Interleukin-13 prevents autoimmune diabetes in NOD mice

Diabetes

Volumn 48, Issue 8, 1999, Pages 1522-1528

  Zaccone, Paola ^a,b   Phillips, Jenny ^b   Conget, Ignacio ^d   Gomis, Ramon ^d   Haskins, Kathryn ^e   Minty, Adrian ^f   Bendtzen, Klaus ^g   Cooke, Anne ^b,c   Nicoletti, Ferdinando ^b,h  

^a UNIVERSITY OF CATANIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d HOSPITAL CLÍNIC   (Spain)

^e UNIVERSITY OF COLORADO   (United States)

^f SANOFI   (France)

^g Rigshospitalet   (Denmark)

^h NONE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN E; INTERLEUKIN 4; MONOCLONAL ANTIBODY CD3; RECOMBINANT INTERLEUKIN 13; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL;

ANIMALS; AUTOIMMUNE DISEASES; CELL TRANSPLANTATION; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOGLOBULIN E; INFLAMMATION; INTERFERON TYPE II; INTERLEUKIN-13; INTERLEUKIN-4; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; SPLEEN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0032768886     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.48.8.1522     Document Type: Article

References (67)

1. Swain SL: CD4 T cell development and cytokine polarization: an overview. J Leukoc Biol 57:795-798, 1995
2. Rabinovitch A: Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM: therapeutic intervention by immunostimulation? Diabetes 43:613-621, 1994
3. Mandrup-Poulsen T, Nerup J, Reimers JJ, Pociot F, Andersen HU, Karlsen A, Bjerre U, Bergholdt R: Cytokines and the endocrine system. II. Roles in substrate metabolism, modulation of thyroidal and pancreatic endocrine cell functions and autoimmune endocrine diseases. Eur J Endocrinol 134:21-30, 1996
4. Rabinovitch A: An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab Rev 14:129-151, 1998
5. Bach JF: Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr Rev 15:516-542, 1994
6. Sternesjo J, Sandler S: Effects of interleukin-12 in vitro on pancreatic islets isolated from normal rodents and from non-obese diabetic mice. J Endocrinol 158:69-75, 1998
7. Nicoletti F, Di Marco R, Barcellini W, Magro G, Schorlemmer HU, Kurrle R, Lunetta M, Grasso S, Zaccone P, Meroni PL: Protection from experimental autoimmune diabetes in the nonobese diabetic mouse by soluble interleukin-1 receptor. Eur J Immunol 24:1843-1847, 1994
8. Cailleau C, Diu-Hercend A, Ruuth E, Westwood R, Carnaud C: Treatment with neutralizing antibodies specific for IL-1 beta prevents cyclophosphamide-induced diabetes in nonobese diabetic mice. Diabetes 46:937-940, 1997
9. Rothe H, O'Hara RM, Martin S, Kolb H: Suppression of cyclophosphamide induced diabetes development and pancreatic Th1 reactivity in NOD mice treated with the interleukin (IL)-12 antagonist IL-12(p40)2. Diabetologia 39:119-122, 1996
10. Trembleau S, Penna G, Gregori S, Gately MC, Adorini L: Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur J Immunol 27:2330-2339, 1997
11. Campbell IL, Kay TWH, Oxbrow L, Harrison LC: Essential role for interferon-γ and interleukin-6 in autoimmune insulin-dependent diabetes in NOD/Whei mice. J Clin Invest 87:739-742, 1991
12. Debray-Sachs M, Carnaud C, Boitard C, Cohen H, Gresser I, Bedossa P, Bach JF: Prevention of diabetes in NOD mice treated with antibody to murine IFN-γ. J Autoimmun 4:237-248, 1991
13. Pennline KJ, Roque-Gaffney E, Monaham R: Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse. Clin Immunol Immunopathol 71:169-175, 1994
14. Nicoletti F, Zaccone P, Di Marco R, Di Mauro M, Magro G, Grasso S, Mughini L, Meroni PL, Garotta G: The effects of a nonimmunogenic form of murine soluble interferon-gamma receptor on the development of autoimmune diabetes in NOD mouse. Endocrinology 137:5567-5575, 1996
15. Nicoletti F, Zaccone P, Di Marco R, Lunetta M, Magro G, Grasso S, Meroni PL, Garotta G: Prevention of spontaneous autoimmune diabetes in diabetes-prone BB rats by prophylactic treatment with anti-rat interferon-γ antibody. Endocrinology 138:281-288, 1997
16. Yang XD, Tisch R, Singer SM, Cao ZA, Liblau RS, Schreiber RD, McDevitt HO: Effect of tumor necrosis factor-α on insulin-dependent diabetes mellitus in NOD mice. I. The early development of autoimmunity and the diabetogenic process. J Exp Med 180:995-1004, 1994
17. Rapoport MJ, Jaramillo A, Zipris D, Lazarus AH, Serreze DV, Leiter EH, Cyopick P, Danska JS, Delovitch TL: Interleukin-4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J Exp Med 178:87-99, 1993
18. Kallmann BA, Huther M, Tubes M, Feldkamp J, Bertrams J, Gries FA, Lampeter EF, Kolb HK: Systemic bias of cytokine production toward cell-mediated immune regulation in IDDM and toward humoral immunity in Graves' disease. Diabetes 46:237-243, 1997
19. Berman MA, Sandborg CI, Wang Z, Imfeld KL, Zaldivar F, Dadufalza V, Buckingham BA: Decreased IL-4 production in new onset type 1 insulin-dependent diabetes mellitus. J Immunol 157:4690-4696, 1996
20. Gombert JM, Herbelin A, Tancrede-Bohin E, Dy M, Carnaud C, Bach JF: Early quantitative and functional deficiency of NK1+-like thymocytes in the NOD mouse. Eur J Immunol 26:2989-2998, 1996
21. + T-cell deficiency and IDDM in NOD/Lt mice. Diabetes 46:572-582, 1997
22. Wilson SB, Kent SC, Patton KT, Orban T, Jackson RA, Exley M, Procelli S, Schatz DA, Atkinson MA, Balk SP, Strominger JL, Hafler DA: Extreme Th1 bias of invariant Vα24JαQT cells in type 1 diabetes. Nature 391:177-182, 1998
23. Nicoletti F, Scalia G, Condorelli F, Stivala A, Leonardi C, Steinsvag PO, La Rosa L, Lunetta M: Anti-cytomegalovirus IgM and IgG antibodies, islet cell antibodies and gamma Interferon serum levels in newly diagnosed IDDM patients. Int J Immunopathol Pharmacol 4:99-106, 1991
24. Hussain MJ, Peakman M, Gallati H, Lo SSS, Hawa M, Viberti GC, Watkins PJ, Leslie RDG, Vergani D: Elevated serum levels of macrophage derived cytokines precede and accompany the onset of IDDM. Diabetologia 39:60-69, 1996
25. Rabinovitch A, Suarez W, Sorensen O, Bleackley C, Power RF: IFN-γ gene expression in pancreatic islet-infiltrating mononuclear cells correlates with autoimmune diabetes in nonobese diabetic mice. J Immunol 154:4874-4882, 1995
26. Fox CJ, Danska JS: IL-4 expression at the onset of islet inflammation predicts nondestructive insulitis in nonobese diabetic mice. J Immunol 158: 2414-2424, 1997
27. Rabinovitch A, Suarez-Pinzon W, El-Sheikh A, Sorensen O, Power RF: Cytokine gene expression in pancreatic islet-infiltrating leukocytes of BB rate: expression of Th1 cytokines correlate with β-cell destructive insulitis and IDDM. Diabetes 45:749-754, 1996
28. Zipris D, Greiner DL, Malkani S, Whalen B, Mordes JP, Rossini AA: Cytokine gene expression in islets and thyroids of BB rats: IFN-gamma and IL-12p40 mRNA increase with age in both diabetic and insulin-treated nondiabetic rats. J Immunol 56:1315-1321, 1996
29. Kolb H, Worz-Pagenster UW, Kleeman R, Rothe H, Rowsell P, Scott FW: Cytokine gene expression in the BB rat pancreas: natural course and impact of bacterial vaccines. Diabetalogia 39:1448-1464, 1996
30. Cameron MJ, Arreaza GA, Zucker P, Chensue SW, Stricter RM, Chakrabarti S, Delovitch T: IL-4 prevents insulitis and insulin-dependent diabetes mellitus in nonobese diabetic mice by potentiation of regulatory T helper-2 cell function. J Immunol 159:4686-4692, 1997
31. Mueller R, Krahl T, Sarvertnick N: Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 184:1093-1099, 1996
32. Trembleau S, Penna G, Bosi E, Mortara A, Gately MK, Adorini L: Interleukin-12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J Exp Med 181:817-821, 1995
33. O'Hara RM Jr, Henderson SL, Nagelin A: Prevention of a Th1 disease by a Th1 cytokine: IL-12 and diabetes in NOD mice. Ann N Y Acad Sci 759:241-249, 1996
34. Satoh J, Seino H, Tanaka SI, Shintani S, Ohta S, Tamura K, Sawai T, Nobunaga T, Oteki K, Kumagai K, Toyota R: Recombinant human tumor necrosis factor-α suppresses autoimmune diabetes in nonobese diabetic mice. J Clin Invest 84:1345-1348, 1989
35. Nicoletti F, Zaccone P, Di Marco R, Magro G, Grasso S, Stivala F, Calori G, Mughini L, Meroni PL, Garotta G: Paradoxical antidiabetogenic effect of γ-interferon in DP-BB rats. Diabetes 47:32-38, 1998
36. Serreze DV, Hamaguchi K, Leiter EH: Immunostimulation circumvents diabetes in NOD/Lt mice. J Autoimmun 2:759-776, 1989
37. Wogensen L, Lee M-S, Sarvertnick N: Production of interleukin-10 by islet cells accelerates immune-mediated destruction of β cells in nonobese diabetic mice. J Exp Med 179:1379-1384, 1994
38. Wang B, Gonzalez A, Hoglund P, Katz JD, Benoist C, Mathis D: Interleukin-4 deficiency does not exacerbate disease in NOD mice. Diabetes 47:1207-1211, 1998
39. Pakala SV, Kurrer MO, Katz JD: T helper 2 (Th2) T cells induce acute pancreatitis and diabetes in immune-compromised nonobese diabetic (NOD) mice. J Exp Med 186:299-306, 1997
40. Huang X, Yuan J, Goddard A, Foulis A, James RFL, Lernmark A, Pujol-Borrel R, Rabinovitch A, Somoza N, Stewart TA: Interferon expression in the pancreases of patients with type 1 diabetes. Diabetes 44:658-664, 1995
41. de Vries JE: The role of IL-13 and its receptor in allergy and inflammatory responses. J Allergy Clin Immunol 102:165-169, 1998
42. Minty A, Chalon P, Derocq JM, Dumont X, Guillemot JC, Kaghad M, Leplatois P, Liauzun P, Miloux B, Minty C, Casellas P, Loison G, Lupker J, Shire D, Ferrara P, Caput D: Interleukin 13 is a new human lymphokine regulating inflammatory and immune responses. Nature 362:248-250, 1993
43. Baumhofer JM, Beinhauer BG, Wang JE, Brandmeier H, Geissler K, Losert U, Philip R, Aversa G, Rogy MA: Gene transfer with IL4 and IL-13 improves survival in lethal endotoxemia in the mouse and ameliorates peritoneal macrophages immune competence. Eur J Immunol 28:610-615, 1998
44. Bagenstose LM, Salgame P, Monestier M: IL-12 down-regulates autoantibody production in mercury-induced autoimmunity. J Immunol 160:1612-1617, 1998
45. Rossini AA, Handler ES, Mordes JP, Greiner DL: Animal models of human disease: human autoimmune diabetes mellitus: lessons from BB rats and NOD mice-Caveat Emptor. Clin Immunol Immunopathol 74:2-9, 1995
46. Parish NM, Hutchings PR, O'Reilly L, Quartey-Papaflo L, Healey D, Ozegbe P, Cooke A: Tolerance induction as a therapeutic strategy for the control of autoimmune endocrine disease in mouse models. Immunol Rev 144:269-300, 1995
47. Kolb H: Mouse models of insulin-dependent diabetes: low dose streptozotocin-induced diabetes and non obese diabetic (NOD) mice. Diabetes Metab Rev 3:751-778, 1987
48. Matthys P, Froyen G, Verdot L, Huang S, Sobis H, Van Damme J, Vray B, Aguet M, Billiau A: IFN-gamma-receptor deficient mice are hypersensitive to the anti-CD3-induced cytokine release syndrome and thymocyte apoptosis: protective role of endogenous nitric oxide. J Immunol 155:3823-3829, 1995
49. Emson CL, Bell SE, Jones A, Wisden W, McKenzie AN: Interleukin (IL)-4-independent induction of immunoglobulin (Ig)E, and perturbation of T cell development in transgenic mice expressing IL-13. J Exp Med 188:399-404, 1998
50. Minty A, Asselin S, Bensussan A, Shire D, Vita N, Vyakarnam A, Wydenes J, Ferrara P, Caput D: The related cytokines interleukin-13 and interleukin-4 are distinguished by differential production and differential effects on T lymphocytes. Eur Cytokine Netw 8:203-213, 1997
51. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN: A distinct role for interleukin-13 in Th2 cell mediated immune responses. Curr Biol 8:339-342, 1998
52. Lentsch AB, Shanley TP, Sarma V, Ward PA: In vivo suppression of NF-kB and preservation of IkB α by interleukin-10 and interleukin-13. J Clin Invest 100:2443-2448, 1997
53. Muchamuel T, Menon S, Pisacane P, Howard MC, Cockayne DA: IL-13 protects mice from lipopolysaccharide-induced lethal endotoxemia: correlation with down-modulation of TNF-α, IFN-γ and IL-12 production. J Immunol 158:2898-2903, 1997
54. Nicoletti F, Mancuso G, Cusumano V, Di Marco R, Zaccone P, Bendtzen K, Teti G: Prevention of endotoxin-induced lethality in neonatal mice by interleukin-13. Eur J Immunol 27:1580-1583, 1997
55. Bessis N, Boissier MC, Ferrara P, Blankenstein T, Fradelizi D, Fournier C: Attenuation of collagen-induced arthritis in mice by treatment with vector cells engineered to secrete interleukin-13. Eur J Immunol 26:2399-2403, 1996
56. Cash E, Minty A, Ferrara P, Caput D, Fradelizi D, Rott O: Macrophage-inactivating IL-13 suppresses experimental autoimmune encephalomyelitis in rats. J Immunol 153:4258-4267, 1994
57. Mulligan MS, Warner RL, Foreback JL, Shanley TP, Ward PA: Protective effects of IL4, IL-10, IL-12 and IL-13 in IgG immune complex-induced lung injury: role of endogenous IL-12. J Immunol 159:3483-3489, 1997
58. McKenzied GJ, Emson CL, Bell SE, Anderson S, Fallon P, Zurawski G, Murray R, Grencis R, McKenzie AN: Impaired development of Th2 cells in IL-13 deficient mice. Immunity 9:423-432, 1998
59. Vannier E, de Waal Malefyt R, Salazar-Montes A, de Vries JE, Dinarello CA: Interleukin-13 (IL-13) induces IL-1 receptor antagonist gene expression and protein synthesis in peripheral blood mononuclear cells: inhibition by an IL-4 mutant. Blood 87:3307-3315, 1996
60. Doherty TM, Kastelein R, Menon S, Andrade S, Coffinan L: Modulation of murine macrophage function by IL-13. J Immunol 151:7151-7160, 1993
61. Sternesjo J, Sandler S: Interleukin-13 counteracts suppression induced by interleukin-1 beta of glucose metabolism but not of insulin secretion in rat pancreatic islets. Autoimmunity 26:153-159, 1997
62. Manna SK, Aggarwal BB: IL-13 suppresses TNF-induced activation of nuclear factor-kB, activation protein-1 and apoptosis. J Immunol 161:2863-2872, 1998
63. Mauricio D, Mandrup-Poulsen T: Apoptosis and the pathogenesis of IDDM: a question of life and death. Diabetes 47:1537-1543, 1998
64. Di Santo E, Meazza C, Sironi M, Fruscella P, Mantovani A, Sipe JD, Ghezzi P: IL-13 inhibits TNF production but potentiates that of IL-6 in vivo and ex vivo mice. J Immunol 1:379-382, 1997
65. + T cells. J Exp Med 185: 461-469, 1997
66. Zurawski G, De Vries J: Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol Today 15:19-26, 1994
67. Wicker L, Miller BJ, Mullen Y: Transfer of autoimmune diabetes mellitus with splenocytes from nonobese diabetic (NOD) mice. Diabetes 35:855-860, 1986