Chromatin of the Barr body: Histone and non-histone proteins associated with or excluded from the inactive X chromosome

Human Molecular Genetics

Volumn 12, Issue 17, 2003, Pages 2167-2178

  Chadwick, Brian P ^a   Willard, Huntington F ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP PROTEIN; HISTONE; LYSINE; NONHISTONE PROTEIN;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE SILENCING; HETEROCHROMATIN; HUMAN; HUMAN CELL; INTERPHASE; PATTERN RECOGNITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; X CHROMATIN; X CHROMOSOME;

CELL NUCLEUS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN, X; DNA METHYLATION; DNA-BINDING PROTEINS; DOSAGE COMPENSATION, GENETIC; GENE SILENCING; HIGH MOBILITY GROUP PROTEINS; HISTONE DEACETYLASES; HISTONES; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERPHASE; MICROSATELLITE REPEATS; NUCLEOSOMES; REPRESSOR PROTEINS; SEX CHROMATIN; SEX CHROMOSOME ABERRATIONS;

EID: 0042379770     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg229     Document Type: Article

References (84)

1. Lyon, M.F (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature, 190, 372-373.
2. Barr, M.L. and Bertram, E.G. (1949) A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature, 163, 676-677.
3. Moore, K.L. (1966) The Sex Chromatin. W.B. Saunders Co., Philadelphia, PA, London, UK.
4. Miles, C.P. and Koons, A.S. (1960) Sexual dimorphism of rat cells in vitro. Science, 131, 740.
5. Brown, C.J., Ballabio, A., Rupert, J.L., Lafreniere, R.G., Grompe, M., Tonlorenzi, R. and 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, 38-44.
6. Clemson, C.M., McNeil, J.A., Willard, H.F. and 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, 1-17.
7. Chadwick, B.P. and Willard, H.F. (2001) Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum. Mol. Genet., 10, 1101-1113.
8. Costanzi, C. and Pehrson, J.R. (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature, 393, 599-601.
9. Costanzi, C. and Pehrson, J.R. (2001) MacroH2A2, a new member of the MacroH2A core histone family. J. Biol. Chem., 276, 21776-21784.
10. Mohandas, T., Sparkes, R.S. and Shapiro, L.J. (1981) Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science, 211, 393-396.
11. Pfeifer, G.P., Tanguay, R.L., Steigerwald, S.D. and Riggs, A.D. (1990) In vivo footprint and methylation analysis by PCR-aided genomic sequencing: comparison of active and inactive X chromosomal DNA at the CpG island and promoter of human PGK-1. Genes Dev., 4, 1277-1287.
12. Gilbert, C.W., Muldal, S., Lajthal, L.G. and Rowley, J. (1962) Time-sequence of human chromosome duplication. Nature, 195, 869-873.
13. Morishma, A., Grumbach, M.M. and Taylor, J.H. (1962) Asynchronous duplication of human chromosomes and the origin of sex chromatin. Proc. Natl Acad. Sci. USA, 48, 756-763.
14. Berger, S.L. (2002) Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev., 12, 142-148.
15. Strahl, B.D. and Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
16. Belyaev, N., Keohane, A.M. and Turner, B.M. (1996) Differential underacetylation of histones H2A, H3 and H4 on the inactive X chromosome in human female cells. Hum. Genet., 97, 573-578.
17. Boggs, B.A., Connors, B., Sobel, R.E., Chinault, A.C. and Allis, C.D. (1996) Reduced levels of histone H3 acetylation on the inactive X chromosome in human females. Chromosoma, 105, 303-309.
18. Gilbert, S.L. and Sharp, P.A. (1999) Promoter-specific hypoacetylation of X-inactivated genes. Proc. Natl Acad. Sci. USA, 96, 13825-13830.
19. Jeppesen, P. and 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, 281-289.
20. Boggs, B.A., Cheung, P., Heard, E., Spector, D.L., Chinault, A.C. and Allis, C.D. (2002) Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat. Genet., 30, 73-76.
21. Peters, A.H., Mermoud, J.E., O'Carroll, D., Pagani, M., Schweizer, D., Brockdorff, N. and Jenuwein, T. (2002) Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat. Genet., 30, 77-80.
22. Plath, K., Fang, J., Mlynarczyk-Evans, S.K., Cao, R., Worringer, K.A., Wang, H., de la Cruz, C.C., Otte, A.P., Panning, B. and Zhang, Y. (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science, 300, 131-135.
23. Silva, J., Mak, W., Zvetkova, I., Appanah, R., Nesterova, T.B., Webster, Z., Peters, A.H., Jenuwein, T., Otte, A.P. and Brockdorff, N. (2003) Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of eed-enx 1 polycomb group complexes. Dev. Cell, 4, 481-495.
24. Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C. and Kouzarides, T. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature, 410, 120-124.
25. Jacobs, S.A., Taverna, S.D., Zhang, Y., Briggs, S.D., Li, J., Eissenberg, J.C., Allis, D. and Khorasanizadeh, S. (2001) Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J., 20, 5232-5241.
26. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. and Jenuwein, T. (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature, 410, 116-120.
27. Metzler-Guillemain, C., Luciani, J., Depetris, D., Guichaoua, M.R. and Mattei, M.G. (2003) HP 1 beta and HP 1 gamma, but not HP1 alpha, decorate the entire XY body during human male meiosis. Chromosome Res., 11, 73-81.
28. James, T.C. and Elgin, S.C. (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol. Cell. Biol., 6, 3862-3872.
29. Eissenberg, J.C., James, T.C., Foster-Hartnett, D.M., Hartnett, T., Ngan, V. and Elgin, S.C. (1990) Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl Acad. Sci. USA, 87, 9923-9927.
30. Grewal, S.I. and Elgin, S.C.R. (2002) Heterochromatin: new possibilities for the inheritance of structure. Curr. Opin. Genet. Dev., 12, 178-187.
31. Eissenberg, J.C. and Elgin, S.C. (2000) The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev., 10, 204-210.
32. Ma. J., Hwang, K.K., Worman, H.J., Courvalin, J.C. and Eissenberg, J.C. (2001) Expression and functional analysis of three isoforms of human heterochromatin-associated protein HP1 in Drosophila. Chromosoma, 109, 536-544.
33. Wang, G., Ma, A., Chow, C.M., Horsley, D., Brown, N.R., Cowell, I.G. and Singh, P.B. (2000) Conservation of heterochromatin protein 1 function. Mol. Cell. Biol., 20, 6970-6983.
34. Saunders, W.S., Chue, C., Goebl, M., Craig, C., Clark, R.F., Powers, J.A., Eissenberg, J.C., Elgin, S.C., Rothfield, N.F. and Earnshaw, W.C. (1993) Molecular cloning of a human homologue of Drosophila heterochromatin protein HP1 using anti-centromere autoantibodies with anti-chromo specificity. J. Cell Sci., 104, 573-582.
35. Singh, P.B., Miller, J.R., Pearce, J., Kothary, R., Burton, R.D., Paro, R., James, T.C. and Gaunt, S.J. (1991) A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucleic Acids Res., 19, 789-794.
36. Ye, Q. and Worman, H.J. (1996) Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J. Biol. Chem., 271, 14653-14656.
37. Furuta, K., Chan, E.K., Kiyosawa, K., Reimer, G., Luderschmidt, C. and Tan, E.M. (1997) Heterochromatin protein HP1Hsbeta (p25beta) and its localization with centromeres in mitosis. Chromosoma, 106, 11-19.
38. Minc, E., Allory, Y., Worman, H.J., Courvalin, J.-C. and Buendia, B. (1999) Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma, 108, 220-234.
39. Rea, S., Elsenhaber, E, O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D. et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 406, 593-599.
40. Chadwick, B.P. and Willard, H.F. (2002) Cell cycle-dependent localization of macroH2A in chromatin of the inactive X chromosome. J. Cell Biol., 157, 1113-1123.
41. Ramakrishnan, V. (1997) Histone H1 and chromatin higher-order structure. Crit. Rev. Eukaryot. Gene Expr., 7, 215-230.
42. Carruthers, L.M., Bedner, J., Woodcock, C.L. and Hansen, J.C. (1998) Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. Biochemistry, 37, 14776-14787.
43. Bustin, M. (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol., 19, 5237-5246.
44. Reeves, R. and Beckerbauer, L. (2001) HMGI/Y proteins: flexible regulators of transcription and chromatin structure. Biochim. Biophys. Acta., 1519, 13-29.
45. Flickinger, R. (2001) Replication timing and cell differentiation. Differentiation, 69, 18-26.
46. Bonnefoy, E., Bandu, M.T. and Doly, J. (1999) Specific binding of high-mobility-group I (HMGI) protein and histone H1 to the upstream AT-rich region of the murine beta interferon promoter: HMGI protein acts as a potential antirepressor of the promoter. Mol. Cell. Biol., 19, 2803-2816.
47. Hill, D.A. and Reeves, R. (1997) Competition between HMG-I(Y), HMG-1 and histone H1 on four-way junction DNA. Nucleic Acids Res., 25, 3523-3531.
48. Zhao, K., Kas, E., Gonzalez, E. and Laemmli, U.K. (1993) SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J., 12, 3237-3247.
49. Thanos, D. and Maniatis, T. (1995) Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell, 83, 1091-1100.
50. Lobanenkov, V.V., Nicolas, R.H., Adler, V.V., Paterson, H., Klenova, E.M., Polotskaja, A.V. and Goodwin, G.H., (1990) A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5′-flanking sequence of the chicken c-myc gene. Oncogene, 5, 1743-1753.
51. Chao, W., Huynh, K.D., Spencer, R.J., Davidow, L.S. and Lee, J.T. (2002) CTCF, a candidate trans-acting factor for X-inactivation choice. Science, 295, 345-347.
52. Tsukiyama, T. (2002) The in vivo functions of ATP-dependent chromatin-remodelling factors. Nat. Rev. Mol. Cell Biol., 3, 422-429.
53. Hansen, R.S., Stoger, R., Wijmenga, C., Stanek, A.M., Canfield, T.K., Luo, P., Matarazzo, M.R., D'Esposito, M., Feil, R., Gimelli, G. et al. (2000) Escape from gene silencing in ICF syndrome: evidence for advanced replication time as a major determinant. Hum. Mol. Genet., 9, 2575-2587.
54. Miniou, P., Jeanpierre, M., Blanquet, V., Sibella, V., Bonneau, D., Herbelin, C., Fischer, A., Niveleau, A. and Viegas-Pequignot, E. (1994) Abnormal methylation pattern in constitutive and facultative (X inactive chromosome) heterochromatin of ICF patients. Hum. Mol. Genet., 3, 2093-2102.
55. Bannister, A.J., Schneider, R. and Kouzarides, T. (2002) Histone methylation: dynamic or static? Cell, 109, 801-806.
56. Jenuwein, T. (2001) Re-SET-ting beterochromatin by histone methyltransferases. Trends Cell Biol., 11, 266-273.
57. Giacalone, J., Friedes, J. and Francke, U. (1992) A novel GC-rich human macrosatellite VNTR in Xq24 is differentially methylated on active and inactive X chromosomes. Nat. Genet., 1, 137-143.
58. Lachner, M. and Jenuwein, T. (2002) The many faces of histone lysine methylation. Curr. Opin. Cell Biol., 14, 286-298.
59. Nakayama, J., Klar, A.J.S. and Grewal, S.I. (2000) A chromodomain protein, Swi6, performs imprinting functions in fission yeast during mitosis and meiosis. Cell, 101, 307-317.
60. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D. and Grewal, S.I. (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science, 292, 110-113.
61. Kourmouli, N., Theodoropoulos, P.A., Dialynas, G., Bakou, A., Politou, A.S., Cowell, I.G., Singh, P.B. and Georgatos, S.D. (2000) Dynamic associations of heterochromatin protein 1 with the nuclear envelope. EMBO J., 19, 6558-6568.
62. Lechner, M.S., Begg, G.E., Speicher, D.W. and Rauscher, F.J., III (2000) Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol. Cell Biol., 20, 6449-6465.
63. Polioudaki, H., Kourmouli, N., Drosou, V., Bakou, A., Theodoropoulos, P.A., Singh, P.B., Giannakouros, T. and Georgatos, S.D. (2001) Histones H3/H4 form a tight complex with the inner nuclear membrane protein LBR and heterochromatin protein 1. EMBO Rep., 2, 920-925.
64. Ye, Q., Callebaut, I., Pezhman, A., Courvalin, J.C. and Worman, H.J. (1997) Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem., 272, 14983-14989.
65. Perche, P.Y., Vourc'h, C., Konecny, L., Souchier, C., Robert-Nicoud, M., Dimitrov, S. and Khochbin, S. (2000) Higher concentrations of histone macroH2A in the Barr body are correlated with higher nucleosome density. Curr. Biol., 10, 1531-1534.
66. Garrard, W.T. (1991) Histone H1 and the conformation of transcriptionally active chromatin. BioEssays, 13, 87-88.
67. Fasy, T.M., Inoue, A., Johnson, E.M. and Allfrey, V.G. (1979) Phosphorylation of H1 and H5 histones by cyclic AMP-dependent protein kinase reduces DNA binding. Biochim. Biophys. Acta., 564, 322-334.
68. Gurley, L.R., Walters, R.A. and Tobey, R,A. (1975) Sequential phosphorylation of histone sub-fractions in the Chinese hamster cell cycle. J. Biol. Chem., 250, 3936-3944.
69. Solomon, M.J., Lee, T. and Kirschner, M.W. (1992) Role of phosphorylation in p34cdc2 activation: identification of an activating kinase. Mol. Biol. Cell, 3, 13-27.
70. Nissen, M.S., Langan, T.A. and Reeves, R. (1991) Phosporylation by cdc2 kinase modulates DNA binding activity of high mobility group I nonhistone chromatin protein. J. Biol. Chem., 266, 19945-19952.
71. Reeves, R., Langan, T.A. and Nissen, M.S. (1991) Phosphorylation of the DNA-binding domain of nonhistone high-mobility group I protein by cdc2 kinase: reduction of binding affinity. Proc. Natl Acad. Sci. USA, 88, 1671-1675.
72. Krude, T. (1999) Chromatin assembly during DNA replication in somatic cells. Eur. J. Biochem., 263, 1-5.
73. Chadwick, B.P. and Willard, H.F. (2001) A novel chromatin protein, distantly related to histone H2A, is largely excluded from the inactive X chromosome. J. Cell Biol., 152, 375-384.
74. Czermin, B., Schotta, G., Hulsmann, B.B., Brehm, A., Becker, P.B., Reuter, G. and Imhof, A. (2001) Physical and functional association of SU(VAR)3-9 and HDAC1 in Drosophila. EMBO Rep., 2, 915-919.
75. Bauer, U.M., Daujat, S., Nielsen, S.J., Nightingale, K. and Kouzarides, T. (2002) Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep., 3, 39-44.
76. Strahl, B.D., Briggs, S.D., Brame, C.J., Caldwell, J.A., Koh, S.S., Ma, H., Cook, R.G., Shabanowitz, J., Hunt, D.F., Stallcup, M.R. et al. (2001) Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol., 11, 996-1000.
77. Wang, H., Huang, Z.Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B.D., Briggs, S.D., Allis, C.D., Wong, J., Tempst, P. et al. (2001) Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science, 293, 853-857.
78. Zhang, Y. and Reinberg, D. (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev., 15, 2243-2360.
79. Kouzarides, T. (2002) Histone methylation in transcriptional control. Curr. Opin. Genet. Dev., 12, 198-209.
80. Ohlsson, R., Renkawitz, R. and Lobanenkov, V. (2001) CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet., 17, 520-527.
81. Hong, B., Reeves, P., Panning, B., Swanson, M.S. and Yang, T.P. (2001) Identification of an autoimmune serum containing antibodies against the Barr body. Proc. Natl Acad. Sci. USA, 98, 8703-8708.
82. Ganesan, S., Silver, D.P., Greenberg, R.A., Avni, D., Drapkin, R., Miron, A., Mok, S.C., Randrianarison, V., Brodie, S., Salstrom, J. et al. (2002) BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell, 111, 393-405.
83. Ye, Q., Hu, Y.F., Zhong, H., Nye, A.C., Belmont, A.S. and Li, R. (2001) BRCA1-induced large-scale chromatin unfolding and allele-specific effects of cancer-predisposing mutations. J. Cell Biol., 155, 911-921.
84. Nielsen, A.L., Ortiz, J.A., You, J., Oulad-Abdelghani, M., Khechumian, R., Gansmuller, A., Chambon, P. and Losson, R. (1999) Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J., 18, 6385-6395.