1932

Abstract

In vivo, the human genome functions as a complex, folded, three-dimensional chromatin polymer. Understanding how the human genome is spatially organized and folded inside the cell nucleus is therefore central to understanding how genes are regulated in normal development and dysregulated in disease. Established light microscopy–based approaches and more recent molecular chromosome conformation capture methods are now combining to give us unprecedented insight into this fascinating aspect of human genomics.

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2013-08-31
2024-06-18
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Literature Cited

  1. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T. 1.  2009. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev. Cell 16:47–57 [Google Scholar]
  2. Baù D, Sanyal A, Lajoie BR, Capriotti E, Byron M. 2.  et al. 2011. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 18:107–14 [Google Scholar]
  3. Benko S, Fantes JA, Amiel J, Kleinjan D-J, Thomas S. 3.  et al. 2009. Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat. Genet. 41:359–64 [Google Scholar]
  4. Berman BP, Weisenberger DJ, Aman JF, Hinoue T, Ramjan Z. 4.  et al. 2011. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nat. Genet. 44:40–46 [Google Scholar]
  5. Bickmore WA, Teague P. 5.  2002. Influences of chromosome size, gene density and nuclear position on the frequency of constitutional translocations in the human population. Chromosome Res. 10:707–15 [Google Scholar]
  6. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K. 6.  et al. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 3:e157 [Google Scholar]
  7. Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA. 7.  2001. The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet. 10:211–19 [Google Scholar]
  8. Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA. 8.  2011. Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res. 19:901–9Describes a new method that allows for the generation of custom, repeat-free FISH probes to investigate human genome organization. [Google Scholar]
  9. Branco MR, Pombo A. 9.  2006. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 4:e138 [Google Scholar]
  10. Breger KS, Smith L, Thayer MJ. 10.  2005. Engineering translocations with delayed replication: evidence for cis control of chromosome replication timing. Hum. Mol. Genet. 14:2813–27 [Google Scholar]
  11. Bridger JM, Boyle S, Kill IR, Bickmore WA. 11.  2000. Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr. Biol. 10:149–52 [Google Scholar]
  12. Brown JM, Green J, das Neves RP, Wallace HAC, Smith AJH. 12.  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]
  13. Brown JM, Leach J, Reittie JE, Atzberger A, Lee-Prudhoe J. 13.  et al. 2006. Coregulated human globin genes are frequently in spatial proximity when active. J. Cell Biol. 172:177–87 [Google Scholar]
  14. Cao K, Capell BC, Erdos MR, Djabali K, Collins FS. 14.  2007. A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc. Natl. Acad. Sci. USA 104:4949–54 [Google Scholar]
  15. Chambeyron S, Bickmore WA. 15.  2004. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18:1119–30 [Google Scholar]
  16. Chambeyron S, Da Silva NR, Lawson KA, Bickmore WA. 16.  2005. Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Development 132:2215–23 [Google Scholar]
  17. Cornforth MN, Greulich-Bode KM, Loucas BD, Arsuaga J, Vázquez M. 17.  et al. 2002. Chromosomes are predominantly located randomly with respect to each other in interphase human cells. J. Cell Biol. 159:237–44 [Google Scholar]
  18. Craig JM, Bickmore WA. 18.  1993. Chromosome bands—flavours to savour. BioEssays 15:349–54 [Google Scholar]
  19. Cremer M, von Hase J, Volm T, Brero A, Kreth G. 19.  et al. 2001. Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res. 9:541–67 [Google Scholar]
  20. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. 20.  1999. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145:1119–31 [Google Scholar]
  21. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK. 21.  et al. 2008. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22:832–53 [Google Scholar]
  22. Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA. 22.  et al. 2007. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc. Natl. Acad. Sci. USA 104:4955–60 [Google Scholar]
  23. de Laat W, Klous P, Kooren J, Noordermeer D, Palstra R-J. 23.  et al. 2008. Three-dimensional organization of gene expression in erythroid cells. Curr. Top. Dev. Biol. 82:117–39 [Google Scholar]
  24. Deng W, Lee J, Wang H, Miller J, Reik A. 24.  et al. 2012. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 149:1233–44Provides the first demonstration of the targeted reengineering of chromatin looping. [Google Scholar]
  25. Deniaud E, Bickmore WA. 25.  2009. Transcription and the nuclear periphery: edge of darkness?. Curr. Opin. Genet. Dev. 19:187–91 [Google Scholar]
  26. Desprat R, Thierry-Mieg D, Lailler N, Lajugie J, Schildkraut C. 26.  et al. 2009. Predictable dynamic program of timing of DNA replication in human cells. Genome Res. 19:2288–99 [Google Scholar]
  27. de Wit E, de Laat W. 27.  2012. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26:11–24 [Google Scholar]
  28. Dietzel S, Jauch A, Kienle D, Qu G, Holtgreve-Grez H. 28.  et al. 1998. Separate and variably shaped chromosome arm domains are disclosed by chromosome arm painting in human cell nuclei. Chromosome Res. 6:25–33 [Google Scholar]
  29. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y. 29.  et al. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–80Uses deep sequencing of complex Hi-C libraries to identify sub-megabase-size domains in the mammalian genome within which sequences preferentially associate with one another. [Google Scholar]
  30. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL. 30.  et al. 2006. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16:1299–309 [Google Scholar]
  31. Driscoll MC, Dobkin CS, Alter BP. 31.  1989. γδβ-Thalassemia due to a de novo mutation deleting the 5′ β-globin gene activation-region hypersensitive sites. Proc. Natl. Acad. Sci. USA 86:7470–74 [Google Scholar]
  32. Ecker JR, Bickmore WA, Barroso I, Pritchard JK, Gilad Y, Segal E. 32.  2012. Genomics: ENCODE explained. Nature 489:52–55 [Google Scholar]
  33. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S. 33.  et al. 2010. Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol. Cell 38:452–64 [Google Scholar]
  34. Ferreira J, Paolella G, Ramos C, Lamond AI. 34.  1997. Spatial organization of large-scale chromatin domains in the nucleus: a magnified view of single chromosome territories. J. Cell Biol. 139:1597–610 [Google Scholar]
  35. Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E. 35.  et al. 2008. Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 4:e1000039 [Google Scholar]
  36. Fuss SH, Omura M, Mombaerts P. 36.  2007. Local and cis effects of the H element on expression of odorant receptor genes in mouse. Cell 1302:373–84 [Google Scholar]
  37. Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter NP, Bickmore WA. 37.  2004. Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers. Cell 118:555–66 [Google Scholar]
  38. Gilchrist S, Gilbert N, Perry P, Bickmore WA. 38.  2004. Nuclear organization of centromeric domains is not perturbed by inhibition of histone deacetylases. Chromosome Res. 12:505–16 [Google Scholar]
  39. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB. 39.  et al. 2008. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–51 [Google Scholar]
  40. Hakim O, Sung M-H, Voss TC, Splinter E, John S. 40.  et al. 2011. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 21:697–706 [Google Scholar]
  41. Hansen RS, Thomas S, Sandstrom R, Canfield TK, Thurman RE. 41.  et al. 2010. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. USA 107:139–44 [Google Scholar]
  42. Harewood L, Schütz F, Boyle S, Perry P, Delorenzi M. 42.  et al. 2010. The effect of translocation-induced nuclear reorganization on gene expression. Genome Res. 20:554–64 [Google Scholar]
  43. Hewitt SL, High FA, Reiner SL, Fisher AG, Merkenschlager M. 43.  2004. Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur. J. Immunol. 34:3604–13 [Google Scholar]
  44. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M. 44.  et al. 2008. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6:e245 [Google Scholar]
  45. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. 45.  2011. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechol. 30:90–98 [Google Scholar]
  46. Kizilyaprak C, Spehner D, Devys D, Schultz P. 46.  2011. The linker histone H1C contributes to the SCA7 nuclear phenotype. Nucleus 2:444–54 [Google Scholar]
  47. Kleinjan DA, van Heyningen V. 47.  2005. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76:8–32 [Google Scholar]
  48. Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM. 48.  et al. 2002. Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296:158–62 [Google Scholar]
  49. Kubben N, Adriaens M, Meuleman W, Voncken JW, van Steensel B, Misteli T. 49.  2012. Mapping of lamin A- and progerin-interacting genome regions. Chromosoma 121:447–64 [Google Scholar]
  50. Kumaran RI, Spector DL. 50.  2008. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 180:51–65 [Google Scholar]
  51. Küpper K, Kölbl A, Biener D, Dittrich S, von Hase J. 51.  et al. 2007. Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116:285–306 [Google Scholar]
  52. Lettice LA, Hill RE. 52.  2005. Preaxial polydactyly: a model for defective long-range regulation in congenital abnormalities. Curr. Opin. Genet. Dev. 15:294–300 [Google Scholar]
  53. Lettice LA, Williamson I, Wiltshire JH, Peluso S, Devenney PS. 53.  et al. 2012. Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 22:459–67 [Google Scholar]
  54. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T. 54.  et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–93 [Google Scholar]
  55. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R. 55.  2006. Interchromosomal interactions and olfactory receptor choice. Cell 126:403–13 [Google Scholar]
  56. Mahy NL, Perry PE, Bickmore WA. 56.  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]
  57. Marquès-Bonet T, Cáceres M, Bertranpetit J, Preuss TM, Thomas JW, Navarro A. 57.  2004. Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees. Trends Genet. 20:524–29 [Google Scholar]
  58. Maurano MT, Humbert R, Rynes E, Thurman RE, Haugen E. 58.  et al. 2012. Systematic localization of common disease-associated variation in regulatory DNA. Science 337:1190–95 [Google Scholar]
  59. Meaburn KJ, Cabuy E, Bonne G, Lévy N, Morris GE. 59.  et al. 2007. Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6:139–53 [Google Scholar]
  60. Mehta IS, Amira M, Harvey AJ, Bridger JM. 60.  2010. Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol. 11:R5 [Google Scholar]
  61. Mehta IS, Eskiw CH, Arican HD, Kill IR, Bridger JM. 61.  2011. Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford progeria syndrome cells. Genome Biol. 12:R74 [Google Scholar]
  62. Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L. 62.  et al. 2011. A regulatory archipelago controls Hox genes transcription in digits. Cell 147:1132–45 [Google Scholar]
  63. Morey C, Da Silva NR, Perry P, Bickmore WA. 63.  2007. Nuclear reorganisation and chromatin decondensation are conserved, but distinct, mechanisms linked to Hox gene activation. Development 134:909–19 [Google Scholar]
  64. Morey C, Kress C, Bickmore WA. 64.  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]
  65. Müller I, Boyle S, Singer RH, Bickmore WA, Chubb JR. 65.  2010. Stable morphology, but dynamic internal reorganisation, of interphase human chromosomes in living cells. PLoS ONE 5:e11560 [Google Scholar]
  66. Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D. 66.  et al. 2010. Initial genomics of the human nucleolus. PLoS Genet. 6:e1000889 [Google Scholar]
  67. Neusser M, Schubel V, Koch A, Cremer T, Müller S. 67.  2007. Evolutionarily conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates. Chromosoma 116:307–20 [Google Scholar]
  68. Nishizumi H, Kumasaka K, Inoue N, Nakashima A, Sakano H. 68.  2007. Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis. Proc. Natl. Acad. Sci. USA 104:20067–72 [Google Scholar]
  69. Noordermeer D, Branco MR, Splinter E, Klous P, van Ijcken W. 69.  et al. 2008. Transcription and chromatin organization of a housekeeping gene cluster containing an integrated β-globin locus control region. PLoS Genet. 4:e1000016 [Google Scholar]
  70. Noordermeer D, de Wit E, Klous P, van de Werken H, Simonis M. 70.  et al. 2011. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat. Cell Biol. 13:944–51Shows that 3D associations in the nucleus with endogenous globin loci can result in transactivation of gene expression in “jackpot” cells. [Google Scholar]
  71. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I. 71.  et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–85Uses 5C analysis of a portion of the mouse X chromosome to reveal TADs that appear to be similar to those identified in Ref. 29. [Google Scholar]
  72. O'Keefe RT, Henderson SC, Spector DL. 72.  1992. Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J. Cell Biol. 116:1095–110 [Google Scholar]
  73. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL. 73.  et al. 2007. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol. 5:e192 [Google Scholar]
  74. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SWM, Solovei I. 74.  et al. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38:603–13Uses DamID to show that some associations of the genome with lamin B1 are modulated cumulatively during differentiation. [Google Scholar]
  75. Pope BD, Chandra T, Buckley Q, Hoare M, Ryba T. 75.  et al. 2012. Replication-timing boundaries facilitate cell-type and species-specific regulation of a rearranged human chromosome in mouse. Hum. Mol. Genet. 21:4162–70 [Google Scholar]
  76. Reddy KL, Zullo JM, Bertolino E, Singh H. 76.  2008. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452:243–47 [Google Scholar]
  77. Roix JJ, McQueen PG, Munson PJ, Parada LA, Misteli T. 77.  2003. Spatial proximity of translocation-prone gene loci in human lymphomas. Nat. Genet. 34:287–91 [Google Scholar]
  78. Ryba T, Battaglia D, Chang BH, Shirley JW, Buckley Q. 78.  et al. 2012. Abnormal developmental control of replication-timing domains in pediatric acute lymphoblastic leukemia. Genome Res. 22:1833–44 [Google Scholar]
  79. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M. 79.  et al. 2010. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 20:761–70 [Google Scholar]
  80. Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T. 80.  2005. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132:797–803 [Google Scholar]
  81. Sanyal A, Lajoie BR, Jain G, Dekker J. 81.  2012. The long-range interaction landscape of gene promoters. Nature 489:109–13 [Google Scholar]
  82. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A. 82.  et al. 2010. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42:53–61 [Google Scholar]
  83. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B. 83.  et al. 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148:458–72 [Google Scholar]
  84. Shopland LS, Lynch CR, Peterson KA, Thornton K, Kepper N. 84.  et al. 2006. Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J. Cell Biol. 174:27–38 [Google Scholar]
  85. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R. 85.  et al. 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture–on-chip (4C). Nat. Genet. 38:1348–54 [Google Scholar]
  86. Solovei I, Kreysing M, Lanctôt C, Kösem S, Peichl L. 86.  et al. 2009. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–68Demonstrates that the usual radial organization of the mammalian nucleus is dramatically inverted in the photoreceptor cells of nocturnal animals after birth. [Google Scholar]
  87. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S. 87.  et al. 2013. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152:584–98 [Google Scholar]
  88. Splinter J, de Wit E, Nora EP, Klous P, van de Werken HJ. 88.  et al. 2011. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 25:1371–83 [Google Scholar]
  89. Strickfaden H, Zunhammer A, van Koningsbruggen S, Köhler D, Cremer T. 89.  2010. 4D chromatin dynamics in cycling cells: Theodor Boveri's hypotheses revisited. Nucleus 1:284–97 [Google Scholar]
  90. Sutherland H, Bickmore WA. 90.  2009. Transcription factories: gene expression in unions?. Nat. Rev. Genet. 10:457–66 [Google Scholar]
  91. Thomson I, Gilchrist S, Bickmore WA, Chubb JR. 91.  2004. The radial positioning of chromatin is not inherited through mitosis but is established de novo in early G1. Curr. Biol. 14:166–72 [Google Scholar]
  92. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT. 92.  et al. 2012. The accessible chromatin landscape of the human genome. Nature 489:75–82 [Google Scholar]
  93. Tolhuis B, Blom M, Kerkhoven RM, Pagie L, Teunissen H. 93.  et al. 2011. Interactions among Polycomb domains are guided by chromosome architecture. PLoS Genet. 7:e1001343Uses fly genetics to elegantly show that the extent of associations between different Polycomb target regions is strongly influenced by the overall chromatin architecture. [Google Scholar]
  94. van de Corput MPC, de Boer E, Knoch TA, van Cappellen WA, Quintanilla A. 94.  et al. 2012. Super-resolution imaging reveals 3D folding dynamics of the β-globin locus upon gene activation. J. Cell Sci. 125:4630–39 [Google Scholar]
  95. van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton GJ. 95.  et al. 2010. High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 21:3735–48 [Google Scholar]
  96. Visser M, Kayser M, Palstra R-J. 96.  2012. HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter. Genome Res. 22:446–55 [Google Scholar]
  97. Walter J, Schermelleh L, Cremer M, Tashiro S, Cremer T. 97.  2003. Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J. Cell Biol. 160:685–97 [Google Scholar]
  98. Weierich C, Brero A, Stein S, von Hase J, Cremer C. 98.  et al. 2003. Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res. 11:485–502 [Google Scholar]
  99. Williams RRE, Azuara V, Perry P, Sauer S, Dvorkina M. 99.  et al. 2006. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119:132–40 [Google Scholar]
  100. Williamson I, Eskeland R, Lettice LA, Hill AE, Boyle S. 100.  et al. 2012. Anterior-posterior differences in HoxD chromatin topology in limb development. Development 139:3157–67 [Google Scholar]
  101. Würtele H, Chartrand P. 101.  2006. Genome-wide scanning of HoxB1-associated loci in mouse ES cells using an open-ended Chromosome Conformation Capture methodology. Chromosome Res. 14:477–95 [Google Scholar]
  102. Yaffe E, Tanay A. 102.  2011. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 43:1059–65 [Google Scholar]
  103. Yokota H, Singer MJ, van den Engh GJ, Trask BJ. 103.  1997. Regional differences in the compaction of chromatin in human G0/G1 interphase nuclei. Chromosome Res. 5:157–66 [Google Scholar]
  104. Zhang X, Cowper-Sal·lari R, Bailey SD, Moore JH, Lupien M. 104.  2012. Integrative functional genomics identifies an enhancer looping to the SOX9 gene disrupted by the 17q24.3 prostate cancer risk locus. Genome Res. 22:1437–46 [Google Scholar]
  105. Zhang Y, McCord RP, Ho Y-J, Lajoie BR, Hildebrand DG. 105.  et al. 2012. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148:908–21 [Google Scholar]
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