5-Hydroxymethylcytosine: Generation, fate, and genomic distribution

Current Opinion in Cell Biology

Volumn 25, Issue 3, 2013, Pages 289-296

  Shen, Li ^a,b,c   Zhang, Yi ^a,b,c,d,e  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b Program in Cellular and Molecular Medicine   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; DNA METHYLTRANSFERASE 1; GENOMIC DNA;

DEMETHYLATION; DNA MODIFICATION; DNA REPLICATION; DNA SYNTHESIS; EUCHROMATIN; EXCISION REPAIR; HETEROCHROMATIN; HUMAN; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE DISTRIBUTION;

5-METHYLCYTOSINE; ANIMALS; CYTOSINE; DIOXYGENASES; DNA METHYLATION; EPIGENESIS, GENETIC; GENOME; GENOME-WIDE ASSOCIATION STUDY; HUMANS;

MAMMALIA;

EID: 84879235514     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.02.017     Document Type: Review

References (59)

1. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
2. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., Agarwal S., Iyer L.M., Liu D.R., Aravind L., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
3. 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, 466:1129-1133.
4. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., Ding J., Jia Y., Chen Z., Li L., et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
5. 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.
6. 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 2011, 286:35334-35338.
7. 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.
8. Yildirim O., Li R., Hung J.H., Chen P.B., Dong X., Ee L.S., Weng Z., Rando O.J., Fazzio T.G. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 2011, 147:1498-1510.
9. Ficz G., Branco M.R., Seisenberger S., Santos F., Krueger F., Hore T.A., Marques C.J., Andrews S., Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473:398-402.
10. Jin S.G., Wu X., Li A.X., Pfeifer G.P. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res 2011, 39:5015-5024.
11. Pastor W.A., Pape U.J., Huang Y., Henderson H.R., Lister R., Ko M., McLoughlin E.M., Brudno Y., Mahapatra S., Kapranov P., et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011, 473:394-397.
12. Robertson A.B., Dahl J.A., Vagbo C.B., Tripathi P., Krokan H.E., Klungland A. A novel method for the efficient and selective identification of 5-hydroxymethylcytosine in genomic DNA. Nucleic Acids Res 2011, 39:e55.
13. Song C.X., Szulwach K.E., Fu Y., Dai Q., Yi C., Li X., Li Y., Chen C.H., Zhang W., Jian X., et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 2011, 29:68-72.
14. Stroud H., Feng S., Morey Kinney S., Pradhan S., Jacobsen S.E. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 2011, 12:R54.
15. Szulwach K.E., Li X., Li Y., Song C.X., Han J.W., Kim S., Namburi S., Hermetz K., Kim J.J., Rudd M.K., et al. Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet 2011, 7:e1002154.
16. Szulwach K.E., Li X., Li Y., Song C.X., Wu H., Dai Q., Irier H., Upadhyay A.K., Gearing M., Levey A.I., et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 2011, 14:1607-1616.
17. Wang T., Pan Q., Lin L., Szulwach K.E., Song C.X., He C., Wu H., Warren S.T., Jin P., Duan R., et al. Genome-wide DNA hydroxymethylation changes are associated with neurodevelopmental genes in the developing human cerebellum. Hum Mol Genet 2012, 21:5500-5510.
18. 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.
19. Wu H., D'Alessio A.C., Ito S., Wang Z., Cui K., Zhao K., Sun Y.E., Zhang Y. 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.
20. Xu Y., Wu F., Tan L., Kong L., Xiong L., Deng J., Barbera A.J., Zheng L., Zhang H., Huang S., et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 2011, 42:451-464.
21. Booth M.J., Branco M.R., Ficz G., Oxley D., Krueger F., Reik W., Balasubramanian S. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 2012, 336:934-937.
22. Yu M., Hon G.C., Szulwach K.E., Song C.X., Zhang L., Kim A., Li X., Dai Q., Shen Y., Park B., et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 2012, 149:1368-1380.
23. Wyatt G.R., Cohen S.S. A new pyrimidine base from bacteriophage nucleic acids. Nature 1952, 170:1072-1073.
24. Kornberg A., Zimmerman S.B., Kornberg S.R., Josse J. Enzymatic synthesis of deoxyribonucleic acid. Influence of bacteriophage T2 on the synthetic pathway in host cells. Proc Natl Acad Sci USA 1959, 45:772-785.
25. Shedlovsky A., Brenner S. A chemical basis for the host-induced modification of T-even bacteriophages. Proc Natl Acad Sci USA 1963, 50:300-305.
26. Hattman S., Fukasawa T. Host-induced modification of T-even phages due to defective glucosylation of their DNA. Proc Natl Acad Sci USA 1963, 50:297-300.
27. 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.
28. Kothari R.M., Shankar V. 5-Methylcytosine content in the vertebrate deoxyribonucleic acids: species specificity. J Mol Evol 1976, 7:325-329.
29. Steinberg J.J., Cajigas A., Brownlee M. Enzymatic shot-gun 5'-phosphorylation and 3'-sister phosphate exchange: a two-dimensional thin-layer chromatographic technique to measure DNA deoxynucleotide modification. J Chromatogr 1992, 574:41-55.
30. 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.
31. Iyer L.M., Tahiliani M., Rao A., Aravind L. Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 2009, 8:1698-1710.
32. Iyer L.M., Abhiman S., Aravind L. Natural history of eukaryotic DNA methylation systems. Prog Mol Biol Transl Sci 2011, 101:25-104.
33. Koh K.P., Yabuuchi A., Rao S., Huang Y., Cunniff K., Nardone J., Laiho A., Tahiliani M., Sommer C.A., Mostoslavsky G., 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.
34. Dawlaty M.M., Ganz K., Powell B.E., Hu Y.C., Markoulaki S., Cheng A.W., Gao Q., Kim J., Choi S.W., Page D.C., et al. Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 2011, 9:166-175.
35. Gu T.P., Guo F., Yang H., Wu H.P., Xu G.F., Liu W., Xie Z.G., Shi L., He X., Jin S.G., et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 2011, 477:606-610.
36. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010, 11:607-620.
37. 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.
38. Inoue A., Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 2011, 334:194.
39. 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, 2:241.
40. Cortellino S., Xu J., Sannai M., Moore R., Caretti E., Cigliano A., Le Coz M., Devarajan K., Wessels A., Soprano D., et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146:67-79.
41. Iqbal K., Jin S.G., Pfeifer G.P., Szabo P.E. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 2011, 108:3642-3647.
42. Hashimoto H., Liu Y., Upadhyay A.K., Chang Y., Howerton S.B., Vertino P.M., Zhang X., Cheng X. Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res 2012, 40:4841-4849.
43. 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.
44. Nabel C.S., 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.
45. 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.
46. 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.
47. Chen C.C., Wang K.Y., Shen C.K. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012, 287:33116-33121.
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.
49. Bestor T.H. The DNA methyltransferases of mammals. Hum Mol Genet 2000, 9:2395-2402.
50. Sharif J., Muto M., Takebayashi S., Suetake I., Iwamatsu A., Endo T.A., Shinga J., Mizutani-Koseki Y., Toyoda T., Okamura K., et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
51. Bostick M., Kim J.K., Esteve 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.
52. 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.
53. Wu H., Zhang Y. Tet1 and 5-hydroxymethylation: a genome-wide view in mouse embryonic stem cells. Cell Cycle 2011, 10:2428-2436.
54. Kubiura M., Okano M., Kimura H., Kawamura F., Tada M. Chromosome-wide regulation of euchromatin-specific 5mC to 5hmC conversion in mouse ES cells and female human somatic cells. Chromosome Res 2012.
55. 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.
56. Meissner A., Mikkelsen T.S., Gu H., Wernig M., Hanna J., Sivachenko A., Zhang X., Bernstein B.E., Nusbaum C., Jaffe D.B., et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770.
57. Song C.X., Clark T.A., Lu X.Y., Kislyuk A., Dai Q., Turner S.W., He C., Korlach J. Sensitive and specific single-molecule sequencing of 5-hydroxymethylcytosine. Nat Methods 2012, 9:75-77.
58. Wanunu M., Cohen-Karni D., Johnson R.R., Fields L., Benner J., Peterman N., Zheng Y., Klein M.L., Drndic M. Discrimination of methylcytosine from hydroxymethylcytosine in DNA molecules. J Am Chem Soc 2011, 133:486-492.
59. Wallace E.V., Stoddart D., Heron A.J., Mikhailova E., Maglia G., Donohoe T.J., Bayley H. Identification of epigenetic DNA modifications with a protein nanopore. Chem Commun (Camb) 2010, 46:8195-8197.