Epigenetic therapy: Use of agents targeting deacetylation and methylation in cancer management

OncoTargets and Therapy

Volumn 6, Issue , 2013, Pages 223-232

  Ho, Allen S ^a   Turcan, Sevin ^a   Chan, Timothy A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Acetylation; Cancer; Epigenetics; Histone; Methylation; Transcription; Tumor

Indexed keywords

3 DEAZANEPLANOCIN A; 5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; AZACITIDINE; JQ 1; MOCETINOSTAT; PANOBINOSTAT; PLACEBO; ROMIDEPSIN; UNCLASSIFIED DRUG; VORINOSTAT;

ACUTE GRANULOCYTIC LEUKEMIA; ANEMIA; ANOREXIA; BONE MARROW SUPPRESSION; CANCER THERAPY; CARCINOGENESIS; CARDIOTOXICITY; CHEMOTHERAPY INDUCED NAUSEA AND VOMITING; CUTANEOUS T CELL LYMPHOMA; DEACETYLATION; DEMETHYLATION; DIARRHEA; DNA METHYLATION; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRUG SAFETY; EPIGENETICS; FATIGUE; FOLLICULAR LYMPHOMA; GENETIC ASSOCIATION; HISTONE ACETYLATION; HISTONE METHYLATION; HODGKIN DISEASE; HUMAN; HYPERCHOLESTEROLEMIA; LARGE CELL LYMPHOMA; LYMPHOCYTOPENIA; MALIGNANT NEOPLASTIC DISEASE; MOLECULARLY TARGETED THERAPY; MYELODYSPLASTIC SYNDROME; NAUSEA; NEUTROPENIA; NONHUMAN; REVIEW; SIDE EFFECT; T WAVE; THROMBOCYTOPENIA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TREATMENT OUTCOME;

EID: 84875432959     PISSN: 11786930     EISSN: None     Source Type: Journal    
DOI: 10.2147/OTT.S34680     Document Type: Review

References (112)

1. Olsen EA, Kim YH, Kuzel TM, et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol. 2007;25(21):3109-3115.
2. Duvic M, Talpur R, Ni X, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109(1):31-39.
3. Whittaker SJ, Demierre MF, Kim EJ, et al. Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. J Clin Oncol. 2010;28(29):4485-4491.
4. Piekarz RL, Frye R, Turner M, et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol. 2009;27(32): 5410-5417.
5. Schrump DS, Fischette MR, Nguyen DM, et al. Clinical and molecular responses in lung cancer patients receiving romidepsin. Clin Cancer Res. 2008;14(1):188-198.
6. Molife LR, Attard G, Fong PC, et al. Phase II, two-stage, single-arm trial of the histone deacetylase inhibitor (HDACi) romidepsin in metastatic castration-resistant prostate cancer (CRPC). Ann Oncol. 2010;21(1): 109-113.
7. Bauman J, Verschraegen C, Belinsky S, et al. A phase I study of 5-azacytidine and erlotinib in advanced solid tumor malignancies. Cancer Chemother Pharmacol. 2012;69(2):547-554.
8. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science. 2003;300(5618):455.
9. Wang Y, Leung FC. An evaluation of new criteria for CpG islands in the human genome as gene markers. Bioinformatics. 2004;20(7): 1170-1177.
10. Irizarry RA, Ladd-Acosta C, Wen B, et al. The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet. 2009;41(2):178-186.
11. Varambally S, Cao Q, Mani RS, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2in cancer. Science. 2008;322(5908):1695-1699.
12. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell. 2007;130(1):77-88.
13. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6-21.
14. Endres M, Fan G, Meisel A, Dirnagl U, Jaenisch R. Effects of cerebral ischemia in mice lacking DNA methyltransferase 1in post-mitotic neurons. Neuroreport. 2001;12(17):3763-3766.
15. Gao Q, Steine EJ, Barrasa MI, et al. Deletion of the de novo DNA methyltransferase Dnmt3a promotes lung tumor progression. Proc Natl Acad Sci U S A. 2011;108(44):18061-18066.
16. Nosho K, Shima K, Irahara N, et al. DNMT3B expression might contribute to CpG island methylator phenotype in colorectal cancer. Clin Cancer Res. 2009;15(11):3663-3671.
17. Linhart HG, Lin H, Yamada Y, et al. Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev. 2007;21(23):3110-3122.
18. Lister R, Pelizzola M, Dowen RH, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009;462(7271):315-322.
19. Ito S, Shen L, Dai Q, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333(6047): 1300-1303.
20. Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med. 2011;17(3):330-339.
21. Campos EI, Reinberg D. Histones: annotating chromatin. Annu Rev Genet. 2009;43:559-599.
22. Beck DB, Bonasio R, Kaneko S, et al. Chromatin in the nuclear landscape. Cold Spring Harb Symp Quant Biol. 2011;75:11-22.
23. Sawan C, Herceg Z. Histone modifications and cancer. Adv Genet. 2010;70:57-85.
24. Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823-837.
25. Rosenfeld JA, Wang Z, Schones DE, Zhao K, DeSalle R, Zhang MQ. Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics. 2009;10:143.
26. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128(4):707-719.
27. Hu G, Cui K, Northrup D, et al. H2A. Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell. 2013;12(2):180-192.
28. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459(7243):108-112.
29. Gaffney DJ, McVicker G, Pai AA, et al. Controls of nucleosome positioning in the human genome. PLoS Genet. 2012;8(11):e1003036.
30. Baylin SB, Jones PA. A decade of exploring the cancer epigenome-biological and translational implications. Nat Rev Cancer. 2011;11(10): 726-734.
31. Wen B, Wu H, Loh YH, Briem E, Daley GQ, Feinberg AP. Euchromatin islands in large heterochromatin domains are enriched for CTCF binding and differentially DNA-methylated regions. BMC Genomics. 2012;13:566.
32. Keller C, Adaixo R, Stunnenberg R, Woolcock KJ, Hiller S, Buhler M. HP1(Swi6) mediates the recognition and destruction of heterochromatic RNA transcripts. Mol Cell. 2012;47(2):215-227.
33. Fujimura Y, Isono K, Vidal M, et al. Distinct roles of Polycomb group gene products in transcriptionally repressed and active domains of Hoxb8. Development. 2006;133(12):2371-2381.
34. Asangani IA, Ateeq B, Cao Q, et al. Characterization of the EZH2-MMSET histone methyltransferase regulatory axis in cancer. Mol Cell. 2013;49(1):80-93.
35. Banerjee R, Mani RS, Russo N, et al. The tumor suppressor gene rap1GAP is silenced by miR-101-mediated EZH2 overexpression in invasive squamous cell carcinoma. Oncogene. 2011;30(42):4339-4349.
36. Sakurai T, Bilim VN, Ugolkov AV, et al. The enhancer of zeste homolog 2 (EZH2), a potential therapeutic target, is regulated by miR-101in renal cancer cells. Biochem Biophys Res Commun. 2012;422(4):607-614.
37. Esteller M. Epigenetics in cancer. N Engl J Med. 2008;358(11): 1148-1159.
38. Feinberg AP. Cancer epigenetics is no Mickey Mouse. Cancer Cell. 2005;8(4):267-268.
39. Fraga MF, Ballestar E, Villar-Garea A, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet. 2005;37(4):391-400.
40. Seligson DB, Horvath S, Shi T, et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature. 2005;435(7046): 1262-1266.
41. You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell. 2012;22(1):9-20.
42. Dawson MA, Kouzarides T, Huntly BJ. Targeting epigenetic readers in cancer. N Engl J Med. 2012;367(7):647-657.
43. Ley TJ, Ding L, Walter MJ, et al. DNMT3A mutations in acute myeloid leukemia. N Engl J Med. 2010;363(25):2424-2433.
44. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4): 683-692.
45. Iwama A, Oguro H, Negishi M, et al. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity. 2004;21(6):843-851.
46. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 1999;397(6715): 164-168.
47. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;3(6):415-428.
48. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490(7418):61-70.
49. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012; 487(7407):330-337.
50. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609-615.
51. Cancer Genome Atlas Research N. Comprehensive genomic characterization of squamous cell lung cancers. Nature. 2012;489(7417): 519-525.
52. Figueroa ME, Abdel-Wahab O, Lu C, et al. Leukemic IDH1 and IDH2mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell. 2010;18(6):553-567.
53. Issa JP. CpG island methylator phenotype in cancer. Nat Rev Cancer. 2004;4(12):988-993.
54. Turcan S, Rohle D, Goenka A, et al. IDH1mutation is sufficient to establish the glioma hypermethylator phenotype. Nature. 2012;483(7390):479-483.
55. Fang F, Turcan S, Rimner A, et al. Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci Transl Med. 2011;3(75): 75ra25.
56. van den Bent MJ, Gravendeel LA, Gorlia T, et al. A hypermethylated phenotype is a better predictor of survival than MGMT methylation in anaplastic oligodendroglial brain tumors: a report from EORTC study 26951. Clin Cancer Res. 2011;17(22):7148-7155.
57. Delhommeau F, Dupont S, Della Valle V, et al. Mutation in TET2in myeloid cancers. N Engl J Med. 2009;360(22):2289-2301.
58. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. Epigenetic reprogramming by adenovirus e1a. Science. 2008;321(5892):1086-1088.
59. Rasti M, Grand RJ, Mymryk JS, Gallimore PH, Turnell AS. Recruitment of CBP/p300, TATA-binding protein, and S8 to distinct regions at the N terminus of adenovirus E1A. J Virol. 2005;79(9):5594-5605.
60. Cao P, Deng Z, Wan M, et al. MicroRNA-101 negatively regulates Ezh2 and its expression is modulated by androgen receptor and HIF-1alpha/HIF-1beta. Mol Cancer. 2010;9:108.
61. Smits M, Nilsson J, Mir SE, et al. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget. 2010;1(8):710-720.
62. Jeronimo C, Henrique R, Hoque MO, et al. A quantitative promoter methylation profile of prostate cancer. Clin Cancer Res. 2004;10(24): 8472-8478.
63. Brooks JD, Weinstein M, Lin X, et al. CG island methylation changes near the GSTP1gene in prostatic intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev. 1998;7(6):531-536.
64. Henrique R, Jeronimo C. Molecular detection of prostate cancer: a role for GSTP1 hypermethylation. Eur Urol. 2004;46(5):660-669; discussion 669.
65. Esteller M, Garcia-Foncillas J, Andion E, et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med. 2000;343(19):1350-1354.
66. Plumb JA, Strathdee G, Sludden J, Kaye SB, Brown R. Reversal of drug resistance in human tumor xenografts by 2′-deoxy-5-azacytidine-induced demethylation of the hMLH1gene promoter. Cancer Res. 2000;60(21):6039-6044.
67. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction? Nat Rev Cancer. 2006;6(2):107-116.
68. Schneider-Stock R, Diab-Assef M, Rohrbeck A, et al. 5-Aza-cytidine is a potent inhibitor of DNA methyltransferase 3a and induces apoptosis in HCT-116 colon cancer cells via Gadd45-and p53-dependent mechanisms. J Pharmacol Exp Ther. 2005;312(2):525-536.
69. Kelly TK, De Carvalho DD, Jones PA. Epigenetic modifications as therapeutic targets. Nat Biotechnol. 2010;28(10):1069-1078.
70. Kantarjian H, Issa JP, Rosenfeld CS, et al. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer. 2006;106(8):1794-1803.
71. Silverman LR, Demakos EP, Peterson BL, et al. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. J Clin Oncol. 2002;20(10):2429-2440.
72. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol. 2009;10(3):223-232.
73. Blum W, Garzon R, Klisovic RB, et al. Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proc Natl Acad Sci U S A. 2010;107(16):7473-7478.
74. Cashen AF, Schiller GJ, O'Donnell MR, DiPersio JF. Multicenter, phase II study of decitabine for the first-line treatment of older patients with acute myeloid leukemia. J Clin Oncol. 2010;28(4):556-561.
75. Yoo CB, Jeong S, Egger G, et al. Delivery of 5-aza-2′-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res. 2007;67(13): 6400-6408.
76. Brueckner B, Rius M, Markelova MR, et al. Delivery of 5-azacytidine to human cancer cells by elaidic acid esterification increases therapeutic drug efficacy. Mol Cancer Ther. 2010;9(5):1256-1264.
77. Kuck D, Caulfield T, Lyko F, Medina-Franco JL. Nanaomycin A selectively inhibits DNMT3B and reactivates silenced tumor suppressor genes in human cancer cells. Mol Cancer Ther. 2010;9(11): 3015-3023.
78. Saunders LR, Verdin E. Sirtuins: critical regulators at the crossroads between cancer and aging. Oncogene. 2007;26(37):5489-5504.
79. Federico M, Bagella L. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. J Biomed Biotechnol. 2011;2011:475641.
80. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol. 2009;27(32):5459-5468.
81. Younes A, Sureda A, Ben-Yehuda D, et al. Panobinostat in patients with relapsed/refractory Hodgkin's lymphoma after autologous stem-cell transplantation: results of a phase II study. J Clin Oncol. 2012;30(18): 2197-2203.
82. Younes A, Oki Y, Bociek RG, et al. Mocetinostat for relapsed classical Hodgkin's lymphoma: an open-label, single-arm, phase 2 trial. Lancet Oncol. 2011;12(13):1222-1228.
83. Garcia-Manero G, Assouline S, Cortes J, et al. Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103in leukemia. Blood. 2008;112(4):981-989.
84. Mack GS. To selectivity and beyond. Nat Biotechnol. 2010;28(12): 1259-1266.
85. Yang Z, He N, Zhou Q. Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1gene expression and cell cycle progression. Mol Cell Biol. 2008;28(3):967-976.
86. Filippakopoulos P, Qi J, Picaud S, et al. Selective inhibition of BET bromodomains. Nature. 2010;468(7327):1067-1073.
87. Nicodeme E, Jeffrey KL, Schaefer U, et al. Suppression of inflammation by a synthetic histone mimic. Nature. 2010;468(7327):1119-1123.
88. Balasubramanyam K, Varier RA, Altaf M, et al. Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J Biol Chem. 2004;279(49):51163-51171.
89. Balasubramanyam K, Altaf M, Varier RA, et al. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J Biol Chem. 2004;279(32):33716-33726.
90. Sun Y, Jiang X, Chen S, Price BD. Inhibition of histone acetyltransferase activity by anacardic acid sensitizes tumor cells to ionizing radiation. FEBS Lett. 2006;580(18):4353-4356.
91. Lall S. Primers on chromatin. Nat Struct Mol Biol. 2007;14(11): 1110-1115.
92. Metzger E, Wissmann M, Yin N, et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature. 2005;437(7057):436-439.
93. Lim S, Janzer A, Becker A, et al. Lysine-specific demethylase 1 (LSD1) is highly expressed in ER-negative breast cancers and a biomarker predicting aggressive biology. Carcinogenesis. 2010;31(3): 512-520.
94. Schulte JH, Lim S, Schramm A, et al. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res. 2009;69(5):2065-2071.
95. Huang Y, Stewart TM, Wu Y, et al. Novel oligoamine analogues inhibit lysine-specific demethylase 1 and induce reexpression of epigenetically silenced genes. Clin Cancer Res. 2009;15(23):7217-7228.
96. Wu Y, Steinbergs N, Murray-Stewart T, Marton LJ, Casero RA. Oligoamine analogues in combination with 2-difluoromethylornithine synergistically induce re-expression of aberrantly silenced tumour-suppressor genes. Biochem J. 2012;442(3):693-701.
97. Wang J, Hevi S, Kurash JK, et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet. 2009;41(1):125-129.
98. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006;20(9):1123-1136.
99. Albert M, Helin K. Histone methyltransferases in cancer. Semin Cell Dev Biol. 2010;21(2):209-220.
100. Gannon O, Endo-Munoz LB, Merida de Long L, Hazar-Rethinam M, Saunders NA. Dysregulation of the repressive H3K27 trimethylation mark in head and neck squamous cell carcinoma contributes to dysregulated squamous differentiation. Clin Cancer Res. 2013;19(2):428-441.
101. Tan J, Yang X, Zhuang L, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 2007;21(9):1050-1063.
102. Bradley D, Rathkopf D, Dunn R, et al. Vorinostat in advanced prostate cancer patients progressing on prior chemotherapy (National Cancer Institute Trial 6862): trial results and interleukin-6 analysis: a study by the Department of Defense Prostate Cancer Clinical Trial Consortium and University of Chicago Phase 2 Consortium. Cancer. 2009;115(23):5541-5549.
103. Vansteenkiste J, Van Cutsem E, Dumez H, et al. Early phase II trial of oral vorinostat in relapsed or refractory breast, colorectal, or non-small cell lung cancer. Invest New Drugs. 2008;26(5):483-488.
104. Blumenschein GR Jr, Kies MS, Papadimitrakopoulou VA, et al. Phase II trial of the histone deacetylase inhibitor vorinostat (Zolinza, suberoylanilide hydroxamic acid, SAHA) in patients with recurrent and/or metastatic head and neck cancer. Invest New Drugs. 2008;26(1):81-87.
105. Ramalingam SS, Maitland ML, Frankel P, et al. Carboplatin and Paclitaxel in combination with either vorinostat or placebo for first-line therapy of advanced non-small-cell lung cancer. J Clin Oncol. 2010;28(1):56-62.
106. Stadler WM, Margolin K, Ferber S, McCulloch W, Thompson JA. A phase II study of depsipeptide in refractory metastatic renal cell cancer. Clin Genitourin Cancer. 2006;5(1):57-60.
107. Gorgun G, Calabrese E, Hideshima T, et al. A novel Aurora-A kinase inhibitor MLN8237induces cytotoxicity and cell-cycle arrest in multiple myeloma. Blood. 2010;115(25):5202-5213.
108. den Hollander J, Rimpi S, Doherty JR, et al. Aurora kinases A and B are up-regulated by Myc and are essential for maintenance of the malignant state. Blood. 2010;116(9):1498-1505.
109. Martin JA, Wang Z. Next-generation transcriptome assembly. Nat Rev Genet. 2011;12(10):671-682.
110. Furey TS. ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat Rev Genet. 2012;13(12):840-852.
111. Wong KM, Hudson TJ, McPherson JD. Unraveling the genetics of cancer: genome sequencing and beyond. Annu Rev Genomics Hum Genet. 2011;12:407-430.
112. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997-1003.