1932

Abstract

The packaging and organization of the genome within the eukaryotic interphase nucleus directly influence how the genes are expressed. An underappreciated aspect of genome structure is that it is highly dynamic and that the physical positioning of a gene can impart control over its transcriptional status. In this review, we assess the current knowledge of how gene positioning at different levels of genome organization can directly influence gene expression during interphase. The levels of organization discussed include chromatin looping, topologically associated domains, chromosome territories, and nuclear compartments. We discuss specific studies demonstrating that gene positioning is a dynamic and highly regulated feature of the eukaryotic genome that allows for the essential spatiotemporal regulation of genes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-055008
2015-11-23
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-055008.html?itemId=/content/journals/10.1146/annurev-genet-112414-055008&mimeType=html&fmt=ahah

Literature Cited

  1. Andrey G, Montavon T, Mascrez B, Gonzalez F, Noordermeer D. 1.  et al. 2013. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 340:1234167 [Google Scholar]
  2. Bateman JR, Johnson JE, Locke MN. 2.  2012. Comparing enhancer action in cis and in trans. Genetics 191:1143–55 [Google Scholar]
  3. Berger AB, Cabal GG, Fabre E, Duong T, Buc H. 3.  et al. 2008. High-resolution statistical mapping reveals gene territories in live yeast. Nat. Methods 5:1031–37 [Google Scholar]
  4. Bettinger BT, Gilbert DM, Amberg DC. 4.  2004. Actin up in the nucleus. Nat. Rev. Mol. Cell Biol. 5:410–15 [Google Scholar]
  5. Bickmore WA, van Steensel B. 5.  2013. Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–84 [Google Scholar]
  6. Bieker JJ. 6.  2001. Krüppel-like factors: three fingers in many pies. J. Biol. Chem. 276:3734355–58 [Google Scholar]
  7. Blackwood EM, Kadonaga JT. 7.  1998. Going the distance: a current view of enhancer action. Science 281:60–63 [Google Scholar]
  8. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K. 8.  et al. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLOS Biol. 3:e157 [Google Scholar]
  9. Bornfleth H, Edelmann P, Zink D, Cremer T, Cremer C. 9.  1999. Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy. Biophys. J. 77:2871–86 [Google Scholar]
  10. Bothma JP, Magliocco J, Levine M. 10.  2011. The snail repressor inhibits release, not elongation, of paused Pol II in the Drosophila embryo. Curr. Biol. 21:1571–77 [Google Scholar]
  11. Boveri T. 11.  1909. Die blastomerenkerne von Ascaris megalocephala und die theorie der chromosomenindividualität. Arch Zellforsch. 1909:181–268 [Google Scholar]
  12. Branco MR, Pombo A. 12.  2006. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLOS Biol. 4:e138 [Google Scholar]
  13. Bridger JM, Kalla C, Wodrich H, Weitz S, King JA. 13.  et al. 2005. Nuclear RNAs confined to a reticular compartment between chromosome territories. Exp. Cell Res. 302:180–93 [Google Scholar]
  14. Brown JM, Green J, das Neves RP, Wallace HA, Smith AJ. 14.  et al. 2008. Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J. Cell Biol. 182:1083–97 [Google Scholar]
  15. Brown JM, Leach J, Reittie JE, Atzberger A, Lee-Prudhoe J. 15.  et al. 2006. Coregulated human globin genes are frequently in spatial proximity when active. J. Cell Biol. 172:177–87 [Google Scholar]
  16. Capelson M, Corces VG. 16.  2006. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J. 25:1906–14 [Google Scholar]
  17. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW. 17.  2010. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140:372–83 [Google Scholar]
  18. Caron H, van Schaik B, van der Mee M, Baas F, Riggins G. 18.  et al. 2001. The human transcriptome map: clustering of highly expressed genes in chromosomal domains. Science 291:1289–92 [Google Scholar]
  19. Chambeyron S, Bickmore WA. 19.  2004. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18:1119–30 [Google Scholar]
  20. Chepelev I, Wei G, Wangsa D, Tang Q, Zhao K. 20.  2012. Characterization of genome-wide enhancer-promoter interactions reveals co-expression of interacting genes and modes of higher order chromatin organization. Cell Res. 22:490–503 [Google Scholar]
  21. Chopra VS, Kong N, Levine M. 21.  2012. Transcriptional repression via antilooping in the Drosophila embryo. PNAS 109:9460–64 [Google Scholar]
  22. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS. 22.  2006. Long-range directional movement of an interphase chromosome site. Curr. Biol. 16:825–31 [Google Scholar]
  23. Ciabrelli F, Cavalli G. 23.  2015. Chromatin-driven behavior of topologically associating domains. J. Mol. Biol. 427:608–25 [Google Scholar]
  24. Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A. 24.  et al. 2013. Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341:664–67 [Google Scholar]
  25. Clowney EJ, LeGros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC. 25.  et al. 2012. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151:724–37 [Google Scholar]
  26. Cremer T, Cremer M. 26.  2010. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2:a003889 [Google Scholar]
  27. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. 27.  1999. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145:1119–31 [Google Scholar]
  28. Cullen KE, Kladde MP, Seyfred MA. 28.  1993. Interaction between transcription regulatory regions of prolactin chromatin. Science 261:203–6 [Google Scholar]
  29. Deng W, Lee J, Wang H, Miller J, Reik A. 29.  et al. 2012. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 149:1233–44 [Google Scholar]
  30. Deng W, Rupon JW, Krivega I, Breda L, Motta I. 30.  et al. 2014. Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell 158:849–60 [Google Scholar]
  31. Dietzel S, Schiebel K, Little G, Edelmann P, Rappold GA. 31.  et al. 1999. The 3D positioning of ANT2 and ANT3 genes within female X chromosome territories correlates with gene activity. Exp. Cell Res. 252:363–75 [Google Scholar]
  32. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y. 32.  et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80 [Google Scholar]
  33. El-Kady A, Klenova E. 33.  2005. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett. 579:1424–34 [Google Scholar]
  34. Fanucchi S, Shibayama Y, Burd S, Weinberg MS, Mhlanga MM. 34.  2013. Chromosomal contact permits transcription between coregulated genes. Cell 155:606–20 [Google Scholar]
  35. Federico C, Cantarella CD, Di Mare P, Tosi S, Saccone S. 35.  2008. The radial arrangement of the human chromosome 7 in the lymphocyte cell nucleus is associated with chromosomal band gene density. Chromosoma 117:399–410 [Google Scholar]
  36. Ferrai C, Xie SQ, Luraghi P, Munari D, Ramirez F. 36.  et al. 2010. Poised transcription factories prime silent uPA gene prior to activation. PLOS Biol. 8:e1000270 [Google Scholar]
  37. Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E. 37.  et al. 2008. Recruitment to the nuclear periphery can alter expression of genes in human cells. PLOS Genet. 4:e1000039 [Google Scholar]
  38. Galiova G, Bartova E, Kozubek S. 38.  2004. Nuclear topography of beta-like globin gene cluster in IL-3-stimulated human leukemic K-562 cells. Blood Cells Mol. Dis. 33:4–14 [Google Scholar]
  39. Gaszner M, Felsenfeld G. 39.  2006. Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 7:703–13 [Google Scholar]
  40. Gonsior SM, Platz S, Buchmeier S, Scheer U, Jockusch BM, Hinssen H. 40.  1999. Conformational difference between nuclear and cytoplasmic actin as detected by a monoclonal antibody. J. Cell Sci. 112:Pt. 6797–809 [Google Scholar]
  41. Griffith J, Hochschild A, Ptashne M. 41.  1986. DNA loops induced by cooperative binding of lambda repressor. Nature 322:750–52 [Google Scholar]
  42. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB. 42.  et al. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–51 [Google Scholar]
  43. Guo C, Yoon HS, Franklin A, Jain S, Ebert A. 43.  et al. 2011. CTCF-binding elements mediate control of V(D)J recombination. Nature 477:424–30 [Google Scholar]
  44. Guo Y, Monahan K, Wu H, Gertz J, Varley KE. 44.  et al. 2012. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. PNAS 109:21081–86 [Google Scholar]
  45. Harr JC, Luperchio TR, Wong X, Cohen E, Wheelan SJ, Reddy KL. 45.  2015. Directed targeting of chromatin to the nuclear lamina is mediated by chromatin state and A-type lamins. J. Cell Biol. 208:33–52 [Google Scholar]
  46. Hou C, Li L, Qin ZS, Corces VG. 46.  2012. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 48:471–84 [Google Scholar]
  47. Iborra FJ, Pombo A, Jackson DA, Cook PR. 47.  1996. Active RNA polymerases are localized within discrete transcription “factories” in human nuclei. J. Cell. Sci. 109:1427–36 [Google Scholar]
  48. Jackson DA, Iborra FJ, Manders EM, Cook PR. 48.  1998. Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. Mol. Biol. Cell 9:1523–36 [Google Scholar]
  49. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z. 49.  et al. 2013. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503:290–94 [Google Scholar]
  50. Kalverda B, Pickersgill H, Shloma VV, Fornerod M. 50.  2010. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140:360–71 [Google Scholar]
  51. Kapoor P, Shen X. 51.  2014. Mechanisms of nuclear actin in chromatin-remodeling complexes. Trends Cell Biol. 24:238–46 [Google Scholar]
  52. Kleinjan DA, van Heyningen V. 52.  2005. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76:8–32 [Google Scholar]
  53. Ktistaki E, Garefalaki A, Williams A, Andrews SR, Bell DM. 53.  et al. 2010. CD8 locus nuclear dynamics during thymocyte development. J. Immunol. 184:5686–95 [Google Scholar]
  54. Kurz A, Lampel S, Nickolenko JE, Bradl J, Benner A. 54.  et al. 1996. Active and inactive genes localize preferentially in the periphery of chromosome territories. J. Cell Biol. 135:1195–205 [Google Scholar]
  55. Le Dily F, Bau D, Pohl A, Vicent GP, Serra F. 55.  et al. 2014. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 28:2151–62 [Google Scholar]
  56. Lee HY, Johnson KD, Boyer ME, Bresnick EH. 56.  2011. Relocalizing genetic loci into specific subnuclear neighborhoods. J. Biol. Chem. 286:18834–44 [Google Scholar]
  57. Lewis EB. 57.  1978. A gene complex controlling segmentation in Drosophila. Nature 276:565–70 [Google Scholar]
  58. Li L, Lyu X, Hou C, Takenaka N, Nguyen HQ. 58.  et al. 2015. Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Mol. Cell 58:216–31 [Google Scholar]
  59. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 59.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  60. Mahy NL, Perry PE, Bickmore WA. 60.  2002. Gene density and transcription influence the localization of chromatin outside of chromosome territories detectable by FISH. J. Cell Biol. 159:753–63 [Google Scholar]
  61. Mahy NL, Perry PE, Gilchrist S, Baldock RA, Bickmore WA. 61.  2002. Spatial organization of active and inactive genes and noncoding DNA within chromosome territories. J. Cell Biol. 157:579–89 [Google Scholar]
  62. Malyavantham KS, Bhattacharya S, Alonso WD, Acharya R, Berezney R. 62.  2008. Spatio-temporal dynamics of replication and transcription sites in the mammalian cell nucleus. Chromosoma 117:553–67 [Google Scholar]
  63. Malyavantham KS, Bhattacharya S, Barbeitos M, Mukherjee L, Xu J. 63.  et al. 2008. Identifying functional neighborhoods within the cell nucleus: proximity analysis of early S-phase replicating chromatin domains to sites of transcription, RNA polymerase II, HP1γ, matrin 3 and SAF-A. J. Cell Biochem. 105:391–403 [Google Scholar]
  64. Mitchell JA, Fraser P. 64.  2008. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev. 22:20–25 [Google Scholar]
  65. Mizuguchi T, Fudenberg G, Mehta S, Belton JM, Taneja N. 65.  et al. 2014. Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 516:432–35 [Google Scholar]
  66. Morey C, Kress C, Bickmore WA. 66.  2009. Lack of bystander activation shows that localization exterior to chromosome territories is not sufficient to up-regulate gene expression. Genome Res. 19:1184–94 [Google Scholar]
  67. Mukherjee S, Erickson H, Bastia D. 67.  1988. Detection of DNA looping due to simultaneous interaction of a DNA-binding protein with two spatially separated binding sites on DNA. PNAS 85:6287–91 [Google Scholar]
  68. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I. 68.  et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–85 [Google Scholar]
  69. Nowak G, Pestic-Dragovich L, Hozak P, Philimonenko A, Simerly C. 69.  et al. 1997. Evidence for the presence of myosin I in the nucleus. J. Biol. Chem. 272:17176–81 [Google Scholar]
  70. Ong CT, Van Bortle K, Ramos E, Corces VG. 70.  2013. Poly(ADP-ribosyl)ation regulates insulator function and intrachromosomal interactions in Drosophila. Cell 155:148–59 [Google Scholar]
  71. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A. 71.  et al. 2004. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 36:1065–71 [Google Scholar]
  72. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL. 72.  et al. 2007. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLOS Biol. 5:e192 [Google Scholar]
  73. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S. 73.  et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–33 [Google Scholar]
  74. Park SK, Xiang Y, Feng X, Garrard WT. 74.  2014. Pronounced cohabitation of active immunoglobulin genes from three different chromosomes in transcription factories during maximal antibody synthesis. Genes Dev. 28:1159–64 [Google Scholar]
  75. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I. 75.  et al. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38:603–13 [Google Scholar]
  76. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B. 76.  2006. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38:1005–14 [Google Scholar]
  77. Ragoczy T, Telling A, Sawado T, Groudine M, Kosak ST. 77.  2003. A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements. Chromosome Res. 11:513–25 [Google Scholar]
  78. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID. 78.  et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–80 [Google Scholar]
  79. Reddy KL, Zullo JM, Bertolino E, Singh H. 79.  2008. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452:243–47 [Google Scholar]
  80. Riddiford LM, Cherbas P, Truman JW. 80.  2000. Ecdysone receptors and their biological actions. Vitam. Horm. 60:1–73 [Google Scholar]
  81. Rieder D, Ploner C, Krogsdam AM, Stocker G, Fischer M. 81.  et al. 2014. Co-expressed genes prepositioned in spatial neighborhoods stochastically associate with SC35 speckles and RNA polymerase II factories. Cell Mol. Life Sci. 71:1741–59 [Google Scholar]
  82. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN. 82.  et al. 2008. CTCF physically links cohesin to chromatin. PNAS 105:8309–14 [Google Scholar]
  83. Sanjana NE, Cong L, Zhou Y, Cunniff M, Feng G. 83.  2012. A transcription activator-like effector (TALE) toolbox for genome engineering. Nat. Protoc. 7:1171–92 [Google Scholar]
  84. Sanyal A, Lajoie BR, Jain G, Dekker J. 84.  2012. The long-range interaction landscape of gene promoters. Nature 489:109–13 [Google Scholar]
  85. Schardin M, Cremer T, Hager HD, Lang M. 85.  1985. Specific staining of human chromosomes in Chinese hamster × man hybrid cell lines demonstrates interphase chromosome territories. Hum. Genet. 71:281–87 [Google Scholar]
  86. Scheuermann MO, Tajbakhsh J, Kurz A, Saracoglu K, Eils R, Lichter P. 86.  2004. Topology of genes and nontranscribed sequences in human interphase nuclei. Exp. Cell Res. 301:266–79 [Google Scholar]
  87. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A. 87.  et al. 2010. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42:53–61 [Google Scholar]
  88. Sexton T, Cavalli G. 88.  2015. The role of chromosome domains in shaping the functional genome. Cell 160:1049–59 [Google Scholar]
  89. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B. 89.  et al. 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148:458–72 [Google Scholar]
  90. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. 90.  2005. Interchromosomal associations between alternatively expressed loci. Nature 435:637–45 [Google Scholar]
  91. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, Lieberman PM. 91.  2008. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 27:654–66 [Google Scholar]
  92. Tanabe H, Habermann FA, Solovei I, Cremer M, Cremer T. 92.  2002. Non-random radial arrangements of interphase chromosome territories: evolutionary considerations and functional implications. Mutat. Res. 504:37–45 [Google Scholar]
  93. Tanabe H, Muller S, Neusser M, von Hase J, Calcagno E. 93.  et al. 2002. Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. PNAS 99:4424–29 [Google Scholar]
  94. Tark-Dame M, Jerabek H, Manders EM, Heermann DW, van Driel R. 94.  2014. Depletion of the chromatin looping proteins CTCF and cohesin causes chromatin compaction: insight into chromatin folding by polymer modelling. PLOS Comput. Biol. 10:e1003877 [Google Scholar]
  95. Van Bortle K, Nichols MH, Li L, Ong CT, Takenaka N. 95.  et al. 2014. Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol. 15:R82 [Google Scholar]
  96. Vernimmen D, De Gobbi M, Sloane-Stanley JA, Wood WG, Higgs DR. 96.  2007. Long-range chromosomal interactions regulate the timing of the transition between poised and active gene expression. EMBO J. 26:2041–51 [Google Scholar]
  97. Verschure PJ, Van Der Kraan I, Enserink JM, Mone MJ, Manders EM, Van Driel R. 97.  2002. Large-scale chromatin organization and the localization of proteins involved in gene expression in human cells. J. Histochem. Cytochem. 50:1303–12 [Google Scholar]
  98. Verschure PJ, van Der Kraan I, Manders EM, van Driel R. 98.  1999. Spatial relationship between transcription sites and chromosome territories. J. Cell Biol. 147:13–24 [Google Scholar]
  99. Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J. 99.  et al. 2000. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J. Cell Sci. 113:Pt. 91565–76 [Google Scholar]
  100. Wasser M, Chia W. 100.  2000. The EAST protein of Drosophila controls an expandable nuclear endoskeleton. Nat. Cell Biol. 2:268–75 [Google Scholar]
  101. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B. 101.  et al. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801 [Google Scholar]
  102. Williams RR, Broad S, Sheer D, Ragoussis J. 102.  2002. Subchromosomal positioning of the epidermal differentiation complex (EDC) in keratinocyte and lymphoblast interphase nuclei. Exp. Cell Res. 272:163–75 [Google Scholar]
  103. Wood AM, Van Bortle K, Ramos E, Takenaka N, Rohrbaugh M. 103.  et al. 2011. Regulation of chromatin organization and inducible gene expression by a Drosophila insulator. Mol. Cell 44:29–38 [Google Scholar]
  104. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J. 104.  et al. 2004. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 36:1105–10 [Google Scholar]
  105. Zirbel RM, Mathieu UR, Kurz A, Cremer T, Lichter P. 105.  1993. Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Res. 1:93–106 [Google Scholar]
  106. Zuin J, Dixon JR, van der Reijden MI, Ye Z, Kolovos P. 106.  et al. 2014. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. PNAS 111:996–1001 [Google Scholar]
  107. Zullo JM, Demarco IA, Pique-Regi R, Gaffney DJ, Epstein CB. 107.  et al. 2012. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149:1474–87 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-055008
Loading
/content/journals/10.1146/annurev-genet-112414-055008
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