DNA demethylation, Tet proteins and 5-hydroxymethylcytosine in epigenetic reprogramming: An emerging complex story

Genomics

Volumn 104, Issue 5, 2014, Pages 324-333

  Hill, Peter W S ^a   Amouroux, Rachel ^a   Hajkova, Petra ^a  

^a MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

Author keywords

5 Hydroxymethylcytosine; Demethylation; Germ cells; IPS; Methylation; Reprogramming; Tet

Indexed keywords

5 CARBOXYLCYTOSINE; 5 FORMYLCYTOSINE; 5 HYDROXYMETHYLCYTOSINE; PROTEIN; TET PROTEIN; UNCLASSIFIED DRUG; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; CYTOSINE; DNA BINDING PROTEIN;

CATALYSIS; CHROMATIN; DNA DEMETHYLATION; DNA METABOLISM; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETIC REPROGRAMMING; EPIGENETICS; GERM LINE; IN VITRO STUDY; MAMMAL; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REVIEW; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL MODEL; GENETIC EPIGENESIS; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NUCLEAR REPROGRAMMING; OXIDATION REDUCTION REACTION;

MAMMALIA;

5-METHYLCYTOSINE; ANIMALS; CELLULAR REPROGRAMMING; CYTOSINE; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION;

EID: 84923132296     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2014.08.012     Document Type: Review

References (92)

1. Waddington C. The Strategy of the Genes; a Discussion of Some Aspects of Theoretical Biology 1957, Allen & Unwin, London.
2. Leitch H., McEwen K.R., Turp A., Encheva V., Carroll T., Grabole N., Mansfield W., Nashun B., Knezovich J.G., Smith A., Surani M.A., Hajkova P. Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 2013, 20:311-316.
3. Meshorer E., Yellajoshula D., George E., Scambler P.J., Brown D.T., Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 2006, 10:105-116.
4. Chen J., Liu H., Liu J., Qi J., Wei B., Yang J., Liang H., Chen Y., Chen J., Wu Y., Guo L., Zhu J., Zhao X., Peng T., Zhang Y., Chen S., Li X., Li D., Wang T., Pei D. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat. Genet. 2013, 45:34-42.
5. Mikkelsen T., Hanna J., Zhang X., Ku M., Wernig M., Schorderet P., Bernstein B.E., Jaenisch R., Lander E.S., Meissner A. Dissecting direct reprogramming through integrative genomic analysis. Nature 2008, 454:49-55.
6. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
7. Wu H., Zhang Y. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 2014, 156:45-68.
8. He Y., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., Ding J., Jia Y., Chen Z., Li L., Sun Y., Li X., Dai Q., Song C.X., Zhang K., He C., Xu G.L. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
9. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., He C., Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
10. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
11. Chuang L., Ian H.I., Koh T.W., Ng H.H., Xu G., Li B.F. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 1997, 277:1996-2000.
12. Sharif J., Muto M., Takebayashi S., Suetake I., Iwamatsu A., Endo T.A., Shinga J., Mizutani-Koseki Y., Toyoda T., Okamura K., Tajima S., Mitsuya K., Okano M., Koseki H. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
13. Bostick M., Kim J.K., Estève P.O., Clark A., Pradhan S., Jacobsen S.E. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 317:1760-1764.
14. Kangaspeska S., Stride B., Métivier R., Polycarpou-Schwarz M., Ibberson D., Carmouche R.P., Benes V., Gannon F., Reid G. Transient cyclical methylation of promoter DNA. Nature 2008, 452:112-115.
15. Métivier R., Gallais R., Tiffoche C., Le Péron C., Jurkowska R.Z., Carmouche R.P., Ibberson D., Barath P., Demay F., Reid G., Benes V., Jeltsch A., Gannon F., Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
16. Shen J., Rideout W.M., Jones P.A. High frequency mutagenesis by a DNA methyltransferase. Cell 1992, 71:1073-1080.
17. Bhattacharya S., Ramchandani S., Cervoni N., Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature 1999, 397:579-583.
18. Zhu B., Zheng Y., Angliker H., Schwarz S., Thiry S., Siegmann M., Jost J.P. 5-Methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. Nucleic Acid Res. 2000, 28:4157-4165.
19. Morales-Ruiz T., Ortega-Galisteo A.P., Ponferrada-Marín M.I., Martínez-Macías M.I., Ariza R.R., Roldán-Arjona T. Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. PNAS 2006, 103:6853-6858.
20. Barreto G., Schäfer A., Marhold J., Stach D., Swaminathan S.K., Handa V., Döderlein G., Maltry N., Wu W., Lyko F., Niehrs C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
21. Hajkova P., Jeffries S.J., Lee C., Miller N., Jackson S.P., Surani M.A. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 2010, 329:78-82.
22. Morgan H., Dean W., Coker H.A., Reik W., Petersen-Mahrt S.K. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J. Biol. Chem. 2004, 279:52353-52360.
23. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., Jacobsen S.E., Reik W. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010, 463:1101-1105.
24. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135:1201-1212.
25. Bhutani N., Brady J.J., Damian M., Sacco A., Corbel S.Y., Blau H.M. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 2010, 463:1042-1047.
26. Nabel C., Jia H., Ye Y., Shen L., Goldschmidt H.L., Stivers J.T., Zhang Y., Kohli R.M. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 2012, 8:751-758.
27. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
28. Valinluck V., Sowers L.C. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res. 2007, 67:946-950.
29. Torres-Padilla M., Bannister A.J., Hurd P.J., Kouzarides T., Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 2006, 50:455-461.
30. Oswald J., Engemann S., Lane N., Mayer W., Olek A., Fundele R., Dean W., Reik W., Walter J. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 2000, 10:475-478.
31. Mayer W., Niveleau A., Walter J., Fundele R., Haaf T. Demethylation of the zygotic paternal genome. Nature 2000, 403:501-502.
32. Wang L., Zhang J., Duan J., Gao X., Zhu W., Lu X., Yang L., Zhang J., Li G., Ci W., Li W., Zhou Q., Aluru N., Tang F., He C., Huang X., Liu J. Programming and inheritance of parental DNA methylomes in mammals. Cell 2014, 157:979-991.
33. Smith Z., Chan M.M., Mikkelsen T.S., Gu H., Gnirke A., Regev A., Meissner A. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 2012, 484:339-344.
34. Seisenberger S., Andrews S., Krueger F., Arand J., Walter J., Santos F., Popp C., Thienpont B., Dean W., Reik W. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 2012, 48:849-862.
35. Hirasawa R., Sasaki H. Dynamic transition of Dnmt3b expression in mouse pre- and early post-implantation embryos. Gene Expr. Patterns 2009, 9:27-30.
36. Wu S., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 2010, 11:607-620.
37. Wossidlo M., Arand J., Sebastiano V., Lepikhov K., Boiani M., Reinhardt R., Schöler H., Walter J. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 2010, 29:1877-1888.
38. Wossidlo M., Nakamura T., Lepikhov K., Marques C.J., Zakhartchenko V., Boiani M., Arand J., Nakano T., Reik W., Walter J. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2011, 2.
39. Gu T., Guo F., Yang H., Wu H.P., Xu G.F., Liu W., Xie Z.G., Shi L., He X., Jin S.G., Iqbal K., Shi Y.G., Deng Z., Szabó P.E., Pfeifer G.P., Li X., Xu G.L. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 2011, 477:606-610.
40. Inoue A., Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 2011, 334:194.
41. Santos F., Peat J., Burgess H., Rada C., Reik W., Dean W. Active demethylation in mouse zygotes involves cytosine deamination and base excision repair. Epigenetics Chromatin 2013, 6:39.
42. Jiang L., Zhang J., Wang J.J., Wang L., Zhang L., Li G., Yang X., Ma X., Sun X., Cai J., Zhang J., Huang X., Yu M., Wang X., Liu F., Wu C.I., He C., Zhang B., Ci W., Liu J. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 2013, 153:773-784.
43. Potok M., Nix D.A., Parnell T.J., Cairns B.R. Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern. Cell 2013, 153:759-772.
44. Frauer C., Hoffmann T., Bultmann S., Casa V., Cardoso M.C., Antes I., Leonhardt H. Recognition of 5-hydroxymethylcytosine by the Uhrf1 SRA domain. PLoS One 2011, 6:e21306.
45. Spruijt C., Gnerlich F., Smits A.H., Pfaffeneder T., Jansen P.W.T.C., Bauer C., Münzel M., Wagner M., Müller M., Khan F., Eberl H.C., Mensinga A., Brinkman A.B., Lephikov K., Müller U., Walter J., Boelens R., van Ingen H., Leonhardt H., Carell T., Vermeulen M. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013, 152:1146-1159.
46. Inoue A., Shen L., Dai Q., He C., Zhang Y. Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res. 2011, 21:1670-1676.
47. Lawson K., Hage W.J. Clonal analysis of the origin of primordial germ cells in the mouse. CIBA Found. Symp. 1994, 182:84-91.
48. Hajkova P., Ancelin K., Waldmann T., Lacoste N., Lange U.C., Cesari F., Lee C., Almouzni G., Schneider R., Surani M.A. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 2008, 452:877-881.
49. Seki Y., Yamaji M., Yabuta Y., Sano M., Shigeta M., Matsui Y., Saga Y., Tachibana M., Shinkai Y., Saitou M. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 2007, 134:2627-2638.
50. Anderson R., Copeland T.K., Schöler H., Heasman J., Wylie C. The onset of germ cell migration in the mouse embryo. Mech. Dev. 2000, 91:61-68.
51. Molyneaux K., Stallock J., Schaible K., Wylie C. Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 2001, 240:488-498.
52. Guibert S., Forné T., Weber M. Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 2012, 22:633-641.
53. Cedar H., Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 2009, 10:295-304.
54. Kurimoto K., Yabuta Y., Ohinata Y., Shigeta M., Yamanaka K., Saitou M. Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 2008, 1617-1635.
55. Yamaguchi S., Hong K., Liu R., Inoue A., Shen L., Zhang K., Zhang Y. Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res. 2013, 23:329-339.
56. Kagiwada S., Kurimoto K., Hirota T., Yamaji M., Saitou M. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J. 2013, 32:340-353.
57. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., Walter J., Surani M.A. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 2002, 117:15-23.
58. Hackett J., Sengupta R., Zylicz J.J., Murakami K., Lee C., Down T.A., Surani M.A. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013, 339:448-452.
59. Vincent J., Huang Y., Chen P.Y., Feng S., Calvopin J.H., Nee K., Lee S.A., Le T., Yoon A.J., Faull K., Fan G., Rao A., Jacobsen S.E., Pellegrini M., Clark A.T. Stage-specific roles for Tet1 and Tet2 in DNA demethylation in primordial germ cells. Cell Stem Cell 2013, 12:470-478.
60. Hayashi K., Ohta H., Kurimoto K., Aramaki S., Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 2011, 146:519-532.
61. Vincent J., Ziwei L., Lee S.A., Liu X., Etter M.O., Diaz-Perez S.V., Taylor S.K., Gkountela S., Lindgreen A.G., Clark A.T. Single cell analysis facilitates staging of Blimp1-dependent primordial germ cells derived from mouse embryonic stem cells. PLoS One 2011, 6:e28960.
62. Ying Q., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
63. Grabole N., Tischler J., Hackett J.A., Kim S., Tang F., Leitch H.G., Magnu E., Surani M.A. Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep. 2013, 14:629-637.
64. Ficz G., Hore T.A., Santos F., Lee H.J., Dean W., Arand J., Krueger F., Oxley D., Paul Y.L., Walter J., Cook S.J., Andrews S., Branco M.R., Reik W. FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 2013, 13:351-359.
65. Chuva de Sousa Lopes S., Hayashi K., Shovlin T.C., Mifsud W., Surani M.A., McLaren A. X chromosome activity in mouse XX primordial germ cells. PLoS Genet. 2008, 4:e30.
66. Kelsey G., Feil R. New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 368:20110336.
67. Huang Y., Pastor W.A., Shen Y., Tahiliani M., Liu D.R., Rao A. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One 2010, 5:e8888.
68. Dawlaty M., Breiling A., Le T., Raddatz G., Barrasa M.I., Cheng A.W., Gao Q., Powell B.E., Li Z., Xu M., Faull F.F., Lyko F., Jaenisch R. Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev. Cell 2013, 24:310-323.
69. Yamaguchi S., Shen L., Liu Y., Sendler D., Zhang Y. Role of Tet1 in erasure of genomic imprinting. Nature 2013, 504:460-464.
70. Yamaguchi S., Hong K., Liu R., Shen L., Inoue A., Diep D., Zhang K., Zhang Y. Tet1 controls meiosis by regulating meiotic gene expression. Nature 2012, 492:443-447.
71. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
72. Koche R., Smith Z.D., Adli M., Gu H., Ku M., Gnirke A., Bernstein B.E., Meissner A. Reprogramming factor expression initiates widespread targeted chromatin remodeling. Cell Stem Cell 2011, 8:96-105.
73. Papp B., Plath K. Epigenetics of reprogramming to induced pluripotency. Cell 2013, 152:1324-1343.
74. Koh K., Yabuuchi A., Rao S., Huang Y., Cunniff K., Nardone J., Laiho A., Tahiliani M., Sommer C.A., Mostoslavsky G., Lahesmaa R., Orkin S.H., Rodig S.J., Daley G.Q., Rao A. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011, 200-213.
75. Doege C., Inoue K., Yamashita T., Rhee D.B., Travis S., Fujita R., Guarnieri P., Bhagat G., Vanti W.B., Shih A., Levine R.L., Nik S., Chen E.I., Abeliovich A. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 2012, 488:652-655.
76. Chen J., Guo L., Zhang L., Wu H., Yang J., Liu H., Wang X., Hu X., Gu T., Zhou Z., Liu J., Liu J., Wu H., Mao S.Q., Mo K., Li Y., Lai K., Qi J., Yao H., Pan G., Xu G.L., Pei D. Vitamin C modulates TET1 function during somatic cell reprogramming. Nat. Genet. 2013, 45:1504-1509.
77. Costa Y., Ding J., Theunissen T.W., Faiola F., Hore T.A., Shliaha P.V., Fidalgo M., Saunders A., Lawrence M., Dietmann S., Das S., Levasseur D.N., Li Z., Xu M., Reik W., Silva J.C., Wang J. NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature 2013, 495:370-374.
78. Gao Y., Chen J., Li K., Wu T., Huang B., Liu W., Kou X., Zhang Y., Huang H., Jiang Y., Yao C., Liu X., Lu Z., Xu Z., Kang L., Chen J., Wang H., Cai T., Gao S. Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 2013, 12:453-469.
79. Hu X., Zhang L., Mao S.Q., Li Z., Chen J., Zhang R.R., Wu H.P., Gao J., Guo F., Liu W., Xu G.F., Dai H.Q., Shi Y.G., Li X., Hu B., Tang F., Pei D., Xu G.L. Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell 2014, 14:512-522.
80. Gurdon J., Elsdale T.R., Fischberg M. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 1958, 182:64-65.
81. Rideout W., Eggan K., Jaenisch R. Nuclear cloning and epigenetic reprogramming of the genome. Science 2001, 293:1093-1098.
82. Chan M., Smith Z.D., Egli D., Regev A., Meissner A. Mouse ooplasm confers context-specific reprogramming capacity. Nat. Genet. 2012, 44:978-980.
83. Tada M., Takahama Y., Abe K., Nakatsuji N., Tada T. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr. Biol. 2001, 11:1553-1558.
84. Cowan C., Atienza J., Melton D.A., Eggan K. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 2005, 309:1369-1373.
85. Piccolo F., Pereira C.F., Cantone I., Brown K., Tsubouchi T., Soza-Ried J., Merkenschlager M., Fisher A.G. Using heterokaryons to understand pluripotency and reprogramming. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:2260-2265.
86. Piccolo F., Bagci H., Brown K.E., Landeira D., Soza-Ried J., Feytout A., Mooijman D., Hajkova P., Leitch H.G., Tada T., Kriaucionis S., Dawlaty M.M., Jaenisch R., Merkenschlager M., Fisher A.G. Different roles for Tet1 and Tet2 proteins in reprogramming-mediated erasure of imprints induced by EGC fusion. Mol. Cell 2013, 49:1023-1033.
87. Williams K., Christensen J., Pedersen M.T., Johansen J.V., Cloos P.A., Rappsilber J., Helin K. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011, 473:343-348.
88. Jin C., Lu Y., Jelinek J., Liang S., Estecio M.R., Barton M.C., Issa J.P. TET1 is a maintenance DNA demethylase that prevents methylation spreading in differentiated cells. Nucleic Acid Res. 2014, 42:6956-6971.
89. Mellén M., Ayata P., Dewell S., Kriaucionis S., Heintz N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 2012, 151:1417-1430.
90. Sun Z., Terragni J., Borgaro J.G., Liu Y., Yu L., Guan S., Wang H., Sun D., Cheng X., Zhuemail Z., Pradhan S., Zheng Y. High-resolution enzymatic mapping of genomic 5-hydroxymethylcytosine in mouse embryonic stem cells. Cell Rep. 2013, 3:567-576.
91. Wu H., D'Alessio A.C., Ito S., Xia K., Wang Z., Cui K., Zhao K., Sun Y.E., Zhang Y. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 2011, 473:389-393.
92. Chen Q., Chen Y., Bian C., Fujiki R., Yu X. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 2013, 493:561-564.