Dynamic regulation of DNA methylation during mammalian development

Epigenomics

Volumn 1, Issue 1, 2009, Pages 81-98

  Guibert, Sylvain ^a   Forné, Thierry ^a   Weber, Michael ^a  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

CpG island; DNA methylation; DNMT; Methylome; Primordial germ cell; Reprogramming

Indexed keywords

CYTOSINE; DNA; DNA (CYTOSINE 5) METHYLTRANSFERASE;

ANIMAL; ANIMAL EMBRYO; CPG ISLAND; CYTOLOGY; DNA METHYLATION; EMBRYO DEVELOPMENT; GENETICS; GENOME; GERM CELL; METABOLISM; PROMOTER REGION; REVIEW;

ANIMALS; CPG ISLANDS; CYTOSINE; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GENOME; GERM CELLS; PROMOTER REGIONS, GENETIC;

EID: 73549111178     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.09.5     Document Type: Review

References (103)

1. Ptashne M: On the use of the word 'epigenetic'. Curr. Biol. 17, R233-R236 (2007).
2. Bird A: DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21 (2002). (Pubitemid 34049633)
3. Wang Y, Jorda M, Jones PL et al.: Functional CpG methylation system in a social insect. Science 314, 645-647 (2006). (Pubitemid 44646387)
4. Zilberman D, Gehring M, Tran R.K., Ballinger T., Henikoff S: Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61-69 (2007). (Pubitemid 46026502)
5. Suzuki MM, Kerr AR, De Sousa D, Bird A: CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res. 17, 625-631 (2007). (Pubitemid 46715513)
6. Tweedie S, Charlton J, Clark V., Bird A: Methylation of genomes and genes at the invertebrate-vertebrate boundary. Mol. Cell. Biol. 17, 1469-1475 (1997). (Pubitemid 27097376)
7. Suzuki MM, Bird A: DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476 (2008). (Pubitemid 351693975)
8. Esteller M: Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8, 286-298 (2007). (Pubitemid 46439286)
9. Weber M, Davies JJ, Wittig D et al.: Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet 37, 853-862 (2005). (Pubitemid 41077111)
10. Rauch T, Li H, Wu X., Pfeifer GP: MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res. 66, 7939-7947 (2006). (Pubitemid 44299157)
11. Cokus SJ, Feng S, Zhang X et al.: Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219 (2008). (Pubitemid 351380251)
12. Meissner A, Mikkelsen TS, Gu H et al.: Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 (2008).
13. Walsh CP, Chaillet JR, Bestor TH: Transcription of 1AP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20, 116-117(1998). (Pubitemid 28455441)
14. Bourc'his D, Bestor TH: Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99 (2004). (Pubitemid 39215115)
15. Chen T, Hevi S, Gay F et al.: Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet. 19, 391-396 (2007). (Pubitemid 46328497)
16. Dodge JE, Okano M, Dick F et al.: Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem. 280, 17986-17991 (2005). (Pubitemid 41389041)
17. Maloisel L, Rossignol JL: Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 12, 1381-1389 (1998). (Pubitemid 28213413)
18. Li E, Bestor TH, Jaenisch R: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
19. Lei H, Oh SP, Okano M et al.: De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122, 3195-3205 (1996).
20. Bostick M, Kim JK, Esteve P.O., Clark A., Pradhan S, Jacobsen SE: UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760-1764 (2007). (Pubitemid 47461842)
21. Sharif J, Muto M, Takebayashi S et al.: The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmtl to methylated DNA. Nature 450, 908-912 (2007). (Pubitemid 350231331)
22. Okano M, Bell DW, Haber D.A., Li E: DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999). (Pubitemid 29519904)
23. Hirasawa R, Chiba H, Kaneda M et al.: Maternal and zygotic Dnmtl are necessary and sufficient for the maintenance of DNA mechylation imprints during preimplantacion development. Genes Dev. 22, 1607-1616 (2008). (Pubitemid 351846841)
24. Watanabe D, Suetake I, Tada T., Tajima S: Stage- and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis. Meek Dev. 118, 187-190(2002). (Pubitemid 35292136)
25. Kato Y, Kaneda M, Hata K 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). (Pubitemid 47423893)
26. Kaneda M, Okano M, Hata K et al.: Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900-903 (2004). (Pubitemid 38843304)
27. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH: Dnmt3L and the establishment of maternal genomic imprints. Science 294, 2536-2539 (2001). (Pubitemid 34027291)
28. Hata K, Okano M, Lei H., Li E: Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129, 1983-1993 (2002). (Pubitemid 34874213)
29. Ooi SK, Qiu C, Bernstein E et al.: DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717 (2007). (Pubitemid 47236857)
30. Jia D, Jurkowska RZ, Zhang X, Jeltsch A., Cheng X: Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251 (2007). (Pubitemid 47402375)
31. Klose RJ, Bird AP: Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89-97 (2006). (Pubitemid 43221841)
32. Filion GJ, Zhenilo S, Salozhin S., Yamada D, Prokhortchouk E, Defossez PA: A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol. Cell. Biol. 26, 169-181 (2006).
33. Fournier C, Goto Y, Ballestar E et al.: Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J 21, 6560-6570 (2002). (Pubitemid 35448433)
34. Klose RJ, Sarraf SA, Schmiedeberg L, McDermott S.M., Stancheva I., Bird AP: DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol. Cell 19, 667-678 (2005). (Pubitemid 41219442)
35. Yasui DH, Peddada S, Bieda MC et al.: Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl Acad. Sci. USA 104, 19416-19421 (2007).
36. Hutchins AS, Mullen AC, Lee HW et al.: Gene silencing quantitatively controls the function of a developmental trans-activator. Mol. Cell 10, 81-91 (2002). (Pubitemid 34876564)
37. Zhao X, Ueba T, Christie BR et al.: Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl Acad. Sci. USA 100, 6777-6782 (2003). (Pubitemid 36666656)
38. Prokhortchouk A, Sansom O, Selfridge J et al.: Kaiso-deficient mice show resistance to intestinal cancer. Mol. Cell. Biol. 26, 199-208 (2006).
39. Guy J, Hendrich B, Holmes M., Martin JE, Bird A: A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27, 322-326 (2001). (Pubitemid 32201856)
40. Martin Caballero I., Hansen J, Leaford D., Pollard S, Hendrich BD: The methyl-CpG binding proteins Mecp2, Mbd2 and Kaiso are dispensable for mouse embryogenesis, but play a redundant function in neural differentiation. PLoS ONE 4, e4315 (2009).
41. Walsh CP, Bestor TH: Cytosine methylation and mammalian development. Genes Dev. 13, 26-34 (1999). (Pubitemid 29045113)
42. Jackson-Grusby L., Beard C, Possemato R et al.: Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27, 31-39 (2001). (Pubitemid 32044515)
43. Fouse SD, Shen Y, Pellegrini M et al.: 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 (2008). (Pubitemid 351168712)
44. Eckhardt F, Lewin J, Cortese R et al.: DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet. 38, 1378-1385 (2006). (Pubitemid 44837559)
45. Farthing CR, Ficz G, Ng RK et al.: Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, e1000116(2008).
46. Illingworth R, Kerr A, Desousa D et al.: A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6, e22 (2008).
47. Rakyan VK, Down TA, Thorne NP et al.: An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Genome Res. 18, 1518-1529(2008).
48. Rauch TA, Wu X, Zhong X., Riggs AD, Pfeifer GP: A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci U SA 106, 671-678 (2009).
49. Shen L, Kondo Y, Guo Y et al.: Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet. 3, 2023-2036 (2007).
50. Weber M, Hellmann I, Stadler MB et al.: Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genct. 39 457-466 (2007). (Pubitemid 46514772)
51. Yagi S, Hirabayashi K, Sato S et al.: DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Genome Res. 18, 1969-1978 (2008).
52. Mohn F, Weber M, Rebhan M et al.: Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766 (2008).
53. Zhang Y, Rohde C, Tierling S et al.: DNA methylation analysis of chromosome 21 gene promoters at single base pair and single allele resolution. PLoS Genet. 5, e1000438 (2009).
54. Straussman R, Nejman D, Roberts D et al.: Developmental programming of CpG island methylation profiles in the human genome. Nat. Struct. Mol. Biol. 16, 564-571 (2009).
55. Ball MP, Li JB, Gao Y et al.: Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 27, 361-368 (2009).
56. Schmidl C, Klug M, Boeld TJ et al.: Lineage-specific DNA methylation in T cells correlates with histone methylation and enhancer activity. Genome Res. 19(7), 1165-1174(2009).
57. Wan LB, Bartolomei MS: Regulation of imprinting in clusters: noncoding RNAs versus insulators. Adv. Genet. 61, 207-223 (2008).
58. Hellman A, Chess A: Gene body-specific methylation on the active X chromosome. Science 3\5, 1141-1143 (2007). (Pubitemid 46328027)
59. Waterland RA, Kellermayer R, Rached MT et al.: Epigenomic profiling indicates a role for DNA methylation in early postnatal liver development. Hum. Mol. Genet., 18(16), 3026-3038 (2009).
60. Brown SE, Szyf M: Epigenetic programming of the rRNA promoter by MBD3. Mol. Cell. Biol. 27, 4938-4952 (2007). (Pubitemid 47016143)
61. Kangaspeska S, Stride B, Metivier K et al.: Transient cyclical methylation of promoter DNA. Nature 452, 112-115(2008). (Pubitemid 351355094)
62. Metivier R, Gallais R, Tiffoche C et al.: Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45-50 (2008). (Pubitemid 351355084)
63. Osborne CS, Chakalova L, Brown KE et al.: Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 36, 1065-1071 (2004). (Pubitemid 41184467)
64. Oda M, Yamagiwa A, Yamamoto S et al.: DNA methylation regulates long-range gene silencing of an X-linked homeobox gene cluster in a lineage-specific manner. Genes Dev. 20, 3382-3394 (2006). (Pubitemid 44969157)
65. Feldman N, Gerson A, Fang J et al.: G9amediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat. Cell Biol. 8, 188-194 (2006).
66. Reik W: Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432 (2007). (Pubitemid 46816749)
67. Ng RK, Dean W, Dawson C et al.: Epigenetic restriction of embryonic cell lineage fate by methylation of E1f5. Nat. Cell Biol. 10, 1280-1290 (2008).
68. Epsztejn-Litman S., Feldman N, Abu-Remaileh M et al.: De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat. Struct. Mol. Biol. 15, 1176-1183 (2008).
69. Mikkelsen TS, Hanna J, Zhang X et al.: Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49-55 (2008). (Pubitemid 351931978)
70. Mayer W, Niveleau A, Walter J., Fundele R, Haaf T: Demethylation of the zygotic paternal genome. Nature 403, 501-502 (2000). (Pubitemid 30082186)
71. Oswald J, Engemann S, Lane N et al.: Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478 (2000). (Pubitemid 30247337)
72. Nakamura T, Arai Y, Umehara H et al.: PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 64-71 (2007). (Pubitemid 46024198)
73. Li X, Ito M, Zhou F et al.: A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15, 547-557 (2008).
74. Lees-Murdock D.J., Walsh CP: DNA methylation reprogramming in the germ line. Epigenetics 3, 5-13 (2008). (Pubitemid 351540958)
75. Sasaki H, Matsui Y: Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140 (2008).
76. Hajkova P, Erhardt S, Lane N et al.: Epigenetic reprogramming in mouse primordial germ cells. Meek Dev. 117, 15-23 (2002). (Pubitemid 36158711)
77. Li JY, Lees-Murdock DJ, Xu G.L., Walsh CP: Timing of establishment of paternal methylation imprints in the mouse. Genomics 84, 952-960 (2004). (Pubitemid 39469120)
78. Seki Y, Hayashi K, Itoh K., Mizugaki M, Saitou M, Matsui Y: Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440-458 (2005). (Pubitemid 40175041)
79. Hajkova P, Ancelin K, Waldmann T et al.: Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452, 877-881 (2008). (Pubitemid 351550855)
80. Seki Y, Yamaji M, Yabuta Y et al.: Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134, 2627-2638 (2007). (Pubitemid 47225959)
81. Lees-Murdock D.J., De Felici M, Walsh CP: Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82, 230-237 (2003). (Pubitemid 36808623)
82. Maatouk DM, Kellam LD, Mann MR et al.: DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133, 3411-3418 (2006). (Pubitemid 44501843)
83. Lucifero D, Mann MR, Bartolomei M.S., Trasler JM: Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 13, 839-849 (2004). (Pubitemid 38515213)
84. Chotalia M, Smallwood SA, Ruf N et al.: Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 23, 105-117 (2009).
85. Gehring M, Reik W, Henikoff S: DNA demethylation by DNA repair. Trends Genet. 25(2), 82-90 (2009).
86. Morgan H.D., Dean W, Coker H.A., Reik W., Petersen-Mahrt SK: Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J. Biol. Chem. 279, 52353-52360 (2004). (Pubitemid 39656611)
87. Rai K, Huggins IJ, James S.R., Karpf AR, Jones DA, Cairns BR: DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135, 1201-1212(2008).
88. Barreto G, Schafer A, Marhold J et al.: Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671-675 (2007). (Pubitemid 46232889)
89. Schmitz KM, Schmitt N, Hoffmann-Rohrer U, Schafer A., Grummt I, Mayer C: 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 (2009).
90. Engel N, Tront JS, Erinle T et al.: Conserved DNA methylation in Gadd45a(-/-) mice. Epigenetics 4, 98-99 (2009).
91. Suzuki M, Yamada T, Kihara-Negishi F et al.: Site-specific DNA methylation by a complex of PU.l and Dnmt3a/b. Oncogene 25, 2477-2488 (2006).
92. Wiznerowicz M, Jakobsson J, Szulc J et al.: The Kruppcl-associated box repressor domain can trigger de novo promoter methylation during mouse early embryogenesis. J. Biol. Chem. 282, 34535-34541 (2007). (Pubitemid 350159433)
93. Kuramochi-Miyagawa S., Watanabe T, Gotoh K et al.: DNA methylation of retrotransposon genes is regulated by Piwi family members MIL1 and MIWI2 in murine fetal testes. Genes Dev. 22, 908-917 (2008). (Pubitemid 351482844)
94. Aravin AA, Sachidanandam R, Bourc'his D et al.: A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31, 785-799 (2008).
95. Freitag M, Selker EU: Controlling DNA methylation: many roads to one modification. Curr. Opin. Genet. Dev. 15, 191-199 (2005). (Pubitemid 40410665)
96. Delaval K, Govin J, Cerqueira F., Rousseaux S, Khochbin S, Feil R: Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26, 720-729 (2007).
97. Zhao Q, Rank G, Tan YT et al.: PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat. Struct. Mol. Biol. 16(3), 304-311 (2009).
98. Lane N, Dean W, Erhardt S et al.: Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93 (2003). (Pubitemid 36330631)
99. Chong S, Whitelaw E: Epigenetic gcrmline inheritance. Curr. Opin. Genet. Dev. 14, 692-696 (2004).
100. Blewitt ME, Vickaryous NK, Paldi A, Koseki H., Whitelaw E: Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet. 2, e49 (2006).
101. Chan TL, Yuen ST, Kong CK et al.: Heritable gcrmline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat. Genet. 38, 1178-1183 (2006). (Pubitemid 44470364)
102. Suter CM, Martin DI, Ward RL: Germline epimutation of MLHl in individuals with multiple cancers. Nat. Genet. 36, 497-501 (2004). (Pubitemid 38620035)
103. Hitchins MP, Ward RL: Erasure of MLHl methylation in spermatozoa - implications for epigenetic inheritance. Nat. Genet. 39, 1289 (2007). (Pubitemid 350035008)