Cited by 475Genomics and Chromatin DynamicsChromatin Remodeling and CancerNuclear Structure and Function

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Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl

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Busslinger, Georg A., Stocsits, Roman R., van der Lelij, Petra, Axelsson, Elin, Tedeschi, Antonio, Galjart, Niels, Peters, Jan-Michael·2017·Nature

DOI 10.1038/nature22063PMC PMC6080695

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Abstract

Mammalian genomes are spatially organized by CCCTC-binding factor (CTCF) and cohesin into chromatin loops and topologically associated domains, which have important roles in gene regulation and recombination. By binding to specific sequences, CTCF defines contact points for cohesin-mediated long-range chromosomal cis-interactions. Cohesin is also present at these sites, but has been proposed to be loaded onto DNA elsewhere and to extrude chromatin loops until it encounters CTCF bound to DNA. How cohesin is recruited to CTCF sites, according to this or other models, is unknown. Here we show that the distribution of cohesin in the mouse genome depends on transcription, CTCF and the cohesin release factor Wings apart-like (Wapl). In CTCF-depleted fibroblasts, cohesin cannot be properly recruited to CTCF sites but instead accumulates at transcription start sites of active genes, where the cohesin-loading complex is located. In the absence of both CTCF and Wapl, cohesin accumulates in up to 70 kilobase-long regions at 3'-ends of active genes, in particular if these converge on each other. Changing gene expression modulates the position of these 'cohesin islands'. These findings indicate that transcription can relocate mammalian cohesin over long distances on DNA, as previously reported for yeast cohesin, that this translocation contributes to positioning cohesin at CTCF sites, and that active genes can be freed from cohesin either by transcription-mediated translocation or by Wapl-mediated release.

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Background
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Background
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Background
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Influential
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Method
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Hot debate in hot springs: Report on the second international meeting on SMC proteins
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“Dale Dorsett (St. Louis U., USA) and Jan- Michael Peters (IMP, Austria) reported genomewide distribution and relocation of cohesin and its related proteins in Drosophila and mammalian cells, respectively (Busslinger et al., 2017).”
Background
Chromatin stability generated by stochastic binding and unbinding of cross-linkers at looping sites revealed by Markov models
Papale, A., & Holcman, D. (2021) · Physical Biology · doi:10.1088/1478-3975/abf93a · Cited by 2
“These loops are controlled by speciﬁc structures such as the cohesin ring and CTCF chromatin binding sites [6–12], concentrated in the majority of borders that demarcate TADs [13].”
A Robust Protocol for Investigating the Cohesin Complex by ChIP-Sequencing
Gines, M. M., & Wendt, K. S. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2140-0_7 · Cited by 2
Rearrangement of T Cell genome architecture regulates GVHD
Sun, Y., Dotson, G. A., Muir, L. A., Ronquist, S., Oravecz-Wilson, K. I., Peltier, D., Seike, K., Li, L., Meixner, W., Rajapakse, I., et al. (2022) · iScience · doi:10.1016/j.isci.2022.104846 · Cited by 2
MYC overexpression leads to increased chromatin interactions at superenhancers and c-Myc binding sitesPreprint
See, Y. X., Chen, K., & Fullwood, M. J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.04.425344 · Cited by 2
Oncogenic c-Myc induces replication stress by increasing cohesins chromatin occupancyPreprint
Peripolli, S., Singh, T., Patel, H., Meneguello, L., Kiso, K., Thorpe, P. H., Bertoli, C., & de Bruin, R. A. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.25.453647 · Cited by 3
Context-dependent 3D genome regulation by cohesin and related factorsPreprint
Nakato, R., Sakata, T., Wang, J., Nagai, L. A. E., Oba, G. M., Bando, M., & Shirahige, K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.24.493188 · Cited by 2
Cohesin regulates promoter-proximal pausing of RNA Polymerase II by limiting recruitment of super elongation complexPreprint
Tei, S., Sakata, T., Yoshimura, A., Natsume, T., Kanemaki, M. T., Bando, M., & Shirahige, K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.15.584908 · Cited by 2
“9,25,12,13,26 Thus, the contribution of cohesin-mediated promoter-enhancer interactions to gene expression remains unclear.”
Background
A guide to studying 3D genome structure and dynamics in the kidney
Beliveau, B. J., & Akilesh, S. (2024) · Nature Reviews Nephrology · doi:10.1038/s41581-024-00894-2 · Cited by 1
Promoter- and enhancer-dependent cohesin loading initiates chromosome looping to fold Tcrb loci for long-range recombination
Allyn, B. M., Hayer, K. E., Oyeniran, C., Nganga, V. K., Lee, K. D., Saçan, A., Oltz, E. M., & Bassing, C. H. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116133 · Cited by 2
Distinct and compensatory roles of STAG1 and STAG2 in post-mitotic genome refolding
Wang, M., Zhang, Y., Shan, F., Pei, C., Liu, F., Xia, S., Shu, L., Li, B., Jing, D., Weng, Y., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-74870-8 · Cited by 1
“Reformation of structural loops after mitosis is tightly controlled by cohesin recruitment 25,34,36 .”
CTCF’s loop-independent functions prevail over chromatin looping in the acute degradation system
Hu, G., Ji, B., Zhang, J., Liu, Y., Lu, Y., Wang, X., Ren, H., Liao, J., & Yao, H. (2025) · Protein & Cell · doi:10.1093/procel/pwaf087 · Cited by 1
The sex-biased chromatin modifier SMC1A promotes autoimmunity by shaping inflammatory pathways in patients with SLE
Κοσμαρά, Δ., Papanikolaou, S., Stathopoulou, C., Papamatheakis, D.-A., Vatsellas, G., Cimmarrusti, A., Banos, A., Sidiropoulos, P. I., Lavigne, M. D., Verginis, P., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65309-7 · Cited by 1
“Together with other subunits (SMC3, RAD21, STAG1/2),SMC1A forms the cohesin complex involved in chromosome segregation, homologous recombination, and genome regulation 44 – 46 .”
A functional overlap between actively transcribed genes and chromatin insulator elements
Cornell, L., Harrold, C. L., Holliman, S., Tsang, F. H., Gosden, M. E., Hanssen, L. E., Stolper, R. J., Downes, D. J., Biggs, D., Preece, C., et al. (2026) · The EMBO Journal · doi:10.1038/s44318-026-00730-2 · Cited by 3
“…genomes, transcription has been also been associated with domain boundaries (Bonev et al, 2017; Dixon et al, 2012); reported to interact with the cohesin loop extrusion machinery (Busslinger et al, 2017); and with disruption of expression of downstream genes (Bozhilov et al, 2021; Cho et al, 2018).”
RNAPII and DNA supercoiling regulate cohesin engagement in neurons
Crewe, M., Delint‐Ramírez, I., Halawa, O., Heady, L., & Madabhushi, R. (2026) · Nucleic Acids Research · doi:10.1093/nar/gkag553 · Cited by 1
“These results are consistent with observations in other cells suggesting that either RNAPII or R-loops act as barriers for cohesin-mediated loop extrusion [ 25 , 27 , 67–69 ].”
Promoter strength and position govern promoter competition through transcript-dependent insulation
Koska, M., Nagano, M., Swigut, T., Boettiger, A. N., Hansen, A. S., & Wysocka, J. (2026) · Nature Genetics · doi:10.1038/s41588-026-02691-y · Cited by 6
STAG2-RAD21 complex: A unidirectional DNA ratchet mechanism in loop extrusion
Ros‐Pardo, D., Gómez‐Puertas, P., & Marcos‐Alcalde, Í. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.133822 · Cited by 1
“During interphase, loop extrusion organizes chromatin in TADs (Topologically Associating Domains) which are limited by DNA-bound transcriptional factors CTCF (CCCTC-binding factor) [25,26].”
Three-dimensional genome rewiring during the development of antibody-secreting cells
Chan, W. F., Johanson, T. M., & Allan, R. S. (2020) · Biochemical Society Transactions · doi:10.1042/bst20191104 · Cited by 1
Chromatin: A Semi-Structured Polymer
Dawson, W., Łaźniewski, M., & Plewczyński, D. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.20240-9 · Cited by 1
The CTCF Anatomy of Topologically Associating DomainsPreprint
Nanni, L., Wang, C., Manders, F., Groh, L. A., Haro, P., Oldenkamp, R., Ceri, S., & Logie, C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/746610 · Cited by 1
“In human cells, Cohesin complexes only accumulate at RNA polymerase II poly-adenylation sites when CTCF is absent (Busslinger et al., 2017).”
Background
Upon microbial challenge human neutrophils undergo rapid changes in nuclear architecture to orchestrate an immediate inflammatory gene programPreprint
Denholtz, M., Zhu, Y., He, Z., Lu, H., Isoda, T., Döhrmann, S., Nizet, V., & Murre, C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/808568 · Cited by 1
MyoD is a structure organizer of 3D genome architecture in muscle cellsPreprint
Chen, Q., Chen, F., Wang, R., Shi, M., Chen, A. K., Ma, Z., Li, G., Wang, M., Li, H., Zhang, X., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.29.273375 · Cited by 1
From DNA Topology to Pubertal Onset: Using Integrative Genomic Approaches to Study Transcriptional Regulation
Hou, H. (2019) · TSpace (University of Toronto) · Cited by 1
Different NIPBL requirements of cohesin-STAG1 and cohesin-STAG2Preprint
Gil, D. A., Cuadrado, A., Giménez-Llorente, D., Rodríguez-Corsino, M., & Losada, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.29.518367 · Cited by 1
RNA Pol II antagonises mitotic chromatin folding and chromosome segregation by condensinPreprint
Lebreton, J., Colin, L., Chatre, E., & Bernard, P. (2023) · bioRxiv · doi:10.1101/2023.08.08.552486 · Cited by 1
BRWD1 establishes epigenetic states for germinal center initiation, maintenance, and functionPreprint
Wright, N., Kennedy, D. E., Ai, J., Veselits, M., Attaway, M., Yoon, Y. M., Durkee, M. S., Veselits, J., Maienschein‐Cline, M., Mandal, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.25.591154 · Cited by 1
CTCF depletion decouples enhancer-mediated gene activation from chromatin hub formation during cellular differentiationPreprint
Karpińska, M. A., Zhu, Y., Ghazvini, Z. F., Ramasamy, S., Barbieri, M., Cao, T. B. N., Varahram, N., Aljahani, A., Lidschreiber, M., Papantonis, A., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.20.624447 · Cited by 1
Cohesin extrudes chromatin loop unidirectionally through two modes of mechanisms in human cellsPreprint
Wang, P., Meng, L., Jiang, L., Li, Y., Huang, J., Tiancheng, Y. U., Chai, H., Kim, M., Wang, X., & Ruan, Y. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.01.722300 · Cited by 1
Conserved lifestyle-associated chromosome architectures across mammalian symbiontsPreprint
Viehboeck, T., Krause, N., Weber, P., Shea, E., Noetzel, V., Pende, N., Gölles-Kirth, H., Varoquaux, N., Boccard, F., Junier, I., et al. (2026) · bioRxiv · doi:10.64898/2026.07.20.739713 · Cited by 1
“These loops are observed as corner peaks at TAD boundaries and result from the structural maintenance of chromosomes (SMC) cohesin complexes and the CCCTC-binding factor (CTCF) binding the DNA at specific sites (Busslinger et al., 2017; Wutz et al., 2017; Sanborn et al., 2015).”
Promoter interactions direct chromatin folding in embryonic stem cells
Sanyal, S., Molnárová, L., & Gregáň, J. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3421 · Cited by 1
Roles of the Brca2 and Wapl complexes with Pds5 in sister chromatid cohesion, cohesin localization, and gene expression
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Genomic dissection of Systemic Lupus Erythematosus: Distinct Susceptibility, Activity and Severity SignaturesPreprint
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Twenty-First Century Glucocorticoid Receptor Molecular Biology
Wang, C., Oldenkamp, R., Oellers, R., & Logie, C. (2018) · InTech eBooks · doi:10.5772/intechopen.72016
“Cohesin is most likely loaded onto its chromatid substrate by the NIPBL2/Mau2 cohesin-loading complex, which is enriched at transcription start sites (TSS) [60, 61].”
Background
Novel Approaches for Pluripotent Reprogramming
Weltner, J. (2018) · Työväentutkimus Vuosikirja
Synergy of Topoisomerase and Structural-Maintenance-of-Chromosomes Proteins Creates a Universal Pathway to Simplify Genome TopologyPreprint
Orlandini, E., Marenduzzo, D., & Michieletto, D. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/410019
Organizing Principles for the Spatial Folding of Chromosomes
Josipović, N., & Papantonis, A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814879-2.00005-4
Synergy of Topoisomerase and Structural-Maintenance-of-Chromosomes Proteins Creates a Universal Pathway to Simplify Genome TopologyPreprint
Orlandini, E., Marenduzzo, D., & Michieletto, D. (2018) · arXiv (Cornell University) · doi:10.48550/arxiv.1809.01267
“While a population of condensins is stably bound in mitosis (55), cohesin is known to turn over in about τ =20 min through interphase (56).”
Background
Compartments in the Ring
Nishiyama, T. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.002
The Effect of rs77275268 on Gene Expression at the Transcriptional Hub at 6q25.1
Mackie, S. (2020) · Otago University Research Archive (University of Otago)
Extrusion without a motor: a new take on the loop extrusion model of genome organizationPreprint
Brackley, C. A., Johnson, J., Michieletto, D., Morozov, A. N., Nicodemi, M., Cook, P. R., & Marenduzzo, D. (2020) · arXiv (Cornell University) · doi:10.48550/arxiv.2010.02548
“Additionally, cohesin has been observed to translocate away from its loading sites to become enriched elsewhere [15,16].”
Background
Nipped-B-like Protein Sensitizes Esophageal Squamous Cell Carcinoma Cells to Cisplatin via Upregulation of PUMA
Zhang, S., Zhou, Y. F., Wang, Q., Donahue, K., Feng, J., Yao, Y., Chen, A., Li, X., & Hong, L. (2020) · Technology in Cancer Research & Treatment · doi:10.1177/1533033820960726
“Increasing evidence has shown that NIPBL is involved in the transcriptional regulation of downstream genes by recruiting the cohesin complex and CCCTC-binding factor (CTCF) to maintain the 3-dimensional structure and stability of genomes, and long-range interactions of chromatin.(31-33) Furthermore, NIPBL has been sho…”
Background
Eukaryotic Genome in Three Dimensions
Razin, S. V., Gavrilov, A. A., & Ulianov, S. V. (2020) · Springer eBooks · doi:10.1007/978-3-030-62532-0_2

Authors: Busslinger, G. A., Stocsits, R. R., van der Lelij, P., Axelsson, E., Tedeschi, A., Galjart, N., & Peters, J.-M.
Affiliations: Research Institute of Molecular Pathology (AT)
Erasmus MC (NL)
Corresponding author: Peters, Jan-Michael
ORCID: Busslinger, Georg A.
Stocsits, Roman R.
Axelsson, Elin
Tedeschi, Antonio
Galjart, Niels
Peters, Jan-Michael
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2017-04
Volume: 544
Issue: 7651
Pages: 503-507
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature22063
PMC: PMC6080695
OpenAlex: W2607008467
Cited by: 468
References: 51
Citations by year: 2026: 30 · 2025: 36 · 2024: 36 · 2023: 45 · 2022: 58 · 2021: 52 · 2020: 59 · 2019: 67 · 2018: 50 · 2017: 35
FWCI: 23.91
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Keywords: cohesin, CTCF, WAPL, transcription, cohesin loading, chromatin looping, topologically associating domains, 3D genome organization, transcription start sites, mouse genome, cis-interactions, gene expression regulation, recombination, mouse fibroblasts
MeSH terms: CCCTC-Binding Factor, Cohesins, Animals, Binding Sites, Cells, Cultured, Chromatin, Chromosomal Proteins, Non-Histone, DNA, Female, Fibroblasts, Male, Proteins, Chondroitin Sulfate Proteoglycans, Repressor Proteins, Transcription, Genetic, Genome, Cell Cycle Proteins, Protein Transport, Transcription Initiation Site, Chromosomes, Mammalian, Mice

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Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl

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