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Cited by 137Genomics and Chromatin DynamicsNuclear Structure and FunctionChromatin Remodeling and Cancer

Suppression of liquid–liquid phase separation by 1,6-hexanediol partially compromises the 3D genome organization in living cells

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Ulianov, Sergey V, Velichko, Artem K, Magnitov, Mikhail D, Luzhin, Artem V, Golov, Arkadiy K, Ovsyannikova, Natalia, Kireev, Igor I, Gavrikov, Alexey S +6 more·2021·Nucleic Acids Research
DOI 10.1093/nar/gkab249PMC PMC8501969

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Abstract

Liquid-liquid phase separation (LLPS) contributes to the spatial and functional segregation of molecular processes within the cell nucleus. However, the role played by LLPS in chromatin folding in living cells remains unclear. Here, using stochastic optical reconstruction microscopy (STORM) and Hi-C techniques, we studied the effects of 1,6-hexanediol (1,6-HD)-mediated LLPS disruption/modulation on higher-order chromatin organization in living cells. We found that 1,6-HD treatment caused the enlargement of nucleosome clutches and their more uniform distribution in the nuclear space. At a megabase-scale, chromatin underwent moderate but irreversible perturbations that resulted in the partial mixing of A and B compartments. The removal of 1,6-HD from the culture medium did not allow chromatin to acquire initial configurations, and resulted in more compact repressed chromatin than in untreated cells. 1,6-HD treatment also weakened enhancer-promoter interactions and TAD insulation but did not considerably affect CTCF-dependent loops. Our results suggest that 1,6-HD-sensitive LLPS plays a limited role in chromatin spatial organization by constraining its folding patterns and facilitating compartmentalization at different levels.

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  • Some enhancer-promoter loops are destroyed or weakened upon cell treatment with 1,6-hexanediol, an agent that destroys phase condensates.

    “Indeed, some enhancer-promoter loops are destroyed or weakened upon cell treatment with 1,6-hexanediol, an agent that destroys phase condensates [106].”

    From Enhancer Function in the 3D Genome (2023) · cites this paper as [106]

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  1. [1]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
  2. [4]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
  3. [5]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
  4. [6]Rowley M.J., Corces V.G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 2018; 19: 789– 800. 30367165 PMC6312108
  5. [8]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. U.S.A. 2018; 115: E6697– E6706. 29967174 PMC6055145
  6. [9]Fudenberg G., Abdennur N., Imakaev M., Goloborodko A., Mirny L.A. Emerging evidence of chromosome folding by loop extrusion. Cold Spring Harb. Symp. Quant. Biol. 2017; 82: 45– 55. 29728444 PMC6512960
  7. [11]Courchaine E.M., Lu A., Neugebauer K.M. Droplet organelles. EMBO J. 2016; 35: 1603– 1612. 27357569 PMC4969579
  8. [12]Banani S.F., Lee H.O., Hyman A.A., Rosen M.K. Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 2017; 18: 285– 298. 28225081 PMC7434221
  9. [13]Boeynaems S., Alberti S., Fawzi N.L., Mittag T., Polymenidou M., Rousseau F., Schymkowitz J., Shorter J., Wolozin B., Van Den Bosch L. et al. Protein phase separation: a new phase in cell biology. Trends Cell Biol. 2018; 28: 420– 435. 29602697 PMC6034118
  10. [14]Gomes E., Shorter J. The molecular language of membraneless organelles. J. Biol. Chem. 2019; 294: 7115– 7127. 30045872 PMC6509512
  11. [15]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
  12. [16]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
  13. [17]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
  14. [18]Darling A.L., Liu Y., Oldfield C.J., Uversky V.N. Intrinsically disordered proteome of human membrane-less organelles. Proteomics. 2018; 18: e1700193. 29068531
  15. [19]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
  16. [20]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
  17. [21]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
  18. [22]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. U.S.A. 2018; 115: 11964– 11969. 30301810 PMC6255207
  19. [23]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
  20. [24]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
  21. [25]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
  22. [26]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
  23. [27]Cho W.K., Spille J.H., Hecht M., Lee C., Li C., Grube V., Cisse II. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science. 2018; 361: 412– 415. 29930094 PMC6543815
  24. [28]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
  25. [29]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
  26. [30]Hahn S. Phase separation, protein disorder, and enhancer function. Cell. 2018; 175: 1723– 1725. 30550782
  27. [31]Gurumurthy A., Shen Y., Gunn E.M., Bungert J. Phase separation and transcription regulation: are super-enhancers and locus control regions primary sites of transcription complex assembly. Bioessays. 2019; 41: e1800164. 30500078 PMC6484441
  28. [32]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
  29. [33]Guo Y.E., Manteiga J.C., Henninger J.E., Sabari B.R., Dall’Agnese A., Hannett N.M., Spille J.H., Afeyan L.K., Zamudio A.V., Shrinivas K. et al. Pol II phosphorylation regulates a switch between transcriptional and splicing condensates. Nature. 2019; 572: 543– 548. 31391587 PMC6706314
  30. [34]Kantidze O.L., Razin S.V. Weak interactions in higher-order chromatin organization. Nucleic Acids Res. 2020; 48: 4614– 4626. 32313950 PMC7229822
  31. [35]Razin S.V., Gavrilov A.A. The role of liquid-liquid phase separation in the compartmentalization of cell nucleus and spatial genome organization. Biochemistry (Mosc.). 2020; 85: 643– 650. 32586227
  32. [37]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
  33. [38]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
  34. [39]Garcia H., Miecznikowski J.C., Safina A., Commane M., Ruusulehto A., Kilpinen S., Leach R.W., Attwood K., Li Y., Degan S. et al. Facilitates chromatin transcription complex is an “accelerator” of tumor transformation and potential marker and target of aggressive cancers. Cell Rep. 2013; 4: 159– 173. 23831030 PMC5886782
  35. [40]Shin Y., Berry J., Pannucci N., Haataja M.P., Toettcher J.E., Brangwynne C.P. Spatiotemporal control of intracellular phase transitions using light-activated optodroplets. Cell. 2017; 168: 159– 171. 28041848 PMC5562165
  36. [41]Nozaki T., Imai R., Tanbo M., Nagashima R., Tamura S., Tani T., Joti Y., Tomita M., Hibino K., Kanemaki M.T. et al. Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging. Mol. Cell. 2017; 67: 282– 293. 28712725
  37. [42]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
  38. [43]Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012; 9: 357– 359. 22388286 PMC3322381
  39. [45]Abdennur N., Mirny L. Cooler: scalable storage for Hi-C data and other genomically-labeled arrays. Bioinformatics. 2019; 36: 311– 316. PMC8205516 31290943
  40. [46]Davis C.A., Hitz B.C., Sloan C.A., Chan E.T., Davidson J.M., Gabdank I., Hilton J.A., Jain K., Baymuradov U.K., Narayanan A.K. et al. The encyclopedia of DNA elements (ENCODE): data portal update. Nucleic Acids Res. 2018; 46: D794– D801. 29126249 PMC5753278
  41. [47]Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T.R. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013; 29: 15– 21. 23104886 PMC3530905
  42. [48]Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. Genome Project Data Processing, S. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25: 2078– 2079. 19505943 PMC2723002
  43. [49]Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26: 841– 842. 20110278 PMC2832824
  44. [52]Crane E., Bian Q., McCord R.P., Lajoie B.R., Wheeler B.S., Ralston E.J., Uzawa S., Dekker J., Meyer B.J. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature. 2015; 523: 240– 244. 26030525 PMC4498965
  45. [53]Flyamer I.M., Illingworth R.S., Bickmore W.A. Coolpup.py: versatile pile-up analysis of Hi-C data. Bioinformatics. 2020; 36: 2980– 2985. 32003791 PMC7214034
  46. [54]Durand N.C., Shamim M.S., Machol I., Rao S.S., Huntley M.H., Lander E.S., Aiden E.L. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016; 3: 95– 98. 27467249 PMC5846465
  47. [55]Dao L.T.M., Galindo-Albarran A.O., Castro-Mondragon J.A., Andrieu-Soler C., Medina-Rivera A., Souaid C., Charbonnier G., Griffon A., Vanhille L., Stephen T. et al. Genome-wide characterization of mammalian promoters with distal enhancer functions. Nat. Genet. 2017; 49: 1073– 1081. 28581502
  48. [56]Arrigoni L., Richter A.S., Betancourt E., Bruder K., Diehl S., Manke T., Bonisch U. Standardizing chromatin research: a simple and universal method for ChIP-seq. Nucleic Acids Res. 2016; 44: e67. 26704968 PMC4838356
  49. [57]Pena-Hernandez R., Marques M., Hilmi K., Zhao T., Saad A., Alaoui-Jamali M.A., del Rincon S.V., Ashworth T., Roy A.L., Emerson B.M. et al. Genome-wide targeting of the epigenetic regulatory protein CTCF to gene promoters by the transcription factor TFII-I. Proc. Natl Acad. Sci. U.S.A. 2015; 112: E677– E686. 25646466 PMC4343169
  50. [58]Ramirez F., Ryan D.P., Gruning B., Bhardwaj V., Kilpert F., Richter A.S., Heyne S., Dundar F., Manke T. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016; 44: W160– W165. 27079975 PMC4987876
  51. [59]Amemiya H.M., Kundaje A., Boyle A.P. The ENCODE blacklist: identification of problematic regions of the genome. Sci. Rep. 2019; 9: 9354. 31249361 PMC6597582
  52. [60]Zhang Y., Lin Y.H., Johnson T.D., Rozek L.S., Sartor M.A. PePr: a peak-calling prioritization pipeline to identify consistent or differential peaks from replicated ChIP-Seq data. Bioinformatics. 2014; 30: 2568– 2575. 24894502 PMC4155259
  53. [61]Lesne A., Baudement M.O., Rebouissou C., Forne T. Exploring mammalian genome within phase-separated nuclear bodies: experimental methods and implications for gene expression. Genes. 2019; 10: 1049. PMC6947181 31861077
  54. [62]Alberti S., Gladfelter A., Mittag T. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell. 2019; 176: 419– 434. 30682370 PMC6445271
  55. [63]Kroschwald S., Maharana S., Simon A. Hexanediol: a chemical probe to investigate the material properties of membrane-less compartments. Matters. 2017; doi:10.19185/matters.201702000010. · DOI
  56. [64]Ming Y., Chen X., Xu Y., Wu Y., Wang C., Zhang T., Mao R., Fan Y. Targeting liquid–liquid phase separation in pancreatic cancer. Transl. Cancer Res. 2019; 8: 96– 103. PMC8798987 35116738
  57. [65]Michelini F., Rossiello F., d’Adda di Fagagna F., Francia S. RNase A treatment and reconstitution with DNA damage response RNA in living cells as a tool to study the role of non-coding RNA in the formation of DNA damage response foci. Nat. Protoc. 2019; 14: 1489– 1508. 30962605
  58. [66]Molliex A., Temirov J., Lee J., Coughlin M., Kanagaraj A.P., Kim H.J., Mittag T., Taylor J.P. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell. 2015; 163: 123– 133. 26406374 PMC5149108
  59. [67]Oshidari R., Huang R., Medghalchi M., Tse E.Y.W., Ashgriz N., Lee H.O., Wyatt H., Mekhail K. DNA repair by Rad52 liquid droplets. Nat. Commun. 2020; 11: 695. 32019927 PMC7000754
  60. [68]Yamazaki T., Souquere S., Chujo T., Kobelke S., Chong Y.S., Fox A.H., Bond C.S., Nakagawa S., Pierron G., Hirose T. Functional domains of NEAT1 architectural lncRNA induce paraspeckle assembly through phase separation. Mol. Cell. 2018; 70: 1038– 1053. 29932899
  61. [69]Zhang S., Hinde E., Parkyn Schneider M., Jans D.A., Bogoyevitch M.A. Nuclear bodies formed by polyQ-ataxin-1 protein are liquid RNA/protein droplets with tunable dynamics. Sci. Rep. 2020; 10: 1557. 32005838 PMC6994494
  62. [70]Francia S., Michelini F., Saxena A., Tang D., de Hoon M., Anelli V., Mione M., Carninci P., d’Adda di Fagagna F. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature. 2012; 488: 231– 235. 22722852 PMC3442236
  63. [71]Lin Y., Mori E., Kato M., Xiang S., Wu L., Kwon I., McKnight S.L. Toxic PR poly-dipeptides encoded by the C9orf72 repeat expansion target LC domain polymers. Cell. 2016; 167: 789– 802. 27768897 PMC5076566
  64. [72]Xu J., Ma H., Jin J., Uttam S., Fu R., Huang Y., Liu Y. Super-resolution imaging of higher-order chromatin structures at different epigenomic states in single mammalian cells. Cell Rep. 2018; 24: 873– 882. 30044984 PMC6154382
  65. [73]Su J.H., Zheng P., Kinrot S.S., Bintu B., Zhuang X. Genome-scale imaging of the 3D organization and transcriptional activity of chromatin. Cell. 2020; 182: 1641– 1659. 32822575 PMC7851072
  66. [74]Tan L., Xing D., Chang C.H., Li H., Xie X.S. Three-dimensional genome structures of single diploid human cells. Science. 2018; 361: 924– 928. 30166492 PMC6360088
  67. [75]Amat R., Bottcher R., Le Dily F., Vidal E., Quilez J., Cuartero Y., Beato M., de Nadal E., Posas F. Rapid reversible changes in compartments and local chromatin organization revealed by hyperosmotic shock. Genome Res. 2019; 29: 18– 28. 30523037 PMC6314167
  68. [76]Mirny L.A., Imakaev M., Abdennur N. Two major mechanisms of chromosome organization. Curr. Opin. Cell Biol. 2019; 58: 142– 152. 31228682 PMC6800258
  69. [77]Ernst J., Kellis M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 2010; 28: 817– 825. 20657582 PMC2919626
  70. [79]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
  71. [80]Wang L., Gao Y., Zheng X., Liu C., Dong S., Li R., Zhang G., Wei Y., Qu H., Li Y. et al. Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Mol. Cell. 2019; 76: 646– 659. 31543422
  72. [81]Plys A.J., Davis C.P., Kim J., Rizki G., Keenen M.M., Marr S.K., Kingston R.E. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2. Genes Dev. 2019; 33: 799– 813. 31171700 PMC6601514
  73. [82]Strickfaden H., Tolsma T.O., Sharma A., Underhill D.A., Hansen J.C., Hendzel M.J. Condensed chromatin behaves like a solid on the mesoscale in vitro and in living cells. Cell. 2020; 183: 1772– 1784. 33326747
  74. [83]Stephens A.D., Liu P.Z., Kandula V., Chen H., Almassalha L.M., Herman C., Backman V., O’Halloran T., Adam S.A., Goldman R.D. et al. Physicochemical mechanotransduction alters nuclear shape and mechanics via heterochromatin formation. Mol. Biol. Cell. 2019; 30: 2320– 2330. 31365328 PMC6743459
  75. [84]Itoh Y., Iida S., Tamura S., Nagashima R., Shiraki K., Goto T., Hibino K., Ide S., Maeshima K. 1,6-hexanediol rapidly immobilizes and condenses chromatin in living human cells. Life Sci. Alliance. 2021; 4: e202001005. 33536240 PMC7898662
  76. [85]Razin S.V., Ulianov S.V. Divide and rule: phase separation in eukaryotic genome functioning. Cells. 2020; 9: 2480. PMC7696541 33203115
  77. [86]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
  78. [87]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
  79. [88]Mitchell J.A., Fraser P. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev. 2008; 22: 20– 25. 18172162 PMC2151011
  80. [89]Sanulli S., Gross J.D., Narlikar G.J. Biophysical properties of HP1-mediated heterochromatin. Cold Spring Harb. Symp. Quant. Biol. 2019; 84: 217– 225. 32493764 PMC9128075
  81. [90]Sanulli S., Geeta J.N. Liquid-like interactions in heterochromatin: implications for mechanism and regulation. Curr. Opin. Cell Biol. 2020; 64: 90– 96. 32434105 PMC7371496
  82. [91]Buchwalter A., Kaneshiro J.M., Hetzer M.W. Coaching from the sidelines: the nuclear periphery in genome regulation. Nat. Rev. Genet. 2019; 20: 39– 50. 30356165 PMC6355253
  83. [92]Shevelyov Y.Y., Ulianov S.V. The nuclear lamina as an organizer of chromosome architecture. Cells. 2019; 8: 136. PMC6406483 30744037
  84. [93]Ray J., Munn P.R., Vihervaara A., Lewis J.J., Ozer A., Danko C.G., Lis J.T. Chromatin conformation remains stable upon extensive transcriptional changes driven by heat shock. Proc. Natl Acad. Sci. U.S.A. 2019; 116: 19431– 19439. 31506350 PMC6765289

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Authors
Ulianov, S. V., Velichko, A. K., Magnitov, M. D., Luzhin, A. V., Golov, A. K., Ovsyannikova, N., Kireev, I. I., Gavrikov, A. S., Mishin, A. S., Garaev, A. K., Tyakht, A. V., Gavrilov, A. A., Kantidze, O. L., & Razin, S. V.
Affiliations
  • Lomonosov Moscow State University (RU)
  • Russian Academy of Sciences (RU)
  • Institute of Gene Biology (RU)
  • A.N. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992 Moscow, Russia
Corresponding author
  • Kantidze, Omar L
  • Razin, Sergey V
ORCID
Venue
Nucleic Acids Research
Publisher
Oxford University Press (OUP)
Published
2021-04-09
Volume
49
Issue
18
Pages
10524-10541
ISSN
  • 0305-1048 (ISSN-L)
  • 1362-4962
DOI
10.1093/nar/gkab249
PMC
PMC8501969
OpenAlex
W3150768399
Cited by
137
References
10
Citations by year
2026: 22 · 2025: 30 · 2024: 24 · 2023: 32 · 2022: 14 · 2021: 14 · 2020: 1
FWCI
6.67
Type
journal article
Language
en
Open access
Licence
Locations
  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • Russian Science Foundation (19-74-10009)
  • Ministry of Science and Higher Education of the Russian Federation (075-15-2019-1661)
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
liquid-liquid phase separation, 1,6-hexanediol, 3D genome organization, chromatin folding, nuclear compartments, enhancer-promoter interactions, chromatin condensation, chromatin spatial organization
MeSH terms
Chromatin, Enhancer Elements, Genetic, Glycols, HeLa Cells, Humans, Microscopy, Promoter Regions, Genetic, Genome, Human

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