Reduced Genomic Cytosine Methylation and Defective Cellular Differentiation in Embryonic Stem Cells Lacking CpG Binding Protein

REFERENCES

• Aasland, R., T. J. Gibson, and F. Stewart. 1995. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20:56–59.
   PubMed Web of Science ®Google Scholar
• 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
• Ariel, M., H. Cedar, and J. McCarrey. 1994. Developmental changes in methylation of spermatogenesis-specific genes include reprogramming in the epididymis. Nat. Genet. 7:59–63.
   PubMed Web of Science ®Google Scholar
• Balaghi, M., and C. Wagner. 1993. DNA methylation in folate deficiency: use of CpG methylase. Biochem. Biophys. Res. Commun. 193:1184–1190.
   PubMed Web of Science ®Google Scholar
• Bestor, T. H. 1992. Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO J. 11:2611–2617.
   PubMed Web of Science ®Google Scholar
• Bestor, T. H., and G. L. Verdine. 1994. DNA methyltransferases. Curr. Opin. Cell Biol. 6:380–389.
   PubMed Web of Science ®Google Scholar
• Biniszkiewicz, D., J. Gribnau, B. Ramsahoye, F. Gaudet, K. Eggan, D. Humpherys, M.-A. Mastrangelo, Z. Jun, J. Walter, and R. Jaenisch. 2002. Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell. Biol. 22:2124–2135.
   PubMed Web of Science ®Google Scholar
• Bird, A. P. 1987. CpG islands as gene markers in the vertebrate nucleus. Trends Genet. 3:342–347.
   Web of Science ®Google Scholar
• Burgers, W. A., F. Fuks, and T. Kouzarides. 2002. DNA methyltransferases get connected to chromatin. Trends Genet. 18:275–277.
   PubMed Web of Science ®Google Scholar
• Carlone, D. L., S. R. L. Hart, P. D. Ladd, and D. G. Skalnik. 2002. Cloning and characterization of the gene encoding the mouse homologue of CpG binding protein. Gene 295:71–77.
   PubMedGoogle Scholar
• Carlone, D. L., and D. G. Skalnik. 2001. CpG binding protein is crucial for early embryonic development. Mol. Cell. Biol. 21:7601–7606.
   PubMedGoogle Scholar
• Chan, M. F., R. Van Amerongen, T. Jijjar, E. Cuppen, P. A. Jones, and P. W. Laird. 2001. Reduced rates of gene loss, gene silencing, and gene mutation in Dnmt1-deficient embryonic stem cells. Mol. Biol. Cell. 21:7587–7600.
   Google Scholar
• Chen, T., Y. Ueda, J. E. Dodge, Z. Wang, and E. Li. 2003. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23:5594–5605.
   PubMed Web of Science ®Google Scholar
• Cross, S. H., R. R. Meehan, X. Nan, and A. Bird. 1997. A component of the transcriptional repressor MeCP1 shares a motif with DNA methyltransferase and HRX proteins. Nat. Genet. 16:256–259.
   PubMedGoogle Scholar
• Dennis, K., T. Fan, T. Geiman, Q. Yan, and K. Muegge. 2001. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 15:2940–2944.
   PubMed Web of Science ®Google 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
• Domer, P. H., S. S. Fakharzadeh, C. S. Chen, J. Jockel, L. Johansen, G. A. Silverman, J. H. Kersey, and S. J. Korsmeyer. 1993. Acute mixed-lineage leukemia t(4;11)(q21;q23) generates an MLL-AF4 fusion product. Proc. Natl. Acad. Sci. USA. 90:7884–7888.
   PubMed Web of Science ®Google Scholar
• Espada, J., E. Ballestar, M. F. Fraga, A. Villar-Garea, A. Juarranz, J. C. Stockert, K. D. Robertson, F. Fuks, and M. Esteller. 2004. Hum. DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern. J. Biol. Chem. 279:37175–37184.
   PubMedGoogle Scholar
• FitzGerald, K. T., and M. O. Diaz. 1999. MLL2: a new mammalian member of the trx/MLL family of genes. Genomics 59:187–192.
   PubMed Web of Science ®Google Scholar
• Fuks, F., W. A. Burgers, A. Brehm, L. Hughes-Davies, and T. Kouzarides. 2000. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nature Genet. 24:88–91.
   PubMed Web of Science ®Google Scholar
• Fuks, F., W. A. Burgers, N. Godin, M. Kasai, and T. Kouzarides. 2001. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J. 20:2536–2544.
   PubMed Web of Science ®Google Scholar
• Fuks, F., P. J. Hurd, R. Deplus, and T. Kouzarides. 2003. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31:2305–2312.
   PubMed Web of Science ®Google Scholar
• Gidekel, S., and Y. Bergman. 2002. A unique developmental pattern of Oct-3/4 DNA methylation is controlled by a cis-demodification element. J. Biol. Chem. 277:34521–34530.
   PubMed Web of Science ®Google Scholar
• Gozani, O., P. Karuman, D. R. Jones, D. Ivanov, J. Cha, A. A. Lugovskoy, C. L. Baird, H. Zhu, S. J. Field, S. L. Lessnick, J. Villasenor, B. Mehrotra, J. Chen, V. R. 'Rao, J. S. Brugge, C. G. Ferguson, B. Payrastre, D. G. Myszka, L. C. Cantley, G. Wagner, N. Divecha, G. D. Prestwich, and J. Yuan. 2003. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphinositide receptor. Cell 114:99–111.
   PubMed Web of Science ®Google Scholar
• Gu, Y., T. Nakamura, H. Alder, R. Prasad, O. Canaani, G. Cimino, C. M. Croce, and E. Canaani. 1992. The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene. Cell 71:701–708.
   PubMed Web of Science ®Google Scholar
• Hattori, N., K. Nishino, Y. Ko, N. Harrori, J. Ohgane, S. Tanaka, and K. Shiota. 2004. Epigenetic control of mouse Oct-4 gene expression in ES cells and TS cells. J. Biol. Chem. 279:17063–17069.
   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
• Jackson-Grusby, L., C. Beard, R. Possemato, M. Tudor, D. Fambrough, G. Csankovszki, J. Dausman, P. Lee, C. Wilson, E. S. Lander, and R. Jaenisch. 2001. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27:31–39.
   PubMed Web of Science ®Google Scholar
• Jeddeloh, J. A., J. Bender, and E. J. Richards. 1998. The DNA methylation locus DDM1 is required for maintenance of gene silencing in Arabidopsis. Genes Dev. 12:1714–1725.
   PubMed Web of Science ®Google Scholar
• Jeddeloh, J. A., T. L. Stokes, and E. J. Richards. 1999. Maintenance of genomic methylation requires a SWI2/SNF-like protein. Nat. Genet. 22:94–97.
   PubMed Web of Science ®Google Scholar
• Keller, G., M. Kennedy, T. Papayannopoulou, and M. Wiles. 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13:473–486.
   PubMed Web of Science ®Google Scholar
• Lee, J.-H., S. R. L. Hart, and D. G. Skalnik. 2004. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 38:32–38.
   PubMed Web of Science ®Google Scholar
• Lee, J.-H., and D. G. Skalnik. 2002. CpG binding protein is a nuclear matrix- and euchromatin-associated protein localized to nuclear speckles containing human trithorax: identification of nuclear matrix targeting signals. J. Biol. Chem. 277:42259–42267.
   PubMedGoogle Scholar
• Lee, J.-H., K. S. Voo, and D. G. Skalnik. 2001. Identification and characterization of the DNA binding domain of CpG-binding protein. J. Biol. Chem. 276:44669–44676.
   PubMed Web of Science ®Google Scholar
• Lehnertz, B., Y. Ueda, A. A. H. A. Derijck, U. Braunschweig, L. Perez-Burgos, S. Kubicek, T. Chen, E. Li, T. Jenuwein, and A. Peters. 2003. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13:1192–1200.
   PubMed Web of Science ®Google Scholar
• Lei, H., S. P. Oh, M. Okano, R. Juttermann, K. A. Goss, R. Jaenisch, and E. Li. 1996. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122:3195–3205.
   PubMed Web of Science ®Google Scholar
• Li, E. 2002. Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3:662–673.
   PubMed Web of Science ®Google Scholar
• Li, E., T. H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926.
   PubMed Web of Science ®Google Scholar
• Ma, Q., H. Alder, K. K. Nelson, D. Chatterjee, Y. Gu, T. Nakamura, E. Canaani, C. M. Croce, L. D. Siracusa, and A. M. Buchberg. 1993. Analysis of the murine ALL-1 gene reveals conserved domains with human ALL-1 and identifies a motif shared with DNA methyltransferases. Proc. Natl. Acad. Sci. USA 90:6350–6354.
   PubMed Web of Science ®Google Scholar
• McClanahan, T., S. Dalrymple, M. Barkett, and F. Lee. 1993. Hematopoietic growth factor receptor genes as markers of lineage commitment during in vitro development of hematopoietic cells. Blood 81:2903–2915.
   PubMed Web of Science ®Google Scholar
• Miller, T., N. J. Krogan, J. Dover, H. Erdjument-Bromage, P. Tempst, M. Johnston, J. F. Greenblatt, and A. Shilatifard. 2001. COMPASS: A complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 98:12902–12907.
   PubMed Web of Science ®Google Scholar
• Miller-Hance, W. C., M. LaCorbiere, S. J. Fuller, S. M. Evans, G. Lyons, C. Schmidt, J. Robbins, and K. R. Chien. 1993. In vitro chamber specification during embryonic stem cell cardiogenesis. J. Biol. Chem. 268:25244–25252.
   PubMedGoogle Scholar
• Milutinovic, S., Q. Zhuang, A. Niveleau, and M. Szyf. 2003. Epigenomic stress response: knockdown of DNA methyltransferase 1 triggers an intra-S-phase arrest of DNA replication and induction of stress response genes. J. Biol. Chem. 278:14985–14995.
   PubMed Web of Science ®Google Scholar
• Monk, M., M. Boubelik, and S. Lehnert. 1987. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99:371–382.
   PubMed Web of Science ®Google Scholar
• Nakamura, T., T. Mori, S. Tada, W. Krajewski, T. Rozovskaia, R. Wassell, G. Dubois, A. Mazo, C. M. Croce, and E. Canaani. 2002. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10:1119–1128.
   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. Teinberg, 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
• Niwa, H., J. Miyazaki, and A. G. Smith. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24:372–376.
   PubMed Web of Science ®Google Scholar
• O'Connell, S., L. Wang, S. Robert, C. A. Jones, R. Saint, and R. S. Jones. 2001. Polycomblike PHD fingers mediate conserved interaction with enhancer of zeste protein. J. Biol. Chem. 276:43065–43073.
   PubMed Web of Science ®Google Scholar
• Okano, M., D. W. Bell, D. A. Haber, and E. Li. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257.
   PubMed Web of Science ®Google Scholar
• Ono, R., T. Taki, T. Taketani, M. Taniwaki, H. Kobayashi, and Y. Hayashi. 2002. LCX, leukemia-associated protein with a CXXC domain, is fused to MLL in acute myeloid leukemia with trilineage dysplasia having t(10;11)(q22;q23). Cancer Res. 62:4075–4080.
   PubMed Web of Science ®Google Scholar
• Ou, X., J. Pollock, M. C. Dinauer, E. Gharehbaghi-Schnell, and D. G. Skalnik. 1999. Identification and functional characterization of the murine Rac2 gene promoter. DNA Cell Biol. 18:253–263.
   PubMedGoogle Scholar
• Pfeifer, G. P., R. L. Tanguay, S. D. Steigerwald, and A. D. Riggs. 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.
   PubMed Web of Science ®Google Scholar
• Prasad, R., T. Yano, C. Sorio, T. Nakamura, R. Rallapalli, Y. Gu, D. Leshkowitz, C. M. Croce, and E. Canaani. 1995. Domains with transcriptional regulatory activity within the ALL1 and AF4 proteins involved in acute leukemia. Proc. Natl. Acad. Sci. USA 92:12160–12164.
   PubMed Web of Science ®Google Scholar
• Reik, W., W. Dean, and J. Walter. 2001. Epigenetic reprogramming in mammalian development. Science 293:1089–1093.
   PubMed Web of Science ®Google Scholar
• Robertson, K. D., S. Ait-Si-Ali, T. Yokochi, P. A. Wade, P. L. Jones, and A. P. Wolffe. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338–342.
   PubMed Web of Science ®Google Scholar
• Roguev, A., D. Schaft, A. Shevchenko, R. Aasland, A. Shevchenko, and A. F. Stewart. 2003. High conservation of the Set1/Rad6 axis of histone 3 lysine 4 methylation in budding and fission yeasts. J. Biol. Chem. 278:8487–8493.
   PubMedGoogle Scholar
• Selker, E. U. 1998. Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc. Natl. Acad. Sci. USA 95:9430–9435.
   PubMedGoogle Scholar
• Singal, R., and G. D. Ginder. 1999. DNA methylation. Blood 93:4059–4070.
   PubMed Web of Science ®Google Scholar
• Stancheva, I., C. Hensey, and R. R. Meehan. 2001. Loss of the maintenance methyltransferase, xDNMT1, induced apoptosis in Xenopus embryos. EMBO J. 20:1963–1973.
   PubMedGoogle Scholar
• Stoger, R., P. Kubicka, C.-G. Liu, T. Kafri, A. Razin, H. Cedar, and D. P. Barlow. 1993. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73:61–71.
   PubMed Web of Science ®Google Scholar
• Szyf, M., V. Bozovic, and G. Tanigawa. 1991. Growth regulation of mouse DNA methyltransferase gene expression. J. Biol. Chem. 266:10027–10030.
   PubMed Web of Science ®Google Scholar
• Tada, M., T. Tada, L. Lefebvre, S. C. Barton, and M. A. Surani. 1997. Embryonic germ cells induce epigenetic reprogramming of somatin nucleus in hybrid cells. EMBO J. 16:6510–6520.
   PubMedGoogle Scholar
• Tamaru, H., X. Zhang, D. McMillen, P. B. Singh, J. I. Nakayama, S. I. Grewal, C. D. Allis, X. Cheng, and E. U. Selker. 2003. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat. Genet. 34:75–79.
   PubMed Web of Science ®Google Scholar
• Thorvaldsen, J. L., K. L. Duran, and M. S. Bartolomei. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12:3693–3702.
   PubMed Web of Science ®Google Scholar
• Tilghman, S. M. 1999. The sins of the fathers and mothers: genomic imprinting in mammalian development. Cell 96:185–193.
   PubMedGoogle Scholar
• Tkachuk, D. C., S. Kohler, and M. L. Cleary. 1992. Involvement of a homolog of Drosophila Trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 71:691–700.
   PubMed Web of Science ®Google Scholar
• Tremblay, K. D., K. L. Duan, and M. S. Bartolomei. 1997. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell. Biol. 17:4322–4329.
   PubMed Web of Science ®Google Scholar
• Tucker, K. L., C. Beard, J. Dausmann, L. Jackson-Grusby, P. W. Laird, H. Lei, E. Li, and R. Jaenisch. 1996. Germ-line passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev. 10:1008–1020.
   PubMed Web of Science ®Google Scholar
• Tucker, K. L., D. Talbot, M. A. Lee, H. Leonhardt, and R. Jaenisch. 1996. Complementation of methylation deficiency in embryonic stem cells by a DNA methyltransferase minigene. Proc. Natl. Acad. Sci. USA 93:12920–12925.
   PubMedGoogle Scholar
• Vannucchi, A. M., S. Linari, C. Cellai, M. J. Koury, and F. Paoletti. 1997. Constitutive and inducible expression of megakaryocyte-specific genes in Friend erythroleukaemia cells. Br. J. Haematol. 99:500–508.
   PubMedGoogle Scholar
• Voo, K. S., D. L. Carlone, B. M. Jacobsen, A. Flodin, and D. G. Skalnik. 2000. Cloning of a mammalian transcriptional activator that binds unmethylated CpG motifs and shares a CXXC domain with DNA methyltransferase, human trithorax, and methyl-CpG binding domain protein 1. Mol. Cell. Biol. 20:2108–2121.
   PubMed Web of Science ®Google Scholar
• Walsh, C. P., J. R. Chaillet, and T. Bestor. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20:116–117.
   PubMed Web of Science ®Google Scholar
• Wilkinson, D. G., S. Bhatt, and B. G. Herrmann. 1990. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343:657–659.
   PubMedGoogle Scholar
• Wobus, A., G. Kaomei, J. Shan, M.-C. Wellner, J. Rohwedel, J. Guanju, B. Fleischmann, H. A. Katus, J. Hescheler, and W.-M. Franz. 1997. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell Cardiol. 29:1525–1539.
   PubMed Web of Science ®Google Scholar
• Wysocka, J., M. P. Myers, C. D. Laherty, R. N. Eisenmann, and W. Herr. 2003. Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3/K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev. 17:896–911.
   PubMed Web of Science ®Google Scholar
• Xu, C., G. Liguori, E. D. Adamson, and M. G. Persico. 1998. Specific arrest of cardiogenesis in cultured embryonic stem cells lacking Cripto-1. Dev. Biol. 196:237–247.
   PubMedGoogle Scholar
• Xu, G.-L., T. H. Bestor, D. Bourc'his, C.-L. Hsieh, N. Tommerup, M. Bugge, M. Hulten, X. Qu, J. J. Russso, and E. Viegas-Pequignot. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187–191.
   PubMed Web of Science ®Google Scholar
• Yoder, J. A., C. P. Walth, and T. H. Bestor. 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13:335–340.
   PubMed Web of Science ®Google Scholar
• Yokoyama, A., Z. Wang, J. Wysocka, M. Sanyal, D. J. Aufiero, I. Kitabayashi, W. Herr, and M. L. Cleary. 2004. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24:5639–5649.
   PubMed Web of Science ®Google Scholar
• Zeleznik-Le, N., A. M. Harden, and J. D. Rowley. 1994. 11q23 translocations split the “AT-hook” cruciform DNA-binding region and the transcriptional repression domain from the activation domain of the mixed-lineage leukemia (MLL) gene. Proc. Natl. Acad. Sci. USA 91:10610–10614.
   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