{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T10:29:53Z","timestamp":1780396193329,"version":"3.54.1"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,6,29]],"date-time":"2021-06-29T00:00:00Z","timestamp":1624924800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,29]],"date-time":"2021-06-29T00:00:00Z","timestamp":1624924800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000011","name":"Howard Hughes Medical Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Epigenetics &amp; Chromatin"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Drosophila\u00a0<\/jats:italic>\n                      dosage compensation is an important model system for defining how active chromatin domains are formed. The male-specific lethal dosage compensation complex (MSLc) increases transcript levels of genes along the length of the single male X-chromosome to equalize with that expressed from the two female X-chromosomes. The strongest binding sites for MSLc cluster together in three-dimensional space largely independent of MSLc because clustering occurs in both sexes. CLAMP, a non-sex specific, ubiquitous zinc finger protein, binds synergistically with MSLc to enrich the occupancy of both factors on the male X-chromosome.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Here, we demonstrate that CLAMP promotes the observed three-dimensional clustering of MSLc binding sites. Moreover, the X-enriched CLAMP protein more strongly promotes longer-range three-dimensional interactions on the X-chromosome than autosomes. Genome-wide, CLAMP promotes three-dimensional interactions between active chromatin regions together with other insulator proteins.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Overall, we define how long-range interactions which are modulated by a locally enriched ubiquitous transcription factor promote hyper-activation of the X-chromosome to mediate dosage compensation.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s13072-021-00399-3","type":"journal-article","created":{"date-parts":[[2021,6,29]],"date-time":"2021-06-29T07:02:44Z","timestamp":1624950164000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["The zinc finger protein CLAMP promotes long-range chromatin interactions that mediate dosage compensation of the Drosophila male X-chromosome"],"prefix":"10.1186","volume":"14","author":[{"suffix":"III","given":"William","family":"Jordan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2484-4921","authenticated-orcid":false,"given":"Erica","family":"Larschan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,6,29]]},"reference":[{"key":"399_CR1","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1038\/nature22989","volume":"547","author":"AR Strom","year":"2017","unstructured":"Strom AR, et al. Phase separation drives heterochromatin domain formation. Nature. 2017;547:241\u20135.","journal-title":"Nature"},{"key":"399_CR2","doi-asserted-by":"publisher","first-page":"1049","DOI":"10.1016\/j.cell.2015.02.040","volume":"160","author":"T Sexton","year":"2015","unstructured":"Sexton T, Cavalli G. The role of chromosome domains in shaping the functional genome. Cell. 2015;160:1049\u201359.","journal-title":"Cell"},{"key":"399_CR3","doi-asserted-by":"publisher","first-page":"1272","DOI":"10.1038\/s41588-019-0462-3","volume":"51","author":"Y Ghavi-Helm","year":"2019","unstructured":"Ghavi-Helm Y, et al. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat Genet. 2019;51:1272\u201382.","journal-title":"Nat Genet"},{"key":"399_CR4","doi-asserted-by":"publisher","first-page":"2289","DOI":"10.1101\/gad.1343705","volume":"19","author":"FN Hamada","year":"2005","unstructured":"Hamada FN, Park PJ, Gordadze PR, Kuroda MI. Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev. 2005;19:2289\u201394.","journal-title":"Genes Dev"},{"key":"399_CR5","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1016\/j.devcel.2011.12.016","volume":"22","author":"T Conrad","year":"2012","unstructured":"Conrad T, et al. The MOF chromobarrel domain controls genome-wide H4K16 acetylation and spreading of the MSL complex. Dev Cell. 2012;22:610\u201324.","journal-title":"Dev Cell"},{"key":"399_CR6","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1038\/nrg2013","volume":"8","author":"T Straub","year":"2007","unstructured":"Straub T, Becker PB. Dosage compensation: the beginning and end of generalization. Nat Rev Genet. 2007;8:47\u201357.","journal-title":"Nat Rev Genet"},{"key":"399_CR7","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1016\/j.tig.2019.02.001","volume":"35","author":"W Jordan","year":"2019","unstructured":"Jordan W, Rieder LE, Larschan E. Diverse genome topologies characterize dosage compensation across species. Trends Genet. 2019;35:308\u201315.","journal-title":"Trends Genet"},{"key":"399_CR8","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1093\/genetics\/96.1.165","volume":"96","author":"JM Belote","year":"1980","unstructured":"Belote JM, Lucchesi JC. Male-specific lethal mutations of Drosophila melanogaster. Genetics. 1980;96:165\u201386.","journal-title":"Genetics"},{"key":"399_CR9","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1002\/bies.950180705","volume":"18","author":"JC Lucchesi","year":"1996","unstructured":"Lucchesi JC. Dosage compensation in Drosophila and the \u2018complex\u2019 world of transcriptional regulation. BioEssays. 1996;18:541\u20137.","journal-title":"BioEssays"},{"key":"399_CR10","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1016\/0092-8674(91)90439-6","volume":"66","author":"MI Kuroda","year":"1991","unstructured":"Kuroda MI, Kernan MJ, Kreber R, Ganetzky B, Baker BS. The maleless protein associates with the X chromosome to regulate dosage compensation in drosophila. Cell. 1991;66:935\u201347.","journal-title":"Cell"},{"key":"399_CR11","doi-asserted-by":"publisher","first-page":"2054","DOI":"10.1093\/emboj\/16.8.2054","volume":"16","author":"A Hilfiker","year":"1997","unstructured":"Hilfiker A, Hilfiker-Kleiner D, Pannuti A, Lucchesi JC. mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J. 1997;16:2054\u201360.","journal-title":"EMBO J"},{"key":"399_CR12","doi-asserted-by":"publisher","first-page":"1084","DOI":"10.1093\/emboj\/21.5.1084","volume":"21","author":"VH Meller","year":"2002","unstructured":"Meller VH, Rattner BP. The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J. 2002;21:1084\u201391.","journal-title":"EMBO J"},{"key":"399_CR13","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/S1097-2765(00)80193-8","volume":"4","author":"A Franke","year":"1999","unstructured":"Franke A, Baker BS. The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol Cell. 1999;4:117\u201322.","journal-title":"Mol Cell"},{"key":"399_CR14","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1016\/j.cell.2008.06.033","volume":"134","author":"AA Alekseyenko","year":"2008","unstructured":"Alekseyenko AA, et al. A sequence motif within chromatin entry sites directs MSL establishment on the drosophila X chromosome. Cell. 2008;134:599\u2013609.","journal-title":"Cell"},{"key":"399_CR15","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1016\/S0092-8674(00)81979-0","volume":"98","author":"RL Kelley","year":"1999","unstructured":"Kelley RL, et al. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell. 1999;98:513\u201322.","journal-title":"Cell"},{"key":"399_CR16","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pgen.1000302","volume":"4","author":"T Straub","year":"2008","unstructured":"Straub T, Grimaud C, Gilfillan GD, Mitterweger A, Becker PB. The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet. 2008;4:1\u201314.","journal-title":"PLoS Genet"},{"key":"399_CR17","doi-asserted-by":"publisher","first-page":"e3000094","DOI":"10.1371\/journal.pbio.3000094","volume":"17","author":"C Ellison","year":"2019","unstructured":"Ellison C, Bachtrog D. Contingency in the convergent evolution of a regulatory network: dosage compensation in drosophila. PLoS Biol. 2019;17:e3000094.","journal-title":"PLoS Biol"},{"key":"399_CR18","doi-asserted-by":"publisher","first-page":"e1006120","DOI":"10.1371\/journal.pgen.1006120","volume":"12","author":"G Kuzu","year":"2016","unstructured":"Kuzu G, et al. Expansion of GA dinucleotide repeats increases the density of CLAMP binding sites on the X-chromosome to promote Drosophila dosage compensation. PLoS Genet. 2016;12:e1006120.","journal-title":"PLoS Genet"},{"key":"399_CR19","doi-asserted-by":"publisher","first-page":"e1002830","DOI":"10.1371\/journal.pgen.1002830","volume":"8","author":"E Larschan","year":"2012","unstructured":"Larschan E, et al. Identification of chromatin-associated regulators of MSL complex targeting in Drosophila dosage compensation. PLoS Genet. 2012;8:e1002830.","journal-title":"PLoS Genet"},{"key":"399_CR20","doi-asserted-by":"publisher","first-page":"1551","DOI":"10.1101\/gad.214585.113","volume":"27","author":"MML Soruco","year":"2013","unstructured":"Soruco MML, et al. The CLAMP protein links the MSL complex to the X chromosome during Drosophila dosage compensation. Genes Dev. 2013;27:1551\u20136.","journal-title":"Genes Dev"},{"key":"399_CR21","doi-asserted-by":"publisher","first-page":"1706","DOI":"10.1093\/nar\/gky1238","volume":"47","author":"C Albig","year":"2019","unstructured":"Albig C, et al. Factor cooperation for chromosome discrimination in Drosophila. Nucleic Acids Res. 2019;47:1706\u201324.","journal-title":"Nucleic Acids Res"},{"key":"399_CR22","doi-asserted-by":"publisher","first-page":"1494","DOI":"10.1101\/gad.300855.117","volume":"31","author":"LE Rieder","year":"2017","unstructured":"Rieder LE, et al. Histone locus regulation by the Drosophila dosage compensation adaptor protein CLAMP. Genes Dev. 2017;31:1494\u2013508.","journal-title":"Genes Dev"},{"key":"399_CR23","doi-asserted-by":"publisher","first-page":"2751","DOI":"10.1242\/dev.122.9.2751","volume":"122","author":"A Franke","year":"1996","unstructured":"Franke A, Dernburg A, Bashaw GJ, Baker BS. Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development. 1996;122:2751\u201360.","journal-title":"Development"},{"key":"399_CR24","doi-asserted-by":"publisher","first-page":"e1000590","DOI":"10.1371\/journal.pbio.1000590","volume":"9","author":"SE Lott","year":"2011","unstructured":"Lott SE, et al. Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-Seq. PLoS Biol. 2011;9:e1000590.","journal-title":"PLoS Biol"},{"key":"399_CR25","doi-asserted-by":"publisher","first-page":"e0186855","DOI":"10.1371\/journal.pone.0186855","volume":"12","author":"J Urban","year":"2017","unstructured":"Urban J, et al. Enhanced chromatin accessibility of the dosage compensated Drosophila male X-chromosome requires the CLAMP zinc finger protein. PLoS ONE. 2017;12:e0186855.","journal-title":"PLoS ONE"},{"key":"399_CR26","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1101\/gad.1400206","volume":"20","author":"AA Alekseyenko","year":"2006","unstructured":"Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI. High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev. 2006;20:848\u201357.","journal-title":"Genes Dev"},{"key":"399_CR27","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1038\/nature09757","volume":"471","author":"E Larschan","year":"2011","unstructured":"Larschan E, et al. X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature. 2011;471:115\u20138.","journal-title":"Nature"},{"key":"399_CR28","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1016\/j.molcel.2015.08.024","volume":"60","author":"F Ram\u00edrez","year":"2015","unstructured":"Ram\u00edrez F, et al. High-affinity sites form an interaction network to facilitate spreading of the MSL complex across the X chromosome in Drosophila. Mol Cell. 2015;60:146\u201362.","journal-title":"Mol Cell"},{"key":"399_CR29","doi-asserted-by":"publisher","first-page":"1854","DOI":"10.15252\/embr.201744292","volume":"18","author":"T Schauer","year":"2017","unstructured":"Schauer T, et al. Chromosome topology guides the Drosophila Dosage Compensation Complex for target gene activation. EMBO Rep. 2017;18:1854\u201368.","journal-title":"EMBO Rep"},{"key":"399_CR30","doi-asserted-by":"publisher","first-page":"jcs-226092","DOI":"10.1242\/jcs.226092","volume":"132","author":"I Bag","year":"2019","unstructured":"Bag I, Dale RK, Palmer C, Lei EP. The zinc-finger protein CLAMP promotes gypsy chromatin insulator function in Drosophila. J Cell Sci. 2019;132:jcs-226092.","journal-title":"J Cell Sci"},{"key":"399_CR31","doi-asserted-by":"publisher","first-page":"E4504","DOI":"10.1073\/pnas.1609643113","volume":"113","author":"EM Darrow","year":"2016","unstructured":"Darrow EM, et al. Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture. Proc Natl Acad Sci USA. 2016;113:E4504\u201312.","journal-title":"Proc Natl Acad Sci USA"},{"key":"399_CR32","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1016\/j.molcel.2017.07.013","volume":"67","author":"KR Kieffer-Kwon","year":"2017","unstructured":"Kieffer-Kwon KR, et al. Myc regulates chromatin decompaction and nuclear architecture during B cell activation. Mol Cell. 2017;67:566-578.e10.","journal-title":"Mol Cell"},{"key":"399_CR33","doi-asserted-by":"publisher","first-page":"1333","DOI":"10.1093\/genetics\/153.3.1333","volume":"153","author":"M Muller","year":"1999","unstructured":"Muller M, Hagstrom K, Gyurkovics H, Pirrotta V, Schedl P. The Mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions. Genetics. 1999;153:1333\u201356.","journal-title":"Genetics"},{"key":"399_CR34","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1126\/science.1207194","volume":"334","author":"D Noordermeer","year":"2011","unstructured":"Noordermeer D, et al. The dynamic architecture of Hox gene clusters. Science (80-). 2011;334:222\u20135.","journal-title":"Science (80-)"},{"key":"399_CR35","doi-asserted-by":"publisher","first-page":"1165","DOI":"10.1016\/j.cell.2018.03.072","volume":"173","author":"L Vian","year":"2018","unstructured":"Vian L, et al. The energetics and physiological impact of cohesin extrusion. Cell. 2018;173:1165-1178.e20.","journal-title":"Cell"},{"key":"399_CR36","doi-asserted-by":"publisher","first-page":"1665","DOI":"10.1016\/j.cell.2014.11.021","volume":"159","author":"SSP Rao","year":"2014","unstructured":"Rao SSP, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159:1665\u201380.","journal-title":"Cell"},{"key":"399_CR37","first-page":"353","volume":"27","author":"I Schneider","year":"1972","unstructured":"Schneider I. Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol. 1972;27:353\u201365.","journal-title":"J Embryol Exp Morphol"},{"key":"399_CR38","doi-asserted-by":"publisher","first-page":"2701","DOI":"10.1093\/bioinformatics\/bty164","volume":"34","author":"O Ursu","year":"2018","unstructured":"Ursu O, et al. GenomeDISCO: a concordance score for chromosome conformation capture experiments using random walks on contact map graphs. Bioinformatics. 2018;34:2701\u20137.","journal-title":"Bioinformatics"},{"key":"399_CR39","doi-asserted-by":"publisher","first-page":"1522","DOI":"10.1016\/j.cell.2018.07.047","volume":"174","author":"S Heinz","year":"2018","unstructured":"Heinz S, et al. Transcription elongation can affect genome 3D structure. Cell. 2018;174:1522-1536.e22.","journal-title":"Cell"},{"key":"399_CR40","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1101\/gr.160374.113","volume":"24","author":"F Ay","year":"2014","unstructured":"Ay F, Bailey TL, Noble WS. Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts. Genome Res. 2014;24:999\u20131011.","journal-title":"Genome Res"},{"key":"399_CR41","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1186\/s12859-015-0683-0","volume":"16","author":"ATL Lun","year":"2015","unstructured":"Lun ATL, Smyth GK. diffHic: a bioconductor package to detect differential genomic interactions in Hi-C data. BMC Bioinform. 2015;16:258.","journal-title":"BMC Bioinform"},{"key":"399_CR42","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2009","unstructured":"Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26:139\u201340.","journal-title":"Bioinformatics"},{"key":"399_CR43","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1038\/nature09725","volume":"471","author":"PV Kharchenko","year":"2011","unstructured":"Kharchenko PV, et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature. 2011;471:480\u20135.","journal-title":"Nature"},{"key":"399_CR44","doi-asserted-by":"publisher","first-page":"3227","DOI":"10.1016\/j.celrep.2018.02.098","volume":"22","author":"EG Kaye","year":"2018","unstructured":"Kaye EG, et al. Differential occupancy of two GA-binding proteins promotes targeting of the drosophila dosage compensation complex to the male X chromosome. Cell Rep. 2018;22:3227\u201339.","journal-title":"Cell Rep"},{"issue":"1","key":"399_CR45","doi-asserted-by":"publisher","first-page":"11.12.1","DOI":"10.1002\/0471250953.bi1112s47","volume":"47","author":"AR Quinlan","year":"2014","unstructured":"Quinlan AR. BEDTools: The Swiss-Army tool for genome feature analysis. Curr Protoc Bioinforma. 2014;47(1):11.12.1-11.12.34.","journal-title":"Curr Protoc Bioinforma"},{"key":"399_CR46","doi-asserted-by":"publisher","first-page":"2490","DOI":"10.1101\/gad.539509","volume":"23","author":"C Grimaud","year":"2009","unstructured":"Grimaud C, Becker PB. The dosage compensation complex shapes the conformation of the X chromosome in Drosophila. Genes Dev. 2009;23:2490\u20135.","journal-title":"Genes Dev"},{"key":"399_CR47","doi-asserted-by":"publisher","first-page":"806","DOI":"10.1038\/371806a0","volume":"371","author":"G Farkas","year":"1994","unstructured":"Farkas G, et al. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994;371:806\u20138.","journal-title":"Nature"},{"key":"399_CR48","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/nmeth.2766","volume":"11","author":"S Kasinathan","year":"2014","unstructured":"Kasinathan S, Orsi GA, Zentner GE, Ahmad K, Henikoff S. High-resolution mapping of transcription factor binding sites on native chromatin. Nat Methods. 2014;11:203\u20139.","journal-title":"Nat Methods"},{"key":"399_CR49","doi-asserted-by":"publisher","first-page":"MCB-00253","DOI":"10.1128\/MCB.00253-17","volume":"37","author":"EG Kaye","year":"2017","unstructured":"Kaye EG, et al. Drosophila dosage compensation loci associate with a boundary-forming insulator complex. Mol Cell Biol. 2017;37:MCB-00253.","journal-title":"Mol Cell Biol"},{"key":"399_CR50","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1534\/genetics.166.1.279","volume":"166","author":"AJ Greenberg","year":"2004","unstructured":"Greenberg AJ, Yanowitz JL, Schedl P. The Drosophila GAGA factor is required for dosage compensation in males and for the formation of the male-specific-lethal complex chromatin entry site at 12DE. Genetics. 2004;166:279\u201389.","journal-title":"Genetics"},{"key":"399_CR51","doi-asserted-by":"publisher","first-page":"e1004780","DOI":"10.1371\/journal.pcbi.1004780","volume":"12","author":"R Raviram","year":"2016","unstructured":"Raviram R, et al. 4C-ker: a method to reproducibly identify genome-wide interactions captured by 4C-seq experiments. PLoS Comput Biol. 2016;12:e1004780.","journal-title":"PLoS Comput Biol"},{"key":"399_CR52","doi-asserted-by":"publisher","first-page":"3563","DOI":"10.1093\/nar\/gkt067","volume":"41","author":"AA Gavrilov","year":"2013","unstructured":"Gavrilov AA, et al. Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub. Nucleic Acids Res. 2013;41:3563\u201375.","journal-title":"Nucleic Acids Res"},{"key":"399_CR53","doi-asserted-by":"publisher","first-page":"969","DOI":"10.1038\/nmeth.2173","volume":"9","author":"HJG Van De Werken","year":"2012","unstructured":"Van De Werken HJG, et al. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat Methods. 2012;9:969\u201372.","journal-title":"Nat Methods"},{"key":"399_CR54","doi-asserted-by":"publisher","first-page":"e0189772","DOI":"10.1371\/journal.pone.0189772","volume":"12","author":"JA Urban","year":"2017","unstructured":"Urban JA, Urban JM, Kuzu G, Larschan EN. The Drosophila CLAMP protein associates with diverse proteins on chromatin. PLoS ONE. 2017;12:e0189772.","journal-title":"PLoS ONE"},{"key":"399_CR55","doi-asserted-by":"publisher","first-page":"e1005108","DOI":"10.1371\/journal.pgen.1005108","volume":"11","author":"NJ Fuda","year":"2015","unstructured":"Fuda NJ, et al. GAGA factor maintains nucleosome-free regions and has a role in rna polymerase II recruitment to promoters. PLOS Genet. 2015;11:e1005108.","journal-title":"PLOS Genet"},{"key":"399_CR56","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/meth.2001.1262","volume":"25","author":"KJ Livak","year":"2001","unstructured":"Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-\u0394\u0394CT method. Methods. 2001;25:402\u20138.","journal-title":"Methods"},{"key":"399_CR57","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1038\/nature13417","volume":"512","author":"Y Ghavi-Helm","year":"2014","unstructured":"Ghavi-Helm Y, et al. Enhancer loops appear stable during development and are associated with paused polymerase. Nature. 2014;512:96\u2013100.","journal-title":"Nature"},{"key":"399_CR58","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1101\/gr.185579.114","volume":"25","author":"RA Hoskins","year":"2015","unstructured":"Hoskins RA, et al. The Release 6 reference sequence of the Drosophila melanogaster genome. Genome Res. 2015;25:445\u201358.","journal-title":"Genome Res"},{"key":"399_CR59","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1186\/s13059-015-0831-x","volume":"16","author":"N Servant","year":"2015","unstructured":"Servant N, et al. HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Genome Biol. 2015;16:259.","journal-title":"Genome Biol"},{"key":"399_CR60","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.cels.2015.07.012","volume":"3","author":"NC Durand","year":"2016","unstructured":"Durand NC, et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 2016;3:99\u2013101.","journal-title":"Cell Syst"},{"key":"399_CR61","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1016\/j.molcel.2010.05.004","volume":"38","author":"S Heinz","year":"2010","unstructured":"Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576\u201389.","journal-title":"Mol Cell"},{"key":"399_CR62","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"9","author":"B Langmead","year":"2012","unstructured":"Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357\u20139.","journal-title":"Nat Methods"},{"key":"399_CR63","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.","journal-title":"Genome Biol"},{"key":"399_CR64","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1093\/bib\/bbs017","volume":"14","author":"H Thorvaldsd\u00f3ttir","year":"2013","unstructured":"Thorvaldsd\u00f3ttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): High-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178\u201392.","journal-title":"Brief Bioinform"},{"key":"399_CR65","first-page":"1787","volume":"330","author":"S Roy","year":"2016","unstructured":"Roy S, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science (80\u2013). 2016;330:1787\u201397.","journal-title":"Science (80\u2013)"},{"key":"399_CR66","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1101\/gr.229102","volume":"12","author":"WJ Kent","year":"2002","unstructured":"Kent WJ, et al. The human genome browser at UCSC. Genome Res. 2002;12:996\u20131006.","journal-title":"Genome Res"},{"key":"399_CR67","first-page":"11.10.1","volume":"43","author":"GA VanderAuwera","year":"2013","unstructured":"VanderAuwera GA, et al. From fastQ data to high-confidence variant calls: The genome analysis toolkit best practices pipeline. Curr Protocols in Bioinform. 2013;43:11.10.1-11.10.33.","journal-title":"Curr Protocols in Bioinform"},{"key":"399_CR68","doi-asserted-by":"publisher","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","volume":"25","author":"H Li","year":"2009","unstructured":"Li H, et al. The Sequence Alignment\/Map format and SAMtools. Bioinformatics. 2009;25:2078\u20139.","journal-title":"Bioinformatics"},{"key":"399_CR69","doi-asserted-by":"publisher","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","volume":"9","author":"Y Zhang","year":"2008","unstructured":"Zhang Y, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9:R137.","journal-title":"Genome Biol"},{"key":"399_CR70","doi-asserted-by":"publisher","first-page":"1752","DOI":"10.1214\/11-AOAS466","volume":"5","author":"Q Li","year":"2011","unstructured":"Li Q, Brown JB, Huang H, Bickel PJ. Measuring reproducibility of high-throughput experiments. Ann Appl Stat. 2011;5:1752\u201379.","journal-title":"Ann Appl Stat"},{"key":"399_CR71","doi-asserted-by":"publisher","first-page":"2204","DOI":"10.1093\/bioinformatics\/btq351","volume":"26","author":"WJ Kent","year":"2010","unstructured":"Kent WJ, Zweig AS, Barber G, Hinrichs AS, Karolchik D. BigWig and BigBed: Enabling browsing of large distributed datasets. Bioinformatics. 2010;26:2204\u20137.","journal-title":"Bioinformatics"},{"key":"399_CR72","doi-asserted-by":"publisher","first-page":"W187","DOI":"10.1093\/nar\/gku365","volume":"42","author":"F Ram\u00edrez","year":"2014","unstructured":"Ram\u00edrez F, D\u00fcndar F, Diehl S, Gr\u00fcning BA, Manke T. DeepTools: A flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 2014;42:W187\u201391.","journal-title":"Nucleic Acids Res"}],"container-title":["Epigenetics &amp; Chromatin"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13072-021-00399-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13072-021-00399-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13072-021-00399-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,4]],"date-time":"2023-02-04T09:07:40Z","timestamp":1675501660000},"score":1,"resource":{"primary":{"URL":"https:\/\/epigeneticsandchromatin.biomedcentral.com\/articles\/10.1186\/s13072-021-00399-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,29]]},"references-count":72,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["399"],"URL":"https:\/\/doi.org\/10.1186\/s13072-021-00399-3","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.11.02.365122","asserted-by":"object"}]},"ISSN":["1756-8935"],"issn-type":[{"value":"1756-8935","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,29]]},"assertion":[{"value":"13 January 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Both authors consent for this work to be published.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"We declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"29"}}