SGI-110 and entinostat therapy reduces lung tumor burden and reprograms the epigenome

International Journal of Cancer

Volumn 135, Issue 9, 2014, Pages 2223-2231

  Tellez, Carmen S ^a   Grimes, Marcie J ^a   Picchi, Maria A ^a   Liu, Yushi ^a   March, Thomas H ^a   Reed, Matthew D ^a   Oganesian, Aram ^b   Taverna, Pietro ^b   Belinsky, Steven A ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b ASTEX PHARMACEUTICALS   (United Kingdom)

Author keywords

DNA methylation; epigenetic therapy; lung cancer; nude rat

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; CANCER TESTIS ANTIGEN; ENTINOSTAT; K RAS PROTEIN; P21 ACTIVATED KINASE; PROTEIN P53; SGI 110; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; BODY WEIGHT; CANCER INHIBITION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DRUG EFFICACY; DRUG HALF LIFE; DRUG SENSITIZATION; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; IMMUNOMODULATION; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; LUNG TUMOR; LUNG WEIGHT; MASS SPECTROMETRY; MAXIMUM PLASMA CONCENTRATION; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TUMOR VOLUME;

DNA METHYLATION; EPIGENETIC THERAPY; LUNG CANCER; NUDE RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AZACITIDINE; BENZAMIDES; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; IMMUNOLOGIC FACTORS; LUNG NEOPLASMS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PYRIDINES; RATS; RATS, NUDE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR BURDEN; TUMOR MARKERS, BIOLOGICAL;

EID: 84906239824     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28865     Document Type: Article

References (50)

1. Santi DV, Norment A, Garrett CE,. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci U S A 1984; 81: 6993-7.
2. Yoo CB, Jones PA,. Epigenetic therapy of cancer: past, present and future. Nat Rev Drug Discov 2006; 5: 37-50.
3. Nieto M, Samper E, Fraga MF, et al. The absence of p53 is critical for the induction of apoptosis by 5-aza-2-deoxycytidine. Oncogene 2004; 23: 735-43.
4. Chai G, Li L, Zhou W, et al. HDAC inhibitors act with 5-aza-2-deoxycytidine to inhibit cell proliferation by suppressing removal of incorporated abases in lung cancer cells. PLoS One 2008; 3: e2445.
5. Singh BN, Zhou H, Li J, et al. Preclinical studies on histone deacetylase inhibitors as therapeutic reagents for endometrial and ovarian cancers. Future Oncol 2011; 7: 1415-28.
6. Cameron EE, Bachman KE, Myohanen S, et al. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 1999; 21: 103-7.
7. Kalac M, Scotto L, Marchi E, et al. HDAC inhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood 2011; 118: 5506-16.
8. Karpf AR, Jones DA,. Reactivating the expression of methylation silenced genes in human cancer. Oncogene 2002; 21: 5496-503.
9. Issa JP, Kantarjian HM,. Targeting DNA methylation. Clin Cancer Res 2009; 15: 3938-46.
10. Jones PA, Taylor SM,. Cellular differentiation, cytidine analogs and DNA methylation. Cell 1980; 20: 85-93.
11. Momparler RL, Goodman J,. In vitro cytotoxic and biochemical effects of 5-aza-2-deoxycytidine. Cancer Res 1977; 37: 1636-9.
12. Christman JK,. 5-Azacytidine and 5-aza-2-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Oncogene 2002; 21: 5483-95.
13. Camiener GW, Smith CG,. Studies of the enzymatic deamination of cytosine arabinoside. I. Enzyme distribution and species specificity. Biochem Pharmacol 1965; 14: 1405-16.
14. Chuang JC, Warner SL, Vollmer D, et al. S110, a 5-Aza-2-deoxycytidine- containing dinucleotide, is an effective DNA methylation inhibitor in vivo and can reduce tumor growth. Mol Cancer Ther 2010; 9: 1443-50.
15. Yoo CB, Jeong S, Egger G, et al. Delivery of 5-aza-2-deoxycytidine to cells using oligodeoxynucleotides. Cancer Res 2007; 67: 6400-8.
16. Grunstein M,. Histone acetylation in chromatin structure and transcription. Nature 1997; 389: 349-52.
17. Spencer VA, Davie JR,. Role of covalent modifications of histones in regulating gene expression. Gene 1999; 240: 1-12.
18. Waterborg JH,. Dynamics of histone acetylation in vivo. A function for acetylation turnover? Biochem Cell Biol 2002; 80: 363-78.
19. Wade PA,. Transcriptional control at regulatory checkpoints by histone deacetylases: molecular connections between cancer and chromatin. Hum Mol Genet 2001; 10: 693-8.
20. Struhl K,. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 1998; 12: 599-606.
21. Van Lint C, Emiliani S, Verdin E,. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr 1996; 5: 245-53.
22. Peart MJ, Smyth GK, van Laar RK, et al. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2005; 102: 3697-702.
23. Shao Y, Gao Z, Marks PA, et al. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci U S A 2004; 101: 18030-5.
24. Marks PA, Richon VM, Rifkind RA,. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst 2000; 92: 1210-6.
25. Yamashita Y, Shimada M, Harimoto N, et al. Histone deacetylase inhibitor trichostatin A induces cell-cycle arrest/apoptosis and hepatocyte differentiation in human hepatoma cells. Int J Cancer 2003; 103: 572-6.
26. Liu S, Cheng H, Kwan W, et al. Histone deacetylase inhibitors induce growth arrest, apoptosis, and differentiation in clear cell sarcoma models. Mol Cancer Ther 2008; 7: 1751-61.
27. Rosato RR, Almenara JA, Grant S,. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1. Cancer Res 2003; 63: 3637-45.
28. Kummar S, Gutierrez M, Gardner ER, et al. Phase I trial of MS-275, a histone deacetylase inhibitor, administered weekly in refractory solid tumors and lymphoid malignancies. Clin Cancer Res 2007; 13: 5411-7.
29. Gojo I, Jiemjit A, Trepel JB, et al. Phase 1 and pharmacologic study of MS-275, a histone deacetylase inhibitor, in adults with refractory and relapsed acute leukemias. Blood 2007; 109: 2781-90.
30. Suzuki H, Gabrielson E, Chen W, et al. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002; 31: 141-9.
31. Bovenzi V, Momparler RL,. Antineoplastic action of 5-aza-2-deoxycytidine and histone deacetylase inhibitor and their effect on the expression of retinoic acid receptor beta and estrogen receptor alpha genes in breast carcinoma cells. Cancer Chemother Pharmacol 2001; 48: 71-6.
32. Juergens RA, Wrangle J, Vendetti FP, et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov 2011; 1: 598-607.
33. March TH, Marron-Terada PG, Belinsky SA,. Refinement of an orthotopic lung cancer model in the nude rat. Vet Pathol 2001; 38: 483-90.
34. Belinsky SA, Grimes MJ, Picchi MA, et al. Combination therapy with vidaza and entinostat suppresses tumor growth and reprograms the epigenome in an orthotopic lung cancer model. Cancer Res 2011; 71: 454-62.
35. Reed MD, Tellez CS, Grimes MJ, et al. Aerosolised 5-azacytidine suppresses tumour growth and reprogrammes the epigenome in an orthotopic lung cancer model. Br J Cancer 2013; 109: 1775-81.
36. Lehman TA, Bennett WP, Metcalf RA, et al. p53 mutations, ras mutations, and p53-heat shock 70 protein complexes in human lung carcinoma cell lines. Cancer Res 1991; 51: 4090-6.
37. Ryan QC, Headlee D, Acharya M, et al. Phase I and pharmacokinetic study of MS-275, a histone deacetylase inhibitor, in patients with advanced and refractory solid tumors or lymphoma. J Clin Oncol 2005; 23: 3912-22.
38. Gore L, Rothenberg ML, O'Bryant CL, et al. A phase I and pharmacokinetic study of the oral histone deacetylase inhibitor, MS-275, in patients with refractory solid tumors and lymphomas. Clin Cancer Res 2008; 14: 4517-25.
39. Belinsky SA, Klinge DM, Stidley CA, et al. Inhibition of DNA methylation and histone deacetylation prevents murine lung cancer. Cancer Res 2003; 63: 7089-93.
40. Varambally S, Dhanasekaran SM, Zhou M, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419: 624-9.
41. Vire E, Brenner C, Deplus R, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-4.
42. Schrump DS, Fischette MR, Nguyen DM, et al. Phase I study of decitabine-mediated gene expression in patients with cancers involving the lungs, esophagus, or pleura. Clin Cancer Res 2006; 12: 5777-85.
43. Coral S, Parisi G, Nicolay HJ, et al. Immunomodulatory activity of SGI-110, a 5-aza-2-deoxycytidine-containing demethylating dinucleotide. Cancer Immunol Immunother 2013; 62: 605-14.
44. Fuks F, Burgers WA, Brehm A, et al. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 2000; 24: 88-91.
45. Rountree MR, Bachman KE, Baylin SB,. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 2000; 25: 269-77.
46. Lehnertz B, Ueda Y, Derijck AA, et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 2003; 13: 1192-200.
47. Komashko VM, Farnham PJ,. 5-azacytidine treatment reorganizes genomic histone modification patterns. Epigenetics 2010; 5: 229-40.
48. Ebrahem Q, Mahfouz RZ, Ng KP, et al. High cytidine deaminase expression in the liver provides sanctuary for cancer cells from decitabine treatment effects. Oncotarget 2012; 3: 1137-45.
49. Lavelle D, Vaitkus K, Ling Y, et al. Effects of tetrahydrouridine on pharmacokinetics and pharmacodynamics of oral decitabine. Blood 2012; 119: 1240-7.
50. Matei D, Fang F, Shen C, et al. Epigenetic resensitization to platinum in ovarian cancer. Cancer Res 2012; 72: 2197-205.