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Research Article

FANCD2-Associated Nuclease 1 Partially Compensates for the Lack of Exonuclease 1 in Mismatch Repair

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Article: e00303-21 | Received 23 Jun 2021, Accepted 28 Jun 2021, Published online: 03 Mar 2023

REFERENCES

  • Peltomaki P. 2003. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21:1174–1179. https://doi.org/10.1200/JCO.2003.04.060.
  • Strand M, Prolla TA, Liskay RM, Petes TD. 1993. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365:274–276. https://doi.org/10.1038/365274a0.
  • Heale SM, Petes TD. 1995. The stabilization of repetitive tracts of DNA by variant repeats requires a functional DNA mismatch repair system. Cell 83:539–545. https://doi.org/10.1016/0092-8674(95)90093-4.
  • Iaccarino I, Palombo F, Drummond J, Totty NF, Hsuan JJ, Modrich P, Jiricny J. 1996. MSH6, a Saccharomyces cerevisiae protein that binds to mismatches as a heterodimer with MSH2. Curr Biol 6:484–486. https://doi.org/10.1016/S0960-9822(02)00516-X.
  • Palombo F, Gallinari P, Iaccarino I, Lettieri T, Hughes M, D'Arrigo A, Truong O, Hsuan JJ, Jiricny J. 1995. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science 268:1912–1914. https://doi.org/10.1126/science.7604265.
  • Drummond JT, Li GM, Longley MJ, Modrich P. 1995. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268:1909–1912. https://doi.org/10.1126/science.7604264.
  • Palombo F, Iaccarino I, Nakajima E, Ikejima M, Shimada T, Jiricny J. 1996. hMutSbeta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr Biol 6:1181–1184. https://doi.org/10.1016/S0960-9822(02)70685-4.
  • Szankasi P, Smith GR. 1995. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267:1166–1169. https://doi.org/10.1126/science.7855597.
  • Tishkoff DX, Boerger AL, Bertrand P, Filosi N, Gaida GM, Kane MF, Kolodner RD. 1997. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A 94:7487–7492. https://doi.org/10.1073/pnas.94.14.7487.
  • Wei K, Clark AB, Wong E, Kane MF, Mazur DJ, Parris T, Kolas NK, Russell R, Hou H Jr, Kneitz B, Yang G, Kunkel TA, Kolodner RD, Cohen PE, Edelmann W. 2003. Inactivation of exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev 17:603–614. https://doi.org/10.1101/gad.1060603.
  • Schaetzlein S, Kodandaramireddy NR, Ju Z, Lechel A, Stepczynska A, Lilli DR, Clark AB, Rudolph C, Kuhnel F, Wei K, Schlegelberger B, Schirmacher P, Kunkel TA, Greenberg RA, Edelmann W, Rudolph KL. 2007. Exonuclease-1 deletion impairs DNA damage signaling and prolongs lifespan of telomere-dysfunctional mice. Cell 130:863–877. https://doi.org/10.1016/j.cell.2007.08.029.
  • Alam NA, Gorman P, Jaeger EE, Kelsell D, Leigh IM, Ratnavel R, Murdoch ME, Houlston RS, Aaltonen LA, Roylance RR, Tomlinson IP. 2003. Germline deletions of EXO1 do not cause colorectal tumors and lesions which are null for EXO1 do not have microsatellite instability. Cancer Genet Cytogenet 147:121–127. https://doi.org/10.1016/S0165-4608(03)00196-1.
  • Tran PT, Erdeniz N, Symington LS, Liskay RM. 2004. EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3:1549–1559. https://doi.org/10.1016/j.dnarep.2004.05.015.
  • Keijzers G, Liu D, Rasmussen LJ. 2016. Exonuclease 1 and its versatile roles in DNA repair. Crit Rev Biochem Mol Biol 51:440–451. https://doi.org/10.1080/10409238.2016.1215407.
  • Genschel J, Bazemore LR, Modrich P. 2002. Human exonuclease I is required for 5′ and 3′ mismatch repair. J Biol Chem 277:13302–13311. https://doi.org/10.1074/jbc.M111854200.
  • Guan J, Lu C, Jin Q, Lu H, Chen X, Tian L, Zhang Y, Ortega J, Zhang J, Siteni S, Chen M, Gu L, Shay JW, Davis AJ, Chen ZJ, Fu YX, Li GM. 2021. MLH1 deficiency-triggered DNA hyperexcision by exonuclease 1 activates the cGAS-STING pathway. Cancer Cell 39:109–121.e105. https://doi.org/10.1016/j.ccell.2020.11.004.
  • Jiricny J. 2006. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7:335–346. https://doi.org/10.1038/nrm1907.
  • Iyer RR, Pluciennik A, Burdett V, Modrich PL. 2006. DNA mismatch repair: functions and mechanisms. Chem Rev 106:302–323. https://doi.org/10.1021/cr0404794.
  • Holmes J, Clark S, Modrich P. 1990. Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines. Proc Natl Acad Sci U S A 87:5837–5841. https://doi.org/10.1073/pnas.87.15.5837.
  • Umar A, Boyer JC, Thomas DC, Nguyen DC, Risinger JI, Boyd J, Ionov Y, Perucho M, Kunkel TA. 1994. Defective mismatch repair in extracts of colorectal and endometrial cancer cell lines exhibiting microsatellite instability. J Biol Chem 269:14367–14370. https://doi.org/10.1016/S0021-9258(17)36630-9.
  • Dzantiev L, Constantin N, Genschel J, Iyer RR, Burgers PM, Modrich P. 2004. A defined human system that supports bidirectional mismatch-provoked excision. Mol Cell 15:31–41. https://doi.org/10.1016/j.molcel.2004.06.016.
  • Constantin N, Dzantiev L, Kadyrov FA, Modrich P. 2005. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J Biol Chem 280:39752–39761. https://doi.org/10.1074/jbc.M509701200.
  • Cannavo E, Gerrits B, Marra G, Schlapbach R, Jiricny J. 2007. Characterization of the interactome of the human MutL homologues MLH1, PMS1, and PMS2. J Biol Chem 282:2976–2986. https://doi.org/10.1074/jbc.M609989200.
  • Yoshikiyo K, Kratz K, Hirota K, Nishihara K, Takata M, Kurumizaka H, Horimoto S, Takeda S, Jiricny J. 2010. KIAA1018/FAN1 nuclease protects cells against genomic instability induced by interstrand cross-linking agents. Proc Natl Acad Sci U S A 107:21553–21557. https://doi.org/10.1073/pnas.1011081107.
  • Ceccaldi R, Sarangi P, D’Andrea AD. 2016. The Fanconi anaemia pathway: new players and new functions. Nat Rev Mol Cell Biol 17:337–349. https://doi.org/10.1038/nrm.2016.48.
  • Kratz K, Schopf B, Kaden S, Sendoel A, Eberhard R, Lademann C, Cannavo E, Sartori AA, Hengartner MO, Jiricny J. 2010. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142:77–88. https://doi.org/10.1016/j.cell.2010.06.022.
  • Liu T, Ghosal G, Yuan J, Chen J, Huang J. 2010. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329:693–696. https://doi.org/10.1126/science.1192656.
  • MacKay C, Declais AC, Lundin C, Agostinho A, Deans AJ, MacArtney TJ, Hofmann K, Gartner A, West SC, Helleday T, Lilley DM, Rouse J. 2010. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142:65–76. https://doi.org/10.1016/j.cell.2010.06.021.
  • Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, Clark AB, Kunkel TA, Harper JW, Colaiacovo MP, Elledge SJ. 2010. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39:36–47. https://doi.org/10.1016/j.molcel.2010.06.023.
  • Pizzolato J, Mukherjee S, Scharer OD, Jiricny J. 2015. FANCD2-associated nuclease 1, but not exonuclease 1 or flap endonuclease 1, is able to unhook DNA interstrand cross-links in vitro. J Biol Chem 290:22602–22611. https://doi.org/10.1074/jbc.M115.663666.
  • Nielsen FC, Jager AC, Lutzen A, Bundgaard JR, Rasmussen LJ. 2004. Characterization of human exonuclease 1 in complex with mismatch repair proteins, subcellular localization and association with PCNA. Oncogene 23:1457–1468. https://doi.org/10.1038/sj.onc.1207265.
  • Tran PT, Simon JA, Liskay RM. 2001. Interactions of Exo1p with components of MutLalpha in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 98:9760–9765. https://doi.org/10.1073/pnas.161175998.
  • Schmutte C, Sadoff MM, Shim KS, Acharya S, Fishel R. 2001. The interaction of DNA mismatch repair proteins with human exonuclease I. J Biol Chem 276:33011–33018. https://doi.org/10.1074/jbc.M102670200.
  • Hoa NN, Akagawa R, Yamasaki T, Hirota K, Sasa K, Natsume T, Kobayashi J, Sakuma T, Yamamoto T, Komatsu K, Kanemaki MT, Pommier Y, Takeda S, Sasanuma H. 2015. 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 20:1059–1076. https://doi.org/10.1111/gtc.12310.
  • Bregenhorn S, Jiricny J. 2014. Biochemical characterization of a cancer-associated E109K missense variant of human exonuclease 1. Nucleic Acids Res 42:7096–7103. https://doi.org/10.1093/nar/gku419.
  • Baerenfaller K, Fischer F, Jiricny J. 2006. Characterization of the “mismatch repairosome” and its role in the processing of modified nucleosides in vitro. Methods Enzymol 408:285–303. https://doi.org/10.1016/S0076-6879(06)08018-9.
  • Thomas DC, Roberts JD, Kunkel TA. 1991. Heteroduplex repair in extracts of human HeLa cells. J Biol Chem 266:3744–3751. https://doi.org/10.1016/S0021-9258(19)67858-0.
  • Kadyrov FA, Genschel J, Fang Y, Penland E, Edelmann W, Modrich P. 2009. A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair. Proc Natl Acad Sci U S A 106:8495–8500. https://doi.org/10.1073/pnas.0903654106.
  • Kadyrov FA, Dzantiev L, Constantin N, Modrich P. 2006. Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126:297–308. https://doi.org/10.1016/j.cell.2006.05.039.
  • Rahman MM, Mohiuddin M, Shamima Keka I, Yamada K, Tsuda M, Sasanuma H, Andreani J, Guerois R, Borde V, Charbonnier JB, Takeda S. 2020. Genetic evidence for the involvement of mismatch repair proteins, PMS2 and MLH3, in a late step of homologous recombination. J Biol Chem 295:17460–17475. https://doi.org/10.1074/jbc.RA120.013521.
  • Zhou B, Huang C, Yang J, Lu J, Dong Q, Sun LZ. 2009. Preparation of heteroduplex enhanced green fluorescent protein plasmid for in vivo mismatch repair activity assay. Anal Biochem 388:167–169. https://doi.org/10.1016/j.ab.2009.02.020.
  • Duckett DR, Drummond JT, Murchie AI, Reardon JT, Sancar A, Lilley DM, Modrich P. 1996. Human MutSalpha recognizes damaged DNA base pairs containing O6-methylguanine, O4-methylthymine, or the cisplatin-d(GpG) adduct. Proc Natl Acad Sci U S A 93:6443–6447. https://doi.org/10.1073/pnas.93.13.6443.
  • Olivera Harris M, Kallenberger L, Artola Boran M, Enoiu M, Costanzo V, Jiricny J. 2015. Mismatch repair-dependent metabolism of O6-methylguanine-containing DNA in Xenopus laevis egg extracts. DNA Repair (Amst) 28:1–7. https://doi.org/10.1016/j.dnarep.2015.01.014.
  • Karran P, Macpherson P, Ceccotti S, Dogliotti E, Griffin S, Bignami M. 1993. O6-methylguanine residues elicit DNA repair synthesis by human cell extracts. J Biol Chem 268:15878–15886. https://doi.org/10.1016/S0021-9258(18)82335-3.
  • Massey A, Xu YZ, Karran P. 2002. Ambiguous coding is required for the lethal interaction between methylated DNA bases and DNA mismatch repair. DNA Repair (Amst), 1:275–286. https://doi.org/10.1016/S1568-7864(02)00004-6.
  • Mojas N, Lopes M, Jiricny J. 2007. Mismatch repair-dependent processing of methylation damage gives rise to persistent single-stranded gaps in newly replicated DNA. Genes Dev 21:3342–3355. https://doi.org/10.1101/gad.455407.
  • Stojic L, Cejka P, Jiricny J. 2005. High doses of SN1 type methylating agents activate DNA damage signaling cascades that are largely independent of mismatch repair. Cell Cycle 4:473–477. https://doi.org/10.4161/cc.4.3.1528.
  • Karran P. 2001. Mechanisms of tolerance to DNA damaging therapeutic drugs. Carcinogenesis 22:1931–1937. https://doi.org/10.1093/carcin/22.12.1931.
  • Yan T, Berry SE, Desai AB, Kinsella TJ. 2003. DNA mismatch repair (MMR) mediates 6-thioguanine genotoxicity by introducing single-strand breaks to signal a G2-M arrest in MMR-proficient RKO cells. Clin Cancer Res 9:2327–2334.
  • Klapacz J, Meira LB, Luchetti DG, Calvo JA, Bronson RT, Edelmann W, Samson LD. 2009. O6-methylguanine-induced cell death involves exonuclease 1 as well as DNA mismatch recognition in vivo. Proc Natl Acad Sci U S A 106:576–581. https://doi.org/10.1073/pnas.0811991106.
  • Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS. 1997. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17:2764–2773. https://doi.org/10.1128/MCB.17.5.2764.
  • Zou X, Owusu M, Harris R, Jackson SP, Loizou JI, Nik-Zainal S. 2018. Validating the concept of mutational signatures with isogenic cell models. Nat Commun 9:1744. https://doi.org/10.1038/s41467-018-04052-8.
  • Engelward BP, Boosalis MS, Chen BJ, Deng Z, Siciliano MJ, Samson LD. 1993. Cloning and characterization of a mouse 3-methyladenine/7-methyl-guanine/3-methylguanine DNA glycosylase cDNA whose gene maps to chromosome 11. Carcinogenesis 14:175–181. https://doi.org/10.1093/carcin/14.2.175.
  • Koh G, Zou X, Nik-Zainal S. 2020. Mutational signatures: experimental design and analytical framework. Genome Biol 21:37. https://doi.org/10.1186/s13059-020-1951-5.
  • Banda DM, Nunez NN, Burnside MA, Bradshaw KM, David SS. 2017. Repair of 8-oxoG:A mismatches by the MUTYH glycosylase: mechanism, metals and medicine. Free Radic Biol Med 107:202–215. https://doi.org/10.1016/j.freeradbiomed.2017.01.008.
  • Zou X, Koh GCC, Nanda AS, Degasperi A, Urgo K, Roumeliotis TI, Agu CA, Side L, Brice G, Perez-Alonso V, Rueda D, Badja C, Young J, Gomez C, Bushell W, Harris R, Choudhary JS, Jiricny J, Skarnes WC, Nik-Zainal S. 2020. Dissecting mutational mechanisms underpinning signatures caused by replication errors and endogenous DNA damage. bioRxiv https://doi.org/10.1101/2020.08.04.234245.
  • Desai A, Gerson S. 2014. Exo1 independent DNA mismatch repair involves multiple compensatory nucleases. DNA Repair (Amst) 21:55–64. https://doi.org/10.1016/j.dnarep.2014.06.005.
  • Lahue RS, Modrich P. 1988. Methyl-directed DNA mismatch repair in Escherichia coli. Mutat Res 198:37–43. https://doi.org/10.1016/0027-5107(88)90037-1.
  • Giannini G, Ristori E, Cerignoli F, Rinaldi C, Zani M, Viel A, Ottini L, Crescenzi M, Martinotti S, Bignami M, Frati L, Screpanti I, Gulino A. 2002. Human MRE11 is inactivated in mismatch repair-deficient cancers. EMBO Rep 3:248–254. https://doi.org/10.1093/embo-reports/kvf044.
  • Cejka P, Stojic L, Mojas N, Russell AM, Heinimann K, Cannavo E, di Pietro M, Marra G, Jiricny J. 2003. Methylation-induced G(2)/M arrest requires a full complement of the mismatch repair protein hMLH1. EMBO J 22:2245–2254. https://doi.org/10.1093/emboj/cdg216.
  • Genschel J, Modrich P. 2003. Mechanism of 5′-directed excision in human mismatch repair. Mol Cell 12:1077–1086. https://doi.org/10.1016/S1097-2765(03)00428-3.
  • Fontebasso Y, Etheridge TJ, Oliver AW, Murray JM, Carr AM. 2013. The conserved Fanconi anemia nuclease Fan1 and the SUMO E3 ligase Pli1 act in two novel Pso2-independent pathways of DNA interstrand crosslink repair in yeast. DNA Repair (Amst) 12:1011–1023. https://doi.org/10.1016/j.dnarep.2013.10.003.
  • Genetic Modifiers of Huntington's Disease Consortium. 2019. CAG repeat not polyglutamine length determines timing of Huntington’s disease onset. Cell 178:887–900. https://doi.org/10.1016/j.cell.2019.06.036.
  • Zhao XN, Usdin K. 2018. FAN1 protects against repeat expansions in a Fragile X mouse model. DNA Repair (Amst) 69:1–5. https://doi.org/10.1016/j.dnarep.2018.07.001.
  • Lai Y, Budworth H, Beaver JM, Chan NL, Zhang Z, McMurray CT, Liu Y. 2016. Crosstalk between MSH2-MSH3 and polbeta promotes trinucleotide repeat expansion during base excision repair. Nat Commun 7:12465. https://doi.org/10.1038/ncomms12465.
  • Loupe JM, Pinto RM, Kim KH, Gillis T, Mysore JS, Andrew MA, Kovalenko M, Murtha R, Seong I, Gusella JF, Kwak S, Howland D, Lee R, Lee JM, Wheeler VC, MacDonald ME. 2020. Promotion of somatic CAG repeat expansion by Fan1 knock-out in Huntington’s disease knock-in mice is blocked by Mlh1 knock-out. Hum Mol Genet 29:3044–3053. https://doi.org/10.1093/hmg/ddaa196.
  • Honma M, Izumi M, Sakuraba M, Tadokoro S, Sakamoto H, Wang W, Yatagai F, Hayashi M. 2003. Deletion, rearrangement, and gene conversion; genetic consequences of chromosomal double-strand breaks in human cells. Environ Mol Mutagen 42:288–298. https://doi.org/10.1002/em.10201.
  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823. https://doi.org/10.1126/science.1231143.
  • Mazouzi A, Battistini F, Moser SC, Ferreira da Silva J, Wiedner M, Owusu M, Lardeau CH, Ringler A, Weil B, Neesen J, Orozco M, Kubicek S, Loizou JI. 2017. Repair of UV-induced DNA damage independent of nucleotide excision repair is masked by MUTYH. Mol Cell 68:797–807.e797. https://doi.org/10.1016/j.molcel.2017.10.021.
  • Okada T, Sonoda E, Yamashita YM, Koyoshi S, Tateishi S, Yamaizumi M, Takata M, Ogawa O, Takeda S. 2002. Involvement of vertebrate polkappa in Rad18-independent postreplication repair of UV damage. J Biol Chem 277:48690–48695. https://doi.org/10.1074/jbc.M207957200.

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