The DOI matches its Crossref record; 49 of the 51 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
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
Sorted by citations
HiGlass: web-based visual exploration and analysis of genome interaction maps
Kerpedjiev, P., Abdennur, N. A., Lekschas, F., McCallum, C., Dinkla, K., Strobelt, H., Luber, J. M., Ouellette, S., Azhir, A., Kumar, N., et al. (2018) · Genome biology · doi:10.1186/s13059-018-1486-1 · Cited by 2,430
Cohesin Loss Eliminates All Loop Domains
Rao, S. S. P., Huang, S.-C., Glenn St Hilaire, B., Engreitz, J. M., Perez, E. M., Kieffer-Kwon, K.-R., Sanborn, A. L., Johnstone, S. E., Bascom, G. D., Bochkov, I. D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.026 · Cited by 1,883
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
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
Wutz, G., Várnai, C., Nagasaka, K., Cisneros, D. A., Stocsits, R. R., Tang, W., Schoenfelder, S., Jessberger, G., Muhar, M., Hossain, M. J., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201798004 · Cited by 864
“…36 | No 24 | 2017 that cohesin’s function in gene regulation is related to CTCF, as this DNA binding protein recruits cohesin to specific sites in mammalian genomes and depends on cohesin for its ability to mediate gene regulation (Parelho et al, 2008; Wendt et al, 2008; Busslinger et al, 2017).”
InfluentialSelf-citationSuper-resolution chromatin tracing reveals domains and cooperative interactions in single cells
Bintu, B., Mateo, L. J., Su, J.-H., Sinnott-Armstrong, N. A., Parker, M., Kinrot, S., Yamaya, K., Boettiger, A. N., & Zhuang, X. (2018) · Science · doi:10.1126/science.aau1783 · Cited by 976
DNA 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
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 742
Resolving the 3D Landscape of Transcription-Linked Mammalian Chromatin Folding
Hsieh, T.-H. S., Cattoglio, C., Slobodyanyuk, E., Hansen, A. S., Rando, O. J., Tjian, R., & Darzacq, X. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.002 · Cited by 661
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 638
“Furthermore, experiments are at odds with a simple picture where the sole function of the Nipbl complex (also termed SCC2/SCC4) is to facilitate cohesin loading while WAPL determines its residence time on chromatin, and rather suggest that SCC4 also regulates the processivity and/or the residence time of cohesin on DN…”
BackgroundPrinciples of genome folding into topologically associating domains
Szabo, Q., Bantignies, F., & Cavalli, G. (2019) · Science Advances · doi:10.1126/sciadv.aaw1668 · Cited by 631
The Energetics and Physiological Impact of Cohesin Extrusion
Vian, L., Pękowska, A., Rao, S. S. P., Kieffer-Kwon, K.-R., Jung, S., Baranello, L., Huang, S.-C., El Khattabi, L., Dose, M., Pruett, N., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.072 · Cited by 581
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 531
Self-citationTranscription 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
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
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 382
“Transcription, however, can affect loading and positioning of cohesin (Kagey et al., 2010; Busslinger et al., 2017).”
BackgroundSelf-citationZhang, Y., Li, T., Preißl, S., Amaral, M. L., Grinstein, J. D., Farah, E. N., Destici, E., Qiu, Y., Hu, R., Lee, A. Y., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0479-7 · Cited by 384
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 349
Isoda, T., Moore, A. J., He, Z., Chandra, V. K., Aida, M., Denholtz, M., van Hamburg, J. P., Fisch, K. M., Chang, A. N., Fahl, S. P., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.001 · Cited by 323
The epigenetic basis of cellular heterogeneity
Carter, B. C., & Zhao, K. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-00300-0 · Cited by 324
Static and Dynamic DNA Loops form AP-1-Bound Activation Hubs during Macrophage Development
Phanstiel, D. H., Van Bortle, K., Spacek, D., Hess, G. T., Shamim, M. S., Machol, I., Love, M. I., Aiden, E. L., Bassik, M. C., & Snyder, M. P. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.08.006 · Cited by 299
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 321
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 298
“Future simulations and experiments will be valuable for probing the consequences of multiple simultaneous perturbations (Busslinger et al. 2017; Wutz et al. 2017).”
BackgroundRecent 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
Kruse, K., Hug, C. B., & Vaquerizas, J. M. (2020) · Genome biology · doi:10.1186/s13059-020-02215-9 · Cited by 242
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
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 238
“Cohesin accumulation is greater for higher levels of transcription (6), and both dots and insulation at cohesin islands are partially suppressed in DKO by treatment with the transcription elongation inhibitor DRB (SI Appendix, Fig.”
BackgroundResultInfluentialSelf-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 232
“The process of transcription can also play a role in pausing loop extrusion and/or relocalizing cohesin [54,85], thereby influencing chromosome organization.”
BackgroundCTCF 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 224
“These data are wholly consistent with the results from the previous studies using CTCF auxininducible degron system and with CTCF knockout mouse fibroblasts where, in the absence of CTCF, cohesin is no longer able to occupy CTCF binding sites (30, 31).”
ResultMolecular 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
Canela, 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
“To determine how cohesin affects the distribution of TOP2 lesions, we examined mouse embryonic fibroblasts (MEFs) in which SMC3, a cohesin subunit, was depleted by CRE-mediated recombination, resulting in the disruption of nuclear architecture (Busslinger et al., 2017) (Smc3+CRE; Figures 1A–1D).”
InfluentialSelf-citationCTCF 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 198
Self-citationScc2 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 196
Chromatin alternates between A and B compartments at kilobase scale for subgenic organization
Harris, H. L., Gu, H., Olshansky, M., Wang, A., Farabella, I., Eliaz, Y., Kalluchi, A., Krishna, A., Jacobs, M., Cauer, G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38429-1 · Cited by 184
“In vitro studies have found that large chromatin complexes can impede looping factors 61,62 , and cohesin was shown to build up near transcriptionally active regions 63 .”
BackgroundA Muscle-Specific Enhancer RNA Mediates Cohesin Recruitment and Regulates Transcription In trans
Tsai, P.-F., Dell’Orso, S., Rodriguez, J., Vivanco, K. O., Ko, K.-D., Jiang, K., Juan, A. H., Sarshad, A. A., Vian, L., Tran, M. D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.008 · Cited by 190
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 173
“as we had previously observed in primary Ctcf “knockout” MEFs arrested in G0 (Busslinger et al., 2017).”
BackgroundSelf-citationThiecke, 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
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
“In addition, based on the documented co-association of cohesin subunits and RNAPII (Busslinger et al, 2017; Zhang et al., 2021), we introduced a weak interaction potential between cohesins and polymerases.”
BackgroundInfluentialWang, Q., Sun, Q., Czajkowsky, D. M., & Shao, Z. (2018) · Nature Communications · doi:10.1038/s41467-017-02526-9 · Cited by 170
WAPL 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
Uyehara, C. M., & Apostolou, E. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112068 · Cited by 143
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 161
Towards a Unified Model of SMC Complex Function
Hassler, M., Shaltiël, I. A., & Haering, C. H. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.034 · Cited by 161
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 169
MCM complexes are barriers that restrict cohesin-mediated loop extrusion
Dequeker, B., 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. (2020) · Nature · doi:10.1038/s41586-022-04730-0 · Cited by 132
Self-citationHuman T Cell Leukemia Virus Type 1: Persistence and Pathogenesis
Bangham, C. R. M. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053222 · Cited by 152
Chromosome 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
“Although current experimental evidence does not support preferential loading of cohesin at CTCF sites in mammals (Busslinger et al., 2017; Fudenberg et al., 2017; Nora et al., 2019, 2017; Parelho et al., 2008; Wendt et al., 2008) , such a mechanism of TAD, stripe, and dot formation is feasible and may be operational i…”
BackgroundInfluentialGuided nuclear exploration increases CTCF target search efficiency
Hansen, A. S., Amitai, A., Cattoglio, C., Tjian, R., & Darzacq, X. (2019) · Nature Chemical Biology · doi:10.1038/s41589-019-0422-3 · Cited by 145
“The similar diffusion mechanisms are especially interesting in light of the fact that how and where cohesin is loaded onto the genome remains poorly understood (Busslinger et al., 2017).”
BackgroundRNA 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
“This idea emerged from the observation that cohesin SMCs are enriched at sites of convergent transcription in yeast (50, 51) and in mammalian cells (35); this is further supported by other experiments demonstrating localization of cohesin mediated by transcription in cells (32) and in vitro (52).”
Developing in 3D: the role of CTCF in cell differentiation
Arzate‐Mejía, R. G., Targa, F. R., & Corces, V. G. (2018) · Development · doi:10.1242/dev.137729 · Cited by 144
“For example, inactivation of the Ctcf gene in primary mouse embryonic fibroblasts results in the mis-regulation of 698 genes (Busslinger et al., 2017), whereas similar experiments in post-mitotic embryonic and postnatal neurons results in changes in the expression of about 400 and 800 genes, respectively (Hirayama et…”
BackgroundThree-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 147
Genome-wide analyses of chromatin interactions after the loss of Pol I, Pol II, and Pol III
Jiang, Y., Huang, J. S., Lun, K., Li, B., Zheng, H., Li, Y., Zhou, R., Duan, W., Wang, C., Feng, Y., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02067-3 · Cited by 144
“On the other hand, many studies have shown that transcription inhibition affects 3D genome structures and Cohesin [15, 16], which seems to conflict with our conclusion.”
SMC Complexes Can Traverse Physical Roadblocks Bigger Than Their Ring Size
Pradhan, B., Barth, R., Kim, E., Davidson, I. F., Bauer, B. W., van Laar, T., Yang, W., Ryu, J., van der Torre, J., Peters, J., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111491 · Cited by 131
Self-citationPrinciples of meiotic chromosome assembly revealed in S. cerevisiae
Schalbetter, S. A., Fudenberg, G., Baxter, J., Pollard, K. S., & Neale, M. J. (2019) · Nature Communications · doi:10.1038/s41467-019-12629-0 · Cited by 140
Nonequilibrium Chromosome Looping via Molecular Slip Links
Brackley, C. A., Johnson, J., Michieletto, D., Morozov, A. N., Nicodemi, M., Cook, P. R., & Marenduzzo, D. (2017) · Physical Review Letters · doi:10.1103/physrevlett.119.138101 · Cited by 131
“Experiments show that cohesin topologically links to DNA (with binding mediated by “loader proteins” [11, 16]), can slide along DNA or chromatin diffusively, and remains bound for τ ∼ 20 minutes before dissociating (a process mediated by “unloader proteins”) [16–21].”
BackgroundInfluentialAttenuated chromatin compartmentalization in meiosis and its maturation in sperm development
Alavattam, K. G., Maezawa, S., Sakashita, A., Khoury, H., Barski, A., Kaplan, N., & Namekawa, S. H. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0189-y · Cited by 141
The three-dimensional genome: regulating gene expression during pluripotency and development
Andrey, G., & Mundlos, S. (2017) · Development · doi:10.1242/dev.148304 · Cited by 134
“Moreover, two studies have shown that transcription can relocate cohesin over long distances and that its chromatin loading/ unloading rate controls the extension of chromatin loops (Busslinger et al., 2017; Haarhuis et al., 2017).”
BackgroundCTCF 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 141
“In the absence of CTCF, cohesins accumulate at sites of convergent transcription which might in principle lead to enhanced contact insulation and boundary formation (Busslinger et al , 2017).”
Single-Cell Heterogeneity Analysis and CRISPR Screen Identify Key β-Cell-Specific Disease Genes
Fang, Z., Weng, C., Li, H., Tao, R., Mai, W., Liu, X., Lu, L., Lai, S., Duan, Q., Álvarez‐González, C. A., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.043 · Cited by 126
“In the mammalian genome, Nipbl mainly binds to promoters and enhancers, while the strongest peaks of cohesin are at intergenic CTCF sites (Busslinger et al., 2017; Kagey et al., 2010; Zuin et al., 2014).”
The chromosome folding problem and how cells solve it
Dekker, J., & Mirny, L. A. (2024) · Cell · doi:10.1016/j.cell.2024.10.026 · Cited by 112
The Mediator complex regulates enhancer-promoter interactions
Ramasamy, S., Aljahani, A., Karpińska, M. A., Cao, T. B. N., Velychko, T., Cruz, J. N., Lidschreiber, M., & Oudelaar, A. M. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01027-2 · Cited by 141
MyoD is a 3D genome structure organizer for muscle cell identity
Wang, R., Chen, F., Chen, Q., Wan, X., Shi, M., Chen, A. K., Ma, Z., Li, G., Wang, M., Ying, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27865-6 · Cited by 128
Pelham‐Webb, B., Polyzos, A., Wojenski, L., Kloetgen, A., Li, J., Giammartino, D. C. D., Sakellaropoulos, T., Tsirigos, A., Core, L. J., & Apostolou, E. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.02.032 · Cited by 121
“However, since our experimental perturbations did not fully eliminate transcription, it is plausible that the remaining transcriptional activity promotes proper chromatin organization, in agreement with its previously instructive role in genome folding (Busslinger et al., 2017; Heinz et al., 2018; Hsieh et al., 2020;…”
BackgroundRowley, 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
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
Organization of DNA in Mammalian Mitochondria
Farge, G., & Falkenberg, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112770 · Cited by 118
“This structure folds into a chromatin fiber, which is further organized into chromatin loops by proteins such as cohesin and the CCCTC-binding factor (CTCF) [27].”
BackgroundLooping 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
“In particular, the notion that cohesin is found in islands be-tween two convergently oriented genes led to the idea that active transcription can push intragenic cohesin toward transcription termination sites ( Figure 6 d ) (126, 166).”
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 113
“, 2016) and ChIP-seq studies in bacteria, yeast and mammalian cells have all revealed that cohesin/SMC enrichment sites can vary in their positions (Lengronne et al., 2004; Hu et al., 2015; Ocampo-Hafalla et al., 2016; Busslinger et al., 2017; Wang et al., 2017; Petela et al., 2018; Wang et al., 2018).”
BackgroundSelf-citationCTCF 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 123
Emerging themes in cohesin cancer biology
Waldman, T. A. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0270-1 · Cited by 117
Barrington, C., Georgopoulou, D., Pezic, D., Varsally, W., Herrero, J., & Hadjur, S. (2019) · Nature Communications · doi:10.1038/s41467-019-10725-9 · Cited by 102
RNA polymerase II is required for spatial chromatin reorganization following exit from mitosis
Zhang, S., Übelmesser, N., Josipović, N., Forte, G., Slotman, J. A., Chiang, M., Gothe, H. J., Gusmao, E. G., Becker, C., Altmüller, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg8205 · Cited by 114
Mechanisms of Chromosome Folding and Nuclear Organization: Their Interplay and Open QuestionsPreprint
Mirny, L. A., & Dekker, J. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a040147 · Cited by 111
Transcription-mediated supercoiling regulates genome folding and loop formation
Neguembor, M. V., Martin, L., Castells-García, Á., Gómez-García, P. A., Vicario, C., Carnevali, D., Abed, J. A., Granados, A., Sebastián-Pérez, R., Sottile, F., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.06.009 · Cited by 106
Transcription-factor-mediated supervision of global genome architecture maintains B cell identity
Johanson, T. M., Lun, A. T. L., Coughlan, H. D., Tan, T., Smyth, G. K., Nutt, S. L., & Allan, R. S. (2018) · Nature Immunology · doi:10.1038/s41590-018-0234-8 · Cited by 109
CTCF as a boundary factor for cohesin-mediated loop extrusion: evidence for a multi-step mechanism
Hansen, A. S. (2020) · Nucleus · doi:10.1080/19491034.2020.1782024 · Cited by 101
“Consistent with this model, RNAi-mediated depletion of ESCO1 and CTCF both decreased cohesin’s residence time [38] and SMC3 acetylation [38,76].”
BackgroundRibosomal DNA and the nucleolus in the context of genome organization
Potapova, T., & Gerton, J. L. (2019) · Chromosome Research · doi:10.1007/s10577-018-9600-5 · Cited by 103
Mondal, G., Stevers, M., Goode, B., Ashworth, A., & Solomon, D. A. (2019) · Nature Communications · doi:10.1038/s41467-019-09659-z · Cited by 105
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 102
Loop extrusion mediates physiological Igh locus contraction for RAG scanning
Dai, H., Hu, H., Lou, J., Ye, A. Y., Ba, Z., Zhang, X., Zhang, Y., Zhao, L., Yoon, H. S., Chapdelaine-Williams, A. M., et al. (2021) · Nature · doi:10.1038/s41586-020-03121-7 · Cited by 96
Regulation of Cohesin-Mediated Chromosome Folding by Eco1 and Other Partners
Dauban, L., Montagne, R., Thierry, A., Lazar‐Stefanita, L., Bastié, N., Gadal, O., Cournac, A., Koszul, R., & Beckouët, F. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.01.019 · Cited by 116
CTCF: a Swiss-army knife for genome organization and transcription regulation
Braccioli, L., & de Wit, E. (2019) · Essays in Biochemistry · doi:10.1042/ebc20180069 · Cited by 106
A Brownian ratchet model for DNA loop extrusion by the cohesin complex
Higashi, T. L., Tang, M., Pobegalov, G., Uhlmann, F., & Molodtsov, M. I. (2021) · eLife · doi:10.7554/elife.67530 · Cited by 100
“plexes as they move along chromosomes during gene transcription (Lengronne et al., 2004; Davidson et al., 2016; Ocampo-Hafalla et al., 2016; Busslinger et al., 2017).”
BackgroundWang, X., Cui, W., & Peng, C. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx735 · Cited by 94
“However, recent research showed that transcription could contribute to the formation of chromatin domains by helping position another key architectural protein complex, cohesion (47).”
BackgroundKhoury, A., Achinger-Kawecka, J., Bert, S. A., Smith, G. C., French, H. J., Luu, P., Peters, T. J., Du, Q., Parry, A., Valdés‐Mora, F., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-13753-7 · Cited by 94
New insights into genome folding by loop extrusion from inducible degron technologies
de Wit, E., & Nora, E. P. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00530-4 · Cited by 91
Casà, V., Gines, M. M., Gusmao, E. G., Slotman, J. A., Zirkel, A., Josipović, N., Oole, E., van IJcken, W. F. J., Houtsmuller, A. B., Papantonis, A., et al. (2020) · Genome Research · doi:10.1101/gr.253211.119 · Cited by 95
SMC Complexes: Universal DNA Looping Machines with Distinct Regulators
van Ruiten, M. S., & Rowland, B. D. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.03.003 · Cited by 86
The Birth of the 3D Genome during Early Embryonic Development
Hug, C. B., & Vaquerizas, J. M. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.09.002 · Cited by 90
LINE-1 transcription activates long-range gene expression
Li, X., Bie, L., Wang, Y., Hong, Y., Zhou, Z., Fan, Y., Yan, X., Tao, Y., Huang, C., Zhang, Y., et al. (2024) · Nature Genetics · doi:10.1038/s41588-024-01789-5 · Cited by 97
The expanding phenotypes of cohesinopathies: one ring to rule them all!
Piché, J., Vliet, P. P. V., Pucéat, M., & Andelfinger, G. (2019) · Cell Cycle · doi:10.1080/15384101.2019.1658476 · Cited by 89
Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis
Lambing, C., Tock, A. J., Choi, K., Topp, S. D., Kuo, P. C., Blackwell, A. R., Zhao, X., Osman, K., Higgins, J. D., Franklin, F. C. H., et al. (2020) · The Plant Cell · doi:10.1105/tpc.19.00866 · Cited by 86
A Role for Chromatin Remodeling in Cohesin Loading onto Chromosomes
Muñoz, S., Minamino, M., Casas-Delucchi, C. S., Patel, H., & Uhlmann, F. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.02.027 · Cited by 93
“Along human chromosomes, the CCCTC-binding factor (CTCF) forms alternative cohesin retention sites (Busslinger et al., 2017; Davidson et al., 2016; Ocampo-Hafalla et al., 2016).”
BackgroundSpatial patterns of CTCF sites define the anatomy of TADs and their boundaries
Nanni, L., Ceri, S., & Logie, C. (2020) · Genome Biology · doi:10.1186/s13059-020-02108-x · Cited by 88
“In human cells, Cohesin complexes only accumulate at RNA polymerase II polyadenylation sites when CTCF is absent [48].”
BackgroundKadota, S., Ou, J., Shi, Y., Lee, J. T., Sun, J., & Yildirim, E. (2020) · Nature Communications · doi:10.1038/s41467-020-16394-3 · Cited by 89
Establishing and dissolving cohesion during the vertebrate cell cycle
Morales, C., & Losada, A. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.01.010 · Cited by 80
Wu, Q., Guo, Y., Lu, Y., Li, J., Guo, Y., & Jia, Z. (2020) · Genome biology · doi:10.1186/s13059-020-01984-7 · Cited by 84
“CTCF mediates specific directional loop formation through asymmetric anchoring of the ring-shaped cohesin complex, which slides along chromatin fibers to actively extrude loops [3, 12, 18, 19, 33, 51] .”
BackgroundStructural basis for Scc3-dependent cohesin recruitment to chromatin
Li, Y., Muir, K., Bowler, M. W., Metz, J., Haering, C. H., & Panne, D. (2018) · eLife · doi:10.7554/elife.38356 · Cited by 84
“Whereas the essential role of cohesin in modulating genome architecture, gene expression and DNA damage repair is increasingly well established, comparatively little information is available concerning the molecular determinants of its association with chromatin (Busslinger et al., 2017; Haarhuis et al., 2017; Schwarz…”
BackgroundXiao, T., Li, X., & Felsenfeld, G. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2023127118 · Cited by 83
Forces driving the three‐dimensional folding of eukaryotic genomes
Rada-Iglesias, Á., Grosveld, F. G., & Papantonis, A. (2018) · Molecular Systems Biology · doi:10.15252/msb.20188214 · Cited by 84
“This possibility would also be in agreement with cohesin positioning being regulated by the very act of transcription (Busslinger et al , 2017) and its ensuing supercoiling (Racko et al , 2018), as well as by the increased mobility of genes and enhancers once they transition from an inactive to an…”
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
