The making of a Barr body: The mosaic of factors that eXIST on the mammalian inactive X chromosome1

Biochemistry and Cell Biology

Volumn 94, Issue 1, 2015, Pages 56-70

  Dixon Mcdougall, Thomas ^a   Brown, Carolyn ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Epigenetics; Gene silencing; Heterochromatin; X chromosome Inactivation (XCI); XIST

Indexed keywords

GENE EXPRESSION; GENES; MAMMALS;

EPIGENETICS; GENE SILENCING; HETEROCHROMATIN; X-CHROMOSOME INACTIVATION; XIST;

CHROMOSOMES;

MAMMAL; X CHROMATIN; X CHROMOSOME; X CHROMOSOME INACTIVATION; ACETYLATION; ANIMAL; DNA METHYLATION; FEMALE; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MOUSE;

DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA BINDING PROTEIN; HISTONE; HISTONE DEACETYLASE; LONG UNTRANSLATED RNA; POLYCOMB GROUP PROTEIN; XIST NON-CODING RNA;

ACETYLATION; ANIMALS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; FEMALE; GENE SILENCING; HISTONE DEACETYLASES; HISTONES; HUMANS; MICE; POLYCOMB-GROUP PROTEINS; RNA, LONG NONCODING; SEX CHROMATIN; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 84955484306     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/bcb-2015-0016     Document Type: Article

References (143)

1. Agrelo R. Souabni A. Novatchkova M. Haslinger C. Leeb M. Komnenovic V. et al 2009. SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev. Cell, 16 (4): 507-516. 10.1016/j.devcel.2009.03.006. 19386260.
2. Angulo M. Corominas M. Serras F. 2004. Activation and repression activities of ash2 in Drosophila wing imaginal discs. Development, 131 (20): 4943-4953. 10.1242/dev.01380. 15371308.
3. Arrigoni R. Alam S.L. Wamstad J.A. Bardwell V.J. Sundquist W.I. Schreiber-Agus N. 2006. The Polycomb-associated protein Rybp is a ubiquitin binding protein. FEBS Lett. 580 (26): 6233-6241. 10.1016/j.febslet.2006.10.027. 17070805.
4. Augui S. Nora E.P. Heard E. 2011. Regulation of X-chromosome inactivation by the X-inactivation centre. Nat. Rev. Genet. 12 (6): 429-442. 10.1038/nrg2987. 21587299.
5. Barakat T.S. Gunhanlar N. Pardo C.G. Achame E.M. Ghazvini M. Boers R. et al 2011. RNF12 activates Xist and is essential for X chromosome inactivation. PLoS Genet. 7 (1): e1002001. 10.1371/journal.pgen.1002001. 21298085.
6. Basu A. Wilkinson F.H. Colavita K. Fennelly C. Atchison M.L. 2014. YY1 DNA binding and interaction with YAF2 is essential for Polycomb recruitment. Nucleic Acids Res. 42 (4): 2208-2223. 10.1093/nar/gkt1187. 24285299.
7. Bhatnagar S. Zhu X. Ou J. Lin L. Chamberlain L. Zhu L.J. Wajapeyee N. Green M.R. 2014. Genetic and pharmacological reactivation of the mammalian inactive X chromosome. Proc. Natl. Acad. Sci. USA. 111 (35): 12591-12598. 10.1073/pnas.1413620111.
8. Baumann C. De La Fuente R. 2009. ATRX marks the inactive X chromosome (Xi) in somatic cells and during imprinted X chromosome inactivation in trophoblast stem cells. Chromosoma, 118 (2): 209-222. 10.1007/s00412-008-0189-x. 19005673.
9. Beck D.B. Burton A. Oda H. Ziegler-Birling C. Torres-Padilla M.E. Reinberg D. 2012. The role of PR-Set7 in replication licensing depends on Suv4-20h. Genes Dev. 26 (23): 2580-2589. 10.1101/gad.195636.112. 23152447.
10. Bellucci M. Agostini F. Masin M. Tartaglia G.G. 2011. Predicting protein associations with long noncoding RNAs. Nat. Methods, 8 (6): 444-445. 10.1038/nmeth.1611. 21623348.
11. Berletch J.B. Yang F. Xu J. Carrel L. Disteche C.M. 2011. Genes that escape from X inactivation. Hum. Genet. 130 (2): 237-245. 10.1007/s00439-011-1011-z. 21614513.
12. Bernstein E. Duncan E.M. Masui O. Gil J. Heard E. Allis C.D. 2006. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26 (7): 2560-2569. 10.1128/MCB.26.7.2560-2569.2006. 16537902.
13. Binda, O. 2013. On your histone mark, SET, methylate! Epigenetics, 8 (5): 457-463. 10.4161/epi.24451. 23625014.
14. Blewitt M.E. Gendrel A.V. Pang Z. Sparrow D.B. Whitelaw N. Craig J.M. et al 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40 (5): 663-669. 10.1038/ng.142. 18425126.
15. Brinkman A.B. Roelofsen T. Pennings S.W. Martens J.H. Jenuwein T. Stunnenberg H.G. 2006. Histone modification patterns associated with the human X chromosome. EMBO Rep. 7 (6): 628-634. 10.1038/sj.embor.7400686. 16648823.
16. Brown C.J. Ballabio A. Rupert J.L. Lafreniere R.G. Grompe M. Tonlorenzi R. Willard H.F. 1991. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature, 349 (6304): 38-44. 10.1038/349038a0. 1985261.
17. Casanova M. Preissner T. Cerase A. Poot R. Yamada D. Li X. et al 2011. Polycomblike 2 facilitates the recruitment of PRC2 Polycomb group complexes to the inactive X chromosome and to target loci in embryonic stem cells. Development, 138 (8): 1471-1482. 10.1242/dev.053652. 21367819.
18. Casas-Delucchi C.S. Brero A. Rahn H.P. Solovei I. Wutz A. Cremer T. et al 2011. Histone acetylation controls the inactive X chromosome replication dynamics. Nat. Commun. 2: 222. 10.1038/ncomms1218. 21364561.
19. Cerase A. Smeets D. Tang Y.A. Gdula M. Kraus F. Spivakov M. et al 2014. Spatial separation of Xist RNA and polycomb proteins revealed by superresolution microscopy. Proc. Natl. Acad. Sci. U.S.A. 111 (6): 2235-2240. 10.1073/pnas.1312951111. 24469834.
20. Chadwick B.P. 2007. Variation in Xi chromatin organization and correlation of the H3K27me3 chromatin territories to transcribed sequences by microarray analysis. Chromosoma, 116 (2): 147-157. 10.1007/s00412-006-0085-1. 17103221.
21. Chadwick B.P. Willard H.F. 2004. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc. Natl. Acad. Sci. U.S.A. 101 (50): 17450-17455. 10.1073/pnas.0408021101. 15574503.
22. Chan K.M. Zhang H. Malureanu L. van Deursen J. Zhang Z. 2011. Diverse factors are involved in maintaining X chromosome inactivation. Proc. Natl. Acad. Sci. U.S.A. 108 (40): 16699-16704. 10.1073/pnas.1107616108. 21940502.
23. Chang S.C. Brown C.J. 2010. Identification of regulatory elements flanking human XIST reveals species differences. BMC Mol. Biol. 11: 20. 10.1186/1471-2199-11-20. 20211024.
24. Chaumeil J. Waters P.D. Koina E. Gilbert C. Robinson T.J. Graves J.A. 2011. Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS One, 6 (4): e19040. 10.1371/journal.pone.0019040. 21541345.
25. Chow J.C. Hall L.L. Baldry S.E. Thorogood N.P. Lawrence J.B. Brown C.J. 2007. Inducible XIST-dependent X-chromosome inactivation in human somatic cells is reversible. Proc. Natl. Acad. Sci. U.S.A. 104 (24): 10104-10109. 10.1073/pnas.0610946104. 17537922.
26. Chow J.C. Ciaudo C. Fazzari M.J. Mise N. Servant N. Glass J.L. et al 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell, 141 (6): 956-969. 10.1016/j.cell.2010.04.042. 20550932.
27. Chu C. Zhang Q.C. da Rocha S.T. Flynn R.A. Bharadwaj M. Calabrese J.M. et al 2015. Systematic discovery of xist RNA binding proteins. Cell, 161 (2): 404-416. 10.1016/j.cell.2015.03.025. 25843628.
28. Chureau C. Chantalat S. Romito A. Galvani A. Duret L. Avner P. Rougeulle C. 2011. Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Hum. Mol. Genet. 20 (4): 705-718. 10.1093/hmg/ddq516. 21118898.
29. Clemson C.M. McNeil J.A. Willard H.F. Lawrence J.B. 1996. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132 (3): 259-275. 10.1083/jcb.132.3.259. 8636206.
30. Cotton A.M. Lam L. Affleck J.G. Wilson I.M. Penaherrera M.S. McFadden D.E. et al 2011. Chromosome-wide DNA methylation analysis predicts human tissue-specific X inactivation. Hum. Genet. 130 (2): 187-201. 10.1007/s00439-011-1007-8. 21597963.
31. Csankovszki G. Panning B. Bates B. Pehrson J.R. Jaenisch R. 1999. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat. Genet. 22 (4): 323-324. 10.1038/11887. 10431231.
32. Csankovszki G. Nagy A. Jaenisch R. 2001. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153 (4): 773-784. 10.1083/jcb.153.4.773. 11352938.
33. da Rocha S.T. Boeva V. Escamilla-Del-Arenal M. Ancelin K. Granier C. Matias N.R. et al 2014. Jarid2 Is Implicated in the Initial Xist-Induced Targeting of PRC2 to the Inactive X Chromosome. Mol. Cell, 53 (2): 301-316. 10.1016/j.molcel.2014.01.002. 24462204.
34. de Napoles M. Mermoud J.E. Wakao R. Tang Y.A. Endoh M. Appanah R. et al 2004. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell, 7 (5): 663-676. 10.1016/j.devcel.2004.10.005. 15525528.
35. Elisaphenko E.A. Kolesnikov N.N. Shevchenko A.I. Rogozin I.B. Nesterova T.B. Brockdorff N. Zakian S.M. 2008. A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS One, 3 (6): e2521. 10.1371/journal.pone.0002521. 18575625.
36. Engreitz J.M. Pandya-Jones A. McDonel P. Shishkin A. Sirokman K. Surka C. et al 2013. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science, 341 (6147): 1237973. 10.1126/science.1237973. 23828888.
37. Escamilla-Del-Arenal M. da Rocha S.T. Spruijt C.G. Masui O. Renaud O. Smits A.H. et al 2013. Cdyl, a new partner of the inactive X chromosome and potential reader of H3K27me3 and H3K9me2. Mol. Cell. Biol. 33 (24): 5005-5020. 10.1128/MCB.00866-13. 24144980.
38. Essien K. Vigneau S. Apreleva S. Singh L.N. Bartolomei M.S. Hannenhalli S. 2009. CTCF binding site classes exhibit distinct evolutionary, genomic, epigenomic and transcriptomic features. Genome Biol. 10 (11): R131. 10.1186/gb-2009-10-11-r131. 19922652.
39. Fang J. Chen T. Chadwick B. Li E. Zhang Y. 2004. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279 (51): 52812-52815. 10.1074/jbc.C400493200. 15509584.
40. Filippova G.N. Cheng M.K. Moore J.M. Truong J.P. Hu Y.J. Nguyen D.K. et al 2005. Boundaries between chromosomal domains of X inactivation and escape bind CTCF and lack CpG methylation during early development. Dev. Cell, 8 (1): 31-42. 10.1016/j.devcel.2004.10.018. 15669143.
41. Franz H. Mosch K. Soeroes S. Urlaub H. Fischle W. 2009. Multimerization and H3K9me3 binding are required for CDYL1b heterochromatin association. J. Biol. Chem. 284 (50): 35049-35059. 10.1074/jbc.M109.052332. 19808672.
42. Gamble M.J. Frizzell K.M. Yang C. Krishnakumar R. Kraus W.L. 2010. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 24 (1): 21-32. 10.1101/gad.1876110. 20008927.
43. Gao Z. Zhang J. Bonasio R. Strino F. Sawai A. Parisi F. Kluger Y. Reinberg D. 2012. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell, 45 (3): 344-356. 10.1016/j.molcel.2012.01.002. 22325352.
44. Gendrel A.V. Apedaile A. Coker H. Termanis A. Zvetkova I. Godwin J. et al 2012. Smchd1-dependent and-independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev. Cell, 23 (2): 265-279. 10.1016/j.devcel.2012.06.011. 22841499.
45. Gil J. OLoghlen A. 2014. PRC1 complex diversity: where is it taking us? Trends Cell Biol. 24 (11): 632-641. 10.1016/j.tcb.2014.06.005. 25065329.
46. Gontan C. Achame E.M. Demmers J. Barakat T.S. Rentmeester E. van IJcken W. et al 2012. RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature, 485 (7398): 386-390. 10.1038/nature11070. 22596162.
47. Gorlach M. Wittekind M. Beckman R.A. Mueller L. Dreyfuss G. 1992. Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 11 (9): 3289-3295. 1380452.
48. Grant J. Mahadevaiah S.K. Khil P. Sangrithi M.N. Royo H. Duckworth J. et al 2012. Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature, 487 (7406): 254-258. 10.1038/nature11171. 22722828.
49. Hansen R.S. Stoger R. Wijmenga C. Stanek A.M. Canfield T.K. Luo P. et al 2000. Escape from gene silencing in ICF syndrome: evidence for advanced replication time as a major determinant. Hum. Mol. Genet. 9 (18): 2575-2587. 10.1093/hmg/9.18.2575. 11063717.
50. Hasegawa Y. Brockdorff N. Kawano S. Tsutui K. Tsutui K. Nakagawa S. 2010. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell, 19 (3): 469-476. 10.1016/j.devcel.2010.08.006. 20833368.
51. Heard E. Rougeulle C. Arnaud D. Avner P. Allis C.D. Spector D.L. 2001. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell, 107 (6): 727-738. 10.1016/S0092-8674(01)00598-0. 11747809.
52. Helbig R. Fackelmayer F.O. 2003. Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma, 112 (4): 173-182. 10.1007/s00412-003-0258-0. 14608463.
53. Hellman A. Chess A. 2007. Gene body-specific methylation on the active X chromosome. Science, 315 (5815): 1141-1143. 10.1126/science.1136352. 17322062.
54. Hernandez-Munoz I. Lund A.H. van der Stoop P. Boutsma E. Muijrers I. Verhoeven E. et al 2005. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc. Natl. Acad. Sci. U.S.A. 102 (21): 7635-7640. 10.1073/pnas.0408918102. 15897469.
55. Hiragami-Hamada K. Shinmyozu K. Hamada D. Tatsu Y. Uegaki K. Fujiwara S. Nakayama J. 2011. N-terminal phosphorylation of HP1{alpha} promotes its chromatin binding. Mol. Cell. Biol. 31 (6): 1186-1200. 10.1128/MCB.01012-10. 21245376.
56. Horakova A.H. Calabrese J.M. McLaughlin C.R. Tremblay D.C. Magnuson T. Chadwick B.P. 2012 a. The mouse DXZ4 homolog retains Ctcf binding and proximity to Pls3 despite substantial organizational differences compared to the primate macrosatellite. Genome Biol. 13 (8): R70. 10.1186/gb-2012-13-8-r70. 22906166.
57. Horakova A.H. Moseley S.C. McLaughlin C.R. Tremblay D.C. Chadwick B.P. 2012 b. The macrosatellite DXZ4 mediates CTCF-dependent long-range intrachromosomal interactions on the human inactive X chromosome. Hum. Mol. Genet. 21 (20): 4367-4377. 10.1093/hmg/dds270. 22791747.
58. Jeon Y. Lee J.T. 2011. YY1 tethers Xist RNA to the inactive X nucleation center. Cell, 146 (1): 119-133. 10.1016/j.cell.2011.06.026. 21729784.
59. Jeppesen P. Turner B.M. 1993. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell, 74 (2): 281-289. 10.1016/0092-8674(93)90419-Q. 8343956.
60. Jiang J. Jing Y. Cost G.J. Chiang J.C. Kolpa H.J. Cotton A.M. et al 2013. Translating dosage compensation to trisomy 21. Nature, 500 (7462): 296-300. 10.1038/nature12394. 23863942.
61. Jones P.A. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13 (7): 484-492. 10.1038/nrg3230. 22641018.
62. Jonkers I. Barakat T.S. Achame E.M. Monkhorst K. Kenter A. Rentmeester E. et al 2009. RNF12 is an X-Encoded dose-dependent activator of X chromosome inactivation. Cell, 139 (5): 999-1011. 10.1016/j.cell.2009.10.034. 19945382.
63. Kalantry S. Magnuson T. 2006. The Polycomb group protein EED is dispensable for the initiation of random X-chromosome inactivation. PLoS Genet. 2 (5): e66. 10.1371/journal.pgen.0020066. 16680199.
64. Kalantry S. Purushothaman S. Bowen R.B. Starmer J. Magnuson T. 2009. Evidence of Xist RNA-independent initiation of mouse imprinted X-chromosome inactivation. Nature, 460 (7255): 647-651. 10.1038/nature08161. 19571810.
65. Kaneko S. Li G. Son J. Xu C.F. Margueron R. Neubert T.A. Reinberg D. 2010. Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev. 24 (23): 2615-2620. 10.1101/gad.1983810. 21123648.
66. Kapoor-Vazirani P. Vertino P.M. 2014. A dual role for the histone methyltransferase PR-SET7/SETD8 and histone H4 lysine 20 monomethylation in the local regulation of RNA polymerase II pausing. J. Biol. Chem. 289 (11): 7425-7437. 10.1074/jbc.M113.520783. 24459145.
67. Kapoor-Vazirani P. Kagey J.D. Vertino P.M. 2011. SUV420H2-mediated H4K20 trimethylation enforces RNA polymerase II promoter-proximal pausing by blocking hMOF-dependent H4K16 acetylation. Mol. Cell. Biol. 31 (8): 1594-1609. 10.1128/MCB.00524-10. 21321083.
68. Kay G.F. Penny G.D. Patel D. Ashworth A. Brockdorff N. Rastan S. 1993. Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation. Cell, 72 (2): 171-182. 10.1016/0092-8674(93)90658-D. 8425217.
69. Keohane A.M. Lavender J.S. ONeill L.P. Turner B.M. 1998. Histone acetylation and X inactivation. Dev. Genet. 22 (1): 65-73. 10.1002/(SICI)1520-6408(1998)22:1%3C65::AID-DVG7%3E3.0.CO;2-5. 9499581.
70. Kim J.D. Hinz A.K. Bergmann A. Huang J.M. Ovcharenko I. Stubbs L. Kim J. 2006. Identification of clustered YY1 binding sites in imprinting control regions. Genome Res. 16 (7): 901-911. 10.1101/gr.5091406. 16760423.
71. Koina E. Chaumeil J. Greaves I.K. Tremethick D.J. Graves J.A. 2009. Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosome Res. 17 (1): 115-126. 10.1007/s10577-009-9020-7. 19214764.
72. Lachner M. OCarroll D. Rea S. Mechtler K. Jenuwein T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature, 410 (6824): 116-120. 10.1038/35065132. 11242053.
73. Lee J.T. Bartolomei M.S. 2013. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell, 152 (6): 1308-1323. 10.1016/j.cell.2013.02.016. 23498939.
74. Lee J.T. Davidow L.S. Warshawsky D. 1999. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat. Genet. 21 (4): 400-404. 10.1038/7734. 10192391.
75. Leeb M. Wutz A. 2007. Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J. Cell Biol. 178 (2): 219-229. 10.1083/jcb.200612127. 17620408.
76. Lewis E.B. 1998. The bithorax complex: the first fifty years. Int. J. Dev. Biol. 42 (3): 403-415. 9654025.
77. Lleres D. Denegri M. Biggiogera M. Ajuh P. Lamond A.I. 2010. Direct interaction between hnRNP-M and CDC5L/PLRG1 proteins affects alternative splice site choice. EMBO Rep. 11 (6): 445-451. 10.1038/embor.2010.64. 20467437.
78. Lomberk G. Bensi D. Fernandez-Zapico M.E. Urrutia R. 2006. Evidence for the existence of an HP1-mediated subcode within the histone code. Nat. Cell Biol. 8 (4): 407-415. 10.1038/ncb1383. 16531993.
79. Lyon M.F. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature, 190: 372-373. 10.1038/190372a0. 13764598.
80. Lyon M.F. 1998. X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80 (1-4): 133-137. 10.1159/000014969. 9678347.
81. Maenner S. Blaud M. Fouillen L. Savoye A. Marchand V. Dubois A. et al 2010. 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biol. 8 (1): e1000276. 10.1371/journal.pbio.1000276. 20052282.
82. Makhlouf M. Ouimette J.F. Oldfield A. Navarro P. Neuillet D. Rougeulle C. 2014. A prominent and conserved role for YY1 in Xist transcriptional activation. Nat. Commun. 5: 4878. 10.1038/ncomms5878. 25209548.
83. Margueron R. Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature, 469 (7330): 343-349. 10.1038/nature09784. 21248841.
84. Margueron R. Li G. Sarma K. Blais A. Zavadil J. Woodcock C.L. et al 2008. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell, 32 (4): 503-518. 10.1016/j.molcel.2008.11.004. 19026781.
85. Marks H. Chow J.C. Denissov S. Francoijs K.J. Brockdorff N. Heard E. Stunnenberg H.G. 2009. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res. 19 (8): 1361-1373. 10.1101/gr.092643.109. 19581487.
86. McHugh C.A. Chen C.K. Chow A. Surka C.F. Tran C. McDonel P. et al 2015. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature, 521: 232-236. 10.1038/nature14443. 25915022.
87. Mermoud J.E. Popova B. Peters A.H. Jenuwein T. Brockdorff N. 2002. Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr. Biol. 12 (3): 247-251. 10.1016/S0960-9822(02)00660-7. 11839280.
88. Mietton F. Sengupta A.K. Molla A. Picchi G. Barral S. Heliot L. et al 2009. Weak but uniform enrichment of the histone variant macroH2A1 along the inactive X chromosome. Mol. Cell. Biol. 29 (1): 150-156. 10.1128/MCB.00997-08. 18936163.
89. Migeon B.R. Do T.T. 1979. In search of non-random X inactivation: studies of fetal membranes heterozygous for glucose-6-phosphate dehydrogenase. Am. J. Hum. Genet. 31 (5): 581-585. 507052.
90. Migeon B.R. Wolf S.F. Axelman J. Kaslow D.C. Schmidt M. 1985. Incomplete X chromosome dosage compensation in chorionic villi of human placenta. Proc. Natl. Acad. Sci. U.S.A. 82 (10): 3390-3394. 10.1073/pnas.82.10.3390. 3858827.
91. Migeon B.R. Lee C.H. Chowdhury A.K. Carpenter H. 2002. Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation. Am. J. Hum. Genet. 71 (2): 286-293. 10.1086/341605. 12023758.
92. Minkovsky A. Sahakyan A. Rankin-Gee E. Bonora G. Patel S. Plath K. 2014. The Mbd1-Atf7ip-Setdb1 pathway contributes to the maintenance of X chromosome inactivation. Epigenetics Chromatin, 7: 12. 10.1186/1756-8935-7-12. 25028596.
93. Minks J. Baldry S.E. Yang C. Cotton A.M. Brown C.J. 2013. XIST-induced silencing of flanking genes is achieved by additive action of repeat a monomers in human somatic cells. Epigenetics Chromatin, 6 (1): 23. 10.1186/1756-8935-6-23. 23915978.
94. Morey L. Aloia L. Cozzuto L. Benitah S.A. Di Croce L. 2013. RYBP and Cbx7 define specific biological functions of polycomb complexes in mouse embryonic stem cells. Cell Rep. 3 (1): 60-69. 10.1016/j.celrep.2012.11.026. 23273917.
95. Nakagawa S. Prasanth K.V. 2011. eXIST with matrix-associated proteins. Trends Cell Biol. 21 (6): 321-327. 10.1016/j.tcb.2011.02.001. 21392997.
96. Nechanitzky R. Davila A. Savarese F. Fietze S. Grosschedl R. 2012. Satb1 and Satb2 are dispensable for X chromosome inactivation in mice. Dev. Cell, 23 (4): 866-871. 10.1016/j.devcel.2012.09.018. 23079603.
97. Nesterova T.B. Slobodyanyuk S.Y. Elisaphenko E.A. Shevchenko A.I. Johnston C. Pavlova M.E. et al 2001. Characterization of the genomic Xist locus in rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. Genome Res. 11 (5): 833-849. 10.1101/gr.174901. 11337478.
98. Nishibuchi G. Machida S. Osakabe A. Murakoshi H. Hiragami-Hamada K. Nakagawa R. et al 2014. N-terminal phosphorylation of HP1alpha increases its nucleosome-binding specificity. Nucleic Acids Res. 42 (20): 12498-12511. 10.1093/nar/gku995. 25332400.
99. Nora E.P. Heard E. 2010. Chromatin structure and nuclear organization dynamics during X-chromosome inactivation. Cold Spring Harb. Symp. Quant. Biol. 75: 333-344. 10.1101/sqb.2010.75.032. 21447823.
100. Nozawa R.S. Nagao K. Igami K.T. Shibata S. Shirai N. Nozaki N. et al 2013. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat. Struct. Mol. Biol. 20 (5): 566-573. 10.1038/nsmb.2532. 23542155.
101. Ohno S. Kaplan W.D. Kinosita R. 1959. Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus norvegicus. Exp. Cell Res. 18: 415-418. 10.1016/0014-4827(59)90031-X. 14428474.
102. Olins A.L. Rhodes G. Welch D.B. Zwerger M. Olins D.E. 2010. Lamin B receptor: multi-tasking at the nuclear envelope. Nucleus, 1 (1): 53-70. 10.4161/nucl.1.1.10515. 21327105.
103. OLoghlen A. Munoz-Cabello A.M. Gaspar-Maia A. Wu H.A. Banito A. Kunowska N. et al 2012. MicroRNA regulation of Cbx7 mediates a switch of Polycomb orthologs during ESC differentiation. Cell Stem Cell, 10 (1): 33-46. 10.1016/j.stem.2011.12.004. 22226354.
104. Pehrson J.R. Changolkar L.N. Costanzi C. Leu N.A. 2014. Mice without macroH2A histone variants. Mol. Cell. Biol. 34 (24): 4523-4533. 10.1128/MCB.00794-14. 25312643.
105. Peters A.H. Kubicek S. Mechtler K. OSullivan R.J. Derijck A.A. Perez-Burgos L. et al 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell, 12 (6): 1577-1589. 10.1016/S1097-2765(03)00477-5. 14690609.
106. Plath K. Fang J. Mlynarczyk-Evans S.K. Cao R. Worringer K.A. Wang H. et al 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science, 300 (5616): 131-135. 10.1126/science.1084274. 12649488.
107. Pullirsch D. Hartel R. Kishimoto H. Leeb M. Steiner G. Wutz A. 2010. The Trithorax group protein Ash2l and Saf-A are recruited to the inactive X chromosome at the onset of stable X inactivation. Development, 137 (6): 935-943. 10.1242/dev.035956. 20150277.
108. Rens W. Wallduck M.S. Lovell F.L. Ferguson-Smith M.A. Ferguson-Smith A.C. 2010. Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc. Natl. Acad. Sci. U.S.A. 107 (41): 17657-17662. 10.1073/pnas.0910322107. 20861449.
109. Rinn J.L. Chang H.Y. 2012. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81: 145-166. 10.1146/annurev-biochem-051410-092902. 22663078.
110. Rougeulle C. Chaumeil J. Sarma K. Allis C.D. Reinberg D. Avner P. Heard E. 2004. Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol. Cell. Biol. 24 (12): 5475-5484. 10.1128/MCB.24.12.5475-5484.2004. 15169908.
111. Russo V. Bernabo N. Di Giacinto O. Martelli A. Mauro A. Berardinelli P. et al 2013. H3K9 trimethylation precedes DNA methylation during sheep oogenesis: HDAC1, SUV39H1, G9a, HP1, and Dnmts are involved in these epigenetic events. J. Histochem. Cytochem. 61 (1): 75-89. 10.1369/0022155412463923. 23019017.
112. Sado T. Fenner M.H. Tan S.S. Tam P. Shioda T. Li E. 2000. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev. Biol. 225 (2): 294-303. 10.1006/dbio.2000.9823. 10985851.
113. Sarma K. Cifuentes-Rojas C. Ergun A. Del Rosario A. Jeon Y. White F. et al 2014. ATRX directs binding of PRC2 to Xist RNA and Polycomb targets. Cell, 159 (4): 869-883. 10.1016/j.cell.2014.10.019. 25417162.
114. Savarese F. Davila A. Nechanitzky R. De La Rosa-Velazquez I. Pereira C.F. Engelke R. et al 2009. Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev. 23 (22): 2625-2638. 10.1101/gad.1815709. 19933152.
115. Schoeftner S. Sengupta A.K. Kubicek S. Mechtler K. Spahn L. Koseki H. et al 2006. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25 (13): 3110-3122. 10.1038/sj.emboj.7601187. 16763550.
116. Shahbazian M.D. Grunstein M. 2007. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76: 75-100. 10.1146/annurev.biochem.76.052705.162114. 17362198.
117. Shaver S. Casas-Mollano J.A. Cerny R.L. Cerutti H. 2010. Origin of the polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics, 5 (4): 301-312. 10.4161/epi.5.4.11608. 20421736.
118. Shinkai Y. 2007. Regulation and function of H3K9 methylation. Subcell. Biochem. 41: 337-350. 10.1007/1-4020-5466-1-15. 17484135.
119. Simon M.D. Pinter S.F. Fang R. Sarma K. Rutenberg-Schoenberg M. Bowman S.K. et al 2013. High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature, 504 (7480): 465-469. 10.1038/nature12719. 24162848.
120. Smeets D. Markaki Y. Schmid V.J. Kraus F. Tattermusch A. Cerase A. et al 2014. 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 Chromatin, 7: 8. 10.1186/1756-8935-7-8. 25057298.
121. Sun S. Del Rosario B.C. Szanto A. Ogawa Y. Jeon Y. Lee J.T. 2013. Jpx RNA activates Xist by evicting CTCF. Cell, 153 (7): 1537-1551. 10.1016/j.cell.2013.05.028. 23791181.
122. Tavares L. Dimitrova E. Oxley D. Webster J. Poot R. Demmers J. et al 2012. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell, 148 (4): 664-678. 10.1016/j.cell.2011.12.029. 22325148.
123. Thorvaldsen J.L. Weaver J.R. Bartolomei M.S. 2011. A YY1 bridge for X inactivation. Cell, 146 (1): 11-13. 10.1016/j.cell.2011.06.029. 21729777.
124. Tian D. Sun S. Lee J.T. 2010. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell, 143 (3): 390-403. 10.1016/j.cell.2010.09.049. 21029862.
125. Trojer P. Li G. Sims R.J. III Vaquero A. Kalakonda N. Boccuni P. et al 2007. L3MBTL1, a histone-methylation-dependent chromatin lock. Cell, 129 (5): 915-928. 10.1016/j.cell.2007.03.048. 17540172.
126. Turner S.A. Bracken A.P. 2013. A "complex" issue: deciphering the role of variant PRC1 in ESCs. Cell Stem Cell, 12 (2): 145-146. 10.1016/j.stem.2013.01.014. 23395440.
127. Urbach A. Benvenisty N. 2009. Studying early lethality of 45, XO (Turners syndrome) embryos using human embryonic stem cells. PLoS One, 4 (1): e4175. 10.1371/journal.pone.0004175. 19137066.
128. Vaskova E.A. Dementyeva E.V. Shevchenko A.I. Pavlova S.V. Grigoreva E.V. Zhelezova A.I. et al 2014. Dynamics of the two heterochromatin types during imprinted X chromosome inactivation in vole Microtus levis. PLoS One, 9 (2): e88256. 10.1371/journal.pone.0088256. 24505450.
129. Visootsak J. Graham J.M. Jr 2009. Social function in multiple X and Y chromosome disorders: XXY, XYY, XXYY, XXXY. Dev. Disabil. Res. Rev. 15 (4): 328-332. 10.1002/ddrr.76. 20014367.
130. Wang Z. Zang C. Rosenfeld J.A. Schones D.E. Barski A. Cuddapah S. et al 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40 (7): 897-903. 10.1038/ng.154. 18552846.
131. Wongtawan T. Taylor J.E. Lawson K.A. Wilmut I. Pennings S. 2011. Histone H4K20me3 and HP1alpha are late heterochromatin markers in development, but present in undifferentiated embryonic stem cells. J. Cell Sci. 124 (11): 1878-1890. 10.1242/jcs.080721. 21576353.
132. Woo C.J. Kharchenko P.V. Daheron L. Park P.J. Kingston R.E. 2010. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell, 140 (1): 99-110. 10.1016/j.cell.2009.12.022. 20085705.
133. Wu H. Min J. Lunin V.V. Antoshenko T. Dombrovski L. Zeng H. et al 2010. Structural biology of human H3K9 methyltransferases. PLoS One, 5 (1): e8570. 10.1371/journal.pone.0008570. 20084102.
134. Wu H. Zhang H. Wang P. Mao Z. Feng L. Wang Y. et al 2013. Short-Form CDYLb but not long-form CDYLa functions cooperatively with histone methyltransferase G9a in hepatocellular carcinomas. Genes Chromosomes Cancer, 52 (7): 644-655. 10.1002/gcc.22060. 23629948.
135. Wutz A. 2011. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12 (8): 542-553. 10.1038/nrg3035. 21765457.
136. Wutz A. Gribnau J. 2007. X inactivation Xplained. Curr. Opin. Genet. Dev. 17 (5): 387-393. 10.1016/j.gde.2007.08.001. 17869504.
137. Xu C. Bian C. Yang W. Galka M. Ouyang H. Chen C. et al 2010. Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc. Natl. Acad. Sci. U.S.A. 107 (45): 19266-19271. 10.1073/pnas.1008937107. 20974918.
138. Yamamoto K. Sonoda M. Inokuchi J. Shirasawa S. Sasazuki T. 2004. Polycomb group suppressor of zeste 12 links heterochromatin protein 1alpha and enhancer of zeste 2. J. Biol. Chem. 279 (1): 401-406. 10.1074/jbc.M307344200. 14570930.
139. Yang F. Deng X. Ma W. Berletch J.B. Rabaia N. Wei G. et al 2015. The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Genome Biol. 16: 52. 10.1186/s13059-015-0618-0. 25887447.
140. Yasukochi Y. Maruyama O. Mahajan M.C. Padden C. Euskirchen G.M. Schulz V. et al 2010. X chromosome-wide analyses of genomic DNA methylation states and gene expression in male and female neutrophils. Proc. Natl. Acad. Sci. U.S.A. 107 (8): 3704-3709. 10.1073/pnas.0914812107. 20133578.
141. Yen Z.C. Meyer I.M. Karalic S. Brown C.J. 2007. A cross-species comparison of X-chromosome inactivation in Eutheria. Genomics, 90 (4): 453-463. 10.1016/j.ygeno.2007.07.002. 15992682.
142. Zhang Y. Yang X. Gui B. Xie G. Zhang D. Shang Y. Liang J. 2011. Corepressor protein CDYL functions as a molecular bridge between polycomb repressor complex 2 and repressive chromatin mark trimethylated histone lysine 27. J. Biol. Chem. 286 (49): 42414-42425. 10.1074/jbc.M111.271064. 22009739.
143. Zhao J. Sun B.K. Erwin J.A. Song J.J. Lee J.T. 2008. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science, 322 (5902): 750-756. 10.1126/science.1163045. 18974356.