6-thioguanine perturbs cytosine methylation at the CpG dinucleotide site by DNA methyltransferases in vitro and acts as a DNA demethylating agent in vivo

Biochemistry

Volumn 48, Issue 10, 2009, Pages 2290-2299

  Wang, Hongxia ^a   Wang, Yinsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6-THIOGUANINE; ACUTE LYMPHOBLASTIC LEUKEMIAS; CHEMOTHERAPEUTIC AGENTS; COMPLEMENTARY STRANDS; CYTOTOXIC EFFECTS; DINUCLEOTIDE; DNA METHYLTRANSFERASES; GENE REGULATIONS; HUMAN DISEASE; IN-VITRO; IN-VIVO; LC-MS/MS; METHYLTRANSFERASE; RESTRICTION ENZYMES; T CELLS;

AGENTS; DNA; ENZYMES; GENES; METHYLATION; NUCLEIC ACIDS;

ALKYLATION;

ANTIINFECTIVE AGENT; CPG OLIGODEOXYNUCLEOTIDE; CYTOSINE; DINUCLEOTIDE; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; MERCAPTOPURINE; METHYLTRANSFERASE; RESTRICTION ENDONUCLEASE; TIOGUANINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; BACTERIAL GENE; BACTERIUM; DIGESTION; DNA METHYLATION; DRUG STRUCTURE; EPIGENETICS; GENE CONTROL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; LIQUID CHROMATOGRAPHY; LYMPHATIC LEUKEMIA; MASS SPECTROMETRY; METHODOLOGY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

AZACITIDINE; CYTOSINE; DINUCLEOSIDE PHOSPHATES; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-CYTOSINE METHYLASES; HUMANS; JURKAT CELLS; OLIGODEOXYRIBONUCLEOTIDES; TANDEM MASS SPECTROMETRY; THIOGUANINE;

BACTERIA (MICROORGANISMS);

EID: 64349105024     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801467z     Document Type: Article

References (37)

1. Elion, G. B. (1989) The purine path to chemotherapy. Science 244, 41-47.
2. Pui, C. H., and Evans, W. E. (1998) Acute lymphoblastic leukemia. N. Engl. J. Med. 339, 605-615.
3. Swann, P. F., Waters, T. R., Moulton, D. C., Xu, Y. Z., Zheng, Q. G., Edwards, M., and Mace, R. (1996) Role of postreplicative DNA mismatch repair in the cytotoxic action of thioguanine. Science 273, 1109-1111.
4. O'Donovan, P., Perrett, C. M., Zhang, X. H., Montaner, B., Xu, Y. Z., Harwood, C. A., McGregor, J. M., Walker, S. L., Hanaoka, F., and Karran, P. (2005) Azathioprine and UVA light generate mutagenic oxidative DNA damage. Science 309, 1871-1874.
5. Gu, C., and Wang, Y. (2007) In vitro replication and thermodynamic studies of methylation and oxidation modifications of 6-thioguanine. Nucleic Acids Res. 35, 3693-3704.
6. Zhang, X. H., Jeffs, G, Ren, X. L., O'Donovan, P., Montaner, B., Perrett, C. M., Karran, P., and Xu, Y. Z. (2007) Novel DNA lesions generated by the interaction between therapeutic thiopurines and UVA light. DNA Repair 6, 344-354.
7. 6-methylthioguanine, and guanine-S 6-sulfonic acid. J. Biol. Chem. 283, 23665-23670.
8. Waters, T. R., and Swann, P. F. (1997) Cytotoxic mechanism of 6-thioguanine: hMutS alpha, the human mismatch binding het-erodimer, binds to DNA containing S-6-methylthioguanine. Biochemistry 36, 2501-2506.
9. Robertson, K. D., and Wolffe, A. P. (2000) DNA methylation in health and disease. Nat. Rev. Genet. 1, 11-19.
10. Bestor, T. H. (2000) The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402.
11. Hendrich, B., and Bird, A. (1998) Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 18, 6538-6547.
12. Klose, R. J., and Bird, A. P. (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89-97.
13. Turk, P. W., Laayoun, A., Steven, S. S., and Weitzman, S. A. (1995) DNA adduct 8-hydroxyl-2'-deoxyguanosine (8-hydrox-yguanine) affects function of human DNA methyltransferase. Carcinogenesis 16, 1253-1255.
14. Weitzman, S. A. T., Milkowski, P. W., Howard, D., and Kozlowski, K. (1994) Free radical adducts induce alterations in DNA cytosine methylation. Proc. Natl. Acad. Sci. U.S.A. 91, 1261-1264.
15. Tan, N. W., and Li, B. F. (1990) Interaction of oligonucleotides containing 6-O-methylguanine with human DNA (cytosine-5-)-methyltransferase. Biochemistry 29, 9234-9240.
16. Smith, S. S., Kan, J. L., Baker, D. J., Kaplan, B. E., and Dembek, P. (1991) Recognition of unusual DNA structures by human DNA (cytosine-5) methyltransferase. J. Mol. Biol. 217, 39-51.
17. Subach, O. M., Maltseva, D. V., Shastry, A., Kolbanovskiy, A., Klimasauskas, S., Geacintov, N. E., and Gromova, E. S. (2007) The stereochemistry of benzo[a]pyrene-2 '-deoxyguanosine adducts affects DNA methylation by SssI and HhaI DNA methyltransferases. FEBS J. 274, 2121-2134.
18. Valinluck, V., and Sowers, L. C. (2007) Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res. 67, 946-950.
19. Ling, Y. H., Chan, J. Y., Beattie, K. L., and Nelson, J. A. (1992) Consequences of 6-thioguanine incorporation into DNA on polymerase, ligase, and endonuclease reactions. Mol. Pharmacol. 42, 802-807.
20. Krynetskaia, N. F., Krynetski, E. Y., and Evans, W. E. (1999) Human RNase H-mediated RNA cleavage from DNA-RNA duplexes is inhibited by 6-deoxythioguanosine incorporation into DNA. Mol. Pharmacol. 56, 841-848.
21. Krynetskaia, N. F., Cai, X., Nitiss, J. L., Krynetski, E. Y., and Relling, M. V. (2000) Thioguanine substitution alters DNA cleavage mediated by topoisomerase II. FASEB J. 14, 2339-2344.
22. Quint, A., and Cedar, H. (1981) In vitro methylation of DNA with Hpa II methylase. Nucleic Acids Res. 9, 633-646.
23. Yoder, J. A., Soman, N. S., Verdine, G L., and Bestor, T. H. (1997) DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 270, 385-395.
24. Apffel, A., Chakel, J. A., Fischer, S., Lichtenwalter, K., and Hancock, W. S. (1997) Analysis of oligonucleotides by HPLC-electrospray ionization mass spectrometry. Anal. Chem. 69, 1320-1325.
25. McLuckey, S. A., Vanberkel, G J., and Glish, G L. (1992) Tandem mass-spectrometry of small, multiply charged oligonucleotides. J. Am. Soc. Mass Spectrom. 3, 60-70.
26. Taylor, K. H., Pena-Hernandez, K. E., Davis, J. W., Arthur, G L., Duff, D. J., Shi, H., Rahmatpanah, F. B., Sjahputera, O., and Caldwell, C. W. (2007) Large-scale CpG methylation analysis identifies novel candidate genes and reveals methylation hotspots in acute lymphoblastic leukemia. Cancer Res. 67, 2617-2625.
27. Jones, P. A., and Taylor, S. M. (1980) Cellular differentiation, cytidine analogs and DNA methylation. Cell 20, 85-93.
28. Jones, P. A., and Baylin, S. B. (2002) The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3, 415-428.
29. Esteller, M. (2002) CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 21, 5427-5440.
30. O'Gara, M., Horton, J. R., Roberts, R. J., and Cheng, X. (1998) Structures of HhaI methyltransferase complexed with substrates containing mismatches at the target base. Nat. Struct. Biol. 5, 872-877.
31. Platts, J. A., Howard, S. T., and Bracke, B. R. F. (1996) Directionality of hydrogen bonds to sulfur and oxygen. J. Am. Chem. Soc. 118, 2726-2733.
32. Lambooy, L. H., Leegwater, P. A., van den Heuvel, L. P., Bokkerink, J. P., and De Abreu, R. A. (1998) Inhibition of DNA methylation in malignant MOLT F4 lymphoblasts by 6-mercap-topurine. Clin. Chem. 44, 556-559.
33. Hogarth, L. A., Redfern, C. P., Teodoridis, J. M., Hall, A. G., Anderson, H., Case, M. C., and Coulthard, S. A. (2008) The effect of thiopurine drugs on DNA methylation in relation to TPMT expression. Biochem. Pharmacol. 76, 1024-1035.
34. Ghoshal, K., Datta, J., Majumder, S., Bai, S., Kutay, H., Motiwala, T., and Jacob, S. T. (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.
35. Jackson-Grusby, L., Laird, P. W., Magge, S. N., Moeller, B. J., and Jaenisch, R. (1997) Mutagenicity of 5-aza-2′-deoxycytidine is mediated by the mammalian DNA methyltransferase. Proc. Natl. Acad. Sci. U.S.A. 94, 4681-4685.
36. Warren, D. J., Andersen, A., and Slordal, L. (1995) Quantitation of 6-thioguanine residues in peripheral-blood leukocyte DNA obtained from patients receiving 6-mercaptopurine-based maintenance therapy. Cancer Res. 55, 1670-1674.
37. Cuffari, C., Li, D. Y., Mahoney, J., Barnes, Y., and Bayless, T. M. (2004) Peripheral blood mononuclear cell DNA 6-thioguanine metabolite levels correlate with decreased interferon-gamma production in patients with Crohn's disease on AZA therapy. Dig. Dis. Sci. 49, 133-137.