Nuclear organization changes and the epigenetic silencing of FLC during vernalization

Journal of Molecular Biology

Volumn 427, Issue 3, 2015, Pages 659-669

  Zhu, Danling ^a   Rosa, Stefanie ^a   Dean, Caroline ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLOWERING LOCUS C; HISTONE H3; POLYCOMB GROUP PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN;

ARABIDOPSIS; ARTICLE; CHROMATIN; COLD EXPOSURE; EMBRYO DEVELOPMENT; EPIGENETICS; GENE CLUSTER; GENE FUNCTION; GENE INSERTION; GENE LOCUS; GENE SILENCING; GENE SWITCHING; GENETIC PARAMETERS; NONHUMAN; NUCLEAR ORGANIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; VERNALIZATION; CELL NUCLEUS; FLOWER; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; EPIGENESIS, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; MADS DOMAIN PROTEINS;

EID: 84925389254     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.08.025     Document Type: Review

References (108)

1. I.R. Henderson, and C. Dean Control of Arabidopsis flowering: the chill before the bloom Development 131 2004 3829 3838
2. S.D. Michaels, and R.M. Amasino FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering Plant Cell 11 1999 949 956
3. C.C. Sheldon, J.E. Burn, P.P. Perez, J. Metzger, J.A. Edwards, and W.J. Peacock The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation Plant Cell 11 1999 445 458
4. C.C. Sheldon, D.T. Rouse, E.J. Finnegan, W.J. Peacock, and E.S. Dennis The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC) Proc Natl Acad Sci USA 97 2000 3753 3758
5. J.E. Burn, D.J. Bagnall, J.D. Metzger, E.S. Dennis, and W.J. Peacock DNA methylation, vernalization, and the initiation of flowering Proc Natl Acad Sci USA 90 1993 287 291
6. U. Johanson, J. West, C. Lister, S. Micheal, R.M. Amasino, and C. Dean Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time Science 290 2000 344 347
7. D. Jiang, X. Gu, and Y. He Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis Plant Cell 21 2009 1733 1746
8. N. Geraldo, I. Baurle, S. Kidou, X. Hu, and C. Dean FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex Plant Physiol 150 2009 1611 1618
9. K. Choi, J. Kim, H.J. Hwang, S. Kim, C. Park, and S.Y. Kim The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors Plant Cell 23 2011 289 303
10. C. Toomajian, T.T. Hu, M.J. Aranzana, C. Lister, C. Tang, and H. Zheng A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome PLoS Biol 4 2006 e137
11. H. Zhang, and S. van Nocker The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C Plant J 31 2002 663 673
12. S. Oh, H. Zhang, P. Ludwig, and S. van Nocker A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family Plant Cell 16 2004 2940 2953
13. H. Zhang, C. Ransom, P. Ludwig, and S. van Nocker Genetic analysis of early flowering mutants in Arabidopsis defines a class of pleiotropic developmental regulator required for expression of the flowering-time switch Flowering Locus C Genetics 164 2003 347 358
14. Y. He, M.R. Doyle, and R.M. Amasino PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis Genes Dev 18 2004 2774 2784
15. X. Yu, and S.D. Michaels The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLOWERING LOCUS C chromatin Plant Physiol 153 2010 1074 1084
16. S. Park, S. Oh, J. Ek-Ramos, and S. van Nocker PLANT HOMOLOGOUS TO PARAFIBROMIN is a component of the PAF1 complex and assists in regulating expression of genes within H3K27ME3-enriched chromatin Plant Physiol 153 2010 821 831
17. S. Pien, D. Fleury, J.S. Mylne, P. Crevillen, D. Inze, and Z. Avramova ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation Plant Cell 20 2008 580 588
18. A. Saleh, R. Alvarez-Venegas, M. Yilmaz, O. Le, G. Hou, and M. Sadder The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions Plant Cell 20 2008 568 579
19. Y. Cao, Y. Dai, S. Cui, and L. Ma Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis Plant Cell 20 2008 2586 2602
20. L. Xu, R. Menard, A. Berr, J. Fuchs, V. Cognat, and D. Meyer The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana Plant J 57 2009 279 288
21. X. Gu, D. Jiang, Y. Wang, A. Bachmair, and Y. He Repression of the floral transition via histone H2B monoubiquitination Plant J 57 2009 522 533
22. I.B. Lolas, K. Himanen, J.T. Gronlund, C. Lynggaard, A. Houben, and M. Melzer The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2 Plant J 61 2010 686 697
23. Y.S. Noh, and R.M. Amasino PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis Plant Cell 15 2003 1671 1682
24. R.B. Deal, M.K. Kandasamy, E.C. McKinney, and R.B. Meagher The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis Plant Cell 17 2005 2633 2646
25. K. Choi, S. Kim, S.Y. Kim, M. Kim, Y. Hyun, and H. Lee SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis Plant Cell 17 2005 2647 2660
26. M. Martin-Trillo, A. Lazaro, R.S. Poethig, C. Gomez-Mena, M.A. Pineiro, and J.M. Martinez-Zapater EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis Development 133 2006 1241 1252
27. R. March-Diaz, M. Garcia-Dominguez, F.J. Florencio, and J.C. Reyes SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6 Plant Physiol 143 2007 893 901
28. K. Choi, C. Park, J. Lee, M. Oh, B. Noh, and I. Lee Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development Development 134 2007 1931 1941
29. A. Lazaro, A. Gomez-Zambrano, L. Lopez-Gonzalez, M. Pineiro, and J.A. Jarillo Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development J Exp Bot 59 2008 653 666
30. R.B. Deal, C.N. Topp, E.C. McKinney, and R.B. Meagher Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z Plant Cell 19 2007 74 83
31. P. Crevillen, and C. Dean Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context Curr Opin Plant Biol 14 2011 38 44
32. I. Baurle, and C. Dean The timing of developmental transitions in plants Cell 125 2006 655 664
33. F. Liu, V. Quesada, P. Crevillen, I. Baurle, S. Swiezewski, and C. Dean The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC Mol Cell 28 2007 398 407
34. F. Liu, S. Marquardt, C. Lister, S. Swiezewski, and C. Dean Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing Science 327 2010 94 97
35. S. Swiezewski, P. Crevillen, F. Liu, J.R. Ecker, A. Jerzmanowski, and C. Dean Small RNA-mediated chromatin silencing directed to the 3′ region of the Arabidopsis gene encoding the developmental regulator, FLC Proc Natl Acad Sci USA 104 2007 3633 3638
36. S. Swiezewski, F. Liu, A. Magusin, and C. Dean Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target Nature 462 2009 799 802
37. C. Hornyik, C. Duc, K. Rataj, L.C. Terzi, and G.G. Simpson Alternative polyadenylation of antisense RNAs and flowering time control Biochem Soc Trans 38 2010 1077 1081
38. C. Hornyik, L.C. Terzi, and G.G. Simpson The spen family protein FPA controls alternative cleavage and polyadenylation of RNA Dev Cell 18 2010 203 213
39. S. Marquardt, O. Raitskin, Z. Wu, F. Liu, Q. Sun, and C. Dean Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription Mol Cell 54 2014 156 165
40. Z.W. Wang, Z. Wu, O. Raitskin, Q. Sun, and C. Dean Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor Proc Natl Acad Sci USA 111 2014 7468 7473
41. Q. Sun, T. Csorba, K. Skourti-Stathaki, N.J. Proudfoot, and C. Dean R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus Science 340 2013 619 621
42. E.J. Finnegan, R.K. Genger, K. Kovac, W.J. Peacock, and E.S. Dennis DNA methylation and the promotion of flowering by vernalization Proc Natl Acad Sci USA 95 1998 5824 5829
43. E.J. Finnegan, K.A. Kovac, E. Jaligot, C.C. Sheldon, W.J. Peacock, and E.S. Dennis The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms Plant J 44 2005 420 432
44. F. De Lucia, P. Crevillen, A.M. Jones, T. Greb, and C. Dean A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization Proc Natl Acad Sci USA 105 2008 16831 16836
45. S. Sung, and R.M. Amasino Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 Nature 427 2004 159 164
46. T. Greb, J.S. Mylne, P. Crevillen, N. Geraldo, H. An, and A.R. Gendall The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC Curr Biol 17 2007 73 78
47. S. Sung, R.J. Schmitz, and R.M. Amasino A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis Genes Dev 20 2006 3244 3248
48. D. Fu, M. Dunbar, and J. Dubcovsky Wheat VIN3-like PHD finger genes are up-regulated by vernalization Mol Genet Genomics 277 2007 301 313
49. D.H. Kim, and S. Sung Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis Plant Cell 25 2013 454 469
50. C.C. Wood, M. Robertson, G. Tanner, W.J. Peacock, E.S. Dennis, and C.A. Helliwell The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3 Proc Natl Acad Sci USA 103 2006 14631 14636
51. M. Nekrasov, T. Klymenko, S. Fraterman, B. Papp, K. Oktaba, and T. Kocher Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes EMBO J 26 2007 4078 4088
52. K. Sarma, R. Margueron, A. Ivanov, V. Pirrotta, and D. Reinberg Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo Mol Cell Biol 28 2008 2718 2731
53. J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, and S.A. Brugmann Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs Cell 129 2007 1311 1323
54. C.A. Helliwell, M. Robertson, E.J. Finnegan, D.M. Buzas, and E.S. Dennis Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts PLoS One 6 2011 e21513
55. J.B. Heo, and S. Sung Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA Science 331 2011 76 79
56. A. Angel, J. Song, C. Dean, and M. Howard A Polycomb-based switch underlying quantitative epigenetic memory Nature 476 2011 105 108
57. E.J. Finnegan, and E.S. Dennis Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells Curr Biol 17 2007 1978 1983
58. Y.Y. Levy, S. Mesnage, J.S. Mylne, A.R. Gendall, and C. Dean Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control Science 297 2002 243 246
59. J.S. Mylne, L. Barrett, F. Tessadori, S. Mesnage, L. Johnson, and Y.V. Bernatavichute LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC Proc Natl Acad Sci USA 103 2006 5012 5017
60. S. Sung, Y. He, T.W. Eshoo, Y. Tamada, L. Johnson, and K. Nakahigashi Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1 Nat Genet 38 2006 706 710
61. C.C. Sheldon, M.J. Hills, C. Lister, C. Dean, E.S. Dennis, and W.J. Peacock Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization Proc Natl Acad Sci USA 105 2008 2214 2219
62. J. Choi, Y. Hyun, M.J. Kang, H.I. Yun, J.Y. Yun, and C. Lister Resetting and regulation of Flowering Locus C expression during Arabidopsis reproductive development Plant J 57 2009 918 931
63. I.B. Dodd, M.A. Micheelsen, K. Sneppen, and G. Thon Theoretical analysis of epigenetic cell memory by nucleosome modification Cell 129 2007 813 822
64. H. Yang, M. Howard, and C. Dean Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC Curr Biol 24 2014 1793 1797
65. L. Corbesier, C. Vincent, S. Jang, F. Fornara, Q. Fan, and I. Searle FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis Science 316 2007 1030 1033
66. C. Lanzuolo, V. Roure, J. Dekker, F. Bantignies, and V. Orlando Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex Nat Cell Biol 9 2007 1167 1174
67. F. Bantignies, V. Roure, I. Comet, B. Leblanc, B. Schuettengruber, and J. Bonnet Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila Cell 144 2011 214 226
68. D. Noordermeer, M. Leleu, E. Splinter, J. Rougemont, W.D. Laat, and D. Duboule The dynamic architecture of Hox gene clusters Science 334 2011 222 225
69. E.P. Nora, B.R. Lajoie, E.G. Schulz, L. Giorgetti, I. Okamoto, and N. Servant Spatial partitioning of the regulatory landscape of the X-inactivation centre Nature 485 2012 381 385
70. P. Fraser, and W. Bickmore Nuclear organization of the genome and the potential for gene regulation Nature 447 2007 413 417
71. M.R. Gartenberg, F.R. Neumann, T. Laroche, M. Blaszczyk, and S.M. Gasser Sir-mediated repression can occur independently of chromosomal and subnuclear contexts Cell 119 2004 955 967
72. B.D. Towbin, C. Gonzalez-Aguilera, R. Sack, D. Gaidatzis, V. Kalck, and P. Meister Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery Cell 150 2012 934 947
73. J.H. Brickner Transcriptional memory at the nuclear periphery Curr Opin Cell Biol 21 2009 127 133
74. J.M. O'Sullivan, S.M. Tan-Wong, A. Morillon, B. Lee, J. Coles, and J. Mellor Gene loops juxtapose promoters and terminators in yeast Nat Genet 36 2004 1014 1018
75. A. Ansari, and M. Hampsey A role for the CPF 3′-end processing machinery in RNAP II-dependent gene looping Genes Dev 19 2005 2969 2978
76. J.P. Laine, B.N. Singh, S. Krishnamurthy, and M. Hampsey A physiological role for gene loops in yeast Genes Dev 23 2009 2604 2609
77. S.M. Tan-Wong, H.D. Wijayatilake, and N.J. Proudfoot Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex Genes Dev 23 2009 2610 2624
78. P. Crevillen, C. Sonmez, Z. Wu, and C. Dean A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization EMBO J 32 2013 140 148
79. T. Jegu, D. Latrasse, M. Delarue, H. Hirt, S. Domenichini, and F. Ariel The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis Plant Cell 26 2014 538 551
80. F. Bantignies, C. Grimaud, S. Lavrov, M. Gabut, and G. Cavalli Inheritance of Polycomb-dependent chromosomal interactions in Drosophila Genes Dev 17 2003 2406 2420
81. T. Cheutin, and G. Cavalli Polycomb silencing: from linear chromatin domains to 3D chromosome folding Curr Opin Genet Dev 25 2014 30 37
82. C. Grimaud, F. Bantignies, M. Pal-Bhadra, P. Ghana, U. Bhadra, and G. Cavalli RNAi components are required for nuclear clustering of Polycomb group response elements Cell 124 2006 957 971
83. S. Rosa, F. De Lucia, J.S. Mylne, D. Zhu, N. Ohmido, and A. Pendle Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization Genes Dev 27 2013 1845 1850
84. O. Masui, I. Bonnet, P. Le Baccon, I. Brito, T. Pollex, and N. Murphy Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation Cell 145 2011 447 458
85. T. Pollex, and E. Heard Recent advances in X-chromosome inactivation research Curr Opin Cell Biol 24 2012 825 832
86. E. Splinter, E. De Wit, E.P. Nora, P. Klous, H.J. Van de Werken, and Y. Zhu The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA Genes Dev 25 2011 1371 1383
87. A.R. Gendall, Y.Y. Levy, A. Wilson, and C. Dean The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis Cell 107 2001 525 535
88. L.M. Octavio, K. Gedeon, and N. Maheshri Epigenetic and conventional regulation is distributed among activators of FLO11 allowing tuning of population-level heterogeneity in its expression PLoS Genet 5 2009 e1000673
89. S.L. Bumgarner, R.D. Dowell, P. Grisafi, D.K. Gifford, and G.R. Fink Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast Proc Natl Acad Sci USA 106 2009 18321 18326
90. L. Giorgetti, R. Galupa, E.P. Nora, T. Piolot, F. Lam, and J. Dekker Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription Cell 157 2014 950 963
91. C.C. Sheldon, E.J. Finnegan, W.J. Peacock, and E.S. Dennis Mechanisms of gene repression by vernalization in Arabidopsis Plant J 59 2009 488 498
92. M.C. Tsai, O. Manor, Y. Wan, N. Mosammaparast, J.K. Wang, and F. Lan Long noncoding RNA as modular scaffold of histone modification complexes Science 329 2010 689 693
93. E.M. Mendenhall, R.P. Koche, T. Truong, V.W. Zhou, B. Lssac, and A.S. Chi GC-rich sequence elements recruit PRC2 in mammalian ES cells PLoS Genet 6 2010 e1001244
94. A.M. Farcas, N.P. Blackledge, I. Sudbery, H.K. Long, J.F. McGouran, and N.R. Rose KDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands Elife 1 2012 e00205
95. E.M. Riising, I. Comet, B. Leblanc, X. Wu, J.V. Johansen, and K. Helin Gene silencing triggers Polycomb repressive complex 2 recruitment to CpG islands genome wide Mol Cell 55 2014 1 14
96. C.C. Sheldon, A.B. Conn, E.S. Dennis, and W.J. Peacock Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression Plant Cell 14 2002 2527 2537
97. V. Coustham, P.J. Li, A. Strange, C. Lister, J. Song, and C. Dean Quantitative modulation of polycomb silencing underlies natural variation in vernalization Science 337 2013 584 587
98. C. Shindo, C. Lister, P. Crevillen, M. Nordborg, and C. Dean Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response Genes Dev 20 2006 3079 3083
99. A. Papantonis, and P.R. Cook Fixing the model for transcription: the DNA moves, not the polymerase Transcription 2 2011 41 44
100. H. Sutherland, and W.A. Bickmore Transcription factories: gene expression in unions? Nat Rev Genet 10 2009 457 466
101. L.B. Edelman, and P. Fraser Transcription factories: genetic programming in three dimensions Curr Opin Genet Dev 22 2012 110 114
102. V. Pirrotta, and H.B. Li A view of nuclear Polycomb bodies Curr Opin Genet Dev 22 2012 101 109
103. R.J. Schmitz, L. Hong, K.E. Fitzpatrick, and R.M. Amasino DICER-LIKE 1 and DICER-LIKE 3 redundantly act to promote flowering via repression of FLOWERING LOCUS C in Arabidopsis thaliana Genetics 176 2007 1359 1362
104. G. Cavalli, and T. Misteli Functional implications of genome topology Nat Struct Mol Biol 20 2013 290 299
105. N. Xu, M.E. Donohoe, S.S. Silva, and J.T. Lee Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein Nat Genet 39 2007 1390 1396
106. M.E. Donohoe, S.S. Silva, S.F. Pinter, N. Xu, and J.T. Lee The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting Nature 460 2009 128 132
107. M. Buhler, and S.M. Gasser Silent chromatin at the middle and ends: lessons from yeasts EMBO J 28 2009 2149 2161
108. D. Moazed Mechanisms for the inheritance of chromatin states Cell 146 2011 510 518