5-Hydroxymethylcytosine: A new kid on the epigenetic block?

Molecular Systems Biology

Volumn 7, Issue 1, 2011, Pages

  Matarese, Filomena ^a   Carrillo De Santa Pau, Enrique ^a   Stunnenberg, Hendrik G ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

5 hydroxymethylcytosine; 5 methylcytosine; DNA demethylation; sixth base; Ten Eleven Translocation

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; CYTOSINE; DRUG DERIVATIVE; OXYGENASE;

ANIMAL; ARTICLE; CELL LINE; CHROMATIN; CLUSTER ANALYSIS; DNA METHYLATION; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; HUMAN; MOUSE; PHYSIOLOGY;

5-METHYLCYTOSINE; ANIMALS; CELL LINE; CHROMATIN; CLUSTER ANALYSIS; CYTOSINE; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; MICE; OXYGENASES; TRANSCRIPTION, GENETIC; TRANSLOCATION, GENETIC;

EID: 84858279865     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2011.95     Document Type: Review

References (59)

1. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG, (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538
2. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES, (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326
3. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM, (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463: 1042-1047
4. Boorstein RJ, Chiu LN, Teebor GW, (1989) Phylogenetic evidence of a role for 5-hydroxymethyluracil-DNA glycosylase in the maintenance of 5-methylcytosine in DNA. Nucleic Acids Res 17: 7653-7661
5. Brinkman AB, Simmer F, Ma K, Kaan A, Zhu J, Stunnenberg HG, (2010) Whole-genome DNA methylation profiling using MethylCap-seq. Methods 52: 232-236
6. Butcher LM, Beck S, (2010) AutoMeDIP-seq: a high-throughput, whole genome, DNA methylation assay. Methods 52: 223-231
7. Cannon-Carlson SV, Gokhale H, Teebor GW, (1989) Purification and characterization of 5-hydroxymethyluracil-DNA glycosylase from calf thymus. Its possible role in the maintenance of methylated cytosine residues. J Biol Chem 264: 13306-13312
8. Cannon SV, Cummings A, Teebor GW, (1988) 5-Hydroxymethylcytosine DNA glycosylase activity in mammalian tissue. Biochem Biophys Res Commun 151: 1173-1179
9. Chen PY, Feng S, Joo JW, Jacobsen SE, Pellegrini M, (2011) A comparative analysis of DNA methylation across human embryonic stem cell lines. Genome Biol 12: R62
10. Clark SJ, Harrison J, Paul CL, Frommer M, (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res 22: 2990-2997
11. Cliffe LJ, Kieft R, Southern T, Birkeland SR, Marshall M, Sweeney K, Sabatini R, (2009) JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes. Nucleic Acids Res 37: 1452-1462
12. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE, (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452: 215-219
13. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, Cigliano A, Le Coz M, Devarajan K, Wessels A, Soprano D, Abramowitz LK, Bartolomei MS, Rambow F, Bassi MR, Bruno T, Fanciulli M, Renner C, Klein-Szanto AJ, Matsumoto Y, Kobi D, et al, (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146: 67-79
14. Cross SH, Charlton JA, Nan X, Bird AP, (1994) Purification of CpG islands using a methylated DNA binding column. Nat Genet 6: 236-244
15. Dawlaty MM, Ganz K, Powell BE, Hu YC, Markoulaki S, Cheng AW, Gao Q, Kim J, Choi SW, Page DC, Jaenisch R, (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9: 166-175
16. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, Kosmider O, Le Couedic JP, Robert F, Alberdi A, Lecluse Y, Plo I, Dreyfus FJ, Marzac C, Casadevall N, Lacombe C, Romana SP, Dessen P, Soulier J, Viguie F, et al, (2009) Mutation in TET2 in myeloid cancers. N Engl J Med 360: 2289-2301
17. Down TA, Rakyan VK, Turner DJ, Flicek P, Li H, Kulesha E, Graf S, Johnson N, Herrero J, Tomazou EM, Thorne NP, Backdahl L, Herberth M, Howe KL, Jackson DK, Miretti MM, Marioni JC, Birney E, Hubbard TJ, Durbin R, et al, (2008) A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat Biotechnol 26: 779-785
18. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W, (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473: 398-402
19. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, Li Y, Bhagwat N, Vasanthakumar A, Fernandez HF, Tallman MS, Sun Z, Wolniak K, Peeters JK, Liu W, Choe SE, Fantin VR, Paietta E, Lowenberg B, Licht JD, et al, (2010) Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18: 553-567
20. Gommers-Ampt JH, Teixeira AJ, van de Werken G, van Dijk WJ, Borst P, (1993a) The identification of hydroxymethyluracil in DNA of Trypanosoma brucei. Nucleic Acids Res 21: 2039-2043
21. Gommers-Ampt JH, Van Leeuwen F, de Beer AL, Vliegenthart JF, Dizdaroglu M, Kowalak JA, Crain PF, Borst P, (1993b) beta-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T brucei. Cell 75: 1129-1136
22. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, Iqbal K, Shi YG, Deng Z, Szabo PE, Pfeifer GP, Li J, Xu GL, (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477: 606-610
23. Hayatsu H, Shiragami M, (1979) Reaction of bisulfite with the 5-hydroxymethyl group in pyrimidines and in phage DNAs. Biochemistry 18: 632-637
24. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, Sun Y, Li X, Dai Q, Song CX, Zhang K, He C, Xu GL, (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307
25. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A, (2010) The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One 5: e8888
26. Inoue A, Zhang Y, (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334: 194
27. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y, (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466: 1129-1133
28. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y, (2011) Tet Proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303
29. Jin SG, Kadam S, Pfeifer GP, (2010) Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res 38: e125
30. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, Liu XS, Aravind L, Agarwal S, Maciejewski JP, Rao A, (2010) Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 468: 839-843
31. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, Lahesmaa R, Orkin SH, Rodig SJ, Daley GQ, Rao A, (2011) Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8: 200-213
32. Kriaucionis S, Heintz N, (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930
33. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE, (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: e1000242
34. Langemeijer SM, Kuiper RP, Berends M, Knops R, Aslanyan MG, Massop M, Stevens-Linders E, van Hoogen P, van Kessel AG, Raymakers RA, Kamping EJ, Verhoef GE, Verburgh E, Hagemeijer A, Vandenberghe P, de Witte T, van der Reijden BA, Jansen JH, (2009) Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet 41: 838-842
35. Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong CT, Low HM, Kin Sung KW, Rigoutsos I, Loring J, Wei CL, (2010) Dynamic changes in the human methylome during differentiation. Genome Res 20: 320-331
36. Levasseur DN, Wang J, Dorschner MO, Stamatoyannopoulos JA, Orkin SH, (2008) Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes Dev 22: 954
37. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR, (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322
38. Lorsbach RB, Moore J, Mathew S, Raimondi SC, Mukatira ST, Downing JR, (2003) 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
39. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G, (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452: 45-50
40. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, et al, (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560
41. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C, Figueroa ME, Vasanthakumar A, Patel J, Zhao X, Perna F, Pandey S, Madzo J, Song C, Dai Q, He C, Ibrahim S, Beran M, Zavadil J, Nimer SD, et al, (2011) Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20: 11-24
42. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M, Tanaka S, Shiota K, Nakano T, (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9: 64-71
43. Nan X, Meehan RR, Bird A, (1993) Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res 21: 4886-4892
44. Nestor C, Ruzov A, Meehan R, Dunican D, (2010) Enzymatic approaches and bisulfite sequencing cannot distinguish between 5-methylcytosine and 5-hydroxymethylcytosine in DNA. Biotechniques 48: 317-319
45. Ono R, Taki T, Taketani T, Taniwaki M, Kobayashi H, Hayashi Y, (2002) 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
46. Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J, (2000) Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10: 475-478
47. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, McLoughlin EM, Brudno Y, Mahapatra S, Kapranov P, Tahiliani M, Daley GQ, Liu XS, Ecker JR, Milos PM, Agarwal S, Rao A, (2011) Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473: 394-397
48. Quivoron C, Couronne L, Della Valle V, Lopez CK, Plo I, Wagner-Ballon O, Do Cruzeiro M, Delhommeau F, Arnulf B, Stern MH, Godley L, Opolon P, Tilly H, Solary E, Duffourd Y, Dessen P, Merle-Beral H, Nguyen-Khac F, Fontenay M, Vainchenker W, et al, (2011) TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20: 25-38
49. Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R, (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci USA 97: 5237-5242
50. Song CX, Szulwach KE, Fu Y, Dai Q, Yi C, Li X, Li Y, Chen CH, Zhang W, Jian X, Wang J, Zhang L, Looney TJ, Zhang B, Godley LA, Hicks LM, Lahn BT, Jin P, He C, (2010) Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 29: 68-72
51. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A, (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935
52. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, Mann M, (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967-980
53. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schubeler D, (2005) Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37: 853-962
54. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, Rappsilber J, Helin K, (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473: 343-348
55. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, Arand J, Nakano T, Reik W, Walter J, (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2: 241
56. Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y, (2011a) Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 25: 679-684
57. Wu H, D'Alessio AC, Ito S, Xia K, Wang Z, Cui K, Zhao K, Eve Sun Y, Zhang Y, (2011b) Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473: 389-393
58. Xu Y, Wu F, Tan L, Kong L, Xiong L, Deng J, Barbera AJ, Zheng L, Zhang H, Huang S, Min J, Nicholson T, Chen T, Xu G, Shi Y, Zhang K, Shi YG, (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42: 451-464
59. Yu Z, Genest PA, ter Riet B, Sweeney K, DiPaolo C, Kieft R, Christodoulou E, Perrakis A, Simmons JM, Hausinger RP, van Luenen HG, Rigden DJ, Sabatini R, Borst P, (2007) The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase. Nucleic Acids Res 35: 2107-2115