X chromosome inactivation and embryonic stem cells

Advances in Experimental Medicine and Biology

Volumn 695, Issue , 2010, Pages 132-154

  Stefan Barakat, Tahsin ^b   Gribnau, Joost ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; DICER; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX3; UBIQUITIN PROTEIN LIGASE E3; LONG UNTRANSLATED RNA;

ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CPG ISLAND; DEACETYLATION; DIPLOIDY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HETEROZYGOSITY; HISTONE MODIFICATION; HOMOZYGOSITY; HUMAN; MOLECULAR DYNAMICS; MOLECULAR IMPRINTING; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SOMATIC CELL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UBIQUITINATION; X CHROMOSOME; X CHROMOSOME INACTIVATION; Y CHROMOSOME; ANIMAL; CYTOLOGY; METABOLISM;

IPS;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HUMANS; RNA, LONG NONCODING; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 79959748567     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-7037-4_10     Document Type: Article

References (226)

1. Ohno S. Sex chromosomes and Sex-linked genes. 1967, Berlin: Springer.
2. Charlesworth B. The evolution of sex chromosomes. Science 1991; 251(4997):1030-3. (Pubitemid 21926193)
3. Graves JA. The origin and function of the mammalian Y chromosome and Y-borne genes-an evolving understanding. Bioessays 1995; 17(4):311-20.
4. Graves JA, Koina E, Sankovic N. How the gene content of human sex chromosomes evolved. Curr Opin Genet Dev 2006; 16(3):219-24.
5. Graves JA. Sex chromosome specialization and degeneration in mammals. Cell 2006; 124(5):901-14. (Pubitemid 43344232)
6. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 2003; 423(6942):825-37. (Pubitemid 36781267)
7. Koopman P, Gubbay J, Vivian N et al. Male development of chromosomally female mice transgenic for Sry. Nature 1991; 351(6322):117-21. (Pubitemid 21896542)
8. Ross MT, Grafham DV, Coffey AJ et al. The DNA sequence of the human X chromosome. Nature 2005; 434(7031):325-37. (Pubitemid 40469169)
9. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961; 190:372-3.
10. Lyon MF, Phillips RJ, Searle AG. A test for mutagenicity of caffeine in mice. Z Vererbungsl 1962; 93:7-13.
11. Lyon MF. Sex chromatin and gene action in the mammalian X-chromosome. Am J Hum Genet 1962; 14: 135-48.
12. Davidson RG, Nitowsky HM, Childs B. Demonstration of two populations of cells in the human female heterozygous for glucose-6-phosphate dehydrogenase variants. Proc Natl Acad Sci USA 1963; 50: 481-5.
13. Adler DA, Rugarli EI, Lingenfelter PA et al. Evidence of evolutionary up-regulation of the single active X chromosome in mammals based on Clc4 expression levels in Mus spretus and Mus musculus. Proc Natl Acad Sci USA 1997; 94(17):9244-8. (Pubitemid 27357814)
14. Birchler JA, Fernandez HR, Kavi HH. Commonalities in compensation. Bioessays 2006; 28(6):565-8. (Pubitemid 43886180)
15. Lin H, Gupta V, Vermilyea MD et al. Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 2007; 5(12):e326.
16. Nguyen DK. Disteche CM. Dosage compensation of the active X chromosome in mammals. Nat Genet 2006; 38(1):47-53. (Pubitemid 43011881)
17. Takagi N, Sasaki M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 1975; 256(5519):640-2.
18. Huynh KD, Lee JT. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 2003; 426(6968):857-62. (Pubitemid 38056873)
19. Okamoto I, Otte AP, Allis CD et al. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 2004; 303(5658):644-9. (Pubitemid 38141624)
20. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292(5819):154-6. (Pubitemid 11050741)
21. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78(12):7634-8. (Pubitemid 12186197)
22. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282(5391):1145-7. (Pubitemid 28516247)
23. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 2005; 19(10):1129-55. (Pubitemid 40696181)
24. Leahy A, Xiong JW, Kuhnert F et al. Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J Exp Zool 1999; 284(1):67-81. (Pubitemid 29270636)
25. Monk M. A stem-line model for cellular and chromosomal differentiation in early mouse-development. Differentiation 1981; 19(2):71-6. (Pubitemid 11000551)
26. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4):663-76. (Pubitemid 44233629)
27. Nakagawa M, Koyanagi M, Tanabe K et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008; 26(1):101-6.
28. Wernig M, Meissner A, ForemanRet al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007; 448(7151):318-24. (Pubitemid 47080337)
29. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318(5858):1917-20.
30. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131(5):861-72. (Pubitemid 350138099)
31. Park IH, Zhao R, West JA et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008; 451(7175):141-6.
32. Maherali N, Sridharan R, Xie W et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007; 1(1):55-70.
33. Stadtfeld M, Maherali N, Breault DT et al. Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2008; 2(3):230-40.
34. Russell LB. Mammalian X-chromosome action: inactivation limited in spread and region of origin. Science 1963; 140:976-8.
35. Rastan S. Non-random X-chromosome inactivation in mouse X-autosome translocation embryos-location of the inactivation centre. J Embryol Exp Morphol 1983; 78:1-22. (Pubitemid 14215355)
36. Rastan S, Robertson EJ. X-chromosome deletions in embryo-derived (EK) cell lines associated with lack of X-chromosome inactivation. J Embryol Exp Morphol 1985; 90:379-88. (Pubitemid 16149379)
37. Brown CJ, Ballabio A, Rupert JL et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991; 349(6304):38-44. (Pubitemid 21912005)
38. Heard E, Avner P. Role play in X-inactivation. Hum Mol Genet 1994; 3 Spec No:1481-5.
39. Borsani G, Tonlorenzi R, Simmler MC et al. Characterization of a murine gene expressed from he inactive X chromosome. Nature 1991; 351(6324):325-9. (Pubitemid 21896592)
40. Brockdorff N, Ashworth A, Kay GF et al. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 1991; 351(6324):329-31. (Pubitemid 21896593)
41. Brockdorff N, Ashworth A, Kay GF et al. 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 1992; 71(3):515-26.
42. Brown CJ, Hendrich BD, Rupert JL et al. 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 1992; 71(3):527-42.
43. Clemson CM, McNeil JA, Willard HF et al. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 1996; 132(3):259-75. (Pubitemid 26052564)
44. Jonkers I, Monkhorst K, Rentmeester E et al. Xist RNA is confined to the nuclear territory of the silenced X chromosome throughout the cell cycle. Mol Cell Biol 2008; 28(18):5583-94.
45. Penny GD, Kay GF, Sheardown SA et al. Requirement for Xist in X chromosome inactivation. Nature 1996; 379(6561):131-7. (Pubitemid 26020194)
46. Marahrens Y, Panning B, Dausman J et al. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev 1997; 11(2):156-66. (Pubitemid 27081893)
47. Csankovszki G, Panning B, Bates B et al. Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet 1999; 22(4):323-4. (Pubitemid 29369518)
48. Kay GF, Penny GD, Patel D et al. Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation. Cell 1993; 72(2):171-82. (Pubitemid 23044933)
49. Sun BK, Deaton AM, Lee JT. A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol Cell 2006; 21(5):617-28. (Pubitemid 43290729)
50. Plath K, Fang J, Mlynarczyk-Evans SK et al. Role of histone H3 lysine 27 methylation in X inactivation. Science 2003; 300(5616):131-5. (Pubitemid 36423045)
51. Silva J, Mak W, Zvetkova I et al. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 2003; 4(4):481-95. (Pubitemid 36437556)
52. Zhao J, Sun BK, Erwin JA et al. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008; 322(5902):750-6.
53. Lee JT, Davidow LS, Warshawsky D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 1999; 21(4):400-4. (Pubitemid 29159577)
54. Lee JT, Lu N. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 1999; 99(1):47-57. (Pubitemid 29468629)
55. Clerc P, Avner P. Role of the region 3′ to Xist exon 6 in the counting process of X-chromosome inactivation. Nat Genet 1998; 19(3):249-53. (Pubitemid 28309335)
56. Shibata S, Lee JT. Characterization and quantitation of differential Tsix transcripts: implications for Tsix function. Hum Mol Genet 2003; 12(2):125-36. (Pubitemid 36124448)
57. Marks H, Chow JC, Denissov S et al. High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res 2009; 19(8):1361-73.
58. Luikenhuis S, Wutz A, and Jaenisch R. Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol Cell Biol 2001; 21(24):8512-20. (Pubitemid 33108610)
59. Navarro P, Pichard S, Ciaudo C et al. Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev 2005; 19(12):1474-84. (Pubitemid 41003014)
60. Vigneau S, Augui S, Navarro P et al. An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proc Natl Acad Sci USA 2006; 103(19):7390-5. (Pubitemid 43727843)
61. Ohhata T, Hoki Y, Sasaki H et al. Crucial role of antisense transcription across the Xist promoter in Tsix-mediatedXist chromatinmodification. Development 2008; 135(2):227-35. (Pubitemid 351228415)
62. Cohen DE, Davidow LS, Erwin JA et al. The DXPas34 repeat regulates random and imprinted X inactivation. Dev Cell 2007; 12(1):57-71. (Pubitemid 46002600)
63. Debrand E, Chureau C, Arnaud D et al. Functional analysis of the DXPas34 locus, a 3' regulator of Xist expression. Mol Cell Biol 1999; 19(12):8513-25. (Pubitemid 30414045)
64. Prissette M, El-Maarri O, Arnaud D et al. Methylation profiles of DXPas34 during the onset of X-inactivation. Hum Mol Genet 2001; 10(1):31-8. (Pubitemid 32051565)
65. Boumil RM, Ogawa Y, Sun BK et al. Differential methylation of Xite and CTCF sites in Tsix mirrors the pattern of X-inactivation choice in mice. Mol Cell Biol 2006; 26(6):2109-17. (Pubitemid 43346914)
66. Ogawa Y, Sun BK, Lee JT. Intersection of the RNA interference and X-inactivation pathways. Science 2008; 320(5881):1336-41. (Pubitemid 351929469)
67. Nesterova TB, Popova BC, Cobb BS et al. Dicer regulates Xist promoter methylation in ES cells indirectly through transcriptional control of Dnmt3a. Epigenetics Chromatin 2008; 1(1):2.
68. Kanellopoulou C, Muljo SA, Dimitrov SD et al. X chromosome inactivation in the absence of Dicer. Proc Natl Acad Sci USA 2009; 106(4):1122-7.
69. Shibata S Lee JT. Tsix transcription- versus RNA-based mechanisms in Xist repression and epigenetic choice. Curr Biol 2004; 14(19):1747-54. (Pubitemid 39301164)
70. Ogawa Y, Lee JT. Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol Cell 2003; 11(3):731-43. (Pubitemid 36385126)
71. Stavropoulos N, Rowntree RK, Lee JT. Identification of developmentally specific enhancers for Tsix in the regulation of X chromosome inactivation. Mol Cell Biol 2005; 25(7):2757-69. (Pubitemid 40381638)
72. Chao W, Huynh KD, Spencer RJ et al. CTCF, a candidate trans-acting factor for X-inactivation choice. Science 2002; 295(5553):345-7. (Pubitemid 34074368)
73. Donohoe ME, Zhang LF, Xu N et al. Identification of a Ctcf cofactor, Yyl, for the X chromosome binary switch. Mol Cell 2007; 25(1):43-56. (Pubitemid 46049057)
74. Donohoe ME, Silva SS, Pinter SF et al. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 2009; 460(7251):128-32.
75. Chambers I, Colby D, Robertson M et al. Functional expression cloning ofNanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113(5):643-55. (Pubitemid 36694189)
76. Mitsui K, Tokuzawa Y, Itoh H et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113(5):631-42. (Pubitemid 36694188)
77. Nichols J, Zevnik B, Anastassiadis K et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998; 95(3):379-91. (Pubitemid 28507326)
78. Avilion AA, Nicolis SK, Pevny LH et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17(1):126-40. (Pubitemid 36062514)
79. Navarro P, Chambers I, Karwacki-Neisius V et al. Molecular coupling of Xist regulation and pluripotency. Science 2008; 321(5896):1693-5.
80. Silva J, Nichols J, Theunissen TW et al. Nanog is the gateway to the pluripotent ground state. Cell 2009; 138(4):722-37.
81. Jonkers I, Barakat TS, Achame EM et al. RNF12 is an X-Encoded dose-dependent activator of X chromosome inactivation. Cell 2009; 139(5):999-1011.
82. Bach I, Rodriguez-Esteban C, Carriere C et al. RLIM inhibits functional activity of LIM homeodomain transcription factors via recruitment of the histone deacetylase complex. Nat Genet 1999; 22(4):394-9. (Pubitemid 29369534)
83. Her YR. Chung IK. Ubiquitin Ligase RLIM Modulates Telomere Length Homeostasis through a Proteolysis of TRF1. J Biol Chem 2009; 284(13):8557-66.
84. JJohnsen SA, Gungor C, Prenzel T et al. Regulation of estrogen-dependent transcription by the LIM cofactors CLIM and RLIM in breast cancer. Cancer Res 2009; 69(1):128-36.
85. Jacobs Pa, Baikie Ag, Brown Wm et al. Evidence for the existence of the human "super female". Lancet 1959; 2(7100):423-5.
86. Maclean N, Mitchell JM. A survey of sex-chromosome abnormalities among 4514 mental defectives. Lancet 1962; 1(7224):293-6.
87. Grumbach MM, Morishima A, Taylor JH. Human Sex Chromosome Abnormalities in Relation to DNA Replication and Heterochromatinization. Proc Natl Acad Sci USA 1963; 49(5):581-9.
88. Carr DH. Chromosome studies in selected spontaneous abortions. 1. Conception after oral contraceptives. Can Med Assoc J 1970; 103(4):343-8.
89. Webb S, de Vries TJ, Kaufman MH. The differential staining pattern ofthe X chromosome in the embryonic and extraembryonic tissues of postimplantation homozygous tetraploid mouse embryos. Genet Res 1992; 59(3):205-14.
90. Harnden DG. Nuclear sex in triploid XXY human cells. Lancet 1961; 2(7200):488.
91. Nicodemi M, Prisco A. Symmetry-breaking model for X-chromosome inactivation. Phys Rev Lett 2007; 98(10):108104.
92. Nicodemi M, Prisco A. Self-assembly and DNA binding ofthe blocking factor in x chromosome inactivation. PLoS Comput Biol 2007; 3(11):e210.
93. Lee JT, Strauss WM, Dausman JA et al. A 450 kb transgene displays properties of the mammalian X-inactivation center. Cell 1996; 86(1):83-94. (Pubitemid 26256580)
94. Herzing LB, Romer JT, Horn JM et al. Xist has properties of the X-chromosome inactivation centre. Nature 1997; 386(6622):272-5. (Pubitemid 27142511)
95. Lee JT, Jaenisch R. Long-range cis effects of ectopic X-inactivation centres on a mouse autosome. Nature 1997; 386(6622):275-9. (Pubitemid 27142512)
96. Lee JT, Lu N, Han Y. Genetic analysis of the mouse X inactivation center defines an 80-kb multifunction domain. Proc Natl Acad Sci USA 1999; 96(7):3836-41. (Pubitemid 29168997)
97. Migeon BR, Kazi E, Haisley-Royster C et al. Human X inactivation center induces random X chromosome inactivation in male transgenic mice. Genomics 1999; 59(2):113-21. (Pubitemid 29365341)
98. Migeon BR, Winter H, Kazi E et al. Low-copy-number human transgene is recognized as an X inactivation center in mouse ES cells, but fails to induce cis-inactivation in chimeric mice. Genomics 2001; 71(2):156-62. (Pubitemid 32165082)
99. Heard E, Kress C, Mongelard F et al. Transgenic mice carrying an Xist-containing YAC. Hum Mol Genet 1996; 5(4):441-50. (Pubitemid 26101139)
100. Matsuura S, Episkopou V, Hamvas R et al. Xist expression from an Xist YAC transgene carried on the mouse Y chromosome. Hum Mol Genet 1996; 5(4):451-9. (Pubitemid 26101140)
101. Heard E, Mongelard F, ArnaudD et al. Xist yeast artificial chromosome transgenes function as X-inactivation centers only in multicopy arrays and not as single copies. Mol Cell Biol 1999; 19(4):3156-66. (Pubitemid 29144560)
102. Gribnau J et al. X chromosome choice occurs independently of asynchronous replication timing. J Cell Biol 2005; 168(3):365-73. (Pubitemid 40205060)
103. MarahrensY, Loring J, Jaenisch R. Role of the Xist gene in X chromosome choosing. Cell 1998; 92(5):657-64. (Pubitemid 28141514)
104. Nesterova TB, Johnston CM, Appanah R et al. Skewing X chromosome choice by modulating sense transcription across the Xist locus. Genes Dev 2003; 17(17):2177-90. (Pubitemid 37052296)
105. Sado T, Li E, Sasaki H. Effect of TSIX disruption on XIST expression in male ES cells. Cytogenet Genome Res 2002; 99(1-4):115-8. (Pubitemid 37467832)
106. Monkhorst K, Jonkers I, Rentmeester E et al. X inactivation counting and choice is a stochastic process: evidence for involvement of an X-linked activator. Cell 2008; 132(3):410-21. (Pubitemid 351191999)
107. Lee JT. Homozygous Tsix mutant mice reveal a sex-ratio distortion and revert to random X-inactivation. Nat Genet 2002; 32(1):195-200. (Pubitemid 34977218)
108. Mlynarczyk-Evans S, Royce-Tolland M, Alexander MK et al. X chromosomes alternate between two states prior to random X-inactivation. PLoS Biol 2006; 4(6):e159.
109. Bacher CP, Guggiari M, Brors B et al. Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol 2006; 8(3):293-9. (Pubitemid 43336072)
110. Xu N, Tsai CL, Lee JT. Transient homologous chromosome pairing marks the onset of X inactivation. Science 2006; 311(5764):1149-52.
111. Xu N, Donohoe ME, Silva SS et al. Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat Genet 2007; 39(11):1390-6. (Pubitemid 350035004)
112. Augui S, Filion GJ, Huart S et al. Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic. Science 2007; 318(5856):1632-6. (Pubitemid 350233663)
113. Takagi N. Variable X chromosome inactivation patterns in near-tetraploid murine EC x somatic cell hybrid cells differentiated in vitro. Genetica 1993; 88(2-3):107-17.
114. Monkhorst K, de Hoon B, Jonkers I et al. The probability to initiate X chromosome inactivation is determined by the X to autosomal ratio and X chromosome specific allelic properties. PLoS One 2009; 4(5):e5616.
115. Barr ML, Bertram EG. A morphological distinction between neurones ofthe male and female and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 1949; 163(4148):676.
116. Ohno S, Hauschka TS. Allocycly of the X-chromosome in tumors and normal tissues. Cancer Res 1960; 20:541-5.
117. Wutz A, Rasmussen TP, Jaenisch R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 2002; 30(2):167-74.
118. Chaumeil J, Le Baccon P, Wutz A et al. A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 2006; 20(16):2223-37.
119. Clemson CM, Hall LL, Byron M et al. The X chromosome is organized into a gene-rich outer rim and an internal core containing silenced nongenic sequences. Proc Natl Acad Sci USA 2006; 103(20):7688-93.
120. Goto Y, Gomez M, Brockdorff N et al. Differential patterns of histone methylation and acetylation distinguish active and repressed alleles at X-linked genes. Cytogenet Genome Res 2002; 99(1-4):66-74. (Pubitemid 37467826)
121. Heard E, Rougeulle C, Arnaud D et al. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 2001; 107(6):727-38. (Pubitemid 34033666)
122. Mak W, Baxter J, Silva J et al. Mitotically stable association of polycomb group proteins eed and enx1 with the inactive x chromosome in trophoblast stem cells. Curr Biol 2002; 12(12):1016-20. (Pubitemid 34703333)
123. Boggs BA, Cheung P, Heard E et al. Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat Genet 2002; 30(1):73-6.
124. Mermoud JE, Popova B, Peters AH et al. Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr Biol 2002; 12(3):247-51. (Pubitemid 34122383)
125. Peters AH, Mermoud JE, O'Carroll D et al. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 2002; 30(1):77-80.
126. Rougeulle C, Chaumeil J, Sarma K et al. Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 2004; 24(12):5475-84. (Pubitemid 38738179)
127. Kohlmaier A, Savarese F, Lachner M et al. A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2004; 2(7):E171.
128. Costanzi C, Pehrson JR. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 1998; 393(6685):599-601. (Pubitemid 28319252)
129. Lock LF, Takagi N, Martin GR. Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation. Cell 1987; 48(1):39-46.
130. Norris DP, Brockdorff N, Rastan S. Methylation status of CpG-rich islands on active and inactive mouse X chromosomes. Mamm Genome 1991; 1(2):78-83.
131. Mohandas T, Sparkes RS, Shapiro LJ. Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science 1981; 211(4480):393-6. (Pubitemid 11128749)
132. Russell LB, Montgomery CS. Comparative studies on X-autosome translocations in the mouse. II. Inactivation of autosomal loci, segregation and mapping of autosomal breakpoints in five T (X;1) S. Genetics 1970; 64(2):281-312.
133. Duthie SM, Nesterova TB, Formstone EJ et al. Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum Mol Genet 1999; 8(2):195-204. (Pubitemid 29054261)
134. Keohane AM et al. H4 acetylation, XIST RNA and replication timing are coincident and define x; autosome boundaries in two abnormal X chromosomes. Hum Mol Genet 1999; 8(2):377-83. (Pubitemid 29054282)
135. Popova BC, Tada T, Takagi N et al. Attenuated spread of X-inactivation in an X; autosome translocation. Proc Natl Acad Sci USA 2006; 103(20):7706-11.
136. Gartler SM, Riggs AD. Mammalian X-chromosome inactivation. Annu Rev Genet 1983; 17:155-90.
137. Lyon MF. X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 1998; 80(1-4):133-7. (Pubitemid 28330373)
138. Lyon MF. LINE-1 elements and X chromosome inactivation: a function for "junk" DNA? Proc Natl Acad Sci USA 2000; 97(12):6248-9. (Pubitemid 30412697)
139. Lyon MF. Do LINEs Have a Role in X-Chromosome Inactivation? J Biomed Biotechnol 2006; 2006(1):59746.
140. Lyon MF. No longer 'all-or-none'. Eur J Hum Genet 2005; 13(7):796-7.
141. Furano AV. The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons. Prog Nucleic Acid Res Mol Biol 2000; 64:255-94.
142. Waters PD, Dobigny G, Pardini AT et al. LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes. Chromosoma 2004; 113(3):137-44. (Pubitemid 39386403)
143. Parish DA, Vise P, Wichman HA et al. Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 2002; 96(1-4):191-7. (Pubitemid 37456598)
144. Wichman HA, Van den Bussche RA, Hamilton MJ et al. Transposable elements and the evolution of genome organization in mammals. Genetica 1992; 86(1-3):287-93.
145. Bailey JA, Carrel L, Chakravarti A et al. Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci USA 2000; 97(12):6634-9. (Pubitemid 30412766)
146. Carrel L, Willard HF. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005; 434(7031):400-4. (Pubitemid 40469185)
147. Wang Z, Willard HF, Mukherjee S et al. Evidence of influence of genomic DNA sequence on human X chromosome inactivation. PLoS Comput Biol 2006; 2(9):e113.
148. Hall LL, Clemson CM, Byron M et al. Unbalanced X; autosome translocations provide evidence for sequence specificity in the association of XIST RNA with chromatin. Hum Mol Genet 2002; 11(25):3157-65. (Pubitemid 35439428)
149. Sharp AJ, Spotswood HT, Robinson DO et al. Molecular and cytogenetic analysis of the spreading of X inactivation in X; autosome translocations. Hum Mol Genet 2002; 11(25):3145-56. (Pubitemid 35439427)
150. Sharp A, Robinson DO, Jacobs P. Absence of correlation between late-replication and spreading of X inactivation in an X; autosome translocation. Hum Genet 2001; 109(3):295-302. (Pubitemid 32926924)
151. White WM, Willard HF, Van Dyke DL et al. The spreading of X inactivation into autosomal material of an x; autosome translocation: evidence for a difference between autosomal and X-chromosomal DNA. Am J Hum Genet 1998; 63(1):20-8. (Pubitemid 30428313)
152. Solari AJ, Rahn IM, Ferreyra ME et al. The behavior of sex chromosomes in two human X-autosome translocations: failure of extensive X-inactivation spreading. Biocell 2001; 25(2):155-66. (Pubitemid 32954580)
153. Dobigny G, Ozouf-Costaz C, Bonillo C et al. Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 2004; 113(1):34-41. (Pubitemid 39236720)
154. Chureau C, Prissette M, Bourdet A et al. Comparative sequence analysis of the X-inactivation center region in mouse, human and bovine. Genome Res 2002; 12(6):894-908. (Pubitemid 34662283)
155. Cantrell MA, Carstens BC, Wichman HA. X chromosome inactivation and Xist evolution in a rodent lacking LINE-1 activity. PLoS One 2009; 4(7):e6252.
156. Ke X, Collins A. CpG islands in human X-inactivation. Ann Hum Genet 2003; 67(Pt 3):242-9. (Pubitemid 38312830)
157. Cao R, Zhang Y. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol Cell 2004; 15(1):57-67. (Pubitemid 38850219)
158. de la Cruz CC, Fang J, Plath K et al. Developmental regulation of Suz 12 localization. Chromosoma 2005; 114(3):183-92.
159. Wang J, Mager J, Chen Y et al. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 2001; 28(4):371-5. (Pubitemid 32702428)
160. Kalantry S, Magnuson T. The Polycomb group protein EED is dispensable for the initiation of random X-chromosome inactivation. PLoS Genet 2006; 2(5):e66.
161. Schoeftner S, Sengupta AK, Kubicek S et al. Recruitment ofPRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J 2006; 25(13):3110-22. (Pubitemid 44121103)
162. de Napoles M, Mermoud JE, Wakao R et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 2004; 7(5):663-76. (Pubitemid 39462687)
163. Fang J, Chen T, Chadwick B et al. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem 2004; 279(51):52812-5.
164. Hernandez-Munoz I, Lund AH, van der Stoop P et al. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci USA 2005; 102(21):7635-40. (Pubitemid 40741023)
165. Nusinow DA, Hernandez-Munoz I, Fazzio TG et al. Poly(ADP-ribose) polymerase 1 is inhibited by a histone H2A variant, MacroH2A and contributes to silencing of the inactive X chromosome. J Biol Chem 2007; 282(17):12851-9.
166. Kim MY, Zhang T, Kraus WL. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 2005; 19(17):1951-67.
167. Rouleau M, Aubin RA, Poirier GG. Poly(ADP-ribosyl)ated chromatin domains: access granted. J Cell Sci 2004; 117(Pt 6):815-25. (Pubitemid 38386940)
168. Hassa PO, Haenni SS, Elser M et al. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 2006; 70(3):789-829. (Pubitemid 44484693)
169. Kim MY, Mauro S, Gevry N et al. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 2004; 119(6):803-14. (Pubitemid 40017687)
170. Helbig R, Fackelmayer FO. Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma 2003; 112(4):173-82. (Pubitemid 38063151)
171. Ganesan S, Silver DP, Greenberg RA et al. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 2002; 111(3):393-405. (Pubitemid 35341392)
172. Silver DP, Dimitrov SD, Feunteun J et al. Further evidence for BRCA1 communication with the inactive X chromosome. Cell 2007; 128(5):991-1002. (Pubitemid 46341424)
173. Vincent-Salomon A, Ganem-Elbaz C, Manie E et al. X inactive-specific transcript RNA coating and genetic instability of the X chromosome in BRCA1 breast tumors. Cancer Res 2007; 67(11):5134-40. (Pubitemid 46997249)
174. Xiao C, Sharp JA, Kawahara M, Davalos AR et al. The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell 2007; 128(5):977-89. (Pubitemid 46350785)
175. Blewitt ME, Gendrel AV, Pang Z et al. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 2008; 40(5):663-9. (Pubitemid 351601224)
176. Garrick D, Sharpe JA, Arkell R et al. Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet 2006; 2(4):e58.
177. Baumann C, De La Fuente R. ATRX marks the inactive X chromosome (Xi) in somatic cells and during imprinted X chromosome inactivation in trophoblast stem cells. Chromosoma 2009; 118(2):209-22.
178. Han HJ, Russo J, Kohwi Y et al. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008; 452(7184):187-93. (Pubitemid 351380252)
179. Agrelo R, Souabni A, Novatchkova M et al. SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 2009; 16(4):507-16.
180. Disteche CM. Escape from X inactivation in human and mouse. Trends Genet 1995; 11(1):17-22.
181. Disteche CM. Escapees on the X chromosome. Proc Natl Acad Sci USA 1999; 96(25):14180-2. (Pubitemid 30000616)
182. Disteche CM, Filippova GN, Tsuchiya KD. Escape from X inactivation. Cytogenet Genome Res 2002; 99(1-4):36-43. (Pubitemid 37467822)
183. Brown CJ, Greally JM. A stain upon the silence: genes escaping X inactivation. Trends Genet 2003; 19(8):432-8. (Pubitemid 36930026)
184. Looijenga LH, Gillis AJ, van Gurp RJ et al. X inactivation in human testicular tumors. XIST expression and androgen receptor methylation status. Am J Pathol 1997; 151(2):581-90. (Pubitemid 27330078)
185. Chow JC, Hall LL, Clemson CM et al. Characterization of expression at the human XIST locus in somatic, embryonal carcinoma and transgenic cell lines. Genomics 2003; 82(3):309-22. (Pubitemid 36952304)
186. Migeon BR, Chowdhury AK, Dunston JA et al. Identification of TSIX, encoding an RNA antisense to human XIST, reveals differences from its murine counterpart: implications for X inactivation. Am J Hum Genet 2001; 69(5):951-60. (Pubitemid 33015810)
187. Chow JC, Hall LL, Lawrence JB et al. Ectopic XIST transcripts in human somatic cells show variable expression and localization. Cytogenet Genome Res 2002; 99(1-4):92-8. (Pubitemid 37467829)
188. Hall LL, Byron M, Sakai K et al. An ectopic human XIST gene can induce chromosome inactivation in postdifferentiation human HT-1080 cells. Proc Natl Acad Sci USA 2002; 99(13):8677-82. (Pubitemid 34693619)
189. Hall LL, Byron M, Butler J et al. X-inactivation reveals epigenetic anomalies in most hESC but identifies sublines that initiate as expected. J Cell Physiol 2008; 216(2):445-52. (Pubitemid 351898472)
190. Shen Y, Matsuno Y, Fouse SD et al. X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci USA 2008; 105(12):4709-14. (Pubitemid 351753811)
191. Silva SS, Rowntree RK, Mekhoubad S et al. X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc Natl Acad Sci USA 2008; 105(12):4820-5. (Pubitemid 351753830)
192. Enver T, Soneji S, Joshi C et al. Cellular differentiation hierarchies in normal and culture-adapted human embryonic stem cells. Hum Mol Genet 2005; 14(21):3129-40. (Pubitemid 41631288)
193. Hoffman LM, Hall L, Batten JL et al. X-inactivation status varies in human embryonic stem cell lines. Stem Cells 2005; 23(10):1468-78. (Pubitemid 41740996)
194. Dhara SK, Benvenisty N. Gene trap as a tool for genome annotation and analysis of X chromosome inactivation in human embryonic stem cells. Nucleic Acids Res 2004; 32(13):3995-4002. (Pubitemid 39199091)
195. Takagi N. Imprinted X-chromosome inactivation: enlightenment from embryos in vivo. Semin Cell Dev Biol 2003; 14(6):319-29. (Pubitemid 38167302)
196. West JD, Papaioannou VE, Frels WI et al. Preferential expression of the maternally derived X chromosome in the mouse yolk sac. Cell 1977; 12(4):873-82. (Pubitemid 8236614)
197. van den Berg IM, Laven JS, Stevens M et al. X chromosome inactivation is initiated in human preimplantation embryos. Am J Hum Genet 2009; 84(6):771-9.
198. Looijenga LH, Gillis AJ, Verkerk AJ et al. Heterogeneous X inactivation in trophoblastic cells of human full-term female placentas. Am J Hum Genet 1999; 64(5):1445-52. (Pubitemid 30468765)
199. Ropers HH, Wolff G, Hitzeroth HW. Preferential X inactivation in human placenta membranes: is the paternal X inactive in early embryonic development of female mammals? Hum Genet 1978; 43(3):265-73. (Pubitemid 8398442)
200. Daniels R, Zuccotti M, Kinis T et al. XIST expression in human oocytes and preimplantation embryos. Am J Hum Genet 1997; 61(1):33-9. (Pubitemid 27323321)
201. Ray PF, Winston RM, Handyside AH. XIST expression from the maternal X chromosome in human male preimplantation embryos at the blastocyst stage. Hum Mol Genet 1997; 6(8):1323-7.
202. Bamforth F, Machin G, Innes M. X-chromosome inactivation is mostly random in placental tissues of female monozygotic twins and triplets. Am J Med Genet 1996; 61(3):209-15.
203. Migeon BR, Wolf SF, Axelman J et al. Incomplete X chromosome dosage compensation in chorionic villi of human placenta. Proc Natl Acad Sci USA 1985; 82(10):3390-4.
204. Migeon BR, Axelman J, Jeppesen P. Differential X reactivation in human placental cells: implications for reversal of X inactivation. Am J Hum Genet 2005; 77(3):355-64. (Pubitemid 41192643)
205. Goto T, Wright E, Monk M. Paternal X-chromosome inactivation in human trophoblastic cells. Mol Hum Reprod 1997; 3(1):77-80. (Pubitemid 127509427)
206. Harrison KB. X-chromosome inactivation in the human cytotrophoblast. Cytogenet Cell Genet 1989; 52(1-2):37-41. (Pubitemid 20027562)
207. Harrison KB, Warburton D. Preferential X-chromosome activity in human female placental tissues. Cytogenet Cell Genet 1986; 41(3):163-8. (Pubitemid 16110184)
208. Liu W, Sun X. Skewed X chromosome inactivation in diploid and triploid female human embryonic stem cells. Hum Reprod 2009; 24(8):1834-43.
209. Sato N, Sanjuan IM, Heke M et al. Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev Biol 2003; 260(2):404-13. (Pubitemid 36960088)
210. Ginis I, Luo Y, Miura T et al. Differences between human and mouse embryonic stem cells. Dev Biol 2004; 269(2):360-80. (Pubitemid 38521104)
211. Xu RH, Peck RM, Li DS et al. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005; 2(3):185-90. (Pubitemid 41122125)
212. Ying QL, Nichols J, Chambers I et al. BMP induction ofId proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 2003; 115(3):281-92. (Pubitemid 37487702)
213. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122(6):947-56. (Pubitemid 41345211)
214. Brons IG, Smithers LE, Trotter MW et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007; 448(7150):191-5. (Pubitemid 47067373)
215. Tesar PJ, Chenoweth JG, Brook FA et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007; 448(7150):196-9. (Pubitemid 47067378)
216. Rossant J. Stem cells and early lineage development. Cell 2008; 132(4):527-31. (Pubitemid 351253691)
217. Lovell-Badge R. Many ways to pluripotency. Nat Biotechnol 2007; 25(10):1114-6. (Pubitemid 47538109)
218. Xu RH, Chen X, Li DS et al. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 2002; 20(12):1261-4. (Pubitemid 35462493)
219. Guo G, Yang J, Nichols J et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009; 136(7):1063-9.
220. Bao S, Tang F, Li X et al. Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 2009; 461(7268):1292-5.
221. Hanna J, Markoulaki S, Mitalipova M et al. Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 2009; 4(6):513-24.
222. Nichols J, Smith A. Naive and primed pluripotent states. Cell Stem Cell 2009; 4(6):487-92.
223. Zvetkova I, Apedaile A, Ramsahoye B et al. Global hypomethylation of the genome in XX embryonic stem cells. Nat Genet 2005; 37(11):1274-9. (Pubitemid 41568713)
224. Lagarkova MA, Volchkov PY, Lyakisheva AV et al. Diverse epigenetic profile of novel human embryonic stem cell lines. Cell Cycle 2006; 5(4):416-20.
225. Rugg-Gunn PJ, Ferguson-Smith AC, Pedersen RA. Epigenetic status of human embryonic stem cells. Nat Genet 2005; 37(6):585-7. (Pubitemid 40770411)
226. Allegrucci C, Wu YZ, Thurston A et al. Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum Mol Genet 2007; 16(10):1253-68. (Pubitemid 47062721)