TOP3A coupling with replication forks and repair of TOP3A cleavage complexes

References

• Pommier Y, Nussenzweig A, Takeda S, et al. Human topoisomerases and their roles in genome stability and organization. Nat Rev Mol Cell Biol. 2022;23(6):407–427. doi: 10.1038/s41580-022-00452-3
   PubMed Web of Science ®Google Scholar
• Bizard AH, Hickson ID. The many lives of type IA topoisomerases. J Biol Chem. 2020;295(20):7138–7153. doi: 10.1074/jbc.REV120.008286
   PubMed Web of Science ®Google Scholar
• Martin CA, Sarlos K, Logan CV, et al. Mutations in TOP3A Cause a Bloom Syndrome-like Disorder. Am J Hum Genet. 2018;103(2):221–231. doi: 10.1016/j.ajhg.2018.07.001
   PubMed Web of Science ®Google Scholar
• Nicholls TJ, Nadalutti CA, Motori E, et al. Topoisomerase 3α is required for decatenation and segregation of human mtDNA. Mol Cell. 2018;69(1):9–23 e6. doi: 10.1016/j.molcel.2017.11.033
   PubMed Web of Science ®Google Scholar
• Jiang W, Jia N, Guo C, et al. Predominant cellular mitochondrial dysfunction in the TOP3A gene-caused bloom syndrome-like disorder. Biochim Biophys Acta Mol Basis Dis. 2021;1867(6):166106. doi: 10.1016/j.bbadis.2021.166106
   PubMed Web of Science ®Google Scholar
• Primiano G, Torraco A, Verrigni D, et al. Novel TOP3A variant associated with mitochondrial disease: expanding the clinical spectrum of topoisomerase III alpha-related diseases. Neurol Genet. 2022;8(4):e200007. doi: 10.1212/NXG.0000000000200007
   PubMed Web of Science ®Google Scholar
• Erdinc D, Rodriguez-Luis A, Fassad MR, et al. Pathological variants in TOP3A cause distinct disorders of mitochondrial and nuclear genome stability. EMBO Mol Med. 2023;15(5):e16775. doi: 10.15252/emmm.202216775
   PubMed Web of Science ®Google Scholar
• Llaurado A, Rovira-Moreno E, Codina-Sola M, et al. Chronic progressive external ophthalmoplegia plus syndrome due to homozygous missense variant in TOP3A gene. Clin Genet. 2023;103(4):492–494. doi: 10.1111/cge.14287
   PubMed Web of Science ®Google Scholar
• Aaltonen LA, Abascal F, Abeshouse A. Consortium ITP-CAoWG. Pan-cancer analysis of whole genomes. Nature. 2020;578(7793):82–93. doi: 10.1038/s41586-020-1969-6
   PubMed Web of Science ®Google Scholar
• Wang Y, Lyu YL, Wang JC. Dual localization of human DNA topoisomerase IIIα to mitochondria and nucleus. Proc Natl Acad Sci U S A. 2002;99(19):12114–12119. doi: 10.1073/pnas.192449499
   PubMed Web of Science ®Google Scholar
• Wu J, Feng L, Hsieh TS. Drosophila topo IIIα is required for the maintenance of mitochondrial genome and male germ-line stem cells. Proc Natl Acad Sci U S A. 2010;107(14):6228–6233. doi: 10.1073/pnas.1001855107
   PubMed Web of Science ®Google Scholar
• Lima CD, Wang JC, Mondragon A. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature. 1994;367(6459):138–146. doi: 10.1038/367138a0
   PubMed Web of Science ®Google Scholar
• Saha LK, Saha S, Yang X, et al. Replication-associated formation and repair of human topoisomerase IIIα cleavage complexes. Nat Commun. 2023;14(1):1925. doi: 10.1038/s41467-023-37498-6
   PubMed Web of Science ®Google Scholar
• Wu L, Hickson ID. The bloom’s syndrome helicase suppresses crossing over during homologous recombination. Nature. 2003;426(6968):870–874. doi: 10.1038/nature02253
   PubMed Web of Science ®Google Scholar
• Wang W, Seki M, Narita Y, et al. Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J. 2000;19(13):3428–3435. doi: 10.1093/emboj/19.13.3428
   PubMed Web of Science ®Google Scholar
• Shorrocks AK, Jones SE, Tsukada K, et al. The bloom syndrome complex senses RPA-coated single-stranded DNA to restart stalled replication forks. Nat Commun. 2021;12(1):585. doi: 10.1038/s41467-020-20818-5
   PubMed Web of Science ®Google Scholar
• Hoadley KA, Xue Y, Ling C, et al. Defining the molecular interface that connects the fanconi anemia protein FANCM to the bloom syndrome dissolvasome. Proc Natl Acad Sci U S A. 2012;109(12):4437–4442. doi: 10.1073/pnas.1117279109
   PubMed Web of Science ®Google Scholar
• Bizard AH, Allemand JF, Hassenkam T, et al. PICH and TOP3A cooperate to induce positive DNA supercoiling. Nat Struct Mol Biol. 2019;26(4):267–274. doi: 10.1038/s41594-019-0201-6
   PubMed Web of Science ®Google Scholar
• Menger KE, Chapman J, Diaz-Maldonado H, et al. Two type I topoisomerases maintain DNA topology in human mitochondria. Nucleic Acids Res. 2022;50(19):11154–11174. doi: 10.1093/nar/gkac857
   PubMed Web of Science ®Google Scholar
• Hangas A, Kekalainen NJ, Potter A, et al. Top3α is the replicative topoisomerase in mitochondrial DNA replication. Nucleic Acids Res. 2022;50(15):8733–8748. doi: 10.1093/nar/gkac660
   PubMed Web of Science ®Google Scholar
• Hand R, German J. A retarded rate of DNA chain growth in bloom’s syndrome. Proc Natl Acad Sci U S A. 1975;72(2):758–762. doi: 10.1073/pnas.72.2.758
   PubMed Web of Science ®Google Scholar
• Ockey CH, Saffhill R. Delayed DNA maturation, a possible cause of the elevated sister-chromatid exchange in Bloom’s syndrome. Carcinogenesis. 1986;7(1):53–57. doi: 10.1093/carcin/7.1.53
   PubMed Web of Science ®Google Scholar
• Lonn U, Lonn S, Nylen U, et al. An abnormal profile of DNA replication intermediates in bloom’s syndrome. Cancer Res. 1990;50(11):3141–3145.
   PubMed Web of Science ®Google Scholar
• Davies SL, North PS, Hickson ID. Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat Struct Mol Biol. 2007;14(7):677–679. doi: 10.1038/nsmb1267
   PubMed Web of Science ®Google Scholar
• Rao VA, Fan AM, Meng L, et al. Phosphorylation of BLM, dissociation from topoisomerase IIIα, and colocalization with γ-H2AX after topoisomerase I-Induced replication damage. Mol Cell Biol. 2005;25(20):8925–8937. doi: 10.1128/MCB.25.20.8925-8937.2005
   PubMed Web of Science ®Google Scholar
• Davies SL, North PS, Dart A, et al. Phosphorylation of the bloom’s syndrome helicase and its role in recovery from S-phase arrest. Mol Cell Biol. 2004;24(3):1279–1291. doi: 10.1128/MCB.24.3.1279-1291.2004
   PubMed Web of Science ®Google Scholar
• Sengupta S, Linke SP, Pedeux R, et al. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J. 2003;22(5):1210–1222. doi: 10.1093/emboj/cdg114
   PubMed Web of Science ®Google Scholar
• Rao VA, Conti C, Guirouilh-Barbat J, et al. Endogenous γ-H2AX-ATM-Chk2 checkpoint activation in bloom’s syndrome helicase–deficient cells is related to DNA replication arrested forks. Mol Cancer Res. 2007;5(7):713–724. doi: 10.1158/1541-7786.MCR-07-0028
   PubMed Web of Science ®Google Scholar
• Yang J, O’Donnell L, Durocher D, et al. RMI1 promotes DNA replication fork progression and recovery from replication fork stress. Mol Cell Biol. 2012;32(15):3054–3064. doi: 10.1128/MCB.00255-12
   PubMed Web of Science ®Google Scholar
• Lee CM, Wang G, Pertsinidis A, et al. Topoisomerase III acts at the replication fork to remove precatenanes. J Bacteriol. 2019;201(7):201. doi: 10.1128/JB.00563-18
   Web of Science ®Google Scholar
• Bakx JAM, Biebricher AS, King GA, et al. Duplex DNA and BLM regulate gate opening by the human TopoIIIα-RMI1-RMI2 complex. Nat Commun. 2022;13(1):584. doi: 10.1038/s41467-022-28082-5
   PubMed Web of Science ®Google Scholar
• Hiasa H, DiGate RJ, Marians KJ. Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J Biol Chem. 1994;269(3):2093–2099. doi: 10.1016/S0021-9258(17)42140-5
   PubMed Web of Science ®Google Scholar
• Hiasa H, Marians KJ. Topoisomerase III, but not topoisomerase I, can support nascent chain elongation during theta-type DNA replication. J Biol Chem. 1994;269(51):32655–32659. doi: 10.1016/S0021-9258(18)31684-3
   PubMed Web of Science ®Google Scholar
• Nurse P, Levine C, Hassing H, et al. Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J Biol Chem. 2003;278(10):8653–8660. doi: 10.1074/jbc.M211211200
   PubMed Web of Science ®Google Scholar
• Perez-Cheeks BA, Lee C, Hayama R, et al. A role for topoisomerase III in Escherichia coli chromosome segregation. Mol Microbiol. 2012;86(4):1007–1022. doi: 10.1111/mmi.12039
   PubMed Web of Science ®Google Scholar
• DiGate RJ, Marians KJ. Identification of a potent decatenating enzyme from Escherichia coli. J Biol Chem. 1988;263(26):13366–13373. doi: 10.1016/S0021-9258(18)37713-5
   PubMed Web of Science ®Google Scholar
• Minden JS, Marians KJ. Escherichia coli topoisomerase I can segregate replicating pBR322 daughter DNA molecules in vitro. J Biol Chem. 1986;261:11906–11917.
   PubMed Web of Science ®Google Scholar
• Suski C, Marians KJ. Resolution of converging replication forks by RecQ and topoisomerase III. Mol Cell. 2008;30(6):779–789. doi: 10.1016/j.molcel.2008.04.020
   PubMed Web of Science ®Google Scholar
• Butland G, Peregrin-Alvarez JM, Li J, et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature. 2005;433(7025):531–537. doi: 10.1038/nature03239
   PubMed Web of Science ®Google Scholar
• Graham JE, Marians KJ, Kowalczykowski SC. Independent and stochastic action of DNA polymerases in the replisome. Cell. 2017;169(7):1201–13 e17. doi: 10.1016/j.cell.2017.05.041
   PubMed Web of Science ®Google Scholar
• Couch FB, Bansbach CE, Driscoll R, et al. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 2013;27(14):1610–1623. doi: 10.1101/gad.214080.113
   PubMed Web of Science ®Google Scholar
• Menger KE, Rodriguez-Luis A, Chapman J, et al. Controlling the topology of mammalian mitochondrial DNA. Open Biol. 2021;11(9):210168. doi: 10.1098/rsob.210168
   PubMed Web of Science ®Google Scholar
• Pommier Y, Sun Y, Huang SN, et al. Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat Rev Mol Cell Biol. 2016;17(11):703–721. doi: 10.1038/nrm.2016.111
   PubMed Web of Science ®Google Scholar
• Lai MS, Seki M, Tada S, et al. Rmi1 functions in S phase-mediated cohesion establishment via a pathway involving the Ctf18–RFC complex and Mrc1. Biochem Biophys Res Commun. 2012;427(3):682–686. doi: 10.1016/j.bbrc.2012.09.124
   PubMed Web of Science ®Google Scholar
• Lai MS, Seki M, Ui A, et al. Rmi1, a member of the Sgs1–Top3 complex in budding yeast, contributes to sister chromatid cohesion. EMBO Rep. 2007;8(7):685–690. doi: 10.1038/sj.embor.7401000
   PubMed Web of Science ®Google Scholar
• Falkenberg M, Garone C, Minczuk M. Mitochondrial DNA replication in mammalian cells: overview of the pathway. Essays Biochem. 2018;62(3):287–296. doi: 10.1042/EBC20170100
   PubMed Web of Science ®Google Scholar
• Holt IJ, Reyes A. Human mitochondrial DNA replication. Cold Spring Harb Perspect Biol. 2012;4(12):a012971–a012971. doi: 10.1101/cshperspect.a012971
   PubMed Web of Science ®Google Scholar
• Zhang H, Barcelo JM, Lee B, et al. Human mitochondrial topoisomerase I. Proc Natl Acad Sci U S A. 2001;98(19):10608–10613. doi: 10.1073/pnas.191321998
   PubMed Web of Science ®Google Scholar
• Tsai HZ, Lin RK, Hsieh TS. Drosophila mitochondrial topoisomerase III alpha affects the aging process via maintenance of mitochondrial function and genome integrity. J Biomed Sci. 2016;23(1):38. doi: 10.1186/s12929-016-0255-2
   PubMedGoogle Scholar
• Zhang H, Zhang YW, Yasukawa T, et al. Increased negative supercoiling of mtDNA in TOP1mt knockout mice and presence of topoisomerases II and II in vertebrate mitochondria. Nucleic Acids Res. 2014;42(11):7259–7267. doi: 10.1093/nar/gku384
   PubMed Web of Science ®Google Scholar
• Hangas A, Aasumets K, Kekalainen NJ, et al. Ciprofloxacin impairs mitochondrial DNA replication initiation through inhibition of topoisomerase 2. Nucleic Acids Res. 2018;46(18):9625–9636. doi: 10.1093/nar/gky793
   PubMed Web of Science ®Google Scholar
• Berk AJ, Clayton DA. Mechanism of mitochondrial DNA replication in mouse L-cells: asynchronous replication of strands, segregation of circular daughter molecules, aspects of topology and turnover of an initiation sequence. J Mol Biol. 1974;86(4):801–824. doi: 10.1016/0022-2836(74)90355-6
   PubMed Web of Science ®Google Scholar
• Bogenhagen D, Clayton DA. Mechanism of mitochondrial DNA replication in mouse L-cells: kinetics of synthesis and turnover of the initiation sequence. J Mol Biol. 1978;119(1):49–68. doi: 10.1016/0022-2836(78)90269-3
   PubMed Web of Science ®Google Scholar
• Zhang H, Pommier Y. Mitochondrial topoisomerase I sites in the regulatory D-loop region of mitochondrial DNA. Biochemistry. 2008;47(43):11196–11203. doi: 10.1021/bi800774b
   PubMed Web of Science ®Google Scholar
• Brown TA, Cecconi C, Tkachuk AN, et al. Replication of mitochondrial DNA occurs by strand displacement with alternative light-strand origins, not via a strand-coupled mechanism. Genes Dev. 2005;19(20):2466–2476. doi: 10.1101/gad.1352105
   PubMed Web of Science ®Google Scholar
• Brown TA, Clayton DA. Genesis and wanderings: origins and migrations in asymmetrically replicating mitochondrial DNA. Cell Cycle. 2006;5(9):917–921. doi: 10.4161/cc.5.9.2710
   PubMed Web of Science ®Google Scholar
• Yasukawa T, Reyes A, Cluett TJ, et al. Replication of vertebrate mitochondrial DNA entails transient ribonucleotide incorporation throughout the lagging strand. EMBO J. 2006;25(22):5358–5371. doi: 10.1038/sj.emboj.7601392
   PubMed Web of Science ®Google Scholar
• Holt IJ, Lorimer HE, Jacobs HT. Coupled leading- and lagging-strand synthesis of mammalian mitochondrial DNA. Cell. 2000;100(5):515–524. doi: 10.1016/S0092-8674(00)80688-1
   PubMed Web of Science ®Google Scholar
• Shutt TE, Gray MW. Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet. 2006;22(2):90–95. doi: 10.1016/j.tig.2005.11.007
   PubMed Web of Science ®Google Scholar
• Kukat C, Wurm CA, Spahr H, et al. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc Natl Acad Sci U S A. 2011;108(33):13534–13539. doi: 10.1073/pnas.1109263108
   PubMed Web of Science ®Google Scholar
• Hudson B, Vinograd J. Catenated circular DNA molecules in HeLa cell mitochondria. Nature. 1967;216(5116):647–652. doi: 10.1038/216647a0
   PubMed Web of Science ®Google Scholar
• Pohjoismaki JL, Goffart S, Tyynismaa H, et al. Human heart mitochondrial DNA is organized in complex catenated networks containing abundant four-way junctions and replication forks. J Biol Chem. 2009;284(32):21446–21457. doi: 10.1074/jbc.M109.016600
   PubMed Web of Science ®Google Scholar
• Kukat C, Davies KM, Wurm CA, et al. Cross-strand binding of TFAM to a single mtDNA molecule forms the mitochondrial nucleoid. Proc Natl Acad Sci U S A. 2015;112(36):11288–11293. doi: 10.1073/pnas.1512131112
   PubMed Web of Science ®Google Scholar
• Kopek BG, Shtengel G, Xu CS, et al. Correlative 3D superresolution fluorescence and electron microscopy reveal the relationship of mitochondrial nucleoids to membranes. Proc Natl Acad Sci U S A. 2012;109(16):6136–6141. doi: 10.1073/pnas.1121558109
   PubMed Web of Science ®Google Scholar
• Albring M, Griffith J, Attardi G. Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. Proc Natl Acad Sci U S A. 1977;74(4):1348–1352. doi: 10.1073/pnas.74.4.1348
   PubMed Web of Science ®Google Scholar
• Rajala N, Gerhold JM, Martinsson P, et al. Replication factors transiently associate with mtDNA at the mitochondrial inner membrane to facilitate replication. Nucleic Acids Res. 2014;42(2):952–967. doi: 10.1093/nar/gkt988
   PubMed Web of Science ®Google Scholar
• Peter B, Falkenberg M. TWINKLE and other human mitochondrial DNA helicases: structure, function and disease. Genes (Basel). 2020;11(4):11. doi: 10.3390/genes11040408
   Web of Science ®Google Scholar
• Tse YC, Kirkegaard K, Wang JC. Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA. J Biol Chem. 1980;255(12):5560–5565. doi: 10.1016/S0021-9258(19)70666-8
   PubMed Web of Science ®Google Scholar
• Wang JC. DNA topoisomerases: why so many? J Biol Chem. 1991;266(11):6659–6662. doi: 10.1016/S0021-9258(20)89545-3
   PubMed Web of Science ®Google Scholar
• Sun Y, Saha LK, Saha S. Debulking of topoisomerase DNA-protein crosslinks (TOP-DPC) by the proteasome, non-proteasomal and non-proteolytic pathways. DNA Repair. 2020;94:102926. doi: 10.1016/j.dnarep.2020.102926
   PubMed Web of Science ®Google Scholar
• Pommier Y, Marchand C. Interfacial inhibitors: targeting macromolecular complexes. Nat Rev Drug Discov. 2011;11(1):25–36. doi: 10.1038/nrd3404
   PubMed Web of Science ®Google Scholar
• Cheng B, Annamalai T, Sorokin E, et al. Asp-to-asn substitution at the first position of the DxD TOPRIM motif of recombinant bacterial topoisomerase I is extremely lethal to E. coli. J Mol Biol. 2009;385(2):558–567. doi: 10.1016/j.jmb.2008.10.073
   PubMed Web of Science ®Google Scholar
• Cheng B, Shukla S, Vasunilashorn S, et al. Bacterial cell killing mediated by topoisomerase I DNA cleavage activity. J Biol Chem. 2005;280(46):38489–38495. doi: 10.1074/jbc.M509722200
   PubMed Web of Science ®Google Scholar
• Narula G, Annamalai T, Aedo S, et al. The strictly conserved arg-321 residue in the active site of Escherichia coli topoisomerase I plays a critical role in DNA rejoining. J Biol Chem. 2011;286(21):18673–18680. doi: 10.1074/jbc.M111.229450
   PubMed Web of Science ®Google Scholar
• Sun Y, Saha S, Wang W. Excision repair of topoisomerase DNA-protein crosslinks (TOP-DPC). DNA Repair. 2020;89:102837. doi: 10.1016/j.dnarep.2020.102837
   PubMed Web of Science ®Google Scholar
• Ruggiano A, Ramadan K. DNA–protein crosslink proteases in genome stability. Commun Biol. 2021;4(1):11. doi: 10.1038/s42003-020-01539-3
   PubMed Web of Science ®Google Scholar
• Saha S, Sun Y, Huang SN, et al. DNA and RNA cleavage complexes and repair pathway for TOP3B RNA- and DNA-Protein crosslinks. Cell Rep. 2020;33(13):108569. doi: 10.1016/j.celrep.2020.108569
   PubMed Web of Science ®Google Scholar
• Sun Y, Miller Jenkins LM, 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
   Web of Science ®Google Scholar
• Liu JCY, Kuhbacher U, Larsen NB, et al. Mechanism and function of DNA replication-independent DNA-protein crosslink repair via the SUMO-RNF4 pathway. EMBO J. 2021;40(18):e107413. doi: 10.15252/embj.2020107413
   PubMed Web of Science ®Google Scholar
• Stingele J, Bellelli R, Alte F, et al. Mechanism and Regulation of DNA-Protein crosslink repair by the DNA-Dependent Metalloprotease SPRTN. Mol Cell. 2016;64(4):688–703. doi: 10.1016/j.molcel.2016.09.031
   PubMed Web of Science ®Google Scholar
• Vaz B, Popovic M, Newman JA, et al. Metalloprotease SPRTN/DVC1 orchestrates replication-coupled DNA-Protein crosslink repair. Mol Cell. 2016;64(4):704–719. doi: 10.1016/j.molcel.2016.09.032
   PubMed Web of Science ®Google Scholar
• Lopez-Mosqueda J, Maddi K, Prgomet S. SPRTN is a mammalian DNA-binding metalloprotease that resolves DNA-protein crosslinks. Elife. 2016;5. doi: 10.7554/eLife.21491
   PubMed Web of Science ®Google Scholar
• Larsen NB, Gao AO, Sparks JL, et al. Replication-coupled DNA-protein crosslink repair by SPRTN and the proteasome in xenopus egg extracts. Mol Cell. 2019;73(3):574–88 e7. doi: 10.1016/j.molcel.2018.11.024
   PubMed Web of Science ®Google Scholar
• Weickert P, Li HY, Gotz MJ, et al. SPRTN patient variants cause global-genome DNA-protein crosslink repair defects. Nat Commun. 2023;14(1):352. doi: 10.1038/s41467-023-35988-1
   PubMed Web of Science ®Google Scholar
• Bhargava V, Goldstein CD, Russell L, et al. GCNA preserves genome integrity and fertility across species. Dev Cell. 2020;52(1):38–52 e10. doi: 10.1016/j.devcel.2019.11.007
   PubMed Web of Science ®Google Scholar
• Dokshin GA, Davis GM, Sawle AD, et al. GCNA interacts with spartan and topoisomerase II to regulate genome stability. Dev Cell. 2020;52(1):53–68 e6. doi: 10.1016/j.devcel.2019.11.006
   PubMed Web of Science ®Google Scholar
• Serbyn N, Noireterre A, Bagdiul I, et al. The aspartic protease Ddi1 contributes to DNA-protein crosslink repair in yeast. Mol Cell. 2020;77(5):1066–79 e9. doi: 10.1016/j.molcel.2019.12.007
   PubMed Web of Science ®Google Scholar
• Kojima Y, Machida Y, Palani S, et al. FAM111A protects replication forks from protein obstacles via its trypsin-like domain. Nat Commun. 2020;11(1):1318. doi: 10.1038/s41467-020-15170-7
   PubMed Web of Science ®Google Scholar
• Pommier Y, Huang SY, Gao R. Tyrosyl-DNA-phosphodiesterases (TDP1 and TDP2). DNA Repair. 2014;19:114–129. doi: 10.1016/j.dnarep.2014.03.020
   PubMed Web of Science ®Google Scholar
• Paull TT. 20 years of Mre11 biology: No end in sight. Mol Cell. 2018;71(3):419–427. doi: 10.1016/j.molcel.2018.06.033
   PubMed Web of Science ®Google Scholar
• Oh J, Symington LS. Role of the Mre11 complex in preserving genome integrity. Genes (Basel). 2018;9(12):589. doi: 10.3390/genes9120589
   PubMed Web of Science ®Google Scholar
• Neale MJ, Pan J, Keeney S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature. 2005;436(7053):1053–1057. doi: 10.1038/nature03872
   PubMed Web of Science ®Google Scholar
• Hartsuiker E, Mizuno K, Molnar M, et al. Ctp1CtIP and Rad32Mre11 Nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol Cell Biol. 2009;29(7):1671–1681. doi: 10.1128/MCB.01182-08
   PubMed Web of Science ®Google Scholar
• Hartsuiker E, Neale MJ, Carr AM. Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) 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
   PubMed Web of Science ®Google Scholar
• Deng C, Brown JA, You D, et al. Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics. 2005;170(2):591–600. doi: 10.1534/genetics.104.028795
   PubMed Web of Science ®Google Scholar
• Sacho EJ, Maizels N. DNA repair factor MRE11/RAD50 cleaves 3’-phosphotyrosyl bonds and resects DNA to repair damage caused by topoisomerase 1 poisons. J Biol Chem. 2011;286(52):44945–44951. doi: 10.1074/jbc.M111.299347
   PubMed Web of Science ®Google Scholar
• Lee KC, Padget K, Curtis H, et al. MRE11 facilitates the removal of human topoisomerase II complexes from genomic DNA. Biol Open. 2012;1(9):863–873. doi: 10.1242/bio.20121834
   PubMed Web of Science ®Google Scholar
• 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(5):1010. doi: 10.1016/j.molcel.2016.11.028
   PubMed Web of Science ®Google Scholar
• Quennet V, Beucher A, Barton O, et al. CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1. Nucleic Acids Res. 2011;39(6):2144–2152. doi: 10.1093/nar/gkq1175
   PubMed Web of Science ®Google Scholar
• Aparicio T, Baer R, Gottesman M, et al. MRN, CtIP, and BRCA1 mediate repair of topoisomerase II–DNA adducts. J Cell Bio. 2016;212(4):399–408. doi: 10.1083/jcb.201504005
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Cannavo E, Cejka P. Sae2 promotes dsDNA endonuclease activity within Mre11–Rad50–Xrs2 to resect DNA breaks. Nature. 2014;514(7520):122–125. doi: 10.1038/nature13771
   PubMed Web of Science ®Google Scholar
• Sartori AA, Lukas C, Coates J, et al. Human CtIP promotes DNA end resection. Nature. 2007;450(7169):509–514. doi: 10.1038/nature06337
   PubMed Web of Science ®Google Scholar
• Anand R, Ranjha L, Cannavo E, et al. Phosphorylated CtIP functions as a Co-factor of the MRE11-RAD50-NBS1 endonuclease in DNA end resection. Mol Cell. 2016;64(5):940–950. doi: 10.1016/j.molcel.2016.10.017
   PubMed Web of Science ®Google Scholar
• Hendriks IA, Vertegaal AC. A comprehensive compilation of SUMO proteomics. Nat Rev Mol Cell Biol. 2016;17(9):581–595. doi: 10.1038/nrm.2016.81
   PubMed Web of Science ®Google Scholar
• Centore RC, Yazinski SA, Tse A, et al. Spartan/C1orf124, a reader of PCNA ubiquitylation and a regulator of UV-induced DNA damage response. Mol Cell. 2012;46(5):625–635. doi: 10.1016/j.molcel.2012.05.020
   PubMed Web of Science ®Google Scholar
• Schellenberg MJ, Lieberman JA, Herrero-Ruiz A, et al. ZATT (ZNF451)–mediated resolution of topoisomerase 2 DNA-protein cross-links. Science. 2017;357(6358):1412–1416. doi: 10.1126/science.aam6468
   PubMed Web of Science ®Google Scholar