Tight correlation of 5-hydroxymethylcytosine and Polycomb marks in health and disease

Cell Cycle

Volumn 12, Issue 12, 2013, Pages 1835-1841

  Haffner, Michael C ^a   Pellakuru, Laxmi G ^b   Ghosh, Susmita ^b   Lotan, Tamara L ^b   Nelson, William G ^a,b   De Marzo, Angelo M ^a,b   Yegnasubramanian, Srinivasan ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 hydroxymethylcytosine; Cancer; Differentiation; DNA methylation; Epigenetics; H3K27me3; Polycomb

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; HISTONE H3; POLYCOMB GROUP PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CORRELATIONAL STUDY; DNA METHYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; PROSTATE EPITHELIUM; REGULATORY MECHANISM; SOLID TUMOR; STEM CELL;

EID: 84879337510     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.25010     Document Type: Article

References (52)

1. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 2007; 447:425-32; PMID:17522676; http://dx.doi.org/10.1038/nature05918 (Pubitemid 46816749)
2. Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358:1148-59; PMID:18337604; http://dx.doi.org/10.1056/NEJMra072067
3. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4:143-53; PMID:14732866; http://dx.doi.org/10.1038/nrc1279 (Pubitemid 38198742)
4. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011; 25:1010-22; PMID:21576262; http://dx.doi.org/10.1101/gad.2037511
5. Wyatt GR, Cohen SS. The bases of the nucleic acids of some bacterial and animal viruses: The occurrence of 5-hydroxymethylcytosine. Biochem J 1953; 55:774-82; PMID:13115372
6. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, 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
7. 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
8. Branco MR, Ficz G, Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 2012; 13:7-13; PMID:22083101
9. 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
10. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, 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
11. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, et al. 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
12. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, 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
13. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, Rappsilber J, et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011; 473:343-8; PMID:21490601; http://dx.doi.org/10.1038/ nature10066
14. Wu H, Zhang Y. Tet1 and 5-hydroxymethylation: A genome-wide view in mouse embryonic stem cells. Cell Cycle 2011; 10:2428-36; PMID:21750410; http://dx.doi.org/10.4161/cc.10.15.16930
15. Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, et al. 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.2036011X
16. Swigut T, Wysocka J. H3K27 demethylases, at long last. Cell 2007; 131:29-32; PMID:17923085; http://dx.doi.org/10.1016/j.cell.2007.09.026 (Pubitemid 47498542)
17. Mills AA. Throwing the cancer switch: Reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 2010; 10:669-82; PMID:20865010; http://dx.doi.org/10.1038/nrc2931
18. Wei Y, Xia W, Zhang Z, Liu J, Wang H, Adsay NV, et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog 2008; 47:701-6; PMID:18176935; http://dx.doi.org/10.1002/mc.20413
19. Chase A, Cross NC. Aberrations of EZH2 in cancer. Clin Cancer Res 2011; 17:2613-8; PMID:21367748; http://dx.doi.org/10.1158/1078-0432.CCR-10-2156
20. Haffner MC, Chaux A, Meeker AK, Esopi DM, Gerber J, Pellakuru LG, 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
21. Pellakuru LG, Iwata T, Gurel B, Schultz D, Hicks J, Bethel C, et al. Global levels of H3K27me3 track with differentiation in vivo and are deregulated by MYC in prostate cancer. Am J Pathol 2012; 181:560-9; PMID:22713676; http://dx.doi.org/10.1016/j.ajpath.2012.04.021
22. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009; 71:241-60; PMID:18808327; ht tp : //d x .doi .org /10.1146 /annur e v.phy s i-ol.010908.163145
23. De Marzo AM, Nelson WG, Bieberich CJ, Yegnasubramanian S. Prostate cancer: New answers prompt new questions regarding cell of origin. Nat Rev Urol 2010; 7:650-2; PMID:21139640; http://dx.doi.org/10.1038/nrurol.2010.188
24. Bello-DeOcampo D, Kleinman HK, Deocampo ND, Webber MM. Laminin-1 and alpha6beta1 integrin regulate acinar morphogenesis of normal and malignant human prostate epithelial cells. Prostate 2001; 46:142-53; PMID:11170142; http://dx.doi.org/10.1002/1097-0045(20010201)46:2<142::AIDPROS1018> 3.0.CO;2-B
25. Webber MM, Bello D, Kleinman HK, Hoffman MP. Acinar differentiation by non-malignant immortalized human prostatic epithelial cells and its loss by malignant cells. Carcinogenesis 1997; 18:1225-31; PMID:9214606; http://dx.doi.org/10.1093/carcin/18.6.1225 (Pubitemid 28132514)
26. Härmä V, Virtanen J, Mäkelä R, Happonen A, Mpindi JP, Knuuttila M, et al. A comprehensive panel of three-dimensional models for studies of prostate cancer growth, invasion and drug responses. PLoS One 2010; 5:e10431; PMID:20454659; http://dx.doi.org/10.1371/journal.pone.0010431
27. Tyson DR, Inokuchi J, Tsunoda T, Lau A, Ornstein DK. Culture requirements of prostatic epithelial cell lines for acinar morphogenesis and lumen formation in vitro: Role of extracellular calcium. Prostate 2007; 67:1601-13; PMID:17705248; http://dx.doi.org/10.1002/pros.20628 (Pubitemid 350036946)
28. Sérandour AA, Avner S, Oger F, Bizot M, Percevault F, Lucchetti-Miganeh C, et al. Dynamic hydroxymethylation of deoxyribonucleic acid marks differentiation-associated enhancers. Nucleic Acids Res 2012; 40:8255-65; PMID:22730288; http://dx.doi.org/10.1093/nar/gks595
29. Bocker MT, Tuorto F, Raddatz G, Musch T, Yang FC, Xu M, et al. Hydroxylation of 5-methylcytosine by TET2 maintains the active state of the mammalian HOXA cluster. Nat Commun 2012; 3:818; PMID:22569366; http://dx.doi.org/10.1038/ncomms1826
30. 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)
31. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004; 10:789-99; PMID:15286780; http://dx.doi.org/10.1038/nm1087 (Pubitemid 39070849)
32. Yang H, Liu Y, Bai F, Zhang JY, Ma SH, Liu J, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene 2013; 32:663-9; PMID:22391558; http://dx.doi.org/10. 1038/onc.2012.67
33. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, Schackert G, et al. 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
34. 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
35. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, 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
36. Lian CG, Xu Y, Ceol C, Wu F, Larson A, Dresser K, 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
37. Cimmino L, Abdel-Wahab O, Levine RL, Aifantis I. TET family proteins and their role in stem cell differentiation and transformation. Cell Stem Cell 2011; 9:193-204; PMID:21885017; http://dx.doi.org/10.1016/j.stem.2011.08.007
38. Abdel-Wahab O, Mullally A, Hedvat C, Garcia-Manero G, Patel J, Wadleigh M, 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
39. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 2011; 20:11-24; PMID:21723200; http://dx.doi.org/10.1016/j.ccr.2011.06.001
40. Hsu CH, Peng KL, Kang ML, Chen YR, Yang YC, Tsai CH, et al. TET1 suppresses cancer invasion by activating the tissue inhibitors of metalloproteinases. Cell Rep 2012; 2:568-79; PMID:22999938; http://dx.doi.org/ 10.1016/j.celrep.2012.08.030
41. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, 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
42. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of a-ketoglutarate-dependent dioxygenases. Cancer Cell 2011; 19:17-30; PMID:21251613; http://dx.doi.org/10. 1016/j.ccr.2010.12.014
43. Williams K, Christensen J, Helin K. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 2012; 13:28-35; PMID:22157888; http://dx.doi.org/10.1038/embor.2011.233
44. Guo JU, Su Y, Zhong C, Ming GL, Song H. Emerging roles of TET proteins and 5-hydroxymethylcytosines in active DNA demethylation and beyond. Cell Cycle 2011; 10:2662-8; PMID:21811096; http://dx.doi.org/10.4161/cc.10.16.17093
45. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, Cigliano A, et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011; 146:67-79; PMID:21722948; http://dx.doi.org/10.1016/j.cell.2011.06.020
46. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011; 145:423-34; PMID:21496894; http://dx.doi.org/10.1016/j.cell.2011.03.022
47. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011; 333:1303-7; PMID:21817016; http://dx.doi.org/10.1126/science.1210944
48. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333:1300-3; PMID:21778364; http://dx.doi.org/10.1126/science. 1210597
49. 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 2011; 286:35334-8; PMID:21862836; http://dx.doi.org/10.1074/jbc. C111.284620
50. Chen CC, Wang KY, Shen CK. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012; 287:33116-21; PMID:22898819; http://dx.doi.org/10.1074/jbc. C112.406975
51. Inoue A, Zhang Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 2011; 334:194; PMID:21940858; http://dx.doi.org/10.1126/science.1212483
52. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30:256-68; PMID:12798140; http://dx.doi.org/10.1016/ S1046-2023(03)00032-X (Pubitemid 36677560)