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Human cohesin compacts DNA by loop extrusion
Open accessAbstract
Cohesin is a chromosome-bound, multisubunit adenosine triphosphatase complex. After loading onto chromosomes, it generates loops to regulate chromosome functions. It has been suggested that cohesin organizes the genome through loop extrusion, but direct evidence is lacking. Here, we used single-molecule imaging to show that the recombinant human cohesin-NIPBL complex compacts both naked and nucleosome-bound DNA by extruding DNA loops. DNA compaction by cohesin requires adenosine triphosphate (ATP) hydrolysis and is force sensitive. This compaction is processive over tens of kilobases at an average rate of 0.5 kilobases per second. Compaction of double-tethered DNA suggests that a cohesin dimer extrudes DNA loops bidirectionally. Our results establish cohesin-NIPBL as an ATP-driven molecular machine capable of loop extrusion.
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“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 [437]
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 [83]
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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001) · Palaeontologia Electronica · Cited by 17,871
Marko, J. F., & Siggia, E. D. (1995) · Macromolecules · doi:10.1021/ma00130a008 · Cited by 2,348
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
Cohesin: Its Roles and Mechanisms
Nasmyth, K., & Haering, C. H. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134233 · Cited by 1,015
Quantum dots: bright and versatile in vitro and in vivo fluorescence imaging biosensors
Wegner, K. D., & Hildebrandt, N. (2015) · Chemical Society Reviews · doi:10.1039/c4cs00532e · Cited by 992
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
Nasmyth, K. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.091334 · Cited by 805
The 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
Real-time imaging of DNA loop extrusion by condensin
Ganji, M., Shaltiel, I. A., Bisht, S., Kim, E., Kalichava, A., Haering, C. H., & Dekker, C. (2018) · Science · doi:10.1126/science.aar7831 · Cited by 793
Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins
Ciosk, R., Shirayama, M., Shevchenko, A., Tanaka, T., Toth, A., Shevchenko, A., & Nasmyth, K. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80420-7 · Cited by 755
Nonexponential “blinking” kinetics of single CdSe quantum dots: A universal power law behavior
Kuno, M. K., Fromm, D. P., Hamann, H. F., Gallagher, A., & Nesbitt, D. J. (2000) · The Journal of Chemical Physics · doi:10.1063/1.480896 · Cited by 729
Stretching of a Single Tethered Polymer in a Uniform Flow
Perkins, T. T., Smith, D. E., Larson, R. G., & Chu, S. (1995) · Science · doi:10.1126/science.7701345 · Cited by 601
Tonkin, E. T., Wang, T.-J., Lisgo, S., Bamshad, M. J., & Strachan, T. (2004) · Nature Genetics · doi:10.1038/ng1363 · Cited by 594
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
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-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
SMC complexes: from DNA to chromosomes
Uhlmann, F. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.30 · Cited by 536
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
Wapl 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
biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes
Weissmann, F., Petzold, G., VanderLinden, R. T., Veld, P. J. H. I. ’., Brown, N. G., Lampert, F., Westermann, S., Stark, H., Schulman, B. A., & Peters, J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604935113 · Cited by 338
Biochemical reconstitution of topological DNA binding by the cohesin ring
Murayama, Y., & Uhlmann, F. (2013) · Nature · doi:10.1038/nature12867 · Cited by 323
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
The condensin complex is a mechanochemical motor that translocates along DNA
Terakawa, T., Bisht, S., Eeftens, J., Dekker, C., Haering, C., & Greene, E. (2017) · Science · doi:10.1126/science.aan6516 · Cited by 269
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
Scc2 Is a Potent Activator of Cohesin’s ATPase that Promotes Loading by Binding Scc1 without Pds5
Petela, N. J., Gligoris, T. G., Metson, J., Lee, B., Voulgaris, M., Hu, B., Kikuchi, S., Chapard, C., Chen, W., Rajendra, E., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.05.022 · Cited by 196
Cohesin and its regulation: on the logic of X-shaped chromosomes
Haarhuis, J. H. I., Elbatsh, A. M. O., & Rowland, B. D. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.09.010 · Cited by 147
A folded conformation of MukBEF and cohesin
Bürmann, F., Lee, B., Than, T., Sinn, L. R., O’Reilly, F. J., Yatskevich, S., Rappsilber, J., Hu, B., Nasmyth, K., & Löwe, J. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0196-z · Cited by 142
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
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
Cohesinopathies, gene expression, and chromatin organization
Bose, T., & Gerton, J. L. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200912129 · Cited by 95
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
MCM2–7-dependent cohesin loading during S phase promotes sister-chromatid cohesion
Zheng, G., Kanchwala, M., Xing, C., & Yu, H. (2018) · eLife · doi:10.7554/elife.33920 · Cited by 72
High-Throughput Universal DNA Curtain Arrays for Single-Molecule Fluorescence Imaging
Gallardo, I. F., Pasupathy, P., Brown, M. W., Manhart, C. M., Neikirk, D. P., Alani, E., & Finkelstein, I. J. (2015) · Langmuir · doi:10.1021/acs.langmuir.5b02416 · Cited by 60
Topology and structure of an engineered human cohesin complex bound to Pds5B
Hons, M., Veld, P. J. H. I. ’., Kaesler, J., Rombaut, P., Schleiffer, A., Herzog, F., Stark, H., & Peters, J. (2016) · Nature Communications · doi:10.1038/ncomms12523 · Cited by 52
Kim, Y., Furman, C. M., Manhart, C. M., Alani, E., & Finkelstein, I. J. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1244 · Cited by 36
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Soniat, M. M., Myler, L. R., Schaub, J. M., Kim, Y., Gallardo, I. F., & Finkelstein, I. J. (2017) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2017.03.011 · Cited by 32
Regulation of sister chromatid cohesion during the mitotic cell cycle
Zheng, G., & Yu, H. (2015) · Science China Life Sciences · doi:10.1007/s11427-015-4956-7 · Cited by 26
Loop formation by SMC complexes: turning heads, bending elbows, and fixed anchors
Sedeño Cacciatore, Á., & Rowland, B. D. (2019) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2019.04.010 · Cited by 24
Assessing Protein Dynamics on Low-Complexity Single-Stranded DNA Curtains
Schaub, J. M., Zhang, H., Soniat, M. M., & Finkelstein, I. J. (2018) · Langmuir · doi:10.1021/acs.langmuir.8b01812 · Cited by 18
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Metadata
- Authors
- Kim, Y., Shi, Z., Zhang, H., Finkelstein, I. J., & Yu, H.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- The University of Texas at Austin (US)
- Corresponding author
- Kim, Yoori
- Shi, Zhubing
- Finkelstein, Ilya J.
- Yu, Hongtao
- Venue
- Science
- Published
- 2019-12-13
- Volume
- 366
- Issue
- 6471
- Pages
- 1345-1349
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC7387118
- OpenAlex
- W2989713781
- Cited by
- 701
- References
- 42
- Citations by year
- 2026: 84 · 2025: 88 · 2024: 84 · 2023: 106 · 2022: 99 · 2021: 132 · 2020: 105 · 2019: 3
- FWCI
- 28.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (GM120554, GM124096)
- Welch Foundation (I-1441, F-1808)
- Cancer Prevention and Research Institute of Texas (RP160667-P2)
- 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 › Diffusion and Search Dynamics
- Keywords
- cohesin, NIPBL, loop extrusion, DNA condensation, chromosome organization, single-molecule imaging, ATP hydrolysis, force sensitivity, processivity
- MeSH terms
- Single Molecule Imaging, Cohesins, Chromosomal Proteins, Non-Histone, DNA, Proton-Translocating ATPases, Humans, Nucleic Acid Conformation, Nucleosomes, Cell Cycle Proteins, Protein Multimerization
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