The depletion of DNA methyltransferase-1 and the epigenetic effects of 5-aza-2'deoxycytidine (decitabine) are differentially regulated by cell cycle progression

Epigenetics

Volumn 6, Issue 8, 2011, Pages 1021-1028

  Al Salihi, Mazin ^a   Yu, Margaret ^b   Burnett, David M ^c   Alexander, Amanda ^c   Samlowski, Wolfram ^d   Fitzpatrick, F A ^e  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b Ortho Biotech Oncology Research and Development   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d NEVADA CANCER INSTITUTE   (United States)

^e KANSAS CITY UNIVERSITY OF MEDICINE AND BIOSCIENCES   (United States)

Author keywords

5 aza 2' deoxycytidine; Cell cycle; Decitabine; DNA methyltransferase 1; P53; S phase; Suicide inactivation

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA METHYLTRANSFERASE 1; MELANOMA ANTIGEN 1; MESSENGER RNA; PROTEIN P53;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL GROWTH; CELL STRAIN HCT116; CONTROLLED STUDY; CPG ISLAND; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DRUG EFFECT; DRUG MECHANISM; EPIGENETICS; GENE EXPRESSION; GENOTYPE; PROMOTER REGION; REGULATORY MECHANISM;

EID: 79961216657     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.8.16064     Document Type: Article

References (39)

1. M. Epigenetics in cancer. N Engl J Med 2008; 358:1148-59
2. Issa JP, Kantarjian HM. Targeting DNA Methylation. Clin Cancer Res 2009; 15:3938-46
3. Wijermans P, Lubbert M, Verhoef G, Bosly A, Ravoet C, Andre M, et al. Low-dose 5-aza-2'-deoxycytidine, a DNA hypomethylating agent, for the treatment of high-risk myelodysplastic syndrome: a multicenter phase II study in elderly patients. J Clin Oncol 2000; 18:956-62
4. Issa JP, Garcia-Manero G, Giles FJ, Mannari R, Thomas D, Faderl S, et al. Phase I study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-2'-deoxycytidine (Decitabine) in hematopoietic malignancies. Blood 2004; 103:1635-40
5. Samlowski WE, Leachman SA, Wade M, Cassidy P, Porter-Gill P, Busby L, et al. Evaluation of a 7-day continuous intravenous infusion of decitabine: inhibition of promoter-specific and global genomic DNA methylation. J Clin Oncol 2006; 23:3897-905
6. Aparicio A, Eads CA, Leong LA, Laird PW, Newman EM, Synold TW, et al. Phase I trial of continuous infusion 5-aza-2'-deoxycytidine. Cancer Chemother Pharmacol 2003; 51:231-9
7. Karpf AR, Moore BC, Ririe TO, Jones DA. Activation of the p53 DNA damage response pathway after inhibition of DNA methyltransferase by 5-aza-2'-deoxycytidine. Mol Pharmacol 2001; 59:751-7
8. Link PA, Baer MR, James SR, Jones DA, Karpf AR. p53-inducible ribonucleotide reductase (p53R2/ RRM2B) is a DNA hypomethylation-independent decitabine gene target that correlates with clinical response in myelodysplastic syndrome/acute myelogenous leukemia. Cancer Res 2008; 68:9358-66
9. Peller S. Clinical implications of p53: effect on prognosis, tumor progression and chemotherapy response. Semin Cancer Biol 1998; 8:379-87
10. Stewart DJ, Issa JP, Kurzrock R, Nunez MI, Jelinek J, Hong D, et al. Decitabine effect on tumor global DNA methylation and other parameters in a phase I trial in refractory solid tumors and lymphomas. Clin Cancer Res 2009; 15:3881-8
11. Creusot F, Acs G, Christman JK. Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2'-deoxycytidine. J Biol Chem 1982; 257:2041-8
12. Santi DV, Norment A, Garrett CE. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci USA 1984; 81:6993-7
13. Juttermann R, Li E, Jaenisch R. Toxicity of 5-aza-2'-deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation. Proc Natl Acad Sci USA 1994; 91:11797-801
14. 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
15. Hermann A, Goyal R, Jeltsch A. The Dnmt1 DNA- (cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem 2004; 279:48350-9
16. Velicescu M, Weisenberger DJ, Gonzales FA, Tsai YC, Nguyen CT, Jones PA. Cell division is required for de novo methylation of CpG islands in bladder cancer cells. Cancer Res 2002; 62:2378-84
17. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T, et al. 5-Aza-Deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain and nuclear localization signal. Mol Cell Biol 2005; 25:4727-41
18. Patel K, Dickson J, Din S, Macleod K, Jodrell D, Ramsahoye B. Targeting of 5-aza-2'-deoxycytidine residues by chromatin-associated DNMT1 induces proteasomal degradation of the free enzyme. Nucleic Acids Res 2010; 38:4313-24
19. Easwaran HP, Schermelleh L, Leonhardt H, Cardoso MC. Replication-independent chromatin loading of Dnmt1 during G2 and M phases. EMBO Rep 2004; 5:1181-6
20. Mortusewicz O, Schermelleh L, Walter J, Cardoso MC, Leonhardt H. Recruitment of DNA methyltransferase I to DNA repair sites. Proc Natl Acad Sci USA 2005; 102:8905-9
21. Bunz F, Hwang PM, Torrance C, Waldman T, Zhang Y, Dillehay L, et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 1999; 104:263-9
22. Appleton K, Mackay HJ, Judson I, Plumb JA, McCormick C, Strathdee G, et al. Phase I and pharmacodynamic trial of the DNA methyltransferase inhibitor decitabine and carboplatin in solid tumors. J Clin Oncol 2007; 25:4603-9
23. Robertson KD, Keyomarsi K, Gonzales FA, Velicescu M, Jones PA. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G(0)/G(1) to S phase transition in normal and tumor cells. Nucleic Acids Res 2000; 28:2108-13
24. Kimura F, Seifert HH, Florl AR, Santourlidis S, Steinhoff C, Swiatkowski S, et al. Decrease of DNA methyltransferase 1 expression relative to cell proliferation in transitional cell carcinoma. Int J Cancer 2003; 104:568-78
25. Schermelleh L, Haemmer A, Spada F, Rösing N, Meilinger D, Rothbauer U, et al. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res 2007; 35:4301-12
26. Tatematsu KI, Yamazaki T, Ishikawa F. MBD2-MBD3 complex binds to hemi-methylated DNA and forms a complex containing DNMT1 at the replication foci in late S phase. Genes Cells 2000; 5:677-88
27. Iwanaga R, Komori H, Ohtani K. Differential regulation of expression of the mammalian DNA repair genes by growth stimulation. Oncogene 2004; 23:8581-90
28. Rancourt RC, Hayes DD, Chess PR, Keng PC, O'Reilly MA. Growth Arrest in G1 Protects Against Oxygen-Induced DNA Damage and Cell Death. J Cell Physiol 2002; 193:26-36
29. Ljungman M. Activation of DNA damage signaling. Mutat Res 2005; 577:203-16
30. Snyder RD. Inhibitors of ribonucleotide reductase alter DNA repair in human fibroblasts through specific depletion of purine deoxynucleotide triphosphates. Cell Biol Toxicol 1984; 1:81-94
31. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 2001; 27:31-9
32. Aladjem MI, Spike BT, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, et al. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 1998; 8:145-55
33. Smith ML, SeoYR. p53 regulation of DNA excision repair. Mutagenesis 2002; 17:149-56
34. Zhou J, Ahn J, Wilson SH, Prives C. A role for p53 in base excision repair. EMBO J 2001; 20:914-23
35. Moll UM, Wolff S, Speidel D, Deppert W. Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 2005; 17:631-6
36. Lin RK, Wu CY, Chang JW, Juan LJ, Hsu HS, Chen CY, et al. Dysregulation of p53/Sp1 control leads to DNA methyltransferase-1 overexpression in lung cancer. Cancer Res 2010; 70:5807-17
37. Estève PO, Chin HG, Pradhan S. Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. Proc Natl Acad Sci USA 2005; 102:1000-5
38. Robertson KD. DNA methylation, methyltransferases and cancer. Oncogene 2001; 20:3139-55.
39. Karpf AR, Jones DA. Reactivating the expression of methylation silenced genes in human cancer. Oncogene 2002; 21:5496-503