{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,3]],"date-time":"2026-11-03T11:02:40Z","timestamp":1793703760506,"version":"4.5.1"},"reference-count":119,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T00:00:00Z","timestamp":1726099200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["R35GM151021"],"award-info":[{"award-number":["R35GM151021"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Oncol."],"abstract":"<jats:p>Aldehyde exposure has been shown to lead to the formation of DNA damage comprising of DNA-protein crosslinks (DPCs), base adducts and interstrand or intrastrand crosslinks. DPCs have recently drawn more attention because of recent advances in detection and quantification of these adducts. DPCs are highly deleterious to genome stability and have been shown to block replication forks, leading to wide-spread mutagenesis. Cellular mechanisms to prevent DPC-induced damage include excision repair pathways, homologous recombination, and specialized proteases involved in cleaving the covalently bound proteins from DNA. These pathways were first discovered in formaldehyde-treated cells, however, since then, various other aldehydes have been shown to induce formation of DPCs in cells. Defects in DPC repair or aldehyde clearance mechanisms lead to various diseases including Ruijs-Aalfs syndrome and AMeD syndrome in humans. Here, we discuss recent developments in understanding how aldehydes form DPCs, how they are repaired, and the consequences of defects in these repair pathways.<\/jats:p>","DOI":"10.3389\/fonc.2024.1478373","type":"journal-article","created":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T02:45:27Z","timestamp":1726109127000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":38,"title":["Aldehyde-induced DNA-protein crosslinks- DNA damage, repair and mutagenesis"],"prefix":"10.3389","volume":"14","author":[{"given":"Thomas","family":"Blouin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalie","family":"Saini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,9,12]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.chemrestox.3c00045","article-title":"Aldehyde-associated mutagenesis\u2500Current state of knowledge","volume":"36","author":"Vijayraghavan","year":"2023","journal-title":"Chem Res Toxicol"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M111.318410","article-title":"T7 RNA polymerases backed up by covalently trapped proteins catalyze highly error prone transcription *","volume":"287","author":"Nakano","year":"2012","journal-title":"J Biol Chem"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M112.419358","article-title":"Translocation and stability of replicative DNA helicases upon encountering DNA-protein cross-links *","volume":"288","author":"Nakano","year":"2013","journal-title":"J Biol Chem"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2011.07.045","article-title":"Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase","volume":"146","author":"Fu","year":"2011","journal-title":"Cell"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1021\/cb5001795","article-title":"Synthesis of site-specific DNA\u2013protein conjugates and their effects on DNA replication","volume":"9","author":"Yeo","year":"2014","journal-title":"ACS Chem Biol"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1002\/anie.201708286","article-title":"Reversible DNA-protein cross-linking at epigenetic DNA marks","volume":"56","author":"Ji","year":"2017","journal-title":"Angew Chem Int Ed Engl"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2020.607045","article-title":"DNA-histone cross-links: formation and repair","volume":"8","author":"Pachva","year":"2020","journal-title":"Front Cell Dev Biol"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1038\/nrm4015","article-title":"DNA\u2013protein crosslink repair","volume":"16","author":"Stingele","year":"2015","journal-title":"Nat Rev Mol Cell Biol"},{"key":"B9","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.tibs.2014.10.012","article-title":"DNA\u2013protein crosslink repair: proteases as DNA repair enzymes","volume":"40","author":"Stingele","year":"2015","journal-title":"Trends Biochem Sci"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/ng.3103","article-title":"Mutations in SPRTN cause early onset hepatocellular carcinoma, genomic instability and progeroid features","volume":"46","author":"Lessel","year":"2014","journal-title":"Nat Genet"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1002\/ajmg.a.10730","article-title":"Atypical progeroid syndrome: An unknown helicase gene defect","author":"Ruijs","year":"2003","journal-title":"Am J Med Genet Part A - Wiley Online Library"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMc1413069","article-title":"Hidden formaldehyde in E-cigarette aerosols","volume":"372","author":"Jensen","year":"2015","journal-title":"N Engl J Med"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1016\/S0024-3205(98)00282-3","article-title":"Formaldehyde derived from dietary aspartame binds to tissue components in vivo","volume":"63","author":"Trocho","year":"1998","journal-title":"Life Sci"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2004.12.012","article-title":"Histone demethylation mediated by the nuclear amine oxidase homolog LSD1","volume":"119","author":"Shi","year":"2004","journal-title":"Cell"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1038\/nature04433","article-title":"Histone demethylation by a family of JmjC domain-containing proteins","volume":"439","author":"Tsukada","year":"2006","journal-title":"Nature"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1038\/nature00908","article-title":"Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage","volume":"419","author":"Trewick","year":"2002","journal-title":"Nature"},{"key":"B17","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1146\/annurev-biochem-060713-035513","article-title":"Mechanism and function of oxidative reversal of DNA and RNA methylation","volume":"83","author":"Shen","year":"2014","journal-title":"Annu Rev Biochem"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1038\/nature23481","article-title":"Mammals divert endogenous genotoxic formaldehyde into one-carbon metabolism","volume":"548","author":"Burgos-Barragan","year":"2017","journal-title":"Nature"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1038\/188327a0","article-title":"Reaction of formaldehyde with deoxyribonucleic acid in phage T1","volume":"188","author":"Sauerbier","year":"1960","journal-title":"Nature"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)57292-6","article-title":"REACTION OF FORMALDEHYDE WITH PROTEINS: VI. CROSS-LINKING OF AMINO GROUPS WITH PHENOL, IMIDAZOLE, OR INDOLE GROUPS","volume":"174","author":"Fraenkel-Conrat","year":"1948","journal-title":"J Biol Chem"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1021\/ja908282f","article-title":"Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers","volume":"132","author":"Lu","year":"2010","journal-title":"J Am Chem Soc"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M310752200","article-title":"Identification of formaldehyde-induced modifications in proteins: REACTIONS WITH MODEL PEPTIDES *","volume":"279","author":"Metz","year":"2004","journal-title":"J Biol Chem"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0004636","article-title":"A temporal threshold for formaldehyde crosslinking and fixation","volume":"4","author":"Schmiedeberg","year":"2009","journal-title":"PloS One"},{"key":"B24","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/0005-2787(73)90415-2","article-title":"The reaction of formaldehyde with deoxynucleotides and DNA in the presence of amino acids and lysine-rich histone","volume":"331","author":"Siomin","year":"1973","journal-title":"Biochim Biophys Acta BBA - Nucleic Acids Protein Synth"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)83362-2","article-title":"Isolation and characterization of proteins cross-linked to DNA by the antitumor agent methylene dimethanesulfonate and its hydrolytic product formaldehyde","volume":"264","author":"O\u2019Connor","year":"1989","journal-title":"J Biol Chem"},{"key":"B26","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1038\/s41467-023-35988-1","article-title":"SPRTN patient variants cause global-genome DNA-protein crosslink repair defects","volume":"14","author":"Weickert","year":"2023","journal-title":"Nat Commun"},{"key":"B27","article-title":"Carcinogenicity of formaldehyde in rats and mice after long-term inhalation exposure","volume":"43","author":"Kerns","year":"1983","journal-title":"Cancer Res"},{"key":"B28","article-title":"Correlation of regional and nonlinear formaldehyde-induced nasal cancer with proliferating populations of cells","volume":"56","author":"Monticello","year":"1996","journal-title":"Cancer Res"},{"key":"B29","article-title":"Induction of squamous cell carcinomas of the rat nasal cavity by inhalation exposure to formaldehyde vapor","volume":"40","author":"Swenberg","year":"1980","journal-title":"Cancer Res"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1186\/1479-7364-5-4-283","article-title":"Update on the aldehyde dehydrogenase gene (ALDH) superfamily","volume":"5","author":"Jackson","year":"2011","journal-title":"Hum Genomics"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2015.08.020","article-title":"Endogenous formaldehyde is a hematopoietic stem cell genotoxin and metabolic carcinogen","volume":"60","author":"Pontel","year":"2015","journal-title":"Mol Cell"},{"key":"B32","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1016\/j.molcel.2020.10.012","article-title":"Two aldehyde clearance systems are essential to prevent lethal formaldehyde accumulation in mice and humans","volume":"80","author":"Dingler","year":"2020","journal-title":"Mol Cell"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-15-2527","article-title":"Measurement of endogenous versus exogenous formaldehyde-induced DNA-protein crosslinks in animal tissues by stable isotope labeling and ultrasensitive mass spectrometry","volume":"76","author":"Lai","year":"2016","journal-title":"Cancer Res"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1016\/j.dnarep.2020.102806","article-title":"DNA-protein crosslink formation by endogenous aldehydes and AP sites","volume":"88","author":"Nakamura","year":"2020","journal-title":"DNA Repair"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1016\/0272-0590(91)90230-2","article-title":"Covalent binding of inhaled formaldehyde to DNA in the respiratory tract of rhesus monkeys: Pharmacolinetics, rat-to-monkey interspecies scaling, and extrapolation to man","volume":"17","author":"Casanova","year":"1991","journal-title":"Fundam Appl Toxicol"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1136\/oem.60.6.403","article-title":"DNA-protein crosslinks and p53 protein expression in relation to occupational exposure to formaldehyde","volume":"60","author":"Shaham","year":"2003","journal-title":"Occup Environ Med"},{"key":"B37","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/0009-2797(95)03632-V","article-title":"Studies of the reaction of acetaldehyde with deoxynucleosides","volume":"98","author":"Vaca","year":"1995","journal-title":"Chem Biol Interact"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1021\/tx000118t","article-title":"Identification of DNA adducts of acetaldehyde","volume":"13","author":"Wang","year":"2000","journal-title":"Chem Res Toxicol"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1093\/carcin\/13.11.2095","article-title":"Reaction kinetics of DNA\u2014histone crosslinking by vinyl acetate and acetaldehyde","volume":"13","author":"Kuykendall","year":"1992","journal-title":"Carcinogenesis"},{"key":"B40","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/0027-5107(94)90072-8","article-title":"Formation and stability of acetaldehyde-induced crosslinks between poly-lysine and poly-deoxyguanosine","volume":"311","author":"Kuykendall","year":"1994","journal-title":"Mutat Res Mol Mech Mutagen"},{"key":"B41","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1080\/15384101.2016.1237326","article-title":"Genetic controls of DNA damage avoidance in response to acetaldehyde in fission yeast","volume":"16","author":"Noguchi","year":"2017","journal-title":"Cell Cycle"},{"key":"B42","doi-asserted-by":"publisher","first-page":"2024.01.07.574575","DOI":"10.1101\/2024.01.07.574575","article-title":"Multiple DNA repair pathways prevent acetaldehyde-induced mutagenesis in yeast","author":"Porcher","year":"2024"},{"key":"B43","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1002\/mnfr.200700412","article-title":"Acrolein: Sources, metabolism, and biomolecular interactions relevant to human health and disease","volume":"52","author":"Stevens","year":"2008","journal-title":"Mol Nutr Food Res"},{"key":"B44","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1021\/ar700246x","article-title":"Interstrand DNA cross-links induced by \u03b1,\u03b2-unsaturated aldehydes derived from lipid peroxidation and environmental sources","volume":"41","author":"Stone","year":"2008","journal-title":"Acc Chem Res"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1016\/j.mrfmmm.2007.08.001","article-title":"Mutagenic potential of DNA\u2013peptide crosslinks mediated by acrolein-derived DNA adducts","volume":"637","author":"Minko","year":"2008","journal-title":"Mutat Res"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1016\/j.jprot.2013.02.004","article-title":"Pathophysiological relevance of aldehydic protein modifications","volume":"92","author":"Zarkovic","year":"2013","journal-title":"J Proteomics"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1093\/toxsci\/kfu233","article-title":"Molecular mechanisms of acrolein toxicity: relevance to human disease","volume":"143","author":"Moghe","year":"2015","journal-title":"Toxicol Sci"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1021\/tx500068v","article-title":"Characterization of the deoxyguanosine\u2013lysine cross-link of methylglyoxal","volume":"27","author":"Petrova","year":"2014","journal-title":"Chem Res Toxicol"},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.1021\/tx050074u","article-title":"Evidence for the formation of adducts and S-(Carboxymethyl)cysteine on reaction of \u03b1-dicarbonyl compounds with thiol groups on amino acids, peptides, and proteins","volume":"18","author":"Zeng","year":"2005","journal-title":"Chem Res Toxicol"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1515\/DMDI.2008.23.1-2.125","article-title":"Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems - role in ageing and disease","volume":"23","author":"Thornalley","year":"2008","journal-title":"Drug Metabol Drug Interact"},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1007\/s00125-005-1810-7","article-title":"Degradation products of proteins damaged by glycation, oxidation and nitration in clinical type 1 diabetes","volume":"48","author":"Ahmed","year":"2005","journal-title":"Diabetologia"},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/29.16.3433","article-title":"Methylglyoxal, an endogenous aldehyde, crosslinks DNA polymerase and the substrate DNA","volume":"29","author":"Murata-Kamiya","year":"2001","journal-title":"Nucleic Acids Res"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1016\/j.numecd.2005.05.003","article-title":"A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress","volume":"15","author":"Rio","year":"2005","journal-title":"Nutr Metab Cardiovasc Dis"},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.3390\/antiox11112217","article-title":"Role of oxidative stress and lipid peroxidation in the pathophysiology of NAFLD","volume":"11","author":"Mart\u00edn-Fern\u00e1ndez","year":"2022","journal-title":"Antioxidants"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2013.00242","article-title":"Interaction of aldehydes derived from lipid peroxidation and membrane proteins","volume":"4","author":"Pizzimenti","year":"2013","journal-title":"Front Physiol"},{"key":"B56","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/0891-5849(91)90192-6","article-title":"Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes","volume":"11","author":"Esterbauer","year":"1991","journal-title":"Free Radic Biol Med"},{"key":"B57","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/S0027-5107(99)00010-X","article-title":"Lipid peroxidation\u2014DNA damage by malondialdehyde","volume":"424","author":"Marnett","year":"1999","journal-title":"Mutat Res Mol Mech Mutagen"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1093\/carcin\/17.5.1167","article-title":"Characterization of an N 6 -oxopropenyl-\u2032-deoxyadenosine adduct in malondialdehyde-modified DNA using liquid chromatography\/electrospry ionization tandem mass spectrometry","volume":"17","author":"Chaudhary","year":"1996","journal-title":"Carcinogenesis"},{"key":"B59","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/s0027-5107(99)00011-1","article-title":"Analysis of DNA-protein crosslinking activity of malondialdehyde in vitro","volume":"424","author":"Voitkun","year":"1999","journal-title":"Mutat Res"},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-07-1038","article-title":"5-Azacytidine induced methyltransferase-DNA adducts block DNA replication in vivo","volume":"67","author":"Kuo","year":"2007","journal-title":"Cancer Res"},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkm032","article-title":"Mechanism of the formation of DNA\u2013protein cross-links by antitumor cisplatin","volume":"35","author":"Chv\u00e1lov\u00e1","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gky444","article-title":"5-Formylcytosine mediated DNA\u2013protein cross-links block DNA replication and induce mutations in human cells","volume":"46","author":"Ji","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1002\/(sici)1098-2280(1998)32:3<260::aid-em9>3.0.co;2-m","article-title":"Significance of formaldehyde-induced DNA-protein crosslinks for mutagenesis","volume":"32","author":"Merk","year":"1998","journal-title":"Environ Mol Mutagen"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2014.04.053","article-title":"A DNA-dependent protease involved in DNA-protein crosslink repair","volume":"158","author":"Stingele","year":"2014","journal-title":"Cell"},{"key":"B65","doi-asserted-by":"publisher","first-page":"8270","DOI":"10.1038\/s41598-017-08834-w","article-title":"Structural analysis of Wss1 protein from saccharomyces cerevisiae","volume":"7","author":"Yang","year":"2017","journal-title":"Sci Rep"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.15252\/embj.2023113609","article-title":"Ubx5-Cdc48 assists the protease Wss1 at DNA-protein crosslink sites in yeast","volume":"42","author":"Noireterre","year":"2023","journal-title":"EMBO J"},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.1016\/j.dnarep.2014.03.020","article-title":"Tyrosyl-DNA-phosphodiesterases (TDP1 and TDP2)","volume":"19","author":"Pommier","year":"2014","journal-title":"DNA Repair"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1111\/mmi.14518","article-title":"Wss1 homolog from Candida albicans and its role in DNA\u2013protein crosslink tolerance","volume":"114","author":"Homchan","year":"2020","journal-title":"Mol Microbiol"},{"key":"B69","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1007\/s00294-020-01057-z","article-title":"Genetic investigation of formaldehyde-induced DNA damage response in Schizosaccharomyces pombe","volume":"66","author":"Anandarajan","year":"2020","journal-title":"Curr Genet"},{"key":"B70","doi-asserted-by":"publisher","DOI":"10.1038\/srep33671","article-title":"Structural studies of the yeast DNA damage-inducible protein Ddi1 reveal domain architecture of this eukaryotic protein family","volume":"6","author":"Trempe","year":"2016","journal-title":"Sci Rep"},{"key":"B71","doi-asserted-by":"publisher","first-page":"1066","DOI":"10.1016\/j.molcel.2019.12.007","article-title":"The aspartic protease ddi1 contributes to DNA-protein crosslink repair in yeast","volume":"77","author":"Serbyn","year":"2020","journal-title":"Mol Cell"},{"key":"B72","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s42003-020-01539-3","article-title":"DNA\u2013protein crosslink proteases in genome stability","volume":"4","author":"Ruggiano","year":"2021","journal-title":"Commun Biol"},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2006.08.086","article-title":"Ddi1, a eukaryotic protein with the retroviral protease fold","volume":"364","author":"Sirkis","year":"2006","journal-title":"J Mol Biol"},{"key":"B74","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.molcel.2017.11.035","article-title":"Removal of RTF2 from stalled replisomes promotes maintenance of genome integrity","volume":"69","author":"Kottemann","year":"2018","journal-title":"Mol Cell"},{"key":"B75","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.dnarep.2019.06.008","article-title":"The yeast proteases Ddi1 and Wss1 are both involved in the DNA replication stress response","volume":"80","author":"Svoboda","year":"2019","journal-title":"DNA Repair"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2014.09.024","article-title":"Repair of a DNA-protein crosslink by replication-coupled proteolysis","volume":"159","author":"Duxin","year":"2014","journal-title":"Cell"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.21491","article-title":"SPRTN is a mammalian DNA-binding metalloprotease that resolves DNA-protein crosslinks","volume":"5","author":"Lopez-Mosqueda","year":"2016","journal-title":"eLife"},{"key":"B78","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1016\/j.molcel.2016.09.031","article-title":"Mechanism and regulation of DNA-protein crosslink repair by the DNA-dependent metalloprotease SPRTN","volume":"64","author":"Stingele","year":"2016","journal-title":"Mol Cell"},{"key":"B79","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.molcel.2020.08.003","article-title":"DNA structure-specific cleavage of DNA-protein crosslinks by the SPRTN protease","volume":"80","author":"Reinking","year":"2020","journal-title":"Mol Cell"},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2016.09.032","article-title":"Metalloprotease SPRTN\/DVC1 orchestrates replication-coupled DNA-protein crosslink repair","volume":"64","author":"Vaz","year":"2016","journal-title":"Mol Cell"},{"key":"B81","doi-asserted-by":"publisher","DOI":"10.1038\/nsmb.2395","article-title":"DVC1 (C1orf124) is a DNA damage\u2013targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks","volume":"19","author":"Mosbech","year":"2012","journal-title":"Nat Struct Mol Biol"},{"key":"B82","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.molcel.2022.12.005","article-title":"The FANCJ helicase unfolds DNA-protein crosslinks to promote their repair","volume":"83","author":"Yaneva","year":"2023","journal-title":"Mol Cell"},{"key":"B83","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/j.dnarep.2018.08.025","article-title":"DNA protein crosslink proteolysis repair: From yeast to premature ageing and cancer in humans","volume":"71","author":"Fielden","year":"2018","journal-title":"DNA Repair"},{"key":"B84","doi-asserted-by":"publisher","first-page":"1318","DOI":"10.1038\/s41467-020-15170-7","article-title":"FAM111A protects replication forks from protein obstacles via its trypsin-like domain","volume":"11","author":"Kojima","year":"2020","journal-title":"Nat Commun"},{"key":"B85","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkab777","article-title":"Replication-dependent cytotoxicity and Spartan-mediated repair of trapped PARP1\u2013DNA complexes","volume":"49","author":"Saha","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1002949","article-title":"Identification of FAM111A as an SV40 host range restriction and adenovirus helper factor","volume":"8","author":"Fine","year":"2012","journal-title":"PloS Pathog"},{"key":"B87","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.19993","article-title":"A widely employed germ cell marker is an ancient disordered protein with reproductive functions in diverse eukaryotes","volume":"5","author":"Carmell","year":"2016","journal-title":"eLife"},{"key":"B88","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2014.08.010","article-title":"The spartan ortholog maternal haploid is required for paternal chromosome integrity in the drosophila zygote","volume":"24","author":"Delabaere","year":"2014","journal-title":"Curr Biol"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.15252\/embj.2019101496","article-title":"SUMOylation promotes protective responses to DNA-protein crosslinks","volume":"38","author":"Borgermann","year":"2019","journal-title":"EMBO J"},{"key":"B90","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.devcel.2019.11.007","article-title":"GCNA preserves genome integrity and fertility across species","volume":"52","author":"Bhargava","year":"2020","journal-title":"Dev Cell"},{"key":"B91","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.devcel.2019.11.006","article-title":"GCNA interacts with spartan and topoisomerase II to regulate genome stability","volume":"52","author":"Dokshin","year":"2020","journal-title":"Dev Cell"},{"key":"B92","doi-asserted-by":"publisher","DOI":"10.1038\/cr.2016.86","article-title":"The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death","volume":"26","author":"Livneh","year":"2016","journal-title":"Cell Res"},{"key":"B93","doi-asserted-by":"publisher","DOI":"10.1093\/carcin\/21.8.1573","article-title":"Loss of DNA\u2013protein crosslinks from formaldehyde-exposed cells occurs through spontaneous hydrolysis and an active repair process linked to proteosome function","volume":"21","author":"Quievryn","year":"2000","journal-title":"Carcinogenesis"},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.1016\/j.taap.2015.03.018","article-title":"Proteasome activity is important for replication recovery, CHK1 phosphorylation and prevention of G2 arrest after low-dose formaldehyde","volume":"286","author":"Ortega-Atienza","year":"2015","journal-title":"Toxicol Appl Pharmacol"},{"key":"B95","doi-asserted-by":"publisher","first-page":"574","DOI":"10.1016\/j.molcel.2018.11.024","article-title":"Replication-coupled DNA-protein crosslink repair by SPRTN and the proteasome in xenopus egg extracts","volume":"73","author":"Larsen","year":"2019","journal-title":"Mol Cell"},{"key":"B96","doi-asserted-by":"publisher","DOI":"10.1016\/0165-1218(85)90058-8","article-title":"Mutagenic characteristics of formaldehyde on bacterial systems","volume":"156","author":"Takahashi","year":"1985","journal-title":"Mutat Res Toxicol"},{"key":"B97","doi-asserted-by":"publisher","DOI":"10.1016\/j.dnarep.2009.06.007","article-title":"Cellular pathways for DNA repair and damage tolerance of formaldehyde-induced DNA-protein crosslinks","volume":"8","author":"de Graaf","year":"2009","journal-title":"DNA Repair"},{"key":"B98","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M702856200","article-title":"Nucleotide excision repair eliminates unique DNA-protein cross-links from mammalian cells *","volume":"282","author":"Baker","year":"2007","journal-title":"J Biol Chem"},{"key":"B99","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M109.019174","article-title":"Homologous recombination but not nucleotide excision repair plays a pivotal role in tolerance of DNA-protein cross-links in mammalian cells *","volume":"284","author":"Nakano","year":"2009","journal-title":"J Biol Chem"},{"key":"B100","doi-asserted-by":"publisher","DOI":"10.1038\/s41556-024-01401-2","article-title":"Endogenous aldehyde-induced DNA\u2013protein crosslinks are resolved by transcription-coupled repair","volume":"26","author":"Oka","year":"2024","journal-title":"Nat Cell Biol"},{"key":"B101","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-07-3028","article-title":"Cells deficient in the FANC\/BRCA pathway are hypersensitive to plasma levels of formaldehyde","volume":"67","author":"Ridpath","year":"2007","journal-title":"Cancer Res"},{"key":"B102","doi-asserted-by":"publisher","DOI":"10.1186\/s13578-019-0366-z","article-title":"DNA\u2013protein cross-link repair: what do we know now","volume":"10","author":"Zhang","year":"2020","journal-title":"Cell Biosci"},{"key":"B103","doi-asserted-by":"publisher","DOI":"10.1038\/nature03872","article-title":"Endonucleolytic processing of covalent protein-linked DNA double-strand breaks","volume":"436","author":"Neale","year":"2005","journal-title":"Nature"},{"key":"B104","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1083\/jcb.201504005","article-title":"MRN, CtIP, and BRCA1 mediate repair of topoisomerase II\u2013DNA adducts","volume":"212","author":"Aparicio","year":"2016","journal-title":"J Cell Biol"},{"key":"B105","doi-asserted-by":"publisher","DOI":"10.1242\/bio.20121834","article-title":"MRE11 facilitates the removal of human topoisomerase II complexes from genomic DNA","volume":"1","author":"Lee","year":"2012","journal-title":"Biol Open"},{"key":"B106","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2016.10.011","article-title":"Mre11 is essential for the removal of lethal topoisomerase 2 covalent cleavage complexes","volume":"64","author":"Hoa","year":"2016","journal-title":"Mol Cell"},{"key":"B107","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkab101","article-title":"Mechanisms of damage tolerance and repair during DNA replication","volume":"49","author":"Ashour","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"B108","doi-asserted-by":"publisher","DOI":"10.1038\/nsmb.2888","article-title":"Visualization of recombination-mediated damage bypass by template switching","volume":"21","author":"Giannattasio","year":"2014","journal-title":"Nat Struct Mol Biol"},{"key":"B109","doi-asserted-by":"publisher","DOI":"10.1111\/j.1349-7006.2012.02360.x","article-title":"Combination of ADH1B*2\/ALDH2*2 polymorphisms alters acetaldehyde-derived DNA damage in the blood of Japanese alcoholics","volume":"103","author":"Yukawa","year":"2012","journal-title":"Cancer Sci"},{"key":"B110","doi-asserted-by":"publisher","DOI":"10.1007\/s13402-018-0390-8","article-title":"Interplay between base excision repair protein XRCC1 and ALDH2 predicts overall survival in lung and liver cancer patients","volume":"41","author":"Chen","year":"2018","journal-title":"Cell Oncol Dordr"},{"key":"B111","doi-asserted-by":"publisher","DOI":"10.1038\/s41417-023-00708-w","article-title":"SPRTN is involved in hepatocellular carcinoma development through the ER stress response","volume":"31","author":"Batel","year":"2024","journal-title":"Cancer Gene Ther"},{"key":"B112","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkx107","article-title":"Spartan deficiency causes accumulation of Topoisomerase 1 cleavage complexes and tumorigenesis","volume":"45","author":"Maskey","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"B113","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-15-2616","article-title":"Endoplasmic reticulum stress protein GRP78 modulates lipid metabolism to control drug sensitivity and antitumor immunity in breast cancer","volume":"76","author":"Cook","year":"2016","journal-title":"Cancer Res"},{"key":"B114","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbrc.2005.08.072","article-title":"Lipid peroxidation: Mechanisms, inhibition, and biological effects","volume":"338","author":"Niki","year":"2005","journal-title":"Biochem Biophys Res Commun"},{"key":"B115","doi-asserted-by":"publisher","DOI":"10.1016\/j.taap.2004.01.018","article-title":"Mechanisms that regulate production of reactive oxygen species by cytochrome P450","volume":"199","author":"Zangar","year":"2004","journal-title":"Toxicol Appl Pharmacol"},{"key":"B116","doi-asserted-by":"publisher","DOI":"10.1155\/2014\/360438","article-title":"Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal","volume":"2014","author":"Ayala","year":"2014","journal-title":"Oxid Med Cell Longev"},{"key":"B117","doi-asserted-by":"publisher","first-page":"776","DOI":"10.1016\/j.chembiol.2020.11.011","article-title":"Lipid-derived electrophiles mediate the effects of chemotherapeutic topoisomerase I poisons","volume":"28","author":"Flor","year":"2021","journal-title":"Cell Chem Biol"},{"key":"B118","doi-asserted-by":"publisher","first-page":"e104","DOI":"10.1093\/nar\/gkt171","article-title":"A rapid and sensitive assay for DNA\u2013protein covalent complexes in living cells","volume":"41","author":"Kiianitsa","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"B119","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41596-024-01004-z","article-title":"Electro-elution-based purification of covalent DNA\u2013protein cross-links","author":"Weickert","year":"2024","journal-title":"Nat Protoc"}],"container-title":["Frontiers in Oncology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fonc.2024.1478373\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,12]],"date-time":"2024-09-12T02:45:33Z","timestamp":1726109133000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fonc.2024.1478373\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,12]]},"references-count":119,"alternative-id":["10.3389\/fonc.2024.1478373"],"URL":"https:\/\/doi.org\/10.3389\/fonc.2024.1478373","relation":{},"ISSN":["2234-943X"],"issn-type":[{"value":"2234-943X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,12]]},"article-number":"1478373"}}