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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 [42,46,48,93].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [48]
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“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]
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“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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Cites
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
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382
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
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., et al. (2009) · Science · doi:10.1126/science.1181369 · Cited by 8,898
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
Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments
Durand, N. C., Shamim, M. S., Machol, I., Rao, S. S. P., Huntley, M. H., Lander, E. S., & Aiden, E. L. (2016) · Cell Systems · doi:10.1016/j.cels.2016.07.002 · Cited by 3,860
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
Mediator and cohesin connect gene expression and chromatin architecture
Kagey, M. H., Newman, J. J., Bilodeau, S., Zhan, Y., Orlando, D. A., van Berkum, N. L., Ebmeier, C. C., Goossens, J., Rahl, P. B., Levine, S. S., et al. (2010) · Nature · doi:10.1038/nature09380 · Cited by 1,939
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
Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene
Bell, A. C., & Felsenfeld, G. (2000) · Nature · doi:10.1038/35013100 · Cited by 1,746
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
Nora, E. P., Goloborodko, A., Valton, A.-L., Gibcus, J. H., Uebersohn, A., Abdennur, N., Dekker, J., Mirny, L. A., & Bruneau, B. G. (2017) · Cell · doi:10.1016/j.cell.2017.05.004 · Cited by 1,709
An auxin-based degron system for the rapid depletion of proteins in nonplant cells
Nishimura, K., Fukagawa, T., Takisawa, H., Kakimoto, T., & Kanemaki, M. (2009) · Nature Methods · doi:10.1038/nmeth.1401 · Cited by 1,663
CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus
Hark, A. T., Schoenherr, C. J., Katz, D. J., Ingram, R. S., Levorse, J. M., & Tilghman, S. M. (2000) · Nature · doi:10.1038/35013106 · Cited by 1,547
Cohesins: Chromosomal Proteins that Prevent Premature Separation of Sister Chromatids
Michaelis, C., Ciosk, R., & Nasmyth, K. (1997) · Cell · doi:10.1016/s0092-8674(01)80007-6 · Cited by 1,473
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
Organization of the mitotic chromosome
Naumova, N., Imakaev, M., Fudenberg, G., Zhan, Y., Lajoie, B. R., Mirny, L. A., & Dekker, J. (2013) · Science · doi:10.1126/science.1236083 · Cited by 976 · cited 2×
“…co-depletion of WAPL, PDS5A, and PDS5B enables cohesin to condense chromosomes to an extent that is normally only seen in early mitosis by creating long-range chromosomal cis-interactions that are reminiscent of the ones observed in mitotic chromosomes (Naumova et al, 2013; Nagano et al, 2017).”
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
Guacci, V., Koshland, D. E., & Strunnikov, A. V. (1997) · Cell · doi:10.1016/s0092-8674(01)80008-8 · Cited by 828
Nasmyth, K. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.091334 · Cited by 805
Cell-cycle dynamics of chromosomal organization at single-cell resolution
Nagano, T., Lubling, Y., Várnai, C., Dudley, C., Leung, W., Baran, Y., Mendelson Cohen, N., Wingett, S., Fraser, P., & Tanay, A. (2017) · Nature · doi:10.1038/nature23001 · Cited by 794
Self-citationThe cohesin release factor WAPL restricts chromatin loop extension
Haarhuis, J. H. I., van der Weide, R. H., Blomen, V. A., Yáñez-Cuna, J. O., Amendola, M., van Ruiten, M. S., Krijger, P. H. L., Teunissen, H., Medema, R. H., van Steensel, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.04.013 · Cited by 793
Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells
Zuin, J., Dixon, J. R., van der Reijden, M. I. J. A., Ye, Z., Kolovos, P., Brouwer, R. W. W., van de Corput, M. P. C., van de Werken, H. J. G., Knoch, T. A., van IJcken, W. F. J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317788111 · Cited by 779
Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition
Flyamer, I. M., Gassler, J., Imakaev, M., Brandão, H. B., Ulianov, S. V., Abdennur, N., Razin, S. V., Mirny, L. A., & Tachibana-Konwalski, K. (2017) · Nature · doi:10.1038/nature21711 · Cited by 753
CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus.
Splinter, E., Heath, H., Kooren, J., Palstra, R.-J., Klous, P., Grosveld, F., Galjart, N., & de Laat, W. (2007) · Genes & Development · doi:10.1016/j.bcmd.2006.10.131 · Cited by 742
HiCUP: pipeline for mapping and processing Hi-C data
Wingett, S., Ewels, P., Furlan-Magaril, M., Nagano, T., Schoenfelder, S., Fraser, P., & Andrews, S. (2015) · F1000Research · doi:10.12688/f1000research.7334.1 · Cited by 734
Self-citationKlein, F., Mahr, P., Gálová, M., Buonomo, S. B. C., Michaelis, C., Nairz, K., & Nasmyth, K. (1999) · Cell · doi:10.1016/s0092-8674(00)80609-1 · Cited by 731
Comparative Hi-C Reveals that CTCF Underlies Evolution of Chromosomal Domain Architecture
Vietri Rudan, M., Barrington, C., Henderson, S., Ernst, C., Odom, D. T., Tanay, A., & Hadjur, S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.004 · Cited by 680 · cited 3×
“However, high-resolution genome-wide chromatin conformation capture experiments coupled with DNA sequencing (“Hi-C”) (Lieberman-Aiden et al, 2009) have revealed that most chromatin loops contain convergent CTCF sites (Rao et al, 2014; Vietri Rudan et al, 2015; de Wit et al, 2015).”
CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus
Splinter, E., Heath, H., Kooren, J., Palstra, R.-J., Klous, P., Grosveld, F., Galjart, N., & de Laat, W. (2006) · Genes & Development · doi:10.1101/gad.399506 · Cited by 677
Spencer, S. L., Cappell, S. D., Tsai, F., Overton, K. W., Wang, C. L., & Meyer, T. (2013) · Cell · doi:10.1016/j.cell.2013.08.062 · Cited by 673
CTCF Binding Polarity Determines Chromatin Looping
de Wit, E., Vos, E. S. M., Holwerda, S. J. B., Valdes-Quezada, C., Verstegen, M. J. A. M., Teunissen, H., Splinter, E., Wijchers, P. J., Krijger, P. H. L., & de Laat, W. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.09.023 · Cited by 641 · cited 3×
“However, high-resolution genome-wide chromatin conformation capture experiments coupled with DNA sequencing (“Hi-C”) (Lieberman-Aiden et al, 2009) have revealed that most chromatin loops contain convergent CTCF sites (Rao et al, 2014; Vietri Rudan et al, 2015; de Wit et al, 2015).”
Wapl controls the dynamic association of cohesin with chromatin
Kueng, S., Hegemann, B., Peters, B. H., Lipp, J. J., Schleiffer, A., Mechtler, K., & Peters, J.-M. (2006) · Cell · doi:10.1016/j.cell.2006.09.040 · Cited by 624
Self-citationIdentification of Xenopus SMC protein complexes required for sister chromatid cohesionPreprint
Losada, A., Hirano, M., & Hirano, T. (1998) · Genes & Development · doi:10.1101/gad.12.13.1986 · Cited by 601
Ono, T., Losada, A., Hirano, M., Myers, M., Neuwald, A. F., & Hirano, T. (2003) · Cell · doi:10.1016/s0092-8674(03)00724-4 · Cited by 588
Cohesin relocation from sites of chromosomal loading to places of convergent transcription
Lengronne, A., Katou, Y., Mori, S., Yokobayashi, S., Kelly, G. P., Itoh, T., Watanabe, Y., Shirahige, K., & Uhlmann, F. (2004) · Nature · doi:10.1038/nature02742 · Cited by 588
The cohesin complex and its roles in chromosome biologyPreprint
Peters, J., Tedeschi, A., & Schmitz, J. (2008) · Genes & Development · doi:10.1101/gad.1724308 · Cited by 552
Self-citationSelf-organization of domain structures by DNA-loop-extruding enzymes
Alipour, E., & Marko, J. F. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks925 · Cited by 540 · cited 1×
“According to this idea, two distal chromosomal elements would be brought into direct proximity by a loop extrusion factor such as cohesin which would processively extrude a chromatin loop (Riggs, 1990; Nasmyth, 2001; Alipour & Marko, 2012; Gruber, 2014; Sanborn et al, 2015; Fudenberg et al, 2016).”
BackgroundCTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation
Narendra, V., Rocha, P. P., An, D., Raviram, R., Skok, J. A., Mazzoni, E. O., & Reinberg, D. (2015) · Science · doi:10.1126/science.1262088 · Cited by 535
Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus
Hadjur, S., Williams, L. M., Ryan, N. K., Cobb, B. S., Sexton, T., Fraser, P., Fisher, A. G., & Merkenschlager, M. (2009) · Nature · doi:10.1038/nature08079 · Cited by 525
Self-citationKurukuti, S., Tiwari, V. K., Tavoosidana, G., Pugacheva, E., Murrell, A., Zhao, Z., Lobanenkov, V., Reik, W., & Ohlsson, R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600326103 · Cited by 511
The cohesin ring concatenates sister DNA molecules
Haering, C. H., Farcas, A.-M., Arumugam, P., Metson, J., & Nasmyth, K. (2008) · Nature · doi:10.1038/nature07098 · Cited by 494
Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl
Busslinger, G. A., Stocsits, R. R., van der Lelij, P., Axelsson, E., Tedeschi, A., Galjart, N., & Peters, J.-M. (2017) · Nature · doi:10.1038/nature22063 · Cited by 468 · cited 21×
“…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-citationGandhi, R., Gillespie, P. J., & Hirano, T. (2006) · Current Biology · doi:10.1016/j.cub.2006.10.061 · Cited by 441
An expanded tool kit for the auxin‐inducible degron system in budding yeast
Morawska, M., & Ulrich, H. D. (2013) · Yeast · doi:10.1002/yea.2967 · Cited by 414
Characterization of Vertebrate Cohesin Complexes and Their Regulation in Prophase
Sumara, I., Vorlaufer, E., Gieffers, C., Peters, B. H., & Peters, J. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.4.749 · Cited by 414
Self-citationThe Hitchhiker’s guide to Hi-C analysis: Practical guidelines
Lajoie, B. R., Dekker, J., & Kaplan, N. (2014) · Methods · doi:10.1016/j.ymeth.2014.10.031 · Cited by 394
Cohesin-mediated interactions organize chromosomal domain architecture
Sofueva, S., Yaffe, E., Chan, W., Georgopoulou, D., Vietri Rudan, M., Mira‐Bontenbal, H., Pollard, S. M., Schroth, G. P., Tanay, A., & Hadjur, S. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.237 · Cited by 394
Sororin Mediates Sister Chromatid Cohesion by Antagonizing Wapl
Nishiyama, T., Ladurner, R., Schmitz, J., Kreidl, E., Schleiffer, A., Bhaskara, V., Bando, M., Shirahige, K., Hyman, A. A., Mechtler, K., et al. (2010) · Cell · doi:10.1016/j.cell.2010.10.031 · Cited by 392
Self-citationA 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
Self-citationBlat, Y., Protacio, R. U., Hunter, N., & Kleckner, N. E. (2002) · Cell · doi:10.1016/s0092-8674(02)01167-4 · Cited by 363
Gerlich, D. W., Koch, B., Dupeux, F., Peters, J., & Ellenberg, J. (2006) · Current Biology · doi:10.1016/j.cub.2006.06.068 · Cited by 362
Self-citationWapl is an essential regulator of chromatin structure and chromosome segregation
Tedeschi, A., Wutz, G., Huet, S., Jaritz, M., Wuensche, A., Schirghuber, E., Davidson, I. F., Tang, W., Cisneros, D. A., Bhaskara, V., et al. (2013) · Nature · doi:10.1038/nature12471 · Cited by 359
Self-citationCohesin Is Required for Higher-Order Chromatin Conformation at the Imprinted IGF2-H19 Locus
Nativio, R., Wendt, K. S., Ito, Y., Huddleston, J. E., Uribe‐Lewis, S., Woodfine, K., Krueger, C., Reik, W., Peters, J., & Murrell, A. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000739 · Cited by 325
Self-citationBiochemical reconstitution of topological DNA binding by the cohesin ring
Murayama, Y., & Uhlmann, F. (2013) · Nature · doi:10.1038/nature12867 · Cited by 323
Seitan, V. C., Faure, A. J., Zhan, Y., McCord, R. P., Lajoie, B. R., Ing-Simmons, E., Lenhard, B., Giorgetti, L., Heard, E., Fisher, A. G., et al. (2013) · Genome Research · doi:10.1101/gr.161620.113 · Cited by 318
Building Sister Chromatid Cohesion: Smc3 Acetylation Counteracts an Antiestablishment Activity
Rowland, B. D., Roig, M. B., Nishino, T., Kurze, A., Uluocak, P., Mishra, A., Beckouët, F., Underwood, P., Metson, J., Imre, R., et al. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.02.028 · Cited by 308
Architecture of metaphase chromosomes and chromosome scaffolds
Earnshaw, W. C., & Laemmli, U. K. (1983) · Journal of Cell Biology · doi:10.1083/jcb.96.1.84 · Cited by 305
Cell-Type-Specific TEV Protease Cleavage Reveals Cohesin Functions in Drosophila Neurons
Pauli, A., Althoff, F., Oliveira, R. A., Heidmann, S. K., Schuldiner, O., Lehner, C. F., Dickson, B. J., & Nasmyth, K. (2008) · Developmental Cell · doi:10.1016/j.devcel.2007.12.009 · Cited by 276
Watrin, E., Schleiffer, A., Tanaka, K., Eisenhaber, F., Nasmyth, K., & Peters, J.-M. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.049 · Cited by 270
Self-citationTachibana-Konwalski, K., Godwin, J., van der Weyden, L., Champion, L., Kudo, N. R., Adams, D. J., & Nasmyth, K. (2010) · Genes & Development · doi:10.1101/gad.605910 · Cited by 265
Saitoh, N., Goldberg, I., Wood, E. R., & Earnshaw, W. C. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.2.303 · Cited by 258
DNA Entry into and Exit out of the Cohesin Ring by an Interlocking Gate Mechanism
Murayama, Y., & Uhlmann, F. (2015) · Cell · doi:10.1016/j.cell.2015.11.030 · Cited by 252
Cohesin’s DNA Exit Gate Is Distinct from Its Entrance Gate and Is Regulated by Acetylation
Chan, K., Roig, M. B., Hu, B., Beckouët, F., Metson, J., & Nasmyth, K. (2012) · Cell · doi:10.1016/j.cell.2012.07.028 · Cited by 249
Rapid movement and transcriptional re-localization of human cohesin on DNA
Davidson, I. F., Goetz, D., Zaczek, M. P., Molodtsov, M. I., Huis in 't Veld, P. J., Weissmann, F., Litos, G., Cisneros, D. A., Ocampo‐Hafalla, M., Ladurner, R., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201695402 · Cited by 246
Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin
Stigler, J., Çamdere, G. Ö., Koshland, D. E., & Greene, E. C. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.003 · Cited by 229 · cited 1×
“…loop extrusion is also consistent with the observation that cohesin can move along DNA, both in vitro (Davidson et al, 2016; Kanke et al, 2016; Stigler et al, 2016) and in vivo (Lengronne & Pasero, 2014; Busslinger et al, 2017) and is constrained during these movements by CTCF (Davidson et…”
Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle
Dewar, H., Tanaka, K., Nasmyth, K., & Tanaka, T. U. (2004) · Nature · doi:10.1038/nature02328 · Cited by 203
Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl–Pds5 and Sgo1
Shintomi, K., & Hirano, T. (2009) · Genes & Development · doi:10.1101/gad.1844309 · Cited by 203
Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster
Mishiro, T., Ishihara, K., Hino, S., Tsutsumi, S., Aburatani, H., Shirahige, K., Kinoshita, Y., & Nakao, M. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.81 · Cited by 197
Characterization of a DNA exit gate in the human cohesin ring
Veld, P. J. H. I. ’., Herzog, F., Ladurner, R., Davidson, I. F., Piric, S., Kreidl, E., Bhaskara, V., Aebersold, R. H., & Peters, J. (2014) · Science · doi:10.1126/science.1256904 · Cited by 189
Self-citationComparison of Hi-C results using in-solution versus in-nucleus ligation
Nagano, T., Várnai, C., Schoenfelder, S., Javierre, B.-M., Wingett, S. W., & Fraser, P. (2015) · Genome Biology · doi:10.1186/s13059-015-0753-7 · Cited by 166
Self-citationHeidinger-Pauli, J. M., Mert, O., Davenport, C., Guacci, V., & Koshland, D. E. (2010) · Current Biology · doi:10.1016/j.cub.2010.04.018 · Cited by 145
Structural Basis and IP6 Requirement for Pds5-Dependent Cohesin Dynamics
Ouyang, Z., Zheng, G., Tomchick, D. R., Luo, X., & Yu, H. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.033 · Cited by 138
Cohesin acetylation and Wapl-Pds5 oppositely regulate translocation of cohesin along DNA
Kanke, M., Tahara, E., Huis in't Veld, P. J., & Nishiyama, T. (2016) · The EMBO Journal · doi:10.15252/embj.201695756 · Cited by 136
Generation and validation of homozygous fluorescent knock-in cells using CRISPR-Cas9 genome editing
Koch, B., Nijmeijer, B., Kueblbeck, M., Cai, Y., Walther, N., & Ellenberg, J. (2018) · Nature Protocols · doi:10.1038/nprot.2018.042 · Cited by 134
Self-citationRiggs, A. D. (1990) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1990.0012 · Cited by 126
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Metadata
- 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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