Nicotinamide prevents the development of diabetes in the cyclophosphamide-induced NOD mouse model by reducing beta-cell apoptosis

Journal of Pathology

Volumn 191, Issue 1, 2000, Pages 86-92

  O'Brien, Bronwyn A ^a   Harmon, Brian V ^a   Cameron, Donald P ^b   Allan, David J ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b PRINCESS ALEXANDRA HOSPITAL   (Australia)

Author keywords

Apoptosis; Beta cell; Cyclophosphamide; Insulin dependent diabetes mellitus; Nicotinamide; Non obese diabetic mouse

Indexed keywords

CYCLOPHOSPHAMIDE; GLUCOSE; NICOTINAMIDE;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; IMMUNOHISTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CYCLOPHOSPHAMIDE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED NOD; NIACINAMIDE;

EID: 0034094769     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9896(200005)191:1<86::AID-PATH573>3.0.CO;2-0     Document Type: Article

References (42)

1. O'Brien BA, Cameron DC, Harmon BH, Allan DJ. Beta cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J Pathol 1996; 178: 176-181.
2. O'Brien BA, Cameron DC, Harmon BH, Allan DJ. Apoptosis is the mode of beta-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse. Diabetes 1997; 46: 750-757.
3. Wegman DR. The immune response to islets in experimental diabetes and insulin-dependent diabetes mellitus. Curr Opin Immunol 1996; 8: 860-864.
4. Makino S, Kunimoto K, Muraoka T, Mizushima Y, Katagiri K, Tochino Y. Breeding of a non-obese diabetic strain of mice. Exp Anim 1980; 29: 1-13.
5. Kataoka S, Satoh J, Fujiya H, et al. Immunologic aspects of the nonobese diabetic (NOD) mouse: abnormalities of cellular immunity. Diabetes 1983; 32: 247-253.
6. Harada M, Makino S. Promotion of spontaneous diabetes in non-obese diabetes-prone mice by cyclophosphamide. Diabetologia 1984; 27: 604-606.
7. Yamada K, Nonaka K, Hanafusa T, Miyazaki A, Toyoshima H, Tanui S. Prevention and therapeutic effects of large-dose nicotinamide injections on diabetes associated with insulitis: an observation in the non-obese diabetic (NOD) mouse. Diabetes 1982; 31: 749-753.
8. Elliott RB, Chase HP. Prevention or delay of type 1 diabetes mellitus in children using nicotinamide. Diabetologia 1991; 34: 362-365.
9. André I, Gonzalez A, Wang B, Katz J, Benoist C, Mathis D. Checkpoints in the progression of autoimmune diseases: lessons from diabetes models. Proc Natl Acad Sci U S A 1996; 93: 2260-2263.
10. Zhang ZL, Georgiou HM, Mandel TE. The effect of cyclophosphamide treatment on lymphocyte subsets in the nonobese diabetic mouse: a comparison of various lymphoid organs. Autoimmunity 1993; 15: 1-10.
11. Barres BA, Hart IK, Coles HSR, et al. Cell death and control of cell survival in the survival in the oligodendrocyte lineage. Cell 1992; 70: 31-46.
12. Wyllie AH, Kerr JFR, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251-306.
13. Howie SE, Sommertield AJ, Gray E, Harrison DJ. Peripheral T lymphocyte depletion by apoptosis after CD4 ligation in vivo: selective loss of CD44 and 'activating' memory T cells. Clin Exp Immunol 1994; 95: 195-200.
14. Pipeleers DG, van der Winkel M. Pancreatic B cells possess defense mechanisms against cell-specific toxicity. Proc Natl Acad Sci U S A 1986; 83: 5267-5271.
15. Ling Z, Malaisse-Lagae F, Malaisse WJ, Pipeleers D. Reduced glutamate decarboxylase activity in rat islet β-cells which survived streptozotocin-induced cytotoxicity. FEBS Lett 1993; 324: 262-264.
16. Pillans PI, Ponzi SF, Parker MI. Cyclophosphamide induced DNA strand breaks in mouse embryos' cephalic tissue in vivo. Carcinogenesis 1989; 10: 83-85.
17. Sanderson BJ, Shield AJ. Mutagenic damage to mammalian cells by therapeutic alkylaling agents. Mutat Res 1996; 355: 41-57.
18. Naruse I, Keino H, Kawarada Y. Antibody against single-stranded DNA detects both programmed cell death and drug-induced apoptosis. Histochemistry 1994; 101: 73-78.
19. Meyn RE, Stephens LC, Hunter NR, Milas L. Induction of apoptosis in murine tumours by cyclophosphamide. Cancer Chemother Pharmacol 1994; 33: 410-414.
20. Kaneto H, Fujii J, Seo HG, et al. Apoptotic cell death triggered by nitric oxide in pancreatic β-cells. Diabetes 1995; 44: 733-738.
21. Bedoya FJ, Solano F, Lucas M. N-monomethyl-arginine and nicotinamide prevent streptozotocin-induced double strand DNA break formation in pancreatic rat islets. Experientia 1996; 52: 344-347.
22. Saini KS, Thompson C, Winterford CM, Walker NI, Cameron DP. Streptozotocin at low doses induces apoptosis and at high doses causes necrosis in a murine pancreatic beta cell line, INS-1. Biochem Mol Biol Int 1996; 39: 1229-1236.
23. Calcinaro F, Gambelunghe G, Lafferty KJ. Protection from autoimmune diabetes by adjuvant therapy in the nonobese diabetic mouse the role of interleukin-4 and interleukin-10. Immunol Cell Biol 1997; 75: 467-471.
24. Giordano C, Stassi G, De Maria R, et al. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto's thyroiditis. Science 1997; 275: 960-963.
25. Knight CRL, Rees RC, Platts A, Johnson T, Griffin M. Interleukin-2-activaled human effector lymphocytes mediate cytotoxicity by inducing apoptosis in human leukemia and solid tumour target cells. Immunology 1993; 79: 535-541.
26. Filep JG, Baron C, Lachance S, Perreault C, Chan JSD. Involvement of nitric oxide in target-cell lysis and DNA fragmentation induced by murine natural killer cells. Blood 1996; 87: 5136-5143.
27. Horio F, Fukuda M, Katoh H, et al. Reactive oxygen intermediates in autoimmune islet cell destruction of the NOD mouse induced by peritoneal exudate cells (rich in macrophages) but not T cells. Diabetologia 1994; 37: 22-31.
28. Sung M-W, Nagashima S, Johnson JT, Van Dongen GA, Whiteside TL. The role of apoptosis in antibody-dependent cell-mediated cytotoxicity against monolayers of human squamous cell carcinoma of the head and neck targets. Cell Immunol 1996; 171: 20-29.
29. Kurrer MO, Pakala SV, Hanson HL, Katz JD. B-cell apoptosis in T cell-mediated autoimmune diabetes. Proc Natl Acad Sci U S A 1997; 94: 213-218.
30. Alarcón-Segovia D, Ruiz-Argüelles A, Llorente L. Broken dogma: penetration of autoantibodies into living cells. Immunol Today 1996; 17: 163-164.
31. Charlton B, Bacelj A, Slattery RM, Mandel TE. Cyclophosphamide-induced diabetes in NOD/WEHI mice: evidence for suppression in spontaneous autoimmune diabetes mellitus. Diabetes 1989; 38: 441-447.
32. Colucci F, Cilio CM, Lejon K, Gonçalves CP, Bergman M-L, Holmberg D. Programmed cell death in the pathogenesis of murine IDDM: resistance to apoptosis induced in lymphocytes by cyclophosphamide. J Autoimmun 1996; 9: 271-276.
33. Schwartzman RA, Cidlowski JA. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 1993; 14: 133-151.
34. Gale FAM. Molecular mechanisms of beta-cell destruction in IDDM: the role nicotinamide. Hormone Res 1996; 45: 40-43.
35. Heller B, Burkle A, Radons J, et al. Analysis of oxygen radical toxicity in pancreatic islets at the single cell level. Biol Chem Hoppe-Seyler 1994; 375: 597-602.
36. Rabinovitch A, Suarezpinzon WL, Shi Y, Morgan AR, Bleackley RC. DNA fragmentation is an early event in cytokine-induced islet beta-cell destruction. Diabetologia 1994; 37: 733-738.
37. Dunger A. Augstein P. Schmidt S, Fischer U. Identification of interleukin-1-induced apoptosis in rat islets using in situ specific labelling of fragmented DNA. J Autoimmun 1996; 9: 309-313.
38. Sjohölm A. Diabetes mellitus and impaired pancreatic β-cell proliferation. J Int Med 1996; 239: 211-220.
39. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA. Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 1992; 356: 314-317.
40. Strasser A, Whittingham S, Vaux D, et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A 1991; 88: 8661-8665.
41. Mountz JD, Wu J, Cheng J, Zhou T. Autoimmune disease: a problem of defective apoptosis. Arthritis Rheum 1994; 37: 1415-1420.
42. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol Today 1994; 15: 7-10.