DNA Methylation Density Influences the Stability of an Epigenetic Imprint and Dnmt3a/b-Independent De Novo Methylation

REFERENCES

• 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 with engineered green fluorescent proteins. Proc. Natl. Acad. Sci. USA 93: 8508–8511.
   PubMedGoogle Scholar
• Bestor, T. H. 2000. The DNA methyltransferases of mammals. Hum. Mol. Genet 9: 2395–2402.
   PubMed Web of Science ®Google Scholar
• Bestor, T. H., and V. M. Ingram. 1983. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc. Natl. Acad. Sci. USA 80: 5559–5563.
   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. 2002. DNA methylation patterns and epigenetic memory. Genes Dev. 16: 6–21.
   PubMed Web of Science ®Google Scholar
• Boyes, J., and A. Bird. 1991. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64: 1123–1134.
   PubMed Web of Science ®Google Scholar
• Boyes, J., and A. Bird. 1992. Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. EMBO J. 11: 327–333.
   PubMed Web of Science ®Google Scholar
• Brandeis, M., D. Frank, I. Keshet, Z. Siegfried, M. Mendelsohn, A. Nemes, V. Temper, A. Razin, and H. Cedar. 1994. Sp1 elements protect a CpG island from de novo methylation. Nature 371: 435–438.
   PubMed Web of Science ®Google Scholar
• Carotti, D., S. Funiciello, F. Palitti, and R. Strom. 1998. Influence of preexisting methylation on the de novo activity of eukaryotic DNA methyltransferase. Biochemistry 37: 1101–1108.
   PubMedGoogle 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
• 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 antitumor immunity. Proc. Natl. Acad. Sci. USA 90: 3539–3543.
   PubMed Web of Science ®Google Scholar
• Eads, C. A., K. D. Danenberg, K. Kawakami, L. B. Saltz, P. V. Danenberg, and P. W. Laird. 1999. CpG island hypermethylation in human colorectal tumors is not associated with DNA methyltransferase overexpression. Cancer Res. 59: 2302–2306.
   PubMed Web of Science ®Google Scholar
• Fatemi, M., A. Hermann, S. Pradhan, and A. Jeltsch. 2001. The activity of the murine DNA methyltransferase Dnmt1 is controlled by interaction of the catalytic domain with the N-terminal part of the enzyme leading to an allosteric activation of the enzyme after binding to methylated DNA. J. Mol. Biol. 309: 1189–1199.
   PubMedGoogle 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
• Graff, J. R., J. G. Herman, S. Myohanen, S. B. Baylin, and P. M. Vertino. 1997. Mapping patterns of CpG island methylation in normal and neoplastic cells implicates both upstream and downstream regions in de novo methylation. J. Biol. Chem. 272: 22322–22329.
   PubMed Web of Science ®Google Scholar
• Grez, M., E. Akgun, F. Hilberg, and W. Ostertag. 1990. Embryonic stem cell virus, a recombinant murine retrovirus with expression in embryonic stem cells. Proc. Natl. Acad. Sci. USA 87: 9202–9206.
   PubMed Web of Science ®Google Scholar
• Groudine, M., and K. F. Conklin. 1985. Chromatin structure and de novo methylation of sperm DNA: implications for activation of the paternal genome. Science 228: 1061–1068.
   PubMedGoogle Scholar
• Harrington, M. A., P. A. Jones, M. Imagawa, and M. Karin. 1988. Cytosine methylation does not affect binding of transcription factor Sp1. Proc. Natl. Acad. Sci. USA 85: 2066–2070.
   PubMed Web of Science ®Google Scholar
• Hsieh, C. L. 1994. Dependence of transcriptional repression on CpG methylation density. Mol. Cell. Biol. 14: 5487–5494.
   PubMed Web of Science ®Google Scholar
• Hsieh, C. L. 1999. Evidence that protein binding specifies sites of DNA demethylation. Mol. Cell. Biol. 19: 46–56.
   PubMedGoogle Scholar
• Hu-Li, J., C. Pannetier, L. Guo, M. Lohning, H. Gu, C. Watson, M. Assenmacher, A. Radbruch, and W. E. Paul. 2001. Regulation of expression of IL-4 alleles: analysis with a chimeric GFP/IL-4 gene. Immunity 14: 1–11.
   PubMed Web of Science ®Google Scholar
• Huang, T. H., M. R. Perry, and D. E. Laux. 1999. Methylation profiling of CpG islands in human breast cancer cells. Hum. Mol. Genet. 8: 459–470.
   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
• Knebel-Morsdorf, D., S. Achten, K. D. Langner, R. Ruger, B. Fleckenstein, and W. Doerfler. 1988. Reactivation of the methylation-inhibited late E2A promoter of adenovirus type 2 by a strong enhancer of human cytomegalovirus. Virology 166: 166–174.
   PubMedGoogle 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., 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
• Liang, G., M. F. Chan, Y. Tomigahara, Y. C. Tsai, F. A. Gonzales, E. Li, P. W. Laird, and P. A. Jones. 2002. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell. Biol. 22: 480–491.
   PubMed Web of Science ®Google Scholar
• Lichtenstein, M., G. Keini, H. Cedar, and Y. Bergman. 1994. B cell-specific demethylation: a novel role for the intronic kappa chain enhancer sequence. Cell 76: 913–923.
   PubMedGoogle Scholar
• Lin, I. G., T. J. Tomzynski, Q. Ou, and C. L. Hsieh. 2000. Modulation of DNA binding protein affinity directly affects target site demethylation. Mol. Cell. Biol. 20: 2343–2349.
   PubMedGoogle Scholar
• Loh, T. P., L. L. Sievert, and R. W. Scott. 1990. Evidence for a stem cell-specific repressor of Moloney murine leukemia virus expression in embryonal carcinoma cells. Mol. Cell. Biol. 10: 4045–4057.
   PubMed Web of Science ®Google Scholar
• Lorincz, M. C., D. Schubeler, 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
• Lorincz, M. C., D. Schubeler, and M. Groudine. 2001. Methylation-mediated proviral silencing is associated with MeCP2 recruitment and localized histone H3 deacetylation. Mol. Cell. Biol. 21: 7913–7922.
   PubMedGoogle Scholar
• Mummaneni, P., K. A. Walker, P. L. Bishop, and M. S. Turker. 1995. Epigenetic gene inactivation induced by a cis-acting methylation center. J. Biol. Chem. 270: 788–792.
   PubMedGoogle 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
• Niwa, O., Y. Yokota, H. Ishida, and T. Sugahara. 1983. Independent mechanisms involved in suppression of the Moloney leukemia virus genome during differentiation of murine teratocarcinoma cells. Cell 32: 1105–1113.
   PubMedGoogle 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
• Okano, M., S. Xie, and E. Li. 1998. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 19: 219–220.
   PubMed Web of Science ®Google Scholar
• Okano, M., S. Xie, and E. Li. 1998. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res. 26: 2536–2540.
   PubMed Web of Science ®Google Scholar
• Paroush, Z., I. Keshet, J. Yisraeli, and H. Cedar. 1990. Dynamics of demethylation and activation of the alpha-actin gene in myoblasts. Cell 63: 1229–1237.
   PubMed Web of Science ®Google Scholar
• Pradhan, S., A. Bacolla, R. D. Wells, and R. J. Roberts. 1999. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J. Biol. Chem. 274: 33002–33010.
   PubMed Web of Science ®Google Scholar
• Rhee, I., K. E. Bachman, B. H. Park, K. W. Jair, R. W. Yen, K. E. Schuebel, H. Cui, A. P. Feinberg, C. Lengauer, K. W. Kinzler, S. B. Baylin, and B. Vogelstein. 2002. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416: 552–556.
   PubMed Web of Science ®Google Scholar
• Riggs, A. D., Z. Xiong, L. Wang, and J. M. LeBon. 1998. Methylation dynamics, epigenetic fidelity and X chromosome structure. Novartis Found. Symp. 214: 214–225.
   PubMedGoogle Scholar
• Robertson, K. D., E. Uzvolgyi, G. Liang, C. Talmadge, J. Sumegi, F. A. Gonzales, and P. A. Jones. 1999. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res. 27: 2291–2298.
   PubMed Web of Science ®Google Scholar
• Schubeler, 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
• Silke, J., K. I. Rother, O. Georgiev, W. Schaffner, and K. Matsuo. 1995. Complex demethylation patterns at Sp1 binding sites in F9 embryonal carcinoma cells. FEBS Lett. 370: 170–174.
   PubMedGoogle Scholar
• Tollefsbol, T. O., and C. A. Hutchison 3rd. 1997. Control of methylation spreading in synthetic DNA sequences by the murine DNA methyltransferase. J. Mol. Biol. 269: 494–504.
   PubMedGoogle Scholar
• Vertino, P. M., R. W. Yen, J. Gao, and S. B. Baylin. 1996. De novo methylation of CpG island sequences in human fibroblasts overexpressing DNA (cytosine-5-)-methyltransferase. Mol. Cell. Biol. 16: 4555–4565.
   PubMed Web of Science ®Google Scholar
• Walters, M. C., S. Fiering, J. Eidemiller, W. Magis, M. Groudine, and D. I. Martin. 1995. Enhancers increase the probability but not the level of gene expression. Proc. Natl. Acad. Sci. USA 92: 7125–7129.
   PubMedGoogle Scholar
• Wolffe, A. P., P. L. Jones, and P. A. Wade. 1999. DNA demethylation. Proc. Natl. Acad. Sci. USA 96: 5894–5896.
   PubMed Web of Science ®Google Scholar
• Yisraeli, J., R. S. Adelstein, D. Melloul, U. Nudel, D. Yaffe, and H. Cedar. 1986. Muscle-specific activation of a methylated chimeric actin gene. Cell 46: 409–416.
   PubMedGoogle Scholar
• Yoder, J. A., N. S. Soman, G. L. Verdine, and T. H. Bestor. 1997. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 270: 385–395.
   PubMed Web of Science ®Google Scholar