The effect of 3-methyladenine DNA glycosylase-mediated DNA repair on the induction of toxicity and diabetes by the β-cell toxicant streptozotocin

Toxicological Sciences

Volumn 95, Issue 2, 2007, Pages 391-400

  Burns, Nicole ^a,b   Gold, Barry ^a,b,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

3 methyladenine; Apoptosis; Base excision repair; Streptozotocin; Type 1 diabetes

Indexed keywords

3 METHYLADENINE DNA GLYCOSYLTRANSFERASE; DNA GLYCOSYLTRANSFERASE; STREPTOZOCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DIABETOGENESIS; DNA ADDUCT; DNA REPAIR; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; MUTAGENICITY; NONHUMAN; PANCREAS ISLET BETA CELL; STREPTOZOCIN DIABETES;

ANIMALS; APOPTOSIS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DNA GLYCOSYLASES; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INSULIN-SECRETING CELLS; MALE; MICE; MICE, KNOCKOUT; STREPTOZOCIN;

MUS; RODENTIA;

EID: 33846478038     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfl164     Document Type: Article

References (40)

1. Akerblom, H. K., Vaarala, O., Hyoty, H., Ilonen, J., and Knip, M. (2002). Environmental factors in the etiology of type 1 diabetes. Am. J. Med. Genet. 115, 18-29.
2. Arison, R. N., and Feudale, E. L. (1967). Induction of renal tumour by streptozotocin in rats. Nature 214, 1254-1255.
3. Bolzan, A. D., and Bianchi, M. S. (2002). Genotoxicity of streptozotocin. Mutat. Res. 512, 121-134.
4. Burkart, V., Wang, Z. Q., Radons, J., Heller, B., Herceg, Z., Stingl, L., Wagner, E. F., and Kolb, H. (1999). Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat. Med. 5, 314-319.
5. Cardinal, J.W., Margison, G. P., Mynett, K. J., Yates, A. P., Cameron, D. P., and Elder, R. H. (2001). Increased susceptibility to streptozotocin-induced beta-cell apoptosis and delayed autoimmune diabetes in alkylpurine-DNA-N-glycosylase-deficient mice. Mol. Cell. Biol. 21, 5605-5613.
6. D'Amours, D., Desnoyers, S., D'Silva, I., and Poirier, G. G. (1999). Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 342 (Pt 2), 249-268.
7. Dor, Y., Brown, J., Martinez, O. I., and Melton, D. A. (2004). Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429, 41-46.
8. Engelward, B. P., Allan, J. M., Dreslin, A. J., Kelly, J. D., Wu, M. M., Gold, B., and Samson, L. D. (1998). A chemical and genetic approach together define the biological consequences of 3-methyladenine lesions in the mammalian genome. J. Biol. Chem. 273, 5412-5418.
9. Engelward, B. P., Dreslin, A., Christensen, J., Huszar, D., Kurahara, C., and Samson, L. (1996). 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.
10. Engelward, B. P., Weeda, G., Wyatt, M. D., Broekhof, J. L., de Wit, J., Donker, I., Allan, J. M., Gold, B., Hoeijmakers, J. H., and Samson, L. D. (1997). Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94, 13087-13092.
11. Glassner, B. J., Weeda, G., Allan, J. M., Broekhof, J. L., Carls, N. H., Donker, I., Engelward, B. P., Hampson, R. J., Hersmus, R., Hickman, et al. (1999). DNA repair methyltransferase (Mgmt) knockout mice are sensitive to the lethal effects of chemotherapeutic alkylating agents. Mutagenesis 14, 339-347.
12. Hayashi, Y., Utsuyama, M., Kurashima, C., and Hirokawa, K. (1989). Spontaneous development of organ-specific autoimmune lesions in aged C57BL/6 mice. Clin. Exp. Immunol. 78, 120-126.
13. Hickman, M. J., and Samson, L. D. (1999). Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents. Proc. Natl. Acad. Sci. U.S.A. 96, 10764-10769.
14. Iwase, M., Nunoi, K., Sadoshima, S., Kikuchi, M., and Fujishima, M. (1989). Liver, kidney and islet cell tumors in spontaneously hypertensive and normotensive rats treated neonatally with streptozotocin. Tohoku J. Exp. Med. 159, 83-90.
15. Kelly, J. D., Shah, D., Chen, F. X., Wurdeman, R., and Gold, B. (1998). Quantitative and qualitative analysis of DNA methylation at N3-adenine by N-methyl-N-nitrosourea. Chem. Res. Toxicol. 11, 1481-1486.
16. Kurrer, M. O., Pakala, S. V., Hanson, H. L., and Katz, J. D. (1997). Beta cell apoptosis in T cell-mediated autoimmune diabetes. Proc. Natl. Acad. Sci. U.S.A. 94, 213-218.
17. Liadis, N., Murakami, K., Eweida, M., Elford, A. R., Sheu, L., Gaisano, H. Y., Hakem, R., Ohashi, P. S., and Woo, M. (2005). Caspase-3-dependent beta-cell apoptosis in the initiation of autoimmune diabetes mellitus. Mol. Cell. Biol. 25, 3620-3629.
18. Masiello, P., Broca, C., Gross, R., Roye, M., Manteghetti, M., Hillaire-Buys, D., Novelli, M., and Ribes, G. (1998). Experimental NIDDM: Development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 47, 224-229.
19. Masutani, M., Suzuki, H., Kamada, N., Watanabe, M., Ueda, O., Nozaki, T., Jishage, K., Watanabe, T., Sugimoto, T., Nakagama, H., et al. (1999). Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. U.S.A. 96, 2301-2304.
20. Mathis, D., Vence, L., and Benoist, C. (2001). Beta-cell death during progression to diabetes. Nature 414, 792-798.
21. Mensah-Brown, E. P., Stosic Grujicic, S., Maksimovic, D., Jasima, A., Shahin, A., and Lukic, M. L. (2002). Downregulation of apoptosis in the target tissue prevents low-dose streptozotocin-induced autoimmune diabetes. Mol. Immunol. 38, 941-946.
22. Murata, M., Takahashi, A., Saito, I., and Kawanishi, S. (1999). Site-specific DNA methylation and apoptosis: Induction by diabetogenic streptozotocin. Biochem. Pharmacol. 57, 881-887.
23. Nakamura, T., Terajima, T., Ogata, T., Ueno, K., Hashimoto, N., Ono, K., and Yano, S. (2006). Establishment and pathophysiological characterization of type 2 diabetic mouse model produced by streptozotocin and nicotinamide. Biol. Pharm. Bull. 29, 1167-1174.
24. Nelson, J. W., Ledoux, S. P., and Wilson, G. L. (1993). Repair of O6-methylguanine in rat pancreatic beta-cells after exposure to N-methyl-N-nitrosourea. Diabetes 42, 1187-1194.
25. Nichols, W. K., Spellman, J. B., Vann, L. L., and Daynes, R. A. (1979). Immune responses of diabetic animals. Direct immunosuppressant effects of streptozotocin in mice. Diabetologia 16, 51-57.
26. O'Brien, B. A., Harmon, B. V., Cameron, D. P., and Allan, D. J. (1996). Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J. Pathol. 178, 176-181.
27. O'Brien, B. A., Harmon, B. V., Cameron, D. P., and Allan, D. J. (1997). Apoptosis is the mode of beta-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse. Diabetes 46, 750-757.
28. Pieper, A. A., Brat, D. J., Krug, D. K., Watkins, C. C., Gupta, A., Blackshaw, S., Verma, A., Wang, Z. Q., and Snyder, S. H. (1999). Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. U.S.A. 96, 3059-3064.
29. Rakieten, N., Gordon, B. S., Beaty, A., Cooney, D. A., Davis, R. D., and Schein, P. S. (1971). Pancreatic islet cell tumors produced by the combined action of streptozotocin and nicotinamide. Proc. Soc. Exp. Biol. Med. 137, 280-283.
30. Rakieten, N., Gordon, B. S., Cooney, D. A., Davis, R. D., and Schein, P. S. (1968). Renal tumorigenic action of streptozotocin (NSC-85998) in rats. Cancer Chemother. Rep. 52, 563-567.
31. Reese, J. S., Qin, X., Ballas, C. B., Sekiguchi, M., and Gerson, S. L. (2001). MGMT expression in murine bone marrow is a major determinant of animal survival after alkylating agent exposure. J. Hematother. Stem Cell Res. 10, 115-123.
32. Robertson, R. P. (2004). Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 279, 42351-42354.
33. Roth, R. B., and Samson, L. D. (2002). 3-Methyladenine DNA glycosylase-deficient Aag null mice display unexpected bone marrow alkylation resistance. Cancer Res. 62, 656-660.
34. Simonelli, V., Narciso, L., Dogliotti, E., and Fortini, P. (2005). Base excision repair intermediates are mutagenic in mammalian cells. Nucleic Acids Res. 33, 4404-4411.
35. Smith, S. A., and Engelward, B. P. (2000). In vivo repair of methylation damage in Aag 3-methyladenine DNA glycosylase null mouse cells. Nucleic Acids Res. 28, 3294-3300.
36. Sobol, R. W., Kartalou, M., Almeida, K. H., Joyce, D. F., Engelward, B. P., Horton, J. K., Prasad, R., Samson, L. D., and Wilson, S. H. (2003). Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses. J. Biol. Chem. 278, 39951-39959.
37. Toniolo, A., Onodera, T., Yoon, J. W., and Notkins, A. L. (1980). Induction of diabetes by cumulative environmental insults from viruses and chemicals. Nature 288, 383-385.
38. Turley, S., Poirot, L., Hattori, M., Benoist, C., and Mathis, D. (2003). Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198, 1527-1537.
39. Varadarajan, S., Shah, D., Dande, P., Settles, S., Chen, F. X., Fronza, G., and Gold, B. (2003). DNA damage and cytotoxicity induced by minor groove binding methyl sulfonate esters. Biochemistry 42, 14318-14327.
40. Yamagami, T., Miwa, A., Takasawa, S., Yamamoto, H., and Okamoto, H. (1985). Induction of rat pancreatic B-cell tumors by the combined administration of streptozotocin or alloxan and poly(adenosine diphosphate ribose) synthetase inhibitors. Cancer Res. 45, 1845-1849.