The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
DNA loop extrusion by human cohesin
Abstract
Eukaryotic genomes are folded into loops and topologically associating domains, which contribute to chromatin structure, gene regulation, and gene recombination. These structures depend on cohesin, a ring-shaped DNA-entrapping adenosine triphosphatase (ATPase) complex that has been proposed to form loops by extrusion. Such an activity has been observed for condensin, which forms loops in mitosis, but not for cohesin. Using biochemical reconstitution, we found that single human cohesin complexes form DNA loops symmetrically at rates up to 2.1 kilo-base pairs per second. Loop formation and maintenance depend on cohesin's ATPase activity and on NIPBL-MAU2, but not on topological entrapment of DNA by cohesin. During loop formation, cohesin and NIPBL-MAU2 reside at the base of loops, which indicates that they generate loops by extrusion. Our results show that cohesin and NIPBL-MAU2 form an active holoenzyme that interacts with DNA either pseudo-topologically or non-topologically to extrude genomic interphase DNA into loops.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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
“Loop extrusion was initially proposed theoretically based on molecular dynamics simulations [342, 435] and then validated in single-molecule assays [436, 437].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [436]
In the citing paper
“loop extrusion mediated by cohesin and CTCF mediates the formation of chromatin loops and self-interacting Topologically Associating Domains (TADs)”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [82]
Citations
Cites
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
Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity
Ran, F. A., Hsu, P. D., Lin, C.-Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., Inoue, A., Matoba, S., Zhang, Y., et al. (2013) · Cell · doi:10.1016/j.cell.2013.08.021 · Cited by 3,299
Spatial partitioning of the regulatory landscape of the X-inactivation centre
Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., et al. (2012) · Nature · doi:10.1038/nature11049 · Cited by 2,895
Formation of chromosomal domains by loop extrusion
Fudenberg, G., Imakaev, M., Lu, C., Goloborodko, A., Abdennur, N., & Mirny, L. A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.085 · Cited by 2,003
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
Sanborn, A. L., Rao, S. S. P., Huang, S.-C., Durand, N. C., Huntley, M. H., Jewett, A. I., Bochkov, I. D., Chinnappan, D., Cutkosky, A., Li, J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518552112 · Cited by 1,730
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
Cohesin mediates transcriptional insulation by CCCTC-binding factor
Wendt, K. S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., et al. (2008) · Nature · doi:10.1038/nature06634 · Cited by 1,193
Cohesins Functionally Associate with CTCF on Mammalian Chromosome Arms
Parelho, V., Hadjur, S., Spivakov, M., Leleu, M., Sauer, S., Gregson, H. C., Jarmuz, A., Canzonetta, C., Webster, Z., Nesterova, T., et al. (2008) · Cell · doi:10.1016/j.cell.2008.01.011 · Cited by 900
Flagged first, then by citations
Cited by
Sorted by citations
The Self-Organizing Genome: Principles of Genome Architecture and Function
Misteli, T. (2020) · Cell · doi:10.1016/j.cell.2020.09.014 · Cited by 742
“This model is supported by the recent demonstration of loop extrusion activity of yeast cohesin in vitro (Davidson et al., 2019).”
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
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
The molecular basis and disease relevance of non-homologous DNA end joining
Zhao, B., Rothenberg, E., Ramsden, D. A., & Lieber, M. R. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00297-8 · Cited by 411
Mechanisms of enhancer action: the known and the unknown
Panigrahi, A., & O’Malley, B. W. (2021) · Genome biology · doi:10.1186/s13059-021-02322-1 · Cited by 376
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
Epigenetic regulation of T cell exhaustion
Belk, J. A., Dániel, B., & Satpathy, A. T. (2022) · Nature Immunology · doi:10.1038/s41590-022-01224-z · Cited by 346
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
Cohesin and CTCF control the dynamics of chromosome folding
Mach, P., Kos, P. I., Zhan, Y., Cramard, J., Gaudin, S., Tünnermann, J., Marchi, E., Eglinger, J., Zuin, J., Kryzhanovska, M., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01232-7 · Cited by 269
Roayaei Ardakany, A., Gezer, H. T., Lonardi, S., & Ay, F. (2020) · Genome Biology · doi:10.1186/s13059-020-02167-0 · Cited by 250
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
Cryo-EM structure of the human cohesin-NIPBL-DNA complex
Shi, Z., Gao, H., Bai, X., & Yu, H. (2020) · Science · doi:10.1126/science.abb0981 · Cited by 228
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
McCord, R. P., Kaplan, N., & Giorgetti, L. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.021 · Cited by 220
“2016) and recent in vitro evidence (Golfier et al. 2019; Davidson et al. 2019), cohesin could extrude DNA loops at rates as high as ~100 kb/ min.”
BackgroundMiron, E., Oldenkamp, R., Brown, J. M., Pinto, D. M. S., Xu, C. S., Faria, A. R., Shaban, H. A., Rhodes, J. D. P., Innocent, C., de Ornellas, S., et al. (2020) · Science Advances · doi:10.1126/sciadv.aba8811 · Cited by 200
Cohesin and condensin extrude DNA loops in a cell cycle-dependent manner
Golfier, S., Quail, T., Kimurâ, H., & Jan Brugués, A. (2020) · eLife · doi:10.7554/elife.53885 · Cited by 201
“Recent in vitro work demonstrated that cohesin can extrude DNA loops symmetrically (Davidson et al., 2019; Kim et al., 2019), though this activity has not been directly visualized in cellular contexts (Rao et al.”
BackgroundRegulation 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 194
“Upon CTCF depletion, the cohesin complex can extrude chromatin 37,38 through TAD borders, inducing ectopic contacts between adjacent TADs and abolishing preferential intra-TAD interactions.”
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 198
Enhancer 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
Huang, 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
Primary Role of the Nucleosome
Kornberg, R. D., & Lorch, Y. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.07.020 · Cited by 178
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
“This hypothesis is supported by recent single-molecule experiments which have shown that in vitro cohesin forms DNA loops by extrusion in a manner that depends on NIPBL-MAU2 (Davidson et al., 2019; Kim et al., 2019).”
BackgroundResultThiecke, 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
Enhancer–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
“…& Phillips-Cremins, 2020) to kbp-sized “loop domains (Rao et al., 2014)] are insulated from one another via CTCF-demarcated boundaries, while the chromatin at and within these domains is actively extruded into loops by cohesin (Fudenberg et al., 2016; Davidson et al., 2019; Kim et al., 2019).”
BackgroundBridging-induced phase separation induced by cohesin SMC protein complexes
Ryu, J., Bouchoux, C., Liu, H. W., Kim, E., Minamino, M., de Groot, R., Katan, A. J., Bonato, A., Marenduzzo, D., Michieletto, D., et al. (2021) · Science Advances · doi:10.1126/sciadv.abe5905 · Cited by 163
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
Human Condensin I and II Drive Extensive ATP-Dependent Compaction of Nucleosome-Bound DNA
Kong, M., Cutts, E., Pan, D., Beuron, F., Kaliyappan, T., Xue, C., Morris, E. P., Musacchio, A., Vannini, A., & Greene, E. C. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.04.026 · Cited by 162
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
Uyehara, C. M., & Apostolou, E. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112068 · Cited by 143
Sanborn, A. L., Yeh, B. T., Feigerle, J. T., Hao, C. V., Townshend, R. J. L., Aiden, E. L., Dror, R. O., & Kornberg, R. D. (2021) · eLife · doi:10.7554/elife.68068 · Cited by 168
Cohesin mediates DNA loop extrusion by a “swing and clamp” mechanism
Bauer, B. W., Davidson, I., Canena, D., Wutz, G., Tang, W., Litos, G., Horn, S., Hinterdorfer, P., & Peters, J. (2021) · Cell · doi:10.1016/j.cell.2021.09.016 · Cited by 142
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
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
“Recent advances in in vitro single molecule imaging experiments of cohesin-mediated DNA extrusion (58,59) offer an exciting opportunity to measure these parameters.”
BackgroundA Structure-Based Mechanism for DNA Entry into the Cohesin Ring
Higashi, T. L., Eickhoff, P., Sousa, J. S., Locke, J., Nans, A., Flynn, H. R., Snijders, A. P., Papageorgiou, G., O’Reilly, N., Chen, Z. A., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.07.013 · Cited by 146
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
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
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 147
Wapl 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 143
The Smc5/6 complex is a DNA loop-extruding motor
Pradhan, B., Kanno, T., Igarashi, M. U., Loke, M. S., Baaske, M. D., Wong, J. S. K., Jeppsson, K. E., Björkegren, C., & Kim, E. (2023) · Nature · doi:10.1038/s41586-023-05963-3 · Cited by 147
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
Ulianov, S. V., Velichko, A. K., Magnitov, M. D., Luzhin, A. V., Golov, A. K., Ovsyannikova, N., Kireev, I. I., Gavrikov, A. S., Mishin, A. S., Garaev, A. K., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab249 · Cited by 137
“Although the DNA loop extrusion machinery has been properly characterized (9,10), the processes/forces that mediate the spatial segregation of active and inactive chromatin remain poorly understood.”
BackgroundDileep, V., Boix, C. A., Mathys, H., Marco, A., Welch, G. M., Meharena, H. S., Loon, A., Jeloka, R., Peng, Z., Bennett, D. A., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.038 · Cited by 130
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 141
“Recently, dedicated microfluidics devices coupled with fluorescence imaging, allowed for the direct visualization of cohesin-mediated loop extrusion in-vitro and in real-time (Davidson et al , 2019; Kim et al , 2019; Golfier et al , 2020).”
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
Mitochondrial base editor induces substantial nuclear off-target mutations
Lei, Z., Meng, H., Liu, L., Zhao, H., Rao, X., Yan, Y., Wu, H., Liu, M., He, A., & Yi, C. (2022) · Nature · doi:10.1038/s41586-022-04836-5 · Cited by 131
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
“, 2019), most of our Hi-C detected chromatin contacts were bound by CTCF and cohesin and their size was inversely correlated with the rate of recovery, further supporting that CTCF/cohesin-mediated loop extrusion (Alipour and Marko, 2012; Davidson et al., 2019; Fudenberg et al., 2016; Golfier et al., 2020; Kim et al.,…”
BackgroundResultA hold-and-feed mechanism drives directional DNA loop extrusion by condensin
Shaltiel, I. A., Datta, S., Lecomte, L., Hassler, M., Kschonsak, M., Bravo, S., Stober, C., Ormanns, J., Eustermann, S., & Haering, C. H. (2022) · Science · doi:10.1126/science.abm4012 · Cited by 112
“Single-molecule experiments have demonstrated that both complexes can create and processively enlarge DNA loops over tens of kilo-base pairs (kbp) in vitro (6-9).”
BackgroundLee, R., Kang, M.-K., Kim, Y.-J., Yang, B., Shim, H., Kim, S., Kim, K., Yang, C. M., Min, B.-G., Jung, W.-J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab1242 · Cited by 123
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
Cohesin regulates homology search during recombinational DNA repair
Piazza, A., Bordelet, H., Dumont, A., Thierry, A., Savocco, J., Girard, F., & Koszul, R. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00783-x · Cited by 125
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
Conformation 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 111
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 123
Emerging themes in cohesin cancer biology
Waldman, T. A. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-0270-1 · Cited by 117
Cryo-EM structures of holo condensin reveal a subunit flip-flop mechanism
Lee, B., Merkel, F., Allegretti, M., Hassler, M., Cawood, C., Lecomte, L., O’Reilly, F. J., Sinn, L. R., Gutiérrez-Escribano, P., Kschonsak, M., et al. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0457-x · Cited by 114
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 125
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
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
Force generation by protein–DNA co-condensation
Quail, T., Golfier, S., Elsner, M., Ishihara, K., Murugesan, V., Renger, R., Jülicher, F., & Jan Brugués, A. (2021) · Nature Physics · doi:10.1038/s41567-021-01285-1 · Cited by 110
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
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
“5 kb/min (cohesin in HCT116 cells [26]); ~6-12 kb/min (condensin II in chicken cells [81]); ~54 kb/min (bacterial SMC complex [82]), and ~30-60 kb/min on naked DNA in vitro [21,23].”
BackgroundInfluentialPopay, T. M., & Dixon, J. R. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102117 · Cited by 94
“The Cohesin complex is generally thought to entrap DNA in its ring-like structure (88), but loop extrusion can be driven by entrapment-incompetent Cohesin in vitro (91).”
BackgroundDeep, A., Gu, Y., Gao, Y.-Q., Ego, K. M., Herzik, M. A., Zhou, H., & Corbett, K. D. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.09.008 · Cited by 106
To loop or not to loop: what is the role of TADs in enhancer function and gene regulation?
Cavalheiro, G. R., Pollex, T., & Furlong, E. E. M. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.12.015 · Cited by 108
Epigenetic Reprogramming in Early Animal DevelopmentPreprint
Du, Z., Zhang, K., & Xie, W. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a039677 · Cited by 105
Surdez, D., Zaïdi, S., Grossetête, S., Laud-Duval, K., Ferre, A. S., Mous, L., Vourc’h, T., Tirode, F., Pierron, G., Raynal, V., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.04.001 · 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
“Loop extrusion rates were determined using FIJI ImageJ software as described (Davidson et al., 2019).”
BackgroundMethodResultInfluentialDNA-loop-extruding SMC complexes can traverse one another in vivo
Brandão, H. B., Ren, Z., Karaboja, X., Mirny, L. A., & Wang, X. (2021) · Nature Structural & Molecular Biology · doi:10.1038/s41594-021-00626-1 · Cited by 90
Multiscale modeling of genome organization with maximum entropy optimization
Lin, X., Qi, Y., Latham, A. P., & Zhang, B. (2021) · The Journal of Chemical Physics · doi:10.1063/5.0044150 · Cited by 93
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
Collier, J., Lee, B.-G., Roig, M. B., Yatskevich, S., Petela, N. J., Metson, J., Voulgaris, M., Llamazares, A. G., Löwe, J., & Nasmyth, K. (2020) · eLife · doi:10.7554/elife.59560 · Cited by 82
“Our finding that Scc3 is essential for S-K but not E-S/E-K entrapment reveals that Scc3 has a unique role in promoting entry of DNA inside the SMC-kleisin ring as well as being necessary for loop extrusion (Davidson et al., 2019).”
BackgroundResultInfluentialChromosome Organization in Early Meiotic Prophase
Grey, C., & de Massy, B. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.688878 · Cited by 100
Visualizing the genome in high resolution challenges our textbook understanding
Lakadamyali, M., & Cosma, M. P. (2020) · Nature Methods · doi:10.1038/s41592-020-0758-3 · Cited by 92
Topology in soft and biological matter
Tubiana, L., Alexander, G. P., Barbensi, A., Buck, D., Cartwright, J. H. E., Chwastyk, M., Cieplak, M., Coluzza, I., Čopar, S., Craik, D. J., et al. (2024) · Physics Reports · doi:10.1016/j.physrep.2024.04.002 · Cited by 102
BRD4 orchestrates genome folding to promote neural crest differentiation
Linares-Saldana, R., Kim, W., Bolar, N. A., Zhang, H., Koch-Bojalad, B. A., Yoon, S., Shah, P. P., Karnay, A. M., Park, D. S., Luppino, J. M., et al. (2021) · Nature Genetics · doi:10.1038/s41588-021-00934-8 · Cited by 91
The condensin holocomplex cycles dynamically between open and collapsed states
Ryu, J., Katan, A. J., van der Sluis, E. O., Wisse, T., de Groot, R., Haering, C. H., & Dekker, C. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0508-3 · Cited by 96
Computational methods for analysing multiscale 3D genome organization
Zhang, Y., Boninsegna, L., Yang, M., Misteli, T., Alber, F., & Ma, J. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00638-1 · Cited by 97
“…cohesin complexes slide along chromatin fibres in different directions to form loops, was proposed more than 20 years ago to play a role in chromatin condensation 93 , but was only recently tested in simulations 7,93–96 and eventually observed in vitro in single-molecule experiments 97,98 (Fig.”
Paulson, J. R., Hudson, D. F., Cisneros-Soberanis, F., & Earnshaw, W. C. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.03.014 · Cited by 96
Ortabozkoyun, H., Huang, P., Cho, H., Narendra, V. K., LeRoy, G., González-Buendía, E., Skok, J. A., Tsirigos, A., Mazzoni, E. O., & Reinberg, D. (2022) · Nature Genetics · doi:10.1038/s41588-021-01008-5 · Cited by 85
Spatial 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
“Conclusions Altogether, we discovered that, when classified properly, CTCF site orientation forms a powerful grammar that is compliant with recently published loop extrusion models [36, 37].”
BackgroundRyu, J.-K., Rah, S.-H., Janissen, R., Kerssemakers, J. W. J., Bonato, A., Michieletto, D., & Dekker, C. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkab1268 · Cited by 87
“…somewhat lower than values that can be estimated by combining the loop extrusion speed and ATPase rates in previous in vitro studies on condensin and cohesin with ∼ 0.5–1 kb / s and 2 ATP / s (11,13,45), and of SMC-ScpAB from B. subtilis and C. crescentus with 300–800 bp / s and 1 ATP / s (46– 48).”
InfluentialThe role of 3D chromatin domains in gene regulation: a multi-facetted view on genome organization
Ibrahim, D. M., & Mundlos, S. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.02.015 · Cited by 87
Jpx RNA regulates CTCF anchor site selection and formation of chromosome loops
Oh, H. J., Aguilar, R., Kesner, B., Lee, H.-G., Kriz, A. J., Chu, H.-P., & Lee, J. T. (2021) · Cell · doi:10.1016/j.cell.2021.11.012 · Cited by 84
Tracking and interpreting long-range chromatin interactions with super-resolution live-cell imaging
Brandão, H. B., Gabriele, M., & Hansen, A. S. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.11.002 · Cited by 77
Architecture and Dynamics of Meiotic Chromosomes
Ur, S. N., & Corbett, K. D. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020235 · Cited by 82
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81
“Loop extrusion was initially proposed theoretically based on molecular dynamics simulations [342, 435] and then validated in single-molecule assays [436, 437].”
MethodDebaugny, R. E., & Skok, J. A. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.02.021 · Cited by 83
“The CCCTC-binding factor (CTCF) is known to play a key role in organizing chromatin into highly self-interacting topologically associated domains (TADs), by promoting the formation of cohesin-mediated loops and boundaries that are important for gene regulation [1-6].”
BackgroundMulti-contact 3C reveals that the human genome during interphase is largely not entangled
Tavares-Cadete, F., Norouzi, D., Dekker, B., Liu, Y., & Dekker, J. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0506-5 · Cited by 78
The cohesin acetylation cycle controls chromatin loop length through a PDS5A brake mechanism
van Ruiten, M. S., van Gent, D., Cacciatore, Á. S., Fauster, A., Willems, L., Hekkelman, M. L., Hoekman, L., Altelaar, M. A. F., Haarhuis, J. H. I., Brummelkamp, T. R., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00773-z · Cited by 82
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
Cryo-EM structure of MukBEF reveals DNA loop entrapment at chromosomal unloading sites
Bürmann, F., Funke, L. F. H., Chin, J. W., & Löwe, J. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.011 · Cited by 74
Convergent genes shape budding yeast pericentromeres
Paldi, F., Alver, B., Robertson, D., Schalbetter, S. A., Kerr, A. R. W., Kelly, D. A., Baxter, J., Neale, M. J., & Marston, A. L. (2020) · Nature · doi:10.1038/s41586-020-2244-6 · Cited by 80
Bastié, N., Chapard, C., Dauban, L., Gadal, O., Beckouët, F., & Koszul, R. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00780-0 · Cited by 70
Jeppsson, K., Sakata, T., Nakato, R., Milanova, S., Shirahige, K., & Björkegren, C. (2022) · Science Advances · doi:10.1126/sciadv.abn7063 · Cited by 59
Chromatin jets define the properties of cohesin-driven in vivo loop extrusion.
Guo, Y., Al-Jibury, E., Garcia-Millan, R., Ntagiantas, K., King, J. W. D., Nash, A. J., Galjart, N., Lenhard, B., Rueckert, D., Fisher, A., et al. (2022) · Molecules and Cells · doi:10.1016/j.molcel.2022.09.003 · Cited by 69
TADs: Dynamic structures to create stable regulatory functions
da Costa-Nunes, J. A., & Noordermeer, D. (2023) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2023.102622 · Cited by 87
Condensin-driven loop extrusion on supercoiled DNA
Kim, E., Gonzalez, A., Pradhan, B., van der Torre, J., & Dekker, C. (2021) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00802-x · Cited by 72
Srinivasan, M., Fumasoni, M., Petela, N. J., Murray, A. W., & Nasmyth, K. (2020) · eLife · doi:10.7554/elife.56611 · Cited by 75
“Scc2 is not merely a loading factor as it is also necessary for maintaining loop extrusion in vitro (Davidson et al., 2019) as well as cohesin’s association with chromatin in vivo during G1 phase (Srinivasan et al.”
BackgroundBRD2 compartmentalizes the accessible genome
Xie, L., Dong, P., Qi, Y., Hsieh, T.-H. S., English, B. P., Jung, S., Chen, X., Marzio, M. D., Casellas, R. C., Chang, H. Y., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01044-9 · Cited by 66
“pAG-Tn5 was ordered from EpiCypher (15-1017).”
Metadata
- Authors
- Davidson, I. F., Bauer, B., Goetz, D., Tang, W., Wutz, G., & Peters, J.-M.
- Affiliations
- Research Institute of Molecular Pathology (AT)
- Corresponding author
- Peters, Jan-Michael
- Venue
- Science
- Published
- 2019-12-13
- Volume
- 366
- Issue
- 6471
- Pages
- 1338-1345
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2991248607
- Cited by
- 863
- References
- 46
- Citations by year
- 2026: 117 · 2025: 126 · 2024: 109 · 2023: 121 · 2022: 123 · 2021: 148 · 2020: 113 · 2019: 5
- FWCI
- 32.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Boehringer Ingelheim
- European Molecular Biology Organization (Long-term Fellowship)
- H2020 European Research Council (693949)
- Human Frontier Science Program (Long-term Fellowship)
- Austrian Research Promotion Agency (FFG-852936)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- cohesin, DNA loop extrusion, topologically associating domains, chromatin folding, interphase chromatin, holoenzyme, condensin
- MeSH terms
- Cohesins, Chromosomal Proteins, Non-Histone, DNA, DNA-Binding Proteins, Proton-Translocating ATPases, HeLa Cells, Humans, Nucleic Acid Conformation, Cell Cycle Proteins, Holoenzymes
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
