Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins
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Abstract
Mammalian genomes are spatially organized into compartments, topologically associating domains (TADs), and loops to facilitate gene regulation and other chromosomal functions. How compartments, TADs, and loops are generated is unknown. It has been proposed that cohesin forms TADs and loops by extruding chromatin loops until it encounters CTCF, but direct evidence for this hypothesis is missing. Here, we show that cohesin suppresses compartments but is required for TADs and loops, that CTCF defines their boundaries, and that the cohesin unloading factor WAPL and its PDS5 binding partners control the length of loops. In the absence of WAPL and PDS5 proteins, cohesin forms extended loops, presumably by passing CTCF sites, accumulates in axial chromosomal positions (vermicelli), and condenses chromosomes. Unexpectedly, PDS5 proteins are also required for boundary function. These results show that cohesin has an essential genome-wide function in mediating long-range chromatin interactions and support the hypothesis that cohesin creates these by loop extrusion, until it is delayed by CTCF in a manner dependent on PDS5 proteins, or until it is released from DNA by WAPL.
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Contacts between convergent CTCF binding sites are established by the extrusion of chromatin loops with cohesin.
“Contacts between convergent CTCF binding sites are established by the extrusion of chromatin loops with cohesin [42,46,48,93].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [48]
The Results report that 73.8% of the analyzed loops in control cells were anchored at convergent CTCF sites, and the Introduction describes cohesin’s role in loop formation. But the Introduction calls loop extrusion a hypothesis that could explain why convergent sites come together; it does not establish extrusion as the mechanism. (LLM, conf=0.88)
Experimental — accuracy not yet measuredConvergent binding sites for CTCF located at TAD borders block the movement of loop extruders.
“Convergent binding sites for the versatile transcription factor CTCF (CCCTC-binding factor) located at TAD borders [46] block the movement of loop extruders [47,48,49].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [48]
The CTCF Y226A F228A mutation, similar to CTCF depletion, causes only a slight change in the contact probability profile.
“The CTCF Y226A F228A mutation, like CTCF depletion, only slightly affects the contact probability profile.”
From The structural basis for cohesin–CTCF-anchored loops (2020) · cites this paper as [12]
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Crystal structure of the cohesin loader Scc2 and insight into cohesinopathy
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How cohesin and CTCF cooperate in regulating gene expression
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Self-citationMetazoan Scc4 Homologs Link Sister Chromatid Cohesion to Cell and Axon Migration Guidance
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Scc2/Nipbl hops between chromosomal cohesin rings after loading
Rhodes, J., Mazza, D., Nasmyth, K., & Uphoff, S. (2017) · eLife · doi:10.7554/elife.30000 · Cited by 99 · see citing works
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Self-citationCohesin’s ATPase Activity Couples Cohesin Loading onto DNA with Smc3 Acetylation
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Self-citationGene regulation and chromatin organization: relevance of cohesin mutations to human disease
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SNW1 enables sister chromatid cohesion by mediating the splicing of sororin and APC2 pre‐mRNAs
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Self-citationMultilayer chromosome organization through DNA bending, bridging and extrusion.
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Bladder cancer: 4 big questions
Berdik, C. (2017) · Nature · doi:10.1038/551s51a · Cited by 54 · see citing works
Topology and structure of an engineered human cohesin complex bound to Pds5B
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Self-citationPreservation of Chromatin Organization after Acute Loss of CTCF in Mouse Embryonic Stem CellsPreprint
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Self-citationMULTOVL: fast multiple overlaps of genomic regions
Aszódi, A. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts607 · Cited by 37 · see citing works
Generation and validation of homozygous fluorescent knock-in cells using CRISPR/Cas9 genome editingPreprint
Koch, B., Nijmeijer, B., Kueblbeck, M., Cai, Y., Walther, N., & Ellenberg, J. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/188847 · Cited by 13 · see citing works
Self-citationClosing the MCM cycle at replication termination sites
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Author response: Scc2/Nipbl hops between chromosomal cohesin rings after loading
Rhodes, J., Mazza, D., Nasmyth, K., & Uphoff, S. (2017) · eLife · doi:10.7554/elife.30000.020 · Cited by 8 · see citing works
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Organizational principles of 3D genome architecture
Rowley, M. J., & Corces, V. G. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0060-8 · Cited by 1,171 · see citing works
Two independent modes of chromatin organization revealed by cohesin removal
Schwarzer, W., Abdennur, N., Goloborodko, A., Pekowska, A., Fudenberg, G., Loe-Mie, Y., Fonseca, N. A., Huber, W., Haering, C. H., Mirny, L., et al. (2017) · Nature · doi:10.1038/nature24281 · Cited by 1,196 · see citing works
Long-range enhancer–promoter contacts in gene expression control
Schoenfelder, S., & Fraser, P. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0128-0 · Cited by 1,102 · see citing works
Self-citationDNA loop extrusion by human cohesin
Davidson, I. F., Bauer, B., Goetz, D., Tang, W., Wutz, G., & Peters, J.-M. (2019) · Science · doi:10.1126/science.aaz3418 · Cited by 863 · see citing works
Self-citationThe role of 3D genome organization in development and cell differentiation
Zheng, H., & Xie, W. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0132-4 · Cited by 711 · see citing works
The Self-Organizing Genome: Principles of Genome Architecture and Function
Misteli, T. (2020) · Cell · doi:10.1016/j.cell.2020.09.014 · Cited by 706 · see citing works
“(B) TADs form via loop-extrusion generated by the cohesin motor (light blue).”
InfluentialHuman cohesin compacts DNA by loop extrusion
Kim, Y., Shi, Z., Zhang, H., Finkelstein, I. J., & Yu, H. (2019) · Science · doi:10.1126/science.aaz4475 · Cited by 701 · see citing works
Chromatin organization by an interplay of loop extrusion and compartmental segregation
Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N. A., & Mirny, L. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717730115 · Cited by 617 · see citing works
“The characteristic hump in contact probability scaling extends to significantly larger distances, reflecting larger loops (14).”
BackgroundInfluentialPrinciples of genome folding into topologically associating domains
Szabo, Q., Bantignies, F., & Cavalli, G. (2019) · Science Advances · doi:10.1126/sciadv.aaw1668 · Cited by 594 · see citing works
Transcription factors and 3D genome conformation in cell-fate decisions
Stadhouders, R., Filion, G. J. P., & Graf, T. (2019) · Nature · doi:10.1038/s41586-019-1182-7 · Cited by 519 · see citing works
Genome folding through loop extrusion by SMC complexes
Davidson, I. F., & Peters, J. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00349-7 · Cited by 507 · see citing works
Self-citationThe structural basis for cohesin–CTCF-anchored loops
Li, Y., Haarhuis, J. H. I., Sedeño Cacciatore, Á., Oldenkamp, R., van Ruiten, M. S., Willems, L., Teunissen, H., Muir, K. W., de Wit, E., Rowland, B. D., et al. (2020) · Nature · doi:10.1038/s41586-019-1910-z · Cited by 459 · see citing works
Dynamics of CTCF- and cohesin-mediated chromatin looping revealed by live-cell imaging
Gabriele, M., Brandão, H. B., Grosse-Holz, S., Jha, A., Dailey, G. M., Cattoglio, C., Hsieh, T.-H. S., Mirny, L., Zechner, C., & Hansen, A. S. (2022) · Science · doi:10.1126/science.abn6583 · Cited by 506 · see citing works
“potentially allowing it to extrude longer and more stable loops (29, 31), WAPL depletion decreased the 3D distances”
BackgroundTranscription Elongation Can Affect Genome 3D Structure
Heinz, S., Texari, L., Hayes, M. G. B., Urbanowski, M., Chang, M. W., Givarkes, N., Rialdi, A., White, K. M., Albrecht, R. A., Pache, L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.047 · Cited by 453 · see citing works
Extensive Heterogeneity and Intrinsic Variation in Spatial Genome Organization
Finn, E. H., Pegoraro, G., Brandão, H. B., Valton, A.-L., Oomen, M. E., Dekker, J., Mirny, L., & Misteli, T. (2019) · Cell · doi:10.1016/j.cell.2019.01.020 · Cited by 459 · see citing works
Hsieh, T.-H. S., Cattoglio, C., Slobodyanyuk, E., Hansen, A. S., Darzacq, X., & Tjian, R. (2022) · Nature Genetics · doi:10.1038/s41588-022-01223-8 · Cited by 406 · see citing works
Understanding 3D genome organization by multidisciplinary methods
Jerković, I., & Cavalli, G. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00362-w · Cited by 389 · see citing works
A mechanism of cohesin‐dependent loop extrusion organizes zygotic genome architecture
Gassler, J., Brandão, H. B., Imakaev, M., Flyamer, I. M., Ladstätter, S., Bickmore, W. A., Peters, J., Mirny, L. A., & Tachibana, K.-E. K. (2017) · The EMBO Journal · doi:10.15252/embj.201798083 · Cited by 363 · see citing works
“Both TADs and loops were stronger in Wapl Δ compared to control zygotes (Figs 3B and EV3C; see also Tables EV1 and EV2), in agreement with what has been observed in Wapl Δ HAP1 and Wapl RNAi HeLa cells (Haarhuis et al , 2017; Wutz et al , 2017).”
BackgroundResultInfluentialSelf-citationSLAM-seq defines direct gene-regulatory functions of the BRD4-MYC axis
Muhar, M., Ebert, A., Neumann, T., Umkehrer, C., Jude, J., Wieshofer, C., Rescheneder, P., Lipp, J., Herzog, V. A., Reichholf, B., et al. (2018) · Science · doi:10.1126/science.aao2793 · Cited by 364 · see citing works
Self-citationHighly rearranged chromosomes reveal uncoupling between genome topology and gene expression
Ghavi-Helm, Y., Jankowski, A., Meiers, S., Viales, R. R., Korbel, J. O., & Furlong, E. E. M. (2019) · Nature Genetics · doi:10.1038/s41588-019-0462-3 · Cited by 354 · see citing works
Organization of Chromosomal DNA by SMC Complexes
Yatskevich, S., Rhodes, J., & Nasmyth, K. (2019) · Annual Review of Genetics · doi:10.1146/annurev-genet-112618-043633 · Cited by 337 · see citing works
Loop extrusion as a mechanism for formation of DNA damage repair foci
Arnould, C., Rocher, V., Finoux, A.-L., Clouaire, T., Li, K., Zhou, F., Caron, P., Mangeot, P. E., Ricci, E. P., Mourad, R., et al. (2021) · Nature · doi:10.1038/s41586-021-03193-z · Cited by 341 · see citing works
The relationship between genome structure and function
Oudelaar, A. M., & Higgs, D. R. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-020-00303-x · Cited by 304 · see citing works
Despang, A., Schöpflin, R., Franke, M., Ali, S., Jerković, I., Paliou, C., Chan, W.-L., Timmermann, B., Wittler, L., Vingron, M., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0466-z · Cited by 306 · see citing works
Emerging Evidence of Chromosome Folding by Loop ExtrusionPreprint
Fudenberg, G., Abdennur, N. A., Imakaev, M., Goloborodko, A. A., & Mirny, L. A. (2017) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2017.82.034710 · Cited by 287 · see citing works
“…of active LEFs, depletion of the cohesin loader Nipbl (Scc2) (Schwarzer et al. 2017) and acute degradation of the cohesin kleisin Rad21 (Scc1) (Wutz et al. 2017; Rao et al. 2017) during interphase led to both: (i) complete erasure of TADs and Hi-C peaks (ii) and decompaction, as evidenced by…”
BackgroundMethodInfluentialPredicting 3D genome folding from DNA sequence with Akita
Fudenberg, G., Kelley, D. R., & Pollard, K. S. (2020) · Nature Methods · doi:10.1038/s41592-020-0958-x · Cited by 292 · see citing works
Distinct Classes of Chromatin Loops Revealed by Deletion of an RNA-Binding Region in CTCF
Hansen, A. S., Hsieh, T.-H. S., Cattoglio, C., Pustova, I., Saldaña-Meyer, R., Reinberg, D., Darzacq, X., & Tjian, R. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.039 · Cited by 279 · see citing works
Mechanisms and Functions of Chromosome Compartmentalization
Hildebrand, E. M., & Dekker, J. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.01.002 · Cited by 268 · see citing works
Recent evidence that TADs and chromatin loops are dynamic structures
Hansen, A. S., Cattoglio, C., Darzacq, X., & Tjian, R. (2018) · Nucleus · doi:10.1080/19491034.2017.1389365 · Cited by 266 · see citing works
Region Capture Micro-C reveals coalescence of enhancers and promoters into nested microcompartments
Goel, V. Y., Huseyin, M. K., & Hansen, A. S. (2023) · Nature Genetics · doi:10.1038/s41588-023-01391-1 · Cited by 271 · see citing works
The role of transcription in shaping the spatial organization of the genome
van Steensel, B., & Furlong, E. E. M. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0114-6 · Cited by 247 · see citing works
X-Chromosome Inactivation: A Crossroads Between Chromosome Architecture and Gene Regulation
Galupa, R., & Heard, É. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024611 · Cited by 246 · see citing works
Transcription shapes 3D chromatin organization by interacting with loop extrusion
Banigan, E. J., Tang, W., van den Berg, A. A., Stocsits, R. R., Wutz, G., Brandão, H. B., Busslinger, G. A., Peters, J., & Mirny, L. A. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2210480120 · Cited by 216 · see citing works
“While cohesin frequently colocalizes with CTCF in WT cells (6, 11, 12, 17, 53, 54), cohesin islands are not associated with CTCF sites (6), and contacts between CTCF sites are reduced in DKO (Fig.”
BackgroundMethodSelf-citationTwo major mechanisms of chromosome organization
Mirny, L. A., Imakaev, M., & Abdennur, N. A. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.001 · Cited by 222 · see citing works
“Consistently, an increase in cohesin activity (in Wapl knockout cells) leads to weakened compartmentalization signal [29,30,43].”
BackgroundMethodCryo-EM structure of the human cohesin-NIPBL-DNA complex
Shi, Z.-B., Gao, H.-S., Bai, X.-C., & Yu, H.-T. (2020) · Science · doi:10.1126/science.abb0981 · Cited by 196 · see citing works
Homotypic clustering of L1 and B1/Alu repeats compartmentalizes the 3D genome
Lu, J. Y., Chang, L., Li, T., Wang, T., Yin, Y., Zhan, G., Han, X., Zhang, K., Tao, Y., Percharde, M., et al. (2021) · Cell Research · doi:10.1038/s41422-020-00466-6 · Cited by 205 · see citing works
CTCF mediates chromatin looping via N-terminal domain-dependent cohesin retention
Pugacheva, E. M., Kubo, N., Loukinov, D. I., Tajmul, M., Kang, S., Kovalchuk, A. L., Strunnikov, A. V., Zentner, G. E., Ren, B., & Lobanenkov, V. V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911708117 · Cited by 215 · see citing works
Giant lungfish genome elucidates the conquest of land by vertebrates
Meyer, A., Schloissnig, S., Franchini, P., Du, K., Woltering, J. M., Irisarri, I., Wong, W. Y., Nowoshilow, S., Kneitz, S., Kawaguchi, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03198-8 · Cited by 211 · see citing works
Molecular basis of CTCF binding polarity in genome folding
Nora, E. P., Caccianini, L., Fudenberg, G., So, K., Kameswaran, V., Nagle, A., Uebersohn, A., Hajj, B., Saux, A. L., Coulon, A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19283-x · Cited by 206 · see citing works
Catarino, R. R., & Stark, A. (2018) · Genes & Development · doi:10.1101/gad.310367.117 · Cited by 205 · see citing works
“…disrupts TADs and seems to instead favor contacts within active or respressive compartments (Hou et al. 2012; Seitan et al. 2013; Zuin et al. 2014; Ing-Simmons et al. 2015; Ulianov et al. 2016; Haarhuis et al. 2017; Nora et al. 2017; Rao et al. 2017; Schwarzer et al. 2017; Wutz et al. 2017).”
BackgroundMcCord, R. P., Kaplan, N., & Giorgetti, L. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.021 · Cited by 204 · see citing works
“Formation of interactions associated with CTCF requires the cohesin complex (Hadjur et al. 2009; Rao et al. 2017; Wutz et al. 2017), which has been proposed to extrude DNA loops until it is arrested by CTCF bound to DNA in a certain orientation or other barrier proteins (Fudenberg et al.”
BackgroundCanela, A., Maman, Y., Huang, S.-Y. N., Wutz, G., Tang, W., Zagnoli-Vieira, G., Callén, E., Wong, N., Day, A., Peters, J., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.04.030 · Cited by 202 · see citing works
“In WAPL-deficient cells, chromatin loops are enlarged because of the increased residence time of cohesin on DNA (Haarhuis et al., 2017; Wutz et al., 2017), and we observed a concomitant increase in ETOinduced damage genome-wide (Figures S1E–S1G).”
Self-citationRegulation of single-cell genome organization into TADs and chromatin nanodomains
Szabo, Q., Donjon, A., Jerković, I., Papadopoulos, G. L., Cheutin, T., Bonev, B., Nora, E. P., Bruneau, B. G., Bantignies, F., & Cavalli, G. (2020) · Nature Genetics · doi:10.1038/s41588-020-00716-8 · Cited by 184 · see citing works
“In mammals, most TADs are defined by the binding of CTCF in a convergent manner at their borders and by the action of the cohesin complex 9–16 .”
Single-allele chromatin interactions identify regulatory hubs in dynamic compartmentalized domains
Oudelaar, A. M., Davies, J. O. J., Hanssen, L. L. P., Telenius, J. M., Schwessinger, R., Liu, Y., Brown, J. M., Downes, D. J., Chiariello, A. M., Bianco, S., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0253-2 · Cited by 196 · see citing works
CTCF is a DNA-tension-dependent barrier to cohesin-mediated loop extrusion
Davidson, I. F., Barth, R., Zaczek, M., van der Torre, J., Tang, W., Nagasaka, K., Janissen, R., Kerssemakers, J. W. J., Wutz, G., Dekker, C., et al. (2023) · Nature · doi:10.1038/s41586-023-05961-5 · Cited by 190 · see citing works
Self-citationEnhancer selectivity in space and time: from enhancer–promoter interactions to promoter activation
Yang, J. H., & Hansen, A. S. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00710-6 · Cited by 191 · see citing works
Scc2 Is a Potent Activator of Cohesin’s ATPase that Promotes Loading by Binding Scc1 without Pds5
Petela, N. J., Gligoris, T. G., Metson, J., Lee, B., Voulgaris, M., Hu, B., Kikuchi, S., Chapard, C., Chen, W., Rajendra, E., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.022 · Cited by 187 · see citing works
“We therefore suggest that CTCF might block LE by somehow hindering replacement of Pds5 by Scc2, as discussed in Wutz et al. (2017).”
BackgroundA quantitative map of human Condensins provides new insights into mitotic chromosome architecture
Walther, N., Hossain, M. J., Politi, A., Koch, B., Kueblbeck, M., Ødegård-Fougner, Ø., Lampe, M., & Ellenberg, J. (2018) · bioRxiv · doi:10.1083/jcb.201801048 · Cited by 181 · see citing works
“Comparison of FWHM for the same Condensin subunit between prometa- and anaphase: CAP-D2 (p = 0.0067), CAP-D3 (p = 0.0064), CAP-H (p = 0.3966), CAP- H2 (p = 0.0391).”
BackgroundMethodInfluentialSelf-citationCohesin Disrupts Polycomb-Dependent Chromosome Interactions in Embryonic Stem Cells
Rhodes, J. D. P., Feldmann, A., Hernández-Rodríguez, B., Díaz, N., Brown, J. M., Fursova, N. A., Blackledge, N. P., Prathapan, P., Dobrinic, P., Huseyin, M. K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.057 · Cited by 187 · see citing works
“, 2017), and HeLa (Wutz et al., 2017), we did not observe obvious punctate interactions between polycomb chromatin domains in control cells, and these sites did not interact following removal of SCC1 (HCT116 and HeLa) or removal of the cohesin loader component SCC4 (HAP1).”
BackgroundResultInfluentialHuang, H., Zhu, Q., Jussila, A., Han, Y., Bintu, B., Kern, C., Conte, M., Zhang, Y., Bianco, S., Chiariello, A. M., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00863-6 · Cited by 187 · see citing works
ESCO1 and CTCF enable formation of long chromatin loops by protecting cohesinSTAG1 from WAPL
Wutz, G., Ladurner, R., Hilaire, B. G. S., Stocsits, R. R., Nagasaka, K., Pignard, B., Sanborn, A. L., Tang, W., Várnai, C., Ivanov, M. P., et al. (2020) · eLife · doi:10.7554/elife.52091 · Cited by 167 · see citing works
“Third, aggregate peak analysis using loop coordinates identified in control or WAPL-depleted cells (Wutz et al., 2017) revealed that genome wide loops were weakest in STAG1-depleted cells, strongest in WAPL-depleted cells and of intermediate strength in STAG2-depleted cells (Figure S11A).”
BackgroundMethodResultInfluentialSelf-citationDistinct roles of cohesin-SA1 and cohesin-SA2 in 3D chromosome organization
Kojic, A., Cuadrado, A., Koninck, M. D., Giménez-Llorente, D., Rodríguez-Corsino, M., Goméz-López, G., Dily, F. L., Martı́-Renom, M. A., & Losada, A. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0070-4 · Cited by 169 · see citing works
Thiecke, M. J., Wutz, G., Muhar, M., Tang, W., Bevan, S., Malysheva, V., Stocsits, R., Neumann, T., Zuber, J., Fraser, P., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107929 · Cited by 177 · see citing works
Self-citationEnhancer–promoter contact formation requires RNAPII and antagonizes loop extrusion
Zhang, S., Übelmesser, N., Barbieri, M., & Papantonis, A. (2023) · Nature Genetics · doi:10.1038/s41588-023-01364-4 · Cited by 165 · see citing works
“Removing CTCF from chromatin leads to the loss of insulation at domain boundaries (Nora et al., 2017), while cohesin removal leads to the elimination of CTCF-anchored loops (Rao et al., 2017; Wutz et al, 2017).”
BackgroundWAPL maintains a cohesin loading cycle to preserve cell-type-specific distal gene regulation
Liu, N. Q., Maresca, M., van den Brand, T., Braccioli, L., Schijns, M. M. G. A., Teunissen, H., Bruneau, B. G., Nora, E. P., & de Wit, E. (2021) · Nature Genetics · doi:10.1038/s41588-020-00744-4 · Cited by 162 · see citing works
“, 5 μg per ChIP), (7) MED1 (A300-793A, Bethyl Laboratories, 5 μg per ChIP), (8) H3K4me3 (pAb-003-050, Diagenode, 5 μg per ChIP), and (9) H3K27ac (ab4729, Abcam, 5 μg per ChIP).”
Independence of chromatin conformation and gene regulation during Drosophila dorsoventral patterning
Ing-Simmons, E., Vaid, R., Bing, X. Y., Levine, M., Mannervik, M., & Vaquerizas, J. M. (2021) · Nature Genetics · doi:10.1038/s41588-021-00799-x · Cited by 159 · see citing works
Cohesin is required for long-range enhancer action at the Shh locus
Kane, L., Williamson, I., Flyamer, I. M., Kumar, Y., Hill, R. E., Lettice, L. A., & Bickmore, W. A. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00821-8 · Cited by 153 · see citing works
Wheat chromatin architecture is organized in genome territories and transcription factories
Concia, L., Veluchamy, A., Ramirez-Prado, J. S., Martin-Ramirez, A., Huang, Y., Perez, M., Domenichini, S., Rodriguez-Granados, N. R., Kim, S., Blein, T., et al. (2020) · Genome Biology · doi:10.1186/s13059-020-01998-1 · Cited by 120 · see citing works
Rinzema, N. J., Sofiadis, K., Tjalsma, S. J. D., Verstegen, M. J. A. M., Oz, Y., Valdes-Quezada, C., Felder, A.-K., Filipovska, T., van der Elst, S., de Andrade dos Ramos, Z., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00787-7 · Cited by 166 · see citing works
Uyehara, C. M., & Apostolou, E. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112068 · Cited by 143 · see citing works
Polycomb Group Proteins Regulate Chromatin Architecture in Mouse Oocytes and Early Embryos.
Du, Z., Zheng, H., Kawamura, Y. K., Zhang, K., Gassler, J., Powell, S. T., Xu, Q.-H., Lin, Z.-L., Xu, K., Zhou, Q., et al. (2019) · Molecules and Cells · doi:10.1016/j.molcel.2019.11.011 · Cited by 149 · see citing works
Topologically associating domain boundaries are required for normal genome function
Rajderkar, S., Barozzi, I., Zhu, Y., Hu, R., Zhang, Y., Li, B., Alcaina‐Caro, A., Fukuda-Yuzawa, Y., Kelman, G., Akeza, A., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04819-w · Cited by 170 · see citing works
“Loss of CTCF, cohesin, or the cohesin loading factor Nipbl results in TAD disruption, while loss of cohesin release factor, Wapl, results in reinforcement of TAD boundaries 20,21 .”
Kaaij, L. J. T., Mohn, F., van der Weide, R. H., de Wit, E., & Bühler, M. (2019) · Cell · doi:10.1016/j.cell.2019.08.007 · Cited by 133 · see citing works
Loop extrusion: theory meets single-molecule experiments
Banigan, E. J., & Mirny, L. A. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.04.011 · Cited by 160 · see citing works
Hi-C analyses with GENOVA: a case study with cohesin variants
van der Weide, R. H., van den Brand, T., Haarhuis, J. H. I., Teunissen, H., Rowland, B. D., & de Wit, E. (2021) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqab040 · Cited by 161 · see citing works
Systemic Loss and Gain of Chromatin Architecture throughout Zebrafish Development
Kaaij, L. J., van der Weide, R. H., Ketting, R., & de Wit, E. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.003 · Cited by 130 · see citing works
The cohesin complex in mammalian meiosis
Ishiguro, K. (2018) · Genes to Cells · doi:10.1111/gtc.12652 · Cited by 146 · see citing works
Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase
Patel, L., Kang, R., Rosenberg, S., Qiu, Y., Raviram, R., Chee, S., Hu, R., Ren, B., Cole, F., & Corbett, K. D. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0187-0 · Cited by 148 · see citing works
“Cohesin depletion causes an almost immediate loss of TADs in aggregate Hi-C data, strengthening and in some cases fragmentation of the A/B compartment structure, and the formation of multivalent enhancer clusters, or “superenhancer hubs” 20–22 .”
InfluentialDynamic chromatin organization without the 30-nm fiber
Maeshima, K., Ide, S., & Babokhov, M. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.02.003 · Cited by 145 · see citing works
Chromatin accessibility: methods, mechanisms, and biological insights
Mansisidor, A., & Risca, V. I. (2022) · Nucleus · doi:10.1080/19491034.2022.2143106 · Cited by 150 · see citing works
“First, the compartment associations are independent of active loop extrusion and are antagonized by it, as observed when compartment contacts appear stronger when cohesin is depleted from chromatin and appear weaker when cohesin’s stability on chromatin is enhanced [234,236,237].”
BackgroundMCM complexes are barriers that restrict cohesin-mediated loop extrusion
Dequeker, B. J. H., Scherr, M. J., Brandão, H. B., Gassler, J., Powell, S. T., Gáspár, I., Flyamer, I. M., Lalic, A., Tang, W., Stocsits, R. R., et al. (2022) · Nature · doi:10.1038/s41586-022-04730-0 · Cited by 149 · see citing works
Self-citationChromosome organization by one-sided and two-sided loop extrusion
Banigan, E. J., van den Berg, A. A., Brandão, H. B., Marko, J. F., & Mirny, L. A. (2020) · eLife · doi:10.7554/elife.53558 · Cited by 146 · see citing works
Genome control by SMC complexes
Hoencamp, C., & Rowland, B. D. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00609-8 · Cited by 138 · see citing works
Diverse silent chromatin states modulate genome compartmentalization and loop extrusion barriers
Spracklin, G., Abdennur, N. A., Imakaev, M., Chowdhury, N., Pradhan, S., Mirny, L. A., & Dekker, J. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00892-7 · Cited by 139 · see citing works
RNA polymerases as moving barriers to condensin loop extrusion
Brandão, H. B., Paul, P., van den Berg, A. A., Rudner, D. Z., Wang, X., & Mirny, L. A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907009116 · Cited by 143 · see citing works
“If eukaryotic RNAPs turn out as permeable to SMC as bacterial RNAPs, transcription in eukaryotes may not have a major effect on chromosome organization by loop extrusion, as compared to other molecules that specifically (and directionally) impede loop extrusion, like CTCF (20, 60).”
BackgroundInfluentialWapl repression by Pax5 promotes V gene recombination by Igh loop extrusion
Hill, L., Ebert, A., Jaritz, M., Wutz, G., Nagasaka, K., Tagoh, H., Kostanova‐Poliakova, D., Schindler, K., Sun, Q., Bönelt, P., et al. (2020) · Nature · doi:10.1038/s41586-020-2454-y · Cited by 136 · see citing works
Self-citationLiquid chromatin Hi-C characterizes compartment-dependent chromatin interaction dynamics
Belaghzal, H., Borrman, T. M., Stephens, A. D., Lafontaine, D. L. J., Venev, S. V., Weng, Z., Marko, J. F., & Dekker, J. (2021) · Nature Genetics · doi:10.1038/s41588-021-00784-4 · Cited by 132 · see citing works
Three-dimensional chromatin packing and positioning of plant genomes
Doğan, E. S., & Liu, C. (2018) · Nature Plants · doi:10.1038/s41477-018-0199-5 · Cited by 138 · see citing works
Acute depletion of CTCF directly affects MYC regulation through loss of enhancer–promoter looping
Hyle, J. W., Zhang, Y., Wright, S., Xu, B., Shao, Y., Easton, J. B., Tian, L., Feng, R., Xu, P., & Li, C. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz462 · Cited by 140 · see citing works
“Our data supported the recent reported data that acute loss of Ctcf does not affect nuclear compartmentalization on the multi-Mb scale, but does significantly disrupt TAD boundary integrity and enhancer–promoter looping (29,34).”
ResultDetermining cellular CTCF and cohesin abundances to constrain 3D genome models
Cattoglio, C., Pustova, I., Walther, N., Ho, J. J., Hantsche-Grininger, M., Inouye, C. J., Hossain, M. J., Dailey, G. M., Ellenberg, J., Darzacq, X., et al. (2019) · eLife · doi:10.7554/elife.40164 · Cited by 133 · see citing works
Self-citationPrinciples of meiotic chromosome assembly revealed in S. cerevisiae
Schalbetter, S., Fudenberg, G., Baxter, J., Pollard, K., & Neale, M. (2019) · Nature Communications · doi:10.1038/s41467-019-12629-0 · Cited by 113 · see citing works
Computer vision for pattern detection in chromosome contact maps
Matthey-Doret, C., Baudry, L., Breuer, A., Montagne, R., Guiglielmoni, N., Scolari, V. F., Jean, É., Campeas, A., Chanut, P. H., Oriol, E., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19562-7 · Cited by 120 · see citing works
CTCF shapes chromatin structure and gene expression in health and disease
Dehingia, B., Milewska, M., Janowski, M., & Pękowska, A. (2022) · EMBO Reports · doi:10.15252/embr.202255146 · Cited by 128 · see citing works
Luppino, J. M., Park, D. S., Nguyen, S. C., Lan, Y., Xu, Z., Yunker, R., & Joyce, E. F. (2020) · Nature Genetics · doi:10.1038/s41588-020-0647-9 · Cited by 118 · see citing works
Mitotic Chromosome Mechanics: How Cells Segregate Their Genome
Batty, P., & Gerlich, D. W. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.05.007 · Cited by 121 · see citing works
Principles of Chromosome Architecture Revealed by Hi-C
Eagen, K. P. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.03.006 · Cited by 120 · see citing works
“Auxin-mediated, acute protein degradation of CTCF [37,38] or cohesin [38,39] altered chromatin looping.”
BackgroundMethodInfluentialRowley, M. J., Lyu, X., Rana, V., Ando‐Kuri, M., Karns, R., Bosco, G., & Corces, V. G. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.116 · Cited by 114 · see citing works
“The loss of Rad21 or CTCF results in the demise of these loops (Nora et al., 2017; Rao et al., 2017; Schwarzer et al., 2017; Wutz et al., 2017).”
Aljahani, A., Hua, P., Karpinska, M. A., Quililan, K., Davies, J. O. J., & Oudelaar, A. M. (2022) · Nature Communications · doi:10.1038/s41467-022-29696-5 · Cited by 121 · see citing works
CTCF orchestrates long-range cohesin-driven V(D)J recombinational scanning
Ba, Z., Lou, J., Ye, A. Y., Dai, H., Dring, E. W., Lin, S. G., Jain, S., Kyritsis, N., Kieffer-Kwon, K.-R., Casellas, R. C., et al. (2020) · Nature · doi:10.1038/s41586-020-2578-0 · Cited by 115 · see citing works
Looping the Genome with SMC Complexes
Kim, E., Barth, R., & Dekker, C. (2023) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-032620-110506 · Cited by 96 · see citing works
Absolute quantification of cohesin, CTCF and their regulators in human cells
Holzmann, J., Politi, A. Z., Nagasaka, K., Hantsche-Grininger, M., Walther, N., Koch, B., Fuchs, J., Dürnberger, G., Tang, W., Ladurner, R., et al. (2019) · eLife · doi:10.7554/elife.46269 · Cited by 109 · see citing works
“CTCF consensus binding sites are frequently oriented convergently at TAD borders (Rao et al., 2014; de Wit et al., 2015; Vietri Rudan et al., 2015) and depletion of CTCF leads to a loss of insulation between TADs (Nora et al., 2017; Wutz et al., 2017).”
BackgroundInfluentialSelf-citationConformation of sister chromatids in the replicated human genome
Mitter, M., Gasser, C., Takács, Z., Langer, C. C. H., Tang, W., Jessberger, G., Beales, C. T., Neuner, E., Ameres, S. L., Peters, J., et al. (2020) · Nature · doi:10.1038/s41586-020-2744-4 · Cited by 107 · see citing works
Self-citationThe solid and liquid states of chromatin
Hansen, J. C., Maeshima, K., & Hendzel, M. J. (2021) · Epigenetics & Chromatin · doi:10.1186/s13072-021-00424-5 · Cited by 112 · see citing works
CTCF and R-loops are boundaries of cohesin-mediated DNA looping
Zhang, H., Shi, Z., Banigan, E. J., Kim, Y., Yu, H., Bai, X., & Finkelstein, I. J. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.07.006 · Cited by 116 · see citing works
Emerging themes in cohesin cancer biology
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Condensed but liquid-like domain organization of active chromatin regions in living human cells
Nozaki, T., Shinkai, S., Ide, S., Higashi, K., Tamura, S., Shimazoe, M. A., Nakagawa, M., Suzuki, Y., Okada, Y., Sasai, M., et al. (2023) · Science Advances · doi:10.1126/sciadv.adf1488 · Cited by 109 · see citing works
Cohesin residency determines chromatin loop patterns
Costantino, L., Hsieh, T.-H. S., Lamothe, R. C., Darzacq, X., & Koshland, D. E. (2020) · eLife · doi:10.7554/elife.59889 · Cited by 114 · see citing works
The role of chromatin loop extrusion in antibody diversification
Zhang, Y., Zhang, X., Dai, H., Hu, H., & Alt, F. W. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00679-3 · Cited by 106 · see citing works
Chromatin topology, condensates and gene regulation: shifting paradigms or just a phase?
Mir, M., Bickmore, W. A., Furlong, E. E. M., & Narlikar, G. J. (2019) · Development · doi:10.1242/dev.182766 · Cited by 109 · see citing works
“If TAD formation is widely disrupted, for example through the removal or depletion of cohesin (Sofueva et al., 2013; Wutz et al., 2017; Schwarzer et al., 2017; Rao et al., 2017; Haarhuis et al., 2017) or CTCF (Nora et al., 2017), the activity of only a subset of genes is disrupted, whereas the…”
Chromatin features constrain structural variation across evolutionary timescales
Fudenberg, G., & Pollard, K. S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1808631116 · Cited by 106 · see citing works
“, 2012), largely dependent on the binding of CTCF (Nora et al., 2017; Wutz et al., 2017), are structural features of the genome of much recent interest and are hypothesized to play an important role in gene regulation.”
- Authors
- Wutz, G., Várnai, C., Nagasaka, K., Cisneros, D. A., Stocsits, R. R., Tang, W., Schoenfelder, S., Jessberger, G., Muhar, M., Hossain, M. J., Walther, N., Koch, B., Kueblbeck, M., Ellenberg, J., Zuber, J., Fraser, P., & Peters, J.
- Affiliations
- Research Institute of Molecular Pathology (AT)
- Babraham Institute (GB)
- European Molecular Biology Laboratory (DE)
- Florida State University (US)
- Corresponding author
- Peters, Jan‐Michael
- ORCID
- Venue
- The EMBO Journal
- Published
- 2017-12-07
- Volume
- 36
- Issue
- 24
- Pages
- 3573-3599
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC5730888
- OpenAlex
- W2775505403
- Cited by
- 864
- References
- 97
- Citations by year
- 2026: 83 · 2025: 77 · 2024: 102 · 2023: 97 · 2022: 119 · 2021: 127 · 2020: 112 · 2019: 87 · 2018: 49 · 2017: 11
- FWCI
- 29.61
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ePrints Soton (University of Southampton) (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Boehringer Ingelheim
- Austrian Research Promotion Agency (FFG‐834223)
- UK Biotechnology and Biological Sciences Research Council (BB/J004480/1)
- European Research Council Advanced Grant (DEVOCHROMO)
- EMBO Long Term Fellowship (ALTF 1335‐2016)
- Austrian Science Fund (SFB F34, Z196‐B20)
- Human Frontier Science Program (LT001527/2017)
- 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
- topologically associating domains, chromatin looping, cohesin, CTCF, WAPL, Pds5, loop extrusion, chromatin compartments, long-range chromatin interactions, chromosome condensation, vermicelli, 3D genome organization
- MeSH terms
- CCCTC-Binding Factor, Cohesins, Carrier Proteins, Chromatin, Chromosomal Proteins, Non-Histone, Chromosomes, DNA-Binding Proteins, HeLa Cells, Humans, Nuclear Proteins, Proto-Oncogene Proteins, Transcription Factors, Genome, Human, Cell Cycle Proteins
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