DNA demethylation by TDG

Epigenomics

Volumn 4, Issue 4, 2012, Pages 459-467

  Dalton, Shannon R ^a,b   Bellacosa, Alfonso ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b ICeutica Inc   (United States)

Author keywords

5 carboxylcytosine; 5 formylcytosine; 5 hydroxymethylcytosine; 5 hydroxymethyluracil; base excision repair; DNA demethylation; DNA methylation; embryonic lethality; histone modification; thymine DNA glycosylase

Indexed keywords

CYTOSINE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; THYMINE DNA GLYCOSYLASE;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; DNA REPLICATION; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME INACTIVATION; EPIGENETICS; EXCISION REPAIR; GENE EXPRESSION; GENE FREQUENCY; HUMAN; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; CPG ISLANDS; DNA METHYLATION; DNA REPAIR; GENE EXPRESSION REGULATION; MICE; THYMINE DNA GLYCOSYLASE; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 84865453255     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.12.36     Document Type: Review

References (74)

1. Bird A. The essentials of DNA methylation. Cell 70, 5-8 (1992).
2. Kass SU, Landsberger N, Wolffe AP. DNA methylation directs a time-dependent repression of transcription initiation. Curr. Biol. 7, 157-165 (1997).
3. Siegfried Z, Cedar H. DNA methylation: a molecular lock. Curr. Biol. 7, R305-R307 (1997).
4. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
5. Okano M, Bell DW, Haber DA et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
6. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat. Rev. Cancer 4, 143-153 (2004).
7. Jones PA, Laird PW. Cancer epigenetics comes of age. Nat. Genet. 21, 163-167 (1999).
8. Mayer W, Niveleau A, Walter J et al. Demethylation of the zygotic paternal genome. Nature 403, 501-502 (2000).
9. Oswald J, Engemann S, Lane N et al. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478 (2000).
10. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 293, 1089-1093 (2001).
11. Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762 (2007).
12. Kress C, Thomassin H, Grange T. Local DNA demethylation in vertebrates: how could it be performed and targeted? FEBS Lett. 494, 135-140 (2001).
13. Niehrs C. Active DNA demethylation and DNA repair. Differentiation 77, 1-11 (2009).
14. Guo JU, Su Y, Zhong C et al. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423-434 (2011).
15. Ma DK, Jang MH, Guo JU et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077 (2009).
16. Barreto G, Schafer A, Marhold J et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671-675 (2007).
17. Niehrs C, Schafer A. Active DNA demethylation by Gadd45 and DNA repair. Trends Cell Biol. 22(4), 220-227 (2012).
18. Buontempo S, Sannai M, Bellacosa A. MBD4/MED1 protein in DNA repair and demethylation, cancer, and other diseases. In: Cancer Epigenetics - Biomolecular Therapeutics for Human Cancer. Giordano A, Macaluso M (Eds). Wiley-Blackwell, NJ, USA, 145-162 (2012).
19. Rai K, Huggins IJ, James SR et al. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase and gadd45. Cell 135, 1201-1212 (2008).
20. Choi Y, Gehring M, Johnson L et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33-42 (2002).
21. Gehring M, Huh JH, Hsieh TF et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495-506 (2006).
22. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marin MI et al. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. USA 103, 6853-6858 (2006).
23. Zheng X, Pontes O, Zhu J et al. ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455, 1259-1262 (2008).
24. Zhu J, Kapoor A, Sridhar VV et al. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr. Biol. 17, 54-59 (2007).
25. Cortazar D, Kunz C, Saito Y et al. The enigmatic thymine DNA glycosylase. DNA Repair (Amst.) 6, 489-504 (2007).
26. Neddermann P, Gallinari P, Lettieri T et al. Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 271, 12767-12774 (1996).
27. Neddermann P, Jiricny J. The purification of a mismatch-specific thymine-DNA glycosylase from HeLa cells. J. Biol. Chem. 268, 21218-21224 (1993).
28. Neddermann P, Jiricny J. Efficient removal of uracil from G. U mispairs by the mismatchspecific thymine DNA glycosylase from HeLa cells. Proc. Natl Acad. Sci. USA 91, 1642-1646 (1994).
29. Bellacosa A. Role of MED1 (MBD4) gene in DNA repair and human cancer. J. Cell. Physiol. 187, 137-144 (2001).
30. Bellacosa A, Cicchillitti L, Schepis F et al. MED1, a novel human methyl-CpG-binding endonuclease, interacts with DNA mismatch repair protein MLH1. Proc. Natl Acad. Sci. USA 96, 3969-3974 (1999).
31. Hendrich B, Hardeland U, Ng HH et al. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401, 301-304 (1999).
32. Petronzelli F, Riccio A, Markham GD et al. Biphasic kinetics of the human DNA repair protein MED1(MBD4), a mismatch-specific DNA N-glycosylase. J. Biol. Chem. 275, 32422-32429 (2000).
33. Um S, Harbers M, Benecke A et al. Retinoic acid receptors interact physically and functionally with the T:G mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 273, 20728-20736 (1998).
34. Chen D, Lucey MJ, Phoenix F et al. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor a. J. Biol. Chem. 278, 38586-38592 (2003).
35. Chevray PM, Nathans D. Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl Acad. Sci. USA 89, 5789-5793 (1992).
36. Missero C, Pirro MT, Simeone S et al. The DNA glycosylase T:G mismatch-specific thymine DNA glycosylase represses thyroid transcription factor-1-activated transcription. J. Biol. Chem. 276, 33569-33575 (2001).
37. Tini M, Benecke A, Um SJ et al. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell. 9, 265-277 (2002).
38. Lucey MJ, Chen D, Lopez-Garcia J et al. T:G mismatch-specific thymine-DNA glycosylase (TDG) as a coregulator of transcription interacts with SRC1 family members through a novel tyrosine repeat motif. Nucleic Acids Res. 33, 6393-6404 (2005).
39. Jost JP, Siegmann M, Sun L et al. Mechanisms of DNA demethylation in chicken embryos. Purification and properties of a 5-methylcytosine-DNA glycosylase. J. Biol. Chem. 270, 9734-9739 (1995).
40. Zhu B, Benjamin D, Zheng Y et al. Overexpression of 5-methylcytosine DNA glycosylase in human embryonic kidney cells EcR293 demethylates the promoter of a hormone-regulated reporter gene. Proc. Natl Acad. Sci. USA 98, 5031-5036 (2001).
41. Zhu B, Zheng Y, Hess D 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 97, 5135-5139 (2000).
42. Kangaspeska S, Stride B, Metivier R et al. Transient cyclical methylation of promoter DNA. Nature 452, 112-115 (2008).
43. Metivier R, Gallais R, Tiffoche C et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45-50 (2008).
44. Li YQ, Zhou PZ, Zheng XD et al. Association of Dnmt3a and thymine DNA glycosylase links DNA methylation with base-excision repair. Nucleic Acids Res. 35, 390-400 (2007).
45. Boland MJ, Christman JK. Characterization of Dnmt3b:thymine-DNA glycosylase interaction and stimulation of thymine glycosylase-mediated repair by DNA methyltransferase (s) and RNA. J. Mol. Biol. 379, 492-504 (2008).
46. Cortazar D, Kunz C, Selfridge J et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 470, 419-423 (2011). □□ Describes the requirement of TDG for development and its role in maintaining proper DNA methylation patterns and chromatin modification; describes the role of TDG in protecting from epigenetic aberrations upon cell lineage commitment and differentiation.
47. Cortellino S, Xu J, Sannai M et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79 (2011). □□ Describes the requirement of TDG for development and its role in maintaining proper DNA methylation patterns and chromatin modification; describes the requirement of TDG glycosylase activity for development and DNA demethylation; describes activity of TDG on 5-hydroxymethyluracil (5hmU).
48. Saito Y, Ono T, Takeda N et al. Embryonic lethality in mice lacking mismatch-specific thymine DNA glycosylase is partially prevented by DOPS, a precursor of noradrenaline. Tohoku J. Exp. Med. 226, 75-83 (2012). □□ Describes the requirement of TDG for development and its role in catecholamine biosynthesis.
49. Mark M, Ghyselinck NB, Chambon P. Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46, 451-480 (2006).
50. Tanaka Y, Naruse I, Hongo T et al. Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech. Dev. 95, 133-145 (2000).
51. Vermot J, Niederreither K, Garnier JM et al. Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc. Natl Acad. Sci. USA 100, 1763-1768 (2003).
52. Yao TP, Oh SP, Fuchs M et al. Gene dosagedependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 93, 361-372 (1998).
53. Lim KC, Lakshmanan G, Crawford SE et al. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 25, 209-212 (2000).
54. Thomas SA, Matsumoto AM, Palmiter RD. Noradrenaline is essential for mouse fetal development. Nature 374, 643-646 (1995).
55. Zhou QY, Quaife CJ, Palmiter RD. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640-643 (1995).
56. Kobayashi K, Morita S, Sawada H et al. Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice. J. Biol. Chem. 270, 27235-27243 (1995).
57. Hardeland U, Bentele M, Jiricny J et al. Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis. J. Biol. Chem. 275, 33449-33456 (2000).
58. Ito S, D'alessio AC, Taranova OV et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133 (2010). □□ Describes the role of Tet proteins in conversion of 5-methylcytosine to 5-hydroxymethylcytosine.
59. Tahiliani M, Koh KP, Shen Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009). □□ Describes the role of Tet proteins in conversion of 5-methylcytosine to 5-hydroxymethylcytosine.
60. Ono R, Taki T, Taketani T et al. 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. 62, 4075-4080 (2002).
61. Lorsbach RB, Moore J, Mathew S et al. TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t (10;11) (q22;q23). Leukemia 17, 637-641 (2003).
62. Bejar R, Levine R, Ebert BL. Unraveling the molecular pathophysiology of myelodysplastic syndromes. J. Clin. Oncol. 29, 504-515 (2011).
63. Bennett MT, Rodgers MT, Hebert AS et al. Specificity of human thymine DNA glycosylase depends on N-glycosidic bond stability. J. Am. Chem. Soc. 128, 12510-12519 (2006). □ Describes the activity of TDG on various substrates including 5hmU.
64. Hardeland U, Bentele M, Jiricny J et al. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res. 31, 2261-2271 (2003). □ Describes the activity of TDG on various substrates including 5hmU.
65. He YF, Li BZ, Li Z et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307 (2011). □□ Describes the production of 5-carboxylcytosine (5caC) by Tet proteins and activity of TDG on 5caC.
66. Ito S, Shen L, Dai Q et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303 (2011). □□ Describes the production of 5-formylcytosine (5fC) and 5caC by Tet proteins.
67. Pfaffeneder T, Hackner B, Truss M et al. The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. Int. Ed. Engl. 50, 7008-7012 (2011).
68. Maiti A, Drohat AC. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 286, 35334-35338 (2011). □ Describes the activity of TDG on 5fC and 5caC.
69. Zhang L, Lu X, Lu J et al. Thymine DNA glycosylase specifically recognizes 5-carboxylcytosine-modified DNA. Nat. Chem. Biol. 8, 328-330 (2012). □ Describes the structural basis of activity of TDG on 5fC and 5caC.
70. Kim MS, Kondo T, Takada I et al. DNA demethylation in hormone-induced transcriptional derepression. Nature 461, 1007-1012 (2009).
71. Peng B, Hurt EM, Hodge DR et al. DNA hypermethylation and partial gene silencing of human thymine-DNA glycosylase in multiple myeloma cell lines. Epigenetics 1, 138-145 (2006).
72. Yatsuoka T, Furukawa T, Abe T et al. Genomic analysis of the thymine-DNA glycosylase (TDG) gene on 12q22-q24.1 in human pancreatic ductal adenocarcinoma. Int. J. Pancreatol. 25, 97-102 (1999).
73. Vasovcak P, Krepelova A, Menigatti M et al. Unique mutational profile associated with a loss of TDG expression in the rectal cancer of a patient with a constitutional PMS2 deficiency. DNA Repair 11(7), 616-623 (2012).
74. Thillainadesan G, Chitilian JM, Isovic M et al. TGF-b-dependent active demethylation and expression of the p15 (ink4b) tumor suppressor are impaired by the ZNF217/CoREST complex. Mol. Cell 46(5), 636-649 (2012).