New concepts in DNA methylation

Trends in Biochemical Sciences

Volumn 39, Issue 7, 2014, Pages 310-318

  Jeltsch, Albert ^a   Jurkowska, Renata Z ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

DNA methylation; DNA methyltransferase regulation; DNA methyltransferase specificity; Epigenetic inheritance; Stochastic model

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; CHROMATIN; METHYLTRANSFERASE;

CELLS; CPG ISLAND; DNA METHYLATION; DNA REPLICATION; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME BINDING; EPIGENETICS; GENE INACTIVATION; GENE TARGETING; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; STOCHASTIC MODEL; ANIMAL; CHROMATIN; GENETICS; METABOLISM;

ANIMALS; CHROMATIN; DNA METHYLATION; DNA REPLICATION; HUMANS; METHYLTRANSFERASES;

EID: 84903435240     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.05.002     Document Type: Review

References (79)

1. Riggs A.D. X inactivation, differentiation, and DNA methylation. Cytogenet. Cell Genet. 1975, 14:9-25.
2. Holliday R., Pugh J.E. DNA modification mechanisms and gene activity during development. Science 1975, 187:226-232.
3. Jeltsch A. On the enzymatic properties of Dnmt1: specificity, processivity, mechanism of linear diffusion and allosteric regulation of the enzyme. Epigenetics 2006, 1:63-66.
4. Jurkowska R.Z., et al. Structure and function of mammalian DNA methyltransferases. Chembiochem 2011, 12:206-222.
5. Li E., et al. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992, 69:915-926.
6. Okano M., et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
7. Riggs A.D., Xiong Z. Methylation and epigenetic fidelity. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4-5.
8. Jones P.A., Liang G. Rethinking how DNA methylation patterns are maintained. Nat. Rev. Genet. 2009, 10:805-811.
9. Lin I.G., et al. Murine de novo methyltransferase Dnmt3a demonstrates strand asymmetry and site preference in the methylation of DNA in vitro. Mol. Cell. Biol. 2002, 22:704-723.
10. Handa V., Jeltsch A. Profound flanking sequence preference of Dnmt3a and Dnmt3b mammalian DNA methyltransferases shape the human epigenome. J. Mol. Biol. 2005, 348:1103-1112.
11. Jurkowska R.Z., et al. Approaches to enzyme and substrate design of the murine Dnmt3a DNA methyltransferase. Chembiochem 2011, 12:1589-1594.
12. Jia D., et al. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007, 449:248-251.
13. Jurkowska R.Z., et al. Formation of nucleoprotein filaments by mammalian DNA methyltransferase Dnmt3a in complex with regulator Dnmt3L. Nucleic Acids Res. 2008, 36:6656-6663.
14. Fatemi M., et al. Dnmt3a and Dnmt1 functionally cooperate during de novo methylation of DNA. Eur. J. Biochem. 2002, 269:4981-4984.
15. Kim G.D., et al. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J. 2002, 21:4183-4195.
16. Fatemi M., et al. 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. 2001, 309:1189-1199.
17. Vilkaitis G., et al. Processive methylation of hemimethylated CpG sites by mouse Dnmt1 DNA methyltransferase. J. Biol. Chem. 2005, 280:64-72.
18. Goyal R., et al. Accuracy of DNA methylation pattern preservation by the Dnmt1 methyltransferase. Nucleic Acids Res. 2006, 34:1182-1188.
19. Lorincz M.C., et al. DNA methylation density influences the stability of an epigenetic imprint and Dnmt3a/b-independent de novo methylation. Mol. Cell. Biol. 2002, 22:7572-7580.
20. Takagi H., et al. Overexpression of DNA methyltransferase in myoblast cells accelerates myotube formation. Eur. J. Biochem. 1995, 231:282-291.
21. Vertino P.M., et al. De novo methylation of CpG island sequences in human fibroblasts overexpressing DNA (cytosine-5-)-methyltransferase. Mol. Cell. Biol. 1996, 16:4555-4565.
22. Biniszkiewicz D., et al. Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell. Biol. 2002, 22:2124-2135.
23. Arand J., et al. In vivo control of CpG and non-CpG DNA methylation by DNA methyltransferases. PLoS Genet. 2012, 8:e1002750.
24. Zhang Y., et al. DNA methylation analysis of chromosome 21 gene promoters at single base pair and single allele resolution. PLoS Genet. 2009, 5:e1000438.
25. Landan G., et al. Epigenetic polymorphism and the stochastic formation of differentially methylated regions in normal and cancerous tissues. Nat. Genet. 2012, 44:1207-1214.
26. Song J., et al. Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation. Science 2011, 331:1036-1040.
27. Song J., et al. Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation. Science 2012, 335:709-712.
28. Bashtrykov P., et al. Mechanistic details of the DNA recognition by the Dnmt1 DNA methyltransferase. FEBS Lett. 2012, 586:1821-1823.
29. Bashtrykov P., et al. Specificity of Dnmt1 for methylation of hemimethylated CpG sites resides in its catalytic domain. Chem. Biol. 2012, 19:572-578.
30. Liang G., et al. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell. Biol. 2002, 22:480-491.
31. Chen T., et al. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 2003, 23:5594-5605.
32. Dodge J.E., et al. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem. 2005, 280:17986-17991.
33. 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. U.S.A. 2006, 103:14080-14085.
34. Feng S., et al. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
35. Jeltsch A. Molecular biology. Phylogeny of methylomes. Science 2010, 328:837-838.
36. Lister R., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
37. Guo J.U., et al. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 2014, 17:215-222.
38. Lister R., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
39. Shirane K., et al. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet. 2013, 9:e1003439.
40. Gowher H., Jeltsch A. Enzymatic properties of recombinant Dnmt3a DNA methyltransferase from mouse: the enzyme modifies DNA in a non-processive manner and also methylates non-CpG [correction of non-CpA] sites. J. Mol. Biol. 2001, 309:1201-1208.
41. Aoki A., et al. Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 2001, 29:3506-3512.
42. Kohli R.M., Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 2013, 502:472-479.
43. Pastor W.A., et al. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 2013, 14:341-356.
44. Wu H., Zhang Y. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 2014, 156:45-68.
45. Metivier R., et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
46. Stevenson T.J., Prendergast B.J. Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16651-16656.
47. Williams K., et al. DNA methylation: TET proteins-guardians of CpG islands?. EMBO Rep. 2012, 13:28-35.
48. Jeong S., et al. Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol. Cell. Biol. 2009, 29:5366-5376.
49. Sharma S., et al. Nucleosomes containing methylated DNA stabilize DNA methyltransferases 3A/3B and ensure faithful epigenetic inheritance. PLoS Genet. 2011, 7:e1001286.
50. Jurkowska R.Z., et al. Oligomerization and binding of the Dnmt3a DNA methyltransferase to parallel DNA molecules: heterochromatic localization and role of Dnmt3L. J. Biol. Chem. 2011, 286:24200-24207.
51. Ooi S.K., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
52. Otani J., et al. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 2009, 10:1235-1241.
53. Zhang Y., et al. Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 2010, 38:4246-4253.
54. Dhayalan A., et al. The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 2010, 285:26114-26120.
55. Neri F., et al. Dnmt3L antagonizes DNA methylation at bivalent promoters and favors DNA methylation at gene bodies in ESCs. Cell 2013, 155:121-134.
56. Arita K., et al. Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12950-12955.
57. Rothbart S.B., et al. Association of UHRF1 with methylated H3K9 directs the maintenance of DNA methylation. Nat. Struct. Mol. Biol. 2012, 19:1155-1160.
58. Chuang L.S., et al. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 1997, 277:1996-2000.
59. Bostick M., et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 317:1760-1764.
60. Sharif J., et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
61. Bashtrykov P., et al. The UHRF1 protein stimulates the activity and specificity of the maintenance DNA methyltransferase DNMT1 by an allosteric mechanism. J. Biol. Chem. 2014, 289:4106-4115.
62. Berkyurek A.C., et al. The DNA Methyltransferase Dnmt1 directly interacts with the SET and RING finger associated (SRA) domain of the multifunctional protein Uhrf1 to facilitate accession of the catalytic center to hemi-methylated DNA. J. Biol. Chem. 2013, 10.1074/jbc.M113.523209.
63. Di Ruscio A., et al. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 2013, 503:371-376.
64. Robertson A.K., et al. Effects of chromatin structure on the enzymatic and DNA binding functions of DNA methyltransferases DNMT1 and Dnmt3a in vitro. Biochem. Biophys. Res. Commun. 2004, 322:110-118.
65. Takeshima H., et al. Distinct DNA methylation activity of Dnmt3a and Dnmt3b towards naked and nucleosomal DNA. J. Biochem. 2006, 139:503-515.
66. Takeshima H., et al. Mouse Dnmt3a preferentially methylates linker DNA and is inhibited by histone H1. J. Mol. Biol. 2008, 383:810-821.
67. Dennis K., et al. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 2001, 15:2940-2944.
68. Zhu H., et al. Lsh is involved in de novo methylation of DNA. EMBO J. 2006, 25:335-345.
69. Haerter J.O., et al. Coll-aboration between CpG sites is needed for stable somatic inheritance of DNA methylation states. Nucleic Acids Res. 2014, 42:2235-2244.
70. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer 2011, 11:726-734.
71. Timp W., Feinberg A.P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 2013, 13:497-510.
72. Shih A.H., et al. The role of mutations in epigenetic regulators in myeloid malignancies. Nat. Rev. Cancer 2012, 12:599-612.
73. You J.S., Jones P.A. Cancer genetics and epigenetics: two sides of the same coin?. Cancer Cell 2012, 22:9-20.
74. Varela-Rey M., et al. S-adenosylmethionine levels regulate the schwann cell DNA methylome. Neuron 2014, 81:1024-1039.
75. Negrotto S., et al. CpG methylation patterns and decitabine treatment response in acute myeloid leukemia cells and normal hematopoietic precursors. Leukemia 2012, 26:244-254.
76. Yan P., et al. Genome-wide methylation profiling in decitabine-treated patients with acute myeloid leukemia. Blood 2012, 120:2466-2474.
77. Cortijo S., et al. Mapping the epigenetic basis of complex traits. Science 2014, 343:1145-1148.
78. Jurkowska R.Z., Jeltsch A. Genomic imprinting-the struggle of the genders at the molecular level. Angew. Chem. Int. Ed Engl. 2013, 52:13524-13536.
79. Jeltsch A., Jurkowska R.Z. Multimerization of the dnmt3a DNA methyltransferase and its functional implications. Prog. Mol. Biol. Transl. Sci. 2013, 117:445-464.