The role of transcription in shaping the spatial organization of the genome
Open accessAbstract
The spatial organization of the genome into compartments and topologically associated domains can have an important role in the regulation of gene expression. But could gene expression conversely regulate genome organization? Here, we review recent studies that assessed the requirement of transcription and/or the transcription machinery for the establishment or maintenance of genome topology. The results reveal different requirements at different genomic scales. Transcription is generally not required for higher-level genome compartmentalization, has only moderate effects on domain organization and is not sufficient to create new domain boundaries. However, on a finer scale, transcripts or transcription does seem to have a role in the formation of subcompartments and subdomains and in stabilizing enhancer-promoter interactions. Recent evidence suggests a dynamic, reciprocal interplay between fine-scale genome organization and transcription, in which each is able to modulate or reinforce the activity of the other.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Transcription can either disrupt or stabilise specific enhancer-promoter loops.
“Whilst it is established that transcription helps shape up higher-level genome conformation (reviewed in [386]), there is also evidence that it can either disrupt or stabilise specific enhancer–promoter loops.”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [386]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
Disruptions of Topological Chromatin Domains Cause Pathogenic Rewiring of Gene-Enhancer Interactions
Lupiáñez, D. G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J. M., Laxova, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.004 · Cited by 2,132 · 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
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
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
Insulator dysfunction and oncogene activation in IDH mutant gliomas
Flavahan, W. A., Drier, Y., Liau, B. B., Gillespie, S. M., Venteicher, A. S., Stemmer-Rachamimov, A. O., Suvà, M. L., & Bernstein, B. E. (2016) · Nature · doi:10.1038/nature16490 · Cited by 1,288 · 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
Higher-Order Inter-chromosomal Hubs Shape 3D Genome Organization in the Nucleus
Quinodoz, S. A., Ollikainen, N., Tabak, B., Palla, A., Schmidt, J. M., Detmar, E., Lai, M. M., Shishkin, A. A., Bhat, P., Takei, Y., et al. (2018) · Cell · doi:10.1016/j.cell.2018.05.024 · Cited by 892 · 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
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
Mapping Nucleosome Resolution Chromosome Folding in Yeast by Micro-C
Hsieh, T.-H. S., Weiner, A., Lajoie, B., Dekker, J., Friedman, N., & Rando, O. J. (2015) · Cell · doi:10.1016/j.cell.2015.05.048 · Cited by 788 · see citing works
Deng, W., Lee, J., Wang, H., Miller, J., Reik, A., Gregory, P. D., Dean, A., & Blobel, G. A. (2012) · Cell · doi:10.1016/j.cell.2012.03.051 · Cited by 734 · 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
Enhancer loops appear stable during development and are associated with paused polymerase
Ghavi-Helm, Y., Klein, F. A., Pakozdi, T., Ciglar, L., Noordermeer, D., Huber, W., & Furlong, E. E. M. (2014) · Nature · doi:10.1038/nature13417 · Cited by 536 · see citing works
Self-citationCohesin 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
Reactivation of developmentally silenced globin genes by forced chromatin looping
Deng, W., Rupon, J. W., Krivega, I., Breda, L., Motta, I., Jahn, K. S., Reik, A., Gregory, P. D., Rivella, S., Dean, A., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.050 · Cited by 443 · see citing works
Functional implications of genome topology
Cavalli, G., & Misteli, T. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2474 · Cited by 415 · see citing works
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 · see citing works
Rubin, A. J., Barajas, B. C., Furlan-Magaril, M., Lopez-Pajares, V., Mumbach, M. R., Howard, I., Kim, D. S., Boxer, L. D., Cairns, J., Spivakov, M., et al. (2017) · Nature Genetics · doi:10.1038/ng.3935 · Cited by 293 · see citing works
Hanssen, L. L. P., Kassouf, M. T., Oudelaar, A. M., Biggs, D., Preece, C., Downes, D. J., Gosden, M., Sharpe, J. A., Sloane-Stanley, J. A., Hughes, J. R., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3573 · Cited by 219 · see citing works
Flagged first, then by citations
Research works printed but not linked: 121
- [2]Shachar S Misteli T Causes and consequences of nuclear gene positioning J Cell Sci 2017 130 1501 1508 10.1242/jcs.199786 28404786 PMC5450234 · DOI
- [3]Dekker J Mirny L The 3D Genome as Moderator of Chromosomal Communication Cell 2016 164 1110 1121 10.1016/j.cell.2016.02.007 26967279 PMC4788811 · DOI · Paper page
- [4]Sexton T Three-dimensional folding and functional organization principles of the Drosophila genome Cell 2012 148 458 472 10.1016/j.cell.2012.01.010 22265598 · DOI · Paper page
- [6]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 2012 48 471 484 10.1016/j.molcel.2012.08.031 23041285 PMC3496039 · DOI
- [8]Brangwynne CP Mitchison TJ Hyman AA Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes Proc Natl Acad Sci U S A 2011 108 4334 4339 10.1073/pnas.1017150108 21368180 PMC3060270 · DOI
- [9]Sirri V Urcuqui-Inchima S Roussel P Hernandez-Verdun D Nucleolus: the fascinating nuclear body Histochem Cell Biol 2008 129 13 31 10.1007/s00418-007-0359-6 18046571 PMC2137947 · DOI
- [10]Nemeth A Grummt I Dynamic regulation of nucleolar architecture Curr Opin Cell Biol 2018 52 105 111 10.1016/j.ceb.2018.02.013 29529563 · DOI
- [11]Falahati H Pelham-Webb B Blythe S Wieschaus E Nucleation by rRNA Dictates the Precision of Nucleolus Assembly Curr Biol 2016 26 277 285 10.1016/j.cub.2015.11.065 26776729 PMC5866055 · DOI
- [12]Heyn P Salmonowicz H Rodenfels J Neugebauer KM Activation of transcription enforces the formation of distinct nuclear bodies in zebrafish embryos RNA Biol 2017 14 752 760 10.1080/15476286.2016.1255397 27858508 PMC5519242 · DOI
- [13]Verheggen C Almouzni G Hernandez-Verdun D The ribosomal RNA processing machinery is recruited to the nucleolar domain before RNA polymerase I during Xenopus laevis development J Cell Biol 2000 149 293 306 10769023 PMC2175160
- [14]Mais C Wright JE Prieto JL Raggett SL McStay B UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery Genes Dev 2005 19 50 64 10.1101/gad.310705 15598984 PMC540225 · DOI
- [15]Hamdane N Disruption of the UBF gene induces aberrant somatic nucleolar bodies and disrupts embryo nucleolar precursor bodies Gene 2017 612 5 11 10.1016/j.gene.2016.09.013 27614293 · DOI
- [16]Caudron-Herger M Alu element-containing RNAs maintain nucleolar structure and function EMBO J 2015 34 2758 2774 10.15252/embj.201591458 26464461 PMC4682651 · DOI
- [18]Filion GJ Systematic protein location mapping reveals five principal chromatin types in Drosophila cells Cell 2010 143 212 224 10.1016/j.cell.2010.09.009 20888037 PMC3119929 · DOI
- [19]Consortium EP An integrated encyclopedia of DNA elements in the human genome Nature 2012 489 57 74 10.1038/nature11247 22955616 PMC3439153 · DOI · Paper page
- [20]Guelen L Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions Nature 2008 453 948 951 10.1038/nature06947 18463634 · DOI
- [21]van Bemmel JG The insulator protein SU(HW) fine-tunes nuclear lamina interactions of the Drosophila genome PLoS One 2010 5 e15013 10.1371/journal.pone.0015013 21124834 PMC2991331 · DOI
- [22]Peric-Hupkes D Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation Mol Cell 2010 38 603 613 10.1016/j.molcel.2010.03.016 20513434 PMC5975946 · DOI · Paper page
- [23]Nemeth A Initial genomics of the human nucleolus PLoS Genet 2010 6 e1000889 10.1371/journal.pgen.1000889 20361057 PMC2845662 · DOI
- [24]van Koningsbruggen S High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli Mol Biol Cell 2010 21 3735 3748 10.1091/mbc.E10-06-0508 20826608 PMC2965689 · DOI
- [25]Dillinger S Straub T Nemeth A Nucleolus association of chromosomal domains is largely maintained in cellular senescence despite massive nuclear reorganisation PLoS One 2017 12 e0178821 10.1371/journal.pone.0178821 28575119 PMC5456395 · DOI
- [26]Kind J Single-cell dynamics of genome-nuclear lamina interactions Cell 2013 153 178 192 10.1016/j.cell.2013.02.028 23523135 · DOI
- [27]Ragoczy T Telling A Scalzo D Kooperberg C Groudine M Functional redundancy in the nuclear compartmentalization of the late-replicating genome Nucleus 2014 5 626 635 10.4161/19491034.2014.990863 25493640 PMC4615584 · DOI
- [28]Kalverda B Pickersgill H Shloma VV Fornerod M Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm Cell 2010 140 360 371 10.1016/j.cell.2010.01.011 20144760 · DOI
- [29]Solovei I Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution Cell 2009 137 356 368 10.1016/j.cell.2009.01.052 19379699 · DOI
- [30]Simonis M Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C) Nat Genet 2006 38 1348 1354 10.1038/ng1896 17033623 · DOI · Paper page
- [31]Lieberman-Aiden E Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 2009 326 289 293 10.1126/science.1181369 19815776 PMC2858594 · DOI · Paper page
- [32]Vieux-Rochas M Fabre PJ Leleu M Duboule D Noordermeer D Clustering of mammalian Hox genes with other H3K27me3 targets within an active nuclear domain Proc Natl Acad Sci U S A 2015 112 4672 4677 10.1073/pnas.1504783112 25825760 PMC4403207 · DOI
- [33]van Steensel B Belmont AS Lamina-Associated Domains: Links with Chromosome Architecture, Heterochromatin, and Gene Repression Cell 2017 169 780 791 10.1016/j.cell.2017.04.022 28525751 PMC5532494 · DOI · Paper page
- [34]Nuebler J Fudenberg G Imakaev M Abdennur N Mirny LA Chromatin organization by an interplay of loop extrusion and compartmental segregation Proc Natl Acad Sci U S A 2018 115 E6697 E6706 10.1073/pnas.1717730115 29967174 PMC6055145 · DOI
- [35]Kueng S Oppikofer M Gasser SM SIR proteins and the assembly of silent chromatin in budding yeast Annu Rev Genet 2013 47 275 306 10.1146/annurev-genet-021313-173730 24016189 · DOI
- [36]Tolhuis B Interactions among Polycomb domains are guided by chromosome architecture PLoS Genet 2011 7 e1001343 10.1371/journal.pgen.1001343 21455484 PMC3063757 · DOI
- [37]Bantignies F Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila Cell 2011 144 214 226 10.1016/j.cell.2010.12.026 21241892 · DOI · Paper page
- [38]Ogiyama Y Schuettengruber B Papadopoulos GL Chang JM Cavalli G Polycomb-Dependent Chromatin Looping Contributes to Gene Silencing during Drosophila Development Mol Cell 2018 71 73 88 e75 10.1016/j.molcel.2018.05.032 30008320 · DOI
- [39]Denholtz M Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization Cell Stem Cell 2013 13 602 616 10.1016/j.stem.2013.08.013 24035354 PMC3825755 · DOI · Paper page
- [40]Zhu Y Comprehensive characterization of neutrophil genome topology Genes Dev 2017 31 141 153 10.1101/gad.293910.116 28167501 PMC5322729 · DOI
- [41]Csink AK Henikoff S Genetic modification of heterochromatic association and nuclear organization in Drosophila Nature 1996 381 529 531 10.1038/381529a0 8632827 · DOI
- [42]Seum C Delattre M Spierer A Spierer P Ectopic HP1 promotes chromosome loops and variegated silencing in Drosophila EMBO J 2001 20 812 818 10.1093/emboj/20.4.812 11179225 PMC145414 · DOI
- [43]Larson AG Liquid droplet formation by HP1alpha suggests a role for phase separation in heterochromatin Nature 2017 547 236 240 10.1038/nature22822 28636604 PMC5606208 · DOI
- [44]Strom AR Phase separation drives heterochromatin domain formation Nature 2017 547 241 245 10.1038/nature22989 28636597 PMC6022742 · DOI
- [45]Cabianca DS Gasser SM Spatial segregation of heterochromatin: Uncovering functionality in a multicellular organism Nucleus 2016 7 301 307 10.1080/19491034.2016.1187354 27187571 PMC4991237 · DOI
- [46]Allshire RC Madhani HD Ten principles of heterochromatin formation and function Nat Rev Mol Cell Biol 2018 19 229 244 10.1038/nrm.2017.119 29235574 PMC6822695 · DOI
- [47]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 2016 44 3503 3512 10.1093/nar/gkw135 27060145 PMC4856988 · DOI
- [49]Hug CB Grimaldi AG Kruse K Vaquerizas JM Chromatin Architecture Emerges during Zygotic Genome Activation Independent of Transcription Cell 2017 169 216 228 e219 10.1016/j.cell.2017.03.024 28388407 · DOI · Paper page
- [50]Battulin N Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach Genome Biol 2015 16 77 10.1186/s13059-015-0642-0 25886366 PMC4434584 · DOI
- [51]Du Z Allelic reprogramming of 3D chromatin architecture during early mammalian development Nature 2017 547 232 235 10.1038/nature23263 28703188 · DOI
- [52]Jung YH Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes Cell Rep 2017 18 1366 1382 10.1016/j.celrep.2017.01.034 28178516 PMC5313040 · DOI
- [53]Carone BR High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm Dev Cell 2014 30 11 22 10.1016/j.devcel.2014.05.024 24998598 PMC4184102 · DOI
- [54]Palstra RJ Maintenance of long-range DNA interactions after inhibition of ongoing RNA polymerase II transcription PLoS One 2008 3 e1661 10.1371/journal.pone.0001661 18286208 PMC2243019 · DOI
- [55]Pinheiro I Heard E X chromosome inactivation: new players in the initiation of gene silencing F1000Res 2017 6 10.12688/f1000research.10707.1 PMC5373419 28408975 · DOI
- [56]McHugh CA The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3 Nature 2015 521 232 236 10.1038/nature14443 25915022 PMC4516396 · DOI
- [57]Probst AV A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development Dev Cell 2010 19 625 638 10.1016/j.devcel.2010.09.002 20951352 · DOI
- [58]Velazquez Camacho O Major satellite repeat RNA stabilize heterochromatin retention of Suv39h enzymes by RNA-nucleosome association and RNA:DNA hybrid formation Elife 2017 6 10.7554/eLife.25293 PMC5538826 28760199 · DOI
- [59]Martienssen R Moazed D RNAi and heterochromatin assembly Cold Spring Harb Perspect Biol 2015 7 a019323 10.1101/cshperspect.a019323 26238358 PMC4526745 · DOI
- [60]Yuan K O'Farrell PH TALE-light imaging reveals maternally guided, H3K9me2/3-independent emergence of functional heterochromatin in Drosophila embryos Genes Dev 2016 30 579 593 10.1101/gad.272237.115 26915820 PMC4782051 · DOI
- [61]Lund E Lamin A/C-promoter interactions specify chromatin state-dependent transcription outcomes Genome Res 2013 23 1580 1589 10.1101/gr.159400.113 23861385 PMC3787256 · DOI
- [62]Kohwi M Lupton JR Lai SL Miller MR Doe CQ Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila Cell 2013 152 97 108 10.1016/j.cell.2012.11.049 23332748 PMC3670710 · DOI
- [63]Tumbar T Belmont AS Interphase movements of a DNA chromosome region modulated by VP16 transcriptional activator Nat Cell Biol 2001 3 134 139 10.1038/35055033 11175745 · DOI
- [64]Chuang CH Long-range directional movement of an interphase chromosome site Curr Biol 2006 16 825 831 10.1016/j.cub.2006.03.059 16631592 · DOI
- [65]Bensaude O Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription 2011 2 103 108 10.4161/trns.2.3.16172 21922053 PMC3173647 · DOI · Paper page
- [66]Therizols P Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells Science 2014 346 1238 1242 10.1126/science.1259587 25477464 PMC6529354 · DOI
- [67]Isoda T Non-coding Transcription Instructs Chromatin Folding and Compartmentalization to Dictate Enhancer-Promoter Communication and T Cell Fate Cell 2017 171 103 119 e118 10.1016/j.cell.2017.09.001 28938112 PMC5621651 · DOI
- [68]Heinz S Transcription Elongation Can Affect Genome 3D Structure Cell 2018 174 1522 1536 e1522 10.1016/j.cell.2018.07.047 30146161 PMC6130916 · DOI · Paper page
- [69]Hu Y Plutz M Belmont AS Hsp70 gene association with nuclear speckles is Hsp70 promoter specific J Cell Biol 2010 191 711 719 10.1083/jcb.201004041 21059845 PMC2983068 · DOI
- [70]Khanna N Hu Y Belmont AS HSP70 transgene directed motion to nuclear speckles facilitates heat shock activation Curr Biol 2014 24 1138 1144 10.1016/j.cub.2014.03.053 24794297 PMC4030642 · DOI
- [71]Chen Y TSA-Seq mapping of nuclear genome organization J Cell Biol 2018 in press PMC6219710 30154186
- [72]Brickner J Genetic and epigenetic control of the spatial organization of the genome Mol Biol Cell 2017 28 364 369 10.1091/mbc.E16-03-0149 28137949 PMC5341720 · DOI
- [73]Osborne CS Myc dynamically and preferentially relocates to a transcription factory occupied by Igh PLoS Biol 2007 5 e192 10.1371/journal.pbio.0050192 17622196 PMC1945077 · DOI
- [74]Schoenfelder S Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells Nat Genet 2010 42 53 61 10.1038/ng.496 20010836 PMC3237402 · DOI
- [76]Beagrie RA Complex multi-enhancer contacts captured by genome architecture mapping Nature 2017 543 519 524 10.1038/nature21411 28273065 PMC5366070 · DOI · Paper page
- [77]de Wit E The pluripotent genome in three dimensions is shaped around pluripotency factors Nature 2013 501 227 231 10.1038/nature12420 23883933 · DOI
- [79]Wang S Spatial organization of chromatin domains and compartments in single chromosomes Science 2016 353 598 602 10.1126/science.aaf8084 27445307 PMC4991974 · DOI
- [80]Szabo Q TADs are 3D structural units of higher-order chromosome organization in Drosophila Sci Adv 2018 4 10.1126/sciadv.aar8082 eaar8082 PMC5829972 29503869 · DOI
- [83]Symmons O The Shh Topological Domain Facilitates the Action of Remote Enhancers by Reducing the Effects of Genomic Distances Dev Cell 2016 39 529 543 10.1016/j.devcel.2016.10.015 27867070 PMC5142843 · DOI · Paper page
- [84]Narendra V CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation Science 2015 347 1017 1021 10.1126/science.1262088 25722416 PMC4428148 · DOI · Paper page
- [85]Sexton T Cavalli G The role of chromosome domains in shaping the functional genome Cell 2015 160 1049 1059 10.1016/j.cell.2015.02.040 25768903 · DOI
- [86]Dekker J Guttman M Lomvardas S A Guide to Packing Your DNA Cell 2016 165 259 261 10.1016/j.cell.2016.03.039 27058655 · DOI
- [87]Dixon JR Gorkin DU Ren B Chromatin Domains: The Unit of Chromosome Organization Mol Cell 2016 62 668 680 10.1016/j.molcel.2016.05.018 27259200 PMC5371509 · DOI · Paper page
- [88]Rowley MJ Corces VG Organizational principles of 3D genome architecture Nat Rev Genet 2018 19 789 800 10.1038/s41576-018-0060-8 30367165 PMC6312108 · DOI · Paper page
- [89]van Ruiten MS Rowland BD SMC Complexes: Universal DNA Looping Machines with Distinct Regulators Trends Genet 2018 34 477 487 10.1016/j.tig.2018.03.003 29606284 · DOI
- [96]Van Bortle K Corces VG tDNA insulators and the emerging role of TFIIIC in genome organization Transcription 2012 3 277 284 10.4161/trns.21579 22889843 PMC3630181 · DOI
- [97]Van Bortle K Insulator function and topological domain border strength scale with architectural protein occupancy Genome Biol 2014 15 R82 10.1186/gb-2014-15-5-r82 24981874 PMC4226948 · DOI
- [98]Phillips-Cremins JE Architectural protein subclasses shape 3D organization of genomes during lineage commitment Cell 2013 153 1281 1295 10.1016/j.cell.2013.04.053 23706625 PMC3712340 · DOI · Paper page
- [99]Rao SS A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping Cell 2014 159 1665 1680 10.1016/j.cell.2014.11.021 25497547 PMC5635824 · DOI · Paper page
- [103]Gambetta MC Furlong EEM The Insulator Protein CTCF Is Required for Correct Hox Gene Expression, but Not for Embryonic Development in Drosophila Genetics 2018 10.1534/genetics.118.301350 PMC6116963 30021792 · DOI
- [105]Donze D Kamakaka RT RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae EMBO J 2001 20 520 531 10.1093/emboj/20.3.520 11157758 PMC133458 · DOI
- [106]Yuen KC Slaughter BD Gerton JL Condensin II is anchored by TFIIIC and H3K4me3 in the mammalian genome and supports the expression of active dense gene clusters Sci Adv 2017 3 e1700191 10.1126/sciadv.1700191 28691095 PMC5479651 · DOI
- [107]Le TB Imakaev MV Mirny LA Laub MT High-resolution mapping of the spatial organization of a bacterial chromosome Science 2013 342 731 734 10.1126/science.1242059 24158908 PMC3927313 · DOI
- [108]Marbouty M Condensin- and Replication-Mediated Bacterial Chromosome Folding and Origin Condensation Revealed by Hi-C and Super-resolution Imaging Mol Cell 2015 59 588 602 10.1016/j.molcel.2015.07.020 26295962 · DOI
- [109]Le TB Laub MT Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries EMBO J 2016 35 1582 1595 10.15252/embj.201593561 27288403 PMC4946140 · DOI
- [110]Liu C Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution Genome Res 2016 26 1057 1068 10.1101/gr.204032.116 27225844 PMC4971768 · DOI
- [111]Crane E Condensin-driven remodelling of X chromosome topology during dosage compensation Nature 2015 523 240 244 10.1038/nature14450 26030525 PMC4498965 · DOI
- [112]Ramirez F High-resolution TADs reveal DNA sequences underlying genome organization in flies Nat Commun 2018 9 189 10.1038/s41467-017-02525-w 29335486 PMC5768762 · DOI
- [113]Ulianov SV Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains Genome Res 2016 26 70 84 10.1101/gr.196006.115 26518482 PMC4691752 · DOI · Paper page
- [115]Li L Widespread rearrangement of 3D chromatin organization underlies polycombmediated stress-induced silencing Mol Cell 2015 58 216 231 10.1016/j.molcel.2015.02.023 25818644 PMC4402144 · DOI
- [116]Giorgetti L Structural organization of the inactive X chromosome in the mouse Nature 2016 535 575 579 10.1038/nature18589 27437574 PMC5443622 · DOI
- [117]Darrow EM Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture Proc Natl Acad Sci U S A 2016 113 E4504 4512 10.1073/pnas.1609643113 27432957 PMC4978254 · DOI · Paper page
- [118]Minajigi A Chromosomes. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation Science 2015 349 10.1126/science.aab2276 PMC4845908 26089354 · DOI
- [119]Ke Y 3D Chromatin Structures of Mature Gametes and Structural Reprogramming during Mammalian Embryogenesis Cell 2017 170 367 381 e320 10.1016/j.cell.2017.06.029 28709003 · DOI
- [120]Kaaij LJT van der Weide RH Ketting RF de Wit E Systemic Loss and Gain of Chromatin Architecture throughout Zebrafish Development Cell Rep 2018 24 1 10 e14 10.1016/j.celrep.2018.06.003 29972771 PMC6047509 · DOI
- [121]Rowley MJ Evolutionarily Conserved Principles Predict 3D Chromatin Organization Mol Cell 2017 67 837 852 e837 10.1016/j.molcel.2017.07.022 28826674 PMC5591081 · DOI
- [122]El-Sharnouby S Regions of very low H3K27me3 partition the Drosophila genome into topological domains PLoS One 2017 12 e0172725 10.1371/journal.pone.0172725 28282436 PMC5345799 · DOI
- [123]Long HK Prescott SL Wysocka J Ever-Changing Landscapes: Transcriptional Enhancers in Development and Evolution Cell 2016 167 1170 1187 10.1016/j.cell.2016.09.018 27863239 PMC5123704 · DOI · Paper page
- [124]Spurrell CH Dickel DE Visel A The Ties That Bind: Mapping the Dynamic Enhancer-Promoter Interactome Cell 2016 167 1163 1166 10.1016/j.cell.2016.10.054 27863237 PMC5131802 · DOI
- [125]Andrey G Mundlos S The three-dimensional genome: regulating gene expression during pluripotency and development Development 2017 144 3646 3658 10.1242/dev.148304 29042476 · DOI
- [126]Furlong EEM Levine M Developmental enhancers and chromosome topology Science 2018 361 1341 1345 10.1126/science.aau0320 30262496 PMC6986801 · DOI · Paper page
- [129]Spilianakis CG Flavell RA Long-range intrachromosomal interactions in the T helper type 2 cytokine locus Nat Immunol 2004 5 1017 1027 10.1038/ni1115 15378057 · DOI
- [130]Andrey G A switch between topological domains underlies HoxD genes collinearity in mouse limbs Science 2013 340 10.1126/science.1234167 1234167 23744951 · DOI
- [132]Chen H Dynamic interplay between enhancer-promoter topology and gene activity Nat Genet 2018 50 1296 1303 10.1038/s41588-018-0175-z 30038397 PMC6119122 · DOI · Paper page
- [133]Lefevre P Witham J Lacroix CE Cockerill PN Bonifer C The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription Mol Cell 2008 32 129 139 10.1016/j.molcel.2008.07.023 18851839 PMC2581490 · DOI
- [134]Lengronne A Cohesin relocation from sites of chromosomal loading to places of convergent transcription Nature 2004 430 573 578 10.1038/nature02742 15229615 PMC2610358 · DOI · Paper page
- [136]Chernukhin I CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide Mol Cell Biol 2007 27 1631 1648 10.1128/MCB.01993-06 17210645 PMC1820452 · DOI
- [137]Ruiz-Velasco M CTCF-Mediated Chromatin Loops between Promoter and Gene Body Regulate Alternative Splicing across Individuals Cell Syst 2017 5 628 637 e626 10.1016/j.cels.2017.10.018 29199022 · DOI
- [138]Hnisz D Shrinivas K Young RA Chakraborty AK Sharp PA A Phase Separation Model for Transcriptional Control Cell 2017 169 13 23 10.1016/j.cell.2017.02.007 28340338 PMC5432200 · DOI · Paper page
- [139]Boehning M RNA polymerase II clustering through carboxy-terminal domain phase separation Nat Struct Mol Biol 2018 10.1038/s41594-018-0112-y 30127355 · DOI
- [140]Jackson DA Hassan AB Errington RJ Cook PR Visualization of focal sites of transcription within human nuclei EMBO J 1993 12 1059 1065 8458323 PMC413307
- [141]van Steensel B Localization of the glucocorticoid receptor in discrete clusters in the cell nucleus J Cell Sci 1995 108 Pt 9 3003 3011 8537440
- [142]Cho WK Mediator and RNA polymerase II clusters associate in transcription-dependent condensates Science 2018 361 412 415 10.1126/science.aar4199 29930094 PMC6543815 · DOI · Paper page
- [143]Boija A Transcription Factors Activate Genes through the Phase-Separation Capacity of Their Activation Domains Cell 2018 175 1842 1855 e1816 10.1016/j.cell.2018.10.042 30449618 PMC6295254 · DOI · Paper page
- [144]Sabari BR Coactivator condensation at super-enhancers links phase separation and gene control Science 2018 361 10.1126/science.aar3958 PMC6092193 29930091 · DOI · Paper page
- [145]Pott S Lieb JD What are super-enhancers? Nat Genet 2015 47 8 12 10.1038/ng.3167 25547603 · DOI
Cited by
Sorted by citations
Gene regulation by long non-coding RNAs and its biological functions
Statello, L., Guo, C.-J., Chen, L.-L., & Huarte, M. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00315-9 · Cited by 4,991 · see citing works
Sequence-based modeling of three-dimensional genome architecture from kilobase to chromosome scale
Zhou, J. (2022) · Nature Genetics · doi:10.1038/s41588-022-01065-4 · Cited by 177 · see citing works
Stochastic motion and transcriptional dynamics of pairs of distal DNA loci on a compacted chromosome
Brückner, D. B., Chen, H., Barinov, L., Zoller, B., & Gregor, T. (2023) · Science · doi:10.1126/science.adf5568 · Cited by 112 · see citing works
Large-scale chromatin reorganization reactivates placenta-specific genes that drive cellular aging
Liu, Z., Ji, Q., Ren, J., Yan, P., Wu, Z., Wang, S., Sun, L., Wang, Z., Li, J., Sun, G., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.05.004 · Cited by 109 · see citing works
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 · see citing works
- Authors
- van Steensel, B., & Furlong, E. E. M.
- Affiliations
- European Molecular Biology Laboratory (DE)
- Corresponding author
- Furlong, Eileen E. M.
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2019-03-18
- Volume
- 20
- Issue
- 6
- Pages
- 327-337
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- PMC
- PMC7116054
- OpenAlex
- W2920852097
- Cited by
- 247
- References
- 23
- Citations by year
- 2026: 8 · 2025: 28 · 2024: 23 · 2023: 23 · 2022: 43 · 2021: 55 · 2020: 50 · 2019: 17
- FWCI
- 3.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- PubMed Central (acceptedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Funders
- KWF Kankerbestrijding
- Oncode Institute
- 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
- transcription, 3D genome organization, topologically associating domains, nuclear compartments, gene expression regulation, enhancer-promoter interactions, subdomains, chromatin topology, transcription machinery
- MeSH terms
- Animals, Chromatin, Enhancer Elements, Genetic, Humans, Promoter Regions, Genetic, Transcription, Genetic, Genome, Human
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