200
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Homologous recombination contributes to the repair of acetaldehyde-induced DNA damage

, , , , , , , , , & show all
Pages 369-384 | Received 04 Nov 2023, Accepted 12 Mar 2024, Published online: 03 Apr 2024

References

  • Rehm J, Shield KD, Weiderpass E. Alcohol consumption. A leading risk factor for cancer. Chem Biol Interact. 2020;331:331. doi: 10.1016/j.cbi.2020.109280
  • IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Alcohol consumption and ethyl carbamate. IARC Monogr Eval Carcinog Risks Hum. 2010;96:3.
  • Aicr, WCRF. Diet, nutrition, physical activity and cancer: a global perspective a summary of the third expert report. [cited 2023 Jun 18]; Available from: http://gco.iarc.fr/today
  • Soerjomataram I, Shield K, Marant-Micallef C, et al. Cancers related to lifestyle and environmental factors in France in 2015. Eur J Cancer. 2018;105:103–113. doi: 10.1016/j.ejca.2018.09.009
  • Larson HN, Zhou J, Chen Z, et al. Structural and functional consequences of coenzyme binding to the inactive Asian variant of mitochondrial aldehyde dehydrogenase: roles of residues 475 and 487. J Biol Chem. 2007;282(17):12940–12950. doi: 10.1074/jbc.M607959200
  • Steinmetz CG, Xie P, Weiner H, et al. Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion. Structure. 1997;5(5):701–711. doi: 10.1016/S0969-2126(97)00224-4
  • Ahmed Laskar A, Younus H. Aldehyde toxicity and metabolism: the role of aldehyde dehydrogenases in detoxification, drug resistance and carcinogenesis. Drug Metab Rev. 2019;51(1):42–64. doi: 10.1080/03602532.2018.1555587
  • Ridpath JR, Nakamura A, Tano K, et al. Cells deficient in the FANC/BRCA pathway are hypersensitive to plasma levels of formaldehyde. Cancer Res. 2007;67(23):11117–11122. doi: 10.1158/0008-5472.CAN-07-3028
  • Rosado IV, Langevin F, Crossan GP, et al. Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat Struct Mol Biol. 2011;18(12):1432–1434. doi: 10.1038/nsmb.2173
  • Garaycoechea JI, Crossan GP, Langevin F, et al. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature. 2012;489(7417):571–575. doi: 10.1038/nature11368
  • Pouliot JJ, Yao KC, Robertson CA, et al. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science (1979). 1999;286(5439):552–555. doi: 10.1126/science.286.5439.552
  • Ledesma FC, El Khamisy SF, Zuma MC, et al. A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature. 2009;461(7264):674–678. doi: 10.1038/nature08444
  • Interthal H, Chen HJ, Champoux JJ. Human Tdp1 cleaves a broad spectrum of substrates, including phosphoamide linkages. J Biol Chem. 2005;280(43):36518–36528. doi: 10.1074/jbc.M508898200
  • Hoa NN, Shimizu T, Zhou ZW, et al. Mre11 is essential for the removal of lethal topoisomerase 2 covalent cleavage complexes. Mol Cell. 2016;64(3):580–592. doi: 10.1016/j.molcel.2016.10.011
  • Deshpande RA, Lee JH, Arora S, et al. Nbs1 converts the human Mre11/Rad50 nuclease complex into an endo/exonuclease machine specific for protein-DNA adducts. Mol Cell. 2016;64(3):593–606. doi: 10.1016/j.molcel.2016.10.010
  • Hartsuiker E, Neale MJ, Carr AM. Distinct requirements for the Rad32Mre11 nuclease and Ctp1CtIP in the removal of covalently bound topoisomerase I and II from DNA. Mol Cell. 2009;33(1):117–123. doi: 10.1016/j.molcel.2008.11.021
  • Dingler FA, Wang M, Mu A, et al. Two aldehyde clearance systems are essential to prevent lethal formaldehyde accumulation in mice and humans. Mol Cell. 2020;80(6):996–1012.e9. doi: 10.1016/j.molcel.2020.10.012
  • Tomita A, Sasanuma H, Owa T, et al. Inducing multiple nicks promotes interhomolog homologous recombination to correct heterozygous mutations in somatic cells. Nat Commun. 2023;14(1):14. doi: 10.1038/s41467-023-41048-5
  • Chen S, Zhou Y, Chen Y, et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–i890. doi: 10.1093/bioinformatics/bty560
  • Dobin A, Gingeras TR. Mapping RNA-seq reads with STAR. Curr Protoc Bioinformatics. 2015;51(1):11.14.1–.11.14.19. doi: 10.1002/0471250953.bi1114s51
  • Layer RM, Skadron K, Robins G, et al. Binary interval search: a scalable algorithm for counting interval intersections. Bioinformatics. 2013;29(1):1–7. doi: 10.1093/bioinformatics/bts652
  • Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 2011;12(1):12. doi: 10.1186/1471-2105-12-323
  • Karasawa S, Araki T, Yamamoto-Hino M, et al. A green-emitting fluorescent protein from galaxeidae coral and its monomeric version for use in fluorescent labeling. J Biol Chem. 2003;278(36):34167–34171. doi: 10.1074/jbc.M304063200
  • Wilson TE, Grawunder U, Lieber MR. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature. 1997;388(6641):495–498. doi: 10.1038/41365
  • Essers J, Hendriks RW, Swagemakers SMA, et al. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell. 1997;89(2):195–204. doi: 10.1016/S0092-8674(00)80199-3
  • Garaycoechea JI, Crossan GP, Langevin F, et al. Alcohol and endogenous aldehydes damage chromosomes and mutate stem cells. Nature. 2018;553(7687):171–177. doi: 10.1038/nature25154
  • Sonohara Y, Yamamoto J, Tohashi K, et al. Acetaldehyde forms covalent GG intrastrand crosslinks in DNA. Sci Rep. 2019;9(1):1–8. doi: 10.1038/s41598-018-37239-6
  • Keka IS, Mohiuddin, Maede Y, et al. Smarcal1 promotes double-strand-break repair by nonhomologous end-joining. Nucleic Acids Res. 2015;43(13):6359–6372. doi: 10.1093/nar/gkv621
  • Rahman MM, Mohiuddin M, Keka IS, et al. Genetic evidence for the involvement of mismatch repair proteins, PMS2 and MLH3, in a late step of homologous recombination. J Biol Chem. 2020;295(51):17460–17475. doi: 10.1074/jbc.RA120.013521
  • Hoa NN, Akagawa R, Yamasaki T, et al. Relative contribution of four nucleases, CtIP, Dna2, Exo1 and Mre11, to the initial step of DNA double-strand break repair by homologous recombination in both the chicken DT40 and human TK6 cell lines. Genes Cells. 2015;20(12):1059–1076. doi: 10.1111/gtc.12310
  • Demin AA, Hirota K, Tsuda M, et al. XRCC1 prevents toxic PARP1 trapping during DNA base excision repair. Mol Cell. 2021;81(14):3018–3030.e5. doi: 10.1016/j.molcel.2021.05.009
  • Sasanuma H, Tsuda M, Morimoto S, et al. BRCA1 ensures genome integrity by eliminating estrogen-induced pathological topoisomerase II–DNA complexes. Proc Natl Acad Sci USA. 2018;115(45):E10642–E10651. doi: 10.1073/pnas.1803177115
  • Mohiuddin M, Evans TJ, Rahman MM, et al. Sumoylation of PCNA by PIAS1 and PIAS4 promotes template switch in the chicken and human B cell lines. Proc Natl Acad Sci USA. 2018;115(50):12793–12798. doi: 10.1073/pnas.1716349115
  • Tsuda M, Terada K, Ooka M, et al. The dominant role of proofreading exonuclease activity of replicative polymerase ε in cellular tolerance to cytarabine (ara-C). Oncotarget. 2017;8(20):33457–33474. doi: 10.18632/oncotarget.16508
  • Peake JD, Horne KI, Noguchi C, et al. The p53 DNA damage response and fanconi anemia DNA repair pathway protect against acetaldehyde-induced replication stress in esophageal keratinocytes. Cell Cycle. 2023;22(18):2088–2096. doi: 10.1080/15384101.2023.2261740
  • Peake JD, Noguchi C, Lin B, et al. FANCD2 limits acetaldehyde-induced genomic instability during DNA replication in esophageal keratinocytes. Mol Oncol. 2021;15(11):3109–3124. doi: 10.1002/1878-0261.13072
  • Lee SL, Wang MF, Lee AI, et al. The metabolic role of human ADH3 functioning as ethanol dehydrogenase. FEBS Lett. 2003;544(1–3):143–147. doi: 10.1016/S0014-5793(03)00492-7
  • Haseba T, Duester G, Shimizu A, et al. In vivo contribution of class III alcohol dehydrogenase (ADH3) to alcohol metabolism through activation by cytoplasmic solution hydrophobicity. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2006;1762(3):276–283. doi: 10.1016/j.bbadis.2005.11.008
  • Koppaka V, Thompson DC, Chen Y, et al. Aldehyde dehydrogenase inhibitors: a comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev. 2012;64(3):520–539. doi: 10.1124/pr.111.005538
  • Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461(7267):1071–1078. doi: 10.1038/nature08467
  • Smiraldo PG, Gruver AM, Osborn JC, et al. Extensive chromosomal instability in Rad51d-deficient mouse cells. Cancer Res. 2005;65(6):2089–2096. doi: 10.1158/0008-5472.CAN-04-2079
  • Polato F, Callen E, Wong N, et al. CtIP-mediated resection is essential for viability and can operate independently of BRCA1. J Exp Med. 2014;211(6):1027–1036. doi: 10.1084/jem.20131939
  • Sonoda E, Sasaki MS, Morrison C, et al. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol Cell Biol. 2023;19(7):5166–5169. doi: 10.1128/MCB.19.7.5166
  • Chaganti RSK, Schonberg S, German J A manyfold increase in sister chromatid exchanges in Bloom’s syndrome lymphocytes. Proceedings of the National Academy of Sciences. 1974;71:4508–4512. doi: 10.1073/pnas.71.11.4508
  • Sun Y, Jenkins LMM, Su YP, et al. A conserved SUMO pathway repairs topoisomerase DNA-protein cross-links by engaging ubiquitin-mediated proteasomal degradation. Sci Adv. 2020;6(46):6. doi: 10.1126/sciadv.aba6290
  • Reinking HK, Hofmann K, Stingele J. Function and evolution of the DNA-protein crosslink proteases Wss1 and SPRTN. DNA Repair. 2020;88:88. doi: 10.1016/j.dnarep.2020.102822
  • Nakano T, Moriwaki T, Tsuda M, et al. SPRTN and TDP1/TDP2 independently suppress 5-aza-2′-deoxycytidine-induced genomic instability in human TK6 cell line. Chem Res Toxicol. 2022;35(11):2059–2067. doi: 10.1021/acs.chemrestox.2c00213
  • Stingele J, Bellelli R, Boulton SJ. Mechanisms of DNA–protein crosslink repair. Nat Rev Mol Cell Biol. 2017;18(9):563–573. doi: 10.1038/nrm.2017.56
  • Vaitsiankova A, Burdova K, Sobol M, et al. PARP inhibition impedes the maturation of nascent DNA strands during DNA replication. Nat Struct Mol Biol. 2022;29(4):329–338. doi: 10.1038/s41594-022-00747-1
  • Fielden J, Ruggiano A, Popović M, et al. DNA protein crosslink proteolysis repair: from yeast to premature ageing and cancer in humans. DNA Repair. 2018;71:198–204. doi: 10.1016/j.dnarep.2018.08.025
  • Mizoi Y, Yamamoto K, Ueno Y, et al. Involvement of genetic polymorphism of alcohol and aldehyde dehydrogenases in individual variation of alcohol metabolism. Alcohol Alcohol. 1994;29(6):707–710.
  • Lachenmeier DW, Monakhova YB. Short-term salivary acetaldehyde increase due to direct exposure to alcoholic beverages as an additional cancer risk factor beyond ethanol metabolism. J Exp Clin Cancer Res. 2011;30(1):30. doi: 10.1186/1756-9966-30-3
  • Yokoyama A, Tsutsumi E, Imazeki H, et al. Salivary acetaldehyde concentration according to alcoholic beverage consumed and aldehyde dehydrogenase-2 genotype. Alcohol Clin Exp Res. 2008;32(9):1607–1614. doi: 10.1111/j.1530-0277.2008.00739.x
  • Wang M, Dingler FA, Patel KJ. Genotoxic aldehydes in the hematopoietic system. Blood. 2022;139(14):2119–2129. doi: 10.1182/blood.2019004316

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.