Demethylation of DNA by decitabine in cancer chemotherapy

Expert Review of Anticancer Therapy

Volumn 4, Issue 4, 2004, Pages 501-510

  Brown, Robert ^a   Plumb, Jane A ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cancer; Chemotherapy; DNA methylation; Epigenetics

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; CARBOPLATIN; CISPLATIN; CYCLOPHOSPHAMIDE; DNA METHYLTRANSFERASE; EPIRUBICIN; MULTIDRUG RESISTANCE PROTEIN 1; PROCAINAMIDE; RETINOIC ACID; TEMOZOLOMIDE; TRICHOSTATIN A; ZEBULARINE;

ANTINEOPLASTIC ACTIVITY; BONE MARROW SUPPRESSION; CANCER INHIBITION; CLINICAL TRIAL; DEMETHYLATION; DNA METHYLATION; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG ELIMINATION; DRUG HALF LIFE; DRUG MECHANISM; DRUG METABOLISM; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HUMAN; LEUKEMIA; LUNG CANCER; MAXIMUM TOLERATED DOSE; NAUSEA AND VOMITING; NEUTROPENIA; NONHUMAN; REVIEW; SOLID TUMOR; TUMOR CELL; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CANCER;

EID: 4444325603     PISSN: 14737140     EISSN: None     Source Type: Journal    
DOI: 10.1586/14737140.4.4.501     Document Type: Review

References (62)

1. Costello JF, Fruhwald MC, Smiraglia DJ et al. Aberrant CpG-island methylation has non-random and tumor-type-specific patterns. Nature Genet. 24, 132-138 (2000).
2. Hendrich B, Bird A. Mammalian methyltransferases and methyl-CpG-binding domains: proteins involved in DNA methylation. Curr. Top. Microbiol. Immunol. 249, 55-74 (2000).
3. Brown R, Strathdee G. Epigenomics and epigenetic therapy of cancer. Trends Mol. Med. 8, S43-S48 (2002).
4. Costello JF, Plass C. Methylation matters. J. Med. Genet. 8, 285-303 (2001).
5. Esteller M, Herman JG. Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumors. J. Pathol. 196, 1-7 (2002).
6. Yan PS, Perry MR, Laux DE, Asare AL, Caldwell CW, Huang TH-M. CpG island arrays: an application towards deciphering epigenetic signatures of breast cancer. Clin. Cancer Res. 6, 1432-1438 (2000).
7. Bestor TH, Verdine GL. DNA methyltransferases. Curr. Opin. Cell. Biol. 6, 380-389 (1994).
8. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
9. Rhee I, Bachman KE, Park BH et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552-556 (2002).
10. Lyons J, Bayar E, Fine G et al. Decitabine: development of a DNA methyltransferase inhibitor for hematological malignancies. Curr. Opin. Investig. Drugs 4, 1442-1450 (2003).
11. Issa JP. Decitabine. Curr. Opin. Oncol. 15, 446, 451 (2003).
12. Taylor SM, Jones PA Multiple new phenotypes induced in 10T2 and 3T3 cells treated with 5-azacytidine. Cell 17, 771-779 (1979).
13. Issa JP Garcia-Manero G, Giles FJ et al. Phase I study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-2′-deoxycytidine (decitabine) in hematopoietic malignancies. Blood 103, 1635-1640 (2004).
14. 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 hMLH1 gene promoter. Cancer Res. 60, 6039-6044 (2000).
15. Cheng JC, Matsen CB, Gonzales FA et al. Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J. Natl Cancer Inst. 95, 399-409 (2003).
16. Zhou L, Cheng X, Connolly BA, Dickman MJ, Hurd PJ, Hornby DP. Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases. J. Mol. Biol. 321, 591-599 (2002).
17. Lin X, Asgari K, Putzi MJ et al. Reversal of GSTP1 CpG island hypermethylation and reactivation of pi-class glutathione S-transferase (GSTPI) expression in human prostate cancer cells by treatment with procainamide. Cancer Res. 61, 8611-8616 (2001).
18. Fournel M, Sapieha P, Beaulieu N, Besterman JM, MacLeod AR. Down-regulation of human DNA (cytosine-5) methyltransferase induces cell cycle regulators p16(ink4A) and p21(WAF/Cip1) by distinct mechanisms. J. Biol. Chem. 274, 24250-24256 (1999).
19. Ramchandani S, MacLeod AR, Pinard M, von Hofe E, Szyf M. Inhibition of tumorigenesis by a cytosine-DNA, methyltransferase, antisense oligodeoxynucleotide. Proc. Natl Acad. Sci. USA 94, 684-689 (1997).
20. Momparler RL, Bouchard J, Samson J. Induction of differentiation and inhibition of DNA methylation in HL-60 myeloid leukemic cells by 5-aza-2′-deoxycytidine. Leuk. Res. 9, 1361-1366 (1985).
21. Tate PH, Bird A. Effects of DNA methylation on DNA binding proteins and gene expression. Curr. Opin. Genet. Dev. 3, 226-231 (1993).
22. Bird A, Wolffe AP. Methylation-induced repression-belts, braces and chromatin. Cell 99, 451-454 (1999).
23. Tyler JK, Kadonaga JT. The 'dark side' of chromatin remodeling: repressive effects on transcription. Cell 99, 443-446 (1999).
24. Chabot GG, Rivard GE, Momparler RL. Plasma and cerebrospinal fluid pharmacokinetics of 5-aza-2′-deoxycytidine in rabbits and dogs. Cancer Res. 43, 592-597 (1983).
25. Momparler RL, Cote S, Eliopoulos N. Pharmacological approach for optimization of the dose schedule of 5-aza-2′-deoxycitidine (decitabine) for the therapy of leukemia. Leukemia 11, 175-180 (1997).
26. Momparler RL, de Vos Haarlem D. 5-aza-2′deoxycytidine: Preclinical and Clinical Studies. PCH Publications, Haarlem, The Netherlands (1990).
27. Lin KT, Momparler RL, Rivard GE. High-performance liquid chromatographic analysis of 2-deoxy-5-azacytidine. J. Pharm. Sci. 70(11), 1228-1232 (1981).
28. Appleton K, Plumb JA, Stuart D et al. Pharmacodynamic responses to 2′-deoxy-5-azacytidine in mice and humans. Proc. Am. Assoc. Cancer Res. 44, 4023 (2003)
29. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, Boon T. The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc. Natl Acad Sci. USA 93, 7149-7153 (1996).
30. Bartolomei MS, Tilghman SM. Genomic imprinting in mammals. Ann. Rev. Genet. 31, 493-525 (1997).
31. Otterson GA. Khleif SN, Chen W, Coxon AB, Kaye FJ. CDKN2 gene silencing in lung cancer by DNA hypermethylation and kinetics of p16INK4 protein induction by 5-aza 2′deoxycytidine. Oncogene 11, 1211-1216 (1995).
32. Pinto A, Attadia V, Fusco A, Ferrara F, Spada OA, Di Fiore PP. 5-aza-2′-deoxycytidine induces terminal differentiation of leukemic blasts from patients with acute myeloid leukemias. Blood 64, 922-929 (1984).
33. Liang G, Gonzales FA, Jones PA, Orntoft TF, Thykjaer T. Analysis of gene induction in human fibroblasts and bladder cancer cells exposed to the methylation inhibitor 5-aza-2′-deoxycytidine. Cancer Res. 62, 961-966 (2002).
34. Herman JG, Latif F, Weng Y et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl Acad. Sci. USA 91, 9700-9704 (1994).
35. Merlo A, Herman JG, Mao L et al. 5′ CpG island methylation is associated with transcriptional silencing of the tumor suppressor p16/CDKN2/MTS1 in human cancers. Nature Med. 1, 686-692 (1995).
36. Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG. Methylation patterns of the E-cadherin 5′ CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J. Biol. Chem. 275, 2727-2732 (2000).
37. Nass SJ, Herman JG, Gabrielson E et al. Aberrant methylation of the estrogen receptor and E-cadherin 5′ CpG islands increases with malignant progression in human breast cancer. Cancer Res. 60, 4346-4348 (2000).
38. Yang X, Phillips DL, Ferguson AT, Nelson WG, Herman JG, Davidson NE. Synergistic activation of functional estrogen receptor (ER)-α by DNA methyltransferase and histone deacetylase inhibition in human ER-α-negative breast cancer cells. Cancer Res. 61, 7025-7029 (2001).
39. Gifford G, Paul J, Vasey PA, Kaye SB, Brown R. The acquisition of HMLH1 methylation in plasma DNA following chemotherapy predicts poor survival for ovarian cancer patients. Clin. Cancer Res. (2004) (In Press).
40. Abele R, Clavel M, Dodion P et al. The EORTC Early Clinical Trials Cooperative Group experience with 5-aza-2′-deoxycytidine (NSC 127716) in patients with colorectal, head and neck, renal carcinomas and malignant melanomas. Eur. J. Cancer Clin. Oncol. 23, 1921-1924 (1987).
41. van Groeningen CJ, Leyva A, O'Brien AM, Gall HE, Pinedo HM. Phase I and pharmacokinetic study of 5-aza-2′-deoxycytidine (NSC 127716) in cancer patients. Cancer Res. 46, 4831-4836 (1986).
42. Jones PA, Taylor SM. Cellular differentiation, cytidine analogs and DNA methylation. Cell 20, 85-93 (1981).
43. Daskalakis M, Nguyen TT, Nguyen C et al. Demethylation of a hypermethylated P15/INK4B gene in patients with myelodysplastic syndrome by 5-aza-2′-deoxycytidine (decitabine) treatment. Blood 100, 2957-2964 (2002).
44. Lubbert M, Wijermans P, Kunzmann R et al. Cytogenetic responses in high-risk myelodysplastic syndrome following low-dose treatment with the DNA methylation inhibitor 5-aza-2′ -deoxycytidine. Br. J. Haematol. 114, 349-357 (2001).
45. Sigalotti L, Altomonte M, Colizzi F et al. 5-aza-2′-deoxycytidine (decitabine) treatment of hematopoietic malignancies: a multimechanism therapeutic approach? Blood 101, 4644-4645 (2003).
46. DeSimone J, Koshy M, Dorn L et al. Maintenance of elevated fetal hemoglobin levels by decitabine during dose interval treatment of sickle cell anemia. Blood 99, 3905-3908 (2002).
47. Saunthararajah Y, Hillery CA, Lavelle D et al. Effects of 5-aza-2′-deoxycytidine on fetal hemoglobin levels, red cell adhesion and hematopoietic differentiation in patients with sickle cell disease. Blood 102, 3865-3870 (2003).
48. Willemze R. Suciu S, Archimbaud E et al. A randomized Phase II study on the effects of 5-aza-2′-deoxycytidine combined with either amsacrine or idarubicin in patients with relapsed acute leukemia: an EORTC Leukemia Cooperative Group Phase II study (06893). Leukemia 11 (Suppl. 1), S24-S27 (1997).
49. Schwartzmann G, Fernandes MS, Schaan MD et al. Decitabine (5-aza-2′-deoxycytidine; DAC) plus daunorubicin as a first line treatment in patients with acute myeloid leukemia: preliminary observations. Leukemia 11 (Suppl. 1), S28-S31 (1997).
50. Aparicio A, Eads CA, Leong LA et al. Phase I trial of continuous infusion 5-aza-2′-deoxycytidine. Cancer Chemother. Pharmacol. 51, 231-239 (2003).
51. Pohlmann P, DiLione LP, Cancella AL et al. Phase II trial of cisplatin plus decitabine, a new DNA hypomethylating agent, in patients with advanced squamous cell carcinoma of the cervix. Am. J. Clin. Oncol. 25, 496-501 (2002).
52. Plumb JA, Finn PW, Williams RJ et al. Pharmacodynamic response and inhibition of growth of human tumor xenografts by the novel histone deacetylase inhibitor PXD101. Mol. Cancer Ther. 2, 721-728 (2003).
53. Schwartzmann G, Schunemann H, Gorini CNF et al. A Phase I trial of cisplatin plus decitabine, a new DNA-hypomethylating agent, in patients with advanced solid tumors and a follow-up early Phase II evaluation in patients with inoperable non-small cell lung cancer. Invest. New Drugs 18, 83-91 (2000).
54. Frost P, Abbruzzese JL, Hunt B, Lee D, Ellis M. Synergistic cytotoxicity using 2′-deoxy-5-azacytidine and cisplatin or 4-hydroperoxycyclophosphamide with human tumor cells. Cancer Res. 50, 4572-4577 (1990).
55. Momparler RL, Dore BT, Momparler LF. Effect of 5-aza-2′-deoxycytidine and retinoic acid on differentiation and c-myc expression in HL-60 myeloid leukemic cells. Cancer Lett. 54, 21-28 (1990).
56. Ellerhorst JA, Frost P, Abbruzzese JL, Newman RA, Chernajovsky Y. 2′-deoxy-5-azacytidine increases binding of cisplatin to DNA by a mechanism independent of DNA hypomethylation. Br. J. Cancer 67, 209-215 (1993).
57. Links M, Brown R. Clinical relevance of the molecular mechanisms or resistance to anti-cancer drugs. Expert Rev. Mol. Med. 1999, 1-21 (1999).
58. Kantharidis P, El-Osta A, deSilva M et al. Altered methylation of the human MDR1 promoter is associated with acquired multidrug resistance. Clin. Cancer Res. 3, 2025-2032 (1997).
59. Efferth T, Futscher BW, Osieka R. 5-azacytidine modulates the response of sensitive and multidrug-resistant K562 leukemic cells to cytostatic drugs. Blood Cells Mol. Dis. 27, 637-648 (2001).
60. Ando T, Nishimura M, Oka Y. Decitabine (5-aza-2′-deoxycytidine) decreased DNA methylation and expression of MDR-1 gene in K562/ADM cells. Leukemia 14, 1915-1920 (2000).
61. 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. Nature Genet. 21, 103-107 (1999).
62. Momparler RL, Bouffard DY, Momparler LF, Dionne J, Belanger K, Ayoub J. Pilot Phase I-II study on 5-aza-2′-deoxycytidine (decitabine) in patients with metastatic lung cancer. Anticancer Drugs 8, 358-368 (1997).