{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T17:07:20Z","timestamp":1786986440086,"version":"build-2736575974"},"reference-count":106,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,4,1]],"date-time":"2021-04-01T00:00:00Z","timestamp":1617235200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,3,22]],"date-time":"2021-03-22T00:00:00Z","timestamp":1616371200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010663","name":"European Research Council","doi-asserted-by":"publisher","award":["ERC-CoG-2014-647359"],"award-info":[{"award-number":["ERC-CoG-2014-647359"]}],"id":[{"id":"10.13039\/100010663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100013060","name":"European Molecular Biology Laboratory","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100013060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100008530","name":"European Regional Development Fund","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["BES-2015-071672"],"award-info":[{"award-number":["BES-2015-071672"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010198","name":"Gobierno de Espa\u00f1a Ministerio de Econom\u00eda y Competitividad","doi-asserted-by":"publisher","award":["SAF2017-89619-R"],"award-info":[{"award-number":["SAF2017-89619-R"]}],"id":[{"id":"10.13039\/501100010198","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100011011","name":"Junta de Andaluc\u00eda","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100011011","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002704","name":"Fundaci\u00f3n Cient\u00edfica Asociaci\u00f3n Espa\u00f1ola Contra el C\u00e1ncer","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002704","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002878","name":"Junta de Andalucia Consejeria de Economia Innovacion y Ciencia","doi-asserted-by":"publisher","award":["CVI-7948"],"award-info":[{"award-number":["CVI-7948"]}],"id":[{"id":"10.13039\/501100002878","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003176","name":"Ministerio de Educaci\u00f3n, Cultura y Deporte","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003176","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003329","name":"Ministerio de Econom\u00eda y Competitividad","doi-asserted-by":"publisher","award":["FPU15\/03656"],"award-info":[{"award-number":["FPU15\/03656"]}],"id":[{"id":"10.13039\/501100003329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003329","name":"Ministerio de Econom\u00eda y Competitividad","doi-asserted-by":"publisher","award":["RYC-2015-17246"],"award-info":[{"award-number":["RYC-2015-17246"]}],"id":[{"id":"10.13039\/501100003329","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Cell Reports"],"published-print":{"date-parts":[[2021,4]]},"DOI":"10.1016\/j.celrep.2021.108977","type":"journal-article","created":{"date-parts":[[2021,4,15]],"date-time":"2021-04-15T10:24:47Z","timestamp":1618482287000},"page":"108977","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":55,"title":["Topoisomerase II\u03b1 represses transcription by enforcing promoter-proximal pausing"],"prefix":"10.1016","volume":"35","author":[{"given":"Andr\u00e9s","family":"Herrero-Ruiz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pedro Manuel","family":"Mart\u00ednez-Garc\u00eda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9","family":"Terr\u00f3n-Bautista","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gonzalo","family":"Mill\u00e1n-Zambrano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jenna Ariel","family":"Lieberman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"Jimeno-Gonz\u00e1lez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felipe","family":"Cort\u00e9s-Ledesma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.celrep.2021.108977_bib1","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1038\/s41586-020-1934-4","article-title":"Negative supercoil at gene boundaries modulates gene topology","volume":"577","author":"Achar","year":"2020","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib2","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1038\/nrg3293","article-title":"Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans","volume":"13","author":"Adelman","year":"2012","journal-title":"Nat. Rev. Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib105","doi-asserted-by":"crossref","first-page":"2134","DOI":"10.1101\/gad.1214104","article-title":"Attenuation of estrogen receptor alpha-mediated transcription through estrogen-stimulated recruitment of a negative elongation factor","volume":"18","author":"Aiyar","year":"2004","journal-title":"Genes Dev."},{"key":"10.1016\/j.celrep.2021.108977_bib3","series-title":"TopGO: Enrichment Analysis for Gene Ontology","author":"Alexa","year":"2019"},{"key":"10.1016\/j.celrep.2021.108977_bib4","doi-asserted-by":"crossref","first-page":"1600","DOI":"10.1093\/bioinformatics\/btl140","article-title":"Improved scoring of functional groups from gene expression data by decorrelating GO graph structure","volume":"22","author":"Alexa","year":"2006","journal-title":"Bioinformatics"},{"key":"10.1016\/j.celrep.2021.108977_bib5","doi-asserted-by":"crossref","first-page":"3347","DOI":"10.1038\/ncomms4347","article-title":"ATM specifically mediates repair of double-strand breaks with blocked DNA ends","volume":"5","author":"\u00c1lvarez-Quil\u00f3n","year":"2014","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib6","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1038\/s41467-020-14638-w","article-title":"Endogenous topoisomerase II-mediated DNA breaks drive thymic cancer predisposition linked to ATM deficiency","volume":"11","author":"\u00c1lvarez-Quil\u00f3n","year":"2020","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib7","author":"Andrews"},{"key":"10.1016\/j.celrep.2021.108977_bib8","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.molcel.2020.02.014","article-title":"NELF Regulates a Promoter-Proximal Step Distinct from RNA Pol II Pause-Release","volume":"78","author":"Aoi","year":"2020","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib9","doi-asserted-by":"crossref","first-page":"2765","DOI":"10.3390\/ijms19092765","article-title":"TOP2B: The First Thirty Years","volume":"19","author":"Austin","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.celrep.2021.108977_bib10","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/j.molcel.2016.04.028","article-title":"In\u00a0Vivo Mapping of Eukaryotic RNA Interactomes Reveals Principles of Higher-Order Organization and Regulation","volume":"62","author":"Aw","year":"2016","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib11","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.jbior.2016.05.001","article-title":"Gene regulation in the immediate-early response process","volume":"62","author":"Bahrami","year":"2016","journal-title":"Adv. Biol. Regul."},{"key":"10.1016\/j.celrep.2021.108977_bib12","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.cell.2016.02.036","article-title":"RNA Polymerase II Regulates Topoisomerase 1 Activity to Favor Efficient Transcription","volume":"165","author":"Baranello","year":"2016","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib13","doi-asserted-by":"crossref","first-page":"e182","DOI":"10.1093\/nar\/gkq687","article-title":"A method for genome-wide analysis of DNA helical tension by means of psoralen-DNA photobinding","volume":"38","author":"Berm\u00fadez","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib14","doi-asserted-by":"crossref","first-page":"e168","DOI":"10.1093\/nar\/gku936","article-title":"Easy quantitative assessment of genome editing by sequence trace decomposition","volume":"42","author":"Brinkman","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib15","doi-asserted-by":"crossref","first-page":"10191","DOI":"10.1038\/ncomms10191","article-title":"Transcriptional elongation requires DNA break-induced signalling","volume":"6","author":"Bunch","year":"2015","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib16","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.cell.2017.06.034","article-title":"Genome Organization Drives Chromosome Fragility","volume":"170","author":"Canela","year":"2017","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib17","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.molcel.2019.04.030","article-title":"Topoisomerase II-Induced Chromosome Breakage and Translocation Is Determined by Chromosome Architecture and Transcriptional Activity","volume":"75","author":"Canela","year":"2019","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib18","doi-asserted-by":"crossref","first-page":"102686","DOI":"10.1016\/j.dnarep.2019.102686","article-title":"Bon voyage: A transcriptional journey around DNA breaks","volume":"82","author":"Caron","year":"2019","journal-title":"DNA Repair (Amst.)"},{"key":"10.1016\/j.celrep.2021.108977_bib19","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1016\/j.cell.2015.07.042","article-title":"PAF1, a Molecular Regulator of Promoter-Proximal Pausing by RNA Polymerase II","volume":"162","author":"Chen","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib20","doi-asserted-by":"crossref","first-page":"24356","DOI":"10.1038\/srep24356","article-title":"CRISPR-Cas9(D10A) nickase-based genotypic and phenotypic screening to enhance genome editing","volume":"6","author":"Chiang","year":"2016","journal-title":"Sci. Rep."},{"key":"10.1016\/j.celrep.2021.108977_bib21","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1016\/j.cell.2014.05.038","article-title":"Mechanism of transcriptional bursting in bacteria","volume":"158","author":"Chong","year":"2014","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-1-4939-4035-6_1","article-title":"Cellular Fractionation and Isolation of Chromatin-Associated RNA","volume":"1468","author":"Conrad","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib23","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1101\/gad.325142.119","article-title":"Promoter-proximal pausing of RNA polymerase II: a nexus of gene regulation","volume":"33","author":"Core","year":"2019","journal-title":"Genes Dev."},{"key":"10.1016\/j.celrep.2021.108977_bib24","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.1126\/science.1162228","article-title":"Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters","volume":"322","author":"Core","year":"2008","journal-title":"Science"},{"key":"10.1016\/j.celrep.2021.108977_bib25","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1016\/j.celrep.2012.08.034","article-title":"Defining the status of RNA polymerase at promoters","volume":"2","author":"Core","year":"2012","journal-title":"Cell Rep."},{"key":"10.1016\/j.celrep.2021.108977_bib26","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s12551-016-0242-6","article-title":"Effects of DNA supercoiling on chromatin architecture","volume":"8","author":"Corless","year":"2016","journal-title":"Biophys. Rev."},{"key":"10.1016\/j.celrep.2021.108977_bib27","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.celrep.2021.108977_bib28","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1186\/s13059-016-0984-2","article-title":"Comprehensive analysis of promoter-proximal RNA polymerase II pausing across mammalian cell types","volume":"17","author":"Day","year":"2016","journal-title":"Genome Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib29","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1038\/s41588-019-0421-z","article-title":"Release of paused RNA polymerase II at specific loci favors DNA double-strand-break formation and promotes cancer translocations","volume":"51","author":"Dellino","year":"2019","journal-title":"Nat. Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib30","first-page":"2578","article-title":"In\u00a0vitro and intracellular inhibition of topoisomerase II by the antitumor agent merbarone","volume":"49","author":"Drake","year":"1989","journal-title":"Cancer Res."},{"key":"10.1016\/j.celrep.2021.108977_bib31","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1016\/j.molcel.2014.03.044","article-title":"How slow RNA polymerase II elongation favors alternative exon skipping","volume":"54","author":"Dujardin","year":"2014","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib32","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1038\/nature12146","article-title":"BAF complexes facilitate decatenation of DNA by topoisomerase II\u03b1","volume":"497","author":"Dykhuizen","year":"2013","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib104","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/nature11247","article-title":"An integrated encyclopedia of DNA elements in the human genome","volume":"489","year":"2012","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib33","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.15252\/embj.201488091","article-title":"Chromatin regulates DNA torsional energy via topoisomerase II-mediated relaxation of positive supercoils","volume":"33","author":"Fern\u00e1ndez","year":"2014","journal-title":"EMBO J."},{"key":"10.1016\/j.celrep.2021.108977_bib34","doi-asserted-by":"crossref","first-page":"17643","DOI":"10.1074\/jbc.273.28.17643","article-title":"Merbarone inhibits the catalytic activity of human topoisomerase IIalpha by blocking DNA cleavage","volume":"273","author":"Fortune","year":"1998","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2021.108977_bib35","doi-asserted-by":"crossref","first-page":"6170","DOI":"10.1093\/nar\/gkm669","article-title":"Tryptophane-205 of human topoisomerase I is essential for camptothecin inhibition of negative but not positive supercoil removal","volume":"35","author":"Fr\u00f8hlich","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib36","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.yexcr.2008.10.032","article-title":"Negative elongation factor NELF controls transcription of immediate early genes in a stimulus-specific manner","volume":"315","author":"Fujita","year":"2009","journal-title":"Exp. Cell Res."},{"key":"10.1016\/j.celrep.2021.108977_bib37","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1146\/annurev-biochem-060815-014908","article-title":"Transcription as a Threat to Genome Integrity","volume":"85","author":"Gaillard","year":"2016","journal-title":"Annu. Rev. Biochem."},{"key":"10.1016\/j.celrep.2021.108977_bib38","doi-asserted-by":"crossref","first-page":"1921","DOI":"10.1101\/gad.1643208","article-title":"NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly","volume":"22","author":"Gilchrist","year":"2008","journal-title":"Genes Dev."},{"key":"10.1016\/j.celrep.2021.108977_bib39","doi-asserted-by":"crossref","first-page":"4846","DOI":"10.1038\/s41467-019-12802-5","article-title":"A nucleotide resolution map of Top2-linked DNA breaks in the yeast and human genome","volume":"10","author":"Gittens","year":"2019","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib40","doi-asserted-by":"crossref","first-page":"e1003226","DOI":"10.1371\/journal.pgen.1003226","article-title":"TDP2-dependent non-homologous end-joining protects against topoisomerase II-induced DNA breaks and genome instability in cells and in\u00a0vivo","volume":"9","author":"G\u00f3mez-Herreros","year":"2013","journal-title":"PLoS Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib41","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.molcel.2019.05.015","article-title":"Spatial Chromosome Folding and Active Transcription Drive DNA Fragility and Formation of Oncogenic MLL Translocations","volume":"75","author":"Gothe","year":"2019","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib42","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1038\/311433a0","article-title":"Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene","volume":"311","author":"Greenberg","year":"1984","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib43","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.cell.2007.05.042","article-title":"A chromatin landmark and transcription initiation at most promoters in human cells","volume":"130","author":"Guenther","year":"2007","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib44","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1038\/ng.613","article-title":"Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements","volume":"42","author":"Haffner","year":"2010","journal-title":"Nat. Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib45","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1038\/nrm2549","article-title":"Transcription-coupled DNA repair: two decades of progress and surprises","volume":"9","author":"Hanawalt","year":"2008","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib46","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.pharmthera.2012.09.001","article-title":"Immediate early response genes and cell transformation","volume":"137","author":"Healy","year":"2013","journal-title":"Pharmacol. Ther."},{"key":"10.1016\/j.celrep.2021.108977_bib47","doi-asserted-by":"crossref","first-page":"1446","DOI":"10.1038\/emboj.2010.38","article-title":"High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome","volume":"29","author":"Iacovoni","year":"2010","journal-title":"EMBO J."},{"key":"10.1016\/j.celrep.2021.108977_bib48","doi-asserted-by":"crossref","first-page":"3068","DOI":"10.1093\/nar\/gkv149","article-title":"A positioned\u00a0+1 nucleosome enhances promoter-proximal pausing","volume":"43","author":"Jimeno-Gonz\u00e1lez","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib49","doi-asserted-by":"crossref","first-page":"7907","DOI":"10.1093\/nar\/gks626","article-title":"Topoisomerase II is required for the production of long Pol II gene transcripts in yeast","volume":"40","author":"Joshi","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib50","doi-asserted-by":"crossref","first-page":"1798","DOI":"10.1126\/science.1127196","article-title":"A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription","volume":"312","author":"Ju","year":"2006","journal-title":"Science"},{"key":"10.1016\/j.celrep.2021.108977_bib51","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1038\/s41467-019-13891-y","article-title":"Chromatin fibers stabilize nucleosomes under torsional stress","volume":"11","author":"Kaczmarczyk","year":"2020","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib52","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1038\/nature03877","article-title":"A high-resolution map of active promoters in the human genome","volume":"436","author":"Kim","year":"2005","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib53","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.cell.2019.08.033","article-title":"Long-Distance Cooperative and Antagonistic RNA Polymerase Dynamics via DNA Supercoiling","volume":"179","author":"Kim","year":"2019","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib54","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1038\/nature12504","article-title":"Topoisomerases facilitate transcription of long genes linked to autism","volume":"501","author":"King","year":"2013","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib55","doi-asserted-by":"crossref","first-page":"5678","DOI":"10.1093\/nar\/gkn550","article-title":"Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin","volume":"36","author":"Kinner","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib56","doi-asserted-by":"crossref","first-page":"1092","DOI":"10.1038\/nsmb848","article-title":"The dynamic response of upstream DNA to transcription-generated torsional stress","volume":"11","author":"Kouzine","year":"2004","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib57","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1038\/nsmb.1372","article-title":"The functional response of upstream DNA to dynamic supercoiling in\u00a0vivo","volume":"15","author":"Kouzine","year":"2008","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib58","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1038\/nsmb.2517","article-title":"Transcription-dependent dynamic supercoiling is a short-range genomic force","volume":"20","author":"Kouzine","year":"2013","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib59","doi-asserted-by":"crossref","first-page":"195","DOI":"10.4161\/nucl.28909","article-title":"DNA topology and transcription","volume":"5","author":"Kouzine","year":"2014","journal-title":"Nucleus"},{"key":"10.1016\/j.celrep.2021.108977_bib60","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1126\/science.1229386","article-title":"Precise maps of RNA polymerase reveal how promoters direct initiation and pausing","volume":"339","author":"Kwak","year":"2013","journal-title":"Science"},{"key":"10.1016\/j.celrep.2021.108977_bib61","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib62","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.gde.2011.01.010","article-title":"Promoter proximal pausing and the control of gene expression","volume":"21","author":"Li","year":"2011","journal-title":"Curr. Opin. Genet. Dev."},{"key":"10.1016\/j.celrep.2021.108977_bib63","doi-asserted-by":"crossref","first-page":"7024","DOI":"10.1073\/pnas.84.20.7024","article-title":"Supercoiling of the DNA template during transcription","volume":"84","author":"Liu","year":"1987","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2021.108977_bib64","doi-asserted-by":"crossref","first-page":"14883","DOI":"10.1073\/pnas.261477898","article-title":"DNA supercoiling allows enhancer action over a large distance","volume":"98","author":"Liu","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2021.108977_bib65","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib66","doi-asserted-by":"crossref","first-page":"7929","DOI":"10.1128\/MCB.00617-06","article-title":"Role of topoisomerase IIbeta in the expression of developmentally regulated genes","volume":"26","author":"Lyu","year":"2006","journal-title":"Mol. Cell. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib67","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s12551-016-0215-9","article-title":"DNA supercoiling during transcription","volume":"8","author":"Ma","year":"2016","journal-title":"Biophys. Rev."},{"key":"10.1016\/j.celrep.2021.108977_bib68","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.1126\/science.1235441","article-title":"Transcription under torsion","volume":"340","author":"Ma","year":"2013","journal-title":"Science"},{"key":"10.1016\/j.celrep.2021.108977_bib69","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.1016\/j.cell.2015.05.032","article-title":"Activity-Induced DNA Breaks Govern the Expression of Neuronal Early-Response Genes","volume":"161","author":"Madabhushi","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib70","series-title":"Bamsignals: Extract read count signals from bam files. R packag. version 1.16.0","author":"Mammana","year":"2019"},{"key":"10.1016\/j.celrep.2021.108977_bib71","doi-asserted-by":"crossref","first-page":"3797","DOI":"10.1242\/jcs.01225","article-title":"Visualization of unconstrained negative supercoils of DNA on polytene chromosomes of Drosophila","volume":"117","author":"Matsumoto","year":"2004","journal-title":"J.\u00a0Cell Sci."},{"key":"10.1016\/j.celrep.2021.108977_bib72","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1038\/35096590","article-title":"DNA topoisomerase IIalpha is required for RNA polymerase II transcription on chromatin templates","volume":"413","author":"Mondal","year":"2001","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2021.108977_bib73","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1038\/nsmb.2509","article-title":"Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures","volume":"20","author":"Naughton","year":"2013","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib74","first-page":"Unit 3.3","article-title":"Topoisomerase assays","volume":"Chapter 3","author":"Nitiss","year":"2012","journal-title":"Curr. Protoc. Pharmacol."},{"key":"10.1016\/j.celrep.2021.108977_bib75","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1038\/nsmb.2224","article-title":"DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks","volume":"19","author":"Pankotai","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib76","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/0092-8674(93)90140-L","article-title":"DNA topology and a minimal set of basal factors for transcription by RNA polymerase II","volume":"73","author":"Parvin","year":"1993","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib77","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.mrfmmm.2012.07.005","article-title":"The DNA topoisomerase II catalytic inhibitor merbarone is genotoxic and induces endoreduplication","volume":"738\u2013739","author":"Pastor","year":"2012","journal-title":"Mutat. Res."},{"key":"10.1016\/j.celrep.2021.108977_bib78","doi-asserted-by":"crossref","first-page":"e1003128","DOI":"10.1371\/journal.pgen.1003128","article-title":"DNA Topoisomerases maintain promoters in a state competent for transcriptional activation in Saccharomyces cerevisiae","volume":"8","author":"Pedersen","year":"2012","journal-title":"PLoS Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib79","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/nrm.2016.111","article-title":"Roles of eukaryotic topoisomerases in transcription, replication and genomic stability","volume":"17","author":"Pommier","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib107","series-title":"R: A language and environment for statistical computing","year":"2018"},{"key":"10.1016\/j.celrep.2021.108977_bib80","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1093\/nar\/gky1091","article-title":"Are TADs supercoiled?","volume":"47","author":"Racko","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib81","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1016\/j.cell.2010.03.030","article-title":"c-Myc regulates transcriptional pause release","volume":"141","author":"Rahl","year":"2010","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib82","doi-asserted-by":"crossref","first-page":"4776","DOI":"10.1073\/pnas.0307241101","article-title":"Promoter unwinding and promoter clearance by RNA polymerase: detection by single-molecule DNA nanomanipulation","volume":"101","author":"Revyakin","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2021.108977_bib83","first-page":"Unit 4.21","article-title":"Production and titration of lentiviral vectors","volume":"Chapter 4","author":"Salmon","year":"2006","journal-title":"Curr. Protoc. Neurosci."},{"key":"10.1016\/j.celrep.2021.108977_bib84","doi-asserted-by":"crossref","first-page":"1756","DOI":"10.1093\/nar\/gkx1225","article-title":"Genome-wide dose-dependent inhibition of histone deacetylases studies reveal their roles in enhancer remodeling and suppression of oncogenic super-enhancers","volume":"46","author":"Sanchez","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.celrep.2021.108977_bib106","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1038\/nmeth.3047","article-title":"Improved vectors and genome-wide libraries for CRISPR screening","volume":"11","author":"Sanjana","year":"2014","journal-title":"Nat. Methods"},{"key":"10.1016\/j.celrep.2021.108977_bib85","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.molcel.2014.08.023","article-title":"Enhancer RNA facilitates NELF release from immediate early genes","volume":"56","author":"Schaukowitch","year":"2014","journal-title":"Mol. Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib86","doi-asserted-by":"crossref","first-page":"1412","DOI":"10.1126\/science.aam6468","article-title":"ZATT (ZNF451)-mediated resolution of topoisomerase 2 DNA-protein cross-links","volume":"357","author":"Schellenberg","year":"2017","journal-title":"Science"},{"key":"10.1016\/j.celrep.2021.108977_bib87","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1038\/nmeth.3542","article-title":"ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors","volume":"12","author":"Schmidl","year":"2015","journal-title":"Nat. Methods"},{"key":"10.1016\/j.celrep.2021.108977_bib88","doi-asserted-by":"crossref","first-page":"e53447","DOI":"10.7554\/eLife.53447","article-title":"Suppressing proteasome mediated processing of topoisomerase II DNA-protein complexes preserves genome integrity","volume":"9","author":"Sciascia","year":"2020","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2021.108977_bib89","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1016\/j.cell.2010.04.038","article-title":"ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks","volume":"141","author":"Shanbhag","year":"2010","journal-title":"Cell"},{"key":"10.1016\/j.celrep.2021.108977_bib90","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1038\/ng.3867","article-title":"Paused RNA polymerase II inhibits new transcriptional initiation","volume":"49","author":"Shao","year":"2017","journal-title":"Nat. Genet."},{"key":"10.1016\/j.celrep.2021.108977_bib91","doi-asserted-by":"crossref","first-page":"12693","DOI":"10.1073\/pnas.1106834108","article-title":"Topoisomerase II binds nucleosome-free DNA and acts redundantly with topoisomerase I to enhance recruitment of RNA Pol II in budding yeast","volume":"108","author":"Sperling","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2021.108977_bib92","first-page":"2097","article-title":"Analysis of topoisomerase I\/DNA complexes in patients administered topotecan","volume":"55","author":"Subramanian","year":"1995","journal-title":"Cancer Res."},{"key":"10.1016\/j.celrep.2021.108977_bib94","doi-asserted-by":"crossref","first-page":"102837","DOI":"10.1016\/j.dnarep.2020.102837","article-title":"Excision repair of topoisomerase DNA-protein crosslinks (TOP-DPC)","volume":"89","author":"Sun","year":"2020","journal-title":"DNA Repair (Amst.)"},{"key":"10.1016\/j.celrep.2021.108977_bib95","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1006\/bbrc.1993.1576","article-title":"Underwinding of DNA on binding of yeast TFIID to the TATA element","volume":"192","author":"Tabuchi","year":"1993","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib96","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nsmb.2723","article-title":"Transcription-generated torsional stress destabilizes nucleosomes","volume":"21","author":"Teves","year":"2014","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1016\/j.celrep.2021.108977_bib97","doi-asserted-by":"crossref","first-page":"2478","DOI":"10.1038\/ncomms3478","article-title":"Gene regulation and priming by topoisomerase II\u03b1 in embryonic stem cells","volume":"4","author":"Thakurela","year":"2013","journal-title":"Nat. Commun."},{"key":"10.1016\/j.celrep.2021.108977_bib98","doi-asserted-by":"crossref","first-page":"E934","DOI":"10.1073\/pnas.1119798109","article-title":"Target genes of Topoisomerase II\u03b2 regulate neuronal survival and are defined by their chromatin state","volume":"109","author":"Tiwari","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2021.108977_bib99","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.bbagrm.2012.11.007","article-title":"Transcription elongation factors DSIF and NELF: promoter-proximal pausing and beyond","volume":"1829","author":"Yamaguchi","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"10.1016\/j.celrep.2021.108977_bib100","doi-asserted-by":"crossref","first-page":"6332","DOI":"10.1021\/bi00417a020","article-title":"Alkali reversal of psoralen cross-link for the targeted delivery of psoralen monoadduct lesion","volume":"27","author":"Yeung","year":"1988","journal-title":"Biochemistry"},{"key":"10.1016\/j.celrep.2021.108977_bib101","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1101\/gr.211615.116","article-title":"Genome-wide TOP2A DNA cleavage is biased toward translocated and highly transcribed loci","volume":"27","author":"Yu","year":"2017","journal-title":"Genome Res."},{"key":"10.1016\/j.celrep.2021.108977_bib102","doi-asserted-by":"crossref","first-page":"35997","DOI":"10.1074\/jbc.M604149200","article-title":"A protease pathway for the repair of topoisomerase II-DNA covalent complexes","volume":"281","author":"Zhang","year":"2006","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1016\/j.celrep.2021.108977_bib103","doi-asserted-by":"crossref","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","article-title":"Model-based analysis of ChIP-Seq (MACS)","volume":"9","author":"Zhang","year":"2008","journal-title":"Genome Biol."}],"container-title":["Cell Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124721002916?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2211124721002916?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T11:17:00Z","timestamp":1761909420000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2211124721002916"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4]]},"references-count":106,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2021,4]]}},"alternative-id":["S2211124721002916"],"URL":"https:\/\/doi.org\/10.1016\/j.celrep.2021.108977","relation":{},"ISSN":["2211-1247"],"issn-type":[{"value":"2211-1247","type":"print"}],"subject":[],"published":{"date-parts":[[2021,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Topoisomerase II\u03b1 represses transcription by enforcing promoter-proximal pausing","name":"articletitle","label":"Article Title"},{"value":"Cell Reports","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.celrep.2021.108977","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 The Authors.","name":"copyright","label":"Copyright"}],"article-number":"108977"}}