How the Genome Folds: The Biophysics of Four-Dimensional Chromatin Organization

Literature Cited

1. 1.

   Akhtar W, de Jong J, Pindyurin AV, Pagie L, Meuleman W et al. 2013. Chromatin position effects assayed by thousands of reporters integrated in parallel. Cell 154:914–27
   [Google Scholar]
2. 2.

   Alabert C, Barth TK, Reverón-Gómez N, Sidoli S, Schmidt A et al. 2015. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 29:585–90
   [Google Scholar]
3. 3.

   Alexander JM, Guan J, Huang B, Lomvardas S, Weiner OD 2018. Live-cell imaging reveals enhancer-dependent Sox2 transcription in the absence of enhancer proximity. bioRxiv 409672. https://doi.org/10.1101/409672
   [Crossref]
4. 4.

   Alipour E, Marko JF 2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 40:11202–12
   [Google Scholar]
5. 5.

   Altmeyer M, Neelsen KJ, Teloni F, Pozdnyakova I, Pellegrino S et al. 2015. Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose). Nat. Commun. 6:8088
   [Google Scholar]
6. 6.

   Arbona JM, Herbert S, Fabre E, Zimmer C 2017. Inferring the physical properties of yeast chromatin through Bayesian analysis of whole nucleus simulations. Genome Biol. 18:81
   [Google Scholar]
7. 7.

   Bak AL, Zeuthen J, Crick FH 1977. Higher-order structure of human mitotic chromosomes. PNAS 74:1595–99
   [Google Scholar]
8. 8.

   Beagrie RA, Scialdone A, Schueler M, Kraemer DC, Chotalia M et al. 2017. Complex multi-enhancer contacts captured by genome architecture mapping. Nature 543:519–24
   [Google Scholar]
9. 9.

   Beliveau BJ, Boettiger AN, Avendaño MS, Jungmann R, McCole RB et al. 2015. Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes. Nat. Commun. 6:7147
   [Google Scholar]
10. 10.

    Berger AB, Cabal GG, Fabre E, Duong T, Buc H 2008. High-resolution statistical mapping reveals gene territories in live yeast. Nat. Methods 5:1031–37
    [Google Scholar]
11. 11.

    Bianco S, Chiariello AM, Annunziatella C, Esposito A, Nicodemi M 2017. Predicting chromatin architecture from models of polymer physics. Chromosome Res. 25:25–34
    [Google Scholar]
12. 12.

    Bintu B, Mateo LJ, Su JH, Sinnott-Armstrong NA, Parker M et al. 2018. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science 362:eaau1783
    [Google Scholar]
13. 13.

    Boehning M, Dugast-Darzacq C, Rankovic M, Hansen AS, Yu T et al. 2018. RNA polymerase II clustering through carboxy-terminal domain phase separation. Nat. Struct. Mol. Biol. 25:833–40
    [Google Scholar]
14. 14.

    Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ et al. 2016. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529:418–22
    [Google Scholar]
15. 15.

    Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI 2007. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8:574–85
    [Google Scholar]
16. 16.

    Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K et al. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLOS Biol. 3:e157
    [Google Scholar]
17. 17.

    Branco MR, Pombo A 2006. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLOS Biol. 4:e138
    [Google Scholar]
18. 18.

    Broedersz CP, MacKintosh FC 2014. Modeling semiflexible polymer networks. Rev. Mod. Phys. 86:995–1036
    [Google Scholar]
19. 19.

    Busslinger GA, Stocsits RR, Van Der Lelij P, Axelsson E, Tedeschi A et al. 2017. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature 544:503–7
    [Google Scholar]
20. 20.

    Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W et al. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155:1479–91
    [Google Scholar]
21. 21.

    Chen H, Levo M, Barinov L, Fujioka M, Jaynes JB, Gregor T 2018. Dynamic interplay between enhancer–promoter topology and gene activity. Nat. Genet. 50:1296–303
    [Google Scholar]
22. 22.

    Chen W, Yan Z, Li S, Huang N, Huang X et al. 2018. RNAs as proximity-labeling media for identifying nuclear speckle positions relative to the genome. iScience 4:204–15
    [Google Scholar]
23. 23.

    Chen Y, Zhang Y, Wang Y, Zhang L, Brinkman EK et al. 2018. Mapping 3D genome organization relative to nuclear compartments using TSA-Seq as a cytological ruler. J. Cell Biol. 217:4025–48
    [Google Scholar]
24. 24.

    Chereji RV, Clark DJ 2018. Major determinants of nucleosome positioning. Biophys. J. 114:2279–89
    [Google Scholar]
25. 25.

    Chong S, Dugast-Darzacq C, Liu Z, Dong P, Dailey GM et al. 2018. Imaging dynamic and selective low-complexity domain interactions that control gene transcription. Science 2555:eaar2555
    [Google Scholar]
26. 26.

    Chubb JR, Boyle S, Perry P, Bickmore WA 2002. Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 12:439–45
    [Google Scholar]
27. 27.

    Cremer T, Cremer M 2010. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2:a003889
    [Google Scholar]
28. 28.

    Croft JA, Bridger JM, Shelagh B, Perry P, Teague P, Bickmore WA 1999. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145:1119–31
    [Google Scholar]
29. 29.

    Davidson IF, Goetz D, Zaczek MP, Molodtsov MI, Huis In 't Veld PJ et al. 2016. Rapid movement and transcriptional relocalization of human cohesin on DNA. EMBO J. 35:2671–85
    [Google Scholar]
30. 30.

    Dekker J, Rippe K, Dekker M, Kleckner N 2002. Capturing chromosome conformation. Science 295:1306–11
    [Google Scholar]
31. 31.

    Deng W, Rupon JW, Krivega I, Breda L, Motta I et al. 2014. Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell 158:849–60
    [Google Scholar]
32. 32.

    Dixon JR, Selvaraj S, Yue F, Kim A, Li Y et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80
    [Google Scholar]
33. 33.

    Doi M, Edwards S 1988. The Theory of Polymer Dynamics Oxford: Clarendon
34. 34.

    Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR, Richmond TJ 2004. Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306:1571–73
    [Google Scholar]
35. 35.

    Du Z, Zheng H, Huang B, Ma R, Wu J et al. 2017. Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547:232–35
    [Google Scholar]
36. 36.

    Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP et al. 2016. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3:99–101
    [Google Scholar]
37. 37.

    Erdel F, Rippe K 2018. Formation of chromatin subcompartments by phase separation. Biophys. J. 114:2262–70
    [Google Scholar]
38. 38.

    Falk M, Feodorova Y, Naumova N, Imakaev M, Lajoie RB 2018. Heterochromatin drives organization of conventional and inverted nuclei. bioRxiv 244038. https://doi.org/10.1101/244038
    [Crossref]
39. 39.

    Feric M, Vaidya N, Harmon TS, Mitrea DM, Zhu L et al. 2016. Coexisting liquid phases underlie nucleolar subcompartments. Cell 165:1686–97
    [Google Scholar]
40. 40.

    Festuccia N, Dubois A, Vandormael-Pournin S, Tejeda EG, Mouren A et al. 2016. Mitotic binding of Esrrb marks key regulatory regions of the pluripotency network. Nat. Cell Biol. 18:1139–48
    [Google Scholar]
41. 41.

    Finch JT, Klug A 1976. Solenoidal model for superstructure in chromatin. PNAS 73:1897–901
    [Google Scholar]
42. 42.

    Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS et al. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529:110–14
    [Google Scholar]
43. 43.

    Flyamer IM, Gassler J, Imakaev M, Ulyanov SV, Abdennur N et al. 2017. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544:110–14
    [Google Scholar]
44. 44.

    Fudenberg G, Abdennur N, Imakaev M, Goloborodko A, Mirny L 2018. Emerging evidence of chromosome folding by loop extrusion. Cold Spring Harb. Symp. Quant. Biol. 82:45–55
    [Google Scholar]
45. 45.

    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA 2016. Formation of chromosomal domains by loop extrusion. Cell Rep. 15:2038–49
    [Google Scholar]
46. 46.

    Fudenberg G, Mirny LA 2012. Higher-order chromatin structure: bridging physics and biology. Curr. Opin. Genet. Dev. 22:115–24
    [Google Scholar]
47. 47.

    Fussner E, Djuric U, Strauss M, Hotta A, Perez-Iratxeta C 2011. Constitutive heterochromatin reorganization during somatic cell reprogramming. EMBO J. 30:1778–89
    [Google Scholar]
48. 48.

    Ganai N, Sengupta S, Menon GI 2014. Chromosome positioning from activity-based segregation. Nucleic Acids Res. 42:4145–59
    [Google Scholar]
49. 49.

    Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Real-time imaging of DNA loop extrusion by condensin. Science 360:102–5
    [Google Scholar]
50. 50.

    Gassler J, Brandão HB, Imakaev M, Flyamer IM, Ladstätter S et al. 2017. A mechanism of cohesin-dependent loop extrusion organizes zygotic genome architecture. EMBO J. 36:e201798083
    [Google Scholar]
51. 51.

    Gerchman SE, Ramakrishnan V 1987. Chromatin higher-order structure studied by neutron scattering and scanning transmission electron microscopy. PNAS 84:7802–6
    [Google Scholar]
52. 52.

    Gibcus JH, Mirny LA, Dekker J 2018. A pathway for mitotic chromosome formation. Science 359:eaao6135
    [Google Scholar]
53. 53.

    Grosberg AY, Nechaev S, Shakhnovich E 1988. The role of topological constraints in the kinetics of collapse of macromolecules. J. Phys. 49:2095–100
    [Google Scholar]
54. 54.

    Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB et al. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–51
    [Google Scholar]
55. 55.

    Haarhuis JH, van der Weide RH, Blomen VA, Yáñez-Cuna JO, Amendola M 2017. The cohesin release factor WAPL restricts chromatin loop extension. Cell 169:693–707.e14
    [Google Scholar]
56. 56.

    Hansen AS, Pustova I, Cattoglio C, Tjian R, Darzacq X 2017. CTCF and cohesin regulate chromatin loop stability with distinct dynamics. eLife 6:e25776
    [Google Scholar]
57. 57.

    Hansen JC, Connolly M, McDonald CJ, Pan A, Pryamkova A 2018. The 10-nm chromatin fiber and its relationship to interphase chromosome organization. Biochem. Soc. Trans. 46:67–76
    [Google Scholar]
58. 58.

    Herbert S, Brion A, Arbona JM, Lelek M, Veillet A et al. 2017. Chromatin stiffening underlies enhanced locus mobility after DNA damage in budding yeast. EMBO J. 36:2595–608
    [Google Scholar]
59. 59.

    Hyman AA, Weber CA, Jülicher F 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58
    [Google Scholar]
60. 60.

    Kakui Y, Rabinowitz A, Barry DJ, Uhlmann F 2017. Condensin-mediated remodeling of the mitotic chromatin landscape in fission yeast. Nat. Genet. 49:1553–57
    [Google Scholar]
61. 61.

    Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L 2012. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 30:90–98
    [Google Scholar]
62. 62.

    Ke Y, Xu Y, Chen X, Feng S, Liu Z 2017. 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170:367–81.e20
    [Google Scholar]
63. 63.

    Kornberg RD, Stryer L 1988. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 16:6677–90
    [Google Scholar]
64. 64.

    Kruithof M, Chien FT, Routh A, Logie C, Rhodes D, van Noort J 2009. Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber. Nat. Struct. Mol. Biol. 16:534–40
    [Google Scholar]
65. 65.

    Kwon I, Kato M, Xiang S, Wu L, Theodoropoulos P et al. 2013. Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low complexity domains. Cell 155:1049–60
    [Google Scholar]
66. 66.

    Larson AG, Elnatan D, Keenen MM, Trnka MJ, Johnston JB et al. 2017. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547:236–40
    [Google Scholar]
67. 67.

    Lazar-Stefanita L, Scolari VF, Mercy G, Muller H, Guérin TM et al. 2017. Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle. EMBO J. 36:2684–97
    [Google Scholar]
68. 68.

    Lieberman-Aiden E, Berkum NLV, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–94
    [Google Scholar]
69. 69.

    Lim B, Heist T, Levine M, Fukaya T 2018. Visualization of transvection in living Drosophila embryos. Mol. Cell 70:287–96
    [Google Scholar]
70. 70.

    Lupiáñez DG, Kraft K, Heinrich V, Krawitz P, Brancati F et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–25
    [Google Scholar]
71. 71.

    Mack AH, Schlingman DJ, Ilagan RP, Regan L, Mochrie SGJ 2012. Kinetics and thermodynamics of phenotype: unwinding and rewinding the nucleosome. J. Mol. Biol. 423:687–701
    [Google Scholar]
72. 72.

    Matera AG 1999. Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol. 9:302–9
    [Google Scholar]
73. 73.

    Merkenschlager M, Nora EP 2016. CTCF and cohesin in genome folding and transcriptional gene regulation. Annu. Rev. Genom. Hum. Genet. 17:17–43
    [Google Scholar]
74. 74.

    Murayama Y, Samora CP, Kurokawa Y, Iwasaki H, Uhlmann F 2018. Establishment of DNA-DNA interactions by the cohesin ring. Cell 172:465–77.e15
    [Google Scholar]
75. 75.

    Murayama Y, Uhlmann F 2014. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505:367–71
    [Google Scholar]
76. 76.

    Murayama Y, Uhlmann F 2015. DNA entry into and exit out of the cohesin ring by an interlocking gate mechanism. Cell 163:1628–40
    [Google Scholar]
77. 77.

    Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E et al. 2013. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64
    [Google Scholar]
78. 78.

    Nagano T, Lubling Y, Várnai C, Dudley C, Leung W et al. 2017. Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature 547:61–67
    [Google Scholar]
79. 79.

    Narlikar GJ, Sundaramoorthy R, Owen-Hughes T 2013. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154:490–503
    [Google Scholar]
80. 80.

    Nasmyth K 2001. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35:673–745
    [Google Scholar]
81. 81.

    Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR 2013. Organization of the mitotic chromosome. Science 342:948–53
    [Google Scholar]
82. 82.

    Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE 2000. Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290:138–41
    [Google Scholar]
83. 83.

    Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A 2017. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169:930–44.e22
    [Google Scholar]
84. 84.

    Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–85
    [Google Scholar]
85. 85.

    Nozaki T, Imai R, Tanbo M, Nagashima R, Tamura S, Tani T 2017. Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging. Mol. Cell 67:282–93
    [Google Scholar]
86. 86.

    Nuebler J, Fudenberg G, Imakaev M, Abdennur N, Mirny LA 2018. Chromatin organization by an interplay of loop extrusion and compartmental segregation. PNAS 115:E6697–706
    [Google Scholar]
87. 87.

    Ou HD, Phan S, Deerinck TJ, Thor A, Ellisman MH, O'Shea CC 2017. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357:eaag0025
    [Google Scholar]
88. 88.

    Padinhateeri R, Marko JF 2011. Nucleosome positioning in a model of active chromatin remodeling enzymes. PNAS 108:7799–803
    [Google Scholar]
89. 89.

    Parmar JJ, Marko JF, Padinhateeri R 2014. Nucleosome positioning and kinetics near transcription-start-site barriers are controlled by interplay between active remodeling and DNA sequence. Nucleic Acids Res. 42:128–36
    [Google Scholar]
90. 90.

    Patel A, Malinovska L, Saha S, Wang J, Alberti S et al. 2017. Biochemistry: ATP as a biological hydrotrope. Science 356:753–56
    [Google Scholar]
91. 91.

    Patrick H, Laroche T, Shimada K, Furrer P, Gasser SM 2001. Chromosome dynamics in the yeast interphase nucleus. Science 294:2181–86
    [Google Scholar]
92. 92.

    Pereira MCF, Brackley CA, Michieletto D, Annunziatella C, Bianco S 2018. Complementary chromosome folding by transcription factors and cohesin. bioRxiv 305359. https://doi.org/10.1101/305359
    [Crossref]
93. 93.

    Pope BD, Ryba T, Dileep V, Yue F, Wu W et al. 2014. Topologically associating domains are stable units of replication-timing regulation. Nature 515:402–5
    [Google Scholar]
94. 94.

    Quinodoz SA, Ollikainen N, Tabak B, Palla A, Schmidt JM et al. 2018. Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell 174:744–57
    [Google Scholar]
95. 95.

    Racko D, Benedetti F, Dorier J, Stasiak A 2017. Transcription-induced supercoiling as the driving force of chromatin loop extrusion during formation of TADs in interphase chromosomes. Nucleic Acids Res. 46:1648–60
    [Google Scholar]
96. 96.

    Ramani V, Deng X, Qiu R, Gunderson KL, Steemers FJ et al. 2017. Massively multiplex single-cell Hi-C. Nat. Methods 14:263–66
    [Google Scholar]
97. 97.

    Rao SS, Huang SC, Hilaire BGS, Engreitz JM, Perez EM 2017. Cohesin loss eliminates all loop domains. Cell 171:305–20.e24
    [Google Scholar]
98. 98.

    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–80
    [Google Scholar]
99. 99.

    Razin SV, Gavrilov AA 2014. Chromatin without the 30-nm fiber. Epigenetics 9:653–57
    [Google Scholar]
100. 100.

     Reddy KL, Zullo JM, Bertolino E, Singh H 2008. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452:243–47
     [Google Scholar]
101. 101.

     Ricci MA, Manzo C, García-Parajo MF, Lakadamyali M, Cosma MP 2015. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160:1145–58
     [Google Scholar]
102. 102.

     Robinson PJJ, Fairall L, Huynh VAT, Rhodes D 2006. EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. PNAS 103:6506–11
     [Google Scholar]
103. 103.

     Rosa A, Everaers R 2008. Structure and dynamics of interphase chromosomes. PLOS Comput. Biol. 4:e1000153
     [Google Scholar]
104. 104.

     Rosa A, Zimmer C 2014. Computational models of large-scale genome architecture. Int. Rev. Cell Mol. Biol. 307:275–349
     [Google Scholar]
105. 105.

     Rubinstein M, Colby R 2003. Polymer Physics Oxford: Oxford Univ. Press
106. 106.

     Sanborn AL, Rao SSP, Huang SC, Durand NC, Huntley MH et al. 2015. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. PNAS 112:E6456–65
     [Google Scholar]
107. 107.

     Sazer S, Schiessel H 2018. The biology and polymer physics underlying large-scale chromosome organization. Traffic 19:87–104
     [Google Scholar]
108. 108.

     Schalbetter SA, Goloborodko A, Fudenberg G, Belton JM, Miles C et al. 2017. SMC complexes differentially compact mitotic chromosomes according to genomic context. Nat. Cell Biol. 19:1071–80
     [Google Scholar]
109. 109.

     Schalch T, Duda S, Sargent DF, Richmond TJ 2005. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436:138–41
     [Google Scholar]
110. 110.

     Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G et al. 2017. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551:51–56
     [Google Scholar]
111. 111.

     Solovei I, Kreysing M, Lanctôt C, Kösem S, Peichl L et al. 2009. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–68
     [Google Scholar]
112. 112.

     Song F, Chen P, Sun D, Wang M, Dong L et al. 2014. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344:376–80
     [Google Scholar]
113. 113.

     Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH 2017. Phase separation drives heterochromatin domain formation. Nature 547:241–45
     [Google Scholar]
114. 114.

     Szabo Q, Jost D, Chang JM, Cattoni DI, Papadopoulos GL et al. 2018. TADs are 3D structural units of higher-order chromosome organization in Drosophila. Sci. Adv. 4:eaar8082
     [Google Scholar]
115. 115.

     Tedeschi A, Wutz G, Huet S, Jaritz M, Wuensche A et al. 2013. WAPL is an essential regulator of chromatin structure and chromosome segregation. Nature 501:564–68
     [Google Scholar]
116. 116.

     Teves SS, An L, Hansen AS, Xie L, Darzacq X, Tjian R 2016. A dynamic mode of mitotic bookmarking by transcription factors. eLife 5:e22280
     [Google Scholar]
117. 117.

     Therizols P, Duong T, Dujon B, Zimmer C, Fabre E 2010. Chromosome arm length and nuclear constraints determine the dynamic relationship of yeast subtelomeres. PNAS 107:2025–30
     [Google Scholar]
118. 118.

     Therizols P, Illingworth RS, Courilleau C, Boyle S, Wood AJ, Bickmore WA 2014. Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 346:1238–42
     [Google Scholar]
119. 119.

     Ulianov S, Razin S, Shevelyov Y 2015. Active chromatin and transcription play a key role in chromosome partitioning into TADs. Genome Res. 26:70–84
     [Google Scholar]
120. 120.

     van Steensel B, Belmont AS 2017. Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169:780–91
     [Google Scholar]
121. 121.

     Vian L, Pekowska A, Rao SS, Kieffer-Kwon KR, Jung S 2018. The energetics and physiological impact of cohesin extrusion. Cell 173:1165–78.e20
     [Google Scholar]
122. 122.

     Walther N, Hossain MJ, Politi AZ, Koch B, Kueblbeck M et al. 2018. A quantitative map of human Condensins provides new insights into mitotic chromosome architecture. J. Cell Biol. 217:2309–28
     [Google Scholar]
123. 123.

     Wang S, Su Jh, Beliveau BJ, Bintu B, Moffitt JR et al. 2016. Spatial organization of chromatin domains and compartments in single chromosomes. Science 353:598–602
     [Google Scholar]
124. 124.

     Widom J, Klug A 1985. Structure of the 3000Å chromatin filament: X-ray diffraction from oriented samples. Cell 43:207–13
     [Google Scholar]
125. 125.

     Wiggins PA, van der Heijden T, Moreno-Herrero F, Spakowitz A, Phillips R 2006. High flexibility of DNA on short length scales probed by atomic force microscopy. Nat. Nanotechnol. 1:137–41
     [Google Scholar]
126. 126.

     Wong H, Marie-Nelly H, Herbert S, Carrivain P, Blanc H et al. 2012. A predictive computational model of the dynamic 3D interphase yeast nucleus. Curr. Biol. 22:1881–90
     [Google Scholar]
127. 127.

     Woringer M, Darzacq X 2018. Protein motion in the nucleus: from anomalous diffusion to weak interactions. Biochem. Soc. Trans 46:4945–56
     [Google Scholar]
128. 128.

     Wutz G, Várnai C, Nagasaka K, Cisneros DA, Stocsits RR et al. 2017. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J. 36:3573–99
     [Google Scholar]
129. 129.

     Xiang W, Roberti MJ, Hériché JK, Huet S, Alexander S, Ellenberg J 2018. Correlative live and super-resolution imaging reveals the dynamic structure of replication domains. J. Cell Biol. 217:1973–84
     [Google Scholar]
130. 130.

     Yan J, Maresca TJ, Skoko D, Adams CD, Xiao B et al. 2007. Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics. Mol. Biol. Cell 18:464–74
     [Google Scholar]
131. 131.

     Zhan Y, Mariani L, Barozzi I, Schulz EG, Blüthgen N et al. 2017. Reciprocal insulation analysis of Hi-C data shows that TADs represent a functionally but not structurally privileged scale in the hierarchical folding of chromosomes. Genome Res. 27:479–90
     [Google Scholar]
132. 132.

     Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF 2011. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332:977–80
     [Google Scholar]
133. 133.

     Zhu L, Brangwynne CP 2015. Nuclear bodies: the emerging biophysics of nucleoplasmic phases. Curr. Opin. Cell Biol. 34:23–30
     [Google Scholar]
134. 134.

     Zuin J, Franke V, van IJcken WF, van der Sloot A, Krantz ID et al. 2014. A cohesin-independent role for NIPBL at promoters provides insights in CdLS. PLOS Genet. 10:e1004153
     [Google Scholar]