Cells , 2006, Drug metabolism reviews.

[7]  Steffen Loft,et al.  Association between 8-oxo-7,8-dihydroguanine excretion and risk of lung cancer in a prospective study. , 2012, Free radical biology & medicine.

[8]  J. Cadet,et al.  Oxidatively generated base damage to cellular DNA. , 2010, Free radical biology & medicine.

[9]  James E Cleaver,et al.  γH2Ax: Biomarker of Damage or Functional Participant in DNA Repair “All that Glitters Is not Gold!” , 2011, Photochemistry and photobiology.

[10]  Amaya Azqueta,et al.  Towards a more reliable comet assay: optimising agarose concentration, unwinding time and electrophoresis conditions. , 2011, Mutation research.

[11]  David R. Liu,et al.  Conversion of 5-Methylcytosine to 5- Hydroxymethylcytosine in Mammalian DNA by the MLL Partner TET1 , 2009 .

[12]  P. Karran,et al.  UVA photosensitization of thiopurines and skin cancer in organ transplant recipients , 2012, Photochemical & Photobiological Sciences.

[13]  C. Burrows,et al.  Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-Oxo-7,8-dihydroguanosine. , 2000, Organic letters.

[14]  A. Ross,et al.  Reactivity of HO2/O−2 Radicals in Aqueous Solution , 1985 .

[15]  V. Bohr,et al.  Base excision repair of oxidative DNA damage and association with cancer and aging. , 2008, Carcinogenesis.

[16]  Cynthia J Burrows,et al.  DNA-protein cross-links between guanine and lysine depend on the mechanism of oxidation for formation of C5 vs C8 guanosine adducts. , 2008, Journal of the American Chemical Society.

[17]  Jean Cadet,et al.  Measurement of oxidatively generated base damage in cellular DNA. , 2011, Mutation research.

[18]  Mihalis I Panayiotidis,et al.  DNA damage induced by endogenous aldehydes: current state of knowledge. , 2011, Mutation research.

[19]  Marc M Greenberg,et al.  Synthesis and characterization of oligodeoxynucleotides containing formamidopyrimidine lesions and nonhydrolyzable analogues. , 2002, Journal of the American Chemical Society.

[20]  Ralf Hass,et al.  Cellular responses to reactive oxygen species-induced DNA damage and aging , 2008, Biological chemistry.

[21]  Cynthia J Burrows,et al.  Surviving an Oxygen Atmosphere: DNA Damage and Repair. , 2009, ACS symposium series. American Chemical Society.

[22]  J. Essigmann,et al.  Biological properties of single chemical-DNA adducts: a twenty year perspective. , 2008, Chemical research in toxicology.

[23]  J. Cadet,et al.  Oxidative damage to DNA: formation, measurement, and biological significance. , 1997, Reviews of physiology, biochemistry and pharmacology.

[24]  Hiroshi Sugiyama,et al.  Product Analysis of GG-Specific Photooxidation of DNA via Electron Transfer: 2-Aminoimidazolone as a Major Guanine Oxidation Product , 1998 .

[25]  Jean Cadet,et al.  Isolation and Characterization of the Radiation-Induced Degradation Products of 2′-Deoxyguanosine in Oxygen-Free Aqueous Solutions , 1985 .

[26]  Michael P. Murphy,et al.  How mitochondria produce reactive oxygen species , 2008, The Biochemical journal.

[27]  James G. Muller,et al.  Sequence and Stacking Dependence of 8-Oxoguanine Oxidation: Comparison of One-Electron vs Singlet Oxygen Mechanisms , 1999 .

[28]  Clemens von Sonntag,et al.  Free-Radical-Induced DNA Damage and Its Repair , 2006 .

[29]  I Iavarone,et al.  The role of CSA in the response to oxidative DNA damage in human cells , 2007, Oncogene.

[30]  Takamichi Ichinose,et al.  The role of iNOS‐mediated DNA damage in infection‐ and asbestos‐induced carcinogenesis , 2010, Annals of the New York Academy of Sciences.

[31]  Dudley T Goodhead,et al.  Energy deposition stochastics and track structure: what about the target? , 2006, Radiation protection dosimetry.

[32]  Ron Weiss,et al.  TDG in Mammalian DNA Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision , 2012 .

[33]  Andrew Collins,et al.  Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[34]  H. Karlsson,et al.  The comet assay in nanotoxicology research , 2010, Analytical and bioanalytical chemistry.

[35]  Kim D Janda,et al.  Evidence for Ozone Formation in Human Atherosclerotic Arteries , 2003, Science.

[36]  Ying Wang,et al.  Quantifying etheno-DNA adducts in human tissues, white blood cells, and urine by ultrasensitive (32)P-postlabeling and immunohistochemistry. , 2011, Methods in molecular biology.

[37]  N. Schnetz-Boutaud,et al.  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. , 2001, Biochemistry.

[38]  Steffen Loft,et al.  Measurement and Meaning of Oxidatively Modified DNA Lesions in Urine , 2008, Cancer Epidemiology Biomarkers & Prevention.

[39]  P. Karran,et al.  Efficient DNA interstrand crosslinking by 6-thioguanine and UVA radiation. , 2011, DNA repair.

[40]  C. Redon,et al.  γH2AX foci as a measure of DNA damage: a computational approach to automatic analysis. , 2011, Mutation research.

[41]  Marc M Greenberg,et al.  Scope and mechanism of interstrand cross-link formation by the C4'-oxidized abasic site. , 2009, Journal of the American Chemical Society.

[42]  H. Wagenknecht,et al.  Electron transfer processes in DNA: mechanisms, biological relevance and applications in DNA analytics. , 2006, Natural product reports.

[43]  Bernd Epe,et al.  DNA damage by bromate: mechanism and consequences. , 2006, Toxicology.

[44]  Steffen Loft,et al.  Influence of the OGG1 Ser326Cys polymorphism on oxidatively damaged DNA and repair activity. , 2012, Free radical biology & medicine.

[45]  Jean Cadet,et al.  Oxidation of the sugar moiety of DNA by ionizing radiation or bleomycin could induce the formation of a cluster DNA lesion , 2007, Proceedings of the National Academy of Sciences.

[46]  C. Winterbourn,et al.  Reconciling the chemistry and biology of reactive oxygen species. , 2008, Nature chemical biology.

[47]  E. Parlanti,et al.  Role of nucleotide excision repair proteins in oxidative DNA damage repair: an updating , 2011, Biochemistry (Moscow).

[48]  Andrew R Collins,et al.  The use of bacterial repair endonucleases in the comet assay. , 2011, Methods in molecular biology.

[49]  Marc M Greenberg,et al.  The formamidopyrimidines: purine lesions formed in competition with 8-oxopurines from oxidative stress. , 2012, Accounts of chemical research.

[50]  B. Epe,et al.  Determination of steady-state levels of oxidative DNA base modifications in mammalian cells by means of repair endonucleases. , 1997, Carcinogenesis.

[51]  Steven R Tannenbaum,et al.  Peroxynitrite-induced oxidation and nitration products of guanine and 8-oxoguanine: structures and mechanisms of product formation. , 2006, Nitric oxide : biology and chemistry.

[52]  B. Van Houten,et al.  Nucleotide excision repair of a DNA interstrand cross-link produces single- and double-strand breaks. , 2010, Biochemistry.

[53]  Chryssostomos Chatgilialoglu,et al.  Radiation-induced formation of purine 5',8-cyclonucleosides in isolated and cellular DNA: high stereospecificity and modulating effect of oxygen. , 2010, Organic & biomolecular chemistry.

[54]  Jean Cadet,et al.  Synthesis and Mass Spectrometry Analysis of Oligonucleotides Bearing 5-Formyl-2′-Deoxyurldlne in Their Structure , 1996 .

[55]  Chuan He,et al.  Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine , 2011, Science.

[56]  N. Geacintov,et al.  Oxidative DNA Damage Associated with Combination of Guanine and Superoxide Radicals and Repair Mechanisms via Radical Trapping* , 2004, Journal of Biological Chemistry.

[57]  Yinsheng Wang,et al.  Bulky DNA lesions induced by reactive oxygen species. , 2008, Chemical research in toxicology.

[58]  S. Powers,et al.  Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. , 2008, Physiological reviews.

[59]  J. Cadet,et al.  Oxidatively generated damage to the guanine moiety of DNA: mechanistic aspects and formation in cells. , 2008, Accounts of chemical research.

[60]  S. J. Culp,et al.  Structural and conformational analyses of 8-hydroxy-2'-deoxyguanosine. , 1989, Chemical research in toxicology.

[61]  Jean Cadet,et al.  One-electron oxidation of DNA and inflammation processes , 2006, Nature chemical biology.

[62]  Leland L Smith,et al.  Oxygen, oxysterols, ouabain, and ozone: a cautionary tale. , 2004, Free radical biology & medicine.

[63]  Chryssostomos Chatgilialoglu,et al.  Purine 5',8-cyclonucleoside lesions: chemistry and biology. , 2011, Chemical Society reviews.

[64]  C. Rithner,et al.  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). , 2001, Biochemistry.

[65]  Jean Cadet,et al.  DNA tandem lesions containing 8-oxo-7,8-dihydroguanine and formamido residues arise from intramolecular addition of thymine peroxyl radical to guanine. , 2002, Chemical research in toxicology.

[66]  N. Schnetz-Boutaud,et al.  Temperature-dependent formation of a conjugate between tris(hydroxymethyl)aminomethane buffer and the malondialdehyde-DNA adduct pyrimidopurinone. , 1997, Chemical research in toxicology.

[67]  Helmut Sies Ozone in arteriosclerotic plaques: searching for the "smoking gun". , 2004, Angewandte Chemie.

[68]  B. Freeman,et al.  Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations. , 1996, Archives of biochemistry and biophysics.

[69]  Y. Hiraku,et al.  Oxidative and nitrative DNA damage as biomarker for carcinogenesis with special reference to inflammation. , 2006, Antioxidants & redox signaling.

[70]  J. Cadet,et al.  Gamma irradiation of 2'-deoxyadenosine in oxygen-free aqueous solutions: identification and conformational features of formamidopyrimidine nucleoside derivatives. , 1995, Chemical research in toxicology.

[71]  Peter C Dedon,et al.  The chemical toxicology of 2-deoxyribose oxidation in DNA. , 2008, Chemical research in toxicology.

[72]  Jean Cadet,et al.  Minor contribution of direct ionization to DNA base damage inducedby heavy ions , 2006, International journal of radiation biology.

[73]  Jean Cadet,et al.  Oxidation reactions of cytosine DNA components by hydroxyl radical and one-electron oxidants in aerated aqueous solutions. , 2010, Accounts of chemical research.

[74]  D. Patel,et al.  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. , 1991, Biochemistry.

[75]  Yves Pommier,et al.  γH2AX and cancer , 2008, Nature Reviews Cancer.

[76]  P. Olive,et al.  Endogenous DNA breaks: γH2AX and the role of telomeres , 2009, Aging.

[77]  Debra L. Laskin,et al.  Nitrative and Oxidative Stress in Toxicology and Disease , 2009, Toxicological sciences : an official journal of the Society of Toxicology.

[78]  Catherine C. Smith,et al.  hOGG1 recognizes oxidative damage using the comet assay with greater specificity than FPG or ENDOIII. , 2006, Mutagenesis.

[79]  Jean Cadet,et al.  Selective one-electron oxidation of duplex DNA oligomers: reaction at thymines. , 2008, Organic & biomolecular chemistry.

[80]  Glen A. Russell,et al.  Deuterium-isotope Effects in the Autoxidation of Aralkyl Hydrocarbons. Mechanism of the Interaction of PEroxy Radicals1 , 1957 .

[81]  W. H. Powell,et al.  A guide to IUPAC nomenclature of organic compounds : recommendations 1993 , 1994 .

[82]  L. Marnett Oxy radicals, lipid peroxidation and DNA damage. , 2002, Toxicology.

[83]  Hiroyuki Kamiya,et al.  Mutagenicity of oxidized DNA precursors in living cells: Roles of nucleotide pool sanitization and DNA repair enzymes, and translesion synthesis DNA polymerases. , 2010, Mutation research.

[84]  A. Kettle,et al.  Radical-radical reactions of superoxide: a potential route to toxicity. , 2003, Biochemical and biophysical research communications.

[85]  Marc M Greenberg,et al.  Probing DNA interstrand cross-link formation by an oxidized abasic site using nonnative nucleotides. , 2011, Bioorganic & medicinal chemistry.

[86]  M. Dizdaroglu,et al.  Monomeric base damage products from adenine, guanine, and thymine induced by exposure of DNA to ultraviolet radiation. , 1995, Biochemistry.

[87]  H. Sandermann,et al.  Ecotoxicology of ozone: bioactivation of extracellular ascorbate. , 2008, Biochemical and biophysical research communications.

[88]  Chris E Cooper,et al.  Exercise-Induced Oxidative Stress , 2005, Sports medicine.

[89]  Jean Cadet,et al.  Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[90]  W. Koppenol,et al.  The basic chemistry of nitrogen monoxide and peroxynitrite. , 1998, Free radical biology & medicine.

[91]  Peter C Dedon,et al.  Mechanisms of oxidation of guanine in DNA by carbonate radical anion, a decomposition product of nitrosoperoxycarbonate. , 2007, Chemistry.

[92]  J. Cadet,et al.  Ultraviolet radiation-mediated damage to cellular DNA. , 2005, Mutation research.

[93]  Steven R Tannenbaum,et al.  Reactive nitrogen species in the chemical biology of inflammation. , 2004, Archives of biochemistry and biophysics.

[94]  S R Tannenbaum,et al.  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. , 2001, Organic letters.

[95]  Jean Cadet,et al.  THYMIDINE HYDROPEROXIDES : STRUCTURAL ASSIGNMENT, CONFORMATIONAL FEATURES,AND THERMAL DECOMPOSITION IN WATER , 1994 .

[96]  Gary B. Schuster,et al.  The sacrificial role of easily oxidizable sites in the protection of DNA from damage , 2005, Nucleic acids research.

[97]  Jerzy Leszczynski,et al.  Determination of redox potentials for the Watson-Crick base pairs, DNA nucleosides, and relevant nucleoside analogues. , 2007, The journal of physical chemistry. B.

[98]  Alexandros G. Georgakilas,et al.  Detection of Complex DNA Damage in γ-Irradiated Acute Lymphoblastic Leukemia Pre-B NALM-6 Cells , 2007 .

[99]  Jean Cadet,et al.  Oxidatively Generated Damage to the Guanine Moiety of DNA: Mechanistic Aspects and Formation in Cells , 2008 .

[100]  Rafael Radi,et al.  Peroxynitrite and reactive nitrogen species: the contribution of ABB in two decades of research. , 2009, Archives of biochemistry and biophysics.

[101]  C. Obinger,et al.  Myeloperoxidase: a target for new drug development? , 2007, British journal of pharmacology.

[102]  Sheila S. David,et al.  Chemistry of Glycosylases and Endonucleases Involved in Base-Excision Repair. , 1998, Chemical reviews.

[103]  E. Ohtsuka,et al.  NMR studies of a DNA containing 8-hydroxydeoxyguanosine. , 1991, Nucleic acids research.

[104]  Yun Hee Jang,et al.  First principles calculations of the tautomers and pK(a) values of 8-oxoguanine: implications for mutagenicity and repair. , 2002, Chemical research in toxicology.

[105]  P. Dedon,et al.  The Biological and Metabolic Fates of Endogenous DNA Damage Products , 2010, Journal of nucleic acids.

[106]  M S Evans,et al.  Vicinal lesions in X-irradiated DNA? , 1993, International journal of radiation biology.

[107]  B. Meunier,et al.  Guanine oxidation: one- and two-electron reactions. , 2006, Chemistry.

[108]  Giselle Cerchiaro,et al.  The carbonate radical and related oxidants derived from bicarbonate buffer , 2007, IUBMB life.

[109]  C. Hawkins,et al.  Ability of hypochlorous acid and N-chloramines to chlorinate DNA and its constituents. , 2010, Chemical research in toxicology.

[110]  J. Cadet,et al.  Chlorination of Guanosine and Other Nucleosides by Hypochlorous Acid and Myeloperoxidase of Activated Human Neutrophils , 2001, The Journal of Biological Chemistry.

[111]  M. Dizdaroglu,et al.  Identification and quantification of 8,5'-cyclo-2'-deoxy-adenosine in DNA by liquid chromatography/ mass spectrometry. , 2001, Free radical biology & medicine.

[112]  B. Halliwell,et al.  Nitrite-induced deamination and hypochlorite-induced oxidation of DNA in intact human respiratory tract epithelial cells. , 2000, Free radical biology & medicine.

[113]  M. Toledano,et al.  ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis , 2007, Nature Reviews Molecular Cell Biology.

[114]  M. Dizdaroglu,et al.  Application of capillary gas chromatography-mass spectrometry to chemical characterization of radiation-induced base damage of DNA: implications for assessing DNA repair processes. , 1985, Analytical biochemistry.

[115]  P. Møller,et al.  Recommendations for standardized description of and nomenclature concerning oxidatively damaged nucleobases in DNA. , 2010, Chemical research in toxicology.

[116]  J. Essigmann,et al.  Chemical-biological fingerprinting: probing the properties of DNA lesions formed by peroxynitrite. , 2007, Chemical research in toxicology.

[117]  Jagadeesan Nair,et al.  Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans. , 2007, Free radical biology & medicine.

[118]  Uzi Landman,et al.  Oxidation of DNA: damage to nucleobases. , 2010, Accounts of chemical research.

[119]  Yong Jiang,et al.  In vivo formation and in vitro replication of a guanine-thymine intrastrand cross-link lesion. , 2007, Biochemistry.

[120]  Trevor M. Penning,et al.  Analysis of 7,8-Dihydro-8-oxo-2′-deoxyguanosine in Cellular DNA during Oxidative Stress , 2009, Chemical research in toxicology.

[121]  M. Hada,et al.  Formation of clustered DNA damage after high-LET irradiation: a review. , 2008, Journal of radiation research.

[122]  Jean Cadet,et al.  Characterization of lysine-guanine cross-links upon one-electron oxidation of a guanine-containing oligonucleotide in the presence of a trilysine peptide. , 2006, Journal of the American Chemical Society.

[123]  Jean Cadet,et al.  Singlet Oxygen Oxidation of Isolated and Cellular DNA: Product Formation and Mechanistic Insights , 2006, Photochemistry and photobiology.

[124]  Jean Cadet,et al.  Cross-linked thymine-purine base tandem lesions: synthesis, characterization, and measurement in gamma-irradiated isolated DNA. , 2002, Chemical research in toxicology.

[125]  S. Nishimura,et al.  Hydroxylation of the C-8 position of deoxyguanosine by reducing agents in the presence of oxygen. , 1983, Nucleic acids symposium series.

[126]  Michael J Morgan,et al.  Crosstalk of reactive oxygen species and NF-κB signaling , 2011, Cell Research.

[127]  P. G. Wells,et al.  Oxidative DNA damage and repair in teratogenesis and neurodevelopmental deficits. , 2010, Birth defects research. Part C, Embryo today : reviews.

[128]  Markus Müller,et al.  The discovery of 5-formylcytosine in embryonic stem cell DNA. , 2011, Angewandte Chemie.

[129]  B. Freeman,et al.  Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[130]  N. Geacintov,et al.  Generation of guanine-thymidine cross-links in DNA by peroxynitrite/carbon dioxide. , 2011, Chemical research in toxicology.

[131]  P. Karran,et al.  Multiple forms of DNA Damage Caused by UVA Photoactivation of DNA 6‐Thioguanine , 2012, Photochemistry and photobiology.

[132]  Chryssostomos Chatgilialoglu,et al.  New insights into the reaction paths of hydroxyl radicals with 2'-deoxyguanosine. , 2011, Chemical research in toxicology.

[133]  G. Lorimer,et al.  Ribulose diphosphate oxygenase. I. Synthesis of phosphoglycolate by fraction-1 protein of leaves. , 1973, Biochemistry.

[134]  S. J. Culp,et al.  Nitrogen-15 nuclear magnetic resonance studies on the tautomerism of 8-hydroxy-2'-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides , 1990 .

[135]  J. E. Lier,et al.  QUINONE SENSITIZED ELECTRON TRANSFER PHOTOOXIDATION OF NUCLEIC ACIDS: CHEMISTRY OF THYMINE AND THYMIDINE RADICAL CATIONS IN AQUEOUS SOLUTION * , 1990, Photochemistry and photobiology.

[136]  Balaraman Kalyanaraman,et al.  Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. , 2012, Free radical biology & medicine.

[137]  Marc M Greenberg,et al.  DNA interstrand cross-link formation by the 1,4-dioxobutane abasic lesion. , 2009, Journal of the American Chemical Society.

[138]  Kent D. Sugden,et al.  Nei deficient Escherichia coli are sensitive to chromate and accumulate the oxidized guanine lesion spiroiminodihydantoin. , 2005, Chemical research in toxicology.

[139]  G. Pfeifer,et al.  Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine , 2011, Proceedings of the National Academy of Sciences.

[140]  Peter C Dedon,et al.  Reactive species and DNA damage in chronic inflammation: reconciling chemical mechanisms and biological fates , 2010, International journal of cancer.

[141]  E. Parlanti,et al.  New functions of XPC in the protection of human skin cells from oxidative damage , 2006, The EMBO journal.

[142]  K. Houk,et al.  Free radical biology and medicine: it's a gas, man! , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[143]  Polycarpos Pissis,et al.  Role of oxidative stress and DNA damage in human carcinogenesis. , 2011, Mutation research.

[144]  S. Kawanishi,et al.  Mechanism of DNA damage induced by bromate differs from general types of oxidative stress. , 2006, Toxicology.

[145]  L. Povirk,et al.  DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. , 1996, Mutation research.

[146]  Yinsheng Wang,et al.  Formation and genotoxicity of a guanine–cytosine intrastrand cross-link lesion in vivo , 2007, Nucleic acids research.

[147]  Sayuri Miyamoto,et al.  Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[148]  Jean Cadet,et al.  Radical Oxidation of the Adenine Moiety of Nucleoside and DNA: 2-Hydroxy-2′-deoxyadenosine is a Minor Decomposition Product , 2002, Free radical research.

[149]  Robert W Sobol,et al.  Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage. , 2011, Antioxidants & redox signaling.

[150]  Jean Cadet,et al.  Characterization and Chemical Stability of Photooxidized Oligonucleotides that Contain 2,2-Diamino-4-[(2-deoxy-β-d-erythro-pentofuranosyl)amino]-5(2H)-oxazolone , 1998 .

[151]  Jerzy Leszczynski,et al.  Tautomeric equilibria in 8-oxopurines: Implications for mutagenicity , 1998, J. Comput. Aided Mol. Des..

[152]  S. J. Culp,et al.  15N nuclear magnetic resonance studies on the tautomerism of 8-hydroxy-2'-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides. , 1990, Chemical research in toxicology.

[153]  R. Floyd,et al.  Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanisms of formation. , 1986, Free radical research communications.

[154]  S. Nishimura,et al.  8-Hydroxyguanine: a base for discovery. , 2011, DNA repair.

[155]  Rafael Radi,et al.  Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. , 2009, ACS chemical biology.

[156]  Jacques Laval,et al.  Clustered DNA Damages Induced by X Rays in Human Cells , 2002, Radiation research.

[157]  Peter C Dedon,et al.  Sequence-dependent variation in the reactivity of 8-Oxo-7,8-dihydro-2'-deoxyguanosine toward oxidation. , 2012, Chemical research in toxicology.

[158]  David Frith,et al.  Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA , 2011, Nucleic acids research.

[159]  Lawrence J. Marnett,et al.  Systems Analysis of Protein Modification and Cellular Responses Induced by Electrophile Stress , 2010, Accounts of chemical research.

[160]  M. Aida,et al.  An ab initio molecular orbital study on the characteristics of 8-hydroxyguanine. , 1987, Mutation research.

[161]  M. Medeiros,et al.  Exocyclic DNA adducts as biomarkers of lipid oxidation and predictors of disease. Challenges in developing sensitive and specific methods for clinical studies. , 2009, Chemical research in toxicology.

[162]  J. Pablo Radicella,et al.  HO• radicals induce an unexpected high proportion of tandem base lesions refractory to repair by DNA glycosylases , 2010, Proceedings of the National Academy of Sciences.

[163]  Jean Cadet,et al.  Effects of duplex stability on charge-transfer efficiency within DNA , 2004 .