Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes

Journal of Experimental Medicine

Volumn 189, Issue 2, 1999, Pages 331-339

  Höglund, Petter ^a   Mintern, Justine ^b   Waltzinger, Caroline ^a   Heath, William ^b   Benoist, Christophe ^a   Mathis, Diane ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Antigen presentation; Autoimmunity; Nonobese diabetic; T lymphocytes; Transgenic mice

Indexed keywords

SUPERANTIGEN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNITY; DIABETES MELLITUS; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PANCREAS ISLET CELL; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; ANTIGEN PRESENTATION; CELL DIVISION; DIABETES MELLITUS, TYPE 1; FLOW CYTOMETRY; ISLETS OF LANGERHANS; LYMPH NODES; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; PANCREAS; RECEPTORS, ANTIGEN, T-CELL; SPLEEN; T-LYMPHOCYTES;

EID: 0033579875     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.2.331     Document Type: Article

References (56)

1. Bach, J.F. 1994. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15:516-542.
2. Tisch, R., and H. McDevitt. 1996. Insulin-dependent diabetes mellitus. Cell. 85:291-297.
3. Bach, J.F., and D. Mathis. 1997. 70th forum in immunology: the NOD mouse. Res. Immunol. 148:285-286.
4. Leslie, R.D., and R.B. Elliott. 1994. Early environmental events as a cause of IDDM. Evidence and implications. Diabetes. 43:843-850.
5. Herrath, M.G., A. Holz, D. Homann, and M.B.A. Oldstone. 1998. Role of viruses in type I diabetes. Semin. Immunol. 10: 87-100.
6. Singh, B., S. Prange, and A.M. Jevnikar. 1998. Protective and destructive effects of microbial infection in insulin-dependent diabetes mellitus. Semin. Immunol. 10:79-86.
7. Wong, F.S., and C.A. Janeway, Jr. 1997. The role of CD4 and CD8 T cells in type I diabetes in the NOD mouse. Res. Immunol. 148:327-332.
8. + T lymphocytes: clarification of their pathogenic roles in diabetes in the NOD mouse. Res. Immunol. 148:320-327.
9. Nepom, G.T. 1995. Glutamic acid decarboxylase and other autoantigens in IDDM. Curr. Opin. Immunol. 7:825-830.
10. Roep, B.O. 1996. T-cell responses to autoantigens in IDDM. The search for the Holy Grail. Diabetes. 45:1147-1156.
11. Wegmann, D.R. 1996. The immune response to islets in experimental diabetes and insulin-dependent diabetes mellitus. Curr. Opin. Immunol. 8:860-864.
12. Butcher, E.G., and L.J. Picker. 1996. Lymphocyte homing and homeostasis. Science. 272:60-66.
13. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
14. 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.
15. Haskins, K., M. Portas, B. Bradley, D. Wegmann, and K.J. Lafferty. 1988. T-lymphocyte clone specific for pancreatic islet antigen. Diabetes. 37:1444-1448.
16. + islet-specific T-cell clone. Science. 249:1433-1436.
17. Gonzalez, A., J.D. Katz, M.G. Mattei, H. Kikutani, C. Benoist, and D. Mathis. 1997. Genetic control of diabetes progression. Immunity. 7:873-883.
18. Philpott, K.L., J.L. Viney, G. Kay, S. Rastan, E.M. Gardiner, S. Chae, A.C. Hayday, and M.J. Owen. 1992. Lymphoid development in mice congenitally lacking T cell receptor αβ-expressing cells. Science. 256:1448-1452.
19. Mombaerts, P., J. Iacomini, R.S. Johnson, K. Herrup, S. Tonegawa, and V.E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 68:869-877.
20. 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.
21. Cosgrove, D., D. Gray, A. Dierich, J. Kaufman, M. Lemeur, C. Benoist, and D. Mathis. 1991. Mice lacking MHC class II molecules. Cell. 66:1051-1066.
22. Trowbridge, I.S., J. Lesley, R. Schuite, R. Human, and J. Trotter. 1982. Biochemical characterization and cellular distribution of a polymorphic, murine cell-surface glycoprotein expressed on lymph node cells. Immunogen. 15:299-305.
23. Gallatin, W.M., I.L. Weissman, and E.G. Butcher. 1983. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 304:30-34.
24. a haplotypes: determination with a Vα2-specific monoclonal antibody. Eur. J. Immunol. 22: 399-404.
25. Kurts, C., J.F.A.P. Miller, R.M. Subramanian, F.R. Carbone, and W.R. Heath. 1998. MHC class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J. Exp. Med. 188:409-414.
26. Bruce, J., F.W. Symington, T.J. McKearn, and J. Sprent. 1981. A monoclonal antibody discriminating between subsets of T and B cells. J. Immunol. 127:2496-2501.
27. Ceredig, R., J.W. Lowenthal, M. Nabholz, and H.R. MacDonald. 1985. Expression of interleukin-2 receptors as a differentiation marker on intrathymic stem cells. Nature. 314: 98-100.
28. Katz, J., C. Benoist, and D. Mathis. 1993. Major histocompatibility complex class I molecules are required for the development of insulitis in non-obese diabetic mice. Eur. J. Immunol. 23:3358-3360.
29. Wicker, L.S., E.H. Leiter, J.A. Todd, R.J. Renjilian, E. Peterson, P.A. Fischer, P.L. Podolin, M. Zijlstra, R. Jaenisch, and L.B. Peterson. 1994. β2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes. 43:500-504.
30. null mice are diabetes and insulitis resistant. Diabetes. 43:505-509.
31. Sumida, T., M. Furukawa, A. Sakamoto, T. Namekawa, T. Maeda, M. Zijlstra, I. Iwamoto, T. Koike, S. Yoshida, H. Tomioka, and M. Taniguchi. 1994. Prevention of insulitis and diabetes in β2-microglobulin-deficient non-obese diabetic mice. Int. Immunol. 6:1445-1449.
32. + T cells in initiation of insulin-dependent diabetes mellitus. Eur. J. Immunol. 26:1762-1769.
33. Wong, F.S., I. Visintin, L. Wen, R.A. Flavell, and C.A. Janeway, Jr. 1996. CD8 T cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells. J. Exp. Med. 183: 67-76.
34. Serreze, D.V., H.D. Chapman, D.S. Varnum, I. Gerling, E.H. Leiter, and L.D. Shultz. 1997. Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J. Immunal. 158:3978-3986.
35. Lühder, F., P. Höglund, J.P. Allison, C. Benoist, and D. Mathis. 1998. Cytotoxic T lymphocyte-associated antigen 4 regulates the unfolding of autoimmune diabetes. J. Exp. Med. 187:427-432.
36. 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.
37. Scott, B., R. Liblau, S. Degermann, L.A. Marconi, L. Ogata, A.J. Caton, H.O. McDevitt, and D. Lo. 1994. A role for non-MHC genetic polymorphism in susceptibility to spontaneous autoimmunity. Immunity. 1:73-82.
38. Sarukhan, A., A. Lanoue, A. Franzke, N. Brousse, J. Buer, and H. von Boehmer. 1998. Changes in function of antigen-specific lymphocytes correlating with progression towards diabetes in a transgenic model. EMBO (Eur. Mol. Biol. Organ.) J. 17:71-80.
39. + T cell-mediated spontaneous diabetes in neonatal mice. J. Immunol 157:978-983.
40. Forster, I., and I. Lieberam. 1996. Peripheral tolerance of CD4 T cells following local activation in adolescent mice. Eur. J. Immunol. 26:3194-3202.
41. Bruno, L., H. von Boehmer, and J. Kirberg. 1996. Cell division in the compartment of naive and memory T lymphocytes. Eur. J. Immunol. 26:3179-3184.
42. Adams, T.E., S. Alpert, and D. Hanahan. 1987. Non-tolerance and autoantibodies to a transgenic self antigen expressed in pancreatic beta cells. Nature. 325:223-228.
43. Heath, W.R., C. Kurts, J.F.A.P. Miller, and F.R. Carbone. 1998. Cross-tolerance: a pathway for inducing tolerance to peripheral tissue antigens. J. Exp. Med. 187:1549-1553.
44. Bergman, B., and K. Haskins. 1994. Islet-specific T-cell clones from the NOD mouse respond to beta-granule antigen. Diabetes. 43:197-203.
45. Dahlen, E., K. Dawe, L. Ohlsson, and G. Hedlund. 1998. Dendritic cells and macrophages are the first and major producers of TNF-alpha in pancreatic islets in the nonobese diabetic mouse. J. Immunol. 160:3585-3593.
46. Lo, D., C.R. Reilly, B. Scott, R. Liblau, H.O. McDevitt, and L.C. Burkly. 1993. Antigen-presenting cells in adoptively transferred and spontaneous autoimmune diabetes. Eur. J. Immunol. 23:1693-1698.
47. Jansen, A., F. Homo-Delarche, H. Hooijkaas, P.J. Leenen, M. Dardenne, and H.A. Drexhage. 1994. Immunohistochemical characterization of monocytes-macrophages and dendritic cells involved in the initiation of the insulitis and beta-cell destruction in NOD mice. Diabetes. 43:667-675.
48. Katz, J.D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulin-dependent diabetes. Science. 268:1185-1188.
49. Lu, C.Y., E.G. Calamai, and E.R. Unanue. 1979. A defect in the antigen-presenting function of macrophages from neonatal mice. Nature. 282:327-329.
50. Rafii-Tabar, E., and A.A. Czitrom. 1986. Ontogeny of priming of cytotoxic T cells to minor alloantigens: the development of direct priming precedes that of cross-priming. Eur. J. Immunol. 16:1025-1027.
51. 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.
52. Roep, B.O., S.D. Arden, R.R. de Vries, and J.C. Hutton. 1990. T-cell clones from a type-1 diabetes patient respond to insulin secretory granule proteins. Nature. 345:632-634.
53. Larger, E., C. Becourt, J.F. Bach, and C. Boitard. 1995. Pancreatic islet beta cells drive T cell-immune responses in the nonobese diabetic mouse model. J. Exp. Med. 181:1635-1642.
54. Balasa, B., T. Krahl, G. Patstone, J. Lee, R. Tisch, H.O. McDevitt, and N. Sarvetnick. 1997. CD40 ligand-CD40 interactions are necessary for the initiation of insulitis and diabetes in nonobese diabetic mice. J. Immunol. 159:4620-4627.
55. Yang, X.D., H.K. Sytwu, H.O. McDevitt, and S.A. Michie. 1997. Involvement of beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAdCAM-1) in the development of diabetes in obese diabetic mice. Diabetes. 46:1542-1547.
56. Clare-Salzler, M., and Y. Mullen. 1992. Marked dendritic cell-T cell cluster formation in the pancreatic lymph node of the non-obese diabetic mouse. Immunology. 76:478-484.