Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes

Diabetes

Volumn 48, Issue 4, 1999, Pages 706-713

  Flodström, Malin ^a,b   Tyrberg, Björn ^a   Eizirik, Dècio L ^a,c   Sandler, Stellan ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c DIABETES RESEARCH CENTER   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; STREPTOZOCIN;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL DEATH; CELL DESTRUCTION; CELL FUNCTION; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN SENSITIVITY; INSULIN SYNTHESIS; MALE; MOUSE; NONHUMAN; PANCREAS FUNCTION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

EID: 0033041283     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.48.4.706     Document Type: Article

References (57)

1. Bach J-F: Insulin-dependent diabetes mellitus as a β-cell targeted disease of immunoregulation. J Autoimmun 8:439-463, 1995
2. Mandrup-Poulsen T: The role of interleukin-1 in the pathogenesis of insulin-dependent diabetes mellitus. Diabetologia 39:1005-1029, 1996
3. Rabinovitch A: An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab Rev 14:129-151, 1998
4. Xie Q, Nathan C: The high-output nitric oxide pathway: role and regulation. J Leukoc Biol 56:576-582, 1994
5. Förstermann U, Gath I, Schwarz P, Closs EI, Kleinert H: Isoforms of nitric oxide synthase: properties, cellular distribution and expressional control. Biochem Pharmacol 50:1321-1332, 1995
6. Vladutiu A Role of nitric oxide in autoimmunity. Clin Immunol Immunopathol 76:1-11, 1995
7. Cook H, Cattell V: Role of nitric oxide in immune-mediated diseases. Clin Sci 91:375-384, 1996
8. Kleeman R, Rothe H, Kolb-Bachofen V, Xie Q-W, Nathan C, Martin S, Kolb H: Transcription and translation of inducible nitric oxide synthase in the pancreas of prediabetic BB rats. FEBS Lett 328:9-12, 1993
9. Rothe H, Faust A, Schade U, Kleeman R, Bosse G, Hibino T, Martin S, Kolb H: Cyclophosphamide treatment of female non-obese diabetic mice causes enhanced expression of inducible nitric oxide synthase and interferon-gamma, but not of interleukin-4. Diabelologia 37:1154-1158, 1994
10. Rabinovitch A, Suarez-Pinzon WL, Sorensen O, Bleackley RC: Inducible nitric oxide synthase (iNOS) in pancreatic islets of nonobese diabetic mice: identification of iNOS expressing cells and relationships to cytokines expressed in the islets. Endocrinology 137:2093-2099, 1996
11. Eizirik DL, Flodström M, Karlsen AE, Welsh N: The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic beta cells. Diabetologia 39:875-890, 1996
12. Eizirik D, Pavlovic D: Is there a role for nitric oxide in β-cell dysfunction and damage in IDDM? Diabetes Metab Rev 13:293-308, 1997
13. Lukic ML, Stosic-Grujicic S, Ostojic N, Chan WL, Liew FY: Inhibition of nitric oxide generation affects the induction of diabetes by streptozotocin in mice. Biochem Biophys Res Commun 178:913-920, 1991
14. Kolb H, Kiesel U, Kränke K-D, Kolb-Bachofen V: Suppression of low-dose streptozotocin induced diabetes in mice by administration of nitric oxide synthase inhibitor. Life Sci 49:PL213-PL217, 1993
15. Corbett JA, Mikhael A, Shimizu J, Frederick K, Misko TP, McDaniel ML, Kanagawa O, Unanue ER: Nitric oxide production in islets from nonobese diabetic mice: aminoguanidine-sensitive and -resistant stages in the immunological diabetic process. Proc Natl Acad Sci U S A 90:8992-8995, 1993
16. w-nitro-L-arginine methyl ester reduces the incidence of IDDM in BB/E rats. Diabetes 44:365-368, 1995
17. G-monomethyl-L-arginine on the onset of diabetes in the spontaneously diabetic BB rat. Diabetes 44:360-364, 1995
18. Andersen HU, Jorgensen KH, Egeberg J, Mandrup-Poulsen T, Nerup J: Nicotinamide prevents Interleukin-1 effects on accumulated insulin release and nitric oxide production in rat islets of Langerhans. Diabetes 43:770-777, 1994
19. Cetkovic-Cvrlje M, Eizirik DL: TNF-alpha and IFN-gamma potentiate the deleterious effects of IL-1 beta on mouse pancreatic islets mainly via generation of nitric oxide. Cytokine 6:399-406, 1994
20. Flodström M, Morris SM Jr, Eizirik DL: Role of the citrulline-nitric oxide cycle in the functional responses of adult human and rodent pancreatic islets to cytokines. Cytokine 8:642-650, 1996
21. Suarez-Pinzon WL, Strynadka K, Rabinovitch A: Destruction of rat pancreatic islet β-cells by cytokines involves the production of cytotoxic aldehydes. Endocrinology 137:5290-5296, 1996
22. Delaney CA, Pavlovic D, Hoorens A, Pipeleers DG, Eizirik DL: Cytokines induce deoxyribonudeic acid strand breaks and apoptosis in human pancreatic islet cells. Endocrinology 138:2610-2614, 1997
23. Holstad M, Sandler S: Aminoguanidine, an inhibitor of nitric oxide formation, fails to protect against insulitis and hyperglycemia induced by multiple low-dose streptozotocin injections in mice. Autoimmunity 15:311-314, 1993
24. Papaccio G, Esposito V, Latronico M, Aurelio Pisanti F: Administration of a nitric oxide synthase inhibitor does not suppress low-dose streptozotocin-induced diabetes in mice. Int J Pancreatol 17:85-68, 1995
25. Bowman MA, Simell OG, Peck AB, Cornelius J, Luchetta R, Look Z, Maclaren NK, Atkinson MA: Pharmacokinetics of aminoguanidine administration and effects on the diabetes frequency in nun-obese diabetic mice. J Pharmacol Exp Ther 279:790-794, 1996
26. Sternesjö J, Welsh N, Sandler S: S-methyl-L-thiocitrulline counteracts interleukin 1 beta induced suppression of pancreatic islet function in vitro, but does not protect against multiple low-dose streptozotocin-induced diabetes in vivo. Cytokine 9:352-359, 1997
27. Moncada S, Higgs A, Furchgott R: XIV. International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev 49:137-142, 1997
28. MacMicking J, Nathan C, Hom G, Chartrain N, Fletcher DS, Traumbauer M, Stevens K, Xie Q-W, Sokol K, Hutchinson N, Chen H, Mudgett JS: Altered responses to bacterial infection and endotoxin shock in mice lacking inducible nitric oxide synthase. Cell 81:541-650, 1995
29. Andersson A: Isolated mouse pancreatic islets in culture: effects of serum and different culture media on the insulin production of islets. Diabetologia 14:397-404, 1978
30. 15N]nitrate in biological fluids. Anal Biochem 126:131-138, 1982
31. Eizirik DL, Björklund A, Cagliero E: Genotoxic agents increase expression of growth arrest and DNA damage: inducible genes GADD 153 and GADD 45 in rat pancreatic islets. Diabetes 42:738-745, 1993
32. Heding LG: Determination of total serum insulin (IRI) in insulin-treated patients. Diabetologia 8:260-266, 1972
33. Hinegardner RT: An improved fluorometric assay for DNA. Anal Biochem 39:197-201, 1971
34. Hulban PA, Wollheim CB, Blondel B, Renold AE: Long-term exposure of isolated pancreatic islets to mannuheptulose: evidence for insulin degradation in the β-cell. Biochem Pharmacol 29:2625-2633, 1980
35. Like AA, Rossini AA: Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 193:415-417, 1976
36. Wallenstein S, Zucker CL, Fleiss JL: Some statistical methods useful in circulation research. Circ Res 47:1-9, 1980
37. Schmidt HHHW, Warner TD, Ishii K, Sheng H, Murad F: Insulin secretion from pancreatic β-cells caused by L-arginine-derived nitric oxide. Science 255:721-723, 1991
38. Yoon J-W, Jun H-S, Santamaria P: Cellular and molecular mechanisms for the initiation and progression of β cell destruction resulting from the collaboration between macrophages and T cells. Autoimmunity 27:109-122, 1998
39. Sandler S, Eizirik DL, Svensson C, Strandell E, Welsh M, Welsh N: Biochemical and molecular actions of interleukin-1 on pancreatic beta-cells. Autoimmunity 10:241-253, 1991
40. Eizirik DL, Welsh N, Hellerström C: Predominance of stimulatory effects of interleukin-1 beta on isolated human pancreatic islets. J Clin Endocrinol Metab 76:399-403, 1993
41. Wilson G, Ledoux S: Interactions of chemicals with pancreatic B-cells. In Lessons From Animal Diabetes IV. Shafrir E, Ed. London, Smith-Gordon, 1993, p. 17-26
42. Turk J, Corbett JA, Ramanadham S, Bohrer A, McDaniel ML: Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochem Biophys Res Commun 197:1458-1464, 1993
43. Krönke K-D, Fehsel K, Sommer A, Rodriguez M-L, Kolb-Bachofen V: Nitric oxide generation during cellular metabolization in the diabetogenic N-methyl-N-nitroso-urea streptozotocin contributes to islet cell DNA damage. Biol Chem Hoppe-Seyler 376:179-185, 1995
44. Tsuji A, Sakurai H: Generation of nitric oxide from streptozotocin (STZ) in the presence of copper (II) plus ascorbate: implication for the development of STZ-induced diabetes. Biochem Biophys Res Commun 245:11-16, 1998
45. Kolb H: Mouse models of insulin-dependent diabetes: low-dose streptozotocin-induced diabetes and nonobese diabetic (NOD) mice. Diabetes Metab Rev 3:751-778, 1987
46. Kolb H, Krönke K-D: IDDM: lessons from the low-dose streptozotocin model in mice. Diabetes Rev 1:116-126, 1993
47. Krönke K-D, Kolb-Bachofen V, Berschick B, Burkart V, Kolh H: Activated macrophages kill pancreatic syngenic islet cells via arginine-dependent nitric oxide generation. Biochem Biophys Res Commun 175:752-758, 1991
48. Corbett JA, McDaniel ML: Intraislet release of interleukin 1 inhibits beta cell function by inducing β-cell expression of inducible nitric oxide synthase. J Exp Med 181:559-568, 1995
49. Takamura T, Kato I, Kimura N, Nakazawa T, Yonekura H, Takasawa S, Okamoto H: Transgenic mice overexpressing type 2 nitric-oxide synthase in pancreatic β-cells develop diabetes without insulitis. J Biol Chem 273:2493-2496, 1998
50. Corbett JA, Sweetland M, Wang J, Lancaster JR Jr, McDaniel ML: Nitric oxide mediates cytokine-induced inhibition of insulin secretion by human islets of Langerhans. Proc Natl Acad Sci U S A 90:1731-1735, 1993
51. Scarim A, Heitmeier M, Corbett J: Irreversible inhibition of metabolic function and islet destruction after a 36-hour exposure to interleukin-1beta. Endocrinology 138:5301-5307, 1997
52. Arnush M, Heitmeyer M, Scarim A, Marino M, Manning P, Corbett J: IL-1 produced and released endogenously within human islets inhibits β-cell function. J clin Invest 102:516-526, 1998
53. Eizirik DL, Sandler S. Welsh N, Cetkovic-Cvrlje M, Nieman A, Geller DA, Pipeleers DG, Bendtzen K, Hellerström C: Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 93:1968-1974, 1994
54. Rabinovitch A, Suarez-Pinzon WL, Strynadka K, Schulz, R, Lakey JRT, Warnock GL, Rajotte, RV: Human pancreatic islet β-cell destruction by cytokines is independent of nitric oxide production. J Clin Endocrinol Metab 79:1058-1062, 1994
55. Eizirik DL, Delaney CA, Green MHL, Cunningham JM, Thorpe JR, Pipeleers DG, Hellerström C, Green IC: Nitric oxide donors decrease the function and survival of human pancreatic islets. Mol Cell Endocrinol 118:71-83, 1996
56. Delaney CA, Tyrberg B, Bouwens L, Vaghef H, Hellman B, Eizirik DL: Sensitivity of human pancreatic islets to peroxynitrite-induced cell dysfunction and death. FEBS Lett 394:300-306, 1996
57. Pavlovic D, Chen M, Bouwens L, Eizirik D, Pipeleers D: Ductal cells are a source of nitric oxide production in isolated human pancreatic islets. Diabetologia (Suppl. 1):A56, 1998