Weak interactions in higher-order chromatin organization
Open accessAbstract
The detailed principles of the hierarchical folding of eukaryotic chromosomes have been revealed during the last two decades. Along with structures composing three-dimensional (3D) genome organization (chromatin compartments, topologically associating domains, chromatin loops, etc.), the molecular mechanisms that are involved in their establishment and maintenance have been characterized. Generally, protein-protein and protein-DNA interactions underlie the spatial genome organization in eukaryotes. However, it is becoming increasingly evident that weak interactions, which exist in biological systems, also contribute to the 3D genome. Here, we provide a snapshot of our current understanding of the role of the weak interactions in the establishment and maintenance of the 3D genome organization. We discuss how weak biological forces, such as entropic forces operating in crowded solutions, electrostatic interactions of the biomolecules, liquid-liquid phase separation, DNA supercoiling, and RNA environment participate in chromosome segregation into structural and functional units and drive intranuclear functional compartmentalization.
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Current results strongly suggest that the demixing of enhancer- and promoter-associated proteins results in the assembly of a phase condensate that keeps the enhancer and promoter in spatial proximity.
“Current results strongly suggest that the demixing of enhancer- and promoter-associated proteins results in the assembly of a phase condensate that keeps the enhancer and promoter in spatial proximity [97,98,99].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [99]
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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
Macromolecular crowding: obvious but underappreciated
Ellis, R. J. (2001) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(01)01938-7 · Cited by 2,309 · 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
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
The long-range interaction landscape of gene promoters
Sanyal, A., Lajoie, B. R., Jain, G., & Dekker, J. (2012) · Nature · doi:10.1038/nature11279 · Cited by 1,489 · see citing works
Looping and Interaction between Hypersensitive Sites in the Active β-globin Locus
Tolhuis, B., Palstra, R.-J., Splinter, E., Grosveld, F., & de Laat, W. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00781-5 · Cited by 1,344 · 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
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 · cited 1× · see citing works
“Although there is clear evidence for the role of active DNA loop extrusion in mammalian TAD formation (41,42,148,156), the mechanisms underlying the formation of contact chromatin domains in other taxa remain less clear.”
BackgroundDNA loop extrusion by human cohesin
Davidson, I. F., Bauer, B., Goetz, D., Tang, W., Wutz, G., & Peters, J.-M. (2019) · Science · doi:10.1126/science.aaz3418 · Cited by 863 · cited 1× · see citing works
“However, a particularly recent discovery of cohesin’s DNA translocase activity (146,147), and the fact that the establishment of loop domains does not require transcription and replication (148), compromise this hypothesis.”
BackgroundMapping 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
Human cohesin compacts DNA by loop extrusion
Kim, Y., Shi, Z., Zhang, H., Finkelstein, I. J., & Yu, H. (2019) · Science · doi:10.1126/science.aaz4475 · Cited by 701 · 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
Mumbach, M. R., Satpathy, A. T., Boyle, E. A., Dai, C., Gowen, B. G., Cho, S. W., Nguyen, M. L., Rubin, A. J., Granja, J. M., Kazane, K. R., et al. (2017) · Nature Genetics · doi:10.1038/ng.3963 · Cited by 490 · cited 1× · see citing works
“Here, there are at least two levels of chromatin folding: chromatin loops, some of which bring promoters into the vicinity of enhancers (1), and partitioning of a chromosome into topologically associating domains (TADs) (2–4) that restrict the areas of enhancers’ action (5).”
BackgroundVisualizing DNA folding and RNA in embryos at single-cell resolution
Mateo, L. J., Murphy, S. E., Hafner, A., Cinquini, I. S., Walker, C. A., & Boettiger, A. N. (2019) · Nature · doi:10.1038/s41586-019-1035-4 · Cited by 446 · see citing works
Distinct Classes of Chromatin Loops Revealed by Deletion of an RNA-Binding Region in CTCF
Hansen, A. S., Hsieh, T.-H. S., Cattoglio, C., Pustova, I., Saldaña-Meyer, R., Reinberg, D., Darzacq, X., & Tjian, R. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.07.039 · Cited by 279 · see citing works
Cardozo Gizzi, A. M., Cattoni, D. I., Fiche, J.-B., Espinola, S. M., Gurgo, J., Messina, O., Houbron, C., Ogiyama, Y., Papadopoulos, G. L., Cavalli, G., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.01.011 · Cited by 258 · see citing works
Supercoiling in DNA and chromatin
Gilbert, N., & Allan, J. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.10.013 · Cited by 128 · see citing works
Flagged first, then by citations
Research works printed but not linked: 182
- [3]Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012; 485: 376– 380. 22495300 PMC3356448
- [4]Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell. 2012; 148: 458– 472. 22265598
- [5]Symmons O., Uslu V.V., Tsujimura T., Ruf S., Nassari S., Schwarzer W., Ettwiller L., Spitz F. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 2014; 24: 390– 400. 24398455 PMC3941104
- [6]van Steensel B., Furlong E.E.M. The role of transcription in shaping the spatial organization of the genome. Nat. Rev. Mol. Cell Biol. 2019; 20: 327– 337. 30886333 PMC7116054
- [7]Zheng H., Xie W. The role of 3D genome organization in development and cell differentiation. Nat. Rev. Mol. Cell Biol. 2019; 20: 535– 550. 31197269
- [8]Kim S., Shendure J. Mechanisms of interplay between transcription factors and the 3D genome. Mol. Cell. 2019; 76: 306– 319. 31521504
- [9]Stadhouders R., Filion G.J., Graf T. Transcription factors and 3D genome conformation in cell-fate decisions. Nature. 2019; 569: 345– 354. 31092938
- [10]Cook P.R., Marenduzzo D. Transcription-driven genome organization: a model for chromosome structure and the regulation of gene expression tested through simulations. Nucleic Acids Res. 2018; 46: 9895– 9906. 30239812 PMC6212781
- [11]Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science. 2002; 295: 1306– 1311. 11847345
- [12]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. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009; 326: 289– 293. 19815776 PMC2858594
- [13]Gavrilov A.A., Gushchanskaya E.S., Strelkova O., Zhironkina O., Kireev I.I., Iarovaia O.V., Razin S.V. Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub. Nucleic Acids Res. 2013; 41: 3563– 3575. 23396278 PMC3616722
- [14]Razin S.V., Gavrilov A.A., Ioudinkova E.S., Iarovaia O.V. Communication of genome regulatory elements in a folded chromosome. FEBS Lett. 2013; 587: 1840– 1847. 23651551
- [15]Rao S.S., 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. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014; 159: 1665– 1680. 25497547 PMC5635824
- [16]Ramani V., Cusanovich D.A., Hause R.J., Ma W., Qiu R., Deng X., Blau C.A., Disteche C.M., Noble W.S., Shendure J. et al. Mapping 3D genome architecture through in situ DNase Hi-C. Nat. Protoc. 2016; 11: 2104– 2121. 27685100 PMC5547819
- [17]Harewood L., Kishore K., Eldridge M.D., Wingett S., Pearson D., Schoenfelder S., Collins V.P., Fraser P. Hi-C as a tool for precise detection and characterisation of chromosomal rearrangements and copy number variation in human tumours. Genome Biol. 2017; 18: 125. 28655341 PMC5488307
- [18]Liu C. In situ Hi-C library preparation for plants to study their three-dimensional chromatin interactions on a genome-wide scale. Methods Mol. Biol. 2017; 1629: 155– 166. 28623585
- [19]Wang Q., Sun Q., Czajkowsky D.M., Shao Z. Sub-kb Hi-C in D. melanogaster reveals conserved characteristics of TADs between insect and mammalian cells. Nat. Commun. 2018; 9: 188. 29335463 PMC5768742
- [20]Johnston M.J., Nikolic A., Ninkovic N., Guilhamon P., Cavalli F.M.G., Seaman S., Zemp F.J., Lee J., Abdelkareem A., Ellestad K. et al. High-resolution structural genomics reveals new therapeutic vulnerabilities in glioblastoma. Genome Res. 2019; 29: 1211– 1222. 31249064 PMC6673710
- [22]Palstra R.J., Tolhuis B., Splinter E., Nijmeijer R., Grosveld F., de Laat W. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 2003; 35: 190– 194. 14517543
- [23]de Laat W., Grosveld F. Spatial organization of gene expression: the active chromatin hub. Chromosome Res. 2003; 11: 447– 459. 12971721
- [24]Mifsud B., Tavares-Cadete F., Young A.N., Sugar R., Schoenfelder S., Ferreira L., Wingett S.W., Andrews S., Grey W., Ewels P.A. et al. Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat. Genet. 2015; 47: 598– 606. 25938943
- [25]Jin F., Li Y., Dixon J.R., Selvaraj S., Ye Z., Lee A.Y., Yen C.A., Schmitt A.D., Espinoza C.A., Ren B. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature. 2013; 503: 290– 294. 24141950 PMC3838900
- [26]Markova E.N., Kantidze O.L., Razin S.V. Transcriptional regulation and spatial organisation of the human AML1/RUNX1 gene. J. Cell. Biochem. 2011; 112: 1997– 2005. 21445863
- [27]Sabari B.R., Dall’Agnese A., Boija A., Klein I.A., Coffey E.L., Shrinivas K., Abraham B.J., Hannett N.M., Zamudio A.V., Manteiga J.C. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science. 2018; 361: eaar3958. 29930091 PMC6092193
- [28]Hahn S. Phase separation, protein disorder, and enhancer function. Cell. 2018; 175: 1723– 1725. 30550782
- [29]Nair S.J., Yang L., Meluzzi D., Oh S., Yang F., Friedman M.J., Wang S., Suter T., Alshareedah I., Gamliel A. et al. Phase separation of ligand-activated enhancers licenses cooperative chromosomal enhancer assembly. Nat. Struct. Mol. Biol. 2019; 26: 193– 203. 30833784 PMC6709854
- [30]Boehning M., Dugast-Darzacq C., Rankovic M., Hansen A.S., Yu T., Marie-Nelly H., McSwiggen D.T., Kokic G., Dailey G.M., Cramer P. et al. RNA polymerase II clustering through carboxy-terminal domain phase separation. Nat. Struct. Mol. Biol. 2018; 25: 833– 840. 30127355
- [31]Nagulapalli M., Maji S., Dwivedi N., Dahiya P., Thakur J.K. Evolution of disorder in Mediator complex and its functional relevance. Nucleic Acids Res. 2016; 44: 1591– 1612. 26590257 PMC4770211
- [32]Cho W.K., Spille J.H., Hecht M., Lee C., Li C., Grube V., Cisse I.I. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science. 2018; 361: 412– 415. 29930094 PMC6543815
- [33]Cramer P. Organization and regulation of gene transcription. Nature. 2019; 573: 45– 54. 31462772
- [34]Golov A.K., Gavrilov A.A., Razin S.V. The role of crowding forces in juxtaposing beta-globin gene domain remote regulatory elements in mouse erythroid cells. PLoS One. 2015; 10: e0139855. 26436546 PMC4593578
- [35]Rowley M.J., Nichols M.H., Lyu X., Ando-Kuri M., Rivera I.S.M., Hermetz K., Wang P., Ruan Y., Corces V.G. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell. 2017; 67: 837– 852. 28826674 PMC5591081
- [36]Rowley M.J., Corces V.G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 2018; 19: 789– 800. 30367165 PMC6312108
- [37]Nuebler J., Fudenberg G., Imakaev M., Abdennur N., Mirny L.A. Chromatin organization by an interplay of loop extrusion and compartmental segregation. Proc. Natl Acad. Sci. USA. 2018; 115: E6697– E6706. 29967174 PMC6055145
- [38]Mir M., Bickmore W., Furlong E.E.M., Narlikar G. Chromatin topology, condensates and gene regulation: shifting paradigms or just a phase. Development. 2019; 146: dev182766. 31554625 PMC6803379
- [39]Finn E.H., Pegoraro G., Brandao H.B., Valton A.L., Oomen M.E., Dekker J., Mirny L., Misteli T. Extensive heterogeneity and intrinsic variation in spatial genome organization. Cell. 2019; 176: 1502– 1515. 30799036 PMC6408223
- [40]Flyamer I.M., Gassler J., Imakaev M., Brandao H.B., Ulianov S.V., Abdennur N., Razin S.V., Mirny L.A., Tachibana-Konwalski K. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature. 2017; 544: 110– 114. 28355183 PMC5639698
- [44]Ulianov S.V., Khrameeva E.E., Gavrilov A.A., Flyamer I.M., Kos P., Mikhaleva E.A., Penin A.A., Logacheva M.D., Imakaev M.V., Chertovich A. et al. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 2016; 26: 70– 84. 26518482 PMC4691752
- [45]Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997; 389: 251– 260. 9305837
- [46]Schalch T., Duda S., Sargent D.F., Richmond T.J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature. 2005; 436: 138– 141. 16001076
- [47]Chodaparambil J.V., Barbera A.J., Lu X., Kaye K.M., Hansen J.C., Luger K. A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat. Struct. Mol. Biol. 2007; 14: 1105– 1107. 17965723 PMC2366819
- [48]Chen Q., Yang R., Korolev N., Liu C.F., Nordenskiold L. Regulation of nucleosome stacking and chromatin compaction by the histone H4 N-terminal tail-H2A acidic patch interaction. J. Mol. Biol. 2017; 429: 2075– 2092. 28322915
- [49]Zhou J., Fan J.Y., Rangasamy D., Tremethick D.J. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat. Struct. Mol. Biol. 2007; 14: 1070– 1076. 17965724
- [50]Kalashnikova A.A., Porter-Goff M.E., Muthurajan U.M., Luger K., Hansen J.C. The role of the nucleosome acidic patch in modulating higher order chromatin structure. J. R. Soc. Interface. 2013; 10: 20121022. 23446052 PMC3627075
- [51]Sinha D., Shogren-Knaak M.A. Role of direct interactions between the histone H4 Tail and the H2A core in long range nucleosome contacts. J. Biol. Chem. 2010; 285: 16572– 16581. 20351095 PMC2878085
- [52]Pepenella S., Murphy K.J., Hayes J.J. Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure. Chromosoma. 2014; 123: 3– 13. 23996014 PMC3938996
- [53]Allahverdi A., Yang R., Korolev N., Fan Y., Davey C.A., Liu C.F., Nordenskiold L. The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res. 2011; 39: 1680– 1691. 21047799 PMC3061077
- [54]Hebbes T.R., Clayton A.L., Thorne A.W., Crane-Robinson C. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 1994; 13: 1823– 1830. 8168481 PMC395022
- [55]Krajewski W.A., Becker P.B. Reconstitution of hyperacetylated, DNase I-sensitive chromatin characterized by high conformational flexibility of nucleosomal DNA. Proc. Natl Acad. Sci. U.S.A. 1998; 95: 1540– 1545. 9465051 PMC19080
- [56]Ou H.D., Phan S., Deerinck T.J., Thor A., Ellisman M.H., O'Shea C.C. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science. 2017; 357: eaag0025. 28751582 PMC5646685
- [57]Maeshima K., Imai R., Tamura S., Nozaki T. Chromatin as dynamic 10-nm fibers. Chromosoma. 2014; 123: 225– 237. 24737122 PMC4031381
- [58]Maeshima K., Imai R., Hikima T., Joti Y. Chromatin structure revealed by X-ray scattering analysis and computational modeling. Methods. 2014; 70: 154– 161. 25168089
- [59]Razin S.V., Gavrilov A.A. Chromatin without the 30-nm fiber: constrained disorder instead of hierarchical folding. Epigenetics. 2014; 9: 653– 657. 24561903 PMC4063823
- [60]Ricci M.A., Manzo C., Garcia-Parajo M.F., Lakadamyali M., Cosma M.P. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell. 2015; 160: 1145– 1158. 25768910
- [61]Maeshima K., Rogge R., Tamura S., Joti Y., Hikima T., Szerlong H., Krause C., Herman J., Seidel E., DeLuca J. et al. Nucleosomal arrays self-assemble into supramolecular globular structures lacking 30-nm fibers. EMBO J. 2016; 35: 1115– 1132. 27072995 PMC4868957
- [62]Hansen J.C., Connolly M., McDonald C.J., Pan A., Pryamkova A., Ray K., Seidel E., Tamura S., Rogge R., Maeshima K. The 10-nm chromatin fiber and its relationship to interphase chromosome organization. Biochem. Soc. Trans. 2018; 46: 67– 76. 29263138 PMC5818668
- [63]Meng F., Na I., Kurgan L., Uversky V.N. Compartmentalization and functionality of nuclear disorder: intrinsic disorder and protein-protein interactions in intra-nuclear compartments. Int. J. Mol. Sci. 2015; 17: 24. PMC4730271 26712748
- [64]Darling A.L., Liu Y., Oldfield C.J., Uversky V.N. Intrinsically disordered proteome of human membrane-less organelles. Proteomics. 2018; 18: e1700193. 29068531
- [65]Uversky V.N. Intrinsically disordered proteins in overcrowded milieu: membrane-less organelles, phase separation, and intrinsic disorder. Curr. Opin. Struct. Biol. 2017; 44: 18– 30. 27838525
- [66]Turner A.L., Watson M., Wilkins O.G., Cato L., Travers A., Thomas J.O., Stott K. Highly disordered histone H1-DNA model complexes and their condensates. Proc. Natl Acad. Sci. USA. 2018; 115: 11964– 11969. 30301810 PMC6255207
- [67]Larson A.G., Elnatan D., Keenen M.M., Trnka M.J., Johnston J.B., Burlingame A.L., Agard D.A., Redding S., Narlikar G.J. Liquid droplet formation by HP1alpha suggests a role for phase separation in heterochromatin. Nature. 2017; 547: 236– 240. 28636604 PMC5606208
- [68]Tatavosian R., Kent S., Brown K., Yao T., Duc H.N., Huynh T.N., Zhen C.Y., Ma B., Wang H., Ren X. Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation. J. Biol. Chem. 2019; 294: 1451– 1463. 30514760 PMC6364756
- [69]Uversky V.N. Protein intrinsic disorder-based liquid-liquid phase transitions in biological systems: complex coacervates and membrane-less organelles. Adv. Colloid Interface Sci. 2017; 239: 97– 114. 27291647
- [70]Shakya A., Park S., Rana N., King J.T. Liquid-liquid phase separation of histone proteins in cells: role in chromatin organization. Biophys. J. 2019; 118: 753– 764. 31952807 PMC7002979
- [71]Gibson B.A., Doolittle L.K., Schneider M.W.G., Jensen L.E., Gamarra N., Henry L., Gerlich D.W., Redding S., Rosen M.K. Organization of chromatin by intrinsic and regulated phase separation. Cell. 2019; 179: 470– 484. 31543265 PMC6778041
- [72]Yaniv M., Cereghini S. Structure of transcriptionally active chromatin. Crit. Rev. Biochem. 1986; 21: 1– 26. 3015490
- [73]Hihara S., Pack C.G., Kaizu K., Tani T., Hanafusa T., Nozaki T., Takemoto S., Yoshimi T., Yokota H., Imamoto N. et al. Local nucleosome dynamics facilitate chromatin accessibility in living mammalian cells. Cell Rep. 2012; 2: 1645– 1656. 23246002
- [74]Marsano R.M., Giordano E., Messina G., Dimitri P. A new portrait of constitutive heterochromatin: lessons from drosophila melanogaster. Trends Genet. 2019; 35: 615– 631. 31320181
- [75]Eberl D.F., Duyf B.J., Hilliker A.J. The role of heterochromatin in the expression of a heterochromatic gene, the rolled locus of Drosophila melanogaster. Genetics. 1993; 134: 277– 292. 8514136 PMC1205430
- [76]Strom A.R., Emelyanov A.V., Mir M., Fyodorov D.V., Darzacq X., Karpen G.H. Phase separation drives heterochromatin domain formation. Nature. 2017; 547: 241– 245. 28636597 PMC6022742
- [77]Erdel F., Rademacher A., Vlijm R., Tunnermann J., Frank L., Weinmann R., Schweigert E., Yserentant K., Hummert J., Bauer C. et al. Mouse heterochromatin adopts digital compaction states without showing hallmarks of HP1-driven liquid-liquid phase separation. Mol. Cell. 2020; 78: 236– 249. 32101700 PMC7163299
- [78]Peng A., Weber S.C. Evidence for and against liquid-liquid phase separation in the Nucleus. Non-coding RNA. 2019; 5: e50. 31683819 PMC6958436
- [79]McSwiggen D.T., Mir M., Darzacq X., Tjian R. Evaluating phase separation in live cells: diagnosis, caveats, and functional consequences. Genes Dev. 2019; 33: 1619– 1634. 31594803 PMC6942051
- [80]McSwiggen D.T., Hansen A.S., Teves S.S., Marie-Nelly H., Hao Y., Heckert A.B., Umemoto K.K., Dugast-Darzacq C., Tjian R., Darzacq X. Evidence for DNA-mediated nuclear compartmentalization distinct from phase separation. eLife. 2019; 8: e47098. 31038454 PMC6522219
- [81]Erdel F., Rippe K. Formation of chromatin subcompartments by phase separation. Biophys. J. 2018; 114: 2262– 2270. 29628210 PMC6129460
- [82]Boija A., Klein I.A., Sabari B.R., Dall’Agnese A., Coffey E.L., Zamudio A.V., Li C.H., Shrinivas K., Manteiga J.C., Hannett N.M. et al. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell. 2018; 175: 1842– 1855. 30449618 PMC6295254
- [83]Tarczewska A., Greb-Markiewicz B. The significance of the intrinsically disordered regions for the functions of the bhlh transcription factors. Int. J. Mol. Sci. 2019; 20: 5306. PMC6862971 31653121
- [84]Shrinivas K., Sabari B.R., Coffey E.L., Klein I.A., Boija A., Zamudio A.V., Schuijers J., Hannett N.M., Sharp P.A., Young R.A. et al. Enhancer features that drive formation of transcriptional condensates. Mol. Cell. 2019; 75: 549– 561. 31398323 PMC6690378
- [85]Hnisz D., Shrinivas K., Young R.A., Chakraborty A.K., Sharp P.A. A phase separation model for transcriptional control. Cell. 2017; 169: 13– 23. 28340338 PMC5432200
- [87]Zhang Y., Wong C.H., Birnbaum R.Y., Li G., Favaro R., Ngan C.Y., Lim J., Tai E., Poh H.M., Wong E. et al. Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature. 2013; 504: 306– 310. 24213634 PMC3954713
- [88]Petrenko N., Jin Y., Wong K.H., Struhl K. Mediator undergoes a compositional change during transcriptional activation. Mol. Cell. 2016; 64: 443– 454. 27773675 PMC5096951
- [89]Liu G., Dean A. Enhancer long-range contacts: The multi-adaptor protein LDB1 is the tie that binds. BBA – Gene Reg. Mech. 2019; 1862: 625– 633. 31022553
- [90]Weintraub A.S., Li C.H., Zamudio A.V., Sigova A.A., Hannett N.M., Day D.S., Abraham B.J., Cohen M.A., Nabet B., Buckley D.L. et al. YY1 is a structural regulator of enhancer-promoter loops. Cell. 2017; 171: 1573– 1588. 29224777 PMC5785279
- [91]Carter D.R., Eskiw C., Cook P.R. Transcription factories. Biochem. Soc. Trans. 2008; 36: 585– 589. 18631121
- [92]Sutherland H., Bickmore W.A. Transcription factories: gene expression in unions. Nat. Rev. Genet. 2009; 10: 457– 466. 19506577
- [93]Razin S.V., Gavrilov A.A., Pichugin A., Lipinski M., Iarovaia O.V., Vassetzky Y.S. Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res. 2011; 39: 9085– 9092. 21880598 PMC3241665
- [94]Canals-Hamann A.Z., das Neves R.P., Reittie J.E., Iniguez C., Soneji S., Enver T., Buckle V.J., Iborra F.J. A biophysical model for transcription factories. BMC Biophysics. 2013; 6: 2. 23394119 PMC3740778
- [95]Chong S., Dugast-Darzacq C., Liu Z., Dong P., Dailey G.M., Cattoglio C., Heckert A., Banala S., Lavis L., Darzacq X. et al. Imaging dynamic and selective low-complexity domain interactions that control gene transcription. Science. 2018; 361: eaar2555. 29930090 PMC6961784
- [96]Zhou G.L., Xin L., Song W., Di L.J., Liu G., Wu X.S., Liu D.P., Liang C.C. Active chromatin hub of the mouse alpha-globin locus forms in a transcription factory of clustered housekeeping genes. Mol. Cell. Biol. 2006; 26: 5096– 5105. 16782894 PMC1489176
- [97]Osborne C.S., Chakalova L., Mitchell J.A., Horton A., Wood A.L., Bolland D.J., Corcoran A.E., Fraser P. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol. 2007; 5: e192. 17622196 PMC1945077
- [98]Osborne C.S., Chakalova L., Brown K.E., Carter D., Horton A., Debrand E., Goyenechea B., Mitchell J.A., Lopes S., Reik W. et al. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 2004; 36: 1065– 1071. 15361872
- [99]Wang Q., Sawyer I.A., Sung M.H., Sturgill D., Shevtsov S.P., Pegoraro G., Hakim O., Baek S., Hager G.L., Dundr M. Cajal bodies are linked to genome conformation. Nat. Commun. 2016; 7: 10966. 26997247 PMC4802181
- [100]Kim J., Venkata N.C., Hernandez Gonzalez G.A., Khanna N., Belmont A.S. Gene expression amplification by nuclear speckle association. J. Cell Biol. 2019; 219: e201904046. PMC7039209 31757787
- [101]Chen Y., Belmont A.S. Genome organization around nuclear speckles. Curr. Opin. Genet. Dev. 2019; 55: 91– 99. 31394307 PMC6759399
- [102]Brown J.M., Green J., das Neves R.P., Wallace H.A., Smith A.J., Hughes J., Gray N., Taylor S., Wood W.G., Higgs D.R. et al. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J. Cell Biol. 2008; 182: 1083– 1097. 18809724 PMC2542471
- [103]Chen Y., Zhang Y., Wang Y., Zhang L., Brinkman E.K., Adam S.A., Goldman R., van Steensel B., Ma J., Belmont A.S. Mapping 3D genome organization relative to nuclear compartments using TSA-Seq as a cytological ruler. J. Cell Biol. 2018; 217: 4025– 4048. 30154186 PMC6219710
- [104]Sawyer I.A., Bartek J., Dundr M. Phase separated microenvironments inside the cell nucleus are linked to disease and regulate epigenetic state, transcription and RNA processing. Semin. Cell Dev. Biol. 2019; 90: 94– 103. 30017905
- [105]Strom A.R., Brangwynne C.P. The liquid nucleome - phase transitions in the nucleus at a glance. J. Cell Sci. 2019; 132: jcs235093. 31754043 PMC6899023
- [107]Hu S., Lv P., Yan Z., Wen B. Disruption of nuclear speckles reduces chromatin interactions in active compartments. Epigenet. Chromatin. 2019; 12: 43. PMC6636040 31315647
- [108]Cho E.J., Kim J.S. Crowding effects on the formation and maintenance of nuclear bodies: insights from molecular-dynamics simulations of simple spherical model particles. Biophys. J. 2012; 103: 424– 433. 22947858 PMC3414890
- [110]Hancock R. Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol. Cell. 2004; 96: 595– 601. 15519694
- [111]Marenduzzo D., Micheletti C., Cook P.R. Entropy-driven genome organization. Biophys. J. 2006; 90: 3712– 3721. 16500976 PMC1440752
- [112]Richter K., Nessling M., Lichter P. Macromolecular crowding and its potential impact on nuclear function. Biochim. Biophys. Acta. 2008; 1783: 2100– 2107. 18723053
- [113]Weiss M. Crowding, diffusion, and biochemical reactions. Int. Rev. Cell Mol. Biol. 2014; 307: 383– 417. 24380600
- [114]Hancock R. Self-association of polynucleosome chains by macromolecular crowding. European Biophys. J. 2008; 37: 1059– 1064. 18259740
- [115]Zinchenko A., Berezhnoy N.V., Chen Q., Nordenskiold L. Compaction of single-molecule megabase-long chromatin under the influence of macromolecular crowding. Biophys. J. 2018; 114: 2326– 2335. 29729833 PMC6129467
- [116]Walter A., Chapuis C., Huet S., Ellenberg J. Crowded chromatin is not sufficient for heterochromatin formation and not required for its maintenance. J. Struct. Biol. 2013; 184: 445– 453. 24145303
- [117]Hancock R. A role for macromolecular crowding effects in the assembly and function of compartments in the nucleus. J. Struct. Biol. 2004; 146: 281– 290. 15099570
- [118]Hancock R., Hadj-Sahraoui Y. Isolation of cell nuclei using inert macromolecules to mimic the crowded cytoplasm. PLoS One. 2009; 4: e7560. 19851505 PMC2762040
- [119]Liu L.F., Wang J.C. Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. U.S.A. 1987; 84: 7024– 7027. 2823250 PMC299221
- [120]Ma J., Wang M.D. DNA supercoiling during transcription. Biophysical Rev. 2016; 8: 75– 87. PMC5338639 28275417
- [121]Chen S.H., Chan N.L., Hsieh T.S. New mechanistic and functional insights into DNA topoisomerases. Annu. Rev. Biochem. 2013; 82: 139– 170. 23495937
- [122]Fernandez X., Diaz-Ingelmo O., Martinez-Garcia B., Roca J. Chromatin regulates DNA torsional energy via topoisomerase II-mediated relaxation of positive supercoils. EMBO J. 2014; 33: 1492– 1501. 24859967 PMC4194091
- [123]Leng F., Amado L., McMacken R. Coupling DNA supercoiling to transcription in defined protein systems. J. Biol. Chem. 2004; 279: 47564– 47571. 15342629
- [124]Herbert A., Rich A. The biology of left-handed Z-DNA. J. Biol. Chem. 1996; 271: 11595– 11598. 8662853
- [125]Oussatcheva E.A., Pavlicek J., Sankey O.F., Sinden R.R., Lyubchenko Y.L., Potaman V.N. Influence of global DNA topology on cruciform formation in supercoiled DNA. J. Mol. Biol. 2004; 338: 735– 743. 15099741
- [126]Corless S., Gilbert N. Effects of DNA supercoiling on chromatin architecture. Biophys. Rev. 2016; 8: 245– 258. 27738453 PMC5039215
- [127]Sperry A.O., Blasquez V.C., Garrard W.T. Dysfunction of chromosomal loop attachment sites: illigetimate recombination linked to matrix association regions and topoisomerase II. Proc. Natl Acad. Sci. U.S.A. 1989; 86: 5497– 5501. 2546156 PMC297650
- [128]Razin S.V., Petrov P., Hancock R. Precise localization of the α-globin gene cluster within one of the 20- to 300-Kilobase DNA fragment released by cleavage of chicken chromosomal DNA at topoisomerase II site in vivo: evidence that the fragment are DNA loops or domains. Proc. Natl. Acad. Sci. U.S.A. 1991; 88: 8515– 8519. 1656447 PMC52539
- [129]Iarovaia O.V., Hancock R., Lagarkova M.A., Miassod R., Razin S.V. Mapping of genomic DNA loop organization in a 500-kilobase region of the Drosophila X chromosome using the topoisomerase II-mediated DNA loop excision protocol. Mol. Cell. Biol. 1996; 16: 302– 308. 8524309 PMC231004
- [130]Kmiec E.B., Razvi F., Worcel A. The role of DNA-mediated transfer of TFIIIA in the concerted gyration and differential activation of the Xenopus 5S RNA genes. Cell. 1986; 45: 209– 218. 3698098
- [131]Petryniak B., Lutter L.C. Topological characterization of the simian virus 40 transcription complex. Cell. 1987; 48: 289– 295. 3026641
- [132]Gruzdev A.D., Lezzi M. Torsional state of DNA in a transcriptionally hyperactive Balbiani ring of polytene chromosomes. Chromosome Res. 1998; 6: 367– 378. 9872666
- [133]Norton V.G., Imai B.S., Yau P., Bradbury E.M. Histone acetylation reduces nucleosome core particle linking number change. Cell. 1989; 57: 449– 457. 2541913
- [134]Choder M., Aloni Y. In vitro transcribed SV40 minichromosomes, as the bulk minichromosomes, have a low level of unconstrained negative supercoils. Nucleic Acids Res. 1988; 16: 895– 905. 2830595 PMC334726
- [135]Havas K., Flaus A., Phelan M., Kingston R., Wade P.A., Lilley D.M., Owen-Hughes T. Generation of superhelical torsion by ATP-dependent chromatin remodeling activities. Cell. 2000; 103: 1133– 1142. 11163188
- [136]Bermudez I., Garcia-Martinez J., Perez-Ortin J.E., Roca J. A method for genome-wide analysis of DNA helical tension by means of psoralen-DNA photobinding. Nucleic Acids Res. 2010; 38: e182. 20685815 PMC2965259
- [137]Corless S., Naughton C., Gilbert N. Profiling DNA supercoiling domains in vivo. Genomics data. 2014; 2: 264– 267. 26484106 PMC4536041
- [138]Kouzine F., Gupta A., Baranello L., Wojtowicz D., Ben-Aissa K., Liu J., Przytycka T.M., Levens D. Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat. Struct. Mol. Biol. 2013; 20: 396– 403. 23416947 PMC3594045
- [139]Teves S.S., Henikoff S. Transcription-generated torsional stress destabilizes nucleosomes. Nat. Struct. Mol. Biol. 2014; 21: 88– 94. 24317489 PMC3947361
- [140]Naughton C., Avlonitis N., Corless S., Prendergast J.G., Mati I.K., Eijk P.P., Cockroft S.L., Bradley M., Ylstra B., Gilbert N. Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat. Struct. Mol. Biol. 2013; 20: 387– 395. 23416946 PMC3689368
- [141]Gittens W.H., Johnson D.J., Allison R.M., Cooper T.J., Thomas H., Neale M.J. A nucleotide resolution map of Top2-linked DNA breaks in the yeast and human genome. Nat. Commun. 2019; 10: 4846. 31649282 PMC6813358
- [143]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. 2018; 46: 1648– 1660. 29140466 PMC5829651
- [144]Racko D., Benedetti F., Dorier J., Stasiak A. Are TADs supercoiled. Nucleic Acids Res. 2019; 47: 521– 532. 30395328 PMC6344874
- [145]Uuskula-Reimand L., Hou H., Samavarchi-Tehrani P., Rudan M.V., Liang M., Medina-Rivera A., Mohammed H., Schmidt D., Schwalie P., Young E.J. et al. Topoisomerase II beta interacts with cohesin and CTCF at topological domain borders. Genome Biol. 2016; 17: 182. 27582050 PMC5006368
- [149]Marcon L., Boissonneault G. Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol. Reprod. 2004; 70: 910– 918. 14645105
- [150]Sakkas D., Manicardi G., Bianchi P.G., Bizzaro D., Bianchi U. Relationship between the presence of endogenous nicks and sperm chromatin packaging in maturing and fertilizing mouse spermatozoa. Biol. Reprod. 1995; 52: 1149– 1155. 7626715
- [151]Smith A., Haaf T. DNA nicks and increased sensitivity of DNA to fluorescence in situ end labeling during functional spermiogenesis. BioTechniques. 1998; 25: 496– 502. 9762447
- [152]Battulin N., Fishman V.S., Mazur A.M., Pomaznoy M., Khabarova A.A., Afonnikov D.A., Prokhortchouk E.B., Serov O.L. Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol. 2015; 16: 77. 25886366 PMC4434584
- [153]Jung Y.H., Sauria M.E.G., Lyu X., Cheema M.S., Ausio J., Taylor J., Corces V.G. Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes. Cell Rep. 2017; 18: 1366– 1382. 28178516 PMC5313040
- [154]Benedetti F., Dorier J., Burnier Y., Stasiak A. Models that include supercoiling of topological domains reproduce several known features of interphase chromosomes. Nucleic Acids Res. 2014; 42: 2848– 2855. 24366878 PMC3950722
- [155]Benedetti F., Dorier J., Stasiak A. Effects of supercoiling on enhancer-promoter contacts. Nucleic Acids Res. 2014; 42: 10425– 10432. 25123662 PMC4176356
- [157]Benedetti F., Racko D., Dorier J., Burnier Y., Stasiak A. Transcription-induced supercoiling explains formation of self-interacting chromatin domains in S. pombe. Nucleic Acids Res. 2017; 45: 9850– 9859. 28973473 PMC5622301
- [158]Consortium E.P., Birney E., Stamatoyannopoulos J.A., Dutta A., Guigo R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007; 447: 799– 816. 17571346 PMC2212820
- [159]Hangauer M.J., Carpenter S., McManus M.T. Discovering the complexity of the metazoan transcriptome. Genome Biol. 2014; 15: 112. 25001157 PMC4054782
- [160]Nozawa R.S., Gilbert N. RNA: nuclear glue for folding the genome. Trends Cell Biol. 2019; 29: 201– 211. 30630665
- [161]Scherrer K. Primary transcripts: from the discovery of RNA processing to current concepts of gene expression - Review. Exp. Cell Res. 2018; 373: 1– 33. 30266658
- [162]Michieletto D., Gilbert N. Role of nuclear RNA in regulating chromatin structure and transcription. Curr. Opin. Cell Biol. 2019; 58: 120– 125. 31009871 PMC6694202
- [163]Colognori D., Sunwoo H., Kriz A.J., Wang C.Y., Lee J.T. Xist deletional analysis reveals an interdependency between Xist RNA and polycomb complexes for spreading along the inactive X. Mol. Cell. 2019; 74: 101– 117. 30827740 PMC6469964
- [164]Engreitz J.M., Pandya-Jones A., McDonel P., Shishkin A., Sirokman K., Surka C., Kadri S., Xing J., Goren A., Lander E.S. et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science. 2013; 341: 1237973. 23828888 PMC3778663
- [165]Giorgetti L., Lajoie B.R., Carter A.C., Attia M., Zhan Y., Xu J., Chen C.J., Kaplan N., Chang H.Y., Heard E. et al. Structural organization of the inactive X chromosome in the mouse. Nature. 2016; 535: 575– 579. 27437574 PMC5443622
- [166]Hacisuleyman E., Goff L.A., Trapnell C., Williams A., Henao-Mejia J., Sun L., McClanahan P., Hendrickson D.G., Sauvageau M., Kelley D.R. et al. Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat. Struct. Mol. Biol. 2014; 21: 198– 206. 24463464 PMC3950333
- [167]Donley N., Stoffregen E.P., Smith L., Montagna C., Thayer M.J. Asynchronous replication, mono-allelic expression, and long range cis-effects of ASAR6. PLoS Genet. 2013; 9: e1003423. 23593023 PMC3617217
- [168]Donley N., Smith L., Thayer M.J. ASAR15, a cis-acting locus that controls chromosome-wide replication timing and stability of human chromosome 15. PLos Genet. 2015; 11: e1004923. 25569254 PMC4287527
- [169]Chujo T., Yamazaki T., Hirose T. Architectural RNAs (arcRNAs): a class of long noncoding RNAs that function as the scaffold of nuclear bodies. Biochim. Biophys. Acta. 2016; 1859: 139– 146. 26021608
- [170]Bell J.C., Jukam D., Teran N.A., Risca V.I., Smith O.K., Johnson W.L., Skotheim J.M., Greenleaf W.J., Straight A.F. Chromatin-associated RNA sequencing (ChAR-seq) maps genome-wide RNA-to-DNA contacts. eLife. 2018; 7: e27024. 29648534 PMC5962340
- [171]Li X., Zhou B., Chen L., Gou L.T., Li H., Fu X.D. GRID-seq reveals the global RNA-chromatin interactome. Nat. Biotechnol. 2017; 35: 940– 950. 28922346 PMC5953555
- [172]Sridhar B., Rivas-Astroza M., Nguyen T.C., Chen W., Yan Z., Cao X., Hebert L., Zhong S. Systematic mapping of RNA-chromatin interactions in vivo. Curr. Biol. 2017; 27: 602– 609. 28132817 PMC5319903
- [173]Bonetti A., Agostini F., Suzuki A.M., Hashimoto K., Pascarella G., Gimenez J., Roos L., Nash A.J., Ghilotti M., Cameron C.J.F. et al. RADICL-seq identifies general and cell type–specific principles of genome-wide RNA-chromatin interactions. Nat. Commun. 2020; 11: 1018. 32094342 PMC7039879
- [174]Amaral P.P., Leonardi T., Han N., Vire E., Gascoigne D.K., Arias-Carrasco R., Buscher M., Pandolfini L., Zhang A., Pluchino S. et al. Genomic positional conservation identifies topological anchor point RNAs linked to developmental loci. Genome Biol. 2018; 19: 32. 29540241 PMC5853149
- [175]Tan J.Y., Smith A.A.T., Ferreira da Silva M., Matthey-Doret C., Rueedi R., Sonmez R., Ding D., Kutalik Z., Bergmann S., Marques A.C. cis-Acting complex-trait-associated lincRNA expression correlates with modulation of chromosomal architecture. Cell Rep. 2017; 18: 2280– 2288. 28249171
- [177]Saldaña-Meyer R., Rodriguez-Hernaez J., Nishana M., Jácome-López K., Nora E.P., Bruneau B.G., Furlan-Magaril M., Skok J., Reinberg D. RNA interactions are essential for CTCF-mediated genome organization. Mol. Cell. 2019; 76: 412– 422. 31522988 PMC7195841
- [178]Fan H., Lv P., Huo X., Wu J., Wang Q., Cheng L., Liu Y., Tang Q.Q., Zhang L., Zhang F. et al. The nuclear matrix protein HNRNPU maintains 3D genome architecture globally in mouse hepatocytes. Genome Res. 2018; 28: 192– 202. 29273625 PMC5793783
- [179]Nozawa R.S., Boteva L., Soares D.C., Naughton C., Dun A.R., Buckle A., Ramsahoye B., Bruton P.C., Saleeb R.S., Arnedo M. et al. SAF-A regulates interphase chromosome structure through oligomerization with chromatin-associated RNAs. Cell. 2017; 169: 1214– 1227. 28622508 PMC5473940
- [180]Huo X., Ji L., Zhang Y., Lv P., Cao X., Wang Q., Yan Z., Dong S., Du D., Zhang F. et al. The nuclear matrix protein SAFB cooperates with major satellite RNAs to stabilize heterochromatin architecture partially through phase separation. Mol. Cell. 2020; 77: 368– 383. 31677973
- [181]Watson M., Stott K. Disordered domains in chromatin-binding proteins. Essays Biochem. 2019; 63: 147– 156. 30940742
- [182]Kim Y.J., Xie P., Cao L., Zhang M.Q., Kim T.H. Global transcriptional activity dynamics reveal functional enhancer RNAs. Genome Res. 2018; 28: 1799– 1811. 30352805 PMC6280751
- [183]Lai F., Gardini A., Zhang A., Shiekhattar R. Integrator mediates the biogenesis of enhancer RNAs. Nature. 2015; 525: 399– 403. 26308897 PMC4718573
- [184]Pefanis E., Wang J., Rothschild G., Lim J., Kazadi D., Sun J., Federation A., Chao J., Elliott O., Liu Z.P. et al. RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity. Cell. 2015; 161: 774– 789. 25957685 PMC4428671
- [185]Hsieh C.L., Fei T., Chen Y., Li T., Gao Y., Wang X., Sun T., Sweeney C.J., Lee G.S., Chen S. et al. Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation. Proc. Natl Acad. Sci. U.S.A. 2014; 111: 7319– 7324. 24778216 PMC4034202
- [186]Lai F., Orom U.A., Cesaroni M., Beringer M., Taatjes D.J., Blobel G.A., Shiekhattar R. Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature. 2013; 494: 497– 501. 23417068 PMC4109059
- [187]Dueva R., Akopyan K., Pederiva C., Trevisan D., Dhanjal S., Lindqvist A., Farnebo M. Neutralization of the positive charges on histone tails by RNA promotes an open chromatin structure. Cell Chem. Biol. 2019; 26: 1436– 1449. 31447351
- [188]Wang C., Liu C., Roqueiro D., Grimm D., Schwab R., Becker C., Lanz C., Weigel D. Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 2015; 25: 246– 256. 25367294 PMC4315298
- [190]Eser U., Chandler-Brown D., Ay F., Straight A.F., Duan Z., Noble W.S., Skotheim J.M. Form and function of topologically associating genomic domains in budding yeast. Proc. Natl Acad. Sci. U.S.A. 2017; 114: E3061– E3070. 28348222 PMC5393236
- [191]Nikolaou C. Invisible cities: segregated domains in the yeast genome with distinct structural and functional attributes. Curr. Genet. 2017; 64: 247– 258. 28780612
- [192]Szabo Q., Jost D., Chang J.M., Cattoni D.I., Papadopoulos G.L., Bonev B., Sexton T., Gurgo J., Jacquier C., Nollmann M. et al. TADs are 3D structural units of higher-order chromosome organization in Drosophila. Sci. Adv. 2018; 4: eaar8082. 29503869 PMC5829972
- [193]Bintu B., Mateo L.J., Su J.H., Sinnott-Armstrong N.A., Parker M., Kinrot S., Yamaya K., Boettiger A.N., Zhuang X. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science. 2018; 362: eaau1783. 30361340 PMC6535145
- [196]Shahbazian M.D., Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007; 76: 75– 100. 17362198
- [197]Shogren-Knaak M., Ishii H., Sun J.M., Pazin M.J., Davie J.R., Peterson C.L. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science. 2006; 311: 844– 847. 16469925
- [198]Zhang R., Erler J., Langowski J. Histone acetylation regulates chromatin accessibility: role of H4K16 in inter-nucleosome interaction. Biophys. J. 2017; 112: 450– 459. 27931745 PMC5300776
- [199]Ackermann B.E., Debelouchina G.T. Heterochromatin protein HP1alpha gelation dynamics revealed by solid-state NMR spectroscopy. Angew. Chem. 2019; 58: 6300– 6305. 30845353 PMC6482055
- [200]Lupianez D.G., Spielmann M., Mundlos S. Breaking TADs: how alterations of chromatin domains result in disease. Trends Genet. 2016; 32: 225– 237. 26862051
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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
Self-citation
- Authors
- Kantidze, O. L., & Razin, S. V.
- Affiliations
- Russian Academy of Sciences (RU)
- Corresponding author
- Razin, Sergey V
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2020-04-20
- Volume
- 48
- Issue
- 9
- Pages
- 4614-4626
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC7229822
- OpenAlex
- W3016788739
- Cited by
- 64
- References
- 18
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 11 · 2023: 8 · 2022: 12 · 2021: 19 · 2020: 4 · 2019: 2
- FWCI
- 1.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nucleic Acids Research (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Russian Science Foundation (19-14-00016)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- weak interaction, 3D genome organization, chromatin folding, chromatin compartments, topologically associating domains, chromatin looping, entropic force, electrostatic interactions, liquid-liquid phase separation, DNA supercoiling, RNA, nuclear compartmentalization, chromosome segregation
- MeSH terms
- Chromatin, DNA, Superhelical, RNA, Static Electricity
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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 ›
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