Dynamics of bivalent chromatin domains upon drug induced reactivation and resilencing in cancer cells

Epigenetics

Volumn 6, Issue 9, 2011, Pages 1138-1148

  Mayor, Regina ^a   Muñoz, Mar ^a   Coolen, Marcel W ^b,c   Custodio, Joaquin ^a   Esteller, Manel ^d   Clark, Susan J ^b,e   Peinado, Miguel A ^a  

^a Institut de Medicina Predictiva i Personalitzada del Cancer IMPPC   (Spain)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Chromatin remodeling; Colorectal cancer; DNA methylation; Epigenetic drugs; Epigenetic silencing

Indexed keywords

HISTONE H3; LYSINE;

ARTICLE; CANCER CELL CULTURE; CELL STRAIN HCT116; CHROMATIN; CHROMOSOME 2Q; CHROMOSOME 5Q; CHROMOSOME BIVALENT; COLON CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DRUG EXPOSURE; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENE THERAPY; GENETIC MODEL; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; IN VITRO STUDY; PROMOTER REGION; TREATMENT RESPONSE;

EID: 80052555414     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.9.16066     Document Type: Article

References (49)

1. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8:286-98.
2. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683-92.
3. Frigola J, Song J, Stirzaker C, Hinshelwood RA, Peinado MA, Clark S. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat Genet 2006; 38:540-9.
4. Clark SJ. Action at a distance: epigenetic silencing of large chromosomal regions in carcinogenesis. Hum Mol Genet 2007; 16:88-95.
5. Hitchins MP, Lin VA, Buckle A, Cheong K, Halani N, Ku S, et al. Epigenetic inactivation of a cluster of genes flanking MLH1 in microsatellite-unstable colorectal cancer. Cancer Res 2007; 67:9107-16.
6. Rodriguez J, Muñoz M, Vives L, Frangou CG, Groudine M, Peinado MA. Bivalent domains enforce transcriptional memory of DNA methylated genes in cancer cells. Proc Natl Acad Sci USA 2008; 105:19809-14.
7. Novak P, Jensen T, Oshiro MM, Watts GS, Kim CJ, Futscher BW. Agglomerative epigenetic aberrations are a common event in human breast cancer. Cancer Res 2008; 68:8616-25.
8. Dallosso AR, Hancock AL, Szemes M, Moorwood K, Chilukamarri L, Tsai HH, et al. Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Genet 2009; 5:1000745.
9. Coolen MW, Stirzaker C, Song JZ, Statham AL, Kassir Z, Moreno CS, et al. Consolidation of the cancer genome into domains of repressive chromatin by long-range epigenetic silencing (LRES) reduces transcriptional plasticity. Nat Cell Biol 2010; 12:235-46.
10. Devaney J, Stirzaker C, Qu W, Song JZ, Statham AL, Patterson KI, et al. Epigenetic deregulation across 2q14.2 differentiates normal from prostate cancer and provides a regional part of novel DNA methylation cancer biomarkers. Cancer Epidemiol Biomarkers Prev 2010; 10.1158/055-9965. EPI-10-0719.
11. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705.
12. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Poly comb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39:232-6.
13. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439:871-4.
14. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hyper-methylation and heritable silencing. Nat Genet 2007; 39:237-42.
15. McGarvey KM, Van Neste L, Cope L, Ohm JE, Herman JG, Van Criekinge W, et al. Defining a chromatin pattern that characterizes DNA-hypermethylated genes in colon cancer cells. Cancer Res 2008; 68:5753-9.
16. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315-26.
17. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448:553-60.
18. Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007; 1:299-312.
19. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007; 1:286-98.
20. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129:823-37.
21. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 2008; 4:1000242.
22. Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H, et al. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 2010; 20:434-9.
23. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 2010; 20:440-6.
24. Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell 2006; 124:1111-5.
25. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40:499-507.
26. Spivakov M, Fisher AG. Epigenetic signatures of stemcell identity. Nat Rev Genet 2007; 8:263-71.
27. Sharma S, Kelly TK, Jones PA. Epigenetics in Cancer. Carcinogenesis 2010; 31:27-36.
28. Komashko VM, Farnham PJ. 5-azacytidine treatment reorganizes genomic histone modification patterns. Epigenetics 2010; 5:229-40.
29. Si J, Boumber YA, Shu J, Qin T, Ahmed S, He R, et al. Chromatin remodeling is required for gene reactivation after decitabine-mediated DNA hypomethylation. Cancer Res 2010; 70:6968-77.
30. Mayor R, Casadome L, Azuara D, Moreno V, Clark SJ, Capella G, et al. Long-range epigenetic silencing at 2q14.2 affects most human colorectal cancers and may have application as a non-invasive biomarker of disease. Br J Cancer 2009; 100:1534-9.
31. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, et al. Epigenetic stem cell signature in cancer. Nat Genet 2007; 39:157-8.
32. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004; 429:457-63.
33. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002; 416:552-6.
34. Egger G, Jeong S, Escobar SG, Cortez CC, Li TW, Saito Y, et al. Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc Natl Acad Sci USA 2006; 103:14080-5.
35. Das PM, Singal R. DNA methylation and cancer. J Clin Oncol 2004; 22:4632-42.
36. Bender CM, Gonzalgo ML, Gonzales FA, Nguyen CT, Robertson KD, Jones PA. Roles of cell division and gene transcription in the methylation of CpG islands. Mol Cell Biol 1999; 19:6690-8.
37. Liang G, Gonzalgo ML, Salem C, Jones PA. Identification of DNA methylation differences during tumorigenesis by methylation-sensitive arbitrarily primed polymerase chain reaction. Methods 2002; 27:150-5.
38. Egger G, Aparicio AM, Escobar SG, Jones PA. Inhibition of histone deacetylation does not block resilencing of p16 after 5-aza-2'-deoxycytidine treatment. Cancer Res 2007; 67:346-53.
39. Kagey JD, Kapoor-Vazirani P, McCabe MT, Powell DR, Vertino PM. Long-term stability of demethylation after transient exposure to 5-aza-2'-deoxycytidine correlates with sustained RNA polymerase II occupancy. Mol Cancer Res 2010; 8:1048-59.
40. McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, Baylin SB. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res 2006; 66:3541-9.
41. Stirzaker C, Song JZ, Davidson B, Clark SJ. Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res 2004; 64:3871-7.
42. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999; 21:103-7.
43. Zhu B, Benjamin D, Zheng Y, Angliker H, Thiry S, Siegmann M, et al. Overexpression of 5-methylcytosine DNA glycosylase in human embryonic kidney cells EcR293 demethylates the promoter of a hormone-regulated reporter gene. Proc Natl Acad Sci USA 2001; 98:5031-6.
44. Paz MF, Wei S, Cigudosa JC, Rodriguez-Perales S, Peinado MA, Huang TH, et al. Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum Mol Genet 2003; 12:2209-19.
45. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, Kelly TK, et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther 2009; 8:1579-88.
46. Rhee I, Jair KW, Yen RW, Lengauer C, Herman JG, Kinzler KW, et al. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 2000; 404:1003-7.
47. Ormerod MG. Analysis of cell proliferation using the bromodeoxyuridine/Hoechst-ethidium bromide method. Methods Mol Biol 1997; 75:357-65.
48. Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res 2007; 35:119.
49. Rodriguez J, Vives L, Jorda M, Morales C, Munoz M, Vendrell E, et al. Genome-wide tracking of unmethyl-ated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res 2008; 36:770-84.