{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T14:23:34Z","timestamp":1790778214035,"version":"4.1.0"},"reference-count":57,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2019,11,13]],"date-time":"2019-11-13T00:00:00Z","timestamp":1573603200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["310913"],"award-info":[{"award-number":["310913"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["340988"],"award-info":[{"award-number":["340988"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003246","name":"Netherlands Organisation for Scientific Research","doi-asserted-by":"publisher","award":["ALWOP.143"],"award-info":[{"award-number":["ALWOP.143"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003246","name":"Netherlands Organisation for Scientific Research","doi-asserted-by":"publisher","award":["855-01-074"],"award-info":[{"award-number":["855-01-074"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]},{"name":"NTC Netherlands Toxicogenomics Center","award":["050-060-510"],"award-info":[{"award-number":["050-060-510"]}]},{"name":"LUMC research fellowship and NWO-VIDI","award":["016.161.320"],"award-info":[{"award-number":["016.161.320"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cockayne Syndrome (CS) is a severe neurodegenerative and premature aging autosomal-recessive disease, caused by inherited defects in the CSA and CSB genes, leading to defects in transcription-coupled nucleotide excision repair (TC-NER) and consequently hypersensitivity to ultraviolet (UV) irradiation. TC-NER is initiated by lesion-stalled RNA polymerase II, which stabilizes the interaction with the SNF2\/SWI2 ATPase CSB to facilitate recruitment of the CSA E3 Cullin ubiquitin ligase complex. However, the precise biochemical connections between CSA and CSB are unknown. The small ubiquitin-like modifier SUMO is important in the DNA damage response. We found that CSB, among an extensive set of other target proteins, is the most dynamically SUMOylated substrate in response to UV irradiation. Inhibiting SUMOylation reduced the accumulation of CSB at local sites of UV irradiation and reduced recovery of RNA synthesis. Interestingly, CSA is required for the efficient clearance of SUMOylated CSB. However, subsequent proteomic analysis of CSA-dependent ubiquitinated substrates revealed that CSA does not ubiquitinate CSB in a UV-dependent manner. Surprisingly, we found that CSA is required for the ubiquitination of the largest subunit of RNA polymerase II, RPB1. Combined, our results indicate that the CSA, CSB, RNA polymerase II triad is coordinated by ubiquitin and SUMO in response to UV irradiation. Furthermore, our work provides a resource of SUMO targets regulated in response to UV or ionizing radiation.<\/jats:p>","DOI":"10.1093\/nar\/gkz977","type":"journal-article","created":{"date-parts":[[2019,10,14]],"date-time":"2019-10-14T19:28:47Z","timestamp":1571081327000},"source":"Crossref","is-referenced-by-count":6,"title":["Transcription-coupled nucleotide excision repair is coordinated by ubiquitin and SUMO in response to ultraviolet irradiation"],"prefix":"10.1093","author":[{"given":"Frauke","family":"Liebelt","sequence":"first","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joost","family":"Schimmel","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"},{"name":"Department of Human Genetics, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matty","family":"Verlaan\u00a0\u2013\u00a0de\u00a0Vries","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esra","family":"Klemann","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin E","family":"van\u00a0Royen","sequence":"additional","affiliation":[{"name":"Department of Pathology, Cancer Treatment Screening Facility (CTSF), Erasmus Optical Imaging Centre (OIC), Erasmus University Medical Center, Wytemaweg 80, 3015 CN Rotterdam, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yana","family":"van\u00a0der\u00a0Weegen","sequence":"additional","affiliation":[{"name":"Department of Human Genetics, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martijn S","family":"Luijsterburg","sequence":"additional","affiliation":[{"name":"Department of Human Genetics, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leon H","family":"Mullenders","sequence":"additional","affiliation":[{"name":"Department of Human Genetics, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"},{"name":"Department of Genetics, Research Institute of Environmental Medicine (RIeM), Nagoya University, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Pines","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, Oncode Institute, Erasmus MC, University Medical Center Rotterdam, Dr Molewaterplein 40, 3015 GD Rotterdam, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wim","family":"Vermeulen","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, Oncode Institute, Erasmus MC, University Medical Center Rotterdam, Dr Molewaterplein 40, 3015 GD Rotterdam, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alfred C O","family":"Vertegaal","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, Einthovenweg 20, Leiden 2333 ZC, the Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,11,13]]},"reference":[{"key":"2019111316335425100_B1","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1056\/NEJMra0804615","article-title":"DNA damage, aging, and cancer","volume":"361","author":"Hoeijmakers","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"2019111316335425100_B2","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.tcb.2015.07.009","article-title":"Repair pathway choices and consequences at the Double-Strand break","volume":"26","author":"Ceccaldi","year":"2016","journal-title":"Trends Cell Biol."},{"key":"2019111316335425100_B3","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.mrrev.2012.06.002","article-title":"Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography","volume":"751","author":"Thompson","year":"2012","journal-title":"Mutat. Res."},{"key":"2019111316335425100_B4","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.dnarep.2014.02.007","article-title":"Alternative end-joining pathway(s): bricolage at DNA breaks","volume":"17","author":"Frit","year":"2014","journal-title":"DNA Repair (Amst.)"},{"key":"2019111316335425100_B5","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1038\/nrm3822","article-title":"Understanding nucleotide excision repair and its roles in cancer and ageing","volume":"15","author":"Marteijn","year":"2014","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2019111316335425100_B6","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/j.molcel.2013.01.017","article-title":"Regulation of DNA damage responses by ubiquitin and SUMO","volume":"49","author":"Jackson","year":"2013","journal-title":"Mol. Cell"},{"key":"2019111316335425100_B7","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1146\/annurev-biochem-061909-093311","article-title":"Sumoylation: a regulatory protein modification in health and disease","volume":"82","author":"Flotho","year":"2013","journal-title":"Annu. Rev. Biochem."},{"key":"2019111316335425100_B8","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1038\/nrm3478","article-title":"Function and regulation of SUMO proteases","volume":"13","author":"Hickey","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2019111316335425100_B9","doi-asserted-by":"crossref","first-page":"878","DOI":"10.15252\/embr.201438534","article-title":"SUMO2 is essential while SUMO3 is dispensable for mouse embryonic development","volume":"15","author":"Wang","year":"2014","journal-title":"EMBO Rep."},{"key":"2019111316335425100_B10","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nrm.2016.81","article-title":"A comprehensive compilation of SUMO proteomics","volume":"17","author":"Hendriks","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2019111316335425100_B11","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1038\/nature03634","article-title":"Crystal structure of thymine DNA glycosylase conjugated to SUMO-1","volume":"435","author":"Baba","year":"2005","journal-title":"Nature"},{"key":"2019111316335425100_B12","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1016\/j.cub.2005.02.054","article-title":"Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation","volume":"15","author":"Steinacher","year":"2005","journal-title":"Curr. Biol."},{"key":"2019111316335425100_B13","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1038\/nature08593","article-title":"The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress","volume":"462","author":"Morris","year":"2009","journal-title":"Nature"},{"key":"2019111316335425100_B14","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1038\/nature00991","article-title":"RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO","volume":"419","author":"Hoege","year":"2002","journal-title":"Nature"},{"key":"2019111316335425100_B15","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/nature07963","article-title":"Principles of ubiquitin and SUMO modifications in DNA repair","volume":"458","author":"Bergink","year":"2009","journal-title":"Nature"},{"key":"2019111316335425100_B16","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1101\/gad.188284.112","article-title":"RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair","volume":"26","author":"Galanty","year":"2012","journal-title":"Genes Dev."},{"key":"2019111316335425100_B17","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1101\/gad.189274.112","article-title":"SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage","volume":"26","author":"Yin","year":"2012","journal-title":"Genes Dev."},{"key":"2019111316335425100_B18","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1083\/jcb.201212075","article-title":"RNF111\/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response","volume":"201","author":"Poulsen","year":"2013","journal-title":"J. Cell Biol."},{"key":"2019111316335425100_B19","doi-asserted-by":"crossref","first-page":"4023","DOI":"10.1093\/nar\/gki684","article-title":"DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation","volume":"33","author":"Wang","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"2019111316335425100_B20","doi-asserted-by":"crossref","first-page":"7499","DOI":"10.1038\/ncomms8499","article-title":"SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair","volume":"6","author":"van\u00a0Cuijk","year":"2015","journal-title":"Nat. Commun."},{"key":"2019111316335425100_B21","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1101\/gad.378206","article-title":"CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome","volume":"20","author":"Groisman","year":"2006","journal-title":"Genes Dev."},{"key":"2019111316335425100_B22","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/ng.2230","article-title":"UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair","volume":"44","author":"Schwertman","year":"2012","journal-title":"Nat. Genet."},{"key":"2019111316335425100_B23","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1038\/ng.2228","article-title":"Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair","volume":"44","author":"Zhang","year":"2012","journal-title":"Nat. Genet."},{"key":"2019111316335425100_B24","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1038\/ng.2229","article-title":"Mutations in UVSSA cause UV-sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair","volume":"44","author":"Nakazawa","year":"2012","journal-title":"Nat. Genet."},{"key":"2019111316335425100_B25","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1038\/s41467-018-03484-6","article-title":"TRiC controls transcription resumption after UV damage by regulating Cockayne syndrome protein A","volume":"9","author":"Pines","year":"2018","journal-title":"Nat. Commun."},{"key":"2019111316335425100_B26","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/j.ymeth.2006.08.001","article-title":"Quantitative proteomics to study mitogen-activated protein kinases","volume":"40","author":"Blagoev","year":"2006","journal-title":"Methods"},{"key":"2019111316335425100_B27","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1016\/j.molcel.2014.02.001","article-title":"Uncovering SUMOylation dynamics during cell-cycle progression reveals FoxM1 as a key mitotic SUMO target protein","volume":"53","author":"Schimmel","year":"2014","journal-title":"Mol. Cell"},{"key":"2019111316335425100_B28","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1074\/mcp.O114.044792","article-title":"System-wide analysis of SUMOylation dynamics in response to replication stress reveals novel SUMO target proteins and acceptor lysines relevant for genome stability","volume":"14","author":"Xiao","year":"2015","journal-title":"Mol. Cell Proteomics"},{"key":"2019111316335425100_B29","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1242\/jcs.004523","article-title":"Activation of multiple DNA repair pathways by sub-nuclear damage induction methods","volume":"120","author":"Dinant","year":"2007","journal-title":"J. Cell Sci."},{"key":"2019111316335425100_B30","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/978-1-4939-6358-4_13","article-title":"Label-free identification and quantification of SUMO target proteins","volume":"1475","author":"Hendriks","year":"2016","journal-title":"Methods Mol. Biol."},{"key":"2019111316335425100_B31","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1038\/s41467-018-03486-4","article-title":"SUMO targets the APC\/C to regulate transition from metaphase to anaphase","volume":"9","author":"Eifler","year":"2018","journal-title":"Nat. Commun."},{"key":"2019111316335425100_B32","doi-asserted-by":"crossref","first-page":"1896","DOI":"10.1038\/nprot.2007.261","article-title":"Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips","volume":"2","author":"Rappsilber","year":"2007","journal-title":"Nat. Protoc."},{"key":"2019111316335425100_B33","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/S0003-2697(04)00378-1","article-title":"Overproduction of eukaryotic SUMO-1- and SUMO-2-conjugated proteins in Escherichia coli","volume":"331","author":"Uchimura","year":"2004","journal-title":"Anal. Biochem."},{"key":"2019111316335425100_B34","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.1038\/emboj.2012.158","article-title":"Sumoylation of MDC1 is important for proper DNA damage response","volume":"31","author":"Luo","year":"2012","journal-title":"EMBO J."},{"key":"2019111316335425100_B35","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.mrrev.2016.04.004","article-title":"Role of nucleotide excision repair proteins in response to DNA damage induced by topoisomerase II inhibitors","volume":"768","author":"Rocha","year":"2016","journal-title":"Mutat. Res. Rev. Mutat. Res."},{"key":"2019111316335425100_B36","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1266\/ggs.86.83","article-title":"Fission yeast homologs of human XPC and CSB, rhp41 and rhp26, are involved in transcription-coupled repair of methyl methanesulfonate-induced DNA damage","volume":"86","author":"Kanamitsu","year":"2011","journal-title":"Genes Genet. Syst."},{"key":"2019111316335425100_B37","doi-asserted-by":"crossref","first-page":"103","DOI":"10.4161\/trns.2.3.16172","article-title":"Inhibiting eukaryotic transcription: which compound to choose? How to evaluate its activity","volume":"2","author":"Bensaude","year":"2011","journal-title":"Transcription"},{"key":"2019111316335425100_B38","first-page":"1473","article-title":"Failure of RNA synthesis to recover after UV irradiation: an early defect in cells from individuals with Cockayne's syndrome and xeroderma pigmentosum","volume":"42","author":"Mayne","year":"1982","journal-title":"Cancer Res."},{"key":"2019111316335425100_B39","doi-asserted-by":"crossref","first-page":"2744","DOI":"10.1093\/nar\/gkv148","article-title":"DNA repair and recovery of RNA synthesis following exposure to ultraviolet light are delayed in long genes","volume":"43","author":"Andrade-Lima","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"2019111316335425100_B40","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1007\/s00441-014-1964-z","article-title":"Emerging role of polymerase-1 and transcript release factor (PTRF\/ Cavin-1) in health and disease","volume":"357","author":"Low","year":"2014","journal-title":"Cell Tissue Res."},{"key":"2019111316335425100_B41","doi-asserted-by":"crossref","first-page":"e17508","DOI":"10.7554\/eLife.17508","article-title":"PTRF\/Cavin-1 promotes efficient ribosomal RNA transcription in response to metabolic challenges","volume":"5","author":"Liu","year":"2016","journal-title":"Elife"},{"key":"2019111316335425100_B42","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1016\/S1097-2765(02)00678-0","article-title":"CSB is a component of RNA pol I transcription","volume":"10","author":"Bradsher","year":"2002","journal-title":"Mol. Cell"},{"key":"2019111316335425100_B43","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/978-1-61779-474-2_18","article-title":"Bioinformatical detection of recognition factors for ubiquitin and SUMO","volume":"832","author":"Vogt","year":"2012","journal-title":"Methods Mol. Biol."},{"key":"2019111316335425100_B44","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1016\/S0021-9258(19)57421-X","article-title":"DNA repair synthesis in human fibroblasts requires DNA polymerase delta","volume":"263","author":"Nishida","year":"1988","journal-title":"J. Biol. Chem."},{"key":"2019111316335425100_B45","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1101\/gad.14.3.349","article-title":"Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK","volume":"14","author":"Araujo","year":"2000","journal-title":"Genes Dev."},{"key":"2019111316335425100_B46","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1073\/pnas.012473199","article-title":"Translocation of Cockayne syndrome group A protein to the nuclear matrix: possible relevance to transcription-coupled DNA repair","volume":"99","author":"Kamiuchi","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"2019111316335425100_B47","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0092-8674(03)00316-7","article-title":"The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage","volume":"113","author":"Groisman","year":"2003","journal-title":"Cell"},{"key":"2019111316335425100_B48","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1038\/35008103","article-title":"The major substrates for TAP in vivo are derived from newly synthesized proteins","volume":"404","author":"Reits","year":"2000","journal-title":"Nature"},{"key":"2019111316335425100_B49","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1038\/35008096","article-title":"Rapid degradation of a large fraction of newly synthesized proteins by proteasomes","volume":"404","author":"Schubert","year":"2000","journal-title":"Nature"},{"key":"2019111316335425100_B50","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.bbagrm.2012.08.002","article-title":"Ubiquitylation and degradation of elongating RNA polymerase II: the last resort","volume":"1829","author":"Wilson","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"2019111316335425100_B51","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/j.molcel.2007.10.008","article-title":"Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1","volume":"28","author":"Anindya","year":"2007","journal-title":"Mol. Cell"},{"key":"2019111316335425100_B52","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1016\/j.molcel.2010.04.017","article-title":"A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair","volume":"38","author":"Anindya","year":"2010","journal-title":"Mol. Cell"},{"key":"2019111316335425100_B53","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1074\/jbc.M115.683235","article-title":"The C-terminal region and SUMOylation of cockayne syndrome group B protein play critical roles in Transcription-coupled nucleotide excision repair","volume":"291","author":"Sin","year":"2016","journal-title":"J. Biol. Chem"},{"key":"2019111316335425100_B54","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1016\/j.cell.2012.10.021","article-title":"Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair","volume":"151","author":"Psakhye","year":"2012","journal-title":"Cell"},{"key":"2019111316335425100_B55","doi-asserted-by":"crossref","first-page":"11586","DOI":"10.1073\/pnas.93.21.11586","article-title":"UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells","volume":"93","author":"Bregman","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2019111316335425100_B56","doi-asserted-by":"crossref","first-page":"D447","DOI":"10.1093\/nar\/gkv1145","article-title":"2016 update of the PRIDE database and its related tools","volume":"44","author":"Vizcaino","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"2019111316335425100_B57","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1111\/j.1365-2443.2010.01467.x","article-title":"Mutant Cockayne syndrome group B protein inhibits repair of DNA topoisomerase I-DNA covalent complex","volume":"16","author":"Horibata","year":"2011","journal-title":"Genes Cells"}],"container-title":["Nucleic Acids Research"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/nar\/advance-article-pdf\/doi\/10.1093\/nar\/gkz977\/30699283\/gkz977.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/nar\/advance-article-pdf\/doi\/10.1093\/nar\/gkz977\/30699283\/gkz977.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,1]],"date-time":"2022-10-01T19:22:04Z","timestamp":1664652124000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/nar\/advance-article\/doi\/10.1093\/nar\/gkz977\/5624976"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,13]]},"references-count":57,"URL":"https:\/\/doi.org\/10.1093\/nar\/gkz977","relation":{},"ISSN":["0305-1048","1362-4962"],"issn-type":[{"value":"0305-1048","type":"print"},{"value":"1362-4962","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,13]]},"article-number":"gkz977"}}