Mammalian 3-methyladenine DNA glycosylase protects against the toxicity and clastogenicity of certain chemotherapeutic DNA cross-linking agents

Cancer Research

Volumn 58, Issue 17, 1998, Pages 3965-3973

  Allan, James M ^a   Engelward, Bevin P ^a,c   Dreslin, Andrew J ^a   Wyatt, Michael D ^a   Tomasz, Maria ^b   Samson, Leona D ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CARMUSTINE; CHLORAMBUCIL; CHLORMETHINE; DNA GLYCOSYLTRANSFERASE; MELPHALAN; MESYLIC ACID METHYL ESTER; MITOMYCIN C; PROTEIN P53;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL KILLING; CELL PROTECTION; CHROMOSOME ABERRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DNA ALKYLATION; DNA CROSS LINKING; DNA REPAIR; EMBRYO CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SISTER CHROMATID EXCHANGE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; CARMUSTINE; CELL SURVIVAL; DNA GLYCOSYLASES; DNA REPAIR; G2 PHASE; GUANINE; HUMANS; MICE; MITOMYCIN; MITOSIS; MUTAGENS; N-GLYCOSYL HYDROLASES;

EID: 0032170023     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Kaldor, J. M., Day, N. E., Band, P., Choi, N. W., Clarke, E. A., Coleman, M. P., Hakama, M., Koch, M., Langmark, F., Neal, F. E., Pettersson, F., Pompe-Kim, V., Prior, P., and Storm, H. H. Second malignancies following testicular cancer, ovarian cancer, and Hodgkin's disease: an international collaborative study among cancer registries. Int. J. Cancer, 39: 571-585, 1987.
2. Swerdlow, A. J., Douglas, A. J., and Hudson, C. V. Risk of second primary cancers after Hodgkin's disease by type of treatment: analysis of 2846 patients in the British National Lymphoma Investigation: relationships to host factors, histology and stage of Hodgkin's disease, and splenectomy. Br. Med. J., 304: 1137-1143, 1992.
3. Erickson, L. C., Laurent, G., Sharkey, N. A., and Kohn, K. W. DNA cross-linking and monoadduct repair in nitrosourea-treated human tumour cells. Nature (Lond.), 288: 727-729, 1980.
4. 6-methylguanine-DNA methyltransferase (MGMT) on the cytotoxic and recombinogenic activity of different antineoplastic drugs. Int. J. Cancer, 65: 506-512, 1996.
5. 6-alkylguanine alkyltransferase activity and sensitivity to alkylation-induced sister chromatid exchanges in human lymphoblastoid cells. Carcinogenesis (Lond.), 10: 681-685, 1989.
6. 6-alkylguanine DNA adducts in glioma-derived human cells that are resistant to the cytotoxic and cytogenetic effects of 1,3-bis(2-chloroethyl)-1-nitrosourea. Carcinogenesis (Lond.), 7: 879-883, 1986.
7. 6-alkylguanine-DNA alkyltransferase activity based on cellular DNA content in human, rat and mouse tissue. Carcinogenesis (Lond.), 7: 745-749, 1986.
8. Moritz, T., Mackay, W., Glassner, B. J., Williams, D. A., and Samson, L. Retrovirus-mediated expression of a DNA repair protein in bone marrow protects hematopoietic cells from nitrosourea-induced toxicity in vitro and in vivo. Cancer Res., 55: 2608-2614, 1995.
9. Schabel, F. M., Jr. Nitrosoureas: a review of experimental antitumour activity. Cancer Treat. Rep., 60: 665-698, 1976.
10. Maze, R., Carney, J. P., Kelley, M. R., Glassner, B. J., Williams, D. A., and Samson, L. D. Increasing DNA repair methyltransferase levels via bone marrow stem cell transduction rescues mice from the toxic effects of 1,3-bis(2-chloroethyl)-1-nitrosourea, a chemotherapeutic alkylating agent. Proc. Natl. Acad. Sci. USA, 93: 206-210, 1996.
11. Davis, B. M., Reese, R. J., Koc, O. N., Lee, K., Schupp, J. E., and Gerson, S. L. Selection for G156A O-6-methylguanine DNA methyltransferase gene-induced hematopoietic progenitors and protection from lethality in mice treated with O-6-benzylguanine and 1,3-bis(2-chloroethyl)-1-nitrosourea. Cancer Res., 57: 5093-5099, 1997.
12. Wang, G., Weiss, C., Sheng, P. H., and Bresnick, E. Retrovirus-mediated transfer of the human O-6-methylguanine-DNA methyltransferase gene into a murine hematopoietic stem cell line and resistance to the toxic effects of certain alkylating agents. Biochem. Pharmacol., 51: 1221-1228, 1996.
13. 6-benzylguanine potentiates the in vivo toxicity and clastogenicity of temozolomide and BCNU in mouse bone marrow. Blood, 89: 1566-1573, 1997.
14. Dolan, M. E., Mitchell, R. B., Mummert, C., Moschel, R. C., and Pegg, A. E. Effect of O6-benzylguanine analogues on sensitivity of human tumor cells to the cytotoxic effects of alkylating agents. Cancer Res., 51: 3367-3372, 1991.
15. 6-methylguanine-DNA methyltransferases. J. Biol. Chem., 269: 730-733, 1994.
16. 4-methylthymine. J. Biol. Chem., 266: 2767-2771, 1991.
17. 4 MeT from nucleotide excision repair. Carcinogenesis (Lond.), 18: 919-924, 1997.
18. Lawley, P. D., and Phillips, D. H. DNA adducts from chemotherapeutic agents. Mutat. Res., 355: 13-40, 1996.
19. Ludlum, D. B. DNA alkylation by the haloethylnitrosoureas: nature of modifications produced and their enzymatic repair or removal. Mutat. Res., 233: 117-126, 1990.
20. Singer, B., and Hang, B. What structural features determine repair enzyme specificity and mechanism in chemically modified DNA. Chem. Res. Toxicol., 10: 713-732, 1997.
21. Bessho, T., Roy, R., Yamamoto, K., Kasai, H., Nishimura, S., Tano, K., and Mitra, S. Repair of 8-hydroxyguanine in DNA by mammalian N-methylpurine-DNA glycosylase. Proc. Natl. Acad. Sci. USA, 90: 8901-8904, 1993.
22. Dosanjh, M. K., Roy, R., Mitra, S., and Singer, B. 1,N6-ethenoadenine is preferred over 3-methyladenine as a substrate by a cloned human N-methylpurine-DNA glycosylase (3-methyladenine-DNA glycosylase). Biochemistry, 33: 1624-1628, 1994.
23. Saparbaev, M., and Laval, J. Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylase. Proc. Natl. Acad. Sci. USA, 91: 5873-5877, 1994.
24. Saparbaev, M., Kleibl, K., and Laval, J. Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1, N6-ethenoadenine when present in DNA. Nucleic Acids Res., 23: 3750-3755, 1995.
25. Singer, B., Antoccia, A., Basu, A. K., Dosanjh, M. K., Fraenkel-Conrat, H., Gallagher, P. E., Kusmierek, J. T., Qui, Z-H., and Rydberg, B. Both purified human 1-N6-ethenoadenine-binding protein and purified human 3-methyladenine-DNA glycosylase act on 1 N6-ethenoadenine and 3-methyladenine. Proc. Natl. Acad. Sci. USA, 89: 9386-9390, 1992.
26. Engelward, B. P., Boosalis, M. S., Chen, B. J., Deng, Z., Siciliano, M. J., and Samson, L. D. Cloning and characterization of a mouse 3-methyladenine/7-methylguanine/3-methylguanine DNA glycosylase cDNA whose gene maps to chromosome 11. Carcinogenesis (Lond.), 14: 175-181, 1993.
27. Engelward, B. P., Weeda, G., Wyatt, M. D., Broekhof, J. L. M., de Wit, J., Donker, I., Allan, J. M., Gold, B., Hoeijmakers, J. H. J., and Samson, L. D. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. USA, 94: 13087-13092, 1997.
28. Mattes, W. B., Lee, C-S., Laval, J., and O'Connor, T. R. Excision of DNA adducts of nitrogen mustards by bacterial and mammalian 3-methyladenine DNA glycosylases. Carcinogenesis (Lond.), 17: 643-648, 1996.
29. Matijasivec, Z., Boosalis, M., Mackay, W., Samson, L., and Ludlum, D. B. Protection against chloroethylnitrosourea cytotoxicity by eukaryotic 3-methyladenine DNA glycosylase. Proc. Natl. Acad. Sci. USA, 90: 11855-11859, 1993.
30. Engelward, B. P., Dreslin, A., Christensen, J., Huszar, D., Kurahara, C., and Samson, L. Repair-deficient 3-methyladenine DNA glycosylase homozygous mutant mouse cells have increased sensitivity to alkylation-induced chromosome damage and cell killing. EMBO J., 15: 945-952, 1996.
31. Mereau, A., Grey, L., Piquet-Pellorce, C., and Heath, J. K. Characterization of a binding protein for leukemia inhibitory factor localized in extracellular matrix. J. Cell. Biol., 122: 713-719, 1993.
32. Perry, P., and Wolff, S. New Giemsa method for the differential staining of sister chromatids. Nature (Lond.), 251: 156-158, 1974.
33. Natajaran, A. T., and Obe, G. Molecular mechanisms involved in the production of chromosomal aberrations. III. Restriction endonucleases. Chromosoma, 90: 120-127, 1984.
34. Nicoletti, I., Migliorati, G., Pagliacci, M, C., Grignami, F., and Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods, 139: 271-279, 1991.
35. Tomasz, M., Chawla, A. K., and Lipman, R. Mechanism of monofunctional and bifunctional alkylation of DNA by mitomycin C. Biochemistry, 27: 3182-3187, 1988.
36. Tomasz, M., Lipman, R., McGuinness, B. F., and Nakanishi, K. Isolation and characterization of a major adduct between mitomycin C and DNA. J. Am. Chem. Soc., 110: 5892-5896, 1988.
37. Kumar, G. S., Lipman, R., Cummings, J., and Tomasz, M. Mitomycin C-DNA adducts generated by DT-diaphorase: revised mechanism of the enzymatic reductive activation of mitomycin C. Biochemistry, 36: 14128-14136, 1997.
38. Tomasz, M., Lipman, R., Chowdary, D., Pawlak, J., Verdine, G. L., and Nakanishi, K. Isolation and structure of a covalent cross-link adduct between mitomycin C and DNA. Science (Washington DC), 235: 1204-1208, 1987.
39. Bizanek, R., McGuinness, B. F., Nakanishi, K., and Tomasz, M. Isolation and structure of an intrastrand cross-link adduct of mitomycin C and DNA. Biochemistry, 31: 3084-3091, 1992.
40. Bachur, N. R., Gordon, S. L., and Gee, M. V. A general mechanism for microsomal activation of quinone anticancer agents to free radicals. Cancer Res., 38: 1745-1750, 1978.
41. Bachur, N. R., Gordon, S. L., Gee, M. V., and Kon, H. NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proc. Natl. Acad. Sci. USA, 76: 954-957, 1979.
42. Pristos, C. A., and Sartorelli, A. C. Generation of reactive oxygen radicals through bioactivation of mitomycin antibiotics. Cancer Res., 46: 3528-3532, 1986.
43. 2 generation during the redox cycle of mitomycin C and DNA-bound mitomycin C. Chem. Biol. Interact., 13: 89-97, 1976.
44. Engelward, B. P., Allan, J. M., Dreslin, A. J., Kelly, J. D., Wu, M., Gold, B., and Samson, L. D. A chemical and genetic approach together define the biological consequences of 3-methyladenine lesions in the mammalian genome. J. Biol. Chem., 273: 5412-5418, 1998.
45. Clarke, P. R., Purdie, C. A., Harrison, D. J., Morris, R. G., Bird, C. C., Hooper, M. L., and Wyllie, A. H. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature (Lond.), 362: 849-852, 1993.
46. Kumar, G. S., Johnson, W. S., and Tomasz, M. Orientation isomers of the mitomycin C interstrand cross-link in non-self-complementary DNA. Biochemistry, 32: 1364-1372, 1993.
47. Sasaki, M. S., and Tonomura, A. A high susceptibility of Fanconi's anemia to chromosome breakage by DNA cross-linking agents. Cancer Res., 33: 1829-1836, 1973.
48. Dutrillaux, B., Aurias, A., Dutrillaux, A. M., Buriot, D., and Prieur, M. The cell cycle of lymphocytes in Fanconi anemia. Hum. Genet., 62: 327-332, 1982.
49. Kubbies, M., Schindler, D., Hoehm, H., Schinzel, A., and Rabinovitch, P. S. Endogenous blockage and delay of the chromosome cycle despite normal recruitment and growth phase explain poor proliferation and frequent endomitosis in Fanconi anemia cells. Am. J. Hum. Genet., 37: 1022-1030, 1985.
50. Kruyt, F. A. E., Dijkmans, L. M., van den Berg, T. K., and Joenje, H. Fanconi anemia genes act to suppress a cross-linker-inducible p53-independent apoptosis pathway in lymphoblastoid cell lines. Blood, 87: 938-948, 1996.
51. Ridet, A., Guillouf, C., Duchaud, E., Cundari, E., Fiore, M., Moustacchi, E., and Rosselli, F. Deregulated apoptosis is a hallmark of the Fanconi anemia syndrome. Cancer Res., 57: 1722-1730, 1997.
52. Dizdaroglu, M. Oxidative damage to DNA in mammalian chromatin. Mutat. Res., 275: 331-342.
53. 1-deoxyguanosyl]-ethane, in DNA treated with. N. N′-bis-(2-chloroethyl)-N-nitrosourea (BCNU). Cancer Res., 42: 3102-3105, 1982.
54. Carter, C. A., Habraken, Y., and Ludlum, D. B. Release of 7-alkylguanines from haloethylnitrosourea-treated DNA by E. coli 3-methyladenine-DNA glycosylase II. Biochem. Biophys. Res. Commun., 155: 1261-1265.
55. Habraken, Y., Carter, C. A., Kirk, M. C., and Ludlum, D. B. Release of 7-alkylguanines from N-(2-chloroethyl)-N′-cyclohexyl-N-nitrosourea-modified DNA by 3-methyladenine DNA glycosylase II. Cancer Res., 51: 499-503, 1991.
56. Weksberg, R., Buchwald, M., Sargent, P., Thompson, M. W., and Siminovitch, L. Specific cellular defects in patients with Fanconi anemia. J. Cell Physiol., 101: 311-324, 1979.
57. Miura, K., Morimoto, K., and Koizumi, A. Proliferative kinetics and mitomycin C-induced chromosome damage in Fanconi's anemia lymphocytes. Hum. Genet., 63: 19-23, 1983.