Chemistry of ROS-mediated oxidation to the guanine base in DNA and its biological consequences

References

• Aller P, Ye Y, Wallace SS, Burrows CJ, Doublie S. 2010. Crystal structure of a replicative DNA polymerase bound to the oxidized guanine lesion guanidinohydantoin. Biochemistry. 49(11):2502–2509.
   PubMed Web of Science ®Google Scholar
• Alshykhly OR, Fleming AM, Burrows CJ. 2015a. Guanine oxidation product 5-carboxamido-5-formamido-2-iminohydantoin induces mutations when bypassed by DNA polymerases and is a substrate for base excision repair. Chem Res Toxicol. 28(9):1861–1871.
   PubMed Web of Science ®Google Scholar
• Alshykhly OR, Fleming AM, Burrows CJ. 2015b. 5-Carboxamido-5-formamido-2-iminohydantoin, in addition to 8-oxo-7,8-dihydroguanine, is the major product of the iron-Fenton or X-ray radiation-induced oxidation of guanine under aerobic reducing conditions in nucleoside and DNA contexts. J Org Chem. 80(14):6996–7007.
   PubMed Web of Science ®Google Scholar
• Amente S, Di Palo G, Scala G, Castrignanò T, Gorini F, Cocozza S, Moresano A, Pucci P, Ma B, Stepanov I, et al. 2019. Genome-wide mapping of 8-oxo-7,8-dihydro-2’-deoxyguanosine reveals accumulation of oxidatively-generated damage at DNA replication origins within transcribed long genes of mammalian cells. Nucleic Acids Res. 47(1):221–236.
   PubMed Web of Science ®Google Scholar
• Berger M, Cadet J. 1985. Isolation and characterization of the radiation-induced degradation products of 2`-deoxyguanosine in oxygen-free aqueou solutions. Z Naturforsch. 40(11):1519–1531.
   Google Scholar
• Cadet J, Douki T, Ravanat J-L. 2008. Oxidatively generated damage to the guanine moiety of DNA: mechanistic aspects and formation in cells. Acc Chem Res. 41(8):1075–1083.
   PubMed Web of Science ®Google Scholar
• Cadet J, Loft S, Olinski R, Evans MD, Bialkowski K, Wagner RJ, Dedon PC, Møller P, Greenberg MM, Cooke MS. 2012. Biologically relevant oxidants and terminology, classification and nomenclature of oxidatively generated damage to nucleobases and 2-deoxyribose in nucleic acids. Free Radic Res. 46(4):367–381.
   PubMed Web of Science ®Google Scholar
• Cadet J, Wagner RJ, Shafirovich V, Geacintov NE. 2014. One-electron oxidation reactions of purine and pyrimidine bases in cellular DNA. Int J Radiat Biol. 90(6):423–432.
   PubMed Web of Science ®Google Scholar
• Chatgilialoglu C, Ferreri C, Terzidis MA. 2011. Purine 5’,8-cyclonucleoside lesions: chemistry and biology. Chem Soc Rev. 40(3):1368–1382.
   PubMed Web of Science ®Google Scholar
• Cho BP, Kadlubar FF, Culp SJ, Evans FE. 1990. 15N nuclear magnetic resonance studies on the tautomerism of 8-hydroxy-2’-deoxyguanosine, 8-hydroxyguanosine, and other C8-substituted guanine nucleosides. Chem Res Toxicol. 3(5):445–452.
   PubMed Web of Science ®Google Scholar
• Cooke MS, Evans MD, Dizdaroglu M, Lunec J. 2003. Oxidative DNA damage: mechanisms, mutation, and disease. Faseb J. 17(10):1195–1214.
   PubMed Web of Science ®Google Scholar
• Crean C, Geacintov NE, Shafirovich V. 2005. Oxidation of guanine and 8-oxo-7,8-dihydroguanine by carbonate radical anions: insight from oxygen-18 labeling experiments. Angew Chem Int Ed Engl. 44(32):5057–5060.
   PubMed Web of Science ®Google Scholar
• Cui L, Ye W, Prestwich EG, Wishnok JS, Taghizadeh K, Dedon PC, Tannenbaum SR. 2013. Comparative analysis of four oxidized guanine lesions from reactions of DNA with peroxynitrite, singlet oxygen, and γ-radiation. Chem Res Toxicol. 26(2):195–202.
   PubMed Web of Science ®Google Scholar
• David SS, O’Shea VL, Kundu S. 2007. Base-excision repair of oxidative DNA damage. Nature. 447(7147):941–950.
   PubMed Web of Science ®Google Scholar
• De Bont R, van Larebeke N. 2004. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis. 19(3):169–185.
   PubMed Web of Science ®Google Scholar
• Ding Y, Fleming AM, Burrows CJ. 2017. Sequencing the mouse genome for the oxidatively modified base 8-oxo-7,8-dihydroguanine by OG-Seq. J Am Chem Soc. 139(7):2569–2572.
   PubMed Web of Science ®Google Scholar
• Dizdaroglu M. 2015. Oxidatively induced DNA damage and its repair in cancer. Mutat Res Rev Mutat Res. 763:212–245.
   PubMed Web of Science ®Google Scholar
• Douki T, Martini R, Ravanat JL, Turesky RJ, Cadet J. 1997. 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. 18(12):2385–2391.
   PubMed Web of Science ®Google Scholar
• Eckenroth BE, Fleming AM, Sweasy JB, Burrows CJ, Doublie S. 2014. Crystal structure of DNA polymerase β with DNA containing the base lesion spiroiminodihydantoin in a templating position. Biochemistry. 53(13):2075–2077.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2013. G-Quadruplex folds of the human telomere sequence alter the site reactivity and reaction pathway of guanine oxidation compared to duplex DNA. Chem Res Toxicol. 26(4):593–607.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2017a. Formation and processing of DNA damage substrates for the hNEIL enzymes. Free Radic Biol Med. 107:35–52.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2017b. 8-Oxo-7,8-dihydro-2’-deoxyguanosine and abasic site tandem lesions are oxidation prone yielding hydantoin products that strongly destabilize duplex DNA. Org Biomol Chem. 15(39):8341–8353.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2020a. Iron Fenton oxidation of 2’-deoxyguanosine in physiological bicarbonate buffer yields products consistent with the reactive oxygen species carbonate radical anion not the hydroxyl radical. Chem Commun. 56(68):9779–9782.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2020b. Interplay of guanine oxidation and G-quadruplex folding in gene promoters. J Am Chem Soc. 142(3):1115–1136.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2020c. On the irrelevancy of hydroxyl radical to DNA damage from oxidative stress and implications for epigenetics. Chem Soc Rev. 49(18):6524–6528.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Burrows CJ. 2021. Oxidative stress-mediated epigenetic regulation by G-quadruplexes. NAR Cancer. 3(3):zcab038.
   PubMedGoogle Scholar
• Fleming AM, Ding Y, Burrows CJ. 2017. Oxidative DNA damage is epigenetic by regulating gene transcription via base excision repair. Proc Natl Acad Sci USA. 114(10):2604–2609.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Muller JG, Dlouhy AC, Burrows CJ. 2012. Context effects in the oxidation of 8-oxo-7,8-dihydro-2’-deoxyguanosine to hydantoin products: electrostatics, base stacking, and base pairing. J Am Chem Soc. 134(36):15091–15102.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Muller JG, Ji I, Burrows CJ. 2011. Characterization of 2’-deoxyguanosine oxidation products observed in the Fenton-like system Cu(II)/H2O2/reductant in nucleoside and oligodeoxynucleotide contexts. Org Biomol Chem. 9(9):3338–3348.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Orendt AM, He Y, Zhu J, Dukor RK, Burrows CJ. 2013. Reconciliation of chemical, enzymatic, spectroscopic and computational data to assign the absolute configuration of the DNA base lesion spiroiminodihydantoin. J Am Chem Soc. 135(48):18191–18204.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Zhu J, Ding Y, Burrows CJ. 2019. Location dependence of the transcriptional response of a potential G-quadruplex in gene promoters under oxidative stress. Nucleic Acids Res. 47(10):5049–5060.
   PubMed Web of Science ®Google Scholar
• Fleming AM, Zhu J, Howpay Manage SA, Burrows CJ. 2019. Human NEIL3 gene expression Regulated by Epigenetic-Like Oxidative DNA Modification. J Am Chem Soc. 141(28):11036–11046.
   PubMed Web of Science ®Google Scholar
• Frelon S, Douki T, Ravanat J-L, Pouget J-P, Tornabene C, Cadet J. 2000. High-performance liquid chromatography-tandem mass spectrometry measurement of radiation-induced base damage to isolated and cellular DNA. Chem Res Toxicol. 13(10):1002–1010.
   PubMed Web of Science ®Google Scholar
• Georgakilas AG, O'Neill P, Stewart RD. 2013. Induction and repair of clustered DNA lesions: what do we know so far? Radiat Res. 180(1):100–109.
   PubMed Web of Science ®Google Scholar
• Goodhead DT. 1994. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol. 65(1):7–17.
   PubMed Web of Science ®Google Scholar
• Greenberg MM. 2021. Tandem and Clustered Lesions from Radicals in Nucleic Acids from a Single Initial Chemical Event. In: Dizdaroglu M, Lloyd RS, editors. DNA Damage, Repair and Disease. London: Royal Society of Chemistry; p. 27–60.
   Google Scholar
• Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, Ames BN. 1998. DNA oxidation matters: The HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA. 95(1):288–293.
   PubMed Web of Science ®Google Scholar
• Henderson PT, Delaney JC, Muller JG, Neeley WL, Tannenbaum SR, Burrows CJ, Essigmann JM. 2003. The hydantoin lesions formed from oxidation of 7,8-dihydro-8-oxoguanine are potent sources of replication errors in vivo. Biochemistry. 42(31):9257–9262.
   PubMed Web of Science ®Google Scholar
• Illes E, Mizrahi A, Marks V, Meyerstein D. 2019. Carbonate-radical-anions, and not hydroxyl radicals, are the products of the Fenton reaction in neutral solutions containing bicarbonate. Free Radic Biol Med. 131:1–6.
   PubMed Web of Science ®Google Scholar
• Jia L, Shafirovich V, Shapiro R, Geacintov NE, Broyde S. 2005. Structural and thermodynamic features of spiroiminodihydantoin damaged DNA duplexes. Biochemistry. 44(40):13342–13353.
   PubMed Web of Science ®Google Scholar
• Joffe A, Geacintov NE, Shafirovich V. 2003. DNA lesions derived from the site selective oxidation of guanine by carbonate radical anions. Chem Res Toxicol. 16(12):1528–1538.
   PubMed Web of Science ®Google Scholar
• Klungland A, Rosewell I, Hollenbach S, Larsen E, Daly G, Epe B, Seeberg E, Lindahl T, Barnes DE. 1999. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci USA. 96(23):13300–13305.
   PubMed Web of Science ®Google Scholar
• Kornyushyna O, Burrows CJ. 2003. Effect of the oxidized guanosine lesions spiroiminodihydantoin and guanidinohydantoin on proofreading by Escherichia coli DNA polymerase I (Klenow Fragment) in different sequence contexts. Biochemistry. 42(44):13008–13018.
   PubMed Web of Science ®Google Scholar
• Kowalska M, Piekut T, Prendecki M, Sodel A, Kozubski W, Dorszewska J. 2020. Mitochondrial and nuclear DNA oxidative damage in physiological and pathological aging. DNA Cell Biol. 39(8):1410–1420.
   PubMed Web of Science ®Google Scholar
• Krishnamurthy N, Zhao X, Burrows CJ, David SS. 2008. Superior removal of hydantoin lesions relative to other oxidized bases by the human DNA glycosylase hNEIL1. Biochemistry. 47(27):7137–7146.
   PubMed Web of Science ®Google Scholar
• Kumar A, Pottiboyina V, Sevilla MD. 2011. Hydroxyl radical (OH•) reaction with guanine in an aqueous environment: a DFT study. J Phys Chem B. 115(50):15129–15137.
   PubMed Web of Science ®Google Scholar
• Lapi A, Pratviel G, Meunier B. 2001. Guanine oxidation in double-stranded DNA by MnTMPyP/KHSO(5): at least three independent reaction pathways. Met Based Drugs. 8(1):47–56.
   PubMedGoogle Scholar
• Li C, Delaney S. 2019. Challenges for base excision repair enzymes: acquiring access to damaged DNA in chromatin. Enzymes. 45:27–57.
   PubMedGoogle Scholar
• Liu M, Bandaru V, Bond JP, Jaruga P, Zhao X, Christov PP, Burrows CJ, Rizzo CJ, Dizdaroglu M, Wallace SS. 2010. The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc Natl Acad Sci USA. 107(11):4925–4930.
   PubMed Web of Science ®Google Scholar
• Lonkar P, Dedon PC. 2011. Reactive species and DNA damage in chronic inflammation: reconciling chemical mechanisms and biological fates. Int J Cancer. 128(9):1999–2009.
   PubMed Web of Science ®Google Scholar
• Luo W, Muller JG, Rachlin EM, Burrows CJ. 2000. Characterization of spiroiminodihydantoin as a product of one-electron oxidation of 8-oxo-7,8-dihydroguanosine. Org Lett. 2(5):613–616.
   PubMed Web of Science ®Google Scholar
• Luo W, Muller JG, Rachlin EM, Burrows CJ. 2001. Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem Res Toxicol. 14(7):927–938.
   PubMed Web of Science ®Google Scholar
• Mangerich A, Knutson CG, Parry NM, Muthupalani S, Ye W, Prestwich E, Cui L, McFaline JL, Mobley M, Ge Z, et al. 2012. Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci USA. 109(27):E1820–E1829.
   PubMed Web of Science ®Google Scholar
• McKelvey KJ, Hudson AL, Back M, Eade T, Diakos CI. 2018. Radiation, inflammation and the immune response in cancer. Mamm Genome. 29(11–12):843–865.
   PubMed Web of Science ®Google Scholar
• Moore SP, Toomire KJ, Strauss PR. 2013. DNA modifications repaired by base excision repair are epigenetic. DNA Repair. 12(12):1152–1158.
   PubMed Web of Science ®Google Scholar
• Neeley WL, Delaney S, Alekseyev YO, Jarosz DF, Delaney JC, Walker GC, Essigmann JM. 2007. DNA Polymerase V allows bypass of toxic guanine oxidation products in vivo. J Biol Chem. 282(17):12741–12748.
   PubMed Web of Science ®Google Scholar
• Neeley WL, Essigmann JM. 2006. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol. 19(4):491–505.
   PubMed Web of Science ®Google Scholar
• Pan L, Zhu B, Hao W, Zeng X, Vlahopoulos SA, Hazra TK, Hegde ML, Radak Z, Bacsi A, Brasier AR, et al. 2016. Oxidized guanine base lesions function in 8-oxoguanine DNA Glycosylase-1-mediated epigenetic regulation of nuclear factor κB-driven gene expression. J Biol Chem. 291(49):25553–25566.
   PubMed Web of Science ®Google Scholar
• Pastukh V, Roberts JT, Clark DW, Bardwell GC, Patel M, Al-Mehdi AB, Borchert GM, Gillespie MN. 2015. An oxidative DNA “damage” and repair mechanism localized in the VEGF promoter is important for hypoxia-induced VEGF mRNA expression. Am J Physiol Lung Cell Mol Physiol. 309(11):L1367–1375.
   PubMed Web of Science ®Google Scholar
• Perillo B, Ombra MN, Bertoni A, Cuozzo C, Sacchetti S, Sasso A, Chiariotti L, Malorni A, Abbondanza C, Avvedimento EV. 2008. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science. 319(5860):202–206.
   PubMed Web of Science ®Google Scholar
• Pogozelski WK, Tullius TD. 1998. Oxidative strand scission of nucleic acids: routes initiated by hydrogen abstraction from the sugar moiety. Chem Rev. 98(3):1089–1108.
   PubMed Web of Science ®Google Scholar
• Riedl J, Ding Y, Fleming AM, Burrows CJ. 2015. Identification of DNA lesions using a third base pair for amplification and nanopore sequencing. Nat Commun. 6:8807.
   PubMed Web of Science ®Google Scholar
• Rokhlenko Y, Geacintov NE, Shafirovich V. 2012. Lifetimes and reaction pathways of guanine radical cations and neutral guanine radicals in an oligonucleotide in aqueous solutions. J Am Chem Soc. 134(10):4955–4962.
   PubMed Web of Science ®Google Scholar
• Saito I, Takayama M, Sugiyama H, Nakatani K, Tsuchida A, Yamamoto M. 1995. Photoinduced DNA cleavage via electron transfer: demonstration that guanine residues located 5’ to guanine are the most electron-donating sites. J Am Chem Soc. 117(23):6406–6407.
   Web of Science ®Google Scholar
• Scully R, Panday A, Elango R, Willis NA. 2019. DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat Rev Mol Cell Biol. 20(11):698–714.
   PubMed Web of Science ®Google Scholar
• Steenken S, Jovanovic SV, Bietti M, Bernhard K. 2000. The trap depth (in DNA) of 8-oxo-7,8-dihydro-2’deoxyguanosine as derived from electron-transfer equilibria in aqueous solution. J Am Chem Soc. 122(10):2373–2374.
   Web of Science ®Google Scholar
• Steenken S. 1989. Purine bases, nucleosides, and nucleotides: aqueous solution redox chemistry and transformation reactions of their radical cations and e- and OH adducts. Chem Rev. 89(3):503–520.
   Web of Science ®Google Scholar
• Sutherland BM, Bennett PV, Sidorkina O, Laval J. 2000. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc Natl Acad Sci USA. 97(1):103–108.
   PubMed Web of Science ®Google Scholar
• Swarts SG, Smith GS, Miao L, Wheeler KT. 1996. Effects of formic acid hydrolysis on the quantitative analysis of radiation-induced DNA base damage products assayed by gas chromatography/mass spectrometry. Radiat Environ Biophys. 35(1):41–53.
   PubMed Web of Science ®Google Scholar
• Tse ECM, Zwang TJ, Bedoya S, Barton JK. 2019. Effective distance for DNA-mediated charge transport between repair proteins. ACS Cent Sci. 5(1):65–72.
   PubMed Web of Science ®Google Scholar
• Vialas C, Claparols C, Pratviel G, Meunier B. 2000. Guanine oxidation in double-stranded DNA by Mn-TMPyP/KHSO5: 5,8-Dihydroxy-7,8-dihydroguanine residue as a key precursor of imidazolone and parabanic acid derivatives. J Am Chem Soc. 122(10):2157–2167.
   Web of Science ®Google Scholar
• Vidal AE, Hickson ID, Boiteux S, Radicella JP. 2001. Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step. Nucleic Acids Res. 29(6):1285–1292.
   PubMed Web of Science ®Google Scholar
• Wu J, McKeague M, Sturla SJ. 2018. Nucleotide-resolution genome-wide mapping of oxidative DNA damage by click-code-seq. J Am Chem Soc. 140(31):9783–9787.
   PubMed Web of Science ®Google Scholar
• Ye W, Sangaiah R, Degen DE, Gold A, Jayaraj K, Koshlap KM, Boysen G, Williams J, Tomer KB, Mocanu V, et al. 2009. Iminohydantoin lesion induced in DNA by peracids and other epoxidizing oxidants. J Am Chem Soc. 131(17):6114–6123.
   PubMed Web of Science ®Google Scholar
• Ye Y, Munk BH, Muller JG, Cogbill A, Burrows CJ, Schlegel HB. 2009. Mechanistic aspects of the formation of guanidinohydantoin from spiroiminodihydantoin under acidic conditions. Chem Res Toxicol. 22(3):526–535.
   PubMed Web of Science ®Google Scholar
• Yeo J, Goodman RA, Schirle NT, David SS, Beal PA. 2010. RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc Natl Acad Sci USA. 107(48):20715–20719.
   PubMed Web of Science ®Google Scholar
• Zhou J, Liu M, Fleming AM, Burrows CJ, Wallace SS. 2013. Neil3 and NEIL1 DNA glycosylases remove oxidative damages from quadruplex DNA and exhibit preferences for lesions in the telomeric sequence context. J Biol Chem. 288(38):27263–27272.
   PubMed Web of Science ®Google Scholar