Novel DNA methyltransferase-1 (DNMT1) depleting anticancer nucleosides, 4′-thio-2′-deoxycytidine and 5-aza-4′-thio-2′- deoxycytidine

Cancer Chemotherapy and Pharmacology

Volumn 74, Issue 2, 2014, Pages 291-302

  Thottassery, Jaideep V ^a,c   Sambandam, Vijaya ^a   Allan, Paula W ^a   Maddry, Joseph A ^a   Maxuitenko, Yulia Y ^a   Tiwari, Kamal ^a   Hollingshead, Melinda ^b   Parker, William B ^a,c  

^a SOUTHERN RESEARCH INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Azacytidine; Decitabine; Deoxycytidine; DNA methyltransferase; DNMT1; Zebularine

Indexed keywords

4' THIO' 2' DEOXYCYTIDINE; 5 AZA 4' THIO' 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; DEOXYCYTIDINE; DNA METHYLTRANSFERASE 1; NUCLEOSIDE DERIVATIVE; PROTEIN P15; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CELL VIABILITY; COLON CARCINOMA; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; DRUG EFFICACY; DRUG HALF LIFE; DRUG METABOLISM; DRUG SYNTHESIS; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; LEUKEMIA CELL LINE; LUNG CARCINOMA; MOUSE; NONHUMAN; OVARY TUMOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEPLETION; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; AZACITIDINE; BLOTTING, WESTERN; CELL PROLIFERATION; DEOXYCYTIDINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA, NEOPLASM; FEMALE; HUMANS; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; REAL-TIME POLYMERASE CHAIN REACTION; THIONUCLEOSIDES; TUMOR CELLS, CULTURED;

EID: 84907598834     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-014-2503-z     Document Type: Article

References (37)

1. Brown KD, Robertson KD (2007) DNMT1 knockout delivers a strong blow to genome stability and cell viability. Nat Genet 39:289-290 (Pubitemid 46328481)
2. Esteller M, Corn PG, Baylin SB, Herman JG (2001) A gene hypermethylation profile of human cancer. Cancer Res 61:3225-3229 (Pubitemid 32695003)
3. Jones PA, Baylin SB (2007) The epigenomics of cancer. Cell 128:683-692 (Pubitemid 46273572)
4. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6:107-116 (Pubitemid 43361543)
5. Ooi SK, O'Donnell AH, Bestor TH (2009) Mammalian cytosine methylation at a glance. J Cell Sci 122:2787-2791
6. Wu J, Issa JP, Herman J, Bassett DE Jr, Nelkin BD, Baylin SB (1993) Expression of an exogenous eukaryotic DNA methyltransferase gene induces transformation of NIH 3T3 cells. Proc Natl Acad Sci USA 90:8891-8895 (Pubitemid 23306416)
7. Vertino PM, Issa JP, Pereira-Smith OM, Baylin SB (1994) Stabilization of DNA methyltransferase levels and CpG island hypermethylation precede SV40-induced immortalization of human fibroblasts. Cell Growth Differ 5:1395-1402 (Pubitemid 24381529)
8. Bakin AV, Curran T (1999) Role of DNA 5-methylcytosine transferase in cell transformation by fos. Science 283:387-390
9. Robert MF, Morin S, Beaulieu N, Gauthier F, Chute IC, Barsalou A, MacLeod AR (2003) DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat Genet 33:61-65 (Pubitemid 36068683)
10. Laird PW, Jackson-Grusby L, Fazeli A, Dickinson SL, Jung WE, Li E, Weinberg RA, Jaenisch R (1995) Suppression of intestinal neoplasia by DNA hypomethylation. Cell 81:197-205
11. Belinsky SA, Klinge DM, Stidley CA, Issa JP, Herman JG, March TH, Baylin SB (2003) Inhibition of DNA methylation and histone deacetylation prevents murine lung cancer. Cancer Res 63:7089-7093 (Pubitemid 37413444)
12. Milutinovic S, Knox JD, Szyf M (2000) DNA methyltransferase inhibition induces the transcription of the tumor suppressor p21(WAF1/CIP1). J Biol Chem 275:6353-6359 (Pubitemid 30129929)
13. Milutinovic S, Brown SE, Zhuang Q, Szyf M (2004) DNA methyltransferase 1 knock down induces gene expression by a mechanism independent of DNA methylation and histone deacetylation. J Biol Chem 279:27915-27927 (Pubitemid 38900060)
14. Egger G, Jeong S, Escobar SG, Cortez CC, Li TW, Saito Y, Yoo CB, Jones PA, Liang G (2006) Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc Natl Acad Sci USA 103:14080-14085 (Pubitemid 44452983)
15. Agoston AT, Argani P, Yegnasubramanian S, De Marzo AM, Ansari-Lari MA, Hicks JL, Davidson NE, Nelson WG (2005) Increased protein stability causes DNA methyltransferase 1 dysregulation in breast cancer. J Biol Chem 280:18302-18310 (Pubitemid 41389076)
16. Zhou Q, Agoston AT, Atadja P, Nelson WG, Davidson NE (2008) Inhibition of histone deacetylases promotes ubiquitin-dependent proteasomal degradation of DNA methyltransferase 1 in human breast cancer cells. Mol Cancer Res 6:873-883
17. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T, Jacob ST (2005) 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 25:4727-4741 (Pubitemid 40705775)
18. Patel K, Dickson J, Din S, Macleod K, Jodrell D, Ramsahoye B (2010) Targeting of 5-aza-2′-deoxycytidine residues by chromatin-associated DNMT1 induces proteasomal degradation of the free enzyme. Nucleic Acids Res 38:4313-4324
19. Santi DV, Norment A, Garrett CE (1984) Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc Natl Acad Sci USA 81:6993-6997 (Pubitemid 15216684)
20. Beumer JH, Parise RA, Newman EM, Doroshow JH, Synold TW, Lenz HJ, Egorin MJ (2008) Concentrations of the DNA methyltransferase inhibitor 5-fluoro-2′-deoxycytidine (FdCyd) and its cytotoxic metabolites in plasma of patients treated with FdCyd and tetrahydrouridine. Cancer Chemother Pharmacol 62:363-368 (Pubitemid 351692084)
21. Marquez VE, Barchi JJ Jr, Kelley JA, Rao KV, Agbaria R, Ben-Kasus T, Cheng JC, Yoo CB, Jones PA (2005) Zebularine: a unique molecule for an epigenetically based strategy in cancer chemotherapy. The magic of its chemistry and biology. Nucleosides, Nucleotides Nucleic Acids 24:305-318 (Pubitemid 41440605)
22. Parker WB, Shaddix SC, Rose LM, Waud WR, Shewach DS, Tiwari KN, Secrist JA III (2000) Metabolism of 4′-thio-beta-Darabinofuranosylcytosine in CEM cells. Biochem Pharmacol 60:1925-1932
23. Thottassery JV, Tiwari KN, Westbrook L, Secrist JA III, Parker WB (2011) Novel 2′-deoxycytidine analogs as DNA demethylation agents. Proc Am Assoc Cancer Res 71:2537. doi:10.1158/1538-7445.AM2011-2537
24. Secrist JA III, Tiwari KN, Riordan JM, Montgomery JA (1991) Synthesis and biological activity of 2′-deoxy-4′-thio pyrimidine nucleosides. J Med Chem 34:2361-2366
25. Tiwari KN, Cappellacci L, Montgomery JA, Secrist JA III (2003) Synthesis and anti-cancer activity of some novel 5-azacytosine nucleosides. Nucleosides, Nucleotides Nucleic Acids 22:2161-2170 (Pubitemid 37523720)
26. Someya H, Shaddix SC, Tiwari KN, Secrist JA III, Parker WB (2003) Phosphorylation of 4′-thio-beta-D-arabinofuranosylcytosine and its analogs by human deoxycytidine kinase. J Pharmacol Exp Ther 304:1314-1322 (Pubitemid 36254447)
27. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93:9821-9826 (Pubitemid 26296693)
28. Dodge JE, Munson C, List AF (2001) KG-1 and KG-1a model the p15 CpG island methylation observed in acute myeloid leukemia patients. Leuk Res 25:917-925 (Pubitemid 32776583)
29. Kumar S, Horton JR, Jones GD, Walker RT, Roberts RJ, Cheng X (1997) DNA containing 4′-thio-2′-deoxycytidine inhibits methylation by HhaI methyltransferase. Nucleic Acids Res 25:2773-2783 (Pubitemid 27299791)
30. Herman JG, Civin CI, Issa JP, Collector MI, Sharkis SJ, Baylin SB (1997) Distinct patterns of inactivation of p15INK4B and p16INK4A characterize the major types of hematological malignancies. Cancer Res 57:837-841 (Pubitemid 27098005)
31. Dodge JE, List AF, Futscher BW (1998) Selective variegated methylation of the p15 CpG island in acute myeloid leukemia. Int J Cancer 78:561-567 (Pubitemid 28507178)
32. Verri A, Focher F, Duncombe RJ, Basnak I, Walker RT, Coe PL, de Clercq E, Andrei G, Snoeck R, Balzarini J, Spadari S (2000) Anti-(herpes simplex virus) activity of 4′-thio-2′-deoxyuridines: a biochemical investigation for viral and cellular target enzymes. Biochem J 351(Pt 2):319-326
33. Rogstad DK, Herring JL, Theruvathu JA, Burdzy A, Perry CC, Neidigh JW, Sowers LC (2009) Chemical decomposition of 5-aza-2′-deoxycytidine (Decitabine): kinetic analyses and identification of products by NMR, HPLC, and mass spectrometry. Chem Res Toxicol 22:1194-1204
34. Esteve PO, Chin HG, Benner J, Feehery GR, Samaranayake M, Horwitz GA, Jacobsen SE, Pradhan S (2009) Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc Natl Acad Sci USA 106:5076-5081
35. Parker WB, Shaddix SC, Rose LM, Tiwari KN, Montogmery JA, Secrist JA III, Bennett L Jr (1995) Metabolism and metabolic actions of 4′-thiothymidine in L1210 cells. Biochem Pharmacol 50:687-695
36. Someya H, Waud WR, Parker WB (2006) Long intracellular retention of 4′-thio-arabinofuranosylcytosine 5′-triphosphate as a critical factor for the anti-solid tumor activity of 4′-thio- arabinofuranosylcytosine. Cancer Chemother Pharmacol 57:772-780
37. Richardson KA, Vega TP, Richardson FC, Moore CL, Rohloff JC, Tomkinson B, Bendele RA, Kutcha RD (2004) Polymerization of the triphosphates of araC, 2′,2′-difluorodeoxycytidine (dFdC) and OSI-7836 (T-araC)by human DNA polymerase alpha and DNA primase. Biochem Pharmacol 68:2337-2346 (Pubitemid 39535106)