Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA

Nature Chemical Biology

Volumn 10, Issue 7, 2014, Pages 574-581

  Pfaffeneder, Toni ^a   Spada, Fabio ^a   Wagner, Mirko ^a   Brandmayr, Caterina ^a   Laube, Silvia K ^a   Eisen, David ^a   Truss, Matthias ^b   Steinbacher, Jessica ^a   Hackner, Benjamin ^a   Kotljarova, Olga ^a   Schuermann, David ^c   Michalakis, Stylianos ^a   Kosmatchev, Olesea ^a   Schiesser, Stefan ^a   Steigenberger, Barbara ^a   Raddaoui, Nada ^a   Kashiwazaki, Gengo ^a   Müller, Udo ^a   Spruijt, Cornelia G ^d   Vermeulen, Michiel ^d,e   Leonhardt, Heinrich ^a   Schär, Primo ^c   Müller, Markus ^a   Carell, Thomas ^a   more..

^a UNIVERSITY OF MUNICH   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d Center for Integrated Protein Science Department of Pharmacy Ludwig Maximilians Universität München ^*  (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLURACIL; CELL DNA; PEPTIDE; PROTEIN DERIVATIVE; PROTEIN TET; PURINE; PYRIMIDINE; THYMINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; EMBRYO; EMBRYONIC STEM CELL; ENZYME SUBSTRATE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; STEADY STATE;

ANIMALS; BASE SEQUENCE; CARBON ISOTOPES; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATOGRAPHY, LIQUID; CYTOSINE; DNA; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE EXPRESSION; MICE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PENTOXYL; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THYMINE; TRANSCRIPTION FACTORS;

EID: 84902831568     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1532     Document Type: Article

References (54)

1. Smith, Z.D. & Meissner, A. DNA methylation: Roles in mammalian development. Nat. Rev. Genet. 14, 204-220 (2013).
2. Franchini, D.M., Schmitz, K.M. & Petersen-Mahrt, S.K. 5-Methylcytosine DNA demethylation: More than losing a methyl group. Annu. Rev. Genet. 46, 419-441 (2012).
3. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
4. Pfaffeneder, T. et al. The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. Int. Ed. Engl. 50, 7008-7012 (2011).
5. Ito, S. et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303 (2011).
6. He, Y.F. et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307 (2011).
7. Tan, L. & Shi, Y.G. Tet family proteins and 5-hydroxymethylcytosine in development and disease. Development 139, 1895-1902 (2012).
8. Maiti, A. & Drohat, A.C. 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).
9. Bjelland, S. et al. Oxidation of thymine to 5-formyluracil in DNA: Mechanisms of formation, structural implications, and base excision by human cell free extracts. Biochemistry 34, 14758-14764 (1995).
10. Mouret, J.F., Polverelli, M., Sarrazini, F. & Cadet, J. Ionic and radical oxidations of DNA by hydrogen peroxide. Chem. Biol. Interact. 77, 187-201 (1991).
11. 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 145, 423-434 (2011).
12. Cortellino, S. et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79 (2011).
13. Nabel, C.S. et al. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 8, 751-758 (2012).
14. Rangam, G., Schmitz, K.M., Cobb, A.J. & Petersen-Mahrt, S.K. AID enzymatic activity is inversely proportional to the size of cytosine C5 orbital cloud. PLoS ONE 7, e43279 (2012).
15. Jacobs, A.L. & Schär, P. DNA glycosylases: In DNA repair and beyond. Chromosoma 121, 1-20 (2012).
16. Zhang, Q.M. et al. DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the hNEIL1 and hNTH1 enzymes in human cells. DNA Repair (Amst.) 4, 71-79 (2005).
17. Burrows, C.J. Surviving an oxygen atmosphere: DNA damage and repair. ACS Symp. Ser. Am. Chem. Soc. 2009, 147-156 (2009).
18. Taghizadeh, K. et al. Quantification of DNA damage products resulting from deamination, oxidation and reaction with products of lipid peroxidation by liquid chromatography isotope dilution tandem mass spectrometry. Nat. Protoc. 3, 1287-1298 (2008).
19. Globisch, D. et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS ONE 5, e15367 (2010).
20. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930 (2009).
21. Münzel, M. et al. Quantification of the sixth DNA base hydroxymethylcytosine in the brain. Angew. Chem. Int. Ed. Engl. 49, 5375-5377 (2010).
22. Liu, S. et al. Quantitative assessment of Tet-induced oxidation products of 5-methylcytosine in cellular and tissue DNA. Nucleic Acids Res. 41, 6421-6429 (2013).
23. Ficz, G. et al. FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 13, 351-359 (2013).
24. Habibi, E. et al. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13, 360-369 (2013).
25. Leitch, H.G. et al. Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20, 311-316 (2013).
26. 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 146, 519-532 (2011).
27. Ying, Q.L., Stavridis, M., Griffiths, D., Li, M. & Smith, A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186 (2003).
28. Iurlaro, M. et al. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol. 14, R119 (2013).
29. Spruijt, C.G. et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152, 1146-1159 (2013).
30. Burley, G.A. et al. Directed DNA metallization. J. Am. Chem. Soc. 128, 1398-1399 (2006).
31. Rostovtsev, V.V., Green, L.G., Fokin, V.V. & Sharpless, K.B. A stepwise huisgen cycloaddition process: Copper(i)-catalyzed regioselective "ligation" of azides and terminal alkynes. Angew. Chem. Int. Ed. 41, 2596-2599 (2002).
32. Thompson, A. et al. Tandem mass tags: A novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 75, 1895-1904 (2003); erratum 75, 4942 (2003); erratum 78, 4235 (2006).
33. Gygi, S.P. et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994-999 (1999).
34. Frauer, C. et al. Recognition of 5-hydroxymethylcytosine by the Uhrf1 SRA domain. PLoS ONE 6, e21306 (2011).
35. Pichler, G. et al. Cooperative DNA and histone binding by Uhrf2 links the two major repressive epigenetic pathways. J. Cell. Biochem. 112, 2585-2593 (2011).
36. Lewis, H.L., Muhleman, D.R. & Ward, J.F. Serologic assay of DNA base damage. I. 5-Hydroxymethyldeoxyuridine, a radiation product of thymidine. Radiat. Res. 75, 305-316 (1978).
37. Boorstein, R.J. et al. Definitive identification of mammalian 5-hydroxymethyluracil DNA N-glycosylase activity as SMUG1. J. Biol. Chem. 276, 41991-41997 (2001).
38. Kavli, B., Otterlei, M., Slupphaug, G. & Krokan, H.E. Uracil in DNA-general mutagen, but normal intermediate in acquired immunity. DNA Repair (Amst.) 6, 505-516 (2007).
39. Santos, F. et al. Active demethylation in mouse zygotes involves cytosine deamination and base excision repair. Epigenetics Chromatin 6, 39 (2013).
40. Silva, J. & Smith, A. Capturing pluripotency. Cell 132, 532-536 (2008).
41. Moore, S.P.G., Toomire, K.J. & Strauss, P.R. DNA modifications repaired by base excision repair are epigenetic. DNA Repair (Amst.) 12, 1152-1158 (2013).
42. Schiesser, S. et al. Deamination, oxidation, and C-C bond cleavage reactivity of 5-hydroxymethylcytosine, 5-formylcytosine, and 5-carboxycytosine. J. Am. Chem. Soc. 135, 14593-14599 (2013).
43. Gierlich, J. et al. Click chemistry as a reliable method for the high-density postsynthetic functionalization of alkyne-modified DNA. Org. Lett. 8, 3639-3642 (2006).
44. Cao, H. & Wang, Y. Collisionally activated dissociation of protonated 2'-deoxycytidine, 2'-deoxyuridine, and their oxidatively damaged derivatives. J. Am. Soc. Mass Spectrom. 17, 1335-1341 (2006).
45. Wang, J. et al. Quantification of oxidative DNA lesions in tissues of Long-Evans Cinnamon rats by capillary high-performance liquid chromatography-Tandem mass spectrometry coupled with stable isotope-dilution method. Anal. Chem. 83, 2201-2209 (2011).
46. Chen, T., Ueda, Y., Dodge, J.E., Wang, Z. & Li, E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23, 5594-5605 (2003).
47. Cortazar, D. et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 470, 419-423 (2011).
48. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. & Roder, J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428 (1993).
49. Li, E., Bestor, T.H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
50. Montanez, E. et al. Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 22, 1325-1330 (2008).
51. Ying, Q.L. & Smith, A.G. Defined conditions for neural commitment and differentiation. Methods Enzymol. 365, 327-341 (2003).
52. Williams, K. et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473, 343-348 (2011).
53. Kittler, R., Heninger, A.K., Franke, K., Habermann, B. & Buchholz, F. Production of endoribonuclease-prepared short interfering RNAs for gene silencing in mammalian cells. Nat. Methods 2, 779-784 (2005).
54. Yu, M. et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149, 1368-1380 (2012).