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 and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Smeets, Daniel ^a,b   Markaki, Yolanda ^a   Schmid, Volker J ^a   Kraus, Felix ^a,b   Tattermusch, Anna ^b   Cerase, Andrea ^b   Sterr, Michael ^a   Fiedler, Susanne ^a   Demmerle, Justin ^b   Popken, Jens ^a   Leonhardt, Heinrich ^a   Brockdorff, Neil ^b   Cremer, Thomas ^a   Schermelleh, Lothar ^a,b   Cremer, Marion ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Barr body; Chromatin domain; Chromosome territory; CT; Inactive X chromosome; Interchromatin compartment; SAF A; Super resolution microscopy; X chromosome inactivation; Xist RNA

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG; XIST RNA;

ACTIVE NUCLEAR COMPARTMENT; ANIMAL CELL; ARTICLE; CELL NUCLEUS MATRIX; CELL NUCLEUS MEMBRANE; CHROMOSOME PAINTING; EMBRYONIC STEM CELL; FEMALE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MALE; MICROSCOPY; MOUSE; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; SOMATIC CELL; THREE DIMENSIONAL IMAGING; THREE DIMENSIONAL STRUCTURED ILLUMINATION MICROSCOPY; X CHROMATIN; X CHROMOSOME INACTIVATION;

MAMMALIA;

EID: 84900824181     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-8     Document Type: Article

References (121)

1. Recent advances in X-chromosome inactivation. Heard E, Curr Opin Cell Biol 2004 16 247 255 10.1016/j.ceb.2004.03.005 15145348 (Pubitemid 38610404)
2. X chromosome dosage compensation: how mammals keep the balance. Payer B, Lee JT, Annu Rev Genet 2008 42 733 772 10.1146/annurev.genet.42.110807.091711 18729722
3. Xist regulation and function explored. Pontier DB, Gribnau J, Hum Genet 2011 130 223 236 10.1007/s00439-011-1008-7 21626138
4. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Barr ML, Bertram EG, Nature 1949 163 676 10.1038/163676a0 18120749
5. Gene action in the X-chromosome of the mouse (Mus musculus L.). Lyon MF, Nature 1961 190 372 373 10.1038/190372a0 13764598
6. Epigenetic dynamics of imprinted X inactivation during early mouse development. Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E, Science 2004 303 644 649 10.1126/science.1092727 14671313 (Pubitemid 38141624)
7. Mouse Xist expression begins at zygotic genome activation and is timed by a zygotic clock. Zuccotti M, Boiani M, Ponce R, Guizzardi S, Scandroglio R, Garagna S, Redi CA, Mol Reprod Dev 2002 61 14 20 10.1002/mrd.1126 11774371 (Pubitemid 135715261)
8. X-inactivation and X-reactivation: epigenetic hallmarks of mammalian reproduction and pluripotent stem cells. Payer B, Lee JT, Namekawa SH, Hum Genet 2011 130 265 280 10.1007/s00439-011-1024-7 21667284
9. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF, Nature 1991 349 38 44 10.1038/349038a0 1985261 (Pubitemid 21912005)
10. Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns. Brockdorff N, Development 2011 138 5057 5065 10.1242/dev.065276 22069184
11. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Gendrel AV, Apedaile A, Coker H, Termanis A, Zvetkova I, Godwin J, Tang YA, Huntley D, Montana G, Taylor S, Giannoulatou E, Heard E, Stancheva I, Brockdorff N, Dev Cell 2012 23 265 279 10.1016/j.devcel.2012.06.011 22841499
12. Mammalian X-chromosome inactivation: an epigenetics paradigm. Heard E, Chaumeil J, Masui O, Okamoto I, Cold Spring Harb Symp Quant Biol 2004 69 89 102 10.1101/sqb.2004.69.89 16117637 (Pubitemid 41056542)
13. New and Xisting regulatory mechanisms of X chromosome inactivation. Jeon Y, Sarma K, Lee JT, Curr Opin Genet Dev 2012 22 62 71 10.1016/j.gde.2012.02.007 22424802
14. X-chromosome inactivation: molecular mechanisms from the human perspective. Yang C, Chapman AG, Kelsey AD, Minks J, Cotton AM, Brown CJ, Hum Genet 2011 130 175 185 10.1007/s00439-011-0994-9 21553122
15. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJ, Zhu Y, Kaaij LJ, van Ijcken W, Gribnau J, Heard E, de Laat W, Genes Dev 2011 25 1371 1383 10.1101/gad.633311 21690198
16. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nozawa RS, Nagao K, Igami KT, Shibata S, Shirai N, Nozaki N, Sado T, Kimura H, Obuse C, Nat Struct Mol Biol 2013 20 566 573 10.1038/nsmb.2532 23542155
17. Chromosome territories. Cremer T, Cremer M, Cold Spring Harb Perspect Biol 2010 2 003889 20300217
18. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B, Nature 2012 485 376 380 10.1038/nature11082 22495300
19. The hierarchy of the 3D genome. Gibcus JH, Dekker J, Mol Cell 2013 49 773 782 10.1016/j.molcel.2013.02.011 23473598
20. Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Albiez H, Cremer M, Tiberi C, Vecchio L, Schermelleh L, Dittrich S, Küpper K, Joffe B, Thormeyer T, von Hase J, Yang S, Rohr K, Leonhardt H, Solovei I, Cremer C, Fakan S, Cremer T, Chromosome Res 2006 14 707 733 10.1007/s10577-006-1086-x 17115328 (Pubitemid 44787905)
21. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Cremer T, Cremer C, Nat Rev Genet 2001 2 292 301 10.1038/35066075 11283701 (Pubitemid 33674777)
22. Chromosome territories-a functional nuclear landscape. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S, Curr Opin Cell Biol 2006 18 307 316 10.1016/j.ceb.2006.04.007 16687245
23. Revealing the high-resolution three-dimensional network of chromatin and interchromatin space: a novel electron-microscopic approach to reconstructing nuclear architecture. Rouquette J, Genoud C, Vazquez-Nin GH, Kraus B, Cremer T, Fakan S, Chromosome Res 2009 17 801 810 10.1007/s10577-009-9070-x 19731052
24. Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. Walter J, Schermelleh L, Cremer M, Tashiro S, Cremer T, J Cell Biol 2003 160 685 697 10.1083/jcb.200211103 12604593 (Pubitemid 36298264)
25. Structure and dynamics of human interphase chromosome territories in vivo. Zink D, Cremer T, Saffrich R, Fischer R, Trendelenburg MF, Ansorge W, Stelzer EH, Hum Genet 1998 102 241 251 10.1007/s004390050686 9521598 (Pubitemid 28185252)
26. The perichromatin region: a functional compartment in the nucleus that determines large-scale chromatin folding. Fakan S, van Driel R, Semin Cell Dev Biol 2007 18 676 681 10.1016/j.semcdb.2007.08.010 17920313 (Pubitemid 350026434)
27. Perichromatin fibrils are in situ forms of nascent transcripts. Fakan S, Trends Cell Biol 1994 4 86 90 10.1016/0962-8924(94)90180-5 14731598 (Pubitemid 24068106)
28. Localization of newly-synthesized DNA in a mammalian cell as visualized by high resolution autoradiography. Fakan S, Hancock R, Exp Cell Res 1974 83 95 102 10.1016/0014-4827(74)90692-2 4130365
29. Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, Neumann J, Heidemann M, Leonhardt H, Eick D, Cremer C, Cremer T, Cold Spring Harb Symp Quant Biol 2010 75 475 492 10.1101/sqb.2010.75.042 21467142
30. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Mor A, Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y, Nat Cell Biol 2010 12 543 552 10.1038/ncb2056 20453848
31. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Schermelleh L1, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MG, Leonhardt H, Sedat JW, Science 2008 320 1332 1336 10.1126/science.1156947 18535242 (Pubitemid 351929468)
32. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Clemson CM, Hall LL, Byron M, McNeil J, Lawrence JB, Proc Natl Acad Sci U S A 2006 103 7688 7693 10.1073/pnas.0601069103 16682630
33. Three-dimensional reconstruction of painted human interphase chromosomes: active and inactive X chromosome territories have similar volumes but differ in shape and surface structure. Eils R, Dietzel S, Bertin E, Schrock E, Speicher MR, Ried T, Robert-Nicoud M, Cremer C, Cremer T, J Cell Biol 1996 135 1427 1440 10.1083/jcb.135.6.1427 8978813 (Pubitemid 26427642)
34. A top-down analysis of Xa- and Xi-territories reveals differences of higher order structure at ≥20 Mb genomic length scales. Teller K, Illner D, Thamm S, Casas-Delucchi CS, Versteeg R, Indemans M, Cremer T, Cremer M, Nucleus 2011 2 465 477 10.4161/nucl.2.5.17862 21970989
35. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Chaumeil J, Le Baccon P, Wutz A, Heard E, Genes Dev 2006 20 2223 2237 10.1101/gad.380906 16912274
36. Site-specific silencing of regulatory elements as a mechanism of X inactivation. Calabrese JM, Sun W, Song L, Mugford JW, Williams L, Yee D, Starmer J, Mieczkowski P, Crawford GE, Magnuson T, Cell 2012 151 951 963 10.1016/j.cell.2012.10.037 23178118
37. The facultative heterochromatin of the inactive X chromosome has a distinctive condensed ultrastructure. Rego A, Sinclair PB, Tao W, Kireev I, Belmont AS, J Cell Sci 2008 121 1119 1127 10.1242/jcs.026104 18334550 (Pubitemid 351639430)
38. Superresolution imaging of biological nanostructures by spectral precision distance microscopy. Cremer C, Kaufmann R, Gunkel M, Pres S, Weiland Y, Müller P, Ruckelshausen T, Lemmer P, Geiger F, Degenhard S, Wege C, Lemmermann NA, Holtappels R, Strickfaden H, Hausmann M, Biotechnol J 2011 6 1037 1051 10.1002/biot.201100031 21910256
39. Far-field optical nanoscopy. Hell SW, Science 2007 316 1153 1158 10.1126/science.1137395 17525330 (Pubitemid 46877470)
40. Breaking the diffraction barrier: super-resolution imaging of cells. Huang B, Babcock H, Zhuang X, Cell 2010 143 1047 1058 10.1016/j.cell.2010.12.002 21168201
41. Functional nuclear architecture studied by microscopy: present and future. Rouquette J, Cremer C, Cremer T, Fakan S, Int Rev Cell Mol Biol 2010 282 1 90 20630466
42. A guide to super-resolution fluorescence microscopy. Schermelleh L, Heintzmann R, Leonhardt H, J Cell Biol 2010 190 165 175 10.1083/jcb.201002018 20643879
43. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW, Biophys J 2008 94 4957 4970 10.1529/biophysj.107.120345 18326650
44. The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture: 3D structured illumination microscopy of defined chromosomal structures visualized by 3D (immuno)-FISH opens new perspectives for studies of nuclear architecture. Markaki Y, Smeets D, Fiedler S, Schmid VJ, Schermelleh L, Cremer T, Cremer M, Bioessays 2012 34 412 426 10.1002/bies.201100176 22508100
45. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Blüthgen N, Dekker J, Heard E, Nature 2012 485 381 385 10.1038/nature11049 22495304
46. Mechanistic insights into chromosome-wide silencing in X inactivation. Arthold S, Kurowski A, Wutz A, Hum Genet 2011 130 295 305 10.1007/s00439-011- 1002-0 21567178
47. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Wutz A, Nat Rev Genet 2011 12 542 553 10.1038/nrg3035 21765457
48. Fluorescence in situ hybridization applications for super-resolution 3D structured illumination microscopy. Markaki Y, Smeets D, Cremer M, Schermelleh L, Methods Mol Biol 2013 950 43 64 23086869
49. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Wutz A, Jaenisch R, Mol Cell 2000 5 695 705 10.1016/S1097-2765(00)80248-8 10882105
50. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, Kadri S, Xing J, Goren A, Lander ES, Plath K, Guttman M, Science 2013 341 1237973 10.1126/science.1237973 23828888
51. Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, Cremer C, Fakan S, Cremer T, Exp Cell Res 2002 276 10 23 10.1006/excr.2002.5513 11978004 (Pubitemid 34948347)
52. Labeling nuclear DNA using DAPI. Chazotte B, Cold Spring Harb Protoc 2011 doi: 10.1101/pdb.prot5556
53. Initial sequencing and comparative analysis of the mouse genome. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Mouse Genome Sequencing Consortium, et al. Nature 2002 420 520 562 10.1038/nature01262 12466850 (Pubitemid 35477048)
54. Charting histone modifications and the functional organization of mammalian genomes. Zhou VW, Goren A, Bernstein BE, Nat Rev Genet 2011 12 7 18 21116306
55. A conserved organization of transcription during embryonic stem cell differentiation and in cells with high C value. Faro-Trindade I, Cook PR, Mol Biol Cell 2006 17 2910 2920 10.1091/mbc.E05-11-1024 16624866 (Pubitemid 43993496)
56. Genes that escape from X inactivation. Berletch JB, Yang F, Xu J, Carrel L, Disteche CM, Hum Genet 2011 130 237 245 10.1007/s00439-011-1011-z 21614513
57. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B, Nature 2008 453 948 951 10.1038/nature06947 18463634 (Pubitemid 351832561)
58. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW, Cell 2010 140 372 383 10.1016/j.cell.2009.12.054 20144761
59. X chromosome inactivation. Sengupta AK, Ohhata T, Wutz A, Epigenetics Norwich: Caister Aademic Press, Tost J, 2008 273 301
60. A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Sun BK, Deaton AM, Lee JT, Mol Cell 2006 21 617 628 10.1016/j.molcel.2006.01.028 16507360 (Pubitemid 43290729)
61. Stabilization and localization of Xist RNA are controlled by separate mechanisms and are not sufficient for X inactivation. Clemson CM, Chow JC, Brown CJ, Lawrence JB, J Cell Biol 1998 142 13 23 10.1083/jcb.142.1.13 9660859 (Pubitemid 28341136)
62. Correlative microscopy of individual cells: sequential application of microscopic systems with increasing resolution to study the nuclear landscape. Hubner B, Cremer T, Neumann J, Methods Mol Biol 2013 1042 299 336 10.1007/978-1-62703-526-2-21 23980016
63. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Nakagawa S, Dev Cell 2010 19 469 476 10.1016/j.devcel.2010.08.006 20833368
64. eXIST with matrix-associated proteins. Nakagawa S, Prasanth KV, Trends Cell Biol 2011 21 321 327 10.1016/j.tcb.2011.02.001 21392997
65. Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Helbig R, Fackelmayer FO, Chromosoma 2003 112 173 182 10.1007/s00412-003-0258-0 14608463 (Pubitemid 38063151)
66. Spatial separation of Xist RNA and polycomb proteins revealed by superresolution microscopy. Cerase A, Smeets D, Tang YA, Gdula M, Kraus F, Spivakov M, Moindrot B, Leleu M, Tattermusch A, Demmerle J, Nesterova TB, Green C, Otte AP, Schermelleh L, Brockdorff N, Proc Natl Acad Sci U S A 2014 111 2235 2240 10.1073/pnas.1312951111 24469834
67. Variation in Xi chromatin organization and correlation of the H3K27me3 chromatin territories to transcribed sequences by microarray analysis. Chadwick BP, Chromosoma 2007 116 147 157 10.1007/s00412-006-0085-1 17103221 (Pubitemid 46404510)
68. High-resolution analysis of epigenetic changes associated with X inactivation. Marks H, Chow JC, Denissov S, Francoijs KJ, Brockdorff N, Heard E, Stunnenberg HG, Genome Res 2009 19 1361 1373 10.1101/gr.092643.109 19581487
69. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Chadwick BP, Willard HF, Proc Natl Acad Sci U S A 2004 101 17450 17455 10.1073/pnas.0408021101 15574503 (Pubitemid 39657425)
70. Xist RNA is confined to the nuclear territory of the silenced X chromosome throughout the cell cycle. Jonkers I, Monkhorst K, Rentmeester E, Grootegoed JA, Grosveld F, Gribnau J, Mol Cell Biol 2008 28 5583 5594 10.1128/MCB.02269-07 18625719
71. Stabilization of Xist RNA mediates initiation of X chromosome inactivation. Sheardown SA, Duthie SM, Johnston CM, Newall AE, Formstone EJ, Arkell RM, Nesterova TB, Alghisi GC, Rastan S, Brockdorff N, Cell 1997 91 99 107 10.1016/S0092-8674(01)80012-X 9335338 (Pubitemid 27431316)
72. X chromosome inactivation is mediated by Xist RNA stabilization. Panning B, Dausman J, Jaenisch R, Cell 1997 90 907 916 10.1016/S0092-8674(00)80355-4 9298902 (Pubitemid 27381629)
73. Tsix, a gene antisense to Xist at the X-inactivation centre. Lee JT, Davidow LS, Warshawsky D, Nat Genet 1999 21 400 404 10.1038/7734 10192391 (Pubitemid 29159577)
74. Long-range cis effects of ectopic X-inactivation centres on a mouse autosome. Lee JT, Jaenisch R, Nature 1997 386 275 279 10.1038/386275a0 9069285 (Pubitemid 27142512)
75. Efficiency of Xist-mediated silencing on autosomes is linked to chromosomal domain organisation. Tang YA, Huntley D, Montana G, Cerase A, Nesterova TB, Brockdorff N, Epigenetics Chromatin 2010 3 10 10.1186/1756-8935-3- 10 20459652
76. Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture. Cremer T, Kreth G, Koester H, Fink RH, Heintzmann R, Cremer M, Solovei I, Zink D, Cremer C, Crit Rev Eukaryot Gene Expr 2000 10 179 212 11186332
77. DNA replication and nuclear architecture. Jaunin F, Fakan S, J Cell Biochem 2002 85 1 9 11891845 (Pubitemid 34204064)
78. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J, Science 2009 326 289 293 10.1126/science.1181369 19815776
79. Genome architecture: domain organization of interphase chromosomes. Bickmore WA, van Steensel B, Cell 2013 152 1270 1284 10.1016/j.cell.2013.02.001 23498936
80. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Dekker J, Marti-Renom MA, Mirny LA, Nat Rev Genet 2013 14 390 403 10.1038/nrg3454 23657480
81. Retinoic acid accelerates downregulation of the Xist repressor, Oct4, and increases the likelihood of Xist activation when Tsix is deficient. Ahn JY, Lee JT, BMC Dev Biol 2010 10 90 10.1186/1471-213X-10-90 20727175
82. The ins and outs of gene regulation and chromosome territory organisation. Heard E, Bickmore W, Curr Opin Cell Biol 2007 19 311 316 10.1016/j.ceb.2007.04.016 17467967 (Pubitemid 46899518)
83. YY1 tethers Xist RNA to the inactive X nucleation center. Jeon Y, Lee JT, Cell 2011 146 119 133 10.1016/j.cell.2011.06.026 21729784
84. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. Clemson CM, McNeil JA, Willard HF, Lawrence JB, J Cell Biol 1996 132 259 275 10.1083/jcb.132.3.259 8636206 (Pubitemid 26052564)
85. A system for imaging the regulatory noncoding Xist RNA in living mouse embryonic stem cells. Ng K, Daigle N, Bancaud A, Ohhata T, Humphreys P, Walker R, Ellenberg J, Wutz A, Mol Biol Cell 2011 22 2634 2645 10.1091/mbc.E11-02-0146 21613549
86. Quantitative RT-PCR assays show Xist RNA levels are low in mouse female adult tissue, embryos and embryoid bodies. Buzin CH, Mann JR, Singer-Sam J, Development 1994 120 3529 3536 7529677 (Pubitemid 24366997)
87. A NMR strategy to unambiguously distinguish nucleic acid hairpin and duplex conformations applied to a Xist RNA A-repeat. Duszczyk MM, Zanier K, Sattler M, Nucleic Acids Res 2008 36 7068 7077 10.1093/nar/gkn776 18987004
88. 2-D structure of the A region of Xist RNA and its implication for PRC2 association. Maenner S, Blaud M, Fouillen L, Savoye A, Marchand V, Dubois A, Sanglier-Cianferani S, Van Dorsselaer A, Clerc P, Avner P, Visvikis A, Branlant C, PLoS Biol 2010 8 1000276 10.1371/journal.pbio.1000276 20052282
89. Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Duthie SM, Nesterova TB, Formstone EJ, Keohane AM, Turner BM, Zakian SM, Brockdorff N, Hum Mol Genet 1999 8 195 204 10.1093/hmg/8.2.195 9931327 (Pubitemid 29054261)
90. Spreading of X chromosome inactivation via a hierarchy of defined Polycomb stations. Pinter SF, Sadreyev RI, Yildirim E, Jeon Y, Ohsumi TK, Borowsky M, Lee JT, Genome Res 2012 22 1864 1876 10.1101/gr.133751.111 22948768
91. Characterization of SAF-A, a novel nuclear DNA binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. Romig H, Fackelmayer FO, Renz A, Ramsperger U, Richter A, EMBO J 1992 11 3431 3440 1324173
92. Functional diversity of the hnRNPs: past, present and perspectives. Han SP, Tang YH, Smith R, Biochem J 2010 430 379 392 10.1042/BJ20100396 20795951
93. Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear-matrix protein which binds DNA and RNA in vivo and in vitro. Fackelmayer FO, Dahm K, Renz A, Ramsperger U, Richter A, Eur J Biochem 1994 221 749 757 10.1111/j.1432-1033.1994.tb18788.x 8174554
94. A scaffold for X chromosome inactivation. Tattermusch A, Brockdorff N, Hum Genet 2011 130 247 253 10.1007/s00439-011-1027-4 21660507
95. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Heard E, Rougeulle C, Arnaud D, Avner P, Allis CD, Spector DL, Cell 2001 107 727 738 10.1016/S0092-8674(01)00598-0 11747809 (Pubitemid 34033666)
96. Chromatin structure and nuclear organization dynamics during X-chromosome inactivation. Nora EP, Heard E, Cold Spring Harb Symp Quant Biol 2010 75 333 344 10.1101/sqb.2010.75.032 21447823
97. Gene density and transcription influence the localization of chromatin outside of chromosome territories detectable by FISH. Mahy NL, Perry PE, Bickmore WA, J Cell Biol 2002 159 753 763 10.1083/jcb.200207115 12473685 (Pubitemid 36008358)
98. Radial chromatin positioning is shaped by local gene density, not by gene expression. Kupper K, Kolbl A, Biener D, Dittrich S, Von Hase J, Thormeyer T, Fiegler H, Carter NP, Speicher MR, Cremer T, Cremer M, Chromosoma 2007 116 285 306 10.1007/s00412-007-0098-4 17333233 (Pubitemid 46712017)
99. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J, Beck S, Campbell RD, Goldsworthy M, Powis SH, Ragoussis J, Trowsdale J, Sheer D, J Cell Sci 2000 113 Pt 9 1565 1576 10751148 (Pubitemid 30312505)
100. Attenuated spread of X-inactivation in an X;autosome translocation. Popova BC, Tada T, Takagi N, Brockdorff N, Nesterova TB, Proc Natl Acad Sci U S A 2006 103 7706 7711 10.1073/pnas.0602021103 16679409
101. Measurement of replication structures at the nanometer scale using super-resolution light microscopy. Baddeley D, Chagin VO, Schermelleh L, Martin S, Pombo A, Carlton PM, Gahl A, Domaing P, Birk U, Leonhardt H, Cremer C, Cardoso MC, Nucleic Acids Res 2010 38 8 10.1093/nar/gkp901 19864256
102. Spatial and temporal dynamics of DNA replication sites in mammalian cells. Ma H, Samarabandu J, Devdhar RS, Acharya R, Cheng PC, Meng C, Berezney R, J Cell Biol 1998 143 1415 1425 10.1083/jcb.143.6.1415 9852140 (Pubitemid 29006492)
103. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P, Scherthan H, Ried T, Cremer C, Lichter P, Cold Spring Harb Symp Quant Biol 1993 58 777 792 10.1101/SQB.1993. 058.01.085 7525149 (Pubitemid 24219540)
104. Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Chandra T, Kirschner K, Thuret JY, Pope BD, Ryba T, Newman S, Ahmed K, Samarajiwa SA, Salama R, Carroll T, Stark R, Janky R, Narita M, Xue L, Chicas A, Nũnez S, Janknecht R, Hayashi-Takanaka Y, Wilson MD, Marshall A, Odom DT, Babu MM, Bazett-Jones DP, Tavaré S, Edwards PA, Lowe SW, Kimura H, Gilbert DM, Narita M, Mol Cell 2012 47 203 214 10.1016/j.molcel.2012.06.010 22795131
105. Remodeling of nuclear architecture by the thiodioxoxpiperazine metabolite chaetocin. Illner D, Zinner R, Handtke V, Rouquette J, Strickfaden H, Lanctot C, Conrad M, Seiler A, Imhof A, Cremer T, Cremer M, Exp Cell Res 2010 316 1662 1680 10.1016/j.yexcr.2010.03.008 20302859
106. Major genome activation in bovine embryos involves a massive reorganization of nuclear architecture. Popken J, Brero A, Koehler D, Schmid VJ, Strauss A, Wuensch A, Guengoer T, Zakhartchenko V, Wolf E, Cremer T, Nucleus 2014 in press
107. The fractal globule as a model of chromatin architecture in the cell. Mirny LA, Chromosome Res 2011 19 37 51 21274616
108. Histone acetylation controls the inactive X chromosome replication dynamics. Casas-Delucchi CS, Brero A, Rahn HP, Solovei I, Wutz A, Cremer T, Leonhardt H, Cardoso MC, Nat Commun 2011 2 222 21364561
109. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Kanda T, Sullivan KF, Wahl GM, Curr Biol 1998 8 377 385 10.1016/S0960-9822(98)70156-3 9545195 (Pubitemid 28173996)
110. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Lee JT, Lu N, Cell 1999 99 47 57 10.1016/S0092-8674(00)80061-6 10520993 (Pubitemid 29468629)
111. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Cremer M, Grasser F, Lanctot C, Muller S, Neusser M, Zinner R, Solovei I, Cremer T, Methods Mol Biol 2008 463 205 239 18951171
112. Cracking the RNA polymerase II CTD code. Egloff S, Murphy S, Trends Genet 2008 24 280 288 10.1016/j.tig.2008.03.008 18457900
113. OMX: a new platform for multimodal, multichannel wide-field imaging. Dobbie IM, King E, Parton RM, Carlton PM, Sedat JW, Swedlow JR, Davis I, Cold Spring Harb Protoc 2011 2011 899 909 21807861
114. R Development Core Team, R: A Language and Environment for Statistical Computing Vienna: R Foundation for Statistical Computing 2011
115. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. Zhang Y, Brady M, Smith S, IEEE Trans Med Imaging 2001 20 45 57 10.1109/42.906424 11293691 (Pubitemid 32293419)
116. TANGO: a generic tool for high-throughput 3D image analysis for studying nuclear organization. Ollion J, Cochennec J, Loll F, Escude C, Boudier T, Bioinformatics 2013 29 1840 1841 10.1093/bioinformatics/btt276 23681123
117. DAPI: a DNA-specific fluorescent probe. Kapuscinski J, Biotech Histochem 1995 70 220 233 10.3109/10520299509108199 8580206
118. GC/AT-content spikes as genomic punctuation marks. Zhang L, Kasif S, Cantor CR, Broude NE, Proc Natl Acad Sci U S A 2004 101 16855 16860 10.1073/pnas.0407821101 15548610 (Pubitemid 39601328)
119. Tandemly repeated DNA families in the mouse genome. Komissarov AS, Gavrilova EV, Demin SJ, Ishov AM, Podgornaya OI, BMC Genomics 2011 12 531 10.1186/1471-2164-12-531 22035034
120. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. Kimura H, Cook PR, J Cell Biol 2001 153 1341 1353 10.1083/jcb.153.7.1341 11425866 (Pubitemid 34286121)
121. PCNA, the maestro of the replication fork. Moldovan GL, Pfander B, Jentsch S, Cell 2007 129 665 679 10.1016/j.cell.2007.05.003 17512402 (Pubitemid 46802385)