5-hydroxymethylcytosine: A new insight into epigenetics in cancer

Cancer Biology and Therapy

Volumn 15, Issue 1, 2014, Pages 10-15

  Ye, Chao ^a   Li, Lanjuan ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

5 hmC; Cancer; DNA methylation; Epigenetics; TET

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE;

ARTICLE; BRAIN TUMOR; CANCER FAMILY; EPIGENETICS; GENOME; HUMAN; NEOPLASM; SOLID TUMOR;

5-HMC; CANCER; DNA METHYLATION; EPIGENETICS; TET;

5-METHYLCYTOSINE; ANIMALS; BRAIN NEOPLASMS; CYTOSINE; DIOXYGENASES; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HUMANS; LEUKEMIA; NEOPLASMS; PROTO-ONCOGENE PROTEINS;

EID: 84988375135     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.27144     Document Type: Article

References (67)

1. Lim DH, Maher ER. Genomic imprinting syndromes and cancer. Adv Genet 2010; 70:145-75; PMID:20920748; http://dx.doi.org/10.1016/B978-0-12-380866-0. 60006-X
2. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683-92; PMID:17320506; http://dx.doi.org/10.1016/j.cell.2007.01.029 (Pubitemid 46273572)
3. Grønbaek K, Hother C, Jones PA. Epigenetic changes in cancer. APMIS 2007; 115:1039-59; PMID:18042143; http://dx.doi.org/10.1111/j.1600-0463. 2007.apm-636.xml.x (Pubitemid 350179474)
4. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009; 324:929-30; PMID:19372393; http://dx.doi.org/10.1126/science.1169786
5. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324:930-5; PMID:19372391; http://dx.doi.org/10.1126/science.1170116
6. Wyatt GR, Cohen SS. A new pyrimidine base from bacteriophage nucleic acids. Nature 1952; 170:1072-3; PMID:13013321; http://dx.doi.org/10.1038/ 1701072a0
7. Penn NW, Suwalski R, O'Riley C, Bojanowski K, Yura R. The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochem J 1972; 126:781-90; PMID:4538516
8. Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 2011; 25:679-84; PMID:21460036; http://dx.doi.org/10.1101/gad.2036011
9. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, McLoughlin EM, Brudno Y, Mahapatra S, Kapranov P, et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011; 473:394-7; PMID:21552279; http://dx.doi.org/10.1038/nature10102
10. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473:398-402; PMID:21460836; http://dx.doi.org/10.1038/nature10008
11. Stroud H, Feng S, Morey Kinney S, Pradhan S, Jacobsen SE. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 2011; 12:R54; PMID:21689397; http://dx.doi.org/10.1186/gb-2011-12-6-r54
12. Globisch D, Münzel M, Müller M, Michalakis S, Wagner M, Koch S, Brückl T, Biel M, Carell T. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 2010; 5:e15367; PMID:21203455; http://dx.doi.org/10.1371/journal.pone.0015367
13. Song CX, Szulwach KE, Fu Y, Dai Q, Yi C, Li X, Li Y, Chen CH, Zhang W, Jian X, et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 2011; 29:68-72; PMID:21151123; http://dx.doi.org/10.1038/nbt.1732
14. Li W, Liu M. Distribution of 5-hydroxymethylcytosine in different human tissues. J Nucleic Acids 2011; 2011:870726; PMID:21772996; http://dx.doi.org/10. 4061/2011/870726
15. Nestor CE, Ottaviano R, Reddington J, Sproul D, Reinhardt D, Dunican D, Katz E, Dixon JM, Harrison DJ, Meehan RR. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res 2012; 22:467-77; PMID:22106369; http://dx.doi.org/10.1101/gr.126417.111
16. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010; 466:1129-33; PMID:20639862; http://dx.doi.org/10. 1038/nature09303
17. Thalhammer A, Hansen AS, El-Sagheer AH, Brown T, Schofield CJ. Hydroxylation of methylated CpG dinucleotides reverses stabilisation of DNA duplexes by cytosine 5-methylation. Chem Commun (Camb) 2011; 47:5325-7; PMID:21451870; http://dx.doi.org/10.1039/c0cc05671e
18. Rougier N, Bourc'his D, Gomes DM, Niveleau A, Plachot M, Pàldi A, Viegas-Péquignot E. Chromosome methylation patterns during mammalian preimplantation development. Genes Dev 1998; 12:2108-13; PMID:9679055; http://dx.doi.org/10.1101/gad.12.14.2108 (Pubitemid 28348034)
19. Valinluck V, Sowers LC. Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res 2007; 67:946-50; PMID:17283125; http://dx.doi.org/10.1158/0008-5472.CAN-06-3123
20. Cannon SV, Cummings A, Teebor GW. 5-Hydroxymethylcytosine DNA glycosylase activity in mammalian tissue. Biochem Biophys Res Commun 1988; 151:1173-9; PMID:3355548; http://dx.doi.org/10.1016/S0006-291X(88)80489-3 (Pubitemid 18095244)
21. Zhang P, Su L, Wang Z, Zhang S, Guan J, Chen Y, Yin Y, Gao F, Tang B, Li Z. The involvement of 5-hydroxymethylcytosine in active DNA demethylation in mice. Biol Reprod 2012; 86:104; PMID:22262693; http://dx.doi.org/10.1095/ biolreprod.111.096073
22. Jin SG, Kadam S, Pfeifer GP. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res 2010; 38:e125; PMID:20371518; http://dx.doi.org/10.1093/nar/gkq223
23. Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC. 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; 32:4100-8; PMID:15302911; http://dx.doi.org/10.1093/nar/gkh739 (Pubitemid 39232282)
24. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16:6-21; PMID:11782440; http://dx.doi.org/10.1101/gad.947102 (Pubitemid 34049633)
25. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009; 10:295-304; PMID:19308066; http://dx.doi.org/10.1038/nrg2540
26. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008; 9:465-76; PMID:18463664; http://dx.doi.org/10. 1038/nrg2341 (Pubitemid 351693975)
27. Privat E, Sowers LC. Photochemical deamination and demethylation of 5-methylcytosine. Chem Res Toxicol 1996; 9:745-50; PMID:8831819; http://dx.doi.org/10.1021/tx950182o (Pubitemid 26181625)
28. Adams TB, Hallagan JB, Putnam JM, Gierke TL, Doull J, Munro IC, Newberne P, Portoghese PS, Smith RL, Wagner BM, et al. The FEMA GRAS assessment of alicyclic substances used as flavour ingredients. Food Chem Toxicol 1996; 34:763-828; PMID:8972877; http://dx.doi.org/10.1016/S0278-6915(96)00051-8 (Pubitemid 26420126)
29. Xu Y, Wu F, Tan L, Kong L, Xiong L, Deng J, Barbera AJ, 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; 42:451-64; PMID:21514197; http://dx.doi.org/10.1016/j.molcel.2011.04.005
30. Iyer LM, 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; 8:1698-710; PMID:19411852; http://dx.doi.org/10. 4161/cc.8.11.8580
31. Loenarz C, Schofield CJ. Oxygenase catalyzed 5-methylcytosine hydroxylation. Chem Biol 2009; 16:580-3; PMID:19549596; http://dx.doi.org/10. 1016/j.chembiol.2009.06.002
32. Long HK, Blackledge NP, Klose RJ. ZF-CxxC domain-containing proteins, CpG islands and the chromatin connection. Biochem Soc Trans 2013; 41:727-40; PMID:23697932; http://dx.doi.org/10.1042/BST20130028
33. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8:200-13; PMID:21295276; http://dx.doi.org/10.1016/j.stem.2011.01.008
34. Dawlaty MM, Ganz K, Powell BE, Hu YC, Markoulaki S, Cheng AW, Gao Q, Kim J, Choi SW, Page DC, 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; PMID:21816367; http://dx.doi.org/10.1016/j.stem.2011.07.010
35. Ko M, Bandukwala HS, An J, Lamperti ED, Thompson EC, Hastie R, Tsangaratou A, Rajewsky K, Koralov SB, Rao A. Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc Natl Acad Sci U S A 2011; 108:14566-71; PMID:21873190; http://dx.doi.org/10.1073/pnas.1112317108
36. Lorsbach RB, Moore J, Mathew S, Raimondi SC, Mukatira ST, Downing JR. TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;q23). Leukemia 2003; 17:637-41; PMID:12646957; http://dx.doi.org/10.1038/sj.leu.2402834 (Pubitemid 36395661)
37. Langemeijer SM, Aslanyan MG, Jansen JH. TET proteins in malignant hematopoiesis. Cell Cycle 2009; 8:4044-8; PMID:19923888; http://dx.doi.org/10. 4161/cc.8.24.10239
38. Ko M, An J, Bandukwala HS, Chavez L, Aijö T, Pastor WA, Segal MF, Li H, Koh KP, Lähdesmäki H, et al. Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX. Nature 2013; 497:122-6; PMID:23563267; http://dx.doi.org/10.1038/nature12052
39. Xu Y, Xu C, Kato A, Tempel W, Abreu JG, Bian C, Hu Y, Hu D, Zhao B, Cerovina T, et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 2012; 151:1200-13; PMID:23217707; http://dx.doi.org/10.1016/j. cell.2012.11.014
40. Deplus R, Delatte B, Schwinn MK, Defrance M, Méndez J, Murphy N, Dawson MA, Volkmar M, Putmans P, Calonne E, et al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J 2013; 32:645-55; PMID:23353889; http://dx.doi.org/10.1038/emboj.2012.357
41. Chen Q, Chen Y, Bian C, Fujiki R, Yu X. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 2013; 493:561-4; PMID:23222540; http://dx.doi.org/10.1038/nature11742
42. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301:89-92; PMID:6185846; http://dx.doi.org/10.1038/301089a0 (Pubitemid 13154475)
43. Gama-Sosa MA, Slagel VA, Trewyn RW, Oxenhandler R, Kuo KC, Gehrke CW, Ehrlich M. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res 1983; 11:6883-94; PMID:6314264; http://dx.doi.org/10.1093/nar/11.19.6883
44. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3:415-28; PMID:12042769 (Pubitemid 34587077)
45. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349:2042-54; PMID:14627790; http://dx.doi.org/10.1056/NEJMra023075 (Pubitemid 37448928)
46. Ushijima T. Detection and interpretation of altered methylation patterns in cancer cells. Nat Rev Cancer 2005; 5:223-31; PMID:15719030; http://dx.doi.org/10.1038/nrc1571 (Pubitemid 40314953)
47. Sun L, Hui AM, Kanai Y, Sakamoto M, Hirohashi S. Increased DNA methyltransferase expression is associated with an early stage of human hepatocarcinogenesis. Jpn J Cancer Res 1997; 88:1165-70; PMID:9473734; http://dx.doi.org/10.1111/j.1349-7006.1997.tb00345.x (Pubitemid 28048263)
48. Peng DF, Kanai Y, Sawada M, Ushijima S, Hiraoka N, Kosuge T, Hirohashi S. Increased DNA methyltransferase 1 (DNMT1) protein expression in precancerous conditions and ductal carcinomas of the pancreas. Cancer Sci 2005; 96:403-8; PMID:16053511; http://dx.doi.org/10.1111/j.1349-7006.2005.00071.x (Pubitemid 41179741)
49. Nakagawa T, Kanai Y, Saito Y, Kitamura T, Kakizoe T, Hirohashi S. Increased DNA methyltransferase 1 protein expression in human transitional cell carcinoma of the bladder. J Urol 2003; 170:2463-6; PMID:14634451; http://dx.doi.org/10.1097/01. ju.0000095919.50869.c9 (Pubitemid 37414035)
50. Lian CG, Xu Y, Ceol C, Wu F, Larson A, Dresser K, Xu W, Tan L, Hu Y, Zhan Q, et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell 2012; 150:1135-46; PMID:22980977; http://dx.doi.org/10.1016/j. cell.2012.07.033
51. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, Li Y, Bhagwat N, Vasanthakumar A, Fernandez HF, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010; 18:553-67; PMID:21130701; http://dx.doi.org/10.1016/j. ccr.2010.11.015
52. Minor EA, Court BL, Young JI, Wang G. Ascorbate induces ten-eleven translocation (Tet) methylcytosine dioxygenase-mediated generation of 5-hydroxymethylcytosine. J Biol Chem 2013; 288:13669-74; PMID:23548903; http://dx.doi.org/10.1074/jbc.C113.464800
53. Ono R, Taki T, Taketani T, Taniwaki M, Kobayashi H, Hayashi Y. 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 2002; 62:4075-80; PMID:12124344 (Pubitemid 34791077)
54. Abdel-Wahab O, Mullally A, Hedvat C, Garcia-Manero G, Patel J, Wadleigh M, Malinge S, Yao J, Kilpivaara O, Bhat R, et al. Genetic characterization of TET1, TET2, and TET3 alterations in myeloid malignancies. Blood 2009; 114:144-7; PMID:19420352; http://dx.doi.org/10.1182/blood-2009-03-210039
55. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 2010; 468:839-43; PMID:21057493; http://dx.doi.org/10.1038/nature09586
56. Pronier E, Almire C, Mokrani H, Vasanthakumar A, Simon A, da Costa Reis Monte Mor B, Massé A, Le Couédic JP, Pendino F, Carbonne B, et al. Inhibition of TET2-mediated conversion of 5-methylcytosine to 5-hydroxymethylcytosine disturbs erythroid and granulomonocytic differentiation of human hematopoietic progenitors. Blood 2011; 118:2551-5; PMID:21734233; http://dx.doi.org/10.1182/blood-2010-12-324707
57. Albano F, Anelli L, Zagaria A, Coccaro N, Minervini A, Rossi AR, Specchia G. Decreased TET2 gene expression during chronic myeloid leukemia progression. Leuk Res 2011; 35:e220-2; PMID:21794915; http://dx.doi.org/10.1016/j. leukres.2011.07.013
58. Pérez C, Martínez-Calle N, Martín-Subero JI, Segura V, Delabesse E, Fernandez-Mercado M, Garate L, Alvarez S, Rifon J, Varea S, et al. TET2 mutations are associated with specific 5-methylcytosine and 5-hydroxymethylcytosine profiles in patients with chronic myelomonocytic leukemia. PLoS One 2012; 7:e31605; PMID:22328940; http://dx.doi.org/10.1371/ journal.pone.0031605
59. Mancini M, Veljkovic N, Leo E, Aluigi M, Borsi E, Galloni C, Iacobucci I, Barbieri E, Santucci MA. Cytoplasmatic compartmentalization by Bcr-Abl promotes TET2 loss-of-function in chronic myeloid leukemia. J Cell Biochem 2012; 113:2765-74; PMID:22467095; http://dx.doi.org/10.1002/jcb.24154
60. Li Z, Cai X, Cai CL, Wang J, Zhang W, Petersen BE, Yang FC, Xu M. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 2011; 118:4509-18; PMID:21803851; http://dx.doi.org/10.1182/blood-2010-12-325241
61. Orr BA, Haffner MC, Nelson WG, Yegnasubramanian S, Eberhart CG. Decreased 5-hydroxymethylcytosine is associated with neural progenitor phenotype in normal brain and shorter survival in malignant glioma. PLoS One 2012; 7:e41036; PMID:22829908; http://dx.doi.org/10.1371/journal.pone.0041036
62. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, Schackert G, Krex D, Lu Q, Pfeifer GP. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res 2011; 71:7360-5; PMID:22052461; http://dx.doi.org/10.1158/0008-5472.CAN-11-2023
63. Shih AH, Levine RL. IDH1 mutations disrupt blood, brain, and barriers. Cancer Cell 2012; 22:285-7; PMID:22975371; http://dx.doi.org/10.1016/j. ccr.2012.08.022
64. Kraus TF, Globisch D, Wagner M, Eigenbrod S, Widmann D, Münzel M, Müller M, Pfaffeneder T, Hackner B, Feiden W, et al. Low values of 5-hydroxymethylcytosine (5hmC), the "sixth base," are associated with anaplasia in human brain tumors. Int J Cancer 2012; 131:1577-90; PMID:22234893; http://dx.doi.org/10.1002/ijc.27429
65. Kudo Y, Tateishi K, Yamamoto K, Yamamoto S, Asaoka Y, Ijichi H, Nagae G, Yoshida H, Aburatani H, Koike K. Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci 2012; 103:670-6; PMID:22320381; http://dx.doi.org/10.1111/j.1349-7006.2012.02213.x
66. Haffner MC, Chaux A, Meeker AK, Esopi DM, Gerber J, Pellakuru LG, Toubaji A, Argani P, Iacobuzio-Donahue C, Nelson WG, et al. Global 5- hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget 2011; 2:627-37; PMID:21896958
67. Tan L, Shi YG. Tet family proteins and 5-hydroxymethylcytosine in development and disease. Development 2012; 139:1895-902; PMID:22569552; http://dx.doi.org/10.1242/dev.070771