Oxidative DNA demethylation mediated by Tet enzymes

National Science Review

Volumn 2, Issue 3, 2015, Pages 318-328

  Xu, Guo Liang ^a   Wong, Jiemin ^b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

5mC oxidation; DNA demethylation; Epigenetic reprograming; TDG; Tet dioxygenase

Indexed keywords

EID: 84954105591     PISSN: 20955138     EISSN: 2053714X     Source Type: Journal    
DOI: 10.1093/nsr/nwv029     Document Type: Review

References (106)

1. Cedar, H and Bergman, Y. Programming of DNA methylation patterns. Annu Rev Biochem 2012; 81: 97-117.
2. Miranda, TB and Jones, PA. DNA methylation: the nuts and bolts of repression. J Cell Physiol 2007; 213: 384-90.
3. Hellman, A and Chess, A. Gene body-specific methylation on the active X chromosome. Science 2007; 315: 1141-3.
4. Suzuki, MM and Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008; 9: 465-76.
5. Maunakea, AK, Nagarajan, RP and Bilenky, Met al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010; 466: 253-7.
6. Jones, PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13: 484-92.
7. Rauch, TA, Wu, X and Zhong, X et al. A human B cellmethylome at 100-base pair resolution. Proc Natl Acad Sci USA 2009; 106: 671-8.
8. Feinberg, AP and Tycko, B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4: 143-53.
9. Sproul, D and Meehan, RR. Genomic insights into cancerassociated aberrant CpG island hypermethylation. Brief Funct Genomics 2013; 12: 174-90.
10. Li, E, Bestor, TH and Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992; 69: 915-26.
11. Yoder, JA, Soman, NS and Verdine, GL et al. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 1997; 270: 385-95.
12. Leonhardt, H, Page, AW and Weier, HU et al. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 1992; 71: 865-73.
13. Sharif, J, Muto, M and Takebayashi, S et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007; 450: 908-12.
14. Bostick, M, Kim, JK and Esteve, PO et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007; 317: 1760-4.
15. Lei, H, Oh, SP and Okano, M et al. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 1996; 122: 3195-205.
16. Okano, M, Xie, S and Li, E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998; 19: 219-20.
17. Okano, M, Bell, DW and Haber, DA et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99: 247-57.
18. Chen, T, Ueda, Y and Dodge, JE et al. Establishment and maintenance of genomic methylation patterns in mouse cells by Dnmt3a and Dnmt3b.Mol Cell Biol 2003; 23: 5594-605.
19. Oswald, J, Engemann, S and Lane, N et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000; 10: 475-8.
20. Mayer, W, Niveleau, A and Walter, J et al. Demethylation of the zygotic paternal genome. Nature 2000; 403: 501-2.
21. Ooi, SK and Bestor, TH. The colorful history of active DNA demethylation. Cell 2008; 133: 1145-8.
22. Tahiliani, M, Koh, KP and Shen, Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324: 930-5.
23. He, YF, Li, BZ and Li, Z et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011; 333: 1303-7.
24. Ito, S, Shen, L and Dai, Q et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333: 1300-3.
25. Valinluck, V and Sowers, LC. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res 2007; 67: 946-50.
26. Gu, TP, Guo, F and Yang, H et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 2011; 477: 606-10.
27. Hu, X, Zhang, L and Mao, SQ et al. Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell 2014; 14: 512-22.
28. Gao, Y, Chen, J and Li, K et al. Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 2013; 12: 453-69.
29. Ficz, G, Branco, MR and Seisenberger, S et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473: 398-402.
30. Koh, KP, Yabuuchi, A and Rao, S et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8: 200-13.
31. Ito, S, D'Alessio, AC and Taranova, OV et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010; 466: 1129-33.
32. Zhang, RR, Cui, QY and Murai, K et al. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 2013; 13: 237-45.
33. Williams, K, Christensen, J and Pedersen, MT et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011; 473: 343-8.
34. Xu, Y, Wu, F and Tan, L 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.
35. Hon, GC, Song, CX and Du, T et al. 5mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol Cell 2014; 56: 286-97.
36. Booth, MJ, Marsico, G and Bachman, M et al. Quantitative sequencing of 5-formylcytosine in DNA at single-base resolution. Nat Chem 2014; 6: 435-40.
37. Dawlaty, MM, Breiling, A and Le, T et al. Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 2013; 24: 310-23.
38. Hashimoto, H, Liu, Y and Upadhyay, AK et al. Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res 2012; 40: 4841-9.
39. Inoue, A and Zhang, Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 2011; 334: 194.
40. Inoue, A, Shen, L and Dai, Q et al. Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res 2011; 21: 1670-6.
41. Rougier, N, Bourc'his, D and Gomes, DM et al. Chromosome methylation patterns during mammalian preimplantation development. Gene Dev 1998; 12: 2108-13.
42. Hackett, JA, Sengupta, R and Zylicz, JJ et al. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013; 339: 448-52.
43. Smiley, JA, Kundracik, M and Landfried, DA et al. Genes of the thymidine salvage pathway: thymine-7-hydroxylase from a Rhodotorula glutinis cDNA library and iso-orotate decarboxylase from Neurospora crassa. Biochim Biophys Acta 2005; 1723: 256-64.
44. Xu, S, Li, W and Zhu, J et al. Crystal structures of isoorotate decarboxylases reveal a novel catalytic mechanism of 5-carboxyl-uracil decarboxylation and shed light on the search for DNA decarboxylase. Cell Res 2013; 23: 1296-309.
45. Zhang, H and Zhu, JK. Active DNA demethylation in plants and animals. Cold Spring Harb Symp Quant Biol 2012; 77: 161-73.
46. Maiti, A and Drohat, AC. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem 2011; 286: 35334-8.
47. Neddermann, P and Jiricny, J. The purification of amismatch-specific thymine-DNA glycosylase from HeLa cells. J Biol Chem 1993; 268: 21218-24.
48. Cortazar, D, Kunz, C and Selfridge, J et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 2011; 470: 419-23.
49. Cortellino, S, Xu, J and Sannai, Met al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011; 146: 67-79.
50. Zhang, L, Lu, X and Lu, J et al. Thymine DNA glycosylase specifically recognizes 5-carboxylcytosine-modified DNA. Nat Chem Biol 2012; 8: 328-30.
51. Shen, L, Wu, H and Diep, D et al. Genome-wide analysis reveals TET-and TDGdependent 5-methylcytosine oxidation dynamics. Cell 2013; 153: 692-706.
52. Song, CX, Szulwach, KE and Dai, Q et al. Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 2013; 153: 678-91.
53. Wu, H, Wu, X and Shen, L et al. Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing. Nat Biotechnol 2014; 32: 1231-40.
54. Wheldon, LM, Abakir, A and Ferjentsik, Z et al. Transient accumulation of 5-carboxylcytosine indicates involvement of active demethylation in lineage specification of neural stem cells. Cell Rep 2014; 7: 1353-61.
55. Guo, F, Li, X and Liang, D et al. Active and passive demethylation of male and female pronuclear DNA in the Mammalian zygote. Cell Stem Cell 2014; 15: 447-58.
56. Hajkova, P, Jeffries, SJ and Lee, C et al. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 2010; 329: 78-82.
57. Wossidlo, M, Arand, J and Sebastiano, V et al. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J 2010; 29: 1877-88.
58. Dawlaty, MM, Ganz, K and Powell, BE et al. Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 2011; 9: 166-75.
59. Dawlaty, MM, Breiling, A and Le, T et al. Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev Cell 2014; 29: 102-11.
60. Yin, R, Mao, SQ and Zhao, B et al. Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J Am Chem Soc 2013; 135: 10396-403.
61. Ficz, G, Hore, TA and Santos, F et al. FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 2013; 13: 351-9.
62. Hackett, JA, Dietmann, S and Murakami, K et al. Synergistic mechanisms of DNA demethylation during transition to ground-state pluripotency. Stem Cell Rep 2013; 1: 518-31.
63. Li, E and Zhang, Y. DNA methylation in mammals. Cold Spring Harb Perspect Biol 2014; 6: a019133.
64. Yamaguchi, S, Hong, K and Liu, R et al. Tet1 controls meiosis by regulating meiotic gene expression. Nature 2012; 492: 443-7.
65. Yamaguchi, S, Shen, L and Liu, Y et al. Role of Tet1 in erasure of genomic imprinting. Nature 2013; 504: 460-4.
66. Solary, E, Bernard, OA and Tefferi, A et al. The Ten-Eleven Translocation-2 (TET2) gene in hematopoiesis and hematopoietic diseases. Leukemia 2014; 28: 485-96.
67. Kriaucionis, S and Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009; 324: 929-30.
68. Iqbal, K, Jin, SG and Pfeifer, GP et al. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 2011; 108: 3642-7.
69. Wossidlo, M, Nakamura, T and Lepikhov, K et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2011; 2: 241.
70. Carlson, LL, Page, AW and Bestor, TH. Properties and localization of DNA methyltransferase in preimplantation mouse embryos: implications for genomic imprinting. Gene Dev 1992; 6: 2536-41.
71. Arand, J, Wossidlo, M and Lepikhov, K et al. Selective impairment of methylation maintenance is the major cause of DNA methylation reprogramming in the early embryo. Epigenetics Chromatin 2015; 8: 1.
72. Shen, L, Inoue, A and He, J et al. Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell 2014; 15: 459-70.
73. Peat, JR, Dean, W and Clark, SJ et al. Genome-wide bisulfite sequencing in zygotes identifies demethylation targets and maps the contribution of TET3 oxidation. Cell Rep 2014; 9: 1990-2000.
74. Wang, L, Zhang, J and Duan, J et al. Programming and inheritance of parental DNA methylomes in mammals. Cell 2014; 157: 979-91.
75. Nakamura, T, Liu, YJ and Nakashima, H et al. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 2012; 486: 415-9.
76. Okashita, N, Kumaki, Y and Ebi, K et al. PRDM14 promotes active DNA demethylation through the ten-eleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells. Development 2014; 141: 269-80.
77. Imamura, M, Miura, K and Iwabuchi, K et al. Transcriptional repression and DNA hypermethylation of a small set of ES cell marker genes in male germline stem cells. BMC Dev Biol 2006; 6: 34.
78. Farthing, CR, Ficz, G and Ng, RK et al. Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet 2008; 4: e1000116.
79. Yu, C, Zhang, YL and Pan, WW et al. CRL4 complex regulates mammalian oocyte survival and reprogramming by activation of TET proteins. Science 2013; 342: 1518-21.
80. Guo, H, Zhu, P and Yan, L et al. The DNA methylation landscape of human early embryos. Nature. 2014; 511: 606-10.
81. Smith, ZD, Chan, MM and Humm, KC et al. DNA methylation dynamics of the human preimplantation embryo. Nature 2014; 511: 611-5.
82. Lu, F, Liu, Y and Jiang, L et al. Role of Tet proteins in enhancer activity and telomere elongation. Gene Dev 2014; 28: 2103-19.
83. Wu, H and Zhang, Y. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 2014; 156: 45-68.
84. Liutkeviciute, Z, Kriukiene, E and Licyte, J et al. Direct decarboxylation of 5-carboxylcytosine by DNA C5-methyltransferases. J Am Chem Soc 2014; 136: 5884-7.
85. Wu, JC and Santi, DV. Kinetic and catalytic mechanism of HhaI methyltransferase. J Biol Chem 1987; 262: 4778-86.
86. Liutkeviciute, Z, Lukinavicius, G and Masevicius, V et al. Cytosine-5-methyltransferases add aldehydes to DNA. Nat Chem Biol 2009; 5: 400-2.
87. Chen, CC, Wang, KY and Shen, CK. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012; 287: 33116-21.
88. Chen, CC, Wang, KY and Shen, CK. DNA 5-methylcytosine demethylation activities of the mammalian DNA methyltransferases. J Biol Chem 2013; 288: 9084-91.
89. Schiesser, S, Hackner, B and Pfaffeneder, T et al. Mechanism and stem-cell activity of 5-carboxycytosine decarboxylation determined by isotope tracing. Angew Chem Int Ed Engl 2012; 51: 6516-20.
90. Morgan, HD, Dean, Wand Coker, HA et al. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem 2004; 279: 52353-60.
91. Popp, C, Dean, Wand Feng, S et al. Genome-wide erasure of DNAmethylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010; 463: 1101-5.
92. Hogenbirk, MA, Heideman, MR and Velds, A et al. Differential programming of B cells in AID deficient mice. PLoS One 2013; 8: e69815.
93. Arioka, Y, Watanabe, A and Saito, K et al. Activation-induced cytidine deaminase alters the subcellular localization of Tet family proteins. PLoS One 2012; 7: e45031.
94. Nabel, CS, Jia, H and Ye, Y et al. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol 2012; 8: 751-8.
95. Wu, H, D'Alessio, AC and Ito, S et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 2011; 473: 389-93.
96. Wu, H, D'Alessio, AC and Ito, S et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Gene Dev 2011; 25: 679-84.
97. Chen, Q, Chen, Y and Bian, C et al. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 2013; 493: 561-4.
98. Deplus, R, Delatte, B and Schwinn, MK et al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J 2013; 32: 645-55.
99. Vella, P, Scelfo, A and Jammula, S et al. Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol Cell 2013; 49: 645-56.
100. Zhang, Q, Liu, X and Gao, W et al. Differential regulation of the teneleven translocation (TET) family of dioxygenases by O-linked beta-Nacetylglucosamine transferase (OGT). J Biol Chem 2014; 289: 5986-96.
101. Wang, Y and Zhang, Y. Regulation of TET protein stability by calpains. Cell Rep 2014; 6: 278-84.
102. Nakagawa, T, Lv, L and Nakagawa, M et al. CRL4(VprBP) E3 ligase promotes monoubiquitylation and chromatin binding of TET dioxygenases. Mol Cell 2015; 57: 247-60.
103. Pfaffeneder, T, Spada, F and Wagner, M et al. Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA. Nat Chem Biol 2014; 10: 574-81.
104. Fu, L, Guerrero, CR and Zhong, N et al. Tet-mediated formation of 5-hydroxymethylcytosine in RNA. J Am Chem Soc 2014; 136: 11582-5.
105. Bachman, M, Uribe-Lewis, S and Yang, X et al. 5-Hydroxymethylcytosine is a predominantly stable DNA modification. Nat Chem 2014; 6: 1049-55.
106. Sweatt, JD. The emerging field of neuroepigenetics. Neuron 2013; 80: 624-32.