The genomics of oxidative DNA damage, repair, and resulting mutagenesis

Computational and Structural Biotechnology Journal - Tập 18 - Trang 207-219 - 2020
Anna R. Poetsch1
1St. Anna Children’s Cancer Research Institute, Zimmermannplatz 10, 1090 Vienna, Austria

Tài liệu tham khảo

Markkanen, 2017, Not breathing is not an option: How to deal with oxidative DNA damage, DNA Repair (Amst), 59, 82, 10.1016/j.dnarep.2017.09.007 Paiva, 2014, Are reactive oxygen species always detrimental to pathogens, Antioxid Redox Signal, 20, 1000, 10.1089/ars.2013.5447 Reuter, 2010, Oxidative stress, inflammation, and cancer: how are they linked, Free Radic Biol Med, 49, 1603, 10.1016/j.freeradbiomed.2010.09.006 van Loon, 2010, Oxygen as a friend and enemy: How to combat the mutational potential of 8-oxo-guanine, DNA Repair (Amst), 9, 604, 10.1016/j.dnarep.2010.03.004 Roots, 1972, Protection of DNA molecules of cultured mammalian cells from radiation-induced single-strand scissions by various alcohols and SH compounds, Int J Radiat Biol Relat Stud Phys Chem Med, 21, 329, 10.1080/09553007214550401 Ward, 2000, Complexity of damage produced by ionizing radiation, Cold Spring Harb Symp Quant Biol, 65, 377, 10.1101/sqb.2000.65.377 Lehner, 2007 Sasani, 2019, Large, three-generation human families reveal post-zygotic mosaicism and variability in germline mutation accumulation, Elife, 8, 10.7554/eLife.46922 Crow, 2000, The origins, patterns and implications of human spontaneous mutation, Nat Rev Genet, 10.1038/35049558 Tubbs, 2017, Endogenous DNA damage as a source of genomic instability in cancer, Cell, 168, 644, 10.1016/j.cell.2017.01.002 Martincorena, 2015, Somatic mutation in cancer and normal cells, Science, 349, 1483, 10.1126/science.aab4082 Finkel, 2007, The common biology of cancer and ageing, Nature, 448, 767, 10.1038/nature05985 Kennedy, 2012, Somatic mutations in aging, cancer and neurodegeneration, Mech Ageing Dev, 133, 118, 10.1016/j.mad.2011.10.009 Lodato, 2018, Aging and neurodegeneration are associated with increased mutations in single human neurons, Science, 359, 555, 10.1126/science.aao4426 Ding, 2017, Sequencing the mouse genome for the oxidatively modified base 8-oxo-7,8-dihydroguanine by OG-seq, J Am Chem Soc, 139, 2569, 10.1021/jacs.6b12604 Wu, 2018, Nucleotide-resolution genome-wide mapping of oxidative DNA damage by click-code-seq, J Am Chem Soc Poetsch, 2018, Genomic landscape of oxidative DNA damage and repair reveals regioselective protection from mutagenesis, Genome Biol, 19, 215, 10.1186/s13059-018-1582-2 Amente, 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, 221, 10.1093/nar/gky1152 Pastukh, 2007, Sequence-specific oxidative base modifications in hypoxia-inducible genes, Free Radic Biol Med, 43, 1616, 10.1016/j.freeradbiomed.2007.08.027 Park, 2019, 8-OxoG in GC-rich Sp1 binding sites enhances gene transcription during adipose tissue development in juvenile mice, Sci Rep, 9, 15618, 10.1038/s41598-019-52139-z Pich, 2018, Somatic and germline mutation periodicity follow the orientation of the DNA minor groove around nucleosomes, Cell, 175, 1074, 10.1016/j.cell.2018.10.004 Tomkova, 2018, Mutational signature distribution varies with DNA replication timing and strand asymmetry, Genome Biol, 19, 129, 10.1186/s13059-018-1509-y Moore, 2013, DNA modifications repaired by base excision repair are epigenetic, DNA Repair (Amst), 12, 1152, 10.1016/j.dnarep.2013.10.002 Park, 2016, Gene-specific assessment of guanine oxidation as an epigenetic modulator for cardiac specification of mouse embryonic stem cells, PLoS One, 11 Fleming, 2017, 8-Oxo-7,8-dihydroguanine, friend and foe: Epigenetic-like regulator versus initiator of mutagenesis, DNA Repair (Amst), 56, 75, 10.1016/j.dnarep.2017.06.009 Coluzzi, 2014, Oxidative stress induces persistent telomeric DNA damage responsible for nuclear morphology change in mammalian cells, PLoS One, 9, 10.1371/journal.pone.0110963 Fouquerel, 2019, Targeted and persistent 8-oxoguanine base damage at telomeres promotes telomere loss and crisis, Mol Cell, 75, 117, 10.1016/j.molcel.2019.04.024 von Zglinicki, 2002, Oxidative stress shortens telomeres, Trends Biochem Sci, 27, 339, 10.1016/S0968-0004(02)02110-2 Allgayer, 2016, Widespread transcriptional gene inactivation initiated by a repair intermediate of 8-oxoguanine, Nucleic Acids Res, 44, 7267 Tornaletti, 2004, Effect of 8-oxoguanine on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II, DNA Repair (Amst), 3, 483, 10.1016/j.dnarep.2004.01.003 Liu, 2019, Sequencing abasic sites in DNA at single-nucleotide resolution, Nat Chem, 11, 629, 10.1038/s41557-019-0279-9 The International Cancer Genome Consortium et al, 2010, International network of cancer genome projects, Nature, 464, 993, 10.1038/nature08987 The Cancer Genome Atlas Research Network, 2013, The Cancer Genome Atlas Pan-Cancer analysis project, Nat Genet, 45, 1113, 10.1038/ng.2764 Blokzijl, 2016, Tissue-specific mutation accumulation in human adult stem cells during life, Nature, 538, 260, 10.1038/nature19768 Lee-Six, 2018, Population dynamics of normal human blood inferred from somatic mutations, Nature, 561, 473, 10.1038/s41586-018-0497-0 Martincorena, 2012, Evidence of non-random mutation rates suggests an evolutionary risk management strategy, Nature, 485, 95, 10.1038/nature10995 Martincorena, 2018, Somatic mutant clones colonize the human esophagus with age, Science, 362, 911, 10.1126/science.aau3879 Cadet, 2006, One-electron oxidation of DNA and inflammation processes, Nat Chem Biol, 2, 348, 10.1038/nchembio0706-348 Margolin, 2006, Paradoxical hotspots for guanine oxidation by a chemical mediator of inflammation, Nat Chem Biol, 2, 365, 10.1038/nchembio796 Cadet, 2017, Formation and repair of oxidatively generated damage in cellular DNA, Free Radic Biol Med, 107, 13, 10.1016/j.freeradbiomed.2016.12.049 Di Mascio, 2019, Singlet molecular oxygen reactions with nucleic acids, lipids, and proteins, Chem Rev, 119, 2043, 10.1021/acs.chemrev.8b00554 Lindahl, 1993, Instability and decay of the primary structure of DNA, Nature, 362, 709, 10.1038/362709a0 Maki, 1992, MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis, Nature, 355, 273, 10.1038/355273a0 Inoue, 1998, Induction of chromosomal gene mutations in Escherichia coli by direct incorporation of oxidatively damaged nucleotides. New evaluation method for mutagenesis by damaged DNA precursors in vivo, J. Biol. Chem., 273, 11069, 10.1074/jbc.273.18.11069 Satou, 2007, Mutagenic effects of 8-hydroxy-dGTP in live mammalian cells, Free Radic Biol Med, 42, 1552, 10.1016/j.freeradbiomed.2007.02.024 Satou, 2009, Involvement of specialized DNA polymerases in mutagenesis by 8-hydroxy-dGTP in human cells, DNA Repair (Amst), 8, 637, 10.1016/j.dnarep.2008.12.009 David, 2007, Base-excision repair of oxidative DNA damage, Nature, 447, 941, 10.1038/nature05978 Hamilton, 2001, A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA, Nucleic Acids Res, 29, 2117, 10.1093/nar/29.10.2117 Lindahl, 1972, Rate of depurination of native deoxyribonucleic acid, Biochemistry, 11, 3610, 10.1021/bi00769a018 Yamaguchi, 1996, Increased 8-hydroxyguanine levels in DNA and its repair activity in rat kidney after administration of a renal carcinogen, ferric nitrilotriacetate, Carcinogenesis, 17, 2419, 10.1093/carcin/17.11.2419 Gedik, 2005, Establishing the background level of base oxidation in human lymphocyte DNA, FASEB J, 19, 82, 10.1096/fj.04-1767fje Swenberg, 2011, Endogenous versus exogenous DNA adducts: their role in carcinogenesis, epidemiology, and risk assessment, Toxicol Sci, 120, S130, 10.1093/toxsci/kfq371 Rahimoff, 2017, 5-Formyl- and 5-carboxydeoxycytidines do not cause accumulation of harmful repair intermediates in stem cells, J Am Chem Soc, 139, 10359, 10.1021/jacs.7b04131 Birben, 2012, Oxidative stress and antioxidant defense, World Allergy Organ J, 5, 9, 10.1097/WOX.0b013e3182439613 Ramon, 1999, Effects of 8-oxo-7,8-dihydro-2′-deoxyguanosine on the binding of the transcription factor Sp1 to its cognate target DNA sequence (GC box), Free Radic Res, 31, 217, 10.1080/10715769900300781 Hailer-Morrison, 2003, Oxidized guanine lesions as modulators of gene transcription. Altered p50 binding affinity and repair shielding by 7,8-dihydro-8-oxo-2′-deoxyguanosine lesions in the NF-kappaB promoter element, Biochemistry, 42, 9761, 10.1021/bi034546k Khobta, 2010, Gene silencing induced by oxidative DNA base damage: association with local decrease of histone H4 acetylation in the promoter region, Nucleic Acids Res, 38, 4285, 10.1093/nar/gkq170 Larsen, 2004, Transcription activities at 8-oxoG lesions in DNA, DNA Repair (Amst), 3, 1457, 10.1016/j.dnarep.2004.06.008 Ruchko, 2009, Hypoxia-induced oxidative base modifications in the VEGF hypoxia-response element are associated with transcriptionally active nucleosomes, Free Radic Biol Med, 46, 352, 10.1016/j.freeradbiomed.2008.09.038 Pastukh, 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, L1367, 10.1152/ajplung.00236.2015 Fleming, 2017, Oxidative DNA damage is epigenetic by regulating gene transcription via base excision repair, Proc Natl Acad Sci U S A, 114, 2604, 10.1073/pnas.1619809114 Wang, 2018, The roles of base excision repair enzyme OGG1 in gene expression, Cell Mol Life Sci, 75, 3741, 10.1007/s00018-018-2887-8 Fleming, 2017, 8-Oxo-7,8-dihydroguanine in the context of a gene promoter g-quadruplex is an on-off switch for transcription, ACS Chem Biol, 12, 2417, 10.1021/acschembio.7b00636 Kwok, 2017, G-Quadruplexes: prediction, characterization, and biological application, Trends Biotechnol, 10.1016/j.tibtech.2017.06.012 Graham, 2017, Telomeres and telomerase in prostate cancer development and therapy, Nat Rev Urol, 14, 607, 10.1038/nrurol.2017.104 Sedletska, 2013, Replication fork collapse is a major cause of the high mutation frequency at three-base lesion clusters, Nucleic Acids Res, 41, 9339, 10.1093/nar/gkt731 Boiteux, 2004, Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae, DNA Repair (Amst), 3, 1, 10.1016/j.dnarep.2003.10.002 Sczepanski, 2010, Rapid DNA–protein cross-linking and strand scission by an abasic site in a nucleosome core particle, Proc Natl Acad Sci, 107, 22475, 10.1073/pnas.1012860108 Bravard, 2006, Redox regulation of human OGG1 activity in response to cellular oxidative stress, Mol Cell Biol, 26, 7430, 10.1128/MCB.00624-06 Morreall, 2015, Inactivation of a common OGG1 variant by TNF-alpha in mammalian cells, DNA Repair (Amst), 26, 15, 10.1016/j.dnarep.2014.11.007 Yoshihara, 2014, Genome-wide profiling of 8-oxoguanine reveals its association with spatial positioning in nucleus, DNA Res, 21, 603, 10.1093/dnares/dsu023 Poetsch A.R. AP-seq, a method to measure apurinic sites and small base adducts genome-wide. Methods in Molecular Biology - The Nucleus, 3rd edition (Springer) 2020. Kubo, 1992, A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion, Biochemistry, 31, 3703, 10.1021/bi00129a020 Atamna, 2000, A method for detecting abasic sites in living cells: age-dependent changes in base excision repair, Proc Natl Acad Sci USA, 97, 686, 10.1073/pnas.97.2.686 Nakamura, 1998, Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions, Cancer Res, 58, 222 Nakano, 2002, Detection of NO-induced DNA lesions by the modified aldehyde reactive probe (ARP) assay, Nucleic Acids Res Suppl, 239–240 Roberts, 2006, Determination of apurinic/apyrimidinic lesions in DNA with high-performance liquid chromatography and tandem mass spectrometry, Chem Res Toxicol, 19, 300, 10.1021/tx0502589 Mitchell, 2002, Development and application of a novel immunoassay for measuring oxidative DNA damage in the environment, Photochem Photobiol, 75, 257, 10.1562/0031-8655(2002)075<0257:DAAOAN>2.0.CO;2 Serrano, 1996, Determination of 8-hydroxydeoxyguanosine in biological tissue by liquid chromatography/electrospray ionization-mass spectrometry/mass spectrometry, Rapid Commun Mass Spectrom, 10, 1789, 10.1002/(SICI)1097-0231(199611)10:14<1789::AID-RCM752>3.0.CO;2-6 Krishnamurthy, 2008, Efficient removal of formamidopyrimidines by 8-oxoguanine glycosylases, Biochemistry, 47, 1043, 10.1021/bi701619u David, 1998, Chemistry of glycosylases and endonucleases involved in base-excision repair, Chem Rev, 98, 1221, 10.1021/cr980321h Raiber, 2012, Genome-wide distribution of 5-formylcytosine in embryonic stem cells is associated with transcription and depends on thymine DNA glycosylase, Genome Biol, 13, R69, 10.1186/gb-2012-13-8-r69 Ravanat, 2002, Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up, Carcinogenesis, 23, 1911, 10.1093/carcin/23.11.1911 Costello, 2013, Discovery and characterization of artifactual mutations in deep coverage targeted capture sequencing data due to oxidative DNA damage during sample preparation, Nucleic Acids Res, 41, 10.1093/nar/gks1443 Akatsuka, 2006, Contrasting genome-wide distribution of 8-hydroxyguanine and acrolein-modified adenine during oxidative stress-induced renal carcinogenesis, Am J Pathol, 169, 1328, 10.2353/ajpath.2006.051280 van Steensel, 2017, Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression, Cell, 169, 780, 10.1016/j.cell.2017.04.022 Larson, 2017, Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin, Nature, 547, 236, 10.1038/nature22822 Strom, 2017, Phase separation drives heterochromatin domain formation, Nature, 547, 241, 10.1038/nature22989 Campalans, 2007, UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles, J Cell Sci, 120, 23, 10.1242/jcs.03312 Amouroux, 2010, Oxidative stress triggers the preferential assembly of base excision repair complexes on open chromatin regions, Nucleic Acids Res, 38, 2878, 10.1093/nar/gkp1247 Kubota, 2009, Localization of X-ray cross complementing gene 1 protein in the nuclear matrix is controlled by casein kinase II-dependent phosphorylation in response to oxidative damage, DNA Repair (Amst), 8, 953, 10.1016/j.dnarep.2009.06.003 Goodarzi, 2008, ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin, Mol Cell, 31, 167, 10.1016/j.molcel.2008.05.017 Kanu, 2010, The ATM cofactor ATMIN protects against oxidative stress and accumulation of DNA damage in the aging brain, J Biol Chem, 285, 38534, 10.1074/jbc.M110.145896 Blake, 2016, Inactivation of the ATMIN/ATM pathway protects against glioblastoma formation, Elife, 5, 10.7554/eLife.08711 Beard, 2003, Suppressed catalytic activity of base excision repair enzymes on rotationally positioned uracil in nucleosomes, Proc Natl Acad Sci USA, 100, 7465, 10.1073/pnas.1330328100 Menoni, 2007, ATP-dependent chromatin remodeling is required for base excision repair in conventional but not in variant H2A.Bbd nucleosomes, Mol Cell Biol, 27, 5949, 10.1128/MCB.00376-07 Menoni, 2017, Chromatin associated mechanisms in base excision repair – nucleosome remodeling and DNA transcription, two key players, Free Radic Biol Med, 107, 159, 10.1016/j.freeradbiomed.2016.12.026 Nilsen, 2002, DNA base excision repair of uracil residues in reconstituted nucleosome core particles, EMBO J, 21, 5943, 10.1093/emboj/cdf581 Bhakat, 2006, Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo, Mol Cell Biol, 26, 1654, 10.1128/MCB.26.5.1654-1665.2006 Margolin, 2008, DNA sequence context as a determinant of the quantity and chemistry of guanine oxidation produced by hydroxyl radicals and one-electron oxidants, J Biol Chem, 283, 35569, 10.1074/jbc.M806809200 Senthilkumar, 2003, Mapping the sites for selective oxidation of guanines in DNA, J Am Chem Soc, 125, 13658, 10.1021/ja037027d Rhee, 2011, Factors that influence telomeric oxidative base damage and repair by DNA glycosylase OGG1, DNA Repair (Amst), 10, 34, 10.1016/j.dnarep.2010.09.008 Zhou, 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, 27263, 10.1074/jbc.M113.479055 Cogoi, 2018, The regulatory G4 motif of the Kirsten ras (KRAS) gene is sensitive to guanine oxidation: implications on transcription, Nucleic Acids Res, 46, 661, 10.1093/nar/gkx1142 Broxson, 2014, Human AP endonuclease inefficiently removes abasic sites within G4 structures compared to duplex DNA, Nucleic Acids Res, 42, 7708, 10.1093/nar/gku417 Georgakopoulos-Soares, 2018, Noncanonical secondary structures arising from non-B DNA motifs are determinants of mutagenesis, Genome Res, 28, 1264, 10.1101/gr.231688.117 Farkash, 2006, Gamma radiation increases endonuclease-dependent L1 retrotransposition in a cultured cell assay, Nucleic Acids Res, 34, 1196, 10.1093/nar/gkj522 Liu, 2018, Selective silencing of euchromatic L1s revealed by genome-wide screens for L1 regulators, Nature, 553, 228, 10.1038/nature25179 Fleming, 2019, Location dependence of the transcriptional response of a potential G-quadruplex in gene promoters under oxidative stress, Nucleic Acids Res, 47, 5049, 10.1093/nar/gkz207 Weiner, 2015, High-resolution chromatin dynamics during a yeast stress response, Mol Cell, 58, 371, 10.1016/j.molcel.2015.02.002 Li, 2013, The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSα, Cell, 153, 590, 10.1016/j.cell.2013.03.025 Frigola, 2017, Reduced mutation rate in exons due to differential mismatch repair, Nat Genet, 49, 1684, 10.1038/ng.3991 Supek, 2015, Differential DNA mismatch repair underlies mutation rate variation across the human genome, Nature, 521, 81, 10.1038/nature14173 Supek, 2019, Scales and mechanisms of somatic mutation rate variation across the human genome, DNA Repair (Amst), 102647 Mao, 2017, Genome-wide maps of alkylation damage, repair, and mutagenesis in yeast reveal mechanisms of mutational heterogeneity, Genome Res, 27, 1674, 10.1101/gr.225771.117 Natale, 2017, Identification of the elementary structural units of the DNA damage response, Nat Commun, 8, 15760, 10.1038/ncomms15760 Kim, 2012, Transcription as a source of genome instability, Nat Rev Genet, 13, 204, 10.1038/nrg3152 Sondka, 2018, The COSMIC Cancer Gene Census: describing genetic dysfunction across all human cancers, Nat Rev Cancer, 18, 696, 10.1038/s41568-018-0060-1 Jiang, 2017, Direct LC-MS/MS detection of guanine oxidations in exon 7 of the p53 tumor suppressor gene, Anal Chem, 89, 12872, 10.1021/acs.analchem.7b03487 Kawai, 2002, Regulation of one-electron oxidation rate of guanine by base pairing with cytosine derivatives, J Am Chem Soc, 124, 3586, 10.1021/ja016530s Ming, 2014, Mapping structurally defined guanine oxidation products along DNA duplexes: influence of local sequence context and endogenous cytosine methylation, J Am Chem Soc, 136, 4223, 10.1021/ja411636j Sassa, 2014, Base excision repair of tandem modifications in a methylated CpG dinucleotide, J Biol Chem, 289, 13996, 10.1074/jbc.M114.557769 Kasymov, 2013, Excision of 8-oxoguanine from methylated CpG dinucleotides by human 8-oxoguanine DNA glycosylase, FEBS Lett, 587, 3129, 10.1016/j.febslet.2013.08.008 Xia, 2017, CHD4 has oncogenic functions in initiating and maintaining epigenetic suppression of multiple tumor suppressor genes, Cancer Cell, 31, 653, 10.1016/j.ccell.2017.04.005 Kamenisch, 2010, Proteins of nucleotide and base excision repair pathways interact in mitochondria to protect from loss of subcutaneous fat, a hallmark of aging, J Exp Med, 207, 379, 10.1084/jem.20091834 Noren Hooten, 2011, Poly(ADP-ribose) polymerase 1 (PARP-1) binds to 8-oxoguanine-DNA glycosylase (OGG1), J Biol Chem, 286, 44679, 10.1074/jbc.M111.255869 Pal, 2015, CUX2 protein functions as an accessory factor in the repair of oxidative DNA damage, J Biol Chem, 290, 22520, 10.1074/jbc.M115.651042 Ramdzan, 2014, RAS transformation requires CUX1-dependent repair of oxidative DNA damage, PLoS Biol, 12, 10.1371/journal.pbio.1001807 Ewing, 2007, Large-scale mapping of human protein-protein interactions by mass spectrometry, Mol Syst Biol, 3, 89, 10.1038/msb4100134 Bhakat, 2003, Role of acetylated human AP-endonuclease (APE1/Ref-1) in regulation of the parathyroid hormone gene, EMBO J, 22, 6299, 10.1093/emboj/cdg595 Yamamori, 2010, SIRT1 deacetylates APE1 and regulates cellular base excision repair, Nucleic Acids Res, 38, 832, 10.1093/nar/gkp1039 Vascotto, 2009, APE1/Ref-1 interacts with NPM1 within nucleoli and plays a role in the rRNA quality control process, Mol Cell Biol, 29, 1834, 10.1128/MCB.01337-08 Kuninger, 2002, Human AP-endonuclease 1 and hnRNP-L interact with a nCaRE-like repressor element in the AP-endonuclease 1 promoter, Nucleic Acids Res, 30, 823, 10.1093/nar/30.3.823 Hirota, 1997, AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1, Proc Natl Acad Sci USA, 94, 3633, 10.1073/pnas.94.8.3633 Berquist, 2008, Characterization of abasic endonuclease activity of human Ape1 on alternative substrates, as well as effects of ATP and sequence context on AP site incision, J Mol Biol, 379, 17, 10.1016/j.jmb.2008.03.053 Fleming, 2019, Oxidative modification of guanine in a potential Z-DNA-forming sequence of a gene promoter impacts gene expression, Chem Res Toxicol, 32, 899, 10.1021/acs.chemrestox.9b00041 Cogoi, 2014, HRAS is silenced by two neighboring G-quadruplexes and activated by MAZ, a zinc-finger transcription factor with DNA unfolding property, Nucleic Acids Res, 42, 8379, 10.1093/nar/gku574 Yin, 2017, Impact of cytosine methylation on DNA binding specificities of human transcription factors, Science, 356, 10.1126/science.aaj2239 Tomkova, 2018, DNA modifications: naturally more error prone, Trends Genet, 34, 627, 10.1016/j.tig.2018.04.005 Perillo, 2008, DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression, Science, 319, 202, 10.1126/science.1147674 Duncan, 1980, Mutagenic deamination of cytosine residues in DNA, Nature, 287, 560, 10.1038/287560a0 Cooper, 1989, Cytosine methylation and the fate of CpG dinucleotides in vertebrate genomes, Hum Genet, 83, 181, 10.1007/BF00286715 Shibutani, 1991, Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG, Nature, 349, 431, 10.1038/349431a0 Markkanen, 2013, MUTYH DNA glycosylase: the rationale for removing undamaged bases from the DNA, Front Genet, 4, 18, 10.3389/fgene.2013.00018 Loeb, 1985, Apurinic sites as mutagenic intermediates, Cell, 40, 483, 10.1016/0092-8674(85)90191-6 Sagher, 1983, Insertion of nucleotides opposite apurinic/apyrimidinic sites in deoxyribonucleic acid during in vitro synthesis: uniqueness of adenine nucleotides, Biochemistry, 22, 4518, 10.1021/bi00288a026 Shibutani, 1997, Translesional synthesis on DNA templates containing a single abasic site. A mechanistic study of the “A rule”, J Biol Chem, 272, 13916, 10.1074/jbc.272.21.13916 Suzuki, 2017, Mutations induced by 8-hydroxyguanine (8-oxo-7,8-dihydroguanine), a representative oxidized base, in mammalian cells, Genes Environ, 39, 2, 10.1186/s41021-016-0051-y Murugaesu, 2015, Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy, Cancer Discov, 5, 821, 10.1158/2159-8290.CD-15-0412 Ross-Innes, 2015, Whole-genome sequencing provides new insights into the clonal architecture of Barrett’s esophagus and esophageal adenocarcinoma, Nat Genet, 47, 1038, 10.1038/ng.3357 Dulak, 2013, Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity, Nat Genet, 45, 478, 10.1038/ng.2591 Nones, 2014, Genomic catastrophes frequently arise in esophageal adenocarcinoma and drive tumorigenesis, Nat Commun, 5, 5224, 10.1038/ncomms6224 Gonzalez-Perez, 2019, Local determinants of the mutational landscape of the human genome, Cell, 177, 101, 10.1016/j.cell.2019.02.051 Kucab, 2019, A Compendium of Mutational Signatures of Environmental Agents, Cell, 177, 821, 10.1016/j.cell.2019.03.001 Arbeithuber, 2016, Artifactual mutations resulting from DNA lesions limit detection levels in ultrasensitive sequencing applications, DNA Res, 23, 547, 10.1093/dnares/dsw038 Ma, 2019, Analysis of error profiles in deep next-generation sequencing data, Genome Biol, 20, 50, 10.1186/s13059-019-1659-6 Alexandrov, 2013, Signatures of mutational processes in human cancer, Nature, 500, 415, 10.1038/nature12477 Nik-Zainal, 2012, Mutational processes molding the genomes of 21 breast cancers, Cell, 149, 979, 10.1016/j.cell.2012.04.024 Alexandrov, 2018, The repertoire of mutational signatures in human cancer, bioRxiv, 322859 Connor, 2018, Mutational landscape of a chemically-induced mouse model of liver cancer, J Hepatol, 69, 840, 10.1016/j.jhep.2018.06.009 Meier, 2014, elegans whole-genome sequencing reveals mutational signatures related to carcinogens and DNA repair deficiency, Genome Res, 24, 1624, 10.1101/gr.175547.114 Zou, 2018, Validating the concept of mutational signatures with isogenic cell models, Nat Commun, 9, 1744, 10.1038/s41467-018-04052-8 Helleday, 2014, Mechanisms underlying mutational signatures in human cancers, Nat Rev Genet, 15, 585, 10.1038/nrg3729 Volkova, 2019, Mutational signatures are jointly shaped by DNA damage and repair, bioRxiv Peña-Diaz, 2017, Noncanonical mismatch repair as a source of genomic instability in human cells, Mol Cell, 67, 162, 10.1016/j.molcel.2017.06.026 Zlatanou, 2011, The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol η in response to oxidative DNA damage in human cells, Mol Cell, 43, 649, 10.1016/j.molcel.2011.06.023 Petljak, 2019, Characterizing mutational signatures in human cancer cell lines reveals episodic APOBEC mutagenesis, Cell, 176, 1282, 10.1016/j.cell.2019.02.012 Supek, 2017, Clustered mutation signatures reveal that error-prone DNA repair targets mutations to active genes, Cell, 170, 534, 10.1016/j.cell.2017.07.003 Rashid, 2016, Adenoma development in familial adenomatous polyposis and MUTYH-associated polyposis: somatic landscape and driver genes, J Pathol, 238, 98, 10.1002/path.4643 Pich, 2019, The mutational footprints of cancer therapies, Nat Genet, 51, 1732, 10.1038/s41588-019-0525-5 Christensen, 2019, 5-Fluorouracil treatment induces characteristic T>G mutations in human cancer, Nat Commun, 10, 4571, 10.1038/s41467-019-12594-8 Lujan, 2014, Heterogeneous polymerase fidelity and mismatch repair bias genome variation and composition, Genome Res, 24, 1751, 10.1101/gr.178335.114 Reijns, 2015, Lagging-strand replication shapes the mutational landscape of the genome, Nature, 518, 502, 10.1038/nature14183 Schuster-Böckler, 2012, Chromatin organization is a major influence on regional mutation rates in human cancer cells, Nature, 488, 504, 10.1038/nature11273 Polak, 2014, Reduced local mutation density in regulatory DNA of cancer genomes is linked to DNA repair, Nat Biotechnol, 32, 71, 10.1038/nbt.2778 Morganella, 2016, The topography of mutational processes in breast cancer genomes, Nat Commun, 7, 11383, 10.1038/ncomms11383 Liu, 2012, Proton-coupled hole hopping in nucleosomal and free DNA initiated by site-specific hole injection, Phys Chem Chem Phys, 14, 7400, 10.1039/c2cp40759k