Advances in understanding chromosome silencing by the long non-coding RNA Xist

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1609, 2013, Pages

  Sado, Takashi ^a   Brockdorff, Neil ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Silencing compartment; X chromosome; Xist RNA

Indexed keywords

CHROMOSOME; FEMALE; GENE EXPRESSION; GENOMICS; GENOTYPE; HERITABILITY; MAMMAL; MOLECULAR ANALYSIS; PHYSIOLOGY; RNA;

CELL CYCLE PROTEIN; HISTONE; LONG UNTRANSLATED RNA; PRC1 PROTEIN, HUMAN; XIST NON CODING RNA; XIST NON-CODING RNA;

ALLELE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; FEMALE; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MALE; METABOLISM; REVIEW; X CHROMOSOMAL INHERITANCE; X CHROMOSOME; X CHROMOSOME INACTIVATION;

ALLELES; ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CHROMOSOMES, HUMAN, X; EMBRYONIC STEM CELLS; FEMALE; GENES, X-LINKED; GENETIC LOCI; HISTONES; HUMANS; MALE; RNA, LONG UNTRANSLATED; TRANSCRIPTION, GENETIC; X CHROMOSOME INACTIVATION;

EID: 84876546175     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0325     Document Type: Review

References (87)

1. Lyon MF. 1961 Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190, 372-373. (doi:10.1038/190372a0)
2. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HJ. 1991 A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349, 38-44. (doi:10.1038/349038a0)
3. Brockdorff N et al. 1991 Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351, 329-331. (doi:10.1038/351329a0)
4. Borsani G et al. 1991 Characterization of a murine gene expressed from the inactive X chromosome. Nature 351, 325-329. (doi:10.1038/351325a0)
5. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF. 1992 The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71, 527-542. (doi:10.1016/0092-8674(92)90520-M)
6. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S. 1992 The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71, 515-526. (doi:10.1016/0092-8674(92)90519-I)
7. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. 1997 Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 11, 156-166. (doi:10.1101/gad.11.2.156)
8. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. 1996 Requirement for Xist in X chromosome inactivation. Nature 379, 131-137. (doi:10.1038/379131a0)
9. Sheardown SA et al. 1997 Stabilization of Xist RNA mediates initiation of X chromosome inactivation. Cell 91, 99-107. (doi:10.1016/S0092-8674(01)80012-X)
10. Panning B, Jaenisch R. 1996 DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev. 10, 1991-2002. (doi:10.1101/gad.10.16.1991)
11. Herzing LBK, Romer JT, Horn JM, Ashworth A. 1997 Xist has properties of the X-chromosome inactivation centre. Nature 386, 272-275. (doi:10.1038/386272a0)
12. Lee J, Strauss WM, Dausman JA, Jaenisch R. 1996 A 450 kb transgene displays properties of the mammalian X-inactivation center. Cell 86, 83-94. (doi:10.1016/S0092-8674(00)80079-3)
13. Lee J, Davidow LS, Warshawsky D. 1999 Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet. 21, 400-404. (doi:10.1038/7734)
14. Lee JT. 2000 Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell 103, 17-27. (doi:10.1016/S0092-8674(00)00101-X)
15. Sado T, Wang Z, Sasaki H, Li E. 2001 Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development 128, 1275-1286.
16. Sado T, Hoki Y, Sasaki H. 2005 Tsix silences Xist through modification of chromatin structure. Dev Cell. 9, 159-165. (doi:10.1016/j. devcel.2005.05.015)
17. Navarro P, Pichard S, Ciaudo C, Avner P, Rougeulle C. 2005 Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev. 19, 1474-1484. (doi:10. 1101/gad.341105)
18. Sun BK, Deaton AM, Lee JT. 2006 A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol. Cell. 21, 617-628. (doi:10.1016/j.molcel.2006.01.028)
19. Bacher CP, Guggiari M, Brors B, Augui S, Clerc P, Avner P, Elis R, Heard E. 2006 Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat. Cell Biol. 8, 293-299. (doi:10.1038/ncb1365)
20. Xu N, Tsai CL, Lee JT. 2006 Transient homologous chromosome pairing marks the onset of X inactivation. Science 311, 1149-1152. (doi:10. 1126/science.1122984)
21. Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P. 2008 Molecular coupling of Xist regulation and pluripotency. Science 321, 1693-1695. (doi:10.1126/science.1160952)
22. Navarro P et al. 2010 Molecular coupling of Tsix regulation and pluripotency. Nature 468, 457-460. (doi:10.1038/nature09496)
23. Donohoe ME, Silva SS, Pinter SF, Xu N, Lee JT. 2009 The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 460, 128-132. (doi:10.1038/nature08098)
24. Jonkers I, Barakat TS, Achame EM, Monkhorst K, Kenter A, Rentmeester E, Grosveld F, Grootegoed JA, Gribnau J. 2009 RNF12 is an X-encoded dosedependent activator of X chromosome inactivation. Cell 139, 999-1011. (doi:10.1016/j. cell.2009.10.034)
25. Tian D, Sun S, Lee JT. 2010 The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143, 390-403. (doi:10.1016/j.cell. 2010.09.049)
26. Wutz A, Rasmussen TP, Jaenisch R. 2002 Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30, 167-174. (doi:10.1038/ng820)
27. Barakat TS, Jonkers I, Monkhorst K, Gribnau J. 2010 X-changing information on X inactivation. Exp. Cell Res. 316, 679-687. (doi:10.1016/j.yexcr. 2010.01.015)
28. Jeon Y, Sarma K, Lee JT. 2012 New and Xisting regulatory mechanisms of X chromosome inactivation. Curr. Opin. Genet. Dev. 22, 62-71. (doi:10.1016/j.gde.2012.02.007)
29. Brockdorff N. 2011 Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns. Development 138, 5057-5065. (doi:10.1242/dev.065276)
30. Ma M, Strauss WM. 2005 Analysis of the Xist RNA isoforms suggests two distinctly different forms of regulation. Mamm. Genome 16, 391-404. (doi:10. 1007/s00335-004-2464-3)
31. Beletskii A, Hong YK, Pehrson J, Egholm M, Strauss WM. 2001 PNA interference mapping demonstrates functional domains in the noncoding RNA Xist. Proc. Natl Acad. Sci. USA 98, 9215-9220. (doi:10.1073/pnas.161173098)
32. Sarma K, Levasseur P, Aristarkhov A, Lee JT. 2010 Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc. Natl Acad. Sci. USA 107, 22 196-22 201. (doi:10.1073/pnas.1009785107)
33. Jeon Y, Lee JT. 2011 YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146, 119-133. (doi:10.1016/j.cell.2011.06.026)
34. Duszczyk MM, Wutz A, Rybin V, Sattler M. 2011 The Xist RNA A-repeat comprises a novel AUCG tetraloop fold and a platform for multimerization. RNA 17, 1973-1982. (doi:10.1261/rna.2747411)
35. Maenner S et al. 2010 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biol. 8, e1000276. (doi:10.1371/journal.pbio. 1000276)
36. Royce-Tolland ME, Andersen AA, Koyfman HR, Talbot DJ, Wutz A, Tonks ID, Kay GF, Panning B. 2010 The A-repeat links ASF/SF2-dependent Xist RNA processing with random choice during X inactivation. Nat. Struct. Mol. Biol. 17, 948-954. (doi:10.1038/nsmb.1877)
37. Hoki Y, Kimura N, Kanbayashi M, Amakawa Y, Ohhata T, Sasaki H, Sado T. 2009 A proximal conserved repeat in the Xist gene is essential as a genomic element for X-inactivation in mouse. Development 136, 139-146. (doi:10.1242/dev. 026427)
38. Caparros ML, Alexiou M, Webster Z, Brockdorff N. 2002 Functional analysis of the highly conserved exon IV of Xist RNA. Cytogenet. Genome Res. 99, 99-105. (doi:10.1159/000071580)
39. Senner CE, Nesterova TB, Norton S, Dewchand H, Godwin J, Mak W, Brockdorff N. 2011 Disruption of a conserved region of Xist exon 1 impairs Xist RNA localisation and X-linked gene silencing during random and imprinted X chromosome inactivation. Development 138, 1541-1550. (doi:10.1242/dev.056812)
40. Hoki Y, Ikeda R, Mise N, Sakata Y, Ohhata T, Sasaki H, Sado T. 2011 Incomplete X-inactivation initiated by a hypomorphic Xist allele in the mouse. Development 138, 2649-2659. (doi:10.1242/dev.061226)
41. Ohhata T, Hoki Y, Sasaki H, Sado T. 2008 Crucial role of antisense transcription across the Xist promoter in Tsix-mediated Xist chromatin modification. Development 135, 227-235. (doi:10.1242/dev.008490)
42. Kim JD, Hinz AK, Bergmann A, Huang JM, Ovcharenko I, Stubbs L, Kim J. 2006 Identification of clustered YY1 binding sites in imprinting control regions. Genome Res. 16, 901-911. (doi:10.1101/gr.5091406)
43. Clemson CM, McNeil JA, Willard HF, Lawrence JB. 1996 XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132, 259-275. (doi:10.1083/jcb.132.3.259)
44. Helbig R, Fackelmayer FO. 2003 Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma 112, 173-182. (doi:10.1007/s00412-003-0258-0)
45. 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, 935-943. (doi:10.1242/dev.035956)
46. Kipp M, Gohring F, Ostendorp T, van Drunen CM, van Driel R, Przybylski M, Fackelmayer FO. 2000 SAF-Box, a conserved protein domain that specifically recognizes scaffold attachment region DNA. Mol. Cell Biol. 20, 7480-7489. (doi:10.1128/MCB.20.20.7480-7489.2000)
47. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Nakagawa S. 2010 The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19, 469-476. (doi:10.1016/j.devcel. 2010.08.006)
48. Plath K et al. 2003 Role of histone H3 lysine 27 methylation in X inactivation. Science 300, 131-135. (doi:10.1126/science.1084274)
49. Silva J et al. 2003 Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4, 481-495. (doi:10.1016/S1534-5807(03)00068-6)
50. 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, 52 812-52 815. (doi:10.1074/jbc.C400493200)
51. de Napoles M et al. 2004 Polycomb group proteins ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7, 663-676. (doi:10.1016/j.devcel.2004.10.005)
52. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. 2008 Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750-756. (doi:10.1126/science.1163045)
53. Kaneko S, Li G, Son J, Xu CF, Margueron R, Neubert TA, Reinberg D. 2010 Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and upregulates its binding to ncRNA. Genes Dev. 24, 2615-2620. (doi:10.1101/gad.1983810)
54. Kanhere A et al. 2010 Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol. Cell 38, 675-688. (doi:10.1016/j.molcel.2010.03.019)
55. 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, 219-229. (doi:10.1083/jcb. 200612127)
56. Tavares L et al. 2012 RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148, 664-678. (doi:10.1016/j.cell.2011.12.029)
57. Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A. 2004 A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol. 2, E171. (doi:10.1371/journal.pbio.0020171)
58. Chaumeil J, Le Baccon P, Wutz A, Heard E. 2006 A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev. 20, 2223-2237. (doi:10.1101/gad.380906)
59. Csankovszki G, Panning B, Bates B, Pehrson JR, Jaenisch R. 1999 Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat. Genet. 22, 323-324. (doi:10.1038/11887)
60. Brown CJ, Willard HF. 1994 The human Xinactivation centre is not required for maintenance of X-chromosome inactivation. Nature 368, 154-156. (doi:10.1038/368154a0)
61. Ohhata T, Senner CE, Hemberger M, Wutz A. 2011 Lineage-specific function of the noncoding Tsix RNA for Xist repression and Xi reactivation in mice. Genes Dev. 25, 1702-1715. (doi:10.1101/gad.16997911)
62. 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, 773-784. (doi:10. 1083/jcb.153.4.773)
63. Sado T, Fenner MH, Tan SS, 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, 294-303. (doi:10.1006/dbio.2000.9823)
64. Grant J et al. 2012 Rsx, an RNA that exhibits properties consistent with a role in X-chromosome inactivation in metatherian mammals. Nature 487, 254-258. (doi:10.1038/nature11171)
65. Cooper DW, VandeBerg JL, Sharman GB, Poole WE. 1971 Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat. New Biol. 230, 155-157.
66. Kaslow DC, Migeon BR. 1987 DNA methylation stabilizes X chromosome inactivation in eutherians but not in marsupials: evidence for multistep maintenance of mammalian X dosage compensation. Proc. Natl Acad. Sci. USA 84, 6210-6214. (doi:10.1073/pnas.84.17.6210)
67. Al Nadaf S, Waters PD, Koina E, Deakin JE, Jordan KS, Graves JA. 2010 Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Genome Biol. 11, R122. (doi:10.1186/gb-2010-11-12-r122)
68. Mahadevaiah SK, Royo H, VandeBerg JL, McCarrey JR, Mackay S, Turner JM. 2009 Key features of the X inactivation process are conserved between marsupials and eutherians. Curr. Biol. 19, 1478-1484. (doi:10.1016/j.cub.2009.07.041)
69. Graves JA. 1967 DNA synthesis in chromosomes of cultured leucocytes from two marsupial species. Exp. Cell Res. 46, 37-57. (doi:10.1016/0014-4827(67)90407-7)
70. Sharman GB. 1971 Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230, 231-232. (doi:10.1038/230231a0)
71. Wakefield MJ, Keohane AM, Turner BM, Graves JA. 1997 Histone underacetylation is an ancient component of mammalian X chromosome inactivation. Proc. Natl Acad. Sci. USA 94, 9665-9668. (doi:10.1073/pnas.94.18.9665)
72. Chaumeil J, Waters PD, Koina E, Gilbert C, Robinson TJ, Graves JA. 2011 Evolution from XISTindependent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS ONE 6, e19040. (doi:10. 1371/journal.pone.0019040)
73. Rens W, Wallduck MS, Lovell FL, Ferguson-Smith MA, Ferguson-Smith AC. 2010 Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc. Natl Acad. Sci. USA 107, 17 657-17 662. (doi:10.1073/pnas. 0910322107)
74. Zakharova IS, Shevchenko AI, Shilov AG, Nesterova TB, Vandeberg JL, Zakian SM. 2011 Histone H3 trimethylation at lysine 9 marks the inactive metaphase X chromosome in the marsupial Monodelphis domestica. Chromosoma 120, 177-183. (doi:10.1007/s00412-010-0300-y)
75. Loebel DA, Johnston PG. 1996 Methylation analysis of a marsupial X-linked CpG island by bisulfite genomic sequencing. Genome Res. 6, 114-123. (doi:10.1101/gr.6.2.114)
76. Piper AA, Bennett AM, Noyce L, Swanton MK, Cooper DW. 1993 Isolation of a clone partially encoding hill kangaroo X-linked hypoxanthine phosphoribosyltransferase: sex differences in methylation in the body of the gene. Somat. Cell Mol. Genet. 19, 141-159. (doi:10.1007/BF01233530)
77. Elisaphenko EA, Kolesnikov NN, Shevchenko AI, Rogozin IB, Nesterova TB, Brockdorff N, Zakian SM. 2008 A dual origin of the Xist gene from a proteincoding gene and a set of transposable elements. PLoS ONE 3, e2521. (doi:10.1371/journal.pone. 0002521)
78. Duret L, Chureau C, Samain S, Weissenbach J, Avner P. 2006 The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312, 1653-1655. (doi:10.1126/science.1126316)
79. Orishchenko KE, Elisafenko EA, Kel AE, Zakian SM. 2009 Molecular genetic characterization of the regulatory region of the Xist gene in the common vole Microtus rossiaemeridionalis. Genetika 45, 1341-1352.
80. Heard E, Mongelard F, Arnaud D, Chureau C, Vourc'h C, Avner P. 1999 Human XIST yeast artificial chromosome transgenes show partial X inactivation center function in mouse embryonic stem cells. Proc. Natl Acad. Sci. USA 96, 6841-6846. (doi:10. 1073/pnas.96.12.6841)
81. Wutz A, Jaenisch R. 2000 A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol. Cell. 5, 695-705. (doi:10.1016/S1097-2765(00)80248-8)
82. Plath K, Talbot D, Hamer KM, Otte AP, Yang TP, Jaenisch R, Panning B. 2004 Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J. Cell Biol. 167, 1025-1035. (doi:10.1083/jcb. 200409026)
83. Arrigoni R, Alam SL, Wamstad JA, Bardwell VJ, Sundquist WI, Schreiber-Agus N. 2006 The Polycomb-associated protein Rybp is a ubiquitin binding protein. FEBS Lett. 580, 6233-6241. (doi:10.1016/j.febslet.2006.10.027)
84. Mak W, Baxter J, Silva J, Newall AE, Otte AP, Brockdorff N. 2002 Mitotically stable association of polycomb group proteins eed and enx1 with the inactive X chromosome in trophoblast stem cells. Curr. Biol. 12, 1016-1020. (doi:10.1016/S0960-9822(02)00892-8)
85. Costanzi C, Pehrson JR. 1998 Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393, 599-601. (doi:10. 1038/31275)
86. 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, 209-222. (doi:10.1007/s00412-008-0189-x)
87. Blewitt ME et al. 2008 SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 40, 663-669. (doi:10.1038/ng.142)