DNA methylation-mediated epigenetic control

Journal of Cellular Biochemistry

Volumn 108, Issue 1, 2009, Pages 43-51

  Rottach, Andrea ^a   Leonhardt, Heinrich ^a   Spada, Fabio ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

DNA methylation; Dnmt1; Dnmt3a; Dnmt3b; Epigenetics; Histone modification; Methyl CpG binding protein; Uhrf1

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE; METHYL CPG BINDING PROTEIN;

CHROMATIN STRUCTURE; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; EPIGENETICS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW;

ANIMALS; CHROMATIN; DNA METHYLATION; DNA MODIFICATION METHYLASES; EPIGENESIS, GENETIC; HUMANS; MODELS, GENETIC; TRANSCRIPTION, GENETIC;

VERTEBRATA;

EID: 69249125806     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22253     Document Type: Review

References (93)

1. Agarwal N, Hardt T, Brero A, Nowak D, Rothbauer U, Becker A, Leonhardt H, Cardoso MC. 2007. MeCP2 interacts with HP1 and modulates its heterochromatin association during myogenic differentiation. Nucleic Acids Res 35:5402-5408.
2. Arita K, Ariyoshi M, Tochio H, Nakamura Y, Shirakawa M. 2008. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455:818-821.
3. Avvakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, Arrowsmith CH, Dhe-Paganon S. 2008. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455:822-825.
4. Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, Doderlein G, Maltry N, Wu W, Lyko F, Niehrs C. 2007. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445:671-675.
5. Bird A. 2002. DNA methylation patterns and epigenetic memory. Genes Dev 16:6-21.
6. Bird A. 2007. Perceptions of epigenetics. Nature 447:396-398.
7. Bostick M, Kim JK, Esteve P-O, Clark A, Pradhan S, Jacobsen SE. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317:1760-1764.
8. Bourc'his D, Bestor TH. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96-99.
9. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536-2539.
10. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, Leonhardt H, Cardoso MC. 2005. Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J Cell Biol 169:733-743.
11. Cedar H, Bergman Y. 2009. Linking DNA methylation and histone modification: Patterns and paradigms. Nat Rev Genet 10:295-304.
12. Chen T, Ueda Y, Dodge JE, Wang Z, Li E. 2003. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 23:5594-5605.
13. Chuang LS-H, Ian H-I, Koh T-W, Ng H-H, Xu G, Li BFL. 1997. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277:1996-2000.
14. Citterio E, Papait R, Nicassio F, Vecchi M, Gomiero P, Mantovani R, Di Fiore PP, Bonapace IM. 2004. Np95 is a histone-binding protein endowed with ubiquitin ligase activity. Mol Cell Biol 24:2526-2535.
15. Datta J, Ghoshal K, Sharma SM, Tajima S, Jacob ST. 2003. Biochemical fractionation reveals association of DNA methyltransferase (Dnmt) 3b with Dnmt1 and that of Dnmt 3a with a histone H3 methyltransferase and Hdac1. J Cell Biochem 88:855-864.
16. Dennis K, Fan T, Geiman T, Yan Q, Muegge K. 2001. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev 15:2940-2944.
17. Di Croce L, Raker VA, Corsaro M, Fazi F, Fanelli M, Faretta M, Fuks F, Coco FL, Kouzarides T, Nervi C, Minucci S, Pelicci PG. 2002. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 295:1079-1082.
18. Dodge JE, Okano M, Dick F, Tsujimoto N, Chen T, Wang S, Ueda Y, Dyson N, Li E. 2005. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J Biol Chem 280:17986-17991.
19. Easwaran HP, Schermelleh L, Leonhardt H, Cardoso MC. 2004. Replication-independent chromatin loading of Dnmt1 during G2 and M phases. EMBO Rep 5:1181-1186.
20. Epsztejn-Litman S, Feldman N, Abu-Remaileh M, Shufaro Y, Gerson A, Ueda J, Deplus R, Fuks F, Shinkai Y, Cedar H, Bergman Y. 2008. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat Struct Mol Biol 15:1176-1183.
21. Esteve PO, Chin HG, Pradhan S. 2005. Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. Proc Natl Acad Sci USA 102:1000-1005.
22. Esteve PO, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, Carey MF, Pradhan S. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 20:3089-3103.
23. Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, Stein A, Woodcock CL, Skoultchi AI. 2005. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123:1199-1212.
24. Fatemi M, Hermann A, Pradhan S, Jeltsch A. 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.
25. Filion GJ, Zhenilo S, Salozhin S, Yamada D, Prokhortchouk E, Defossez PA. 2006. A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol 26:169-181.
26. Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, Van Neste L, Jaenisch R, Fan G. 2008. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2:160-169.
27. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. 2000. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24:88-91.
28. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T. 2001. Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J 20:2536-2544.
29. Fuks F, Hurd PJ, Deplus R, Kouzarides T. 2003. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 31:2305-2312.
30. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R. 2003. Induction of tumors in mice by genomic hypomethylation. Science 300:489-492.
31. Geiman TM, Sankpal UT, Robertson AK, Zhao Y, Robertson KD. 2004. DNMT3B interacts with hSNF2H chromatin remodeling enzyme, HDACs 1 and 2, and components of the histone methylation system. Biochem Biophys Res Commun 318:544-555.
32. Georgel PT, Horowitz-Scherer RA, Adkins N, Woodcock CL, Wade PA, Hansen JC. 2003. Chromatin compaction by human MeCP2. Assembly of novel secondary chromatin structures in the absence of DNA methylation. J Biol Chem 278:32181-32188.
33. Gibbons RJ, McDowell TL, Raman S, O'Rourke DM, Garrick D, Ayyub H, Higgs DR. 2000. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat Genet 24:368-371.
34. Gilbert N, Thomson I, Boyle S, Allan J, Ramsahoye B, Bickmore WA. 2007. DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J Cell Biol 177:401-411.
35. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481-514.
36. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH. 2006. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311:395-398.
37. Gowher H, Leismann O, Jeltsch A. 2000. DNA of Drosophila melanogaster contains 5-methylcytosine. EMBO J 19:6918-6923.
38. Guil S, Esteller M. 2009. DNA methylomes, histone codes and miRNAs: Tying it all together. Int J Biochem Cell Biol 41:87-95.
39. Hashimoto H, Horton JR, Zhang X, Bostick M, Jacobsen SE, Cheng X. 2008. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455:826-829.
40. Hata K, Okano M, Lei H, Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983-1993.
41. Hendrich B, Tweedie S. 2003. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet 19:269-277.
42. Hermann A, Gowher H, Jeltsch A. 2004. Biochemistry and biology of mammalian DNA methyltransferases. Cell Mol Life Sci 61:2571-2587.
43. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449:248-251.
44. Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, Jacobsen SE. 2007. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17:379-384.
45. Jorgensen HF, Ben-Porath I, Bird AP. 2004. Mbd1 is recruited to both methylated and nonmethylated CpGs via distinct DNA binding domains. Mol Cell Biol 24:3387-3395.
46. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900-903.
47. Kim GD, Ni J, Kelesoglu N, Roberts RJ, Pradhan S. 2002. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J 21:4183-4195.
48. Kim JK, Esteve PO, Jacobsen SE, Pradhan S. 2009. UHRF1 binds G9a and participates in p21 transcriptional regulation in mammalian cells. Nucleic Acids Res 37:493-505.
49. Kunert N, Marhold J, Stanke J, Stach D, Lyko F. 2003. A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 130:5083-5090.
50. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, Hata K, Li E, Matsuda Y, Kimura T, Okabe M, Sakaki Y, Sasaki H, Nakano T. 2008. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22:908-917.
51. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
52. Laird CD, Pleasant ND, Clark AD, Sneeden JL, Hassan KM, Manley NC, Vary JC Jr, Morgan T, Hansen RS, Stoger R. 2004. Hairpin-bisulfite PCR: Assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proc Natl Acad Sci USA 101:204-209.
53. Lande-Diner L, Zhang J, Ben-Porath I, Amariglio N, Keshet I, Hecht M, Azuara V, Fisher AG, Rechavi G, Cedar H. 2007. Role of DNA methylation in stable gene repression. J Biol Chem 282:12194-12200.
54. Leonhardt H, Page AW, Weier HU, Bestor TH. 1992. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71:865-873.
55. Li E, Bestor TH, Jaenisch R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926.
56. Li H, Rauch T, Chen Z-X, Szabo PE, Riggs AD, Pfeifer GP. 2006. The histone methyltransferase SETDB1 and the DNA methyltransferase DNMT3A interact directly and localize to promoters silenced in cancer cells. J Biol Chem 281:19489-19500.
57. Liang G, Chan MF, Tomigahara Y, Tsai YC, Gonzales FA, Li E, Laird PW, Jones PA. 2002. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol Cell Biol 22:480-491.
58. Lorincz MC, Schubeler D, Hutchinson SR, Dickerson DR, Groudine M. 2002. DNA methylation density influences the stability of an epigenetic imprint and Dnmt3a/b-independent de novo methylation. Mol Cell Biol 22:7572-7580.
59. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H. 2009b. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323:1074-1077.
60. Margot JB, Aguirre-Arteta AM, Di Giacco BV, Pradhan S, Roberts RJ, Cardoso MC, Leonhardt H. 2000. Structure and function of the mouse DNA methyltransferase gene: Dnmt1 shows a tripartite structure. J Mol Biol 297:293-300.
61. Margot JB, Ehrenhofer-Murray AE, Leonhardt H. 2003. Interactions within the mammalian DNA methyltransferase family. BMC Mol Biol 4:7-15.
62. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766-770.
63. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G. 2008. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452:45-50.
64. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D. 2008. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30:755-766.
65. Mund C, Musch T, Strodicke M, Assmann B, Li E, Lyko F. 2004. Comparative analysis of DNA methylation patterns in transgenic Drosophila overexpressing mouse DNA methyltransferases. Biochem J 378:763-768.
66. Myant K, Stancheva I. 2008. LSH cooperates with DNA methyltransferases to repress transcription. Mol Cell Biol 28:215-226.
67. Nan X, Hou J, Maclean A, Nasir J, Lafuente MJ, Shu X, Kriaucionis S, Bird A. 2007. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc Natl Acad Sci USA 104:2709-2714.
68. Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416:103-107.
69. Nikitina T, Shi X, Ghosh RP, Horowitz-Scherer RA, Hansen JC, Woodcock CL. 2007. Multiple modes of interaction between the methylated DNA binding protein MeCP2 and chromatin. Mol Cell Biol 27:864-877.
70. Okano M, Xie S, Li E. 1998. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 26:2536-2540.
71. Okano M, Bell DW, Haber DA, Li E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247-257.
72. Papait R, Pistore C, Negri D, Pecoraro D, Cantarini L, Bonapace IM. 2007. Np95 is implicated in pericentromeric heterochromatin replication and in major satellite silencing. Mol Biol Cell 18:1098-1106.
73. Papait R, Pistore C, Grazini U, Babbio F, Cogliati S, Pecoraro D, Brino L, Morand AL, Dechampesme AM, Spada F, Leonhardt H, McBlane F, Oudet P, Bonapace IM. 2008. The PHD domain of Np95 (mUHRF1) is involved in large-scale reorganization of pericentromeric heterochromatin. Mol Biol Cell 19:3554-3563.
74. Rai K, Chidester S, Zavala CV, Manos EJ, James SR, Karpf AR, Jones DA, Cairns BR. 2007. Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev 21:261-266.
75. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR. 2008. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135:1201-1212.
76. Robertson KD, Ait-Si-Ali S, Yokochi T, Wade PA, Jones PL, Wolffe AP. 2000. DNMT1 forms a complex with rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat Genet 25:338-342.
77. Sarraf SA, Stancheva I. 2004. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 15:595-605.
78. Schermelleh L, Haemmer A, Spada F, Rosing N, Meilinger D, Rothbauer U, Cristina Cardoso M, Leonhardt H. 2007. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucl Acids Res 35:4301-43012.
79. Schmitz KM, Schmitt N, Hoffmann-Rohrer U, Schafer A, Grummt I, Mayer C. 2009. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol Cell 33:344-353.
80. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, Tajima S, Mitsuya K, Okano M, Koseki H. 2007. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450:908-912.
81. Silva AJ, Ward K, White R. 1993. Mosaic methylation in clonal tissue. Dev Biol 156:391-398.
82. Spada F, Haemmer A, Kuch D, Rothbauer U, Schermelleh L, Kremmer E, Carell T, Langst G, Leonhardt H. 2007. 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.
83. Suzuki MM, Bird A. 2008. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465-476.
84. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, Shimotohno K, Ishikawa F, Li E, Ueda HR, Nakayama J, Okano M. 2006. 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.
85. Uemura T, Kubo E, Kanari Y, Ikemura T, Tatsumi K, Muto M. 2000. Temporal and spatial localization of novel nuclear protein NP95 in mitotic and meiotic cells. Cell Struct Funct 25:149-159.
86. Unoki M, Nishidate T, Nakamura Y. 2004. ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene 23:7601-7610.
87. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F. 2006. The polycomb group protein EZH2 directly controls DNA methylation. Nature 439:871-874.
88. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, Su H, Sun W, Chang H, Xu G, Gaudet F, Li E, Chen T. 2009. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 41:125-129.
89. Xi S, Zhu H, Xu H, Schmidtmann A, Geiman TM, Muegge K. 2007. Lsh controls Hox gene silencing during development. Proc Natl Acad Sci USA 104:14366-14371.
90. Xu G-L, Bestor TH, Bourc'his D, Hsieh C-L, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187-191.
91. Yasui DH, Peddada S, Bieda MC, Vallero RO, Hogart A, Nagarajan RP, Thatcher KN, Farnham PJ, Lasalle JM. 2007. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc Natl Acad Sci USA 104:19416-19421.
92. Yoon HG, Chan DW, Reynolds AB, Qin J, Wong J. 2003. N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol Cell 12:723-734.
93. Zhu H, Geiman TM, Xi S, Jiang Q, Schmidtmann A, Chen T, Li E, Muegge K. 2006. Lsh is involved in de novo methylation of DNA. EMBO J 25:335-345.