In autoimmune diabetes the transition from benign to pernicious insulitis requires an islet cell response to tumor necrosis factor α

Journal of Experimental Medicine

Volumn 189, Issue 7, 1999, Pages 1053-1062

  Pakala, Syamasundar V ^a   Chivetta, Marylee ^a   Kelly, Colleen B ^a   Katz, Jonathan D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; Diabetes; Insulitis; T cells; Tumor necrosis factor receptor

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DIABETES MELLITUS; EFFECTOR CELL; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; TARGET CELL; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD95; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CHIMERA; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; GENE TARGETING; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; NEPHRECTOMY; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PANCREATITIS; RECEPTORS, INTERFERON; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; STREPTOZOCIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0033526068     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.7.1053     Document Type: Article

References (58)

1. Bach, J.F. 1994. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15:516-542.
2. Atkinson, M.A., and N.K. MacLaren. 1994. The pathogenesis of insulin-dependent diabetes mellitus. N. Engl. J. Med. 331:1428-1436.
3. Tisch, R., and H. McDevitt. 1996. Insulin-dependent diabetes mellitus. Cell. 85:291-297.
4. Charlton, B., A. Bacelj, and T.E. Mandel. 1988. Administration of silica particles or anti-Lyt2 antibody prevents β-cell destruction in NOD mice given cyclophosphamide. Diabetes. 37:930-935.
5. + T cell subsets are required for transfer of diabetes in nonobese diabetic mice. J. Immunol. 140:52-58.
6. Kurrer, M.O., S.V. Pakala, H.L. Hanson, and J.D. Katz. 1997. Beta cell apoptosis in T cell-mediated autoimmune diabetes. Proc. Natl. Acad. Sci. USA. 94:213-218.
7. O'Brien, B.A., B.V. Harmon, D.P. Cameron, and D.J. Allan. 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.
8. O'Brien, B.A., B.V. Harmon, D.P. Cameron, and D.J. Allan. 1996. Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J. Pathol. 178:176-181.
9. Pober, J.S., and R.S. Cotran. 1990. Cytokines and endothelial cell biology. Physiol. Rev. 70:427-451.
10. Pujol-Borrell, R., I. Todd, M. Doshi, G.F. Bottazzo, R. Sutton, D. Gray, G. Adolf, and M. Feldmann. 1987. HLA class II induction on human islets by interferon-gamma plus tumor necrosis factor or lymphotoxin. Nature. 326:304-306.
11. Feldmann, M., F.M. Brennan, and R. Maini. 1996. Role of cytokines in rheumatoid arthritis. Annu. Rev. Immunol. 14: 397-440.
12. Old, L.J. 1985. Tumor necrosis factor (TNF). Science. 230: 630-632.
13. Abbas, A.K., K.M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature. 383:787-793.
14. Satoh, J., H. Seino, T. Abo, S. Tanaka, S. Shintani, S. Ohta, K. Tamura, T. Sawai, T. Nobunaga, T. Oteki, et al. 1989. Recombinant human tumor necrosis factor α suppresses autoimmune diabetes in nonobese diabetic mice. J. Clin. Invest. 84:1345-1348.
15. Jacob, C.O., S. Aiso, S.A. Michie, H.O. McDevitt, and H. Acha-Orbea. 1990. Prevention of diabetes in nonobese diabetic mice by tumor necrosis factor (TNF): similarities between TNF-α and interleukin 1. Proc. Natl. Acad. Sci. USA. 87:968-972.
16. Yang, X.D., R. Tisch, S.M. Singer, Z.A. Cao, R.S. Liblau, R.D. Schreiber, and H.O. McDevitt. 1994. 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.
17. Picarella, D.E., A. Kratz, C.B. Li, N.H. Ruddle, and R.A. Flavell. 1993. Transgenic tumor necrosis factor (TNF)-alpha production in pancreatic islets leads to insulitis, not diabetes. Distinct patterns of inflammation in TNF-alpha and TNF-beta transgenic mice. J. Immunol. 150:4136-4150.
18. Higuchi, Y., P. Herrera, P. Muniesa, J. Huarte, D. Belin, P. Ohashi, P. Aichele, L. Orci, J.D. Vassalli, and P. Vassalli. 1992. Expression of a tumor necrosis factor alpha transgene in murine pancreatic β cells results in severe and permanent insulitis without evolution towards diabetes. J. Exp. Med. 176:1719-1731.
19. Grewal, I.S., K.D. Grewal, F.S. Wong, D.E. Picarella, C.A. Janeway, Jr., and R.A. Flavell. 1996. Local expression of transgene encoded TNF-α in islets prevents autoimmune diabetes in nonobese diabetic (NOD) mice by preventing the development of auto-reactive islet-specific T cells. J. Exp. Med. 184:1963-1974.
20. Cope, A.P., R.S. Liblau, X.D. Yang, M. Congia, C. Laudanna, R.D. Schreiber, L. Probert, G. Kollias, and H.O. McDevitt. 1997. Chronic tumor necrosis factor alters T cell responses by attenuating T cell receptor signaling. J. Exp. Med. 185:1573-1584.
21. Wang, B., I. Andre, A. Gonzalez, J.D. Katz, M. Aguet, C. Benoist, and D. Mathis. 1997. Interferon gamma impacts at multiple points during the progression of autoimmune diabetes. Proc. Natl. Acad. Sci. USA. 94:13844-13849.
22. von Herrath, M.G., and M.B. Oldstone. 1997. Interferon γ is essential for destruction of β cells and development of insulin-dependent diabetes mellitus. J. Exp. Med. 185:531-539.
23. Hultgren, B., X. Huang, N. Dybdal, and T.A. Stewart. 1996. Genetic absence of gamma-interferon delays but does not prevent diabetes in NOD mice. Diabetes. 45:812-817.
24. Boehm, U., T. Klamp, M. Groot, and J. Howard. 1997. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15:749-795.
25. Deiss, L., H. Galinka, H. Berissi, O. Cohen, and A. Kimichi. 1996. Cathepsin-D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-α. EMBO (Eur. Mol. Biol. Organ.) J. 15:3861-3870.
26. Chaudhary, P., M. Eby, A. Jasmin, A. Bookwalter, J. Murray, and L. Hood. 1997. Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-κB pathway. Immunity. 7:821-830.
27. Ankarcrona, M., J.M. Dypbukt, B. Brune, and P. Nicotera. 1994. Interleukin-1 beta-induced nitric oxide production activates apoptosis in pancreatic RINm5F cells. Exp. Cell Res. 213:172-177.
28. Cailleau, C., A. Diu-Hercend, E. Ruuth, R. Westwood, and C. Carnaud. 1997. Treatment with neutralizing antibodies specific for IL-1β prevents cyclophosphamide-induced diabetes in nonobese diabetic mice. Diabetes. 46:937-940.
29. Corbett, J.A., J.L. Wang, M.A. Sweetland, J.R. Lancaster, Jr., and M.L. McDaniel. 1992. Interleukin 1β induces the formation of nitric oxide by β cells purified from rodent islets of Langerhans. Evidence for the β-cell as a source and site of action of nitric oxide. J. Clin. Invest. 90:2384-2391.
30. Itoh, N., A. Imagawa, T. Hanafusa, M. Waguri, K. Yamamoto. H. Iwahashi, M. Moriwaki, H. Nakajima, J. Miyagawa, M. Namba, et al. 1997. Requirement of Fas for the development of autoimmune diabetes in nonobese diabetic mice. J. Exp. Med. 186:613-618.
31. Chervonsky, A.V., Y. Wang, F.S. Wong, I. Visintin, R.A. Flavell, C.A. Janeway, Jr., and L.A. Matis. 1997. The role of Fas in autoimmune diabetes. Cell. 89:17-24.
32. Katz, J.D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell. 74:1089-1100.
33. Huang, S., W. Hendriks, A. Althage, S. Hemmi, H. Bluethmann, R. Kamijo, J. Vilcek, R.M. Zinkernagel, and M. Aguet. 1993. Immune response in mice that lack the interferon-gamma receptor. Science. 259:1742-1745.
34. Rothe, J., W. Lesslauer, H. Lotscher, Y. Lang, P. Koebel, F. Kontgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann. 1993. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature. 364: 798-802.
35. Erickson, S.L., F.J. de Sauvage, K. Kikly, K. Carver-Moore, S. Pitts-Meek, N. Gillett, K.C. Sheehan, R.D. Schreiber, D.V. Goeddel, and M.W. Moore. 1994. Decreased sensitivity to tumour-necrosis factor but normal T-cell development in TNF receptor-2-deficient mice. Nature. 372:560-563.
36. MacMicking, J.D., C. Nathan, G. Horn, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:641-650. (See published erratum 81: following 1170.)
37. d haplotype. Immunogenetics. 31:333-339.
38. Lacy, P.E., and M. Kostianovsky. 1967. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes. 16:35-39.
39. Sullivan, F.P., C. Ricordi, V. Hauptfeld, and P.E. Lacy. 1987. Effect of low temperature culture and site of transplantation on hamster islet xenograft survival (hamster to mouse). Transplantation. 44:465-468.
40. Leenen, P.J., M.F. de Bruijn, J.S. Voerman, P.A. Campbell, and W. van Ewijk. 1994. Markers of mouse macrophage development detected by monoclonal antibodies. J. Immunol. Methods. 174:5-19.
41. Streeter, P.R., B.T. Rouse, and E.C. Butcher. 1988. Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J. Cell Biol. 107:1853-1862.
42. Pakala, S.V., M.O. Kurrer, and J.D. Katz. 1997. T helper 2 (Th2) T cells induce acute pancreatitis and diabetes in immune-compromised nonobese diabetic (NOD) mice. J. Exp. Med. 186:299-306.
43. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137.
44. Shinkai, Y., S. Koyasu, K. Nakayama, K.M. Murphy, D.Y. Loh, E.L. Reinherz, and F.W. Alt. 1993. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science. 259:822-825.
45. Kuhn, R., F. Schwenk, M. Aguet, and K. Rajewsky. 1995. Inducible gene targeting in mice. Science. 269:1427-1429.
46. Gianani, R., and N. Sarvetnick. 1996. Viruses, cytokines, antigens, and autoimmunity. Proc. Natl. Acad. Sci. USA. 93: 2257-2259.
47. + islet-specific T cell clone. Science. 249:1433-1436.
48. Haskins, K., M. Portas, B. Bradley, D. Wedmann, and K.J. Lafferty. 1988. T-lymphocyte clone specific for pancreatic islet antigen. Diabetes. 37:1444-1448.
49. Haskins, K., M. Portas, B. Bergman, K. Lafferty, and B. Bradley. 1989. Pancreatic islet-specific T-cell clones from nonobese diabetic mice. Proc. Natl. Acad. Sci. USA. 86:8000-8004.
50. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science. 267:1449-1456.
51. Stassi, G., R.D. Maria, G. Trucco, W. Rudert, R. Testi, A. Galluzzo, C. Giordano, and M. Trucco. 1997. Nitric oxide primes pancreatic β cells for Fas-mediated destruction in insulin-dependent diabetes mellitus. J. Exp. Med. 186:1193-1200.
52. McDaniel, M.L., G. Kwon, J.R. Hill, C.A. Marshall, and J.A. Corbett. 1996. Cytokines and nitric oxide in islet inflammation and diabetes. Proc. Soc. Exp. Biol. Med. 211:24-32.
53. Jacob, C.O., S. Aiso, R.D. Schreiber, and H.O. McDevitt. 1992. Monoclonal anti-tumor necrosis factor antibody renders non-obese diabetic mice hypersensitive to irradiation and enhances insulitis development. Int. Immunol. 4:611-614.
54. Green, E.A., E.E. Eynon, and R.A. Flavell. 1998. Local expression of TNF-α in neonatal NOD mice promotes diabetes by enhancing presentation of islet antigens. Immunity. 9:733-743.
55. Picarella, D.E., A. Kratz, C.B. Li, N.H. Ruddle, and R.A. Flavell. 1992. Insulitis in transgenic mice expressing tumor necrosis factor beta (lymphotoxin) in the pancreas. Proc. Natl. Acad. Sci. USA. 89:10036-10040.
56. Kurts, C., W.R. Heath, F.R. Carbone, J. Allison, J.F. Miller, and H. Kosaka. 1996. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184: 923-930.
57. + T cells. J. Exp. Med. 186:239-245.
58. André, I., A. Gonzalez, B. Wang, J. Katz, C. Benoist, and D. Mathis. 1996. Checkpoints in the progression of autoimmune disease: lessons from diabetes models. Proc. Natl. Acad. Sci. USA. 93:2260-2263.