Dual-Label Immunohistochemical Study of Interleukin-4-and Interferon-γ-Expressing Cells within the Pancreas of the NOD Mouse During Disease Acceleration with Cyclophosphamide

References

• Eisenbarth G S, Connelly J, Soeldner J. S. The “natural” history of type 1 diabetes. Diabetes Metab Rev 1987; 3: 873–91
   PubMedGoogle Scholar
• Bach J. F. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr Rev 1994; 15: 516–42
   PubMed Web of Science ®Google Scholar
• Kikutani H, Makino S. The murine autoimmune diabetes model: NOD and related strains. Adv Immunol 1992; 51: 285–322
   PubMed Web of Science ®Google Scholar
• Signore A, Pozzilli P, Gale E AM. Andreani D, Beverley PCL. The natural history of lymphocyte subsets infiltrating the pancreas of NOD mice. Diabetologia 1989; 32: 282–9
   PubMed Web of Science ®Google Scholar
• Jansen A, Homo-Delarche F, Hooijkaas H, Leenen P. J. Dardenne M, Drexhage HA. Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and β-cell destruction in NOD mice. Diabetes 1994; 43: 667–75
   PubMed Web of Science ®Google Scholar
• Reddy S, Wu D, Swinney C, Elliott R. B. Immunohistochemical analyses of pancreatic macrophages and CD4 and CD8 T cell subsets prior to and following diabetes in the NOD mouse. Pancreas 1995; 11: 16–25
   PubMed Web of Science ®Google Scholar
• Harada M, Makino S. Promotion of spontaneous diabetes in non-obese diabetes-prone mice by cyclophosphamide. Diabetologia 1984; 27: 604–6
   PubMed Web of Science ®Google Scholar
• Harada M. Immune disturbance and pathogenesis of non-obese diabetes-prone (NOD) mice. Exp Clin Endocrinol 1987; 89: 251–8
   PubMedGoogle Scholar
• Reddy S, Yip S, Karanam M, Poole C A, Ross J. M. An immunohistochemical study of macrophage influx and the co-localization of inducible nitric oxide synthase in the pancreas of non-obese diabetic (NOD) mice during disease acceleration with cyclophosphamide. Histochemical J 1999; 31: 303–14
   PubMedGoogle Scholar
• Bendtzen K, Mandrup-Poulsen T, Nerup J, Nielsen J H, Din-Arello C. A., Svenson M. Cytotoxicity of human pI 7 inter-leukin-1 for pancreatic islets of Langerhans. Science 1986; 232: 1545–7
   PubMed Web of Science ®Google Scholar
• Southern C, Schulster D, Green I. C. Inhibition of insulin secretion by interleukin-1β and tumour necrosis factor-α via an L-arginine-dependent nitric oxide generating mechanism. FEBSLett 1990; 276: 42–4
   PubMed Web of Science ®Google Scholar
• Sandler S, Andersson A, Hellerstrom C. Inhibitory effects of interleukin-1 on insulin secretion, insulin biosynthesis, and oxidative metabolism of isolated rat pancreatic islets. Endocrinology 1987; 121: 1424–31
   PubMed Web of Science ®Google Scholar
• Mandrup-Poulsen T, Helqvist S, Wogensen L D, Molvig J, Pociot F, Johannesen J, Nerup J. Cytokines and free radicals as effector molecules in the destruction of pancreatic beta cells. Current Topics in Microbiol Immunol 1990; 164: 169–93
   PubMed Web of Science ®Google Scholar
• Cetkovic-Cvrlje M, Eizirik D. L. TNF-cx and INF-y potentiate the deleterious effects of IL-1β on mouse pancreatic islets mainly via generation of nitric oxide. Cytokine 1994; 6: 399–406
   PubMed Web of Science ®Google Scholar
• Eizirik D L, Sandler S, Welsh N, Cetkovic-Cvrlje M, Nieman A, Geller D. A., et al. Cytokines suppress islet function irrespective of their effects on nitric oxide generation. J Clin Invest 1994; 93: 1968–74
   PubMed Web of Science ®Google Scholar
• Rabinovitch A, Suarez-Pinson W L, Strynadka K, Schultz R, Lakey J R, Warnock G. L., et al. Human pancreatic islet (J-cell destruction by cytokines is independent of nitric oxide production. J Clin Endocrinol Metab 1994; 79: 1058–62
   PubMed Web of Science ®Google Scholar
• Mossmann T R, Cherwinski H, Bond M W, Giedlin M A, Coff-Man R. L. Two types of murine helper T cell clone. 1. Definition according to profiles of lymphokine activities and secreted proteins. Adv Immunol 1986; 136: 2348–57
   Google Scholar
• Mossmann T R, Coffman R. L. TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Ann Rev Immunol 1989; 7: 145–73
   PubMed Web of Science ®Google Scholar
• Rabinovitch A. Roles of cytokines in IDDM pathogenesis and islet β-cell destruction. Diabetes Rev 1993; 1: 215–40
   Google Scholar
• Rabinovitch A. Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM. Therapeutic intervention by immunostimulation. Diabetes 1994; 43: 613–21
   PubMed Web of Science ®Google Scholar
• Dunger A, Cunningham J M, Delaney C A, Lowe J E, Green M HL, Bone A J, Green I. C. Tumour necrosis factor-α and interferon-γ inhibit insulin secretion and cause DNA damage in unweaned-rat islets: Extent of nitric oxide involvement. Diabetes 1996; 45: 183–9
   PubMed Web of Science ®Google Scholar
• O'Brien B A, Harmon B V, Cameron D P, Allan D. J. Apoptosis is the mode of β-cell death responsible for the development of IDDM in the non-obese diabetic (NOD) mouse. Diabetes 1997; 46: 750–7
   PubMed Web of Science ®Google Scholar
• Augustein P, Elefanty A G, Allison J, Harrison L. C. Apoptosis and beta cell destruction in pancreatic islets of NOD mice with spontaneous and cyclophosphamide-accelerated diabetes. Diabetologia 1998; 41: 1381–8
   PubMed Web of Science ®Google Scholar
• Rabinovitch A. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes/Metab Rev 1998; 14: 129–51
   PubMed Web of Science ®Google Scholar
• Rapoport M J, Jaramillo A, Zipris D, Lazarus A H, Serreze D V, Leiter E H, Cyopick P, Danska J S, Delovitch T. L. IL-4 reverses T-cell proliferative unresponsiveness and prevents the onset of diabetes in NOD mice. J Exp Med 1993; 178: 87–99
   PubMed Web of Science ®Google Scholar
• Meuller R., Krahl T, Sarvetnick N. Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in non-obese diabetic mice. J Exp Med 1996; 184: 1093–9
   PubMed Web of Science ®Google Scholar
• Hancock W W, Polanski M, Zhang J, Blogg N, Weiner H. L. Suppression of insulitis in non-obese diabetic (NOD) mice by oral insulin administration is associated with selective expression of interleukin-4 and -10, transforming growth factor-β, and prostaglandin-E. Am J Pathol 1995; 147: 1193–9
   PubMed Web of Science ®Google Scholar
• Rabinovitch A, Suarez-Pinson W L, Sorensen O, Bleackley R C, Power R. F. IFN-γ gene expression in pancreatic islet-infiltrating mononuclear cells correlates with autoimmune diabetes in non-obese diabetic mice. J Immunol 1995; 154: 4874–82
   PubMed Web of Science ®Google Scholar
• Rabinovitch A, Suarez-Pinson W L, Sorensen O. Interleukin 12 mRNA expression in islets correlates with β-cell destruction in NOD mice. J Autoimmun 1996; 9: 645–51
   PubMed Web of Science ®Google Scholar
• Faulkner-Jones B E, Dempsey-Collier M, Mandel T E, Harrison L. C. Both TH1 and TH2 cytokine mRNAs are expressed in the NOD mouse pancreas in vivo. Autoimmunity 1996; 23: 99–110
   PubMed Web of Science ®Google Scholar
• Fox C J, Danska J. S. IL-4 expression at the onset of islet inflammation predicts non-destructive insulitis in nonobese diabetic mice. J Immunol 1997; 158: 2414–24
   PubMed Web of Science ®Google Scholar
• Shimada A, Charlton B, Taylor-Edwards C, Fathman C. G. β-cell destruction may be a late consequence of the autoimmune process in non-obese diabetic mice. Diabetes 1996; 45: 1063–7
   PubMed Web of Science ®Google Scholar
• Held W, MacDonald H R, Weissman I L, Hess M W, Mueller C. Genes encoding tumour necrosis factor alpha and granzyme A are expressed during development of autoimmune diabetes. Proc Natl Acad Sci USA 1990; 87: 223–293
   Web of Science ®Google Scholar
• Lindstein T, June C H, Ledbetter J A, Stella G, Thompson C. B. Regulation of lymphokine mRNA stability by a surface-mediated T cell activation pathway. Science 1989; 244: 339–43
   PubMed Web of Science ®Google Scholar
• Rothe H, Faust A, Schade U, Kleeman R, Bosse G, Hibino T, Martin S, Kolb H. 1994Cycophosphamide treatment of female non-obese diabetic mice causes enhanced expression of inducible nitric oxide synthase and interferon-gamma, but not interleukin-4. Diabetologia 1994; 37: 1154–58
   PubMed Web of Science ®Google Scholar
• Rothe H, Hibino T, Itoh Y, Kolb H, Martin S. Systemic production of interferon-gamma inducing factor (IGIF) versus local IFN-γ expression involved in the development of Thl insulitis in NOD mice. J Autoimmun 1997; 10: 251–6
   PubMed Web of Science ®Google Scholar
• Shehadeh N N, Francisco O L, Lafferty K. Altered cytokine activity in adjuvant inhibition of autoimmune diabetes. J Autoimmun 1993; 6: 291–300
   PubMed Web of Science ®Google Scholar
• Suarez-Pinson W L, Rajotte R V, Mosmann T R, Rabinovitch A. Both CD4+ and CD8+ T-cells in syngeneic islet grafts in NOD mice produce interferon-γ during β-cell destruction. Diabetes 1996; 45: 1350–7
   PubMed Web of Science ®Google Scholar
• Charlton B, Bacelj A, Mandel T. E. Administration of silica particles or anti-Lyt2 antibody prevents P-cell destruction in NOD mice given cyclophosphamide. Diabetes 1988; 37: 930–5
   PubMed Web of Science ®Google Scholar
• Zhang Z L, Georgiou H M, Mandel T. E. The effect of cyclophosphamide treatment on lymphocyte subsets in the non-obese diabetic mouse: a comparison of various lymphoid organs. Autoimmunity 1993; 15: 1–10
   PubMed Web of Science ®Google Scholar
• Reddy S, Bibby N J, Elliott R. B. Ontogeny of islet cell antibodies, insulin autoantibodies and insulitis in the nonobese diabetic mouse. Diabetologia 1988; 31: 322–8
   PubMed Web of Science ®Google Scholar
• Reddy S, Kaill S, Poole C A, Ross J. Inducible nitric oxide synthase in pancreatic islets of the non-obese diabetic mouse: a light and confocal microscopical study of its ontogeny, co-localization and up-regulation following cytokine administration. Histochemical J 1997; 29: 53–64
   PubMedGoogle Scholar
• Lo D, Reilly C R, Scott B, Liblau R, McDevitt H O, Burkly L. C. Antigen-presenting cells in adoptively transferred and spontaneous autoimmune diabetes. Eur J Immunol 1993; 23: 1693–8
   PubMed Web of Science ®Google Scholar
• Kagi D, Odermatt B, Seiler P, Zionkernagel R M, Mak T W, Hengartner H. Reduced incidence and delayed onset of diabetes in perforin-deficient non-obese diabetic mice. J Exp Med 1997; 186: 989–97
   PubMed Web of Science ®Google Scholar
• Benoist C, Mathi S. D. Cell death mediators in autoimmune diabetes- no shortage of suspects. Cell 1997; 89: 1–3
   PubMed Web of Science ®Google Scholar
• Chervonsky A V, Wang Y, Wong F S, Visintin I., Flavell R A, Janeway C A, Matis L. A. The role of Fas in autoimmune diabetes. Cell 1997; 89: 17–24
   PubMed Web of Science ®Google Scholar
• De Maria R, Testi R. Fas-FasL interactions: a common pathogenetic mechanism in organ-specific autoimmunity. Immunology Today 1998; 19: 121–5
   PubMedGoogle Scholar
• Pilstrom B, Bjork L, Bohme J. Monokine-producing cells predominate in the recruitment phase of NOD insulitis while cells producing Thl-type cytokines characterize the effector phase. J Autoimmun 1997; 10: 147–55
   PubMed Web of Science ®Google Scholar
• Foulis A K, McGill M, Farquharson M. A. Insulitis in type 1 (insulin-dependent) diabetes mellitus in man- macrophages, lymphocytes, and interferon-γ containing cells. J Pathol 1991; 165: 97–103
   PubMed Web of Science ®Google Scholar
• Huang X, Hultgren B., Dybdal N, Stewart T. A. Islet expression of interferon-α precedes diabetes in both the BB rat and streptozotocin-treated mice. Immunity 1994; 1: 469–78
   PubMed Web of Science ®Google Scholar
• Foulis A K, Farquharson M A, Meager A. Immunoreactive a-interferon in insulin-secreting β cells in type 1 diabetes mellitus. Lancet 1987; 2: 1423–7
   PubMed Web of Science ®Google Scholar
• Huang X, Yuang J, Goddard A, Foulis A, James R FL, Lern-Mark A. et al. Interferon expression in the pancreases of patients with type 1 diabetes. Diabetes 1995; 44: 658–64
   PubMed Web of Science ®Google Scholar
• Kilgore K S, Schmid E, Shanley T P, Flory C M, Maheshwari V, Tramontini N. L., et al. Sublytic concentrations of the membrane attack complex of complement induce endothelial interleukin-8 and monocyte chemoattractant protein-1 through nuclear factor-KB activation. Am J Pathol 1997; 150: 2019–31
   PubMed Web of Science ®Google Scholar
• Munder M, Mallo M, Eichmann K, Modolell M. Murine macrophages secrete interferon γ upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J Exp Med 1998; 187: 2103–8
   PubMed Web of Science ®Google Scholar
• Fultz M J, Barber S A, Dieffenbach C W, Vogel S. N. Induction of IFN-y in macrophages by lipopolysaccharide. Int Immunol 1993; 5: 1383–92
   PubMed Web of Science ®Google Scholar
• Trembleau S, Penna G, Bosi E, Mortara A, Gately M K, Adorini L. Interleukin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J Exp Med 1995; 181: 817–21
   PubMed Web of Science ®Google Scholar
• Debray-Sachs M, Carnaud C, Boitard C, Cohen H, Gresser I, Bedossa P, Bach J F. Prevention of diabetes in NOD mice treated with antibody to murine IFNγ. J Autoimmunity 1991; 4: 237–48
   PubMed Web of Science ®Google Scholar
• Nicoletti F, Zaccone P, Di Marco R, Di Mauro M, Magro G, Grasso S., et al. The effects of a nonimmunogenic form of murine soluble interferon-y receptor on the development of autoimmune diabetes in the NOD mouse. Endocrinology 1996; 137: 5567–75
   PubMed Web of Science ®Google Scholar
• Hultgren B, Huang X, Dybdal N, Stewart T. A. Genetic absence of γ-inteferon delays but does not prevent diabetes in NOD mice. Diabetes 1996; 45: 812–7
   PubMed Web of Science ®Google Scholar
• Sobel D O, Ahvazi B. α-Interferon inhibits the development of diabetes in NOD mice. Diabetes 1998; 47: 1867–72
   PubMed Web of Science ®Google Scholar