Rethinking how DNA methylation patterns are maintained (original) (raw)

• Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nature Rev. Genet. 10, 295–304 (2009).
  Article CAS PubMed Google Scholar
• Probst, A. V., Dunleavy, E. & Almouzni, G. Epigenetic inheritance during the cell cycle. Nature Rev. Mol. Cell Biol. 10, 192–206 (2009).
  Article CAS Google Scholar
• Riggs, A. D. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 14, 9–25 (1975).
  Article CAS PubMed Google Scholar
• Holliday, R. & Pugh, J. E. DNA modification mechanisms and gene activity during development. Science 187, 226–232 (1975).
  Article CAS PubMed Google Scholar
• Smith, H. O. & Kelly, S. V. in DNA Methylation: Biochemistry and Biological Significance (eds Razin, A., Cedar, H. & Riggs, A. D.) 39–71 (Springer, New York, 1984).
  Book Google Scholar
• Chen, T., Ueda, Y., Dodge, J. E., Wang, Z. & Li, E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23, 5594–5605 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Liang, G. et al. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell. Biol. 22, 480–491 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Okano, M., Bell, D. W., Haber, D. A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257 (1999).
  Article CAS PubMed Google Scholar
• Hansen, R. S. et al. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl Acad. Sci. USA 96, 14412–14417 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, G. L. et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187–191 (1999).
  Article CAS PubMed Google Scholar
• Bestor, T., Laudano, A., Mattaliano, R. & Ingram, V. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzyme is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971–983 (1988).
  Article CAS PubMed Google Scholar
• Bestor, T. H. & Ingram, V. M. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc. Natl Acad. Sci. USA 80, 5559–5563 (1983).
  Article CAS PubMed PubMed Central Google Scholar
• Hermann, A., Goyal, R. & Jeltsch, A. The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J. Biol. Chem. 279, 48350–48359 (2004).
  Article CAS PubMed Google Scholar
• Pradhan, S., Bacolla, A., Wells, R. D. & Roberts, R. J. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J. Biol. Chem. 274, 33002–33010 (1999).
  Article CAS PubMed Google Scholar
• Chuang, L. S. et al. Human DNA-(cytosine-5) methyltransferase–PCNA complex as a target for p21WAF1. Science 277, 1996–2000 (1997).
  Article CAS PubMed Google Scholar
• Arita, K., Ariyoshi, M., Tochio, H., Nakamura, Y. & Shirakawa, M. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455, 818–821 (2008).
  Article CAS PubMed Google Scholar
• Avvakumov, G. V. et al. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455, 822–825 (2008).
  Article CAS PubMed Google Scholar
• Bostick, M. et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760–1764 (2007).
  Article CAS PubMed Google Scholar
• Hashimoto, H. et al. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455, 826–829 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Sharif, J. et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908–912 (2007).
  Article CAS PubMed Google Scholar
• Robertson, K. D., Keyomarsi, K., Gonzales, F. A., Velicescu, M. & Jones, P. A. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G0/G1 to S phase transition in normal and tumor cells. Nucleic Acids Res. 28, 2108–2113 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Li, E., Bestor, T. H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926 (1992).
  Article CAS PubMed Google Scholar
• Chen, T. et al. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nature Genet. 39, 391–396 (2007).
  Article CAS PubMed Google Scholar
• Bird, A. P. Use of restriction enzymes to study eukaryotic DNA methylation: II. The symmetry of methylated sites supports semi-conservative copying of the methylation pattern. J. Mol. Biol. 118, 49–60 (1978).
  Article CAS PubMed Google Scholar
• Turker, M. S., Swisshelm, K., Smith, A. C. & Martin, G. M. A partial methylation profile for a CpG site is stably maintained in mammalian tissues and cultured cell lines. J. Biol. Chem. 264, 11632–11636 (1989).
  CAS PubMed Google Scholar
• Pfeifer, G. P., Steigerwald, S. D., Hansen, R. S., Gartler, S. M. & Riggs, A. D. Polymerase chain reaction-aided genomic sequencing of an X chromosome-linked CpG island: methylation patterns suggest clonal inheritance, CpG site autonomy, and an explanation of activity state stability. Proc. Natl Acad. Sci. USA 87, 8252–8256 (1990).
  Article CAS PubMed PubMed Central Google Scholar
• Riggs, A. D. & Xiong, Z. Methylation and epigenetic fidelity. Proc. Natl Acad. Sci. USA 101, 4–5 (2004).
  Article CAS PubMed Google Scholar
• Laird, C. D. et al. Hairpin-bisulfite PCR: assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proc. Natl Acad. Sci. USA 101, 204–209 (2004).
  Article CAS PubMed Google Scholar
• Illingworth, R. S. & Bird, A. P. CpG islands — 'a rough guide'. FEBS Lett. 583, 1713–1720 (2009).
  Article CAS PubMed Google Scholar
• Fatemi, M. et al. Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic Acids Res. 33, e176 (2005).
  Article PubMed PubMed Central Google Scholar
• Gal-Yam, E. N. et al. Constitutive nucleosome depletion and ordered factor assembly at the GRP78 promoter revealed by single molecule footprinting. PLoS Genet. 2, e160 (2006).
  Article PubMed PubMed Central Google Scholar
• Lin, J. C. et al. Role of nucleosomal occupancy in the epigenetic silencing of the MLH1 CpG island. Cancer Cell 12, 432–444 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ooi, S. K. & Bestor, T. H. The colorful history of active DNA demethylation. Cell 133, 1145–1148 (2008).
  Article CAS PubMed Google Scholar
• Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929–930 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Gonzalgo, M. L. et al. The role of DNA methylation in expression of the p19/p16 locus in human bladder cancer cell lines. Cancer Res. 58, 1245–1252 (1998).
  CAS PubMed Google Scholar
• Jeong, S. et al. Selective anchoring of DNA methyltransferases 3A/3B to nucleosomes containing methylated DNA. Mol. Cell. Biol. 20 Jul 2009 (doi:10.1128/MCB.00484-09).
  Article CAS PubMed PubMed Central Google Scholar
• Egger, G. et al. Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc. Natl Acad. Sci. USA 103, 14080–14085 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Schermelleh, L. et al. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res. 35, 4301–4312 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Bernstein, B. E., Meissner, A. & Lander, E. S. The mammalian epigenome. Cell 128, 669–681 (2007).
  Article CAS PubMed Google Scholar
• Zilberman, D., Coleman-Derr, D., Ballinger, T. & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125–129 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ooi, S. K. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714–717 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Dong, K. B. et al. DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity. EMBO J. 27, 2691–2701 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Epsztejn-Litman, S. et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nature Struct. Mol. Biol. 15, 1176–1183 (2008).
  Article CAS Google Scholar
• Smallwood, A., Esteve, P. O., Pradhan, S. & Carey, M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 21, 1169–1178 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Vire, E. et al. The polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871–874 (2006).
  Article CAS PubMed Google Scholar
• Kondo, Y. et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nature Genet. 40, 741–750 (2008).
  Article CAS PubMed Google Scholar
• Fuks, F., Hurd, P. J., Deplus, R. & Kouzarides, T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31, 2305–2312 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Honda, S. & Selker, E. U. Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora crassa. Mol. Cell. Biol. 28, 6044–6055 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Robertson, K. D. et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nature Genet. 25, 338–342 (2000).
  Article CAS PubMed Google Scholar
• Robertson, A. K., Geiman, T. M., Sankpal, U. T., Hager, G. L. & Robertson, K. D. Effects of chromatin structure on the enzymatic and DNA binding functions of DNA methyltransferases DNMT1 and Dnmt3a in vitro. Biochem. Biophys. Res. Commun. 322, 110–118 (2004).
  Article CAS PubMed Google Scholar
• Gowher, H. et al. De novo methylation of nucleosomal DNA by the mammalian Dnmt1 and Dnmt3A DNA methyltransferases. Biochemistry 44, 9899–9904 (2005).
  Article CAS PubMed Google Scholar
• Dennis, K., Fan, T., Geiman, T., Yan, Q. & Muegge, K. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 15, 2940–2944 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Walsh, C. P. & Bestor, T. H. Cytosine methylation and mammalian development. Genes Dev. 13, 26–34 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Spada, F. et al. DNMT1 but not its interaction with the replication machinery is required for maintenance of DNA methylation in human cells. J. Cell Biol. 176, 565–571 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Schlesinger, Y. et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nature Genet. 39, 232–236 (2007).
  Article CAS PubMed Google Scholar
• Felsenfeld, G. & Groudine, M. Controlling the double helix. Nature 421, 448–453 (2003).
  Article PubMed Google Scholar
• Hansen, K. H. et al. A model for transmission of the H3K27me3 epigenetic mark. Nature Cell Biol. 10, 1291–1300 (2008).
  Article CAS PubMed Google Scholar
• Felsenfeld, G. in Epigenetics (eds Allis, C. D., Jenuwein, T. & Reinberg, D.) 15–22 (Cold Spring Harb. Lab. Press, New York, 2007).
  Google Scholar
• Watson, J. D. & Crick, F. H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171, 737–738 (1953).
  Article CAS PubMed Google Scholar
• Berger, S. L., Kouzarides, T., Shiekhattar, R. & Shilatifard, A. An operational definition of epigenetics. Genes Dev. 23, 781–783 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Moving AHEAD with an international human epigenome project. Nature 454, 711–715 (2008).
• Kato, Y. et al. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16, 2272–2280 (2007).
  Article CAS PubMed Google Scholar
• La Salle, S. et al. Loss of spermatogonia and wide-spread DNA methylation defects in newborn male mice deficient in DNMT3L. BMC Dev. Biol. 7, 104 (2007).
  Article PubMed PubMed Central Google Scholar
• Jackson-Grusby, L. et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nature Genet. 27, 31–39 (2001).
  Article CAS PubMed Google Scholar
• Tsumura, A. et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11, 805–814 (2006).
  Article CAS PubMed Google Scholar
• Bourc'his, D., Xu, G. L., Lin, C. S., Bollman, B. & Bestor, T. H. Dnmt3L and the establishment of maternal genomic imprints. Science 294, 2536–2539 (2001).
  Article CAS PubMed Google Scholar
• Goll, M. G. et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311, 395–398 (2006).
  Article CAS PubMed Google Scholar
• Okano, M., Xie, S. & Li, E. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res. 26, 2536–2540 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Tachibana, M. et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779–1791 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, J. et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nature Genet. 41, 125–129 (2009).
  Article CAS PubMed Google Scholar
• Chen, T. & Li, E. Establishment and maintenance of DNA methylation patterns in mammals. Curr. Top. Microbiol. Immunol. 301, 179–201 (2006).
  CAS PubMed Google Scholar
• Rhee, I. et al. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 404, 1003–1007 (2000).
  Article CAS PubMed Google Scholar
• Rhee, I. et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552–556 (2002).
  Article CAS PubMed Google Scholar