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REVIEW ARTICLE

Measurement of oxidatively induced DNA damage and its repair, by mass spectrometric techniques

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Pages 525-548 | Received 06 Jan 2015, Accepted 30 Jan 2015, Published online: 27 Mar 2015

References

  • Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. Oxford: Fourth Edition, Oxford University Press; 2007.
  • Sies H. Oxidative Stress: Oxidants and Antioxidants. London: Academic Press; 1991.
  • Ross AB, Mallard WG, Helman WP, Bielski BHJ, Buxton GV, Cabelli DE, et al NDRL-NIST solution kinetics database. Gaithersburg: National Institute of Standards and Technology; 1992.
  • Huie RE, Padmaja S. The reaction of NO with superoxide. Free Radic Res Commun 1993;18:195–199.
  • von Sonntag C. Free-Radical-Induced DNA Damage and Its Repair. Hiedelberg: Springer; 2006.
  • Dizdaroglu M, Jaruga P. Mechanisms of free radical-induced damage to DNA. Free Radic Res 2012;46:382–419.
  • Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. DNA Repair and Mutagenesis. Washington, D.C.: ASM Press; 2006.
  • Vogelstein B, Kinzler KW. The Genetic Basis of Human Cancer. New York: McGraw-Hill; 1998.
  • Jackson AL, Loeb LA. The contribution of endogenous sources of DNA damage to the multiple mutations in cancer. Mutat Res 2001;477:7–21.
  • Davidson JF, Guo HH, Loeb LA. Endogenous mutagenesis and cancer. Mutat Res 2002;509:17–21.
  • Friedberg EC. DNA damage and repair. Nature 2003;421: 436–440.
  • Dizdaroglu M. Oxidatively induced DNA damage and its repair in cancer. Mutat Res Rev 2014; in press.
  • Collins A, Cadet J, Epe B, Gedik C. Problems in the measurement of 8-oxoguanine in human DNA. Report of a workshop, DNA oxidation, held in Aberdeen, UK 19–21 January, 1997. Carcinogenesis 1997;18:1833–1836.
  • 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.
  • Floyd RA. The development of a sensitive analysis for 8-hydroxy-2’-deoxyguanosine. Free Radic Res Commun 1990;8:139–141.
  • Grollman AP, Moriya M. Mutagenesis by 8-oxoguanine: An enemy within. Trends Genet 1993;9:246–249.
  • 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.
  • ESCODD. Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic Biol Med 2003;34:1089–1099.
  • 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.
  • 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;122:2373–2384.
  • 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.
  • 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.
  • 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.
  • Burrows CJ, Muller JG, Kornyushyna O, Luo W, Duarte V, Leipold MD, et al. 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.
  • 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.
  • 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.
  • Neeley WL, Essigmann JM. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 2006;19:491–505.
  • 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.
  • 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.
  • Jaruga P, Dizdaroglu M. Repair of products of oxidative DNA base damage in human cells. Nucleic Acids Res 1996;24:1389–1394.
  • Dizdaroglu M. Substrate specificities and excision kinetics of DNA glycosylases involved in base-excision repair of oxidative DNA damage. Mutat Res 2003;531:109–126.
  • Dizdaroglu M. Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat Res 2005;591:45–59.
  • Dizdaroglu M. Clemens von Sonntag and the early history of radiation-induced sugar damage in DNA. Int J Radiat Biol 2014;90:446–458.
  • 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.
  • 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.
  • 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.
  • Dizdaroglu M. Quantitative determination of oxidative base damage in DNA by stable isotope-dilution mass spectrometry. FEBS Lett 1993;315:1–6.
  • Nelson VC. Synthesis of isotopically labelled DNA degradation products for use in mass spectrometric studies of cellular DNA damage. J Label Comp Radiopharm 1996; 38:713–723.
  • Sasaki Y, Hashizume T. Gas chromatography of trimethylsilylated bases and nucleosides. Anal Biochem 1966;16: 1–19.
  • Gehrke CW, Stalling DL, Ruyle CD. Quantitative gas-liquid chromatography of TMS nucleic acid constituents. Biochem Biophys Res Commun 1967;28:869–874.
  • McCloskey JA, Lawson AM, Tsuboyama K, Krueger PM, Stillwell RN. Mass spectrometry of nucleic acid components. Trimethylsilyl derivatives of nucleotides, nucleosides, and bases. J Am Chem Soc 1968;90:4182–4184.
  • White E, Krueger VP, McCloskey JA. Mass spectra of trimethylsilyl derivatives of pyrimidine and purine bases. J Org Chem 1972;37:430–438.
  • Watson JT. Introduction to Mass Spectromtery. New York: Raven Press; 1985, pp. 59–74.
  • Schram KH. Mass spectrometry of nucleic acid components. Methods Biochem Anal 1990;34:203–287.
  • Jaruga P, Speina E, Gackowski D, Tudek B, Olinski R. Endogenous oxidative DNA base modifications analysed with repair enzymes and GC/MS technique. Nucleic Acids Res 2000;28:E16.
  • Rodriguez H, Jurado J, Laval J, Dizdaroglu M. Comparison of the levels of 8-hydroxyguanine in DNA as measured by gas chromatography mass spectrometry following hydrolysis of DNA by Escherichia coli Fpg protein or formic acid. Nucleic Acids Res 2000;28:E75.
  • Watson JT. Selected-ion measurements. Methods Enzymol 1990;193:86–106.
  • Dizdaroglu M. Oxidative damage to DNA in mammalian chromatin. Mutat Res 1992;275:331–342.
  • Lovell MA, Markesbery WR. Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer’s disease. Nucleic Acids Res 2007;35:7497–7504.
  • Dizdaroglu M, Kirkali G, Jaruga P. Formamidopyrimidines in DNA: Mechanisms of formation, repair, and biological effects. Free Radic Biol Med 2008;45:1610–1621.
  • Sonnen JA, Breitner JC, Lovell MA, Markesbery WR, Quinn JF, Montine TJ. Free radical-mediated damage to brain in Alzheimer’s disease and its transgenic mouse models. Free Radic Biol Med 2008;45:219–230.
  • Cadet J, Douki T, Ravanat JL. Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 2010;49:9–21.
  • Petersen EJ, Nelson BC. Mechanisms and measurements of nanomaterial-induced oxidative damage to DNA. Anal Bioanal Chem 2010;398:613–650.
  • Dizdaroglu M. Oxidatively induced DNA damage: Mechanisms, repair and disease. Cancer Lett 2012;327:26–47.
  • Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, et al. Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 2012;46:1819–1827.
  • Dizdaroglu M. Formation of an 8-hydroxyguanine moiety in deoxyribonucleic acid on gamma-irradiation in aqueous solution. Biochemistry 1985;24:4476–4481.
  • Dizdaroglu M. Free-radical-induced formation of an 8,5’-cyclo-2’-deoxyguanosine moiety in deoxyribonucleic acid. Biochem J 1986;238:247–254.
  • Dizdaroglu M. Characterization of free radical-induced base damage in DNA by the combined use of enzymatic hydrolysis and gas chromatography-mass spectrometry. J Chromatogr 1986;367:357–366.
  • McCloskey JA. Electron ionization mass spectra of trimethylsilyl derivatives of nucleosides. Methods Enzymol 1990;193:825–842.
  • Reddy PT, Jaruga P, Kirkali G, Tuna G, Nelson BC, Dizdaroglu M. Identification and quantification of human DNA repair Protein NEIL1 by liquid chromatography/isotope-dilution tandem mass spectrometry. J Proteome Res 2013;12:1049–1061.
  • Jacobs AC, Calkins MJ, Jadhav A, Dorjsuren D, Maloney D, Simeonov A, et al. Inhibition of DNA glycosylases via small molecule purine analogs. PLoS ONE 2013;8:e81667.
  • Petersen EJ, Reipa V, Watson SS, Stanley DL, Rabb SA, Nelson BC. DNA damaging potential of photoactivated p25 titanium dioxide nanoparticles. Chem Res Toxicol 2014; 27:1877–1884.
  • Gassman NR, Coskun E, Stefanick DF, Horton JK, Jaruga P, Dizdaroglu M, et al. Bisphenol A promotes cell survival following oxidative DNA damage in mouse fibroblasts. PLoS ONE 2014; (in press).
  • Ravanat JL, Turesky RJ, Gremaud E, Trudel LJ, Stadler RH. Determination of 8-oxoguanine in DNA by gas chromatography mass spectrometry and HPLC-electrochemical detection: Overestimation of the background level of the oxidized base by the gas chromatography mass spectrometry assay. Chem Res Toxicol 1995;8:1039–1045.
  • Douki T, Delatour T, Bianchini F, Cadet J. Observation and prevention of an artefactual formation of oxidized DNA bases and nucleosides in the GC-EIMS method. Carcinogenesis 1996;17:347–353.
  • Cadet J, Douki T, Ravanat JL. Artifacts associated with the measurement of oxidized DNA bases. Environ Health Perspect 1997;105:1034–1039.
  • Sentürker S, Dizdaroglu M. The effect of experimental conditions on the levels of oxidatively modified bases in DNA as measured by gas chromatography-mass spectrometry: how many modified bases are involved? Prepurification or not? Free Radic Biol Med 1999;27:370–380.
  • Halliwell B. Oxidative stress, nutrition and health. Experimental strategies for optimization of nutritional antioxidant intake in humans Free Radic Res 1996;25:57–74.
  • Douki T, Martini R, Ravanat JL, Turesky RJ, Cadet J. Measurement of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 8-oxo- 7,8-dihydroguanine in isolated DNA exposed to gamma radiation in aqueous solution. Carcinogenesis 1997;18:2385–2391.
  • Dizdaroglu M. Mechanisms of free radical damage to DNA. In: Aruoma OI, Halliwell B, editors. DNA & Free Radicals: Techniques, Mechanisms & Applications. Saint Lucia: OICA International; 1998; pp. 3–26.
  • Dizdaroglu M. Facts about the artifacts in the measurement of oxidative DNA base damage by gas chromatography-mass spectrometry. Free Radic Res 1998;29:551–563.
  • Jenner A, England TG, Aruoma OI, Halliwell B. Measurement of oxidative DNA damage by gas chromatography-mass spectrometry: ethanethiol prevents artifactual generation of oxidized DNA bases. Biochem J 1998;331: 365–369.
  • England TG, Jenner A, Aruoma OI, Halliwell B. Determination of oxidative DNA base damage by gas chromatography-mass spectrometry. Effect of derivatization conditions on artifactual formation of certain base oxidation products Free Radic Res 1998;29:321–330.
  • Dizdaroglu M, Jaruga P, Rodriguez H. Measurement of 8-hydroxy-2’-deoxyguanosine in DNA by high-performance liquid chromatography-mass spectrometry: comparison with measurement by gas chromatography-mass spectrometry. Nucleic Acids Res 2001;29:E12.
  • Lin HS, Jenner AM, Ong CN, Huang SH, Whiteman M, Halliwell B. A high-throughput and sensitive methodology for the quantification of urinary 8-hydroxy-2’-deoxyguanosine: measurement with gas chromatography-mass spectrometry after single solid-phase extraction. Biochem J 2004;380: 541–548.
  • Lovell MA, Markesbery WR. Oxidative damage in mild cognitive impairment and early Alzheimer’s disease. J Neurosci Res 2007;85:3036–3040.
  • Spencer JPE, Jenner A, Aruoma OI, Cross CE, Wu R, Halliwell B. Oxidative DNA damage in human respiratory tract epithelial cells. Time course in relation to DNA strand breakage. Biochem Biophys Res Commun 1996;224: 17–22.
  • Abalea V, Cillard J, Dubos MP, Anger JP, Cillard P, Morel I. Iron-induced oxidative DNA damage and its repair in primary rat hepatocyte culture. Carcinogenesis 1998;19: 1053–1059.
  • Douki T, Spinelli S, Ravanat J-L, Cadet J. Hydroxyl radical-induced degradation of 2’-deoxyguanosine under reducing conditions. J Chem Soc Perkin Trans 2 1999:1875–1880.
  • Douki T, Bretonniere Y, Cadet J. Protection against radiation-induced degradation of DNA bases by polyamines. Radiat Res 2000;153:29–35.
  • Pouget J-P, Douki T, Richard M, Cadet J. DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and comet assay. Chem Res Toxicol 2000;13:541–549.
  • Frelon S, Douki T, Ravanat JL, Pouget JP, Tornabene C, Cadet J. High-performance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem Res Toxicol 2000;13:1002–1010.
  • Pouget JP, Frelon S, Ravanat JL, Testard I, Odin F, Cadet J. Formation of modified DNA bases in cells exposed either to gamma radiation or to high-LET particles. Radiat Res 2002; 157:589–595.
  • Douki T, Ravanat J-L, Frelon S, Bourdat A-G, Pouget J-P, Cadet J. Critical Reviews of Oxidative Stress and Aging. Advances in Basic Science, Diagnostics and Intervention. New Jersey: World Scientific; 2003, pp. 190–202.
  • Frelon S, Douki T, Favier A, Cadet J. Hydroxyl radical is not the main reactive species involved in the degradation of DNA bases by copper in the presence of hydrogen peroxide. Chem Res Toxicol 2003;16:191–197.
  • Kaur H, Halliwell B. Measurement of oxidized and methylated DNA bases by HPLC with electrochemical detection. Biochem J 1996;318:21–23.
  • Ravanat JL, Guicherd P, Tuce Z, Cadet J. Simultaneous determination of five oxidative DNA lesions in human urine. Chem Res Toxicol 1999;12:802–808.
  • Malayappan B, Garrett TJ, Segal M, Leeuwenburgh C. Urinary analysis of 8-oxoguanine, 8-oxoguanosine, fapy-guanine and 8-oxo-2’-deoxyguanosine by high-performance liquid chromatography-electrospray tandem mass spectrometry as a measure of oxidative stress. J Chromatogr A 2007;1167:54–62.
  • Hu J, de Souza-Pinto NC, Haraguchi K, Hogue BA, Jaruga P, Greenberg MM, et al. Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. J Biol Chem 2005; 280:40544–40551.
  • Malins DC, Anderson KM, Stegeman JJ, Jaruga P, Green VM, Gilman NK, et al. Biomarkers signal contaminant effects on the organs of English sole (Parophrys vetulus) from Puget Sound. Environ Health Perspect 2006;114:823–829.
  • 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.
  • 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.
  • Gokce G, Ozsarlak-Sozer G, Oktay G, Kirkali G, Jaruga P, Dizdaroglu M, Kerry Z. Glutathione depletion by buthionine sulfoximine induces oxidative damage to DNA in organs of rabbits in vivo. Biochemistry 2009;48:4980–4987.
  • Chan MK, Ocampo-Hafalla MT, Vartanian V, Jaruga P, Kirkali G, Koenig KL, et al. Targeted deletion of the genes encoding NTH1 and NEIL1 DNA N-glycosylases reveals the existence of novel carcinogenic oxidative damage to DNA. DNA Repair (Amst) 2009;8:786–794.
  • Kish A, Kirkali G, Robinson C, Rosenblatt R, Jaruga P, Dizdaroglu M, DiRuggiero J. Salt shield: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ Microbiol 2009;11:1066–1078.
  • Muftuoglu M, de Souza-Pinto NC, Dogan A, Aamann M, Stevnsner T, Rybanska I, et al. Cockayne syndrome group B protein stimulates repair of formamidopyrimidines by NEIL1 DNA glycosylase. J Biol Chem 2009;284: 9270–9279.
  • Liu M, Bandaru V, Bond JP, Jaruga P, Zhao X, Christov PP, et al. The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc Natl Acad Sci U S A 2010;107:4925–4930.
  • Kirkali G, Keles D, Canda AE, Terzi C, Reddy PT, Jaruga P, et al. Evidence for upregulated repair of oxidatively induced DNA damage in human colorectal cancer. DNA Repair (Amst) 2011;10:1114–1120.
  • Robinson CK, Webb K, Kaur A, Jaruga P, Dizdaroglu M, Baliga NS, et al. A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J Bacteriol 2011;193:1653–1662.
  • Petersen EJ, Tu X, Dizdaroglu M, Zheng M, Nelson BC. Protective roles of single-wall carbon nanotubes in ultra- sonication-induced DNA base damage. Small 2013;9: 205–208.
  • 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.
  • Karakaya A, Jaruga P, Bohr VA, Grollman AP, Dizdaroglu M. Kinetics of excision of purine lesions from DNA by Escherichia coli Fpg protein. Nucleic Acids Res 1997;25: 474–479.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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 2004;32:e87.
  • Egler RA, Fernandes E, Rothermund K, Sereika S, de Souza-Pinto N, Jaruga P, et al. Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1. Oncogene 2005;24:8038–8050.
  • D’Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, et al. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J 2006;25:4305–4315.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Altman SA, Zastawny TH, Randers-Eichhorn L, Cacciuttolo MA, Akman SA, Dizdaroglu M, Rao G. Formation of DNA-protein cross-links in cultured mammalian cells upon treatment with iron ions. Free Radic Biol Med 1995; 19:897–902.
  • 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.
  • 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.
  • 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.
  • Gajewski E, Dizdaroglu M. Hydroxyl Radical-Induced Cross-linking of Cytosine and Tyrosine in Nucleohistone. Biochemistry 1990;29:977–980.
  • Reddy DM, Iden CR. Analysis of modified deoxynucleosides by electrospray ionization mass spectrometry. Nucleos Nucleot 1993;12:815–826.
  • Pomerantz SC, McCloskey JA. Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry. Methods Enzymol 1990;193:796–824.
  • Serrano J, Palmeira CM, Wallace KB, Kuehl DW. Determination of 8-hydroxydeoxyguanosine in biological tissue by liquid chromatography/electrospray ionization-mass spectrometry/mass spectrometry. Rapid Commun Mass Spectrom 1996;10:1789–1791.
  • Ravanat JL, Duretz B, Guiller A, Douki T, Cadet J. Isotope dilution high-performance liquid chromatography-electrospray tandem mass spectrometry assay for the measurement of 8-oxo-7,8-dihydro-2’-deoxyguanosine in biological samples. J Chromatogr B Biomed Sci Appl 1998;715:349–356.
  • Podmore ID, Cooper D, Evans MD, Wood M, Lunec J. Simultaneous measurement of 8-oxo-2’-deoxyguanosine and 8-oxo-2’-deoxyadenosine by HPLC-MS/MS. Biochem Biophys Res Commun 2000;277:764–770.
  • Hua Y, Wainhaus SB, Yang T, Shen N, Yiong Y, Xu X, et al. Comparison of negative and positive ion electrospray tandem mass spectrometry for the liquid chromatography tandem mass spectrometry analysis of oxidized deoxynucleosides. J Amer Soc Mass Spectrom 2000;12:80–87.
  • Weimann A, Belling D, Poulsen HE. Measurement of 8-oxo-2’-deoxyguanosine and 8-oxo-2’-deoxyadenosine in DNA and human urine by high performance liquid chromatography-electrospray tandem mass spectrometry. Free Radic Biol Med 2001;30:757–764.
  • 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.
  • Wang J, Cao H, You C, Yuan B, Bahde R, Gupta S, et al. Endogenous formation and repair of oxidatively induced G[8–5 m]T intrastrand cross-link lesion. Nucleic Acids Res 2012;40:7368–7374.
  • Jaruga P, Rodriguez H, Dizdaroglu M. Measurement of 8-hydroxy-2’-deoxyadenosine in DNA by liquid chromatography/mass spectrometry. Free Radic Biol Med 2001;31: 336–344.
  • Cadet J, Wagner JR. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. In: Friedberg EC, Elledge SJ, Lehmann AR, Lindahl T, Muzi-Falconi M, editors. DNA Repair, Mutagenesis, and Other responses to DNA Damage. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2014; pp. 1–18.
  • ESCODD. Comparison of different methods of measuring 8-oxoguanine as a marker of oxidative DNA damage. Free Radic Res 2000;32:333–341.
  • Tuo J, Muftuoglu M, Chen C, Jaruga P, Selzer RR, Brosh RM Jr., et al. The cockayne syndrome group B gene product is involved in general genome base excision repair of 8-hydroxyguanine in DNA. J Biol Chem 2001;276: 45772–45779.
  • Tuo J, Jaruga P, Rodriguez H, Bohr VA, Dizdaroglu M. Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. FASEB J 2003;17:668–674.
  • Rodriguez H, O’Connell C, Barker PE, Atha DH, Jaruga P, Birincioglu M, et al. Measurement of DNA biomarkers for the safety of tissue-engineered medical products, using artificial skin as a model. Tissue Eng 2004;10:1332–1345.
  • Trzeciak AR, Nyaga SG, Jaruga P, Lohani A, Dizdaroglu M, Evans MK. Cellular repair of oxidatively induced DNA base lesions is defective in prostate cancer cell lines, PC-3 and DU-145. Carcinogenesis 2004;25:1–12.
  • Nyaga SG, Lohani A, Jaruga P, Trzeciak AR, Dizdaroglu M, Evans MK. Reduced repair of 8-hydroxyguanine in the human breast cancer cell line, HCC1937. BMC Cancer 2006;6:297.
  • Mambo E, Chatterjee A, de Souza-Pinto NC, Mayard S, Hogue BA, Hoque MO, et al. Oxidized guanine lesions and hOgg1 activity in lung cancer. Oncogene 2005;24: 4496–4508.
  • Malins DC, Anderson KM, Jaruga P, Ramsey CR, Gilman NK, Green VM, et al. Oxidative changes in the DNA of stroma and epithelium from the female breast: Potential implications for breast cancer. Cell Cycle 2006;5: 1629–1632.
  • 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.
  • 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.
  • 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.
  • Anderson KM, Jaruga P, Ramsey CR, Gilman NK, Green VM, Rostad SW, et al. Structural alterations in breast stromal and epithelial DNA: The influence of 8,5’-cyclo-2’-deoxyadenosine. Cell Cycle 2006;5:1240–1244.
  • D’Errico M, Parlanti E, Teson M, Degan P, Lemma T, Calcagnile A, et al. The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 2007; 26:4336–4343.
  • 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.
  • 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.
  • 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.
  • 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.
  • Wang J, Clauson CL, Robbins PD, Niedernhofer LJ, Wang Y. The oxidative DNA lesions 8,5’-cyclopurines accumulate with aging in a tissue-specific manner. Aging Cell 2012; 11:714–716.
  • Tilstra JS, Robinson AR, Wang J, Gregg SQ, Clauson CL, Reay DP, et al. NF-kappaB inhibition delays DNA damage-induced senescence and aging in mice. J Clin Invest 2012;122:2601–2612.
  • Mitra D, Luo X, Morgan A, Wang J, Hoang MP, Lo J, et al. An ultraviolet-radiation-independent pathway to melanoma carcinogenesis in the red hair/fair skin background. Nature 2012;491:449–453.
  • Zhang F, Fu L, Wang Y. 6-Thioguanine induces mitochondrial dysfunction and oxidative DNA damage in acute lymphoblastic leukemia cells. Mol Cell Proteomics 2013;12:3803–3811.
  • Chatgilialoglu C, Ferreri C, Terzidis MA. Purine 5’,8-cyclonucleoside lesions: chemistry and biology. Chem Soc Rev 2011;40:1368–1382.
  • 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 Res 2007;35:7118–7127.
  • Cathcart R, Schwiers E, Saul RL, Ames BN. Thymine glycol and thymidine glycol in human and rat urine: a possible assay for oxidative DNA damage. Proc Natl Acad Sci USA 1984;81:5633–5637.
  • Shigenaga MK, Gimeno CJ, Ames BN. Urinary 8-hydroxy-2’-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc Natl Acad Sci U S A 1989; 86:9697–9701.
  • Gackowski D, Rozalski R, Roszkowski K, Jawien A, Foksinski M, Olinski R. 8-Oxo-7,8-dihydroguanine and 8-oxo-7,8-dihydro-2’-deoxyguanosine levels in human urine do not depend on diet. Free Radic Res 2001;35:825–832.
  • Weimann A, Belling D, Poulsen H. Quantification of 8-oxo-guanine and guanine as the nucleobase, nucleoside and deoxynucleoside forms in human urine by high-performance liquid chromatography-electrospray tandem mass spectrometry. Nucleic Acids Res 2002;30:E7.
  • Rozalski R, Gackowski D, Roszkowski K, Foksinski M, Olinski R. The level of 8-hydroxyguanine, a possible repair product of oxidative DNA damage, is higher in urine of cancer patients than in control subjects. Cancer Epidemiol Biomarkers Prev 2002;11:1072–1075.
  • Foksinski M, Gackowski D, Rozalski R, Olinski R. Cellular level of 8-oxo-2’-deoxyguanosine in DNA does not correlate with urinary excretion of the modified base/nucleoside. Acta Biochim Pol 2003;50:549–553.
  • Weimann A, Riis B, Poulsen HE. Oligonucleotides in human urine do not contain 8-oxo-7,8-dihydrodeoxyguanosine. Free Radic Biol Med 2004;36:1378–1382.
  • Rozalski R, Siomek A, Gackowski D, Foksinski M, Gran C, Klungland A, Olinski R. Substantial decrease of urinary 8-oxo-7,8-dihydroguanine, a product of the base excision repair pathway, in DNA glycosylase defective mice. Int J Biochem Cell Biol 2005;37:1331–1336.
  • de Waard H, de Wit J, Andressoo JO, van Oostrom CT, Riis B, Weimann A, et al. Different effects of CSA and CSB deficiency on sensitivity to oxidative DNA damage. Mol Cell Biol 2004;24:7941–7948.
  • Olinski R, Rozalski R, Gackowski D, Foksinski M, Siomek A, Cooke MS. Urinary measurement of 8-OxodG, 8-OxoGua, and 5HMUra: a noninvasive assessment of oxidative damage to DNA. Antioxid Redox Signal 2006;8:1011–1019.
  • Svoboda P, Maekawa M, Kawai K, Tominaga T, Savela K, Kasai H. Urinary 8-hydroxyguanine may be a better marker of oxidative stress than 8-hydroxydeoxyguanosine in relation to the life spans of various species. Antioxid Redox Signal 2006;8:985–992.
  • Cooke MS, Olinski R, Loft S. Measurement and meaning of oxidatively modified DNA lesions in urine. Cancer Epidemiol Biomarkers Prev 2008;17:3–14.
  • Dziaman T, Gackowski D, Rozalski R, Siomek A, Szulczynski J, Zabielski R, Olinski R. Urinary excretion rates of 8-oxoGua and 8-oxodG and antioxidant vitamins level as a measure of oxidative status in healthy, full-term newborns. Free Radic Res 2007;41:997–1004.
  • Cooke MS, Henderson PT, Evans MD. Sources of extracellular, oxidatively-modified DNA lesions: implications for their measurement in urine. J Clin Biochem Nutr 2009;45: 255–270.
  • Evans MD, Singh R, Mistry V, Farmer PB, Cooke MS. Analysis of urinary 8-oxo-7,8-dihydro-2’-deoxyguanosine by liquid chromatography-tandem mass spectrometry. Methods Mol Biol 2010;610:341–351.
  • Evans MD, Olinski R, Loft S, Cooke MS. Toward consensus in the analysis of urinary 8-oxo-7,8-dihydro-2’-deoxyguanosine as a noninvasive biomarker of oxidative stress. FASEB J 2010;24:1249–1260.
  • Garratt LW, Mistry V, Singh R, Sandhu JK, Sheil B, Cooke MS, et al. Interpretation of urinary 8-oxo-7,8-dihydro-2’-deoxyguanosine is adversely affected by methodological inaccuracies when using a commercial ELISA. Free Radic Biol Med 2010;48:1460–1464.
  • Hu CW, Huang YJ, Li YJ, Chao MR. Correlation between concentrations of 8-oxo-7,8-dihydro-2’-deoxyguanosine in urine, plasma and saliva measured by on-line solid-phase extraction LC-MS/MS. Clin Chim Acta 2010;411: 1218–1222.
  • Hu CW, Chao MR, Sie CH. Urinary analysis of 8-oxo-7,8-dihydroguanine and 8-oxo-7,8-dihydro-2’-deoxyguanosine by isotope-dilution LC-MS/MS with automated solid-phase extraction: Study of 8-oxo-7,8-dihydroguanine stability. Free Radic Biol Med 2010;48:89–97.
  • Mistry V, Teichert F, Sandhu JK, Singh R, Evans MD, Farmer PB, Cooke MS. Non-invasive assessment of oxidatively damaged DNA: liquid chromatography-tandem mass spectrometry analysis of urinary 8-oxo-7,8-dihydro- 2’-deoxyguanosine. Methods Mol Biol 2011;682: 279–289.
  • Roszkowski K, Olinski R. Urinary 8-oxoguanine as a predictor of survival in patients undergoing radiotherapy. Cancer Epidemiol Biomarkers Prev 2012;21:629–634.
  • Rossner P, Jr., Mistry V, Singh R, Sram RJ, Cooke MS. Urinary 8-oxo-7,8-dihydro-2’-deoxyguanosine values determined by a modified ELISA improves agreement with HPLC-MS/MS. Biochem Biophys Res Commun 2013;440: 725–730.
  • Barregard L, Moller P, Henriksen T, Mistry V, Koppen G, Rossner P, Jr., et al. Human and methodological sources of variability in the measurement of urinary 8-oxo-7,8-dihydro-2’-deoxyguanosine. Antioxid Redox Signal 2013;18: 2377–2391.
  • 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.
  • Brooks PJ, Wise DS, Berry DA, Kosmoski JV, Smerdon MJ, Somers RL, et al. The oxidative DNA lesion 8,5’-(S)-cyclo-2’-deoxyadenosine is repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J Biol Chem 2000;275:22355–22362.
  • Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. Removal of oxygen free-radical-induced 5’,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci U S A 2000;97:3832–3837.
  • Jaruga P, Rozalski R, Jawien A, Migdalski A, Olinski R, Dizdaroglu M. DNA damage products (5′R)- and (5′S)- 8,5’-cyclo-2’-deoxyadenosines as potential biomarkers in human urine for atherosclerosis. Biochemistry 2012;51: 1822–1824.
  • Madhusudan S, Middleton MR. The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer. Cancer Treat Rev 2005;31:603–617.
  • Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 2008;8:193–204.
  • Kelley MR. Future directions with DNA repair inhibitors: A roadmap for disruptive approaches to cancer therapy. In: Kelley MR, editor. DNA Repair in Cancer Therapy, Molecular Targets and Clinical Applications. Amsterdam: Elsevier; 2012; pp. 301–310.
  • Beckman RA. Genetic instability of cancer: Biological predictions and clinical implications. In: Madhusudan S, Wilson DM, III, editors. DNA Repair and Cancer From Bench to Clinic. Boca Raton: CRC Press; 2013; pp. 63–91.
  • Holohan C, Van SS, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013;13:714–726.
  • Reddy PT, Jaruga P, Nelson BC, Lowenthal M, Dizdaroglu M. Stable isotope-labeling of DNA repair proteins, and their purification and characterization. Protein Expr Purif 2011; 78:94–101.
  • Dizdaroglu M, Reddy PT, Jaruga P. Identification and quantification of DNA repair proteins by liquid chromatography/isotope-dilution tandem mass spectrometry using their fully 15N-labeled analogues as internal standards. J Proteome Res 2011;10:3802–3813.
  • Kirkali G, Jaruga P, Reddy PT, Tona A, Nelson BC, Li M, et al. Identification and quantification of DNA repair protein apurinic/apyrimidinic endonuclease 1 (APE1) in human cells by liquid chromatography/isotope-dilution tandem mass spectrometry. PLoS ONE 2013;8:e69894.
  • Jaruga P, Birincioglu M, Rosenquist TA, Dizdaroglu M. Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4,6-diamino-5- formamidopyrimidine from oxidatively damaged DNA. Biochemistry 2004;43:15909–15914.
  • Dherin C, Radicella JP, Dizdaroglu M, Boiteux S. Excision of oxidatively damaged DNA bases by the human alpha-hOgg1 protein and the polymorphic alpha-hOgg1(Ser326Cys) protein which is frequently found in human populations. Nucleic Acids Res 1999;27:4001–4007.
  • Dizdaroglu M. Gas chromatography-mass spectrometry of free radical-induced products of pyrimidines and purines in DNA. Methods Enzymol 1990;193:842–857.

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