{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T03:15:07Z","timestamp":1790046907998,"version":"4.0.1"},"reference-count":49,"publisher":"Elsevier BV","issue":"1","license":[{"start":{"date-parts":[[2020,10,1]],"date-time":"2020-10-01T00:00:00Z","timestamp":1601510400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2020,10,1]],"date-time":"2020-10-01T00:00:00Z","timestamp":1601510400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2020,8,11]],"date-time":"2020-08-11T00:00:00Z","timestamp":1597104000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Molecular Cell"],"published-print":{"date-parts":[[2020,10]]},"DOI":"10.1016\/j.molcel.2020.08.003","type":"journal-article","created":{"date-parts":[[2020,8,26]],"date-time":"2020-08-26T10:35:12Z","timestamp":1598438112000},"page":"102-113.e6","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":64,"title":["DNA Structure-Specific Cleavage of DNA-Protein Crosslinks by the SPRTN Protease"],"prefix":"10.1016","volume":"80","author":[{"given":"Hannah K.","family":"Reinking","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4029-5096","authenticated-orcid":false,"given":"Hyun-Seo","family":"Kang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maximilian J.","family":"G\u00f6tz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9739-5365","authenticated-orcid":false,"given":"Hao-Yi","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anja","family":"Kieser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shubo","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6512-7852","authenticated-orcid":false,"given":"Aleida C.","family":"Acampora","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pedro","family":"Weickert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Evelyn","family":"Fessler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lucas T.","family":"Jae","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1594-0527","authenticated-orcid":false,"given":"Michael","family":"Sattler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julian","family":"Stingele","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.molcel.2020.08.003_bib1","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.mrrev.2004.11.003","article-title":"DNA-protein crosslinks: their induction, repair, and biological consequences","volume":"589","author":"Barker","year":"2005","journal-title":"Mutat. Res."},{"key":"10.1016\/j.molcel.2020.08.003_bib2","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.molcel.2014.04.031","article-title":"NCOA4 transcriptional coactivator inhibits activation of DNA replication origins","volume":"55","author":"Bellelli","year":"2014","journal-title":"Mol. Cell"},{"key":"10.1016\/j.molcel.2020.08.003_bib3","doi-asserted-by":"crossref","first-page":"e101496","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":"10.1016\/j.molcel.2020.08.003_bib4","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1016\/j.molcel.2012.05.020","article-title":"Spartan\/C1orf124, a reader of PCNA ubiquitylation and a regulator of UV-induced DNA damage response","volume":"46","author":"Centore","year":"2012","journal-title":"Mol. Cell"},{"key":"10.1016\/j.molcel.2020.08.003_bib5","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1146\/annurev-biochem-061809-100002","article-title":"New mechanistic and functional insights into DNA topoisomerases","volume":"82","author":"Chen","year":"2013","journal-title":"Annu. Rev. Biochem."},{"key":"10.1016\/j.molcel.2020.08.003_bib6","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1038\/nature08444","article-title":"A human 5\u2032-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage","volume":"461","author":"Cortes Ledesma","year":"2009","journal-title":"Nature"},{"key":"10.1016\/j.molcel.2020.08.003_bib7","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1038\/nsmb.2394","article-title":"DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage","volume":"19","author":"Davis","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.molcel.2020.08.003_bib8","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1038\/nrm.2016.177","article-title":"Control of structure-specific endonucleases to maintain genome stability","volume":"18","author":"Deh\u00e9","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.molcel.2020.08.003_bib9","doi-asserted-by":"crossref","first-page":"2281","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":"10.1016\/j.molcel.2020.08.003_bib10","doi-asserted-by":"crossref","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":"10.1016\/j.molcel.2020.08.003_bib11","doi-asserted-by":"crossref","first-page":"346","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":"10.1016\/j.molcel.2020.08.003_bib12","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1038\/s41467-020-15000-w","article-title":"TEX264 coordinates p97- and SPRTN-mediated resolution of topoisomerase 1-DNA adducts","volume":"11","author":"Fielden","year":"2020","journal-title":"Nat. Commun."},{"key":"10.1016\/j.molcel.2020.08.003_bib13","doi-asserted-by":"crossref","first-page":"931","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":"10.1016\/j.molcel.2020.08.003_bib14","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1016\/j.cell.2015.11.015","article-title":"High-Resolution CRISPR Screens Reveal Fitness Genes and Genotype-Specific Cancer Liabilities","volume":"163","author":"Hart","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.molcel.2020.08.003_bib15","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1038\/nature08467","article-title":"The DNA-damage response in human biology and disease","volume":"461","author":"Jackson","year":"2009","journal-title":"Nature"},{"key":"10.1016\/j.molcel.2020.08.003_bib16","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.1126\/science.1252480","article-title":"Virus entry. Lassa virus entry requires a trigger-induced receptor switch","volume":"344","author":"Jae","year":"2014","journal-title":"Science"},{"key":"10.1016\/j.molcel.2020.08.003_bib17","doi-asserted-by":"crossref","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":"10.1016\/j.molcel.2020.08.003_bib18","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nature10192","article-title":"Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice","volume":"475","author":"Langevin","year":"2011","journal-title":"Nature"},{"key":"10.1016\/j.molcel.2020.08.003_bib19","doi-asserted-by":"crossref","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":"10.1016\/j.molcel.2020.08.003_bib49","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1093\/bioinformatics\/btu830","article-title":"NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy","volume":"31","author":"Lee","year":"2015","journal-title":"Bioinformatics"},{"key":"10.1016\/j.molcel.2020.08.003_bib20","doi-asserted-by":"crossref","first-page":"1239","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":"10.1016\/j.molcel.2020.08.003_bib21","doi-asserted-by":"crossref","first-page":"3336","DOI":"10.1016\/j.celrep.2019.02.082","article-title":"Structural Insight into DNA-Dependent Activation of Human Metalloprotease Spartan","volume":"26","author":"Li","year":"2019","journal-title":"Cell Rep."},{"key":"10.1016\/j.molcel.2020.08.003_bib22","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1038\/362709a0","article-title":"Instability and decay of the primary structure of DNA","volume":"362","author":"Lindahl","year":"1993","journal-title":"Nature"},{"key":"10.1016\/j.molcel.2020.08.003_bib23","doi-asserted-by":"crossref","first-page":"e21491","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":"10.1016\/j.molcel.2020.08.003_bib24","doi-asserted-by":"crossref","first-page":"3388","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.\u00a0Am. Chem. Soc."},{"key":"10.1016\/j.molcel.2020.08.003_bib25","doi-asserted-by":"crossref","first-page":"5744","DOI":"10.1038\/ncomms6744","article-title":"Spartan deficiency causes genomic instability and progeroid phenotypes","volume":"5","author":"Maskey","year":"2014","journal-title":"Nat. Commun."},{"key":"10.1016\/j.molcel.2020.08.003_bib26","doi-asserted-by":"crossref","first-page":"4564","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":"10.1016\/j.molcel.2020.08.003_bib27","first-page":"3172","article-title":"DNA-dependent protease activity of human Spartan facilitates replication of DNA-protein crosslink-containing DNA","volume":"45","author":"M\u00f3rocz","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.molcel.2020.08.003_bib28","doi-asserted-by":"crossref","first-page":"1084","DOI":"10.1038\/nsmb.2395","article-title":"DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks","volume":"19","author":"Mosbech","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.molcel.2020.08.003_bib29","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1006\/jmbi.1999.3034","article-title":"Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins","volume":"292","author":"Mulder","year":"1999","journal-title":"J.\u00a0Mol. Biol."},{"key":"10.1016\/j.molcel.2020.08.003_bib30","doi-asserted-by":"crossref","first-page":"6562","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.\u00a0Biol. Chem."},{"key":"10.1016\/j.molcel.2020.08.003_bib31","doi-asserted-by":"crossref","first-page":"4649","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.\u00a0Biol. Chem."},{"key":"10.1016\/j.molcel.2020.08.003_bib32","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.freeradbiomed.2016.11.041","article-title":"Radiation-induced DNA-protein cross-links: Mechanisms and biological significance","volume":"107","author":"Nakano","year":"2017","journal-title":"Free Radic. Biol. Med."},{"key":"10.1016\/j.molcel.2020.08.003_bib33","doi-asserted-by":"crossref","first-page":"1053","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":"10.1016\/j.molcel.2020.08.003_bib34","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1038\/nrc1977","article-title":"Topoisomerase I inhibitors: camptothecins and beyond","volume":"6","author":"Pommier","year":"2006","journal-title":"Nat. Rev. Cancer"},{"key":"10.1016\/j.molcel.2020.08.003_bib35","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1126\/science.286.5439.552","article-title":"Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes","volume":"286","author":"Pouliot","year":"1999","journal-title":"Science"},{"key":"10.1016\/j.molcel.2020.08.003_bib36","doi-asserted-by":"crossref","first-page":"8602","DOI":"10.1073\/pnas.1501101112","article-title":"Enzyme mechanism-based, oxidative DNA-protein cross-links formed with DNA polymerase \u03b2 in\u00a0vivo","volume":"112","author":"Qui\u00f1ones","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.molcel.2020.08.003_bib37","doi-asserted-by":"crossref","first-page":"102822","DOI":"10.1016\/j.dnarep.2020.102822","article-title":"Function and evolution of the DNA-protein crosslink proteases Wss1 and SPRTN","volume":"88","author":"Reinking","year":"2020","journal-title":"DNA Repair (Amst.)"},{"key":"10.1016\/j.molcel.2020.08.003_bib50","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/S0079-6565(98)00025-9","article-title":"Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients","volume":"34","author":"Sattler","year":"1999","journal-title":"Prog. Nucl. Magn. Reson. Spectrosc."},{"key":"10.1016\/j.molcel.2020.08.003_bib38","doi-asserted-by":"crossref","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":"10.1016\/j.molcel.2020.08.003_bib39","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1073\/pnas.64.3.1035","article-title":"Evidence that xeroderma pigmentosum cells do not perform the first step in the repair of ultraviolet damage to their DNA","volume":"64","author":"Setlow","year":"1969","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.molcel.2020.08.003_bib40","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.cell.2018.10.053","article-title":"The CMG Helicase Bypasses DNA-Protein Cross-Links to Facilitate Their Repair","volume":"176","author":"Sparks","year":"2019","journal-title":"Cell"},{"key":"10.1016\/j.molcel.2020.08.003_bib41","doi-asserted-by":"crossref","first-page":"327","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":"10.1016\/j.molcel.2020.08.003_bib42","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.tibs.2014.10.012","article-title":"DNA-protein crosslink repair: proteases as DNA repair enzymes","volume":"40","author":"Stingele","year":"2015","journal-title":"Trends Biochem. Sci."},{"key":"10.1016\/j.molcel.2020.08.003_bib43","doi-asserted-by":"crossref","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":"10.1016\/j.molcel.2020.08.003_bib44","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/nrm.2017.56","article-title":"Mechanisms of DNA-protein crosslink repair","volume":"18","author":"Stingele","year":"2017","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.molcel.2020.08.003_bib45","doi-asserted-by":"crossref","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 (Amst.)"},{"key":"10.1016\/j.molcel.2020.08.003_bib46","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.dnarep.2016.10.007","article-title":"The DNA-binding box of human SPARTAN contributes to the targeting of Pol\u03b7 to DNA damage sites","volume":"49","author":"Toth","year":"2017","journal-title":"DNA Repair (Amst.)"},{"key":"10.1016\/j.molcel.2020.08.003_bib47","doi-asserted-by":"crossref","first-page":"704","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"}],"container-title":["Molecular Cell"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1097276520305463?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1097276520305463?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,22]],"date-time":"2025-10-22T00:33:24Z","timestamp":1761093204000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1097276520305463"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10]]},"references-count":49,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,10]]}},"alternative-id":["S1097276520305463"],"URL":"https:\/\/doi.org\/10.1016\/j.molcel.2020.08.003","relation":{},"ISSN":["1097-2765"],"issn-type":[{"value":"1097-2765","type":"print"}],"subject":[],"published":{"date-parts":[[2020,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"DNA Structure-Specific Cleavage of DNA-Protein Crosslinks by the SPRTN Protease","name":"articletitle","label":"Article Title"},{"value":"Molecular Cell","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.molcel.2020.08.003","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 The Authors. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}