{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T04:03:17Z","timestamp":1790481797449,"version":"4.1.0"},"reference-count":85,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T00:00:00Z","timestamp":1741910400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T00:00:00Z","timestamp":1741910400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2020\/04\/X\/NZ2\/01006"],"award-info":[{"award-number":["2020\/04\/X\/NZ2\/01006"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008349","name":"Boehringer Ingelheim","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008349","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010661","name":"EC | Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["860002"],"award-info":[{"award-number":["860002"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004569","name":"Ministerstwo Nauki i Szkolnictwa Wy\u017cszego","doi-asserted-by":"publisher","award":["BOB-IDUB\/IV.4.1\/4\/2024"],"award-info":[{"award-number":["BOB-IDUB\/IV.4.1\/4\/2024"]}],"id":[{"id":"10.13039\/501100004569","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004382","name":"Polska Akademia Nauk","doi-asserted-by":"publisher","award":["PPN\/STA\/2021\/1\/00087\/DEC\/1"],"award-info":[{"award-number":["PPN\/STA\/2021\/1\/00087\/DEC\/1"]}],"id":[{"id":"10.13039\/501100004382","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Commun Biol"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Chromosome Conformation Capture (3\u2009C) methods, including Hi-C (a high-throughput variation of 3\u2009C), detect pairwise interactions between DNA regions, enabling the reconstruction of chromatin architecture in the nucleus. HiChIP is a modification of the Hi-C experiment that includes a chromatin immunoprecipitation (ChIP) step, allowing genome-wide identification of chromatin contacts mediated by a protein of interest. In mammalian cells, cohesin protein complex is one of the major players in the establishment of chromatin loops. We present an improved cohesin HiChIP experimental protocol. Using comprehensive bioinformatic analysis, we show that a dual chromatin fixation method compared to the standard formaldehyde-only method, results in a substantially better signal-to-noise ratio, increased ChIP efficiency and improved detection of chromatin loops and architectural stripes. Additionally, we propose an automated pipeline called nf-HiChIP (<jats:ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" xlink:href=\"https:\/\/github.com\/SFGLab\/hichip-nf-pipeline\" ext-link-type=\"uri\">https:\/\/github.com\/SFGLab\/hichip-nf-pipeline<\/jats:ext-link>) for processing HiChIP samples starting from raw sequencing reads data and ending with a set of significant chromatin interactions (loops), which allows efficient and timely analysis of multiple samples in parallel, without requiring additional ChIP-seq experiments. Finally, using advanced approaches for biophysical modelling and stripe calling we generate accurate loop extrusion polymer models for a region of interest and provide a detailed picture of architectural stripes, respectively.<\/jats:p>","DOI":"10.1038\/s42003-025-07847-w","type":"journal-article","created":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T01:19:33Z","timestamp":1741915173000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Improved cohesin HiChIP protocol and bioinformatic analysis for robust detection of chromatin loops and stripes"],"prefix":"10.1038","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6103-5915","authenticated-orcid":false,"given":"Karolina","family":"Buka","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6573-2988","authenticated-orcid":false,"given":"Zofia","family":"Parteka-Tojek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4981-8746","authenticated-orcid":false,"given":"Abhishek","family":"Agarwal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8890-9988","authenticated-orcid":false,"given":"Micha\u0142","family":"Denkiewicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sevastianos","family":"Korsak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mateusz","family":"Chili\u0144ski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9573-0804","authenticated-orcid":false,"given":"Krzysztof H.","family":"Banecki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3840-7610","authenticated-orcid":false,"given":"Dariusz","family":"Plewczynski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,3,14]]},"reference":[{"key":"7847_CR1","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1007\/BF00281263","volume":"60","author":"T Cremer","year":"1982","unstructured":"Cremer, T. et al. Rabl\u2019s model of the interphase chromosome arrangement tested in Chinise hamster cells by premature chromosome condensation and laser-UV-microbeam experiments. Hum. Genet. 60, 46\u201356 (1982).","journal-title":"Hum. Genet."},{"key":"7847_CR2","doi-asserted-by":"crossref","unstructured":"Parada, L. A., McQueen, P. G., Munson, P. J. & Misteli, T. Conservation of relative chromosome positioning in normal and cancer Cells. Curr. Biol. 12, 1692\u20131697 (2002).","DOI":"10.1016\/S0960-9822(02)01166-1"},{"key":"7847_CR3","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1126\/science.1181369","volume":"326","author":"E Lieberman-Aiden","year":"2009","unstructured":"Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289\u2013293 (2009).","journal-title":"Science"},{"key":"7847_CR4","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1038\/nature11082","volume":"485","author":"JR Dixon","year":"2012","unstructured":"Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376\u2013380 (2012).","journal-title":"Nature"},{"key":"7847_CR5","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1038\/nature11049","volume":"485","author":"EP Nora","year":"2012","unstructured":"Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381\u2013385 (2012).","journal-title":"Nature"},{"key":"7847_CR6","doi-asserted-by":"publisher","first-page":"1665","DOI":"10.1016\/j.cell.2014.11.021","volume":"159","author":"SSP Rao","year":"2014","unstructured":"Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665\u20131680 (2014).","journal-title":"Cell"},{"key":"7847_CR7","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1038\/nrc3743","volume":"14","author":"A Losada","year":"2014","unstructured":"Losada, A. Cohesin in cancer: chromosome segregation and beyond. Nat. Rev. Cancer 14, 389\u201393 (2014).","journal-title":"Nat. Rev. Cancer"},{"key":"7847_CR8","doi-asserted-by":"crossref","unstructured":"Haering, C. H., L\u00f6we, J., Hochwagen, A. & Nasmyth, K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773\u2013788 (2002).","DOI":"10.1016\/S1097-2765(02)00515-4"},{"key":"7847_CR9","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1242\/jcs.073866","volume":"124","author":"MT Ocampo-Hafalla","year":"2011","unstructured":"Ocampo-Hafalla, M. T. & Uhlmann, F. Cohesin loading and sliding. J. Cell Sci. 124, 685\u2013691 (2011).","journal-title":"J. Cell Sci."},{"key":"7847_CR10","doi-asserted-by":"crossref","unstructured":"Davidson, I. F. et al. Rapid movement and transcriptional re\u2010localization of human cohesin on DNA. EMBO J. 35, 2671\u20132685 (2016)","DOI":"10.15252\/embj.201695402"},{"key":"7847_CR11","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1038\/nature02742","volume":"430","author":"A Lengronne","year":"2004","unstructured":"Lengronne, A. et al. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430, 573\u20138 (2004).","journal-title":"Nature"},{"key":"7847_CR12","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1038\/nature22063","volume":"544","author":"GA Busslinger","year":"2017","unstructured":"Busslinger, G. A. et al. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature 544, 503\u2013507 (2017).","journal-title":"Nature"},{"key":"7847_CR13","doi-asserted-by":"crossref","unstructured":"Parelho, V. et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132, 422\u2013433 (2008).","DOI":"10.1016\/j.cell.2008.01.011"},{"key":"7847_CR14","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1038\/nature06634","volume":"451","author":"KS Wendt","year":"2008","unstructured":"Wendt, K. S. et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451, 796\u2013801 (2008).","journal-title":"Nature"},{"key":"7847_CR15","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1101\/sqb.2017.82.034710","volume":"82","author":"G Fudenberg","year":"2017","unstructured":"Fudenberg, G., Abdennur, N., Imakaev, M., Goloborodko, A. & Mirny, L. A. Emerging evidence of chromosome folding by loop extrusion. Cold Spring Harb. Symp. Quant. Biol. 82, 45\u201355 (2017).","journal-title":"Cold Spring Harb. Symp. Quant. Biol."},{"key":"7847_CR16","doi-asserted-by":"crossref","unstructured":"Vian, L. et al. The energetics and physiological impact of cohesin extrusion. Cell 173, 1165\u20131178.e20 (2018).","DOI":"10.1016\/j.cell.2018.03.072"},{"key":"7847_CR17","doi-asserted-by":"crossref","unstructured":"Hansen, A. S. CTCF as a boundary factor for cohesin-mediated loop extrusion: evidence for a multi-step mechanism. Nucleus 11, 132\u2013148 (2020)","DOI":"10.1080\/19491034.2020.1782024"},{"key":"7847_CR18","doi-asserted-by":"crossref","unstructured":"Ladurner R. et al. Cohesin\u2019s ATPase activity couples cohesin loading onto DNA with Smc3 acetylation. Curr. Biol. 24, 2228\u20132237 (2014).","DOI":"10.1016\/j.cub.2014.08.011"},{"key":"7847_CR19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-03118-9","volume":"7","author":"\u00cd Marcos-Alcalde","year":"2017","unstructured":"Marcos-Alcalde, \u00cd. et al. Two-step ATP-driven opening of cohesin head. Sci. Rep. 7, 1\u201314 (2017).","journal-title":"Sci. Rep."},{"key":"7847_CR20","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2208004119","volume":"119","author":"X Xu","year":"2022","unstructured":"Xu, X., Kanai, R., Wang, L. & Yanagida, M. Cohesin ATPase activities regulate DNA binding and coiled-coil configuration. Proc. Natl Acad. Sci. USA 119, e2208004119 (2022).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"7847_CR21","doi-asserted-by":"crossref","unstructured":"Schmitt, A. D., Hu, M. & Ren, B. Genome-wide mapping and analysis of chromosome architecture. Nat. Rev. Mol. Cell Biol. 17, 743\u2013755 (2016).","DOI":"10.1038\/nrm.2016.104"},{"key":"7847_CR22","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1038\/nmeth.3999","volume":"13","author":"MR Mumbach","year":"2016","unstructured":"Mumbach, M. R. et al. HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13, 919\u2013922 (2016).","journal-title":"Nat. Methods"},{"key":"7847_CR23","doi-asserted-by":"publisher","first-page":"1345","DOI":"10.1038\/cr.2016.137","volume":"26","author":"R Fang","year":"2016","unstructured":"Fang, R. et al. Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seq. Cell Res. 26, 1345\u20131348 (2016).","journal-title":"Cell Res."},{"key":"7847_CR24","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1038\/nature08497","volume":"462","author":"MJ Fullwood","year":"2009","unstructured":"Fullwood, M. J. et al. An oestrogen-receptor-\u03b1-bound human chromatin interactome. Nature 462, 58\u201364 (2009).","journal-title":"Nature"},{"key":"7847_CR25","doi-asserted-by":"crossref","unstructured":"Banigan, E. J., van den Berg, A. A., Brand\u00e3o, H. B., Marko, J. F. & Mirny, L. A. Chromosome organization by one-sided and two-sided loop extrusion. Elife 6, 9:e53558. (2020)","DOI":"10.7554\/eLife.53558"},{"key":"7847_CR26","doi-asserted-by":"crossref","unstructured":"Swygert, S. G. et al. Local chromatin fiber folding represses transcription and loop extrusion in quiescent cells. Elife 4, 10:e72062 (2021).","DOI":"10.7554\/eLife.72062"},{"key":"7847_CR27","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/j.cels.2016.07.002","volume":"3","author":"NC Durand","year":"2016","unstructured":"Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95\u201398 (2016).","journal-title":"Cell Syst."},{"key":"7847_CR28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1006982","volume":"15","author":"I Juric","year":"2019","unstructured":"Juric, I. et al. MAPS: Model-based analysis of long-range chromatin interactions from PLAC-seq and HiChIP experiments. PLoS Comput. Biol. 15, e1006982 (2019).","journal-title":"PLoS Comput. Biol."},{"key":"7847_CR29","doi-asserted-by":"crossref","unstructured":"Lee, B. et al. ChIA-PIPE: A fully automated pipeline for comprehensive ChIA-PET data analysis and visualization. Sci. Adv. 6, eaay2078 (2020).","DOI":"10.1126\/sciadv.aay2078"},{"key":"7847_CR30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-022-29258-9","volume":"13","author":"S Yoon","year":"2022","unstructured":"Yoon, S., Chandra, A. & Vahedi, G. Stripenn detects architectural stripes from chromatin conformation data using computer vision. Nat. Commun. 13, 1\u201314 (2022).","journal-title":"Nat. Commun."},{"key":"7847_CR31","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1038\/nbt.3820","volume":"35","author":"P Di Tommaso","year":"2017","unstructured":"Di Tommaso, P. et al. Nextflow enables reproducible computational workflows. Nat. Biotechnol. 35, 316\u2013319 (2017).","journal-title":"Nat. Biotechnol."},{"key":"7847_CR32","doi-asserted-by":"crossref","unstructured":"Korsak, S. & Plewczynski, D. LoopSage: An energy-based Monte Carlo approach for the loop extrusion modeling of chromatin. Methods 223, 106\u2013117 (2024).","DOI":"10.1016\/j.ymeth.2024.01.015"},{"key":"7847_CR33","doi-asserted-by":"crossref","unstructured":"1000 Genomes Project Consortium, Auton, A et al. Aglobal reference for human genetic variation. Nature 526, 68\u201374 (2015).","DOI":"10.1038\/nature15393"},{"key":"7847_CR34","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1038\/s41592-019-0407-x","volume":"16","author":"MR Mumbach","year":"2019","unstructured":"Mumbach, M. R. et al. HiChIRP reveals RNA-associated chromosome conformation. Nat. Methods 16, 489\u2013492 (2019).","journal-title":"Nat. Methods"},{"key":"7847_CR35","doi-asserted-by":"crossref","unstructured":"Petrovic, J. et al. oncogenic notch promotes long-range regulatory interactions within hyperconnected 3D cliques. Mol. Cell 73, 1174\u20131190.e12 (2019).","DOI":"10.1016\/j.molcel.2019.01.006"},{"key":"7847_CR36","doi-asserted-by":"publisher","first-page":"750","DOI":"10.1126\/science.1242510","volume":"342","author":"M Kasowski","year":"2013","unstructured":"Kasowski, M. et al. Extensive variation in chromatin states across humans. Science 342, 750\u20132 (2013).","journal-title":"Science"},{"key":"7847_CR37","doi-asserted-by":"crossref","unstructured":"Tang, Z. et al. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163, 1611\u20131627 (2015).","DOI":"10.1016\/j.cell.2015.11.024"},{"key":"7847_CR38","doi-asserted-by":"publisher","first-page":"eaao6135","DOI":"10.1126\/science.aao6135","volume":"359","author":"JH Gibcus","year":"2018","unstructured":"Gibcus, J. H. et al. A pathway for mitotic chromosome formation. Science 359, eaao6135 (2018).","journal-title":"Science"},{"key":"7847_CR39","doi-asserted-by":"publisher","first-page":"698","DOI":"10.2144\/000112297","volume":"41","author":"P-Y Zeng","year":"2006","unstructured":"Zeng, P.-Y., Vakoc, C. R., Chen, Z.-C., Blobel, G. A. & Berger, S. L. In vivo dual cross-linking for identification of indirect DNA-associated proteins by chromatin immunoprecipitation. Biotechniques 41, 698 (2006). 694, 696.","journal-title":"Biotechniques"},{"key":"7847_CR40","doi-asserted-by":"crossref","unstructured":"Tian, B., Yang, J. & Brasier, A. R. Two-step cross-linking for analysis of protein\u2013chromatin interactions. In Transcriptional Regulation. Methods in Molecular Biology (eds. Vancura, A.) 809 (Springer, 2012)","DOI":"10.1007\/978-1-61779-376-9_7"},{"key":"7847_CR41","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1038\/nprot.2017.012","volume":"12","author":"X Li","year":"2017","unstructured":"Li, X. et al. Long-read ChIA-PET for base-pair-resolution mapping of haplotype-specific chromatin interactions. Nat. Protoc. 12, 899\u2013915 (2017).","journal-title":"Nat. Protoc."},{"key":"7847_CR42","doi-asserted-by":"publisher","first-page":"1046","DOI":"10.1038\/s41592-021-01248-7","volume":"18","author":"B Akgol Oksuz","year":"2021","unstructured":"Akgol Oksuz, B. et al. Systematic evaluation of chromosome conformation capture assays. Nat. Methods 18, 1046\u20131055 (2021).","journal-title":"Nat. Methods"},{"key":"7847_CR43","doi-asserted-by":"publisher","first-page":"W160","DOI":"10.1093\/nar\/gkw257","volume":"44","author":"F Ram\u00edrez","year":"2016","unstructured":"Ram\u00edrez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160\u2013W165 (2016).","journal-title":"Nucleic Acids Res."},{"key":"7847_CR44","doi-asserted-by":"publisher","first-page":"Article 9","DOI":"10.1515\/1544-6115.1750","volume":"11","author":"A Diaz","year":"2012","unstructured":"Diaz, A., Park, K., Lim, D. A. & Song, J. S. Normalization, bias correction, and peak calling for ChIP-seq. Stat. Appl. Genet. Mol. Biol. 11, Article 9 (2012).","journal-title":"Stat. Appl. Genet. Mol. Biol."},{"key":"7847_CR45","unstructured":"Rossum, G. V., L. Drake, F. L. Python 3 Reference Manual, Vol. 242 (CreateSpace, Scotts Valley, CA, 2009)"},{"key":"7847_CR46","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1038\/nmeth.4583","volume":"15","author":"CA Lareau","year":"2018","unstructured":"Lareau, C. A. & Aryee, M. J. hichipper: a preprocessing pipeline for calling DNA loops from HiChIP data. Nature Methods 15, 155\u2013156 (2018).","journal-title":"Nature Methods"},{"key":"7847_CR47","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-11950-y","volume":"10","author":"S Bhattacharyya","year":"2019","unstructured":"Bhattacharyya, S., Chandra, V., Vijayanand, P. & Ay, F. Identification of significant chromatin contacts from HiChIP data by FitHiChIP. Nat. Commun. 10, 4221 (2019).","journal-title":"Nat. Commun."},{"key":"7847_CR48","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1093\/nar\/gkab1233","volume":"50","author":"Y Cao","year":"2022","unstructured":"Cao, Y., Liu, S., Ren, G., Tang, Q. & Zhao, K. cLoops2: a full-stack comprehensive analytical tool for chromatin interactions. Nucleic Acids Res. 50, 57\u201371 (2022).","journal-title":"Nucleic Acids Res."},{"key":"7847_CR49","doi-asserted-by":"publisher","first-page":"032414","DOI":"10.1103\/PhysRevE.102.032414","volume":"102","author":"M Crippa","year":"2020","unstructured":"Crippa, M., Zhan, Y. & Tiana, G. Effective model of loop extrusion predicts chromosomal domains. Phys. Rev. E 102, 032414 (2020).","journal-title":"Phys. Rev. E"},{"key":"7847_CR50","doi-asserted-by":"crossref","unstructured":"Nicodemi, M. & Prisco, A. Thermodynamic pathways to genome spatial organization in the cell nucleus. Biophys. J. 96, 2168\u20132177 (2009).","DOI":"10.1016\/j.bpj.2008.12.3919"},{"key":"7847_CR51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13059-022-02815-7","volume":"23","author":"R Rossini","year":"2022","unstructured":"Rossini, R., Kumar, V., Mathelier, A., Rognes, T. & Paulsen, J. MoDLE: high-performance stochastic modeling of DNA loop extrusion interactions. Genome Biol 23, 1\u201324 (2022).","journal-title":"Genome Biol"},{"key":"7847_CR52","doi-asserted-by":"publisher","first-page":"e2200240","DOI":"10.1002\/bies.202200240","volume":"45","author":"A Agarwal","year":"2023","unstructured":"Agarwal, A., Korsak, S., Choudhury, A. & Plewczynski, D. The dynamic role of cohesin in maintaining human genome architecture. Bioessays 45, e2200240 (2023).","journal-title":"Bioessays"},{"key":"7847_CR53","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1126\/science.abn6583","volume":"376","author":"M Gabriele","year":"2022","unstructured":"Gabriele, M. et al. Dynamics of CTCF- and cohesin-mediated chromatin looping revealed by live-cell imaging. Science 376, 496\u2013501 (2022).","journal-title":"Science"},{"key":"7847_CR54","doi-asserted-by":"publisher","first-page":"1907","DOI":"10.1038\/s41588-022-01232-7","volume":"54","author":"P Mach","year":"2022","unstructured":"Mach, P. et al. Cohesin and CTCF control the dynamics of chromosome folding. Nat. Genet. 54, 1907\u20131918 (2022).","journal-title":"Nat. Genet."},{"key":"7847_CR55","doi-asserted-by":"publisher","unstructured":"Samejima, K. et al. Rules of engagement for condensins and cohesins guide mitotic chromosome formation. bioRxiv https:\/\/doi.org\/10.1101\/2024.04.18.590027 (2024).","DOI":"10.1101\/2024.04.18.590027"},{"key":"7847_CR56","doi-asserted-by":"publisher","first-page":"1422","DOI":"10.1016\/j.molcel.2024.02.025","volume":"84","author":"EM Hildebrand","year":"2024","unstructured":"Hildebrand, E. M. et al. Mitotic chromosomes are self-entangled and disentangle through a topoisomerase-II-dependent two-stage exit from mitosis. Mol Cell 84, 1422\u20131441.e14 (2024).","journal-title":"Mol Cell"},{"key":"7847_CR57","doi-asserted-by":"publisher","first-page":"6424","DOI":"10.1016\/j.cell.2024.10.026","volume":"187","author":"J Dekker","year":"2024","unstructured":"Dekker, J. & Mirny, L. A. The chromosome folding problem and how cells solve it. Cell 187, 6424\u20136450 (2024).","journal-title":"Cell"},{"key":"7847_CR58","doi-asserted-by":"publisher","first-page":"715","DOI":"10.2144\/000112014","volume":"39","author":"DE Nowak","year":"2005","unstructured":"Nowak, D. E., Tian, B. & Brasier, A. R. Two-step cross-linking method for identification of NF-kappaB gene network by chromatin immunoprecipitation. Biotechniques 39, 715\u2013725 (2005).","journal-title":"Biotechniques"},{"key":"7847_CR59","doi-asserted-by":"publisher","first-page":"554","DOI":"10.1016\/j.molcel.2020.03.003","volume":"78","author":"N Krietenstein","year":"2020","unstructured":"Krietenstein, N. et al. Ultrastructural details of mammalian chromosome architecture. Mol. Cell 78, 554\u2013565.e7 (2020).","journal-title":"Mol. Cell"},{"key":"7847_CR60","doi-asserted-by":"publisher","first-page":"940","DOI":"10.1016\/j.molcel.2018.07.012","volume":"71","author":"X Lyu","year":"2018","unstructured":"Lyu, X., Rowley, M. J. & Corces, V. G. Architectural proteins and poluripotency factors cooperate to orchestrate the transcriptional response of hESCs to temperature stress. Mol. Cell 71, 940\u2013955.e7 (2018).","journal-title":"Mol. Cell"},{"key":"7847_CR61","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1093\/imanum\/drs019","volume":"33","author":"PA Knight","year":"2012","unstructured":"Knight, P. A. & Ruiz, D. A fast algorithm for matrix balancing. IMA J. Numer. Anal. 33, 1029\u20131047 (2012).","journal-title":"IMA J. Numer. Anal."},{"key":"7847_CR62","first-page":"2","volume":"2014","author":"D Merkel","year":"2014","unstructured":"Merkel, D. Docker: lightweight linux containers for consistent development and deployment. Linux J 2014, 2 (2014).","journal-title":"Linux J"},{"key":"7847_CR63","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1016\/j.molcel.2020.03.002","volume":"78","author":"TS Hsieh","year":"2020","unstructured":"Hsieh, T. S. et al. Resolving the 3D landscape of transcription-linked mammalian chromatin folding. Mol. Cell 78, 539\u2013553.e8 (2020).","journal-title":"Mol. Cell"},{"key":"7847_CR64","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1038\/s41556-019-0273-x","volume":"21","author":"K Kraft","year":"2019","unstructured":"Kraft, K. et al. Serial genomic inversions induce tissue-specific architectural stripes, gene misexpression and congenital malformations. Nat. Cell Biol. 21, 305\u2013310 (2019).","journal-title":"Nat. Cell Biol."},{"key":"7847_CR65","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1038\/nmeth.3542","volume":"12","author":"C Schmidl","year":"2015","unstructured":"Schmidl, C., Rendeiro, A. F., Sheffield, N. C. & Bock, C. ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors. Nat. Methods 12, 963\u2013965 (2015).","journal-title":"Nat. Methods"},{"key":"7847_CR66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-023-41964-6","volume":"14","author":"X Lyu","year":"2023","unstructured":"Lyu, X., Rowley, M. J., Kulik, M. J., Dalton, S. & Corces, V. G. Regulation of CTCF loop formation during pancreatic cell differentiation. Nat. Commun. 14, 1\u201318 (2023).","journal-title":"Nat. Commun."},{"key":"7847_CR67","doi-asserted-by":"publisher","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","volume":"25","author":"H Li","year":"2009","unstructured":"Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows\u2013Wheeler transform. Bioinformatics 25, 1754\u20131760 (2009).","journal-title":"Bioinformatics"},{"key":"7847_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 25, 2078\u20132079 (2009).","journal-title":"Bioinformatics"},{"key":"7847_CR69","doi-asserted-by":"publisher","first-page":"1","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. 9, 1\u20139 (2008).","journal-title":"Genome Biol."},{"key":"7847_CR70","unstructured":"Kluyver, T. et al. Jupyter notebooks\u2014a publishing format for reproducible computational workflows. In Positioning and Power in Academic Publishing: Players, Agents and Agendas (eds. Loizides, F., Schmidt, B.) 149 (IOS Press, 2016)."},{"key":"7847_CR71","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/s41586-020-2649-2","volume":"585","author":"Harris","year":"2020","unstructured":"Harris & R, C. et al. Array programming with NumPy. Nature 585, 357\u2013362 (2020).","journal-title":"Nature"},{"key":"7847_CR72","doi-asserted-by":"publisher","unstructured":"Pandas-dev\/pandas: pandas. Zenodo https:\/\/doi.org\/10.5281\/zenodo.10957263 (2024).","DOI":"10.5281\/zenodo.10957263"},{"key":"7847_CR73","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, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187\u2013W191 (2014).","journal-title":"Nucleic Acids Res."},{"key":"7847_CR74","doi-asserted-by":"publisher","first-page":"e31","DOI":"10.1158\/0008-5472.CAN-17-0337","volume":"77","author":"JT Robinson","year":"2017","unstructured":"Robinson, J. T., Thorvaldsd\u00f3ttir, H., Wenger, A. M., Zehir, A. & Mesirov, J. P. Variant review with the integrative genomics viewer. Cancer Res. 77, e31\u2013e34 (2017).","journal-title":"Cancer Res."},{"key":"7847_CR75","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.cels.2015.07.012","volume":"3","author":"NC Durand","year":"2016","unstructured":"Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst 3, 99\u2013101 (2016).","journal-title":"Cell Syst"},{"key":"7847_CR76","doi-asserted-by":"publisher","first-page":"2478","DOI":"10.1038\/nprot.2017.124","volume":"12","author":"J Ernst","year":"2017","unstructured":"Ernst, J. & Kellis, M. Chromatin-state discovery and genome annotation with ChromHMM. Nat Protoc 12, 2478\u20132492 (2017).","journal-title":"Nat Protoc"},{"key":"7847_CR77","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-14743-w","volume":"11","author":"J Zhang","year":"2020","unstructured":"Zhang, J. et al. An integrative ENCODE resource for cancer genomics. Nat Commun 11, 3696 (2020).","journal-title":"Nat Commun"},{"key":"7847_CR78","doi-asserted-by":"publisher","first-page":"2980","DOI":"10.1093\/bioinformatics\/btaa073","volume":"36","author":"IM Flyamer","year":"2020","unstructured":"Flyamer, I. M., Illingworth, R. S. & Bickmore, W. A. Coolpup.py: versatile pile-up analysis of Hi-C data. Bioinformatics 36, 2980\u20132985 (2020).","journal-title":"Bioinformatics"},{"key":"7847_CR79","unstructured":"Grandy, W. T. Jr. & Grandy, W. T. Foundations of Statistical Mechanics: Equilibrium Theory Vol. 380 (Reidel, 2012)."},{"key":"7847_CR80","doi-asserted-by":"crossref","unstructured":"Bernardi, R. C., Melo, M. C. R. & Schulten, K. Enhanced sampling techniques in molecular dynamics simulations of biological systems. Biochim. Biophys. Acta 1850, 872\u2013877 (2015).","DOI":"10.1016\/j.bbagen.2014.10.019"},{"key":"7847_CR81","doi-asserted-by":"crossref","unstructured":"Eastman, P. & Pande, V. OpenMM: A hardware-independent framework for molecular simulations. Comput. Sci. Eng. 12, 34\u201339 (2012).","DOI":"10.1109\/MCSE.2010.27"},{"key":"7847_CR82","doi-asserted-by":"crossref","unstructured":"Eastman, P. et al. OpenMM 4: A reusable, extensible, hardware independent library for high performance molecular simulation. J. Chem. Theory Comput. 9, 461\u2013469 (2012)","DOI":"10.1021\/ct300857j"},{"key":"7847_CR83","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1005659","volume":"13","author":"P Eastman","year":"2017","unstructured":"Eastman, P. et al. OpenMM 7: Rapid development of high performance algorithms for molecular dynamics. PLoS Comput. Biol. 13, e1005659 (2017).","journal-title":"PLoS Comput. Biol."},{"key":"7847_CR84","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1038\/nature23884","volume":"549","author":"J Dekker","year":"2017","unstructured":"Dekker, J. et al. The 4D nucleome project. Nature 549, 219\u2013226 (2017).","journal-title":"Nature"},{"key":"7847_CR85","first-page":"1","volume":"13","author":"SB Reiff","year":"2022","unstructured":"Reiff, S. B. et al. The 4D nucleome data portal as a resource for searching and visualizing curated nucleomics data. Nat. Commun. 13, 1\u201311 (2022).","journal-title":"Nat. Commun."}],"container-title":["Communications Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s42003-025-07847-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-025-07847-w","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-025-07847-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,14]],"date-time":"2025-03-14T13:01:56Z","timestamp":1741957316000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s42003-025-07847-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,14]]},"references-count":85,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["7847"],"URL":"https:\/\/doi.org\/10.1038\/s42003-025-07847-w","relation":{},"ISSN":["2399-3642"],"issn-type":[{"value":"2399-3642","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,14]]},"assertion":[{"value":"14 June 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 February 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 March 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"437"}}