1932

Abstract

Nuclei are central hubs for information processing in eukaryotic cells. The need to fit large genomes into small nuclei imposes severe restrictions on genome organization and the mechanisms that drive genome-wide regulatory processes. How a disordered polymer such as chromatin, which has vast heterogeneity in its DNA and histone modification profiles, folds into discernibly consistent patterns is a fundamental question in biology. Outstanding questions include how genomes are spatially and temporally organized to regulate cellular processes with high precision and whether genome organization is causally linked to transcription regulation. The advent of next-generation sequencing, super-resolution imaging, multiplexed fluorescent in situ hybridization, and single-molecule imaging in individual living cells has caused a resurgence in efforts to understand the spatiotemporal organization of the genome. In this review, we discuss structural and mechanistic properties of genome organization at different length scales and examine changes in higher-order chromatin organization during important developmental transitions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-032321-035734
2021-10-06
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/37/1/annurev-cellbio-032321-035734.html?itemId=/content/journals/10.1146/annurev-cellbio-032321-035734&mimeType=html&fmt=ahah

Literature Cited

  1. Agbleke AA, Amitai A, Buenrostro JD, Chakrabarti A, Chu L et al. 2020. Advances in chromatin and chromosome research: perspectives from multiple fields. Mol. Cell. 79:6881–901
    [Google Scholar]
  2. Alberti S. 2017. Phase separation in biology. Curr. Biol. 27:20R1097–102
    [Google Scholar]
  3. Alipour E, Marko JF. 2012. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res 40:2211202–12
    [Google Scholar]
  4. Andergassen D, Smith ZD, Lewandowski JP, Gerhardinger C, Meissner A, Rinn JL 2019. In vivo firre and Dxz4 deletion elucidates roles for autosomal gene regulation. eLife 8:e47214
    [Google Scholar]
  5. Anderson EC, Frankino PA, Higuchi-Sanabria R, Yang Q, Bian Q et al. 2019. X chromosome domain architecture regulates Caenorhabditis elegans lifespan but not dosage compensation. Dev. Cell. 51:2192–207.e6
    [Google Scholar]
  6. Arroyo A, Kim B, Yeh J. 2020. Luteinizing hormone action in human oocyte maturation and quality: signaling pathways, regulation, and clinical impact. Reprod. Sci. 27:61223–52
    [Google Scholar]
  7. Avner P, Heard E. 2001. X-chromosome inactivation: counting, choice and initiation. Nat. Rev. Genet. 2:159–67
    [Google Scholar]
  8. Banigan EJ, Mirny LA. 2020. Loop extrusion: theory meets single-molecule experiments. Curr. Opin. Cell Biol. 64:124–38
    [Google Scholar]
  9. Banigan EJ, van den Berg AA, Brandão HB, Marko JF, Mirny LA 2020. Chromosome organization by one-sided and two-sided loop extrusion. eLife 9:e53558
    [Google Scholar]
  10. Barbieri M, Chotalia M, Fraser J, Lavitas LM, Dostie J et al. 2012. Complexity of chromatin folding is captured by the strings and binders switch model. PNAS 109:4016173–78
    [Google Scholar]
  11. Baron CS, van Oudenaarden A. 2019. Unravelling cellular relationships during development and regeneration using genetic lineage tracing. Nat. Rev. Mol. Cell Biol. 20:12753–65
    [Google Scholar]
  12. Beagan JA, Phillips-Cremins JE. 2020. On the existence and functionality of topologically associating domains. Nat. Genet. 52:18–16
    [Google Scholar]
  13. Bian Q, Anderson EC, Yang Q, Meyer BJ 2020. Histone H3K9 methylation promotes formation of genome compartments in Caenorhabditis elegans via chromosome compaction and perinuclear anchoring. PNAS 117:2111459–70
    [Google Scholar]
  14. 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 362:6413eaau1783
    [Google Scholar]
  15. Bogolyubova I, Bogolyubov D. 2020. Heterochromatin morphodynamics in late oogenesis and early embryogenesis of mammals. Cells 9:61497
    [Google Scholar]
  16. Boija A, Klein IA, Sabari BR, Dall'Agnese A, Coffey EL et al. 2018. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell 175:71842–55.e16
    [Google Scholar]
  17. Bonev B, Mendelson Cohen N, Szabo Q, Fritsch L, Papadopoulos GL et al. 2017. Multiscale 3D genome rewiring during mouse neural development. Cell 171:3557–72.e24
    [Google Scholar]
  18. Bose DA, Donahue G, Reinberg D, Shiekhattar R, Bonasio R, Berger SL. 2017. RNA binding to CBP stimulates histone acetylation and transcription. Cell 168:1–2135–49.e22
    [Google Scholar]
  19. Boveri T. 1909. Die Blastomerenkerne von Ascaris megalocephala und die Theorie der Chromosomenindividualität [The blastomeric nuclei of Ascaris megalocephala and the theory of chromosome individuality. ]. Arch. Zellforsch. 3:181–268
    [Google Scholar]
  20. Brackley CA, Johnson J, Kelly S, Cook PR, Marenduzzo D. 2016. Simulated binding of transcription factors to active and inactive regions folds human chromosomes into loops, rosettes and topological domains. Nucleic Acids Res 44:83503–12
    [Google Scholar]
  21. Brejc K, Bian Q, Uzawa S, Wheeler BS, Anderson EC et al. 2017. Dynamic control of X chromosome conformation and repression by a histone H4K20 demethylase. Cell 171:185–102.e23
    [Google Scholar]
  22. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M et al. 1991. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349:630438–44
    [Google Scholar]
  23. Cattoni DI, Gizzi AMC, Georgieva M, Di Stefano M, Valeri A et al. 2017. Single-cell absolute contact probability detection reveals chromosomes are organized by multiple low-frequency yet specific interactions. Nat. Commun. 8:11753
    [Google Scholar]
  24. Cavalheiro GR, Pollex T, Furlong EE. 2021. To loop or not to loop: what is the role of TADs in enhancer function and gene regulation?. Curr. Opin. Genet. Dev. 67:119–29
    [Google Scholar]
  25. Cerase A, Armaos A, Neumayer C, Avner P, Guttman M, Tartaglia GG. 2019. Phase separation drives X-chromosome inactivation: a hypothesis. Nat. Struct. Mol. Biol. 26:5331–34
    [Google Scholar]
  26. Chan MM, Smith ZD, Grosswendt S, Kretzmer H, Norman TM et al. 2019. Molecular recording of mammalian embryogenesis. Nature 570:775977–82
    [Google Scholar]
  27. Chen X, Ke Y, Wu K, Zhao H, Sun Y et al. 2019. Key role for CTCF in establishing chromatin structure in human embryos. Nature 576:7786306–10
    [Google Scholar]
  28. Chen X, Wu X, Wu H, Zhang M. 2020. Phase separation at the synapse. Nat. Neurosci. 33:3301–10
    [Google Scholar]
  29. Cho WK, Spille JH, Hecht M, Lee C, Li C et al. 2018. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science 361:6400412–15
    [Google Scholar]
  30. 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 361:6400eaar2555
    [Google Scholar]
  31. Chow K-H, Budde M, Granados A, Cabrera M, Yoon S et al. 2020. Imaging cell lineage with a synthetic digital recording system. bioRxiv 958678. https://doi.org/10.1101/2020.02.21.958678
    [Crossref]
  32. Chuang PT, Albertson DG, Meyer BJ. 1994. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79:3459–74
    [Google Scholar]
  33. Crane E, Bian Q, McCord RP, Lajoie BR, Wheeler BS et al. 2015. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523:7559240–44
    [Google Scholar]
  34. Cremer M, Grasser F, Lanctôt C, Müller S, Neusser M et al. 2012. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. The Nucleus, Volume 1: Nuclei and Subnuclear Components R Hancock 205–39 Totowa, NJ: Humana
    [Google Scholar]
  35. Cremer T, Cremer C. 2006. Part II. Fall and resurrection of chromosome territories during the 1950s to 1980s. The concept of chromosome territories falls in disgrace. Eur. J. Histochem. 50:4223–72
    [Google Scholar]
  36. Csankovszki G, Collette K, Spahl K, Carey J, Snyder M et al. 2009. Three distinct condensin complexes control C. elegans chromosome dynamics. Curr. Biol. 19:19–19
    [Google Scholar]
  37. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. 2002. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319:51097–113
    [Google Scholar]
  38. Davidson IF, Bauer B, Goetz D, Tang W, Wutz G, Peters JM. 2019. DNA loop extrusion by human cohesin. Science 366:64711338–45
    [Google Scholar]
  39. Dekker J, Mirny L. 2016. The 3D genome as moderator of chromosomal communication. Cell 164:61110–21
    [Google Scholar]
  40. Di Pierro M, Potoyan DA, Wolynes PG, Onuchic JN 2018. Anomalous diffusion, spatial coherence, and viscoelasticity from the energy landscape of human chromosomes. PNAS 115:307753–58
    [Google Scholar]
  41. 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 485:7398376–80
    [Google Scholar]
  42. Du Z, Zheng H, Huang B, Ma R, Wu J et al. 2017. Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547:7662232–35
    [Google Scholar]
  43. Earnshaw WC, Laemmli UK. 1983. Architecture of metaphase chromosomes and chromosome scaffolds. J. Cell Biol. 96:184–93
    [Google Scholar]
  44. Eeftens JM, Kapoor M, Brangwynne CP. 2020. Epigenetic memory as a time integral over prior history of Polycomb phase separation. bioRxiv 254706. https://doi.org/10.1101/2020.08.19.254706
    [Crossref]
  45. Eng C-HL, Lawson M, Zhu Q, Dries R, Koulena N et al. 2019. Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+. Nature 568:7751235–39
    [Google Scholar]
  46. Erdel F, Rademacher A, Vlijm R, Tünnermann J, Frank L et al. 2020. Mouse heterochromatin adopts digital compaction states without showing hallmarks of HP1-driven liquid-liquid phase separation. Mol. Cell. 78:2236–49.e7
    [Google Scholar]
  47. Erdel F, Rippe K. 2018. Formation of chromatin subcompartments by phase separation. Biophysical J 114:102262–70
    [Google Scholar]
  48. Espinola SM, Götz M, Fiche J-B, Bellec M, Houbron C et al. 2020. Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development. bioRxiv 191015. https://doi.org/10.1101/2020.07.07.191015
    [Crossref]
  49. Finn EH, Pegoraro G, Brandão HB, Valton AL, Oomen ME et al. 2019. Extensive heterogeneity and intrinsic variation in spatial genome organization. Cell 176:61502–15.e10
    [Google Scholar]
  50. Flavahan WA, Drier Y, Liau BB, Gillespie SM, Venteicher AS et al. 2016. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529:7584110–14
    [Google Scholar]
  51. Flyamer IM, Gassler J, Imakaev M, Brandão HB, Ulianov SV et al. 2017. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544:7648110–14
    [Google Scholar]
  52. Frieda KL, Linton JM, Hormoz S, Choi J, Chow K-HK et al. 2017. Synthetic recording and in situ readout of lineage information in single cells. Nature 541:7635107–11
    [Google Scholar]
  53. Froberg JE, Pinter SF, Kriz AJ, Jégu T, Lee JT. 2018. Megadomains and superloops form dynamically but are dispensable for X-chromosome inactivation and gene escape. Nat. Commun. 9:15004
    [Google Scholar]
  54. Fudenberg G, Abdennur N, Imakaev M, Goloborodko A, Mirny LA. 2017. Emerging evidence of chromosome folding by loop extrusion. Cold Spring Harb. Symp. Quant. Biol. 82:45–55
    [Google Scholar]
  55. Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of chromosomal domains by loop extrusion. Cell Rep 15:92038–49
    [Google Scholar]
  56. Fudenberg G, Pollard KS 2019. Chromatin features constrain structural variation across evolutionary timescales. PNAS 116:62175–80
    [Google Scholar]
  57. Galupa R, Heard E. 2015. X-chromosome inactivation: new insights into cis and trans regulation. Curr. Opin. Genet. Dev. 31:57–66
    [Google Scholar]
  58. Galupa R, Heard E. 2018. X-chromosome inactivation: a crossroads between chromosome architecture and gene regulation. Annu. Rev. Genet. 52:535–66
    [Google Scholar]
  59. Galupa R, Nora EP, Worsley-Hunt R, Picard C, Gard C et al. 2020. A conserved noncoding locus regulates random monoallelic Xist expression across a topological boundary. Mol. Cell. 77:2352–67.e8
    [Google Scholar]
  60. Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A et al. 2018. Real-time imaging of DNA loop extrusion by condensin. Science 360:6384102–5
    [Google Scholar]
  61. 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 36:243600–18
    [Google Scholar]
  62. Ghavi-Helm Y, Jankowski A, Meiers S, Viales RR, Korbel JO, Furlong EEM. 2019. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat. Genet. 51:81272–82
    [Google Scholar]
  63. Ghosh RP, Franklin JM, Draper WE, Shi Q, Beltran B et al. 2019. A fluorogenic array for temporally unlimited single-molecule tracking. Nat. Chem. Biol. 15:4401–9
    [Google Scholar]
  64. Gibcus JH, Samejima K, Goloborodko A, Samejima I, Naumova N et al. 2018. A pathway for mitotic chromosome formation. Science 359:6376eaao6135
    [Google Scholar]
  65. Giorgetti L, Lajoie BR, Carter AC, Attia M, Zhan Y et al. 2016. Structural organization of the inactive X chromosome in the mouse. Nature 535:7613575–79
    [Google Scholar]
  66. Gligoris TG, Scheinost JC, Bürmann F, Petela N, Chan KL et al. 2014. Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science 346:6212963–67
    [Google Scholar]
  67. Golfier S, Quail T, Kimura H, Brugués J 2020. Cohesin and condensin extrude DNA loops in a cell-cycle dependent manner. eLife 9:e53885
    [Google Scholar]
  68. Guo YE, Manteiga JC, Henninger JE, Sabari BR, Dall'Agnese A et al. 2019. Pol II phosphorylation regulates a switch between transcriptional and splicing condensates. Nature 572:7770543–48
    [Google Scholar]
  69. Handel MA, Schimenti JC. 2010. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat. Rev. Genet. 11:2124–36
    [Google Scholar]
  70. Hanssen LLP, Kassouf MT, Oudelaar AM, Biggs D, Preece C et al. 2017. Tissue-specific CTCF-cohesin-mediated chromatin architecture delimits enhancer interactions and function in vivo. Nat. Cell Biol. 19:8952–61
    [Google Scholar]
  71. Hardy WB. 1899. On the structure of cell protoplasm: Part I. The structure produced in a cell by fixative and post-mortem change. The structure of colloidal matter and the mechanism of setting and of coagulation. J. Physiol. 24:2158–210
    [Google Scholar]
  72. Hartl TA, Smith HF, Bosco G. 2008. Chromosome alignment and transvection are antagonized by condensin II. Science 322:59061384–87
    [Google Scholar]
  73. Hassler M, Shaltiel IA, Haering CH. 2018. Towards a unified model of SMC complex function. Curr. Biol. 28:21R1266–81
    [Google Scholar]
  74. Hay D, Hughes JR, Babbs C, Davies JOJ, Graham JB et al. 2016. Genetic dissection of the α-globin super-enhancer in vivo. Nat. Genet. 48:8895–903
    [Google Scholar]
  75. Hildebrand EM, Dekker J. 2020. Mechanisms and functions of chromosome compartmentalization. Trends Biochem. Sci. 45:5385–96
    [Google Scholar]
  76. Hirano T. 1995. Biochemical and genetic dissection of mitotic chromosome condensation. Trends Biochem. Sci. 20:9357–61
    [Google Scholar]
  77. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M et al. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLOS Biol 6:102220–36
    [Google Scholar]
  78. Hnisz D, Weintrau AS, Day DS, Valton AL, Bak RO et al. 2016. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science 351:62801454–58
    [Google Scholar]
  79. Hrvatin S, Hochbaum DR, Nagy MA, Cicconet M, Robertson K et al. 2018. Single-cell analysis of experience-dependent transcriptomic states in the mouse visual cortex. Nat. Neurosci. 21:1120–29
    [Google Scholar]
  80. Hsieh THS, Cattoglio C, Slobodyanyuk E, Hansen AS, Rando OJ et al. 2020. Resolving the 3D landscape of transcription-linked mammalian chromatin folding. Mol. Cell 78:3539–53.e8
    [Google Scholar]
  81. Hyman AA, Weber CA, Jülicher F. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58
    [Google Scholar]
  82. Ing-Simmons E, Vaid R, Mannervik M, Vaquerizas JM. 2020. Independence of 3D chromatin conformation and gene regulation during Drosophila dorsoventral patterning. bioRxiv 186791. htpps://doi.org/10.1101/2020.07.07.186791
    [Crossref]
  83. Jackson DA, Pombo A. 1998. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140:61285–95
    [Google Scholar]
  84. Jégu T, Aeby E, Lee JT. 2017. The X chromosome in space. Nat. Rev. Genet. 18:6377–89
    [Google Scholar]
  85. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z et al. 2013. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503:7475290–94
    [Google Scholar]
  86. Johzuka K, Terasawa M, Ogawa H, Ogawa T, Horiuchi T. 2006. Condensin loaded onto the replication fork barrier site in the rRNA gene repeats during S phase in a FOB1-dependent fashion to prevent contraction of a long repetitive array in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:62226–36
    [Google Scholar]
  87. Jung YH, Sauria MEG, Lyu X, Cheema MS, Ausio J et al. 2017. Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes. Cell Rep 18:61366–82
    [Google Scholar]
  88. Kaaij LJT, van der Weide RH, Ketting RF, de Wit E. 2018. Systemic loss and gain of chromatin architecture throughout zebrafish development. Cell Rep 24:11–10.e4
    [Google Scholar]
  89. Ke Y, Xu Y, Chen X, Feng S, Liu Z et al. 2017. 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170:2367–81.e20
    [Google Scholar]
  90. Kempfer R, Pombo A. 2020. Methods for mapping 3D chromosome architecture. Nat. Rev. Genet. 21:4207–26
    [Google Scholar]
  91. Kent S, Brown K, Yang C, Alsaihati N, Tian C et al. 2020. Phase-separated transcriptional condensates accelerate target-search process revealed by live-cell single-molecule imaging. Cell Rep 33:2108248
    [Google Scholar]
  92. Kim E, Kerssemakers J, Shaltiel IA, Haering CH, Dekker C. 2020. DNA-loop extruding condensin complexes can traverse one another. Nature 579:7799438–42
    [Google Scholar]
  93. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM et al. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465:7295182–87
    [Google Scholar]
  94. Kim Y, Shi Z, Zhang H, Finkelstein IJ, Yu H. 2019. Human cohesin compacts DNA by loop extrusion. Science 366:64711345–49
    [Google Scholar]
  95. Kornberg RD. 1974. Chromatin structure: a repeating unit of histones and DNA. Science 184:4139868–71
    [Google Scholar]
  96. Kragesteen BK, Spielmann M, Paliou C, Heinrich V, Schöpflin R et al. 2018. Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis. Nat. Genet. 50:101463–73
    [Google Scholar]
  97. Krefting J, Andrade-Navarro MA, Ibn-Salem J. 2018. Evolutionary stability of topologically associating domains is associated with conserved gene regulation. BMC Biol 16:87
    [Google Scholar]
  98. Kretzschmar K, Watt FM. 2012. Lineage tracing. Cell 148:1–233–45
    [Google Scholar]
  99. Lappala A, Terentjev EM. 2013.. “ Raindrop” coalescence of polymer chains during coil-globule transition. Macromolecules 46:31239–47
    [Google Scholar]
  100. 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 547:7662236–40
    [Google Scholar]
  101. Lau MS, Schwartz MG, Kundu S, Savol AJ, Wang PI et al. 2017. Mutation of a nucleosome compaction region disrupts Polycomb-mediated axial patterning. Science 355:63291081–84
    [Google Scholar]
  102. Lee JT. 2011. Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat. Rev. Mol. Cell Biol. 12:12815–26
    [Google Scholar]
  103. Lieberman-Aiden E, Van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:5950289–93
    [Google Scholar]
  104. Loda A, Heard E. 2019. Xist RNA in action: past, present, and future. PLOS Genet 15:9e1008333
    [Google Scholar]
  105. Long HS, Powell G, Greenaway S, Mallon AM, Lindgren CM, Simon MM. 2020. Making sense of the linear genome, gene function and TADs. bioRxiv 316786. https://doi.org/10.1101/2020.09.28.316786
    [Crossref]
  106. Lu L, Liu X, Huang W-K, Giusti-Rodríguez P, Cui J et al. 2020. Robust Hi-C maps of enhancer-promoter interactions reveal the function of non-coding genome in neural development and diseases. Mol. Cell. 79:3521–34.e15
    [Google Scholar]
  107. 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 161:51012–25
    [Google Scholar]
  108. Luppino JM, Joyce EF. 2020. Single cell analysis pushes the boundaries of TAD formation and function. Curr. Opin. Genet. Dev. 61:25–31
    [Google Scholar]
  109. Mao YS, Zhang B, Spector DL. 2011. Biogenesis and function of nuclear bodies. Trends Genet 27:8295–306
    [Google Scholar]
  110. Mardinly AR, Spiegel I, Patrizi A, Centofante E, Bazinet JE et al. 2016. Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons. Nature 531:7594371–75
    [Google Scholar]
  111. Marinov G, Trevino A, Xiang T, Kundaje A, Grossman A, Greenleaf W. 2020. Transcription-dependent domain-scale 3D genome organization in dinoflagellates. bioRxiv 181685. https://doi.org/10.1101/2020.07.01.181685
    [Crossref] [Google Scholar]
  112. Marko JF. 2009. Linking topology of tethered polymer rings with applications to chromosome segregation and estimation of the knotting length. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 79:5 Part 1051905
    [Google Scholar]
  113. Marsden MPF, Laemmli UK. 1979. Metaphase chromosome structure: evidence for a radial loop model. Cell 17:4849–58
    [Google Scholar]
  114. Mateo LJ, Murphy SE, Hafner A, Cinquini IS, Walker CA, Boettiger AN. 2019. Visualizing DNA folding and RNA in embryos at single-cell resolution. Nature 568:775049–54
    [Google Scholar]
  115. McSwiggen DT, Hansen AS, Teves SS, Marie-Nelly H, Hao Y et al. 2019a. Evidence for DNA-mediated nuclear compartmentalization distinct from phase separation. eLife 8:e47098
    [Google Scholar]
  116. McSwiggen DT, Mir M, Darzacq X, Tjian R. 2019b. Evaluating phase separation in live cells: diagnosis, caveats, and functional consequences. Genes Dev 33:23–241619–34
    [Google Scholar]
  117. Meyer BJ 2018. Sex and death: from cell fate specification to dynamic control of X-chromosome structure and gene expression. Mol. Biol. Cell 29:222616–21
    [Google Scholar]
  118. Michieletto D, Orlandini E, Marenduzzo D. 2016. Polymer model with epigenetic recoloring reveals a pathway for the de novo establishment and 3D organization of chromatin domains. Phys. Rev. X 6:4041047
    [Google Scholar]
  119. Minajigi A, Froberg JE, Wei C, Sunwoo H, Kesner B et al. 2015. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science 349:6245aab2276
    [Google Scholar]
  120. Mirny LA, Imakaev M, Abdennur N. 2019. Two major mechanisms of chromosome organization. Curr. Opin. Cell Biol. 58:142–52
    [Google Scholar]
  121. Monkhorst K, Jonkers I, Rentmeester E, Grosveld F, Gribnau J. 2008. X inactivation counting and choice is a stochastic process: evidence for involvement of an X-linked activator. Cell 132:3410–21
    [Google Scholar]
  122. Nair SJ, Yang L, Meluzzi D, Oh S, Yang F et al. 2019. Phase separation of ligand-activated enhancers licenses cooperative chromosomal enhancer assembly. Nat. Struct. Mol. Biol. 26:3193–203
    [Google Scholar]
  123. Nand A, Zhan Y, Salazar OR, Aranda M, Voolstra CR, Dekker J. 2020. Chromosome-scale assembly of the coral endosymbiont Symbiodinium microadriaticum genome provides insight into the unique biology of dinoflagellate chromosomes. bioRxiv 182477. https://doi.org/10.1101/2020.07.01.182477
    [Crossref]
  124. Narendra V, Rocha PP, An D, Raviram R, Skok JA et al. 2015. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347:62251017–21
    [Google Scholar]
  125. Nguyen HQ, Chattoraj S, Castillo D, Nguyen SC, Nir G et al. 2020. 3D mapping and accelerated super-resolution imaging of the human genome using in situ sequencing. Nat. Methods 17:8822–32
    [Google Scholar]
  126. Nora EP, Goloborodko A, Valton AL, Gibcus JH, Uebersohn A et al. 2017. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169:5930–44.e22
    [Google Scholar]
  127. Nord AS, West AE. 2020. Neurobiological functions of transcriptional enhancers. Nat. Neurosci. 23:15–14
    [Google Scholar]
  128. Nozaki T, Imai R, Tanbo M, Nagashima R, Tamura S et al. 2017. Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging. Mol. Cell 67:2282–93.e7
    [Google Scholar]
  129. Onuki A. 2002. Phase Transition Dynamics Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  130. 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 357:6349eaag0025
    [Google Scholar]
  131. Patel L, Kang R, Rosenberg SC, Qiu Y, Raviram R et al. 2019. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nat. Struct. Mol. Biol. 26:3164–74
    [Google Scholar]
  132. Paulson JR, Laemmli UK. 1977. The structure of histone-depleted metaphase chromosomes. Cell 12:3817–28
    [Google Scholar]
  133. Plys AJ, Davis CP, Kim J, Rizki G, Keenen MM et al. 2019. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2. Genes Dev 33:13–14799–813
    [Google Scholar]
  134. Pope BD, Ryba T, Dileep V, Yue F, Wu W et al. 2014. Topologically associating domains are stable units of replication-timing regulation. Nature 515:7527402–5
    [Google Scholar]
  135. Rabl C. 1885. Über Zelltheilung [About cell healing]. Morph. Jahrb. 10:214–330
    [Google Scholar]
  136. Rajarajan P, Borrman T, Liao W, Schrode N, Flaherty E et al. 2018. Neuron-specific signatures in the chromosomal connectome associated with schizophrenia risk. Science 362:6420eaat4311
    [Google Scholar]
  137. Rao SSP, Huang SC, St Hilaire BG, Engreitz JM, Perez EM et al. 2017. Cohesin loss eliminates all loop domains. Cell 171:2305–20.e24
    [Google Scholar]
  138. 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 159:71665–80
    [Google Scholar]
  139. Rathke C, Baarends WM, Awe S, Renkawitz-Pohl R. 2014. Chromatin dynamics during spermiogenesis. Gene Regul. Mech. 1839:3155–68
    [Google Scholar]
  140. Ricci MA, Manzo C, García-Parajo MF, Lakadamyali M, Cosma MP. 2015. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160:61145–58
    [Google Scholar]
  141. Rodriques SG, Stickels RR, Goeva A, Martin CA, Murray E et al. 2019. Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363:64341463–67
    [Google Scholar]
  142. Rosa A, Zimmer C. 2014. Computational models of large-scale genome architecture. Int. Rev. Cell Mol. Biol. 307:275–349
    [Google Scholar]
  143. Rosin LF, Nguyen SC, Joyce EF 2018. Condensin II drives large-scale folding and spatial partitioning of interphase chromosomes in Drosophila nuclei. PLOS Genet 14:7e1007393
    [Google Scholar]
  144. Rowley MJ, Nichols MH, Lyu X, Ando-Kuri M, Rivera ISM et al. 2017. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67:5837–52.e7
    [Google Scholar]
  145. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M et al. 2010. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res 20:6761–70
    [Google Scholar]
  146. Sabari BR, Dall'Agnese A, Boija A, Klein IA, Coffey EL et al. 2018. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361:6400eaar3958
    [Google Scholar]
  147. Salvador-Martínez I, Grillo M, Averof M, Telford MJ 2019. Is it possible to reconstruct an accurate cell lineage using CRISPR recorders?. eLife 8:e40292
    [Google Scholar]
  148. 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 112:47E6456–65
    [Google Scholar]
  149. Saurin AJ, Shiels C, Williamson J, Satijn DPE, Otte AP et al. 1998. The human Polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J. Cell Biol. 142:4887–98
    [Google Scholar]
  150. Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, Kim TK. 2014. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell 56:129–42
    [Google Scholar]
  151. Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G et al. 2017. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551:767851–56
    [Google Scholar]
  152. Shaban HA, Barth R, Bystricky K. 2018. Formation of correlated chromatin domains at nanoscale dynamic resolution during transcription. Nucleic Acids Res 46:13e77
    [Google Scholar]
  153. Shaban HA, Barth R, Recoules L, Bystricky K. 2020. Hi-D: nanoscale mapping of nuclear dynamics in single living cells. Genome Biol 21:195
    [Google Scholar]
  154. Sheth RU, Wang HH. 2018. DNA-based memory devices for recording cellular events. Nat. Rev. Genet. 19:11718–32
    [Google Scholar]
  155. Shin Y, Brangwynne CP. 2017. Liquid phase condensation in cell physiology and disease. Science 357:6357eaaf4382
    [Google Scholar]
  156. Shin Y, Chang Y-C, Lee DSW, Berry J, Sanders DW et al. 2018. Liquid nuclear condensates mechanically sense and restructure the genome. Cell 175:61481–91.e13
    [Google Scholar]
  157. Sima J, Chakraborty A, Dileep V, Michalski M, Klein KN et al. 2019. Identifying cis elements for spatiotemporal control of mammalian DNA replication. Cell 176:4816–30.e18
    [Google Scholar]
  158. Singh PB, Newman AG. 2020. On the relations of phase separation and Hi-C maps to epigenetics. R. Soc. Open Sci. 7:2191976
    [Google Scholar]
  159. Skuse DH. 2005. X-linked genes and mental functioning. Hum. Mol. Genet. 14:1R27–32
    [Google Scholar]
  160. Smeets D, Markaki Y, Schmid VJ, Kraus F, Tattermusch A et al. 2014. Three-dimensional super-resolution microscopy of the inactive X chromosome territory reveals a collapse of its active nuclear compartment harboring distinct Xist RNA foci. Epigenetics Chromatin 7:8
    [Google Scholar]
  161. Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH. 2017. Phase separation drives heterochromatin domain formation. Nature 547:7662241–45
    [Google Scholar]
  162. Su JH, Zheng P, Kinrot SS, Bintu B, Zhuang X. 2020. Genome-scale imaging of the 3D organization and transcriptional activity of chromatin. Cell 182:61641–59.e26
    [Google Scholar]
  163. Symmons O, Raj A 2016. What's luck got to do with it: single cells, multiple fates, and biological nondeterminism. Mol. Cell 62:5788–802
    [Google Scholar]
  164. Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD. 2014. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159:3635–46
    [Google Scholar]
  165. Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ et al. 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163:71611–27
    [Google Scholar]
  166. Terakawa T, Bisht S, Eeftens JM, Dekker C, Haering CH, Greene EC. 2017. The condensin complex is a mechanochemical motor that translocates along DNA. Science 358:6363672–76
    [Google Scholar]
  167. Turner JMA. 2007. Meiotic sex chromosome inactivation. Development 134:101823–31
    [Google Scholar]
  168. Vallot A, Tachibana K. 2020. The emergence of genome architecture and zygotic genome activation. Curr. Opin. Cell Biol. 64:50–57
    [Google Scholar]
  169. Valton AL, Dekker J. 2016. TAD disruption as oncogenic driver. Curr. Opin. Genet. Dev. 36:34–40
    [Google Scholar]
  170. van Bemmel JG, Galupa R, Gard C, Servant N, Picard C et al. 2019. The bipartite TAD organization of the X-inactivation center ensures opposing developmental regulation of Tsix and Xist. Nat. Genet. 51:61024–34
    [Google Scholar]
  171. Wachsmuth M, Caudron-Herger M, Rippe K. 2008. Genome organization: balancing stability and plasticity. Mol. Cell Res. 1783:112061–79
    [Google Scholar]
  172. Wallace HA, Bosco G. 2013. Condensins and 3D organization of the interphase nucleus. Curr. Genet. Med. Rep. 1:4219–29
    [Google Scholar]
  173. Wang C-Y, Jégu T, Chu H-P, Oh HJ, Lee JT. 2018. SMCHD1 merges chromosome compartments and assists formation of super-structures on the inactive X. Cell 174:2406–21.e25
    [Google Scholar]
  174. Wang L, Gao Y, Zheng X, Liu C, Dong S et al. 2019. Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Mol. Cell 76:4646–59.e6
    [Google Scholar]
  175. Wang X, Allen WE, Wright MA, Sylwestrak EL, Samusik N et al. 2018. Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361:6400eaat5691
    [Google Scholar]
  176. Wang Y, Wang H, Zhang Y, Du Z, Si W et al. 2019. Reprogramming of meiotic chromatin architecture during spermatogenesis. Mol. Cell 73:3547–61.e6
    [Google Scholar]
  177. Williamson I, Kane L, Devenney PS, Flyamer IM, Anderson E et al. 2019. Developmentally regulated Shh expression is robust to TAD perturbations. Development 146:19dev179523
    [Google Scholar]
  178. Wilson EB. 1899. The structure of protoplasm. Science 10:23733–45
    [Google Scholar]
  179. Woodcock CL, Ghosh RP. 2010. Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol. 2:5a000596
    [Google Scholar]
  180. Woodworth MB, Girskis KM, Walsh CA. 2017. Building a lineage from single cells: genetic techniques for cell lineage tracking. Nat. Rev. Genet. 18:4230–44
    [Google Scholar]
  181. 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 36:243573–99
    [Google Scholar]
  182. Yatskevich S, Rhodes J, Nasmyth K. 2019. Organization of chromosomal DNA by SMC complexes. Annu. Rev. Genet. 53:445–82
    [Google Scholar]
  183. Zhang Y, McCord RP, Ho YJ, Lajoie BR, Hildebrand DG et al. 2012. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148:5908–21
    [Google Scholar]
  184. Zhuang X. 2021. Spatially resolved single-cell genomics and transcriptomics by imaging. Nat. Methods 18:18–22
    [Google Scholar]
  185. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S. 2009. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138:61122–36
    [Google Scholar]
  186. Zuin J, Dixon JR, van der Reijden MIJA, Ye Z, Kolovos P et al. 2014. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. PNAS 111:3996–1001
    [Google Scholar]
  187. Żylicz JJ, Bousard A, Žumer K, Dossin F, Mohammad E et al. 2019. The implication of early chromatin changes in X chromosome inactivation. Cell 176:1–2182–97.e23
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-032321-035734
Loading
/content/journals/10.1146/annurev-cellbio-032321-035734
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error