Organizational principles of 3D genome architecture
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Studies of 3D chromatin organization have suggested that chromosomes are hierarchically organized into large compartments composed of smaller domains called topologically associating domains (TADs). Recent evidence suggests that compartments are smaller than previously thought and that the transcriptional or chromatin state is responsible for interactions leading to the formation of small compartmental domains in all organisms. In vertebrates, CTCF forms loop domains, probably via an extrusion process involving cohesin. CTCF loops cooperate with compartmental domains to establish the 3D organization of the genome. The continuous extrusion of the chromatin fibre by cohesin may also be responsible for the establishment of enhancer-promoter interactions and stochastic aspects of the transcription process. These observations suggest that the 3D organization of the genome is an emergent property of chromatin and its components, and thus may not be only a determinant but also a consequence of its function.
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It has been proposed that Drosophila TADs are formed by condensation of nucleosomes and thus should be rather called 'compartmental domains'.
“It has been proposed that Drosophila TADs are formed by condensation of nucleosomes [123] and thus should be rather called “compartmental domains” [124].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [124]
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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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Single-cell Hi-C reveals cell-to-cell variability in chromosome structure
Nagano, T., Lubling, Y., Stevens, T. J., Schoenfelder, S., Yaffe, E., Dean, W., Laue, E. D., Tanay, A., & Fraser, P. (2013) · Nature · doi:10.1038/nature12593 · Cited by 1,589 · see citing works
Multiscale 3D Genome Rewiring during Mouse Neural Development
Bonev, B., Mendelson Cohen, N., Szabo, Q., Fritsch, L., Papadopoulos, G. L., Lubling, Y., Xu, X., Lv, X., Hugnot, J.-P., Tanay, A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.043 · Cited by 1,338 · see citing works
Two independent modes of chromatin organization revealed by cohesin removal
Schwarzer, W., Abdennur, N., Goloborodko, A., Pekowska, A., Fudenberg, G., Loe-Mie, Y., Fonseca, N. A., Huber, W., Haering, C. H., Mirny, L., et al. (2017) · Nature · doi:10.1038/nature24281 · Cited by 1,196 · see citing works
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 · see citing works
CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function
Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D. U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.038 · Cited by 958 · see citing works
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 · see citing works
3D structures of individual mammalian genomes studied by single-cell Hi-C
Stevens, T. J., Lando, D., Basu, S., Atkinson, L. P., Cao, Y., Lee, S. F., Leeb, M., Wohlfahrt, K. J., Boucher, W., O’Shaughnessy-Kirwan, A., et al. (2017) · Nature · doi:10.1038/nature21429 · Cited by 832 · see citing works
Nasmyth, K. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.091334 · Cited by 805 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
The code and beyond: transcription regulation by the RNA polymerase II carboxy-terminal domain
Harlen, K. M., & Churchman, L. S. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.10 · Cited by 499 · see citing works
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 · see citing works
YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment
Beagan, J. A., Duong, M. T., Titus, K. R., Zhou, L., Cao, Z., Ma, J., Lachanski, C. V., Gillis, D. R., & Phillips-Cremins, J. E. (2017) · Genome Research · doi:10.1101/gr.215160.116 · Cited by 299 · see citing works
Wang, X., Brandão, H. B., Le, T. B. K., Laub, M. T., & Rudner, D. Z. (2017) · Science · doi:10.1126/science.aai8982 · Cited by 293 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Flagged first, then by citations
Research works printed but not linked: 66
- [1]Fraser J, Williamson I, Bickmore WA & Dostie J An Overview of Genome Organization and How We Got There: from FISH to Hi-C. Microbiol. Mol. Biol. Rev. MMBR 79, 347– 372 (2015). 26223848 PMC4517094
- [4]Beliveau BJ Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes. Nat. Commun 6, 7147 (2015). 25962338 PMC4430122
- [5]Ni Y Super-resolution imaging of a 2.5 kb non-repetitive DNA in situ in the nuclear genome using molecular beacon probes. eLife 6, (2017). PMC5433842 28485713
- [6]Nagano T Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature 547, 61– 67 (2017). 28682332 PMC5567812
- [7]Pegoraro G & Misteli T High-Throughput Imaging for the Discovery of Cellular Mechanisms of Disease. Trends Genet. TIG 33, 604– 615 (2017). 28732598 PMC5562530
- [8]Lieberman-Aiden E Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome. Science 326, 289– 293 (2009). 19815776 PMC2858594
- [10]Hou C, Li L, Qin ZS & Corces VG Gene Density, Transcription, and Insulators Contribute to the Partition of the Drosophila Genome into Physical Domains. Mol. Cell 48, 471– 484 (2012). 23041285 PMC3496039
- [11]Sexton T Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome. Cell 148, 458– 472 (2012). 22265598
- [13]Bonev B & Cavalli G Organization and function of the 3D genome. Nat. Rev. Genet 17, 661– 678 (2016). 27739532
- [14]Schmitt AD, Hu M & Ren B Genome-wide mapping and analysis of chromosome architecture. Nat. Rev. Mol. Cell Biol 17, 743– 755 (2016). 27580841 PMC5763923
- [15]Hnisz D, Day DS & Young RA Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control. Cell 167, 1188– 1200 (2016). 27863240 PMC5125522
- [16]Merkenschlager M & Nora EP CTCF and Cohesin in Genome Folding and Transcriptional Gene Regulation. Annu. Rev. Genomics Hum. Genet (2016). doi: 10.1146/annurev-genom-083115-022339 27089971 · DOI
- [17]Ong C-T & Corces VG CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet 15, 234– 246 (2014). 24614316 PMC4610363
- [18]Lajoie BR, Dekker J & Kaplan N The Hitchhiker’s guide to Hi-C analysis: Practical guidelines. Methods 72, 65– 75 (2015). 25448293 PMC4347522
- [19]Rao SSP A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665– 1680 (2014). 25497547 PMC5635824
- [20]Rowley MJ Evolutionarily Conserved Principles Predict 3D Chromatin Organization. Mol. Cell (2017). doi: 10.1016/j.molcel.2017.07.022 PMC5591081 28826674 · DOI
- [22]Dong P 3D Chromatin Architecture of Large Plant Genomes Determined by Local A/B Compartments. Mol. Plant 10, 1497– 1509 (2017). 29175436
- [23]Haddad N, Jost D & Vaillant C Perspectives: using polymer modeling to understand the formation and function of nuclear compartments. Chromosome Res 25, 35– 50 (2017). 28091870 PMC5346151
- [24]Huang J, Marco E, Pinello L & Yuan G-C Predicting chromatin organization using histone marks. Genome Biol 16, (2015). PMC4549084 26272203
- [25]Di Pierro M, Cheng RR, Lieberman Aiden E, Wolynes PG & Onuchic JN De novo prediction of human chromosome structures: Epigenetic marking patterns encode genome architecture. Proc. Natl. Acad. Sci. U. S. A 114, 12126– 12131 (2017). 29087948 PMC5699090
- [27]Le TBK, Imakaev MV, Mirny LA & Laub MT High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342, 731– 734 (2013). 24158908 PMC3927313
- [28]Li L Widespread rearrangement of 3D chromatin organization underlies polycomb- mediated stress-induced silencing. Mol. Cell 58, 216– 231 (2015). 25818644 PMC4402144
- [29]Hug CB, Grimaldi AG, Kruse K & Vaquerizas JM Chromatin Architecture Emerges during Zygotic Genome Activation Independent of Transcription. Cell 169, 216– 228. e19 (2017). 28388407
- [30]Bensaude O Inhibiting eukaryotic transcription. Which compound to choose? How to evaluate its activity?: Which compound to choose? How to evaluate its activity? Transcription 2, 103– 108 (2011). 21922053 PMC3173647
- [31]Du Z Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547, 232– 235 (2017). 28703188
- [32]Ke Y 3D Chromatin Structures of Mature Gametes and Structural Reprogramming during Mammalian Embryogenesis. Cell 170, 367– 381. e20 (2017). 28709003
- [34]Jung YH Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes. Cell Rep 18, 1366– 1382 (2017). 28178516 PMC5313040
- [35]Battulin N Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol 16, (2015). PMC4434584 25886366
- [36]Cubeñas-Potts C & Corces VG Architectural proteins, transcription, and the three- dimensional organization of the genome. FEBS Lett 589, 2923– 2930 (2015). 26008126 PMC4598269
- [37]Cubeñas-Potts C Different enhancer classes in Drosophila bind distinct architectural proteins and mediate unique chromatin interactions and 3D architecture. Nucleic Acids Res 45, 1714– 1730 (2016). PMC5389536 27899590
- [39]Hnisz D, Shrinivas K, Young RA, Chakraborty AK & Sharp PA A Phase Separation Model for Transcriptional Control. Cell 169, 13– 23 (2017). 28340338 PMC5432200
- [40]Larson AG Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236– 240 (2017). 28636604 PMC5606208
- [41]Lin Y, Currie SL & Rosen MK Intrinsically disordered sequences enable modulation of protein phase separation through distributed tyrosine motifs. J. Biol. Chem jbc.M117.800466 (2017). doi: 10.1074/jbc.M117.800466 PMC5704491 28924037 · DOI
- [42]van der Lee R Classification of intrinsically disordered regions and proteins. Chem. Rev 114, 6589– 6631 (2014). 24773235 PMC4095912
- [43]Brackley CA, Johnson J, Kelly S, Cook PR & Marenduzzo D Simulated binding of transcription factors to active and inactive regions folds human chromosomes into loops, rosettes and topological domains. Nucleic Acids Res 44, 3503– 3512 (2016). 27060145 PMC4856988
- [44]Tang Z CTCF-Mediated Human 3D Genome Architecture Reveals Chromatin Topology for Transcription. Cell 163, 1611– 1627 (2015). 26686651 PMC4734140
- [48]Nichols MH & Corces VG A CTCF Code for 3D Genome Architecture. Cell 162, 703– 705 (2015). 26276625 PMC4745123
- [54]Ganji M Real-time imaging of DNA loop extrusion by condensin. Science eaar7831 (2018). doi: 10.1126/science.aar7831 PMC6329450 29472443 · DOI · Paper page
- [55]Terakawa T The condensin complex is a mechanochemical motor that translocates along DNA. Science 358, 672– 676 (2017). 28882993 PMC5862036
- [56]Murayama Y, Samora CP, Kurokawa Y, Iwasaki H & Uhlmann F Establishment of DNA-DNA Interactions by the Cohesin Ring. Cell 172, 465– 477. e15 (2018). 29358048 PMC5786502
- [57]Nagy G Motif oriented high-resolution analysis of ChIP-seq data reveals the topological order of CTCF and cohesin proteins on DNA. BMC Genomics 17, (2016). PMC4986361 27526722
- [61]Gassler J A mechanism of cohesin-dependent loop extrusion organizes zygotic genome architecture. EMBO J 36, 3600– 3618 (2017). 29217590 PMC5730859
- [62]Fu Y, Sinha M, Peterson CL & Weng Z The Insulator Binding Protein CTCF Positions 20 Nucleosomes around Its Binding Sites across the Human Genome. PLoS Genet 4, e1000138 (2008). 18654629 PMC2453330
- [63]Mawhinney MT CTCF-Induced Circular DNA Complexes Observed by Atomic Force Microscopy. J. Mol. Biol 430, 759– 776 (2018). 29409905 PMC5860984
- [65]Kubo N Preservation of Chromatin Organization after Acute Loss of CTCF in Mouse Embryonic Stem Cells (2017). doi: 10.1101/118737 · DOI
- [66]Phanstiel DH Static and Dynamic DNA Loops form AP-1-Bound Activation Hubs during Macrophage Development. Mol. Cell 67, 1037– 1048. e6 (2017). 28890333 PMC5610110
- [68]Gibcus JH A pathway for mitotic chromosome formation. Science 359, eaao6135 (2018). PMC5924687 29348367
- [69]Hansen AS, Pustova I, Cattoglio C, Tjian R & Darzacq X CTCF and cohesin regulate chromatin loop stability with distinct dynamics. eLife 6, (2017). PMC5446243 28467304
- [70]Tran NT, Laub MT & Le TBK SMC Progressively Aligns Chromosomal Arms in Caulobacter crescentus but Is Antagonized by Convergent Transcription. Cell Rep 20, 2057– 2071 (2017). 28854358 PMC5583512
- [71]Brackley CA Nonequilibrium Chromosome Looping via Molecular Slip Links. Phys. Rev. Lett 119, (2017). 29341686
- [72]Flamholz A, Phillips R & Milo R The quantified cell. Mol. Biol. Cell 25, 3497– 3500 (2014). 25368429 PMC4230611
- [74]Ocampo-Hafalla M, Muñoz S, Samora CP & Uhlmann F Evidence for cohesin sliding along budding yeast chromosomes. Open Biol. 6, 150178 (2016). 27278645 PMC4929932
- [75]Bausch C Transcription Alters Chromosomal Locations of Cohesin in Saccharomyces cerevisiae. Mol. Cell. Biol 27, 8522– 8532 (2007). 17923700 PMC2169412
- [77]Racko D, Benedetti F, Dorier J & Stasiak A Transcription-induced supercoiling as the driving force of chromatin loop extrusion during formation of TADs in interphase chromosomes. Nucleic Acids Res (2017). doi: 10.1093/nar/gkx1123 PMC5829651 29140466 · DOI
- [78]Jonkers I & Lis JT Getting up to speed with transcription elongation by RNA polymerase II. Nat. Rev. Mol. Cell Biol 16, 167– 177 (2015). 25693130 PMC4782187
- [79]Moore JM Loss of maternal CTCF is associated with peri-implantation lethality of Ctcf null embryos. PloS One 7, e34915 (2012). 22532833 PMC3332108
- [80]Dowen JM Control of Cell Identity Genes Occurs in Insulated Neighborhoods in Mammalian Chromosomes. Cell 159, 374– 387 (2014). 25303531 PMC4197132
- [81]Wan L-B Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Dev. Camb. Engl 135, 2729– 2738 (2008). PMC2596970 18614575
- [82]Gregor A De novo mutations in the genome organizer CTCF cause intellectual disability. Am. J. Hum. Genet 93, 124– 131 (2013). 23746550 PMC3710752
- [83]Kemp CJ CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer. Cell Rep. 7, 1020– 1029 (2014). 24794443 PMC4040130
- [84]Katainen R CTCF/cohesin-binding sites are frequently mutated in cancer. Nat. Genet 47, 818– 821 (2015). 26053496
- [85]Narendra V CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347, 1017– 1021 (2015). 25722416 PMC4428148
- [88]Fukaya T, Lim B & Levine M Enhancer Control of Transcriptional Bursting. Cell 166, 358– 368 (2016). 27293191 PMC4970759
- [89]Weintraub AS YY1 Is a Structural Regulator of Enhancer-Promoter Loops. Cell 171, 1573– 1588. e28 (2017). 29224777 PMC5785279
- [91]Pan X YY1 controls Igκ repertoire and B-cell development, and localizes with condensin on the Igκ locus. EMBO J 32, 1168– 1182 (2013). 23531880 PMC3630362
- [92]Flyamer IM Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte- to-zygote transition. Nature 544, 110– 114 (2017). 28355183 PMC5639698
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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 · see citing works
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Olan, I., Parry, A. J., Schoenfelder, S., Narita, M., Ito, Y., Chan, A. S. L., Slater, G. S. C., Bihary, D., Bando, M., Shirahige, K., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19878-4 · Cited by 76 · see citing works
Chakraborty, S., Wenzlitschke, N., Anderson, M. J., Eraso, A., Baudic, M., Thompson, J. J., Evans, A. A., Shatford-Adams, L. M., Chari, R., Awasthi, P., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.02.002 · Cited by 22 · see citing works
Enhancer Function in the 3D Genome
Razin, S. V., Ulianov, S. V., & Iarovaia, O. V. (2023) · Genes · doi:10.3390/genes14061277 · Cited by 15 · see citing works
Polymer simulations guide the detection and quantification of chromatin loop extrusion by imaging
Sabaté, T., Lelandais, B., Bertrand, E., & Zimmer, C. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad034 · Cited by 13 · see citing works
Choppavarapu, L., Nosirov, B., Kahn, M., & Jin, V. X. (2026) · Cancers · doi:10.3390/cancers18213416
- Authors
- Rowley, M. J., & Corces, V. G.
- Affiliations
- Emory University (US)
- Corresponding author
- Corces, Victor G.
- Venue
- Nature Reviews Genetics
- Published
- 2018-10-26
- Volume
- 19
- Issue
- 12
- Pages
- 789-800
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- PMC
- PMC6312108
- OpenAlex
- W2898577086
- Cited by
- 1,171
- References
- 26
- Citations by year
- 2026: 135 · 2025: 158 · 2024: 137 · 2023: 141 · 2022: 158 · 2021: 176 · 2020: 151 · 2019: 111 · 2018: 3 · 2014: 1
- FWCI
- 11.52
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (K99GM127671, R00GM127671, R01GM035463)
- 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
- 3D genome organization, topologically associating domains, CTCF, cohesin, chromatin looping, enhancer-promoter interactions, chromatin structure, transcriptional regulation, chromosome conformation
- MeSH terms
- Animals, Chromatin, Enhancer Elements, Genetic, Humans, Promoter Regions, Genetic, Genome, Human, Chromatin Assembly and Disassembly
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