Methylation-Mediated Proviral Silencing Is Associated with MeCP2 Recruitment and Localized Histone H3 Deacetylation

REFERENCES

• Amir, R. E., I. B. Van den Veyver, M. Wan, C. Q. Tran, U. Francke, and H. Y. Zoghbi. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23:185–188.
   PubMed Web of Science ®Google Scholar
• Anderson, M. T., I. M. Tjioe, M. C. Lorincz, D. R. Parks, L. A. Herzenberg, G. P. Nolan, and L. A. Herzenberg. 1996. Simultaneous fluorescence-activated cell sorter analysis of two distinct transcriptional elements within a single cell using engineered green fluorescent proteins. Proc. Natl. Acad. Sci. USA 93:8508–8511.
   PubMedGoogle Scholar
• Baer, A., D. Schübeler, and J. Bode. 2000. Transcriptional properties of genomic transgene integration sites marked by electroporation or retroviral infection. Biochemistry 39:7041–7049.
   PubMedGoogle Scholar
• Bestor, T. H.. 1998. The host defence function of genomic methylation patterns. Novartis Found. Symp. 214:187–195.
   PubMedGoogle Scholar
• Bestor, T. H., and B. Tycko. 1996. Creation of genomic methylation patterns. Nat. Genet. 12:363–367.
   PubMed Web of Science ®Google Scholar
• Bird, A. P., and A. P. Wolffe. 1999. Methylation-induced repression—belts, braces, and chromatin. Cell 99:451–454.
   PubMed Web of Science ®Google Scholar
• Cameron, E. E., K. E. Bachman, S. Myohanen, J. G. Herman, and S. B. Baylin. 1999. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet. 21:103–107.
   PubMed Web of Science ®Google Scholar
• Challita, P. M., and D. B. Kohn. 1994. Lack of expression from a retroviral vector after transduction of murine hematopoietic stem cells is associated with methylation in vivo. Proc. Natl. Acad. Sci. USA 91:2567–2571.
   PubMed Web of Science ®Google Scholar
• Chen, R. Z., S. Akbarian, M. Tudor, and R. Jaenisch. 2001. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27:327–331.
   PubMed Web of Science ®Google Scholar
• Cheung, P., C. D. Allis, and P. Sassone-Corsi. 2000. Signaling to chromatin through histone modifications. Cell 103:263–271.
   PubMed Web of Science ®Google Scholar
• Clark, S. J., J. Harrison, C. L. Paul, and M. Frommer. 1994. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22:2990–2997.
   PubMed Web of Science ®Google Scholar
• Coffee, B., F. Zhang, S. T. Warren, and D. Reines. 1999. Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat. Genet. 22:98–101.
   PubMed Web of Science ®Google Scholar
• Conklin, K. F., and M. Groudine. 1986. Varied interactions between proviruses and adjacent host chromatin. Mol. Cell. Biol. 6:3999–4007.
   PubMedGoogle Scholar
• Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489.
   PubMed Web of Science ®Google Scholar
• Dranoff, G., E. Jaffee, A. Lazenby, P. Golumbek, H. Levitsky, K. Brose, V. Jackson, H. Hamada, D. Pardoll, and R. C. Mulligan. 1993. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 90:3539–3543.
   PubMed Web of Science ®Google Scholar
• Feng, Y. Q., M. C. Lorincz, S. Fiering, J. M. Greally, and E. E. Bouhassira. 2001. Position effects are influenced by the orientation of a transgene with respect to flanking chromatin. Mol. Cell. Biol. 21:298–309.
   PubMedGoogle Scholar
• Feng, Y. Q., J. Seibler, R. Alami, A. Eisen, K. A. Westerman, P. Leboulch, S. Fiering, and E. E. Bouhassira. 1999. Site-specific chromosomal integration in mammalian cells: highly efficient CRE recombinase-mediated cassette exchange. J. Mol. Biol. 292:779–785.
   PubMedGoogle Scholar
• Forrester, W. C., E. Epner, M. C. Driscoll, T. Enver, M. Brice, T. Papayannopoulou, and M. Groudine. 1990. A deletion of the human beta-globin locus activation region causes a major alteration in chromatin structure and replication across the entire beta-globin locus. Genes Dev. 4:1637–1649.
   PubMed Web of Science ®Google Scholar
• Francastel, C., D. Schubeler, D. I. Martin, and M. Groudine. 2000. Nuclear compartmentalization and gene activity. Nat. Rev. Mol. Cell. Biol. 1:137–143.
   PubMedGoogle Scholar
• Fujita, N., S. Takebayashi, K. Okumura, S. Kudo, T. Chiba, H. Saya, and M. Nakao. 1999. Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Mol. Cell. Biol. 19:6415–6426.
   PubMed Web of Science ®Google Scholar
• Granger, S. W., and H. Fan. 1998. In vivo footprinting of the enhancer sequences in the upstream long terminal repeat of Moloney murine leukemia virus: differential binding of nuclear factors in different cell types. J. Virol. 72:8961–8970.
   PubMedGoogle Scholar
• Gregory, R. I., T. E. Randall, C. A. Johnson, S. Khosla, I. Hatada, L. P. O'Neill, B. M. Turner, and R. Feil. 2001. DNA methylation is linked to deacetylation of histone h3, but not h4, on the imprinted genes snrpn and u2af1-rs1. Mol. Cell. Biol. 21:5426–5436.
   PubMed Web of Science ®Google Scholar
• Guy, J., B. Hendrich, M. Holmes, J. E. Martin, and A. Bird. 2001. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27:322–326.
   PubMed Web of Science ®Google Scholar
• Hendrich, B., and A. Bird. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18:6538–6547.
   PubMed Web of Science ®Google Scholar
• Hendrich, B., J. Guy, B. Ramsahoye, V. A. Wilson, and A. Bird. 2001. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 15:710–723.
   PubMedGoogle Scholar
• Hsieh, C. L.. 2000. Dynamics of DNA methylation pattern. Curr. Opin. Genet. Dev. 10:224–228.
   PubMedGoogle Scholar
• Iguchi-Ariga, S. M., and W. Schaffner. 1989. CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev. 3:612–619.
   PubMed Web of Science ®Google Scholar
• Jahner, D., and R. Jaenisch. 1985. Chromosomal position and specific demethylation in enhancer sequences of germ line-transmitted retroviral genomes during mouse development. Mol. Cell. Biol. 5:2212–2220.
   PubMedGoogle Scholar
• Jahner, D., and R. Jaenisch. 1985. Retrovirus-induced de novo methylation of flanking host sequences correlates with gene inactivity. Nature 315:594–597.
   PubMed Web of Science ®Google Scholar
• Jones, P. L., G. J. Veenstra, P. A. Wade, D. Vermaak, S. U. Kass, N. Landsberger, J. Strouboulis, and A. P. Wolffe. 1998. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19:187–191.
   PubMed Web of Science ®Google Scholar
• Kaludov, N. K., and A. P. Wolffe. 2000. MeCP2 driven transcriptional repression in vitro: selectivity for methylated DNA, action at a distance and contacts with the basal transcription machinery. Nucleic Acids Res. 28:1921–1928.
   PubMed Web of Science ®Google Scholar
• Kass, S. U., J. P. Goddard, and R. L. Adams. 1993. Inactive chromatin spreads from a focus of methylation. Mol. Cell. Biol. 13:7372–7379.
   PubMedGoogle Scholar
• Lander, E. S., L. M. Linton, B. Birren, et al.. 2001. Initial sequencing and analysis of the human genome. Nature 409:860–921.
   PubMed Web of Science ®Google Scholar
• Lewis, J. D., R. R. Meehan, W. J. Henzel, F. I. Maurer, P. Jeppesen, F. Klein, and A. Bird. 1992. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69:905–914.
   PubMed Web of Science ®Google Scholar
• Lorincz, M. C., D. Schübeler, S. C. Goeke, M. Walters, M. Groudine, and D. I. Martin. 2000. Dynamic analysis of proviral induction and de novo methylation: implications for a histone deacetylase-independent, methylation density-dependent mechanism of transcriptional repression. Mol. Cell. Biol. 20:842–850.
   PubMed Web of Science ®Google Scholar
• Magdinier, F., and A. P. Wolffe. 2001. Selective association of the methyl-CpG binding protein MBD2 with the silent p14/p16 locus in human neoplasia. Proc. Natl. Acad. Sci. USA 98:4990–4995.
   PubMedGoogle Scholar
• Nakayama, J., J. C. Rice, B. D. Strahl, C. D. Allis, and S. I. Grewal. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110–113.
   PubMed Web of Science ®Google Scholar
• Nan, X., F. J. Campoy, and A. Bird. 1997. MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471–481.
   PubMed Web of Science ®Google Scholar
• Nan, X., H. H. Ng, C. A. Johnson, C. D. Laherty, B. M. Turner, R. N. Eisenman, and A. Bird. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389.
   PubMed Web of Science ®Google Scholar
• Ng, H. H., Y. Zhang, B. Hendrich, C. A. Johnson, B. M. Turner, H. Erdjument-Bromage, P. Tempst, D. Reinberg, and A. Bird. 1999. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23:58–61.
   PubMed Web of Science ®Google Scholar
• Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205–214.
   PubMed Web of Science ®Google Scholar
• Pazin, M. J., and J. T. Kadonaga. 1997. What's up and down with histone deacetylation and transcription?. Cell 89:325–328.
   PubMed Web of Science ®Google Scholar
• Reik, A., A. Telling, G. Zitnik, D. Cimbora, E. Epner, and M. Groudine. 1998. The locus control region is necessary for gene expression in the human beta-globin locus but not the maintenance of an open chromatin structure in erythroid cells. Mol. Cell. Biol. 18:5992–6000.
   PubMed Web of Science ®Google Scholar
• Schübeler, D., C. Francastel, D. M. Cimbora, A. Reik, D. I. Martin, and M. Groudine. 2000. Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev. 14:940–950.
   PubMed Web of Science ®Google Scholar
• Schübeler, D., M. C. Lorincz, D. M. Cimbora, A. Telling, Y. Q. Feng, E. E. Bouhassira, and M. Groudine. 2000. Genomic targeting of methylated DNA: influence of methylation on transcription, replication, chromatin structure, and histone acetylation. Mol. Cell. Biol. 20:9103–9112.
   PubMed Web of Science ®Google Scholar
• Thompson, T., and H. Fan. 1985. Mapping of DNase I-hypersensitive sites in the 5′ and 3′ long terminal repeats of integrated Moloney murine leukemia virus proviral DNA. Mol. Cell. Biol. 5:601–609.
   PubMedGoogle Scholar
• Wade, P. A., A. Gegonne, P. L. Jones, E. Ballestar, F. Aubry, and A. P. Wolffe. 1999. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat. Genet. 23:62–66.
   PubMed Web of Science ®Google Scholar
• Walsh, C. P., J. R. Chaillet, and T. H. Bestor. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20:116–117.
   PubMed Web of Science ®Google Scholar
• Wan, M., K. Zhao, S. S. Lee, and U. Francke. 2001. MECP2 truncating mutations cause histone H4 hyperacetylation in Rett syndrome. Hum. Mol. Genet. 10:1085–1092.
   PubMedGoogle Scholar
• Whitelaw, E., and D. I. Martin. 2001. Retrotransposons as epigenetic mediators of phenotypic variation in mammals. Nat. Genet. 27:361–365.
   PubMed Web of Science ®Google Scholar
• Yu, F., J. Thiesen, and W. H. Stratling. 2000. Histone deacetylase-independent transcriptional repression by methyl-CpG-binding protein 2. Nucleic Acids Res. 28:2201–2206.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., H. H. Ng, H. Erdjument-Bromage, P. Tempst, A. Bird, and D. Reinberg. 1999. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev. 13:1924–1935.
   PubMed Web of Science ®Google Scholar
• Zhu, B., D. Benjamin, Y. Zheng, H. Angliker, S. Thiry, M. Siegmann, and J. P. Jost. 2001. Overexpression of 5-methylcytosine DNA glycosylase in human embryonic kidney cells EcR293 demethylates the promoter of a hormone-regulated reporter gene. Proc. Natl. Acad. Sci. USA 98:5031–5036.
   PubMedGoogle Scholar