Zebularine inhibits human acute myeloid leukemia cell growth in vitro in association with p15INK4B demethylation and reexpression

Experimental Hematology

Volumn 35, Issue 2, 2007, Pages 263-273

  Scott, Stuart A ^a   Lakshimikuttysamma, Ashakumary ^b   Sheridan, David P ^b   Sanche, Stephen E ^b   Geyer, C Ronald ^b   DeCoteau, John F ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROYAL UNIVERSITY HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 2B; TRICHOSTATIN A; ZEBULARINE;

ACETYLATION; ACUTE GRANULOCYTIC LEUKEMIA; AQUEOUS SOLUTION; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL GROWTH; CELL LINE; CELL PROLIFERATION; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; DRUG DOSE COMPARISON; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; DRUG SAFETY; GENE SILENCING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE;

ACETYLATION; ACUTE DISEASE; APOPTOSIS; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYTIDINE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; G2 PHASE; GENE EXPRESSION PROFILING; HISTONES; HL-60 CELLS; HUMANS; HYDROXAMIC ACIDS; LEUKEMIA, MYELOID; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33846362233     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2006.10.005     Document Type: Article

References (52)

1. Toyota M., and Issa J.P. The role of DNA hypermethylation in human neoplasia. Electrophoresis 21 (2000) 329-333
2. Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 21 (2002) 5427-5440
3. Zhou M., Tokumaru Y., Sidransky D., et al. Quantitative GSTP1 methylation levels correlate with Gleason grade and tumor volume in prostate needle biopsies. J Urol 171 (2004) 2195-2198
4. Ricciardiello L., Goel A., Mantovani V., et al. Frequent loss of hMLH1 by promoter hypermethylation leads to microsatellite instability in adenomatous polyps of patients with a single first-degree member affected by colon cancer. Cancer Res 63 (2003) 787-792
5. Sakai T., Toguchida J., Ohtani N., et al. Allele specific hypermethylation of the retinoblastoma tumor-suppressor gene. Am J Hum Genet 48 (1991) 880-888
6. Corn P.G., Heath E.I., Heitmiller R., et al. Frequent hypermethylation of the 5′ CpG island of E-cadherin in esophageal adenocarcinoma. Clin Cancer Res 7 (2001) 2765-2769
7. Herman J.G., Jen J., Merlo A., et al. Hypermethylation-associated inactivation indicates a tumor suppressor role for p15INK4B. Cancer Res 56 (1996) 722-727
8. Bachman K.E., Park B.H., Rhee I., et al. Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene. Cancer Cell 3 (2003) 89-95
9. Cameron E.E., Bachman K.E., Myohanen S., et al. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21 (1999) 103-107
10. Fahrner J.A., Eguchi S., Herman J.G., et al. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 62 (2002) 7213-7218
11. Nguyen C.T., Weisenberger D.J., Velicescu M., et al. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res 62 (2002) 6456-6461
12. Stirzaker C., Song J.Z., Davidson B., et al. Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res 64 (2004) 3871-3877
13. Primeau M., Gagnon J., and Momparler R.L. Synergistic antineoplastic action of DNA methylation inhibitor 5-AZA-2′-deoxycytidine and histone deacetylase inhibitor depsipeptide on human breast carcinoma cells. Int J Cancer 103 (2003) 177-184
14. Shaker S., Bernstein M., Momparler L.F., et al. Preclinical evaluation of antineoplastic activity of inhibitors of DNA methylation (5-aza-2′-deoxycytidine) and histone deacetylation (trichostatin A, depsipeptide) in combination against myeloid leukemic cells. Leuk Res 27 (2003) 437-444
15. Baylin S.B. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2 suppl. 1 (2005) S4-S11
16. Li L.C., Carroll P.R., and Dahiya R. Epigenetic changes in prostate cancer: implication for diagnosis and treatment. J Natl Cancer Inst 97 (2005) 103-115
17. Sheikhnejad G., Brank A., Christman J.K., et al. Mechanism of inhibition of DNA (cytosine C5)-methyltransferases by oligodeoxyribonucleotides containing 5,6-dihydro-5-azacytosine. J Mol Biol 285 (1999) 2021-2034
18. Kumar S., Horton J.R., Jones G.D., et al. DNA containing 4′-thio-2′-deoxycytidine inhibits methylation by HhaI methyltransferase. Nucleic Acids Res 25 (1997) 2773-2783
19. Villar-Garea A., Fraga M.F., Espada J., et al. Procaine is a DNA-demethylating agent with growth-inhibitory effects in human cancer cells. Cancer Res 63 (2003) 4984-4989
20. Issa J.P. Decitabine. Curr Opin Oncol 15 (2003) 446-451
21. Gore S.D. Combination therapy with DNA methyltransferase inhibitors in hematologic malignancies. Nat Clin Pract Oncol 2 suppl 1 (2005) S30-S35
22. Beisler J.A. Isolation, characterization, and properties of a labile hydrolysis product of the antitumor nucleoside, 5-azacytidine. J Med Chem 21 (1978) 204-208
23. Constantinides P.G., Jones P.A., and Gevers W. Functional striated muscle cells from non-myoblast precursors following 5-azacytidine treatment. Nature 267 (1977) 364-366
24. Santi D.V., Norment A., and Garrett C.E. Covalent bond formation between a DNA cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci USA 81 (1984) 6993-6997
25. Kim C.H., Marquez V.E., Mao D.T., et al. Synthesis of pyrimidin-2-one nucleosides as acid-stable inhibitors of cytidine deaminase. J Med Chem 29 (1986) 1374-1380
26. Cheng J.C., Weisenberger D.J., Gonzales F.A., et al. Continuous zebularine treatment effectively sustains demethylation in human bladder cancer cells. Mol Cell Biol 24 (2004) 1270-1278
27. Cheng J.C., Matsen C.B., Gonzales F.A., et al. Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J Natl Cancer Inst 95 (2003) 399-409
28. Pompeia C., Hodge D.R., Plass C., et al. Microarray analysis of epigenetic silencing of gene expression in the KAS-6/1 multiple myeloma cell line. Cancer Res 64 (2004) 3465-3473
29. Yoo C.B., Cheng J.C., and Jones P.A. Zebularine: a new drug for epigenetic therapy. Biochem Soc Trans 32 (2004) 910-912
30. Cheng J.C., Yoo C.B., Weisenberger D.J., et al. Preferential response of cancer cells to zebularine. Cancer Cell 6 (2004) 151-158
31. Marquez V.E., Kelley J.A., Agbaria R., et al. Zebularine: a unique molecule for an epigenetically based strategy in cancer chemotherapy. Ann N Y Acad Sci 1058 (2005) 246-254
32. Kim C.H., Marquez V.E., Mao D.T., et al. Synthesis of pyrimidin-2-one nucleosides as acid-stable inhibitors of cytidine deaminase. J Med Chem 29 (1986) 1374-1380
33. Laliberte J., Marquez V.E., and Momparler R.L. Potent inhibitors for the deamination of cytosine arabinoside and 5-aza-2′-deoxycytidine by human cytidine deaminase. Cancer Chemother Pharmacol 30 (1992) 7-11
34. Christiansen D.H., Andersen M.K., and Pedersen-Bjergaard J. Methylation of p15INK4B is common, is associated with deletion of genes on chromosome arm 7q and predicts a poor prognosis in therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 17 (2003) 1813-1819
35. Herman J.G., Graff J.R., Myohanen S., et al. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 93 (1996) 9821-9826
36. Huang Y., de la Chapelle A., and Pellegata N.S. Hypermethylation, but not LOH, is associated with the low expression of MT1G and CRABP1 in papillary thyroid carcinoma. Int J Cancer 104 (2003) 735-744
37. Jungel A., Baresova V., Ospelt C., et al. Trichostatin A sensitises rheumatoid arthritis synovial fibroblasts for TRAIL-induced apoptosis. Ann Rheum Dis 65 (2006) 910-912
38. Kosugi H., Towatari M., Hatano S., et al. Histone deacetylase inhibitors are the potent inducer/enhancer of differentiation in acute myeloid leukemia: a new approach to anti-leukemia therapy. Leukemia 13 (1999) 1316-1324
39. Cheung W.L., Ajiro K., Samejima K., et al. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113 (2003) 507-517
40. Rogakou E.P., Nieves-Neira W., Boon C., et al. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275 (2000) 9390-9395
41. Prigent C., and Dimitrov S. Phosphorylation of serine 10 in histone H3, what for?. J Cell Sci 116 (2003) 3677-3685
42. Waring P., Khan T., and Sjaarda A. Apoptosis induced by gliotoxin is preceded by phosphorylation of histone H3 and enhanced sensitivity of chromatin to nuclease digestion. J Biol Chem 272 (1997) 17929-17936
43. Fabbri F., Carloni S., Brigliadori G., Zoli W., Lapalombella R., and Marini M. Sequential events of apoptosis involving docetaxel, a microtubule-interfering agent: a cytometric study. BMC Cell Biol 7 (2006) 6
44. Dote H., Cerna D., Burgan W.E., et al. Enhancement of in vitro and in vivo tumor cell radiosensitivity by the DNA methylation inhibitor zebularine. Clin Cancer Res 11 (2005) 4571-4579
45. Lemaire M., Momparler L.F., Bernstein M.L., Marquez V.E., and Momparler R.L. Enhancement of antineoplastic action of 5-aza-2′-deoxycytidine by zebularine on L1210 leukemia. Anticancer Drugs 16 (2005) 301-308
46. Ben-Kasus T., Ben-Zvi Z., Marquez V.E., et al. Metabolic activation of zebularine, a novel DNA methylation inhibitor, in human bladder carcinoma cells. Biochem Pharmacol 70 (2005) 121-133
47. Morales V., and Richard-Foy H. Role of histone N-terminal tails and their acetylation in nucleosome dynamics. Mol Cell Biol 20 (2000) 7230-7237
48. Agalioti T., Chen G., and Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111 (2002) 381-392
49. Levva A., Schwartsmann G., Boeije L.C., et al. Growth inhibitory effects of 5-aza-2′-deoxycytidine in HL-60 promyelocytic leukemia cells resistant to differentiation induction. Biochem Biophys Res Commun 141 (1986) 629-635
50. Tang Q.B., Sun H.W., and Zou S.Q. Inhibitory effect of methylation inhibitor 5-aza-2-deoxycytidine on bile duct cancer cell line in vivo and in vitro. Hepatobiliary Pancreat Dis Int 3 (2004) 124-128
51. Yang Q., Shan L., Yoshimura G., et al. 5-aza-2′-deoxycytidine induces retinoic acid receptor beta 2 demethylation, cell cycle arrest and growth inhibition in breast carcinoma cells. Anticancer Res 22 (2002) 2753-2756
52. Nazarov I.B., Smirnova A.N., Krutilina R.I., et al. Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat Res 160 (2003) 309-317