{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T12:10:46Z","timestamp":1790770246305,"version":"4.1.0"},"reference-count":64,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,2,22]],"date-time":"2020-02-22T00:00:00Z","timestamp":1582329600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,2,22]],"date-time":"2020-02-22T00:00:00Z","timestamp":1582329600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001843","name":"Science and Engineering Research Board","doi-asserted-by":"publisher","award":["EMR\/2015\/001681"],"award-info":[{"award-number":["EMR\/2015\/001681"]}],"id":[{"id":"10.13039\/501100001843","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001407","name":"Department of Biotechnology , Ministry of Science and Technology","doi-asserted-by":"publisher","award":["BT\/PR16366\/BID\/7\/598\/2016"],"award-info":[{"award-number":["BT\/PR16366\/BID\/7\/598\/2016"]}],"id":[{"id":"10.13039\/501100001407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001407","name":"Department of Biotechnology , Ministry of Science and Technology","doi-asserted-by":"publisher","award":["BT\/PR13596\/GET\/119\/31\/2015"],"award-info":[{"award-number":["BT\/PR13596\/GET\/119\/31\/2015"]}],"id":[{"id":"10.13039\/501100001407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001407","name":"Department of Biotechnology , Ministry of Science and Technology","doi-asserted-by":"publisher","award":["BT\/PR8688\/AGR\/36\/755\/2013"],"award-info":[{"award-number":["BT\/PR8688\/AGR\/36\/755\/2013"]}],"id":[{"id":"10.13039\/501100001407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001411","name":"Indian Council of Medical Research","doi-asserted-by":"publisher","award":["F.No.90\/09\/2012\/SCRT(TF)\/BMS"],"award-info":[{"award-number":["F.No.90\/09\/2012\/SCRT(TF)\/BMS"]}],"id":[{"id":"10.13039\/501100001411","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Genomics"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Proximity ligation based techniques, like Hi-C, involve restriction digestion followed by ligation of formaldehyde cross-linked chromatin. Distinct chromatin states can impact the restriction digestion, and hence the visibility in the contact maps, of engaged loci. Yet, the extent and the potential impact of digestion bias remain obscure and under-appreciated in the literature.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Through analysis of 45 Hi-C datasets, lamina-associated domains (LADs), inactive X-chromosome in mammals, and polytene bands in fly, we first established that the DNA in condensed chromatin had lesser accessibility to restriction endonucleases used in Hi-C as compared to that in decondensed chromatin. The observed bias was independent of known systematic biases, was not appropriately corrected by existing computational methods, and needed an additional optimization step. We then repurposed this bias to identify novel condensed domains outside LADs, which were bordered by insulators and were dynamically associated with the polycomb mediated epigenetic and transcriptional states during development.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>Our observations suggest that the corrected one-dimensional read counts of existing Hi-C datasets can be reliably repurposed to study the gene-regulatory dynamics associated with chromatin condensation and decondensation, and that the existing Hi-C datasets should be interpreted with cautions.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12864-020-6580-6","type":"journal-article","created":{"date-parts":[[2020,2,22]],"date-time":"2020-02-22T14:02:39Z","timestamp":1582380159000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Biased visibility in Hi-C datasets marks dynamically regulated condensed and decondensed chromatin states genome-wide"],"prefix":"10.1186","volume":"21","author":[{"given":"Keerthivasan Raanin","family":"Chandradoss","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prashanth Kumar","family":"Guthikonda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Srinivas","family":"Kethavath","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monika","family":"Dass","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Harpreet","family":"Singh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rakhee","family":"Nayak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sreenivasulu","family":"Kurukuti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7632-6339","authenticated-orcid":false,"given":"Kuljeet Singh","family":"Sandhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,2,22]]},"reference":[{"key":"6580_CR1","doi-asserted-by":"publisher","first-page":"772","DOI":"10.1038\/nrg.2016.147","volume":"17","author":"B Bonev","year":"2016","unstructured":"Bonev B, Cavalli G. Organization and function of the 3D genome. Nat Rev Genet. 2016;17:772.","journal-title":"Nat Rev Genet"},{"key":"6580_CR2","doi-asserted-by":"publisher","first-page":"1238","DOI":"10.1126\/science.1259587","volume":"346","author":"P Therizols","year":"2014","unstructured":"Therizols P, Illingworth RS, Courilleau C, Boyle S, Wood AJ, Bickmore WA. Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science. 2014;346:1238\u201342.","journal-title":"Science"},{"key":"6580_CR3","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1016\/j.cell.2016.02.007","volume":"164","author":"J Dekker","year":"2016","unstructured":"Dekker J, Mirny L. The 3D genome as moderator of chromosomal communication. Cell. 2016;164:1110\u201321.","journal-title":"Cell"},{"key":"6580_CR4","doi-asserted-by":"publisher","first-page":"1333","DOI":"10.1016\/j.cell.2015.10.066","volume":"163","author":"A Gonzalez-Sandoval","year":"2015","unstructured":"Gonzalez-Sandoval A, Towbin BD, Kalck V, Cabianca DS, Gaidatzis D, Hauer MH, Geng L, Wang L, Yang T, Wang X, et al. Perinuclear Anchoring of H3K9-Methylated Chromatin Stabilizes Induced Cell Fate in C. elegans Embryos. Cell. 2015;163:1333\u201347.","journal-title":"Cell"},{"key":"6580_CR5","doi-asserted-by":"publisher","first-page":"2829","DOI":"10.15252\/embj.201796717","volume":"36","author":"PE Garcia-Nieto","year":"2017","unstructured":"Garcia-Nieto PE, Schwartz EK, King DA, Paulsen J, Collas P, Herrera RE, Morrison AJ. Carcinogen susceptibility is regulated by genome architecture and predicts cancer mutagenesis. EMBO J. 2017;36:2829\u201343.","journal-title":"EMBO J"},{"key":"6580_CR6","doi-asserted-by":"publisher","first-page":"1299","DOI":"10.1101\/gr.5571506","volume":"16","author":"J Dostie","year":"2006","unstructured":"Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, et al. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 2006;16:1299\u2013309.","journal-title":"Genome Res"},{"key":"6580_CR7","doi-asserted-by":"publisher","first-page":"1306","DOI":"10.1126\/science.1067799","volume":"295","author":"J Dekker","year":"2002","unstructured":"Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science. 2002;295:1306\u201311.","journal-title":"Science"},{"key":"6580_CR8","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1126\/science.1181369","volume":"326","author":"E Lieberman-Aiden","year":"2009","unstructured":"Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289\u201393.","journal-title":"Science"},{"key":"6580_CR9","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1038\/ng1891","volume":"38","author":"Z Zhao","year":"2006","unstructured":"Zhao Z, Tavoosidana G, Sjolinder M, Gondor A, Mariano P, Wang S, Kanduri C, Lezcano M, Sandhu KS, Singh U, et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet. 2006;38:1341\u20137.","journal-title":"Nat Genet"},{"key":"6580_CR10","doi-asserted-by":"publisher","first-page":"1348","DOI":"10.1038\/ng1896","volume":"38","author":"M Simonis","year":"2006","unstructured":"Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet. 2006;38:1348\u201354.","journal-title":"Nat Genet"},{"key":"6580_CR11","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1186\/s13059-016-1043-8","volume":"17","author":"L Uuskula-Reimand","year":"2016","unstructured":"Uuskula-Reimand L, Hou H, Samavarchi-Tehrani P, Rudan MV, Liang M, Medina-Rivera A, Mohammed H, Schmidt D, Schwalie P, Young EJ, et al. Topoisomerase II beta interacts with cohesin and CTCF at topological domain borders. Genome Biol. 2016;17:182.","journal-title":"Genome Biol"},{"key":"6580_CR12","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1038\/nature11082","volume":"485","author":"JR Dixon","year":"2012","unstructured":"Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376\u201380.","journal-title":"Nature"},{"key":"6580_CR13","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1016\/j.molcel.2016.05.018","volume":"62","author":"JR Dixon","year":"2016","unstructured":"Dixon JR, Gorkin DU, Ren B. Chromatin domains: the unit of chromosome organization. Mol Cell. 2016;62:668\u201380.","journal-title":"Mol Cell"},{"key":"6580_CR14","doi-asserted-by":"publisher","first-page":"1905","DOI":"10.1101\/gr.176586.114","volume":"24","author":"N Heidari","year":"2014","unstructured":"Heidari N, Phanstiel DH, He C, Grubert F, Jahanbani F, Kasowski M, Zhang MQ, Snyder MP. Genome-wide map of regulatory interactions in the human genome. Genome Res. 2014;24:1905\u201317.","journal-title":"Genome Res"},{"key":"6580_CR15","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1038\/s41467-017-00524-5","volume":"8","author":"N Harmston","year":"2017","unstructured":"Harmston N, Ing-Simmons E, Tan G, Perry M, Merkenschlager M, Lenhard B. Topologically associating domains are ancient features that coincide with metazoan clusters of extreme noncoding conservation. Nat Commun. 2017;8:441.","journal-title":"Nat Commun"},{"key":"6580_CR16","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1186\/s12915-018-0556-x","volume":"16","author":"J Krefting","year":"2018","unstructured":"Krefting J, Andrade-Navarro MA, Ibn-Salem J. Evolutionary stability of topologically associating domains is associated with conserved gene regulation. BMC Biol. 2018;16:87.","journal-title":"BMC Biol"},{"key":"6580_CR17","doi-asserted-by":"publisher","first-page":"2038","DOI":"10.1016\/j.celrep.2016.04.085","volume":"15","author":"G Fudenberg","year":"2016","unstructured":"Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. Formation of chromosomal domains by loop extrusion. Cell Rep. 2016;15:2038\u201349.","journal-title":"Cell Rep"},{"key":"6580_CR18","doi-asserted-by":"publisher","first-page":"1338","DOI":"10.1126\/science.aaz3418","volume":"366","author":"IF Davidson","year":"2019","unstructured":"Davidson IF, Bauer B, Goetz D, Tang W, Wutz G, Peters JM. DNA loop extrusion by human cohesin. Science. 2019;366:1338\u201345.","journal-title":"Science"},{"key":"6580_CR19","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1126\/science.aar7831","volume":"360","author":"M Ganji","year":"2018","unstructured":"Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A, Haering CH, Dekker C. Real-time imaging of DNA loop extrusion by condensin. Science. 2018;360:102\u20135.","journal-title":"Science"},{"key":"6580_CR20","doi-asserted-by":"publisher","first-page":"1345","DOI":"10.1126\/science.aaz4475","volume":"366","author":"Y Kim","year":"2019","unstructured":"Kim Y, Shi Z, Zhang H, Finkelstein IJ, Yu H. Human cohesin compacts DNA by loop extrusion. Science. 2019;366:1345\u20139.","journal-title":"Science"},{"key":"6580_CR21","doi-asserted-by":"publisher","first-page":"2051","DOI":"10.1016\/j.bpj.2017.04.018","volume":"112","author":"H Agarwal","year":"2017","unstructured":"Agarwal H, Reisser M, Wortmann C, Gebhardt JCM. Direct observation of cell-cycle-dependent interactions between CTCF and chromatin. Biophys J. 2017;112:2051\u20135.","journal-title":"Biophys J"},{"key":"6580_CR22","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1038\/nature23001","volume":"547","author":"T Nagano","year":"2017","unstructured":"Nagano T, Lubling Y, Varnai C, Dudley C, Leung W, Baran Y, Mendelson Cohen N, Wingett S, Fraser P, Tanay A. Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature. 2017;547:61\u20137.","journal-title":"Nature"},{"key":"6580_CR23","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1101\/gr.241547.118","volume":"29","author":"ME Oomen","year":"2019","unstructured":"Oomen ME, Hansen AS, Liu Y, Darzacq X, Dekker J. CTCF sites display cell cycle-dependent dynamics in factor binding and nucleosome positioning. Genome Res. 2019;29:236\u201349.","journal-title":"Genome Res"},{"key":"6580_CR24","doi-asserted-by":"publisher","first-page":"930","DOI":"10.1016\/j.cell.2017.05.004","volume":"169","author":"EP Nora","year":"2017","unstructured":"Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A, Abdennur N, Dekker J, Mirny LA, Bruneau BG. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell. 2017;169:930\u201344 e922.","journal-title":"Cell"},{"key":"6580_CR25","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1038\/nature24281","volume":"551","author":"W Schwarzer","year":"2017","unstructured":"Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G, Loe-Mie Y, Fonseca NA, Huber W, HH C, Mirny L, Spitz F. Two independent modes of chromatin organization revealed by cohesin removal. Nature. 2017;551:51\u20136.","journal-title":"Nature"},{"key":"6580_CR26","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1038\/nature13986","volume":"515","author":"BD Pope","year":"2014","unstructured":"Pope BD, Ryba T, Dileep V, Yue F, Wu W, Denas O, Vera DL, Wang Y, Hansen RS, Canfield TK, et al. Topologically associating domains are stable units of replication-timing regulation. Nature. 2014;515:402\u20135.","journal-title":"Nature"},{"key":"6580_CR27","doi-asserted-by":"publisher","first-page":"E1691","DOI":"10.1073\/pnas.1521826113","volume":"113","author":"DS Neems","year":"2016","unstructured":"Neems DS, Garza-Gongora AG, Smith ED, Kosak ST. Topologically associated domains enriched for lineage-specific genes reveal expression-dependent nuclear topologies during myogenesis. Proc Natl Acad Sci U S A. 2016;113:E1691\u2013700.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"6580_CR28","doi-asserted-by":"publisher","first-page":"2151","DOI":"10.1101\/gad.241422.114","volume":"28","author":"F Le Dily","year":"2014","unstructured":"Le Dily F, Bau D, Pohl A, Vicent GP, Serra F, Soronellas D, Castellano G, Wright RH, Ballare C, Filion G, et al. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 2014;28:2151\u201362.","journal-title":"Genes Dev"},{"key":"6580_CR29","doi-asserted-by":"publisher","first-page":"852","DOI":"10.15252\/msb.20156492","volume":"11","author":"J Fraser","year":"2015","unstructured":"Fraser J, Ferrai C, Chiariello AM, Schueler M, Rito T, Laudanno G, Barbieri M, Moore BL, Kraemer DC, Aitken S, et al. Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation. Mol Syst Biol. 2015;11:852.","journal-title":"Mol Syst Biol"},{"key":"6580_CR30","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.cell.2017.06.029","volume":"170","author":"Y Ke","year":"2017","unstructured":"Ke Y, Xu Y, Chen X, Feng S, Liu Z, Sun Y, Yao X, Li F, Zhu W, Gao L, et al. 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell. 2017;170:367\u201381 e320.","journal-title":"Cell"},{"key":"6580_CR31","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1038\/nature21711","volume":"544","author":"IM Flyamer","year":"2017","unstructured":"Flyamer IM, Gassler J, Imakaev M, Brandao HB, Ulianov SV, Abdennur N, Razin SV, Mirny LA, Tachibana-Konwalski K. Single-nucleus hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature. 2017;544:110\u20134.","journal-title":"Nature"},{"key":"6580_CR32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.celrep.2018.06.003","volume":"24","author":"LJT Kaaij","year":"2018","unstructured":"Kaaij LJT, van der Weide RH, Ketting RF, de Wit E. Systemic loss and gain of chromatin architecture throughout Zebrafish development. Cell Rep. 2018;24:1\u201310 e14.","journal-title":"Cell Rep"},{"key":"6580_CR33","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1016\/j.cell.2017.09.043","volume":"171","author":"B Bonev","year":"2017","unstructured":"Bonev B, Mendelson Cohen N, Szabo Q, Fritsch L, Papadopoulos GL, Lubling Y, Xu X, Lv X, Hugnot JP, Tanay A, Cavalli G. Multiscale 3D genome rewiring during mouse neural development. Cell. 2017;171:557\u201372 e524.","journal-title":"Cell"},{"key":"6580_CR34","doi-asserted-by":"publisher","first-page":"11070","DOI":"10.1093\/nar\/gkx722","volume":"45","author":"R Boya","year":"2017","unstructured":"Boya R, Yadavalli AD, Nikhat S, Kurukuti S, Palakodeti D, Pongubala JMR. Developmentally regulated higher-order chromatin interactions orchestrate B cell fate commitment. Nucleic Acids Res. 2017;45:11070\u201387.","journal-title":"Nucleic Acids Res"},{"key":"6580_CR35","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1016\/j.jmb.2014.09.013","volume":"427","author":"F Ciabrelli","year":"2015","unstructured":"Ciabrelli F, Cavalli G. Chromatin-driven behavior of topologically associating domains. J Mol Biol. 2015;427:608\u201325.","journal-title":"J Mol Biol"},{"key":"6580_CR36","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1186\/s13059-015-0719-9","volume":"16","author":"S Rafique","year":"2015","unstructured":"Rafique S, Thomas JS, Sproul D, Bickmore WA. Estrogen-induced chromatin decondensation and nuclear re-organization linked to regional epigenetic regulation in breast cancer. Genome Biol. 2015;16:145.","journal-title":"Genome Biol"},{"key":"6580_CR37","doi-asserted-by":"publisher","first-page":"2778","DOI":"10.1101\/gad.251694.114","volume":"28","author":"I Williamson","year":"2014","unstructured":"Williamson I, Berlivet S, Eskeland R, Boyle S, Illingworth RS, Paquette D, Dostie J, Bickmore WA. Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev. 2014;28:2778\u201391.","journal-title":"Genes Dev"},{"key":"6580_CR38","doi-asserted-by":"publisher","first-page":"1119","DOI":"10.1101\/gad.292104","volume":"18","author":"S Chambeyron","year":"2004","unstructured":"Chambeyron S, Bickmore WA. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 2004;18:1119\u201330.","journal-title":"Genes Dev"},{"key":"6580_CR39","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1016\/j.molcel.2010.03.016","volume":"38","author":"D Peric-Hupkes","year":"2010","unstructured":"Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, Graf S, Flicek P, Kerkhoven RM, van Lohuizen M, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 2010;38:603\u201313.","journal-title":"Mol Cell"},{"key":"6580_CR40","doi-asserted-by":"publisher","first-page":"e1002090","DOI":"10.1371\/journal.pgen.1002090","volume":"7","author":"F Lienert","year":"2011","unstructured":"Lienert F, Mohn F, Tiwari VK, Baubec T, Roloff TC, Gaidatzis D, Stadler MB, Schubeler D. Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLoS Genet. 2011;7:e1002090.","journal-title":"PLoS Genet"},{"key":"6580_CR41","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1038\/ng.947","volume":"43","author":"E Yaffe","year":"2011","unstructured":"Yaffe E, Tanay A. Probabilistic modeling of hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat Genet. 2011;43:1059\u201365.","journal-title":"Nat Genet"},{"key":"6580_CR42","doi-asserted-by":"publisher","first-page":"3131","DOI":"10.1093\/bioinformatics\/bts570","volume":"28","author":"M Hu","year":"2012","unstructured":"Hu M, Deng K, Selvaraj S, Qin Z, Ren B, Liu JS. HiCNorm: removing biases in hi-C data via Poisson regression. Bioinformatics. 2012;28:3131\u20133.","journal-title":"Bioinformatics"},{"key":"6580_CR43","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1038\/nmeth.2148","volume":"9","author":"M Imakaev","year":"2012","unstructured":"Imakaev M, Fudenberg G, McCord RP, Naumova N, Goloborodko A, Lajoie BR, Dekker J, Mirny LA. Iterative correction of hi-C data reveals hallmarks of chromosome organization. Nat Methods. 2012;9:999\u20131003.","journal-title":"Nat Methods"},{"key":"6580_CR44","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1186\/1471-2164-13-436","volume":"13","author":"A Cournac","year":"2012","unstructured":"Cournac A, Marie-Nelly H, Marbouty M, Koszul R, Mozziconacci J. Normalization of a chromosomal contact map. BMC Genomics. 2012;13:436.","journal-title":"BMC Genomics"},{"key":"6580_CR45","doi-asserted-by":"publisher","first-page":"1665","DOI":"10.1016\/j.cell.2014.11.021","volume":"159","author":"SS Rao","year":"2014","unstructured":"Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, Aiden EL. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159:1665\u201380.","journal-title":"Cell"},{"key":"6580_CR46","doi-asserted-by":"publisher","first-page":"1104","DOI":"10.1186\/1471-2164-15-1104","volume":"15","author":"PB Chen","year":"2014","unstructured":"Chen PB, Zhu LJ, Hainer SJ, McCannell KN, Fazzio TG. Unbiased chromatin accessibility profiling by RED-seq uncovers unique features of nucleosome variants in vivo. BMC Genomics. 2014;15:1104.","journal-title":"BMC Genomics"},{"key":"6580_CR47","doi-asserted-by":"publisher","first-page":"780","DOI":"10.1016\/j.cell.2017.04.022","volume":"169","author":"B van Steensel","year":"2017","unstructured":"van Steensel B, Belmont AS. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell. 2017;169:780\u201391.","journal-title":"Cell"},{"key":"6580_CR48","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1186\/s13059-015-0753-7","volume":"16","author":"T Nagano","year":"2015","unstructured":"Nagano T, Varnai C, Schoenfelder S, Javierre BM, Wingett SW, Fraser P. Comparison of hi-C results using in-solution versus in-nucleus ligation. Genome Biol. 2015;16:175.","journal-title":"Genome Biol"},{"key":"6580_CR49","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1038\/nature21411","volume":"543","author":"RA Beagrie","year":"2017","unstructured":"Beagrie RA, Scialdone A, Schueler M, Kraemer DC, Chotalia M, Xie SQ, Barbieri M, de Santiago I, Lavitas LM, Branco MR, et al. Complex multi-enhancer contacts captured by genome architecture mapping. Nature. 2017;543:519\u201324.","journal-title":"Nature"},{"key":"6580_CR50","doi-asserted-by":"publisher","first-page":"934","DOI":"10.1016\/j.cell.2015.10.026","volume":"163","author":"KP Eagen","year":"2015","unstructured":"Eagen KP, Hartl TA, Kornberg RD. Stable chromosome condensation revealed by chromosome conformation capture. Cell. 2015;163:934\u201346.","journal-title":"Cell"},{"key":"6580_CR51","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1186\/s13059-015-0728-8","volume":"16","author":"X Deng","year":"2015","unstructured":"Deng X, Ma W, Ramani V, Hill A, Yang F, Ay F, Berletch JB, Blau CA, Shendure J, Duan Z, et al. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 2015;16:152.","journal-title":"Genome Biol"},{"key":"6580_CR52","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1038\/ng0110-4","volume":"42","author":"GJ Filion","year":"2010","unstructured":"Filion GJ, van Steensel B. Reassessing the abundance of H3K9me2 chromatin domains in embryonic stem cells. Nat Genet. 2010;42:4 author reply 5-6.","journal-title":"Nat Genet"},{"key":"6580_CR53","doi-asserted-by":"publisher","first-page":"802","DOI":"10.1016\/j.molcel.2018.05.017","volume":"71","author":"X Zheng","year":"2018","unstructured":"Zheng X, Hu J, Yue S, Kristiani L, Kim M, Sauria M, Taylor J, Kim Y, Zheng Y. Lamins organize the global three-dimensional genome from the nuclear periphery. Mol Cell. 2018;71:802\u201315 e807.","journal-title":"Mol Cell"},{"key":"6580_CR54","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1007\/978-1-61779-343-1_32","volume":"798","author":"Y Ohkawa","year":"2012","unstructured":"Ohkawa Y, Mallappa C, Vallaster CS, Imbalzano AN. An improved restriction enzyme accessibility assay for analyzing changes in chromatin structure in samples of limited cell number. Methods Mol Biol. 2012;798:531\u201342.","journal-title":"Methods Mol Biol"},{"key":"6580_CR55","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1016\/j.devcel.2009.02.002","volume":"16","author":"G Gargiulo","year":"2009","unstructured":"Gargiulo G, Levy S, Bucci G, Romanenghi M, Fornasari L, Beeson KY, Goldberg SM, Cesaroni M, Ballarini M, Santoro F, et al. NA-Seq: a discovery tool for the analysis of chromatin structure and dynamics during differentiation. Dev Cell. 2009;16:466\u201381.","journal-title":"Dev Cell"},{"key":"6580_CR56","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.ymeth.2012.07.022","volume":"58","author":"N Naumova","year":"2012","unstructured":"Naumova N, Smith EM, Zhan Y, Dekker J. Analysis of long-range chromatin interactions using chromosome conformation capture. Methods. 2012;58:192\u2013203.","journal-title":"Methods"},{"key":"6580_CR57","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.ymeth.2017.04.004","volume":"123","author":"H Belaghzal","year":"2017","unstructured":"Belaghzal H, Dekker J, Gibcus JH. Hi-C 2.0: An optimized Hi-C procedure for high-resolution genome-wide mapping of chromosome conformation. Methods. 2017;123:56\u201365.","journal-title":"Methods"},{"key":"6580_CR58","doi-asserted-by":"publisher","first-page":"E4428","DOI":"10.1073\/pnas.1507253112","volume":"112","author":"J Wang","year":"2015","unstructured":"Wang J, Vicente-Garcia C, Seruggia D, Molto E, Fernandez-Minan A, Neto A, Lee E, Gomez-Skarmeta JL, Montoliu L, Lunyak VV, Jordan IK. MIR retrotransposon sequences provide insulators to the human genome. Proc Natl Acad Sci U S A. 2015;112:E4428\u201337.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"6580_CR59","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1101\/gr.082800.108","volume":"19","author":"S Cuddapah","year":"2009","unstructured":"Cuddapah S, Jothi R, Schones DE, Roh TY, Cui K, Zhao K. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 2009;19:24\u201332.","journal-title":"Genome Res"},{"key":"6580_CR60","doi-asserted-by":"publisher","first-page":"1985","DOI":"10.1101\/gr.249326.119","volume":"29","author":"RV Chereji","year":"2019","unstructured":"Chereji RV, Eriksson PR, Ocampo J, Prajapati HK, Clark DJ. Accessibility of promoter DNA is not the primary determinant of chromatin-mediated gene regulation. Genome Res. 2019;29:1985\u201395.","journal-title":"Genome Res"},{"key":"6580_CR61","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.jmb.2012.01.043","volume":"417","author":"J Allan","year":"2012","unstructured":"Allan J, Fraser RM, Owen-Hughes T, Keszenman-Pereyra D. Micrococcal nuclease does not substantially bias nucleosome mapping. J Mol Biol. 2012;417:152\u201364.","journal-title":"J Mol Biol"},{"key":"6580_CR62","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1186\/s13059-019-1815-z","volume":"20","author":"RV Chereji","year":"2019","unstructured":"Chereji RV, Bryson TD, Henikoff S. Quantitative MNase-seq accurately maps nucleosome occupancy levels. Genome Biol. 2019;20:198.","journal-title":"Genome Biol"},{"key":"6580_CR63","doi-asserted-by":"publisher","first-page":"1239","DOI":"10.1093\/nar\/gky1203","volume":"47","author":"U Schwartz","year":"2019","unstructured":"Schwartz U, Nemeth A, Diermeier S, Exler JH, Hansch S, Maldonado R, Heizinger L, Merkl R, Langst G. Characterizing the nuclease accessibility of DNA in human cells to map higher order structures of chromatin. Nucleic Acids Res. 2019;47:1239\u201354.","journal-title":"Nucleic Acids Res"},{"key":"6580_CR64","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1038\/nature06947","volume":"453","author":"L Guelen","year":"2008","unstructured":"Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008;453:948\u201351.","journal-title":"Nature"}],"container-title":["BMC Genomics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-020-6580-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12864-020-6580-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-020-6580-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,21]],"date-time":"2021-02-21T02:30:13Z","timestamp":1613874613000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcgenomics.biomedcentral.com\/articles\/10.1186\/s12864-020-6580-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,22]]},"references-count":64,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["6580"],"URL":"https:\/\/doi.org\/10.1186\/s12864-020-6580-6","relation":{},"ISSN":["1471-2164"],"issn-type":[{"value":"1471-2164","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,22]]},"assertion":[{"value":"10 September 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 February 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 February 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Not applicable.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"175"}}