Something silent this way forms: The functional organization of the repressive nuclear compartment

Annual Review of Cell and Developmental Biology

Volumn 29, Issue , 2013, Pages 241-270

  Politz, Joan C Ritland ^a   Scalzo, David ^a   Groudine, Mark ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

chromatin organization; heterochromatin; nuclear organization; nuclear periphery; nucleolus

Indexed keywords

RIBOSOME RNA; UNTRANSLATED RNA; HETEROCHROMATIN;

CELL DIFFERENTIATION; CELL DIVISION; CELL NUCLEUS; CELL TYPE; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE REPRESSION; HETEROCHROMATIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA TRANSCRIPTION; TELOMERE; TRANSPOSON; ANIMAL; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

ANIMALS; CELL NUCLEUS; GENE SILENCING; HETEROCHROMATIN; HUMANS; TRANSCRIPTION, GENETIC;

EID: 84885774880     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-101512-122317     Document Type: Review

References (200)

1. Aguirre-Lavin T, Adenot P, Bonnet-Garnier A, Lehmann G, Fleurot R, et al. 2012. 3D-FISH analysis of embryonic nuclei inmouse highlights several abrupt changes of nuclear organization during preimplantation development. BMC Dev. Biol. 12:30
2. Ahmed K,Dehghani H, Rugg-Gunn P, Fussner E, Rossant J, Bazett-JonesDP. 2010. Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS ONE 5:e10531
3. Alexander RP, Fang G, Rozowsky J, Snyder M, Gerstein MB. 2010. Annotating non-coding regions of the genome. Nat. Rev. Genet. 11:559-71
4. Aravin AA, Hannon GJ. 2008. Small RNA silencing pathways in germ and stem cells. Cold Spring Harb. Symp. Quant. Biol. 73:283-90
5. Bailey JA, Eichler EE. 2006. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat. Rev. Genet. 7:552-64
6. Bantignies F, Cavalli G. 2006. Cellular memory and dynamic regulation of polycomb group proteins. Curr. Opin. Cell Biol. 18:275-83
7. Bantignies F, Roure V, Comet I, Leblanc B, Schuettengruber B, et al. 2011. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144:214-26
8. Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, et al. 2010. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 18:436-47
9. Black JC, Van Rechem C, Whetstine JR. 2012. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol. Cell 48:491-507
10. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, et al. 2005. Three-dimensionalmaps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 3:e157
11. Brand M, Ranish JA, Kummer NT, Hamilton J, Igarashi K, et al. 2004. Dynamic changes in transcription factor complexes during erythroid differentiation revealed by quantitative proteomics. Nat. Struct. Mol. Biol. 11:73-80
12. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, et al. 2005. Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J. Cell Biol. 169:733-43
13. Brickner DG, Ahmed S, Meldi L, Thompson A, Light W, et al. 2012. Transcription factor binding to a DNA zip code controls interchromosomal clustering at the nuclear periphery. Dev. Cell 22:1234-46
14. Brockdorff N. 2013. Noncoding RNA and polycomb recruitment. RNA 19:429-42
15. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG. 1999. Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol. Cell 3:207-17
16. Burke B, Stewart CL. 2013. The nuclear lamins: flexibility in function. Nat. Rev. Mol. Cell Biol. 14:13-24
17. Butin-Israeli V, Adam SA, Goldman AE, Goldman RD. 2012. Nuclear lamin functions and disease. Trends Genet. 28:464-71
18. Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, et al. 2012. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149:819-31
19. Capelson M, Corces VG. 2005. The ubiquitin ligased Topors directs the nuclear organization of a chromatin insulator. Mol. Cell 20:105-16
20. Chalopin D, Galiana D, Volff J-N. 2012. Genetic innovation in vertebrates: Gypsy integrase genes and other genes derived from transposable elements. Int. J. Evol. Biol. 2012:724519
21. Chandra T, Kirschner K,Thuret J-Y, Pope BD, Ryba T, et al. 2012. Independence of repressive histonemarks and chromatin compaction during senescent heterochromatic layer formation. Mol. Cell 47:203-14
22. Cheutin T, Cavalli G. 2012. Progressive polycomb assembly on H3K27me3 compartments generates polycomb bodies with developmentally regulated motion. PLoS Genet. 8:e1002465
23. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY. 2011. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell 44:667-78
24. Chuang C-H, Belmont AS. 2007. Moving chromatin within the interphase nucleus-controlled transitions? Semin. Cell Dev. Biol. 18:698-706
25. Chung JH, Whiteley M, Felsenfeld G. 1993. A 5 element of the chickenß-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74:505-14
26. Clowney EJ, Le Gros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC, et al. 2012. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151:724-37
27. Cobb BS, Morales-Alcelay S, Kleiger G, Brown KE, Fisher AG, Smale ST. 2000. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 14:2146-60
28. Cremer T, Cremer M. 2010. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2:a003889
29. Csink AK, Henikoff S. 1996. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381:529-31
30. Cva?cková Z, Ma?sata M, Stan?ek D, Fidlerová H, Ra?ska I. 2009. Chromatin position in human HepG2 cells: although being non-random, significantly changed in daughter cells. J. Struct. Biol. 165:107-17
31. Dasilva C, Hadji H, Ozouf-Costaz C, Nicaud S, Jaillon O, et al. 2002. Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome. Proc. Natl. Acad. Sci. USA 99:13636-41
32. De Wit E, De Laat W. 2012. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26:11-24
33. Dechat T, Gajewski A, Korbei B, Gerlich D, Daigle N, et al. 2004. LAP2a and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J. Cell Sci. 117:6117-28
34. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, et al. 2008. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22:832-53
35. Demmerle J, Koch AJ, Holaska JM. 2012. The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J. Biol. Chem. 287:22080-88
36. Dernburg AF, Fung JC, Broman KW, Marshall WF, Philips J, et al. 1996. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85:745-59
37. Dimitri P. 2004. Fluorescent in situ hybridization with transposable element probes to mitotic chromosomal heterochromatin of Drosophila. Methods Mol. Biol. 260:29-39
38. 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
39. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, et al. 2012. Landscape of transcription in human cells. Nature 489:101-8
40. Dmitrova DS. 2011. DNA replication initiation patterns and spatial dynamics of the human ribosomal RNA gene loci. J. Cell Sci. 124:2743-52
41. Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, et al. 2010. Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet. 6:e1001150
42. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, et al. 2010. A three-dimensional model of the yeast genome. Nature 465:363-67
43. Efroni S, Duttagupta R, Cheng J, Dehghani H, Hoeppner DJ, et al. 2008. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2:437-47
44. Egan ED, Collins K. 2012. Biogenesis of telomerase ribonucleoproteins. RNA 18:1747-59
45. Fedoriw AM, Starmer J, Yee D, Magnuson T. 2012. Nucleolar association and transcriptional inhibition through 5S rDNA in mammals. PLoS Genet. 8:e1002468
46. Fedoroff N. 2012. Transposable elements, epigenetics, and genome evolution. Science 338:758-67
47. Felsenfeld G, Dekker J. 2012. Genome architecture and expression. Curr. Opin. Genet. Dev. 22:59-61
48. Ferreira J, Carmo-Fonseca M. 1997. Genome replication in early mouse embryos follows a defined temporal and spatial order. J. Cell Sci. 110:889-97
49. Filion GJ, Van Bemmel JG, Braunschweig U, Talhout W, Kind J, et al. 2010. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143:212-24
50. Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E, et al. 2008. Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 4:e1000039
51. Follmer NE,Wani AH, Francis NJ. 2012. A polycomb group protein is retained at specific sites on chromatin in mitosis. PLoS Genet. 8:e1003135
52. Foltz DR, Jansen LET, Black BE, Bailey AO, Yates JR, Cleveland DW. 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8:458-69
53. Gard S, Light W, Xiong B, Bose T, McNairn AJ, et al. 2009. Cohesinopathy mutations disrupt the subnuclear organization of chromatin. J. Cell Biol. 187:455-62
54. Gehlen LR,Gruenert G, Jones MB, Rodley CD, Langowski J,O'Sullivan JM. 2012. Chromosome positioning and the clustering of functionally related loci in yeast is driven by chromosomal interactions. Nucleus 3:370-83
55. Gent JI, Dawe RK. 2012. RNA as a structural and regulatory component of the centromere. Annu. Rev. Genet. 46:443-53
56. Gerasimova T, Byrd K, Corces VG. 2000. A chromatin insulator determines the nuclear localization of DNA. Mol. Cell 6:1025-35
57. Gerlich D, Beaudouin J, Kalbfuss B, Daigle N, Eils R, Ellenberg J. 2003. Global chromosome positions are transmitted through mitosis in mammalian cells. Cell 112:751-64
58. Gibcus JH, Dekker J. 2013. The hierarchy of the 3D genome. Mol. Cell 49:773-82
59. Gilbert DM, Gasser SM. 2006. DNA replication and nuclear architecture. In DNA Replication and Human Disease, ed. MI De Pamphilis, pp. 175-96. Cold Spring Harb., NY: Cold Spring Harb. Lab.
60. Press Goldowitz D, Mullen RJ. 1982. Nuclear morphology of ichthyosis mutant mice as a cell marker in chimeric brain. Dev. Biol. 89:261-67
61. Gottschling DE, Aparicio OM, Billington BL, Zakian VA. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751-62
62. Grimaud C, Bantignies F, Pal-Bhadra M, Ghana P, Bhadra U, Cavalli G. 2006. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124:957-71
63. 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
64. Guetg C, Lienemann P, Sirri V, Grummt I, Hernandez-Verdun D, et al. 2010. The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO J. 29:2135-46
65. Haeusler RA, Engelke DR. 2006. Spatial organization of transcription by RNA polymerase III. Nucleic Acids Res. 34:4826-36
66. Halic M, Moazed D. 2010. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140:504-16
67. Hathaway NA, Bell O, Hodges C, Miller EL, Neel DS, Crabtree GR. 2012. Dynamics and memory of heterochromatin in living cells. Cell 149:1447-60
68. He B, Caudy A, Parsons L, Rosebrock A, Pane A, et al. 2012. Mapping the pericentric heterochromatin by comparative genomic hybridization analysis and chromosome deletions in Drosophila melanogaster. Genome Res. 22:2507-19
69. Heitz E. 1928. Das Heterochromatin Der Moose. Jahrb. Wiss. Bot. 69:762-818
70. Henikoff S, Furuyama T. 2010. Epigenetic inheritance of centromeres. Cold Spring Harb. Symp. Quant. Biol. 75:51-60
71. Hernandez-Verdun D. 2006. Nucleolus: from structure to dynamics. Histochem. Cell Biol. 125:127-37
72. Heun P, Laroche T, Shimada K, Furrer P, Gasser SM. 2001. Chromosome dynamics in the yeast interphase nucleus. Science 294:2181-86
73. Hewitt SL, Farmer D, Marszalek K, Cadera E, Liang H-E, et al. 2008. Association between the Igk and IgH immunoglobulin loci mediated by the 3 Igk enhancer induces ?decontraction? of the IgH locus in pre-B cells. Nat. Immmunol. 9:396-404
74. Hewitt SL, Yin B, Ji Y, Chaumeil J, Marszalek K, et al. 2009. RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci. Nat. Immunol. 10:655-64
75. Hubner MR, Spector DL. 2010. Chromatin dynamics. Annu. Rev. Biophys. 39:471-89
76. Ide S,Miyazaki T,Maki H, Kobayashi T. 2010. Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327:693-96
77. Ikegami K, Egelhofer T, Strome S, Lieb J. 2010. Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biol. 11:R120
78. Imakaev M, Fudenberg G, McCord RP, Naumova N, Goloborodko A, et al. 2012. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 9:999-1003
79. Joffe B, Leonhardt H, Solovei I. 2010. Differentiation and large scale spatial organization of the genome. Curr. Opin. Genet. Dev. 20:562-69
80. Johnson JM, Edwards S, Shoemaker D, Schadt EE. 2005. Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet. 21:93-102
81. Jost KL, Bertulat B, Cardoso MC. 2012. Heterochromatin and gene positioning: inside, outside, any side? Chromosoma 121:555-63
82. Kalitsis P, Griffiths B, Choo KH. 2006. Mouse telocentric sequences reveal a high rate of homogenization and possible role in Robertsonian translocation. Proc. Natl. Acad. Sci. USA 103:8786-91
83. Kanhere A, Viiri K,Araújo CC, Rasaiyaah J, Bouwman RD, et al. 2010. Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol. Cell 38:675-88
84. Kellum R, Schedl P. 1992. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol. Cell Biol. 12:2424-31
85. Kind J, Pagie L, Ortabozkoyun H, Boyle S, De Vries SS, et al. 2013. Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178-92
86. Kitada T, Kuryan BG, Tran NNH, Song C, Xue Y, et al. 2012. Mechanism for epigenetic variegation of gene expression at yeast telomeric heterochromatin. Genes Dev. 26:2443-55
87. Kohwi-Shigematsu T, Poterlowicz K, Ordinario E, Han H-J, Botchkarev VA, Kohwi Y. 2012. Genome organizing function of SATB1 in tumor progression. Semin. Cancer Biol. 23:72-79
88. Kosak ST, Scalzo D, Alworth SV, Li F, Palmer S, et al. 2007. Coordinate gene regulation during hematopoiesis is related to genomic organization. PLoS Biol. 5:e309
89. Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM, et al. 2002. Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296:158-62
90. Krijger PH, De Laat W. 2013. Identical cells with different 3D genomes; cause and consequences? Curr. Opin. Genet. Dev. 23:191-96
91. Kubben N, Adriaens M, Meuleman W, Voncken J, Van Steensel B,Misteli T. 2012. Mapping of lamin A-and progerin-interacting genome regions. Chromosoma 121:447-64
92. Kumaran RI, Spector DL. 2008. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 180:51-65
93. Lagger G, O?Carroll D, Rembold M, Khier H, Tischler J, et al. 2002. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 21:2672-81
94. Lanctot C, Cheutin T, Cremer M, Cavalli G, Cremer T. 2007. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8:104-15
95. Lee JT. 2012. Epigenetic regulation by long noncoding RNAs. Science 338:1435-39
96. Lemmers RJLF, Van Der Vliet PJ, Klooster R, Sacconi S, Camaño P, et al. 2010. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329:1650-53
97. Lessard JA, Crabtree GR. 2010. Chromatin regulatory mechanisms in pluripotency. Annu. Rev. Cell Dev. Biol. 26:503-32
98. Leung B, Hermann GJ, Priess JR. 1999. Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216:114-34
99. Leung DC, Lorincz MC. 2012. Silencing of endogenous retroviruses: When and why do histone marks predominate? Trends Biochem. Sci. 37:127-33
100. Li H-B, Ohno K, Gui H, Pirrotta V. 2013. Insulators target active genes to transcription factories and Polycomb-repressed genes to Polycomb bodies. PLoS Genet. 9:e1003436
101. 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 326:289-93
102. Lorenz DR, Mikheyeva IV, Johansen P, Meyer L, Berg A, et al. 2012.CENP-B cooperateswith Set1 in bidirectional transcriptional silencing and genome organization of retrotransposons. Mol. Cell Biol. 32:4215-25
103. Lu J, Gilbert DM. 2007. Proliferation-dependent and cell cycle-regulated transcription of mouse pericentric heterochromatin. J. Cell Biol. 179:411-21
104. Lubeck E, Cai L. 2012. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat. Methods 9:743-48
105. Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, et al. 2012. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:57-63
106. Manuelidis L. 1984. Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences. Proc. Natl. Acad. Sci. USA 81:3123-27
107. Manuelidis L, Borden J. 1988. Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma 96:397-410
108. Marshall WF, Straight A, Marko JF, Swedlow J, Dernburg A, et al. 1997. Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol. 7:930-39
109. Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P. 2006. Genome restructuring in mouse embryos during reprogramming and early development. Dev. Biol. 292:317-32
110. Martin J, Han C,Gordon LA, Terry A, Prabhakar S, et al. 2004. The sequence and analysis of duplication-rich human chromosome 16. Nature 432:988-94
111. Matzat LH, Dale RKM, Nellie, Lei EP. 2012. Tissue-specific regulation of chromatin insulator function. PLoS Genet. 8:e1003069
112. Mayer C, Neubert M, Grummt I. 2008. The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep. 9:774-80
113. Mayer R, Brero A, Von Hase J, Schroeder T, Cremer T, Dietzel S. 2005. Common themes and cell type specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biol. 6:44
114. McClintock B. 1934. The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch. Mikrosk. Anat. 21:294-328
115. Mc Stay B, Grummt I. 2008. The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 24:131-57
116. Mehta I, Amira M, Harvey A, Bridger J. 2010. Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Gen. Biol. 11:R5
117. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM. 2010. The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev. 24:766-82
118. Mekhail K, Seebacher J, Gygi SP,Moazed D. 2008. Role for perinuclear chromosome tethering inmaintenance of genome stability. Nature 456:667-70
119. Melcer S, Hezroni H, Rand E, Nissim-Rafinia M, Skoultchi A, et al. 2012. Histone modifications in lamin A regulate chromatin protein dynamics in early embryonic stem cell differentiation. Nat. Commun. 3:910
120. Meuleman W,Peric-Hupkes D, Kind J, Beaudry J-B, Pagie L, et al. 2013. Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence. Genome Res. 23:270-80
121. Misteli T. 2013. The cell biology of genomes: bringing the double helix to life. Cell 152:1209-12
122. Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, et al. 2010. Initial genomics of the human nucleolus. PLoS Genet. 6:e1000889
123. Neusser M, Schubel V, Koch A, Cremer T, Müller S. 2007. Evolutionarily conserved, cell type and speciesspecific higher order chromatin arrangements in interphase nuclei of primates. Chromosoma 116:307-20
124. Noordermeer D, De Wit E, Klous P, Van De Werken H, Simonis M, et al. 2011. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat. Cell Biol. 13:944-51
125. 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
126. O?Keefe RT, Henderson SC, Spector DL. 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
127. O?Sullivan JM, Sontam DM, Grierson R, Jones B. 2009. Repeated elements coordinate the spatial organization of the yeast genome. Yeast 26:125-38
128. Okano M, Bell DW, Haber DA, Li E 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for De novo methylation and mammalian development. Cell 99:247-57
129. Ottaviani A, Schluth-Bolard C, Rival-Gervier S, Boussouar A, Rondier D, et al. 2009. Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF. EMBO J. 28:2428-36
130. Padeken J, Mendiburo MJ, Chlamydas S, Schwarz H-J, Kremmer E, Heun P. 2013. The nucleoplasmin homolog NLP mediates centromere clustering and anchoring to the nucleolus. Mol. Cell 50:236-49
131. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, et al. 2008. Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol. Cell 32:232-46
132. Papantonis A, Larkin JD, Wada Y, Ohta Y, Ihara S, et al 2010. Active RNA polymerases: mobile or immobile molecular machines? PLoS Biol. 8:e1000419
133. Partridge JF, Borgstr?m B, Allshire RC. 2000. Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 14:783-91
134. Pederson T. 2008. As functional nuclear actin comes into view, is it globular, filamentous, or both? J. Cell Biol. 180:1061-64
135. Peng JC, Karpen GH. 2009. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet. 5:e1000435
136. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SWM, Solovei I, et al. 2010. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38:603-13
137. Phillips JE, Corces VG. 2009. CTCF: master weaver of the genome. Cell 137:1194-211
138. Pidoux AL, Allshire RC. 2005. The role of heterochromatin in centromere function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:569-79
139. Pluta AF, Earnshaw WC. 1996. Specific interaction between human kinetochore protein CENP-C and a nucleolar transcriptional regulator. J. Biol. Chem. 271:18767-74
140. Pollex T, Heard E. 2012. Recent advances in X-chromosome inactivation research. Curr. Opin. Cell Biol. 24:825-32
141. Ponicsan SL, Kugel JF, Goodrich JA. 2010. Genomic gems: SINE RNAs regulate mRNA production. Curr. Opin. Genet. Dev. 20:149-55
142. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, et al. 2010. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev. Cell 19:625-38
143. Raab JR, Chiu J, Zhu J, Katzman S, Kurukuti S, et al. 2012. Human tRNA genes function as chromatin insulators. EMBO J. 31:330-50
144. Ragoczy T, Bender MA, Telling A, Byron R, Groudine M. 2006. The locus control region is required for association of the murineß-globin locus with engaged transcription factories during erythroid maturation. Genes Dev. 20:1447-57
145. Ragoczy T, Telling A, Sawado T, Groudine M, Kosak ST. 2003. A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements. Chromosome Res. 11:513-25
146. Rajapakse I, Groudine M. 2011. On emerging nuclear order. J. Cell Biol. 192:711-21
147. Rajapakse I, Perlman MD, Scalzo D, Kooperberg C, Groudine M, et al. 2009. The emergence of lineagespecific chromosomal topologies from coordinate gene regulation. Proc.Natl. Acad. Sci. USA 106:6679-84
148. Rebollo R, Karimi MM, Bilenky M, Gagnier L, Miceli-Royer K, et al. 2011. Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet. 7:e1002301
149. Reddy KL, Zullo JM, Bertolino E, Singh H. 2008. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452:243-47
150. Reik W, Dean W, Walter J. 2001. Epigenetic reprogramming in mammalian development. Science 293:1089-93
151. Romanova L, Korobova F,Noniashvilli E, Dyban A, Zatsepina O. 2006. High resolution mapping of ribosomal DNA in early mouse embryos by fluorescence in situ hybridization. Biol. Reprod. 74:807-15
152. Santoro R, Li J, Grummt I. 2002. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Genet. 32:393-96
153. Schmidt D, Schwalie PC,Wilson MD, Ballester B,Goncalves A , et al. 2012.Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148:335-48
154. Schmitz K-M, Mayer C, Postepska A, Grummt I. 2010. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24:2264-69
155. Schoeftner S, Blasco MA. 2008. Developmentally regulated transcription of mammalian telomeres by DNAdependent RNA polymerase II. Nat. Cell Biol. 10:228-36
156. Sexton T, Schober H, Fraser P, Gasser SM. 2007. Gene regulation through nuclear organization. Nat. Struct. Mol. Biol. 14:1049-55
157. Sharma S, Kelly TK, Jones PA. 2010. Epigenetics in cancer. Carcinogenesis 31:27-36
158. Shav-Tal Y, Darzacq X, Singer RH. 2006. Gene expression within a dynamic nuclear landscape. EMBO J. 25:3469-79
159. Sienski G, Dönertas D, Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and Maelstrom and its impact on chromatin state and gene expression. Cell 151:964-80
160. Singleton MK, Gonzales ML, Leung KN, Yasui DH, Schroeder DI, et al. 2011. MeCP2 is required for global heterochromatic and nucleolar changes during activity-dependent neuronal maturation. Neurobiol. Dis. 43:190-200
161. Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, et al. 2009. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356-68
162. Solovei I, Schermelleh L, Düring K, Engelhardt A, Stein S, et al. 2004. Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112:410-23
163. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, et al. 2013. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152:584-98
164. Stults DM, Killen MW, Pierce HH, Pierce AJ. 2008. Genomic architecture and inheritance of human ribosomal RNA gene clusters. Genome Res. 18:13-18
165. Su RC, Brown KE, Saaber S, Fisher AG, Merkenschlager M, Smale ST. 2004. Dynamic assembly of silent chromatin during thymocyte maturation. Nat. Genet. 36:502-6
166. Sun X, Le HD, Wahlstrom JM, Karpen GH. 2003. Sequence analysis of a functional Drosophila centromere. Genome Res. 13:182-94
167. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, et al. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:1779-91
168. Taddei A, Gasser SM. 2012. Structure and function in the budding yeast nucleus. Genetics 192:107-29
169. Taddei A, Hediger F, Neumann FR, Bauer C, Gasser SM. 2004. Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J. 23:1301-12
170. Taddei A, Schober H,Gasser SM. 2010. The budding yeast nucleus. Cold Spring Harb. Perspect. Biol. 2:a000612
171. Taddei A, Van Houwe G, Nagai S, Erb I, Van Nimwegen E, Gasser SM. 2009. The functional importance of telomere clustering: Global changes in gene expression result from SIR factor dispersion. Genome Res. 19:611-25
172. Tanaka A, Tanizawa H, Sriswasdi S, Iwasaki O,Chatterjee AG, et al. 2012. Epigenetic regulation of condensinmediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation. Mol. Cell 48:532-46
173. Thompson M, Haeusler RA, Good PD, Engelke DR. 2003. Nucleolar clustering of dispersed tRNA genes. Science 302:1399-401
174. Tjong H, Gong K, Chen L, Alber F. 2012. Physical tethering and volume exclusion determine higher-order genome organization in budding yeast. Genome Res. 22:1295-305
175. Tolhuis B, Blom M, Kerkhoven RM, Pagie L, Teunissen H, et al. 2011. Interactions among polycomb domains are guided by chromosome architecture. PLoS Genet. 7:e1001343
176. Trinh LA, Ferrini R, Cobb BS,Weinmann AS, Hahm K, et al. 2001. Down-regulation of TDT transcription in CD4+CD8+ thymocytes by Ikaros proteins in direct competition with an Ets activator. Genes Dev. 15:1817-32
177. van Koningsbruggen S, Gierliński M, Schofield P, Martin D, Barton GJ, et al. 2010. High-resolution wholegenome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 21:3735-48
178. van Steensel B. 2011. Chromatin: constructing the big picture. EMBO J. 30:1885-95
179. van Steensel B, Dekker J. 2010. Genomics tools for unraveling chromosome architecture. Nat. Biotechnol. 28:1089-95
180. Visa N, Percipalle P. 2010. Nuclear functions of actin. Cold Spring Harb. Perspect. Biol. 2:a000620
181. Vodala S, Abruzzi KC, Rosbash M. 2008. The nuclear exosome and adenylation regulate posttranscriptional tethering of yeast GAL genes to the nuclear periphery. Mol. Cell 31:104-13
182. Wallace JA, Felsenfeld G. 2007. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17:400-7
183. Wang J, Kumar RM, Biggs VJ, Lee H, Chen Y, et al. 2011. The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development. Dev. Cell 21:575-88
184. Weierich C, Brero A, Stein S, Von Hase J, Cremer C, et al. 2003. Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome Res. 11:485-502
185. Weintraub H,Groudine M. 1976. Chromosomal subunits in active genes have an altered conformation. Science 193:848-56
186. White RJ. 2011. Transcription by RNA polymerase III: more complex than we thought. Nat. Rev. Genet. 12:459-63
187. 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
188. Wu R, Terry AV, Singh PB, Gilbert DM. 2005. Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol. Biol. Cell 16:2872-81
189. Yaffe E, Tanay A. 2011. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 43:1059-65
190. Yang J, Corces VG. 2012. Insulators, long-range interactions, and genome function. Curr. Opin. Genet. Dev. 22:86-92
191. Yang N, KazazianHHJr. 2006. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat. Struct. Mol. Biol. 13:763-71
192. Yang S-M, Kim BJ, Norwood Toro L, Skoultchi AI. 2013. H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proc. Natl. Acad. Sci. USA 110:1708-13
193. Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T. 2002.SATB1targets chromatin remodelling to regulate genes over long distances. Nature 419:641-45
194. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13:291-98
195. Zatsepina O, Zharskaya O, Prusov A. 2008. Isolation of the constitutive heterochromatin from mouse liver nuclei. In The Nucleus, ed. R Hancock, pp. 169-80. New York: Humana
196. Zhang J, Jackson AF, Naito T, Dose M, Seavitt J, et al. 2012. Harnessing of the nucleosome-remodelingdeacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13:86-94
197. Zhang LF, Huynh KD, Lee JT. 2007. Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 129:693-706
198. Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, et al. 2013. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152:642-54
199. Zimmer C, Fabre E. 2011. Principles of chromosomal organization: lessons from yeast. J. Cell Biol. 192:723-33
200. Zullo JM, Demarco IA, Piqué-Regi R, Gaffney DJ, Epstein CB, et al. 2012. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149:1474-87