Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond

Cell Cycle

Volumn 10, Issue 16, 2011, Pages 2662-2668

  Guo, Junjie U ^a   Su, Yijing ^a   Zhong, Chun ^a   Ming, Guo Li ^a   Song, Hongjun ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 Hydroxymethylcytosine; Active DNA demethylation; BER; DNA methylation; Electroconvulsive stimulation; Epigenetic; Gadd45b; Hippocampus; TET1

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; DNA; DNA METHYLTRANSFERASE; GENOMIC DNA; PROTEIN; TEN ELEVEN TRANSLOCATED PROTEIN 1; TEN ELEVEN TRANSLOCATED PROTEIN 2; TEN ELEVEN TRANSLOCATED PROTEIN 3; UNCLASSIFIED DRUG;

BIOCHEMISTRY; BRAIN; CHEMICAL STRUCTURE; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; GENOME; HUMAN; MAMMAL CELL; NONHUMAN; ONCOGENE; REVIEW;

ANIMALIA; METAZOA;

EID: 80051712275     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.16.17093     Document Type: Review

References (76)

1. Ramsahoye B.H., Biniszkiewicz D., Lyko F., Clark V., Bird A.P., Jaenisch R. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 2000; 97:5237-5242; DOI:10.1073/pnas.97.10.5237; PMID:10805783.
2. Lister R., Pelizzola M., Dowen R.H., Hawkins R.D., Hon G., Tonti-Filippini J., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22; DOI:10.1038/ nature08514; PMID:19829295.
3. Bird A DNA methylation patterns and epigenetic memory Genes Dev 2002; 16:6-21; DOI:10.1101/ gad.947102; PMID:11782440.
4. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005; 74:481-514; DOI:10.1146/annurev.biochem.74.010904.153721; PMID:15952895.
5. Jones P.A., Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009; 10:805-811; DOI:10.1038/nrg2651; PMID:19789556.
6. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010; 11:607-620; DOI:10.1038/nrm2950; PMID:20683471.
7. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119:941-953; DOI:10.1016/j.cell.2004.12.012; PMID:15620353.
8. Klose R.J., Zhang Y Regulation of histone methylation by demethylimination and demethylation Nat Rev Mol Cell Biol 2007; 8:307-18; DOI:10.1038/ nrm2143; PMID:17342184.
9. Zhu J.K. Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 2009; 43:143-166; DOI:10.1146/annurev-genet-102108-134205; PMID:19659441.
10. Surani M.A., Hajkova P. Epigenetic Reprogramming of Mouse Germ Cells toward Totipotency. Cold Spring Harb Symp Quant Biol 75:211-218
11. Bruniquel D., Schwartz R.H. Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat Immunol 2003; 4:235-240; DOI:10.1038/ni887; PMID:12548284.
12. Bhattacharya S.K., Ramchandani S., Cervoni N., Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999; 397:579-583; DOI:10.1038/17533; PMID:10050851.
13. Zhu B., Zheng Y., Hess D., Angliker H., Schwarz S., Siegmann M., et al. 5-methylcytosine-DNA glycosylase activity is present in a cloned G/T mismatch DNA glycosylase associated with the chicken embryo DNA demethylation complex. Proc Natl Acad Sci USA 2000; 97:5135-5139; DOI:10.1073/pnas.100107597; PMID:10779566.
14. Hardeland U., Bentele M., Jiricny J., Schar P. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res 2003; 31:2261-2271; DOI:10.1093/nar/gkg344; PMID:12711670.
15. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns BR DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase and gadd45 Cell 2008; 135:1201-12; DOI:10.1016/j. cell.2008.11.042; PMID:19109892.
16. Métivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R.Z., Carmouche R.P., et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008; 452:45-50; DOI:10.1038/nature06544; PMID:18322525.
17. Wossidlo M., Arand J., Sebastiano V., Lepikhov K., Boiani M., Reinhardt R., et al. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J 2010; 29:1877-88; DOI:10.1038/ emboj.2010.80; PMID:20442707.
18. Hajkova P., Jeffries S.J., Lee C., Miller N., Jackson S.P., Surani MA Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway Science 2010; 329:78-82; DOI:10.1126/science. 1187945; PMID:20595612.
19. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010; 463:1101-1105; DOI:10.1038/nature08829; PMID:20098412.
20. Barreto G., Schafer A., Marhold J., Stach D., Swaminathan S.K., Handa V., et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007; 445:671-675; DOI:10.1038/nature05515; PMID:17268471.
21. Hu X.V., Rodrigues T.M., Tao H., Baker R.K., Miraglia L., Orth A.P., et al. Identification of RING finger protein 4 (RNF4) as a modulator of DNA demethylation through a functional genomics screen. Proc Natl Acad Sci USA 2010; 107:15087-92; DOI:10.1073/ pnas.1009025107; PMID:20696907.
22. Penn N.W., Suwalski R., O'Riley C., Bojanowski K., Yura R. The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochem J 1972; 126:781-790; PMID:4538516.
23. Kinney S.M., Chin H.G., Vaisvila R., Bitinaite J., Zheng Y., Esteve P.O., et al. Tissue specific distribution and dynamic changes of 5- hydroxymethylcytosine in mammalian genome. J Biol Chem.
24. Krais A.M., Park Y.J., Plass C., Schmeiser H.H. Determination of genomic 5-hydroxymethyl-2'-deoxycytidine in human DNA by capillary electrophoresis with laser induced fluorescence. Epigenetics 2011; 6:560-565; DOI:10.4161/epi.6.5. 15678; PMID:21593596.
25. Globisch D., Munzel M., Muller M., Michalakis S., Wagner M., Koch S., et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS ONE 2010; 5:15367; DOI:10.1371/journal.pone. 0015367; PMID:21203455.
26. Münzel M., Globisch D., Bruckl T., Wagner M., Welzmiller V., Michalakis S., et al. Quantification of the sixth DNA base hydroxymethylcytosine in the brain. Angew Chem Int Ed Engl 2010; 49:5375-5377; DOI:10.1002/anie. 201002033; PMID:20583021.
27. Szwagierczak A., Bultmann S., Schmidt C.S., Spada F., Leonhardt H. Sensitive enzymatic quantification of 5-hydroxymethylcytosine in genomic DNA. Nucleic Acids Res 2010; 38:181; DOI:10.1093/nar/gkq684; PMID:20685817.
28. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009; 324:929-930; DOI:10.1126/science.1169786; PMID:19372393.
29. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324:930-935; DOI:10.1126/science.1170116; PMID:19372391.
30. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification Nature 2010; 466:1129-33; DOI:10.1038/ nature09303; PMID:20639862.
31. Zhang H., Zhang X., Clark E., Mulcahey M., Huang S., Shi Y.G. TET1 is a DNA-binding protein that modulates DNA methylation and gene transcription via hydroxylation of 5-methylcytosine. Cell Res 2010; 20:1390-1393; DOI:10.1038/cr.2010.156; PMID:21079648.
32. Warn-Cramer B.J., Macrander L.A., Abbott M.T. Markedly different ascorbate dependencies of the sequential alpha-ketoglutarate dioxygenase reactions catalyzed by an essentially homogeneous thymine 7-hydroxylase from Rhodotorula glutinis. J Biol Chem 1983; 258:10551-10557; PMID:6684117.
33. Aas P.A., Otterlei M., Falnes P.O., Vagbo C.B., Skorpen F., Akbari M., et al. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 2003; 421:859-63; DOI:10.1038/ nature01363; PMID:12594517.
34. Falnes PØ, Johansen R.F., Seeberg E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 2002; 419:178-182; DOI:10.1038/nature01048; PMID:12226668.
35. Koh K.P., Yabuuchi A., Rao S., Huang Y., Cunniff K., Nardone J., et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8:200-213; DOI:10.1016/j.stem.2011.01.008; PMID:21295276.
36. Ono R., Taki T., Taketani T., Taniwaki M., Kobayashi H., Hayashi Y. LCX, leukemia-associated protein with a CXXC domain, is fused to MLL in acute myeloid leukemia with trilineage dysplasia having t(10;11)(q22;q23). Cancer Res 2002; 62:4075-4080; PMID:12124344.
37. Lorsbach R.B., Moore J., Mathew S., Raimondi S.C., Mukatira S.T., Downing J.R. TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;q23). Leukemia 2003; 17:637-641; DOI:10.1038/sj.leu.2402834; PMID:12646957.
38. Bejar R., Levine R., Ebert BL Unraveling the molecular pathophysiology of myelodysplastic syndromes J Clin Oncol 2011; 29:504-15; DOI:10.1200/ JCO.2010.31.1175; PMID:21220588.
39. Ko M., Huang Y., Jankowska A.M., Pape U.J., Tahiliani M., Bandukwala H.S., et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 2010; 468:839-43; DOI:10.1038/ nature09586; PMID:21057493.
40. Figueroa M.E., Abdel-Wahab O., Lu C., Ward P.S., Patel J., Shih A., et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function and impair hematopoietic differentiation. Cancer Cell 2010; 18:553-67; DOI:10.1016/j. ccr.2010.11.015; PMID:21130701.
41. Xu W., Yang H., Liu Y., Yang Y., Wang P., Kim S.H., et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011; 19:17-30; DOI:10.1016/j. ccr.2010.12.014; PMID:21251613.
42. Wossidlo M., Nakamura T., Lepikhov K., Marques C.J., Zakhartchenko V., Boiani M., et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2011; 2:241; PMID:21407207.
43. Iqbal K., Jin S.G., Pfeifer G.P., Szabo PE Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine Proc Natl Acad Sci USA 2011; 108:3642-7; DOI:10.1073/ pnas.1014033108; PMID:21321204.
44. Guo J.U., Su Y., Zhong C., Ming G.L., Song H. Hydroxylation of 5-Methylcytosine by TET1 Promotes Active DNA Demethylation in the Adult Brain. Cell 2011; 145:423-434; DOI:10.1016/j.cell.2011.03.022; PMID:21496894.
45. Pham P., Bransteitter R., Petruska J., Goodman M.F. Processive AID-catalysed cytosine deamination on single- stranded DNA simulates somatic hypermutation. Nature 2003; 424:103-107; DOI:10.1038/nature01760; PMID:12819663.
46. Chaudhuri J., Tian M., Khuong C., Chua K., Pinaud E., Alt F.W. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 2003; 422:726-730; DOI:10.1038/nature01574; PMID:12692563.
47. Cannon S.V., Cummings A., Teebor G.W. 5-Hydroxymethylcytosine DNA glycosylase activity in mammalian tissue. Biochem Biophys Res Commun 1988; 151:1173-1179; DOI:10.1016/S0006-(88)80489-3; PMID:3355548.
48. Liutkeviciute Z., Lukinavicius G., Masevicius V., Daujotyte D., Klimasauskas S. Cytosine-5- methyltransferases add aldehydes to DNA. Nat Chem Biol 2009; 5:400-402; DOI:10.1038/nchembio.172; PMID:19430486.
49. Schmitz K.M., 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 2009; 33:344-53; DOI:10.1016/j. molcel.2009.01.015; PMID:19217408.
50. Valinluck V., Tsai H.H., Rogstad D.K., Burdzy A., Bird A., Sowers L.C. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res 2004; 32:4100-4108; DOI:10.1093/nar/gkh739; PMID:15302911.
51. Ma D.K., Marchetto M.C., Guo J.U., Ming G.L., Gage F.H., Song H. Epigenetic choreographers of neurogenesis in the adult mammalian brain. Nat Neurosci 2010; 13:1338-1344; DOI:10.1038/nn.2672; PMID:20975758.
52. Day J.J., Sweatt J.D. DNA methylation and memory formation. Nat Neurosci 2010; 13:1319-1323; DOI:10.1038/nn.2666; PMID:20975755.
53. Meaney M.J., Ferguson-Smith AC Epigenetic regulation of the neural transcriptome: the meaning of the marks Nat Neurosci 2010; 13:1313-8; DOI:10.1038/ nn1110-1313; PMID:20975754.
54. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003; 302:890-3; DOI:10.1126/science. 1090842; PMID:14593184.
55. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009; 323:1074-1077; DOI:10.1126/science.1166859; PMID:19119186.
56. Elliott E., Ezra-Nevo G., Regev L., Neufeld-Cohen A., Chen A Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice Nat Neurosci 2010; 13:1351-3; DOI:10.1038/ nn.2642; PMID:20890295.
57. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007; 53:857-869; DOI:10.1016/j.neuron.2007.02.022; PMID:17359920.
58. LaPlant Q., Vialou V., Covington H.E., 3rd, Dumitriu D., Feng J., Warren B.L., et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010; 13:1137-43; DOI:10.1038/ nn.2619; PMID:20729844.
59. Feng J., Zhou Y., Campbell S.L., Le T., Li E., Sweatt J.D., et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 2010; 13:423-30; DOI:10.1038/ nn.2514; PMID:20228804.
60. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7:847-854; DOI:10.1038/nn1276; PMID:15220929.
61. Sen G.L., Reuter J.A., Webster D.E., Zhu L., Khavari P.A. DNMT1 maintains progenitor function in selfrenewing somatic tissue. Nature 2010; 463:563-567; DOI:10.1038/nature08683; PMID:20081831.
62. Ma D.K., Guo J.U., Ming G.L., Song H. DNA excision repair proteins and Gadd45 as molecular players for active DNA demethylation. Cell Cycle 2009; 8:1526-1531; DOI:10.4161/cc.8.10.8500; PMID:19377292.
63. Tarpey P.S., Raymond F.L., Nguyen L.S., Rodriguez J., Hackett A., Vandeleur L., et al. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet 2007; 39:1127-33; DOI:10.1038/ ng2100; PMID:17704778.
64. Garbett K., Ebert P.J., Mitchell A., Lintas C., Manzi B., Mirnics K., et al. Immune transcriptome alterations in the temporal cortex of subjects with autism. Neurobiol Dis 2008; 30:303-11; DOI:10.1016/j. nbd.2008.01.012; PMID:18378158.
65. Voineagu I., Wang X., Johnston P., Lowe J.K., Tian Y., Horvath S., et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 2011.
66. Pastor W.A., Pape U.J., Huang Y., Henderson H.R., Lister R., Ko M., et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011; 473:394-397; DOI:10.1038/nature10102; PMID:21552279.
67. Williams K., Christensen J., Pedersen M.T., Johansen J.V., Cloos P.A., Rappsilber J., et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011; 473:343-8; DOI:10.1038/ nature10066; PMID:21490601.
68. Ficz G., Branco M.R., Seisenberger S., Santos F., Krueger F., Hore T.A., et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473:398-402; DOI:10.1038/ nature10008; PMID:21460836.
69. Wu H., D'Alessio A.C., Ito S., Xia K., Wang Z., Cui K., et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 2011; 473:389-393; DOI:10.1038/nature09934; PMID:21451524.
70. Wu H., D'Alessio A.C., Ito S., Wang Z., Cui K., Zhao K., et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 2011; 25:679-684; DOI:10.1101/gad.2036011; PMID:21460036.
71. Song C.X., Szulwach K.E., Fu Y., Dai Q., Yi C., Li X., et al. Selective chemical labeling reveals the genomewide distribution of 5- hydroxymethylcytosine. Nat Biotechnol 2011; 29:68-72; DOI:10.1038/nbt.1732; PMID:21151123.
72. Jin S.G., Wu X., Li A.X., Pfeifer GP Genomic mapping of 5-hydroxymethylcytosine in the human brain Nucleic Acids Res
73. Xu Y., Wu F., Tan L., Kong L., Xiong L., Deng J., et al. Genome-wide Regulation of 5hmC, 5mC and Gene Expression by Tet1 Hydroxylase in Mouse Embryonic Stem Cells. Mol Cell 2011; 42:451-64; DOI:10.1016/j. molcel.2011.04.005; PMID:21514197.
74. Stroud H., Feng S., Morey Kinney S., Pradhan S., Jacobsen SE 5-hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells Genome Biol 2011; 12:54; DOI:10.1186/ gb-2011-12-6-r54; PMID:21689397.
75. Wallace E.V., Stoddart D., Heron A.J., Mikhailova E., Maglia G., Donohoe T.J., et al. Identification of epigenetic DNA modifications with a protein nanopore. Chem Commun (Camb) 2010; 46:8195-7; DOI:10.1039/ c0cc02864a; PMID:20927439.
76. Flusberg B.A., Webster D.R., Lee J.H., Travers K.J., Olivares E.C., Clark T.A., et al. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 2010; 7:461-465; DOI:10.1038/nmeth.1459; PMID:20453866.