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Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl
Open accessAbstract
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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“Since cohesin can remain topologically engaged and slide on both naked DNA42–44 and chromatin,45,46”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [46]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386
Differential expression analysis for sequence count data
Anders, S., & Huber, W. (2010) · Genome Biology · doi:10.1186/gb-2010-11-10-r106 · Cited by 15,581
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,682
A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping
Rao, S. S. P., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.021 · Cited by 9,212
Topological domains in mammalian genomes identified by analysis of chromatin interactions
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., & Ren, B. (2012) · Nature · doi:10.1038/nature11082 · Cited by 6,829
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195
Research works printed but not linked: 1
- Sambrook, J & Russell, D. W. Molecular Cloning: A Laboratory Manual Vol. 3, A9.25–A9.34 (Cold Spring Harbor Laboratory Press, 2001)
Cited by
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Luan, J. Y., Xiang, G., Gómez-García, P. A., Tome, J. M., Zhang, Z., Vermunt, M. W., Zhang, H., Huang, A., Keller, C. A., Giardine, B. M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108783 · Cited by 82
Cohesion and cohesin-dependent chromatin organization
Nishiyama, T. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.11.006 · Cited by 83
Giraud, G., Terrone, S., & Bourgeois, C. F. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.12.234 · Cited by 79
“and orient Cohesin sliding along chromatin fibers (85).”
BackgroundOrientation-dependent Dxz4 contacts shape the 3D structure of the inactive X chromosome
Bonora, G., Deng, X., Fang, H., Ramani, V., Qiu, R., Berletch, J. B., Filippova, G. N., Duan, Z., Shendure, J., Noble, W. S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03694-y · Cited by 72
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Tan, S. Y. X., Zhang, J., & Tee, W. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.931493 · Cited by 86
“These alterations are partially due to the transcription-mediated redistribution of cohesin, forming “cohesin islands” that arise from the accumulation of the cohesin complex at the 3’ ends of active genes caused by the inefficient removal of cohesin, which in turn generates new cohesin-induced DNA loops (Busslinger e…”
BackgroundA cohesin traffic pattern genetically linked to gene regulation
Valton, A.-L., Venev, S. V., Mair, B., Khokhar, E. S., Tong, A. H. Y., Ušaj, M., Chan, K., Pai, A. A., Moffat, J., & Dekker, J. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00890-9 · Cited by 83
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Olan, I., Parry, A. J., Schoenfelder, S., Narita, M., Ito, Y., Chan, A. S. L., Slater, G. S. C., Bihary, D., Bando, M., Shirahige, K., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19878-4 · Cited by 76
Zhu, Y., Denholtz, M., Lu, H., & Murre, C. (2020) · Genes & Development · doi:10.1101/gad.343475.120 · Cited by 70
Specialized functions of cohesins STAG1 and STAG2 in 3D genome architecture
Cuadrado, A., & Losada, A. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.02.024 · Cited by 74
Chromatin remodeling complexes regulate genome architecture in Arabidopsis
Yang, T., Wang, D., Tian, G., Sun, L., Yang, M., Yin, X., Xiao, J. Y., Sheng, Y., Zhu, D., He, H., et al. (2022) · The Plant Cell · doi:10.1093/plcell/koac117 · Cited by 71
Jeppsson, K., Sakata, T., Nakato, R., Milanova, S., Shirahige, K., & Björkegren, C. (2022) · Science Advances · doi:10.1126/sciadv.abn7063 · Cited by 59
Mowel, W. K., McCright, S. J., Kotzin, J. J., Collet, M. A., Uyar, A., Chen, X., DeLaney, A. A., Spencer, S. P., Virtue, A. T., Yang, E., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.012 · Cited by 71
“While CTCF binds specific DNA sequences, recent evidence indicates that transcription significantly contributes to positioning cohesin in the mammalian genome (Busslinger et al., 2017).”
How the Genome Folds: The Biophysics of Four-Dimensional Chromatin Organization
Parmar, J. J., Woringer, M., & Zimmer, C. (2019) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-052118-115638 · Cited by 74
“Moreover, disruption of CTCF (in mouse) results in several new cohesin peaks at the active transcription sites (19), suggesting that absence of CTCF allows cohesin to travel longer distances until it finds another roadblock, which in this case could be active transcription.”
BackgroundInfluentialEnhancer LncRNAs Influence Chromatin Interactions in Different Ways
Hou, Y., Zhang, R., & Sun, X. S. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00936 · Cited by 71
“It is well accepted that loop extrusion should depend on either cohesin slides or ATP-driven motors including transcription and DNA replication (Davidson et al., 2016; Busslinger et al., 2017; Ganji et al., 2018; Vian et al., 2018).”
BackgroundLi, J., Zhang, J., Liu, J., Zhou, Y., Cai, C., Xu, L., Dai, X., Feng, S., Guo, C., Rao, J., et al. (2021) · GigaScience · doi:10.1093/gigascience/giaa142 · Cited by 70
Matthews, B. J., & Waxman, D. J. (2018) · eLife · doi:10.7554/elife.34077 · Cited by 66
“620 621 Cohesin is continuously recycled throughout the genome by loading and release factors [47], and so it is 622 unclear how insulator activity is effectively maintained at TAD and intra-TAD loop anchors in such a dynamic 623 environment.”
BackgroundChen, L.-F., Long, H. K., Park, M., Swigut, T., Boettiger, A. N., & Wysocka, J. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.03.009 · Cited by 66
Transcription factors: building hubs in the 3D space
Giammartino, D. C. D., Polyzos, A., & Apostolou, E. (2020) · Cell Cycle · doi:10.1080/15384101.2020.1805238 · Cited by 67
Gu, B., Comerci, C. J., McCarthy, D. G., Saurabh, S., Moerner, W. E., & Wysocka, J. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.10.001 · Cited by 66
“, 2018), and that RNA polymerase II can reposition cohesin complexes on chromatin (Busslinger et al., 2017; Lengronne et al., 2004).”
BackgroundA walk through the SMC cycle: From catching DNAs to shaping the genome
Oldenkamp, R., & Rowland, B. D. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.04.006 · Cited by 68
See, Y. X., Chen, K., & Fullwood, M. J. (2022) · Genome Research · doi:10.1101/gr.276313.121 · Cited by 64
“Previous studies have linked transcription activity with the formation of chromatin interactions, possibly through cohesin binding and positioning (Busslinger et al. 2017; Isoda et al. 2017; Heinz et al. 2018) and cis -regulatory element mobility (Gu et al. 2018; Naga-shima et al. 2019).”
Orlandini, E., Marenduzzo, D., & Michieletto, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1815394116 · Cited by 65
“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).”
BackgroundHung, T.-C., Kingsley, D. M., & Boettiger, A. N. (2024) · Nature Genetics · doi:10.1038/s41588-023-01641-2 · Cited by 64
“In active cells, PolII binding to Pitx1 and B1 then stalls cohesin extrusion, in a similar way as CTCF does, as suggested by recent experiments and models 81,82 .”
Hypoxic Regulation of Gene Transcription and Chromatin: Cause and Effect
Kindrick, J. D., & Mole, D. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218320 · Cited by 67
“In turn, cohesin may be re-distributed by CCCTC-binding factor (CTCF) in response to transcription [13,14].”
BackgroundAn integrated view of the structure and function of the human 4D nucleome
Dekker, J., Oksuz, B. A., Zhang, Y., Wang, Y., Minsk, M. K., Kuang, S., Yang, L., Gibcus, J. H., Krietenstein, N., Rando, O. J., et al. (2025) · Nature · doi:10.1038/s41586-025-09890-3 · Cited by 64
“The pattern of extrusion along chromosomes is modulated by cis -elements such as enhancers, promoters and insulators 16–18 .”
Lee, D. P., Tan, W. L. W., Anene-Nzelu, C. G., Lee, C. J. M., Li, P. Y., Luu, T. D. A., Chan, C. X., Tiang, Z., Ng, S. L., Huang, X., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.036726 · Cited by 61
Defining Functionally Relevant Spatial Chromatin Domains: It is a TAD Complicated
Sikorska, N., & Sexton, T. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.006 · Cited by 65
Engineering 3D genome organization
Wang, H., Han, M., & Qi, L. S. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-020-00325-5 · Cited by 62
Cohesin Removal Reprograms Gene Expression upon Mitotic Entry
Perea-Resa, C., Bury, L., Cheeseman, I. M., & Blower, M. D. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.01.023 · Cited by 56
Topologically Associating Domains and Regulatory Landscapes in Development, Evolution and Disease
Tena, J. J., & Santos-Pereira, J. M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.702787 · Cited by 65
“, 2017), as well as the depletion of factors regulating cohesin loading on chromatin, which leads to differences in the length of loops formed (Busslinger et al., 2017; Haarhuis et al., 2017; Schwarzer et al., 2017; Wutz et al., 2017).”
BackgroundReed, K. S. M., Davis, E. S., Bond, M. L., Cabrera, A., Thulson, E., Quiroga, I. Y., Cassel, S., Woolery, K. T., Hilton, I. B., Won, H., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111567 · Cited by 56
“cohesin unloader WAPL (Wings apart-like protein homolog) causes cohesin to accumulate at the 3′ end of highly transcribed genes, suggesting that cohesin may be relocated by transcription in the absence of boundary elements (Busslinger et al., 2017).”
BackgroundMethodResultInfluentialNIPBL and cohesin: new take on a classic tale
Gil, D. A., & Losada, A. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.03.006 · Cited by 56
Račko, D., Benedetti, F., Dorier, J., & Stasiak, A. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1091 · Cited by 58
“(A) Cohesin rings preferentially load around transcribed enhancers (67,74).”
BackgroundResultLawrence, E. J., Gao, H., Tock, A. J., Lambing, C., Blackwell, A. R., Feng, X., & Henderson, I. R. (2019) · Current Biology · doi:10.1016/j.cub.2019.06.084 · Cited by 56
Soochit, W., Sleutels, F., Stik, G., Bartkuhn, M., Basu, S., Hernández, S. C., Merzouk, S., Vidal, E., Boers, R., Boers, J., et al. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00722-w · Cited by 55
Self-citationMorgan, S. M., Tanizawa, H., Caruso, L. B., Hulse, M., Kossenkov, A. V., Madžo, J., Keith, K., Tan, Y., Boyle, S., Lieberman, P. M., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27894-1 · Cited by 54
Amat, R., Böttcher, R., Dily, F. L., Vidal, E., Quilez, J., Cuartero, Y., Beato, M., de Nadal, E., & Posas, F. (2018) · Genome Research · doi:10.1101/gr.238527.118 · Cited by 58
“Moreover, our chromatin fractionation experiment showed that the majority of cohesin seemed to remain chromatin-bound, indicating an unspecific distribution due to the lackof available CTCFanchors and the drastically altered Pol II landscape (Busslinger et al. 2017).”
Three-dimensional organization and dynamics of the genome
Szałaj, P., & Plewczyński, D. (2018) · Cell Biology and Toxicology · doi:10.1007/s10565-018-9428-y · Cited by 59
“2017), whereas in human cells, it is translocated from the Nipbl sites to CTCF sites (Busslinger et al. 2017).”
BackgroundMasamsetti, V. P., Low, R. R. J., Mak, K. S., O’Connor, A., Riffkin, C. D., Lamm, N., Crabbé, L., Karlseder, J., Huang, D. C. S., Hayashi, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12255-w · Cited by 56
Arruda, N. L., Carico, Z. M., Justice, M., Liu, Y. F., Zhou, J., Stefan, H. C., & Dowen, J. M. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00353-9 · Cited by 52
Dynamic 3D genome reorganization during senescence: defining cell states through chromatin
Shaban, H. A., & Gasser, S. M. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01197-y · Cited by 59
“Consequently, changes in enhancer-promoter contacts can be characteristic to transcription-dependent cohesin repositioning, by forming cohe-sin islands at the ends of active genes [68].”
Taking cohesin and condensin in context
Yuen, K. C. Y., & Gerton, J. L. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007118 · Cited by 54
Dobersch, S., Rubio, K., Singh, I., Günther, S., Graumann, J., Cordero, J., Castillo‐Negrete, R., Huynh, M. B., Mehta, A., Braubach, P., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21227-y · Cited by 50
Emerging Functions of lncRNA Loci beyond the Transcript Itself
Núñez-Martínez, H. N., & Targa, F. R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116258 · Cited by 53
“Promoter deletion or replacement CRISPR-Cas9 and HDR Yes Yes Yes [12,36,47,48]”
BackgroundCohesin mediates DNA loop extrusion and sister chromatid cohesion by distinct mechanisms
Nagasaka, K., Davidson, I. F., Stocsits, R. R., Tang, W., Wutz, G., Batty, P., Panarotto, M., Litos, G., Schleiffer, A., Gerlich, D. W., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.07.024 · Cited by 53
Self-citationChromatin Remodelers in the 3D Nuclear Compartment
Magaña‐Acosta, M., & Valadéz-Graham, V. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.600615 · Cited by 58
“…while the third hypothesis proposes that the extrusion is actually generated by RNApol II (Davidson et al., 2016; Ocampo-Hafalla et al., 2016; Stigler et al., 2016; Busslinger et al., 2017) suggesting that transcription of the nearby sites is really what defines the formation of these domains.”
BackgroundDynamics of sister chromatid resolution during cell cycle progression
Stanytė, R., Nuebler, J., Blaukopf, C., Hoefler, R., Stocsits, R. R., Peters, J., & Gerlich, D. W. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201801157 · Cited by 49
“It has been hypothesized that cohesin forms TADs by extruding chromatin loops, whereby the boundaries are specified by the protein CTCF (Nasmyth, 2001; Fudenberg et al., 2016; Sanborn et al., 2015; Rao et al., 2017; Busslinger et al., 2017).”
BackgroundInfluentialSelf-citationExtrusion without a motor: a new take on the loop extrusion model of genome organization
Brackley, C. A., Johnson, J., Michieletto, D., Morozov, A. N., Nicodemi, M., Cook, P. R., & Marenduzzo, D. (2018) · Nucleus · doi:10.1080/19491034.2017.1421825 · Cited by 52
“Additionally, cohesin has been observed to translocate away from its loading sites to become enriched elsewhere [15,16].”
BackgroundSequential and directional insulation by conserved CTCF sites underlies the Hox timer in stembryos
Rekaik, H., Lopez‐Delisle, L., Hintermann, A., Mascrez, B., Bochaton, C., Mayran, A., & Duboule, D. (2023) · Nature Genetics · doi:10.1038/s41588-023-01426-7 · Cited by 51
Alteration of genome folding via contact domain boundary insertion
Zhang, D., Huang, P., Sharma, M., Keller, C. A., Giardine, B. M., Zhang, H., Gilgenast, T. G., Phillips‐Cremins, J. E., Hardison, R. C., & Blobel, G. A. (2020) · Nature Genetics · doi:10.1038/s41588-020-0680-8 · Cited by 48
You, Q., Cheng, A. Y., Gu, X., Harada, B. T., Yu, M., Wu, T., Ren, B., Ouyang, Z., & He, C. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0643-8 · Cited by 46
ESCO1/2's roles in chromosome structure and interphase chromatin organizationPreprint
Kawasumi, R., Abe, T., Arakawa, H., Garrè, M., Hirota, K., & Branzei, D. (2017) · Genes & Development · doi:10.1101/gad.306084.117 · Cited by 49
“WAPL is important for the organization of cohesin-defined chromosome territories, as observed in post-mitotic MEFs and haploid human cell lines mutated in WAPL (Tedeschi et al. 2013; Busslinger et al. 2017; Haarhuis et al. 2017).”
BackgroundZNF143 in Chromatin Looping and Gene Regulation
Ye, B., Yang, G., Li, Y., Zhang, C., Wang, Q., & Yu, G. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00338 · Cited by 45
Garcia, P., Fernández‐Hernández, R., Cuadrado, A., Coca, I., Gómez, A., Maqueda, M., Latorre, A., Puisac, B., Ramos, F. J., Sandoval, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24808-z · Cited by 46
The 3D Genome: From Structure to Function
Mohanta, T. K., Mishra, A. K., & Al‐Harrasi, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111585 · Cited by 51
“Transcription leads to the movement of cohesin along the DNA to CTCF sites, suggesting the role of RNA polymerase in loop extrusion [224].”
BackgroundKim, J.-S., He, X., Liu, J., Duan, Z., Kim, T., Gerard, J., Kim, B., Pillai, M. M., Lane, W. S., Noble, W. S., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007832 · Cited by 47
“Chromatin-associated proteins and total soluble proteins were prepared as described (39).”
BackgroundLocal chromatin fiber folding represses transcription and loop extrusion in quiescent cells
Swygert, S. G., Lin, D., Portillo‐Ledesma, S., Lin, P.-Y., Hunt, D. R., Kao, C.-F., Tamar Schlick, A., Noble, W. S., & Tsukiyama, T. (2021) · eLife · doi:10.7554/elife.72062 · Cited by 48
Cell Fate Decisions: The Role of Transcription Factors in Early B-cell Development and Leukemia
Fischer, U., Yang, J. J. J., Ikawa, T., Hein, D., Vicente‐Dueñas, C., Borkhardt, A., & Sánchez-García, I. (2020) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-20-0011 · Cited by 48
The essential but enigmatic regulatory role of HERVH in pluripotency
Sexton, C. E., Tillett, R. L., & Han, M. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.07.007 · Cited by 47
“RNA Pol II and transcription are key factors in cohesin positioning and boundary formation [32,34-36].”
BackgroundMYC-Induced Replicative Stress: A Double-Edged Sword for Cancer Development and Treatment
Curti, L., & Campaner, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126168 · Cited by 44
“In this regard, cohesins, by their coordinated control of DNA repair [101], DNA synthesis [102] and transcription [103], may play a relevant role.”
BackgroundFACT mediates cohesin function on chromatin
García-Luis, J., Lazar‐Stefanita, L., Gutiérrez-Escribano, P., Thierry, A., Cournac, A., García, A., González, S., Sánchez, M., Jarmuz, A., Montoya, A., et al. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0307-x · Cited by 42
Different NIPBL requirements of cohesin-STAG1 and cohesin-STAG2
Gil, D. A., Cuadrado, A., Giménez-Llorente, D., Rodríguez-Corsino, M., & Losada, A. (2023) · Nature Communications · doi:10.1038/s41467-023-36900-7 · Cited by 43
Wu, H., Zhang, J., Tan, L., & Xie, X. S. (2025) · Nature Genetics · doi:10.1038/s41588-025-02247-6 · Cited by 44
Ulianov, S. V., Tachibana-Konwalski, K., & Razin, S. V. (2017) · BioEssays · doi:10.1002/bies.201700104 · Cited by 43
Wapl releases Scc1-cohesin and regulates chromosome structure and segregation in mouse oocytes
Silva, M. C. C., Powell, S. T., Ladstätter, S., Gassler, J., Stocsits, R. R., Tedeschi, A., Peters, J., & Tachibana, K.-E. K. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.201906100 · Cited by 42
“mice were bred on a primarily C57BL/6J background (Busslinger et al., 2017).”
BackgroundSelf-citationDenholtz, M., Zhu, Y., He, Z., Lu, H., Isoda, T., Döhrmann, S., Nizet, V., & Murre, C. (2020) · Genes & Development · doi:10.1101/gad.333708.119 · Cited by 40
“Cohesin is loaded onto transcribed regions located throughout loop bodies (Busslinger et al. 2017).”
BackgroundThe functional impact of nuclear reorganization in cellular senescence
Rocha, A., Dalgarno, A., & Neretti, N. (2022) · Briefings in Functional Genomics · doi:10.1093/bfgp/elab012 · Cited by 38
“impeding CTCF; this creates de novo cohesin peaks and plausibly de novo loops [86, 87].”
BackgroundStructural analyses of inositol phosphate second messengers bound to signaling effector proteins
Blind, R. D. (2019) · Advances in Biological Regulation · doi:10.1016/j.jbior.2019.100667 · Cited by 36
“DNA-loops are three dimensional chromatin “loop” structures which form at sites where the transcription factor CTCF binds DNA (Busslinger et al., 2017; Wendt et al., 2008).”
BackgroundSingle‐cell imaging of genome organization and dynamics
Xie, L., & Liu, Z. J. (2021) · Molecular Systems Biology · doi:10.15252/msb.20209653 · Cited by 35
Chromatin organization by an interplay of loop extrusion and compartmental segregationPreprint
Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N. A., & Mirny, L. A. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/196261 · Cited by 37
DNA double-strand break end synapsis by DNA loop extrusion
Yang, J. H., Brandão, H. B., & Hansen, A. S. (2023) · Nature Communications · doi:10.1038/s41467-023-37583-w · Cited by 36
“Synapsis 376 has largely been assumed to occur by passive 3D diffusion [22].”
InfluentialCaenorhabditis elegans Dosage Compensation: Insights into Condensin-Mediated Gene Regulation
Albritton, S. E., & Ercan, S. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.09.010 · Cited by 33
Eckardt, J., Stasik, S., Röllig, C., Sauer, T., Scholl, S., Hochhaus, A., Crysandt, M. M., Brümmendorf, T. H., Naumann, R., Steffen, B., et al. (2023) · Blood Cancer Journal · doi:10.1038/s41408-023-00790-1 · Cited by 37
“Additionally, the cohesion complex plays a key role in regulation of both structure and function of chromatin where it is recruited to chromatin binding sites via CCCTF-binding-factor [5].”
BackgroundHiGlass: Web-based Visual Exploration and Analysis of Genome Interaction MapsPreprint
Kerpedjiev, P., Abdennur, N. A., Lekschas, F., McCallum, C., Dinkla, K., Strobelt, H., Luber, J. M., Ouellette, S., Azhir, A., Kumar, N., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/121889 · Cited by 43
Hsieh, T.-H. S., Cattoglio, C., Slobodyanyuk, E., Hansen, A. S., Darzacq, X., & Tjian, R. (2021) · doi:10.1101/2021.07.14.452365 · Cited by 42
How DNA loop extrusion mediated by cohesin enables V(D)J recombination
Peters, J. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.11.007 · Cited by 37
Self-citationRapid depletion of CTCF and cohesin proteins reveals dynamic features of chromosome architecturePreprint
Liu, N.-Q., Magnitov, M. D., Schijns, M. M. G. A., van Schaik, T., van der Weide, R. H., Teunissen, H., van Steensel, B., & de Wit, E. (2021) · bioRxiv · doi:10.1101/2021.08.27.457977 · Cited by 34
“In addition to CTCF, RNA polymerase II is also thought to affect the cohesin positioning at the actively transcribed gene body (Busslinger et al., 2017; Heinz et al., 2018).”
BackgroundInfluentialRahman, S., Dong, P., Apontes, P., Fernando, M. B., Kosoy, R., Townsley, K. G., Girdhar, K., Bendl, J. M., Shao, Z., Misir, R., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad798 · Cited by 32
“As cohesin was shown to be recruited to TSS and translocated in the direction of transcription ( 87 ), along with recent evidence demonstrating that transcription-dependent cohesin repositioning rewires chromatin loops ( 88 ), neuronal differential TADs may form primarily through loop extrusion…”
BackgroundExtensive mutual influences of SMC complexes shape 3D genome folding
Zhao, H., Shu, L., Qin, S., Lyu, F., Liu, F., Lin, E., Xia, S., Wang, B., Wang, M., Shan, F., et al. (2025) · Nature · doi:10.1038/s41586-025-08638-3 · Cited by 33
Galupa, R., & Heard, É. (2017) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2017.82.035030 · Cited by 30
Cohesin-mediated 3D contacts tune enhancer-promoter regulationPreprint
Guckelberger, P., Doughty, B. R., Munson, G., Rao, S. S. P., Tan, Y., Cai, X. S., Fulco, C. P., Nasser, J., Mualim, K. S., Bergman, D. T., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.12.603288 · Cited by 33
“Cohesin controls 3D genome organization through loop extrusion 19,21,54 .”
BackgroundSpatial Genome Organization: From Development to Disease
Sivakumar, A., Heras, J. I. D. L., & Schirmer, E. C. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00018 · Cited by 34
Cohesin organizes 3D DNA contacts surrounding active enhancers in C. elegansPreprint
Kim, J., Wang, H., & Ercan, S. (2025) · Genome Research · doi:10.1101/gr.279365.124 · Cited by 31
Kant, A., Guo, Z., Vinayak, V., Neguembor, M. V., Li, W. S., Agrawal, V., Pujadas-Liwag, E. M., Almassalha, L. M., Backman, V., Lakadamyali, M., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48698-z · Cited by 31
“The experimentally observed role of RNAPII-mediated transcription in DNA supercoiling and subsequent loop extrusion 2,12,19,20,33,57 – 60 has also been studied using molecular dynamics simulations and polymer physics-based models at nanoscale 20,61 – 66 .”
BackgroundInfluentialCTCF depletion decouples enhancer-mediated gene activation from chromatin hub formation
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. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01555-z · Cited by 35
“Capture-C samples were sequenced with 150 cycles of paired-end reads, while Tri-C samples were sequenced with 300 cycles of paired-end reads.”
DNA Supercoiling, Topoisomerases, and Cohesin: Partners in Regulating Chromatin Architecture?
Björkegren, C., & Baranello, L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19030884 · Cited by 31
“positioned asymmetrically in such a manner that suggests that transcription of the more active genes pushes cohesin into the more weakly expressed gene [28].”
BackgroundLi, H., Dalgleish, J. L. T., Lister, G., Maristany, M. J., Huertas, J., Dopico-Fernandez, A. M., Hamley, J. C., Denny, N., Bloye, G., Zhang, W., et al. (2025) · Cell · doi:10.1016/j.cell.2025.10.013 · Cited by 35
“7,70 In addition, microscopy studies have shown that CTCF and cohesin localize to the interchromatin and perichromatin compartments.”
Álvarez, V., Bandau, S., Jiang, H., Rios-Szwed, D. O., Hukelmann, J. L., Garcia-Wilson, E., Wiechens, N., Griesser, E., ten Have, S., Owen‐Hughes, T., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.111996 · Cited by 27
“41 Altogether, this analysis reveals differences in abundance of SMC rings and their regulatory factors and raises the possibility that assembling and disassembling mitotic chromosomes may be overcome by distinct strategies in euchromatin and heterochromatin.”
BackgroundTranscription regulates the spatio-temporal dynamics of genes through micro-compartmentalization
Salari, H., Fourel, G., & Jost, D. (2024) · Nature Communications · doi:10.1038/s41467-024-49727-7 · Cited by 35
CTCF blocks antisense transcription initiation at divergent promoters
Luan, J. Y., Vermunt, M. W., Syrett, C. M., Coté, A., Tome, J. M., Zhang, H., Huang, A., Luppino, J. M., Keller, C. A., Giardine, B. M., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00855-y · Cited by 29
Cohesin regulates alternative splicing
Singh, A. K., Chen, Q., Nguyen, C. D., Meerzaman, D. M., & Singer, D. S. (2023) · Science Advances · doi:10.1126/sciadv.ade3876 · Cited by 29
Connected Gene Communities Underlie Transcriptional Changes in Cornelia de Lange Syndrome
Boudaoud, I., Fournier, É., Baguette, A., Vallée, M., Lamaze, F. C., Droit, A., & Bilodeau, S. (2017) · Genetics · doi:10.1534/genetics.117.202291 · Cited by 28
“NIPBL loads cohesin at the promoter of active genes from which cohesin is translocated using Pol II (Lengronne et al. 2004; Busslinger et al. 2017).”
BackgroundMethodInfluentialExtrusion fountains are restricted by WAPL-dependent cohesin release and CTCF barriers
Liu, N. Q., Magnitov, M. D., Schijns, M. M. G. A., van Schaik, T., Teunissen, H., van Steensel, B., & de Wit, E. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf549 · Cited by 33
Xu, D., Ma, R., Zhang, J., Liu, Z., Wu, B., Peng, J., Zhai, Y., Gong, Q., Shi, Y., Wu, J., et al. (2018) · The Journal of Physical Chemistry Letters · doi:10.1021/acs.jpclett.8b01440 · Cited by 25
Bansal, K., Michelson, D. A., Ramírez, R. N., Viny, A. D., Levine, R. L., Benoist, C. O., & Mathis, D. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2110991118 · Cited by 26
Into the Fourth Dimension: Dysregulation of Genome Architecture in Aging and Alzheimer’s Disease
Winick‐Ng, W., & Rylett, R. J. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00060 · Cited by 28
“Mutations in cohesin, a protein that works together with CTCF to spatially organize chromatin loops (Busslinger et al., 2017; Hanssen et al., 2017), causes Cornelia de Lange syndrome (Musio et al., 2006).”
BackgroundMatthews, B. J., & Waxman, D. J. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00350-y · Cited by 22
Live imaging of marked chromosome regions reveals their dynamic resolution and compaction in mitosis
Eykelenboom, J. K., Gierliński, M., Yue, Z., Hégarat, N., Pollard, H. J., Fukagawa, T., Hochegger, H., & Tanaka, T. U. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201807125 · Cited by 26
Co-depletion of NIPBL and WAPL balance cohesin activity to correct gene misexpression
Luppino, J. M., Field, A. R., Nguyen, S. C., Park, D. S., Shah, P. P., Abdill, R. J., Lan, Y., Yunker, R., Jain, R., Adelman, K., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010528 · Cited by 34
Metadata
- 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
- Venue
- Nature
- Published
- 2017-04
- Volume
- 544
- Issue
- 7651
- Pages
- 503-507
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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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