The role of macrophages in T cell-mediated autoimmune diabetes in nonobese diabetic mice

Journal of Experimental Medicine

Volumn 189, Issue 2, 1999, Pages 347-358

  Jun, Hee Sook ^a   Yoon, Chang Soon ^a   Zbytnuik, Lori ^a   Van Rooijen, Nico ^c   Yoon, Ji Won ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b Ajou University   (South Korea)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Autoimmune diabetes; Macrophages; Nonobese diabetic mice; T cell activation; T cells

Indexed keywords

FAS LIGAND; INTERLEUKIN 12; PERFORIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DIABETES MELLITUS; FEMALE; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; AUTOIMMUNITY; CELL DIFFERENTIATION; CLODRONIC ACID; CYTOTOXICITY, IMMUNOLOGIC; DIABETES MELLITUS; FAS LIGAND PROTEIN; FEMALE; INTERLEUKIN-12; ISLETS OF LANGERHANS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED NOD; PANCREAS; PORE FORMING CYTOTOXIC PROTEINS; SPLEEN; T-LYMPHOCYTES; TISSUE TRANSPLANTATION;

EID: 0033579877     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.2.347     Document Type: Article

References (60)

1. + T cells in type I diabetes in the NOD mouse. 7th Forum in Immunology. 327-332.
2. Delovitch, T.L., and S. Bhagirath. 1997. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity. 7:727-738.
3. Yoon, J.W., H.S. Jun, and P.S. Santamaria. 1998. Cellular and molecular mechanisms for the initiation and progression of β-cell destruction resulting from the collaboration between macrophages and T cells. Autoimmunity. 127:109-122.
4. + T-cell clones derived from lymphocytes infiltrating the islets of NOD mice. Diabetes. 41:998-1008.
5. + islet-specific T cell clone. Science. 249:1433-1436.
6. Haskins, K., M. Portas, B. Bradley, D. Wegmann, and K. Lafferty. 1988. T-lymphocyte clone specific for pancreatic islet antigen. Diabetes. 37:1444-1448.
7. Wong, S., L. Wen, I. Visintin, 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 the absence of CD4 T cells. J. Exp. Med. 183:67-76.
8. Nagata, M., P. Santamaria, T. Kawamura, T. Utsugi, and J.W. Yoon. 1994. Evidence for the role of CD8+ cytotoxic T cells in the destruction of pancreatic beta cells in NOD mice. J. Immunol 152:2042-2050.
9. Utsugi, T., J.W. Yoon, B.J. Park, M. Imamura, N. Averil, S. Kawazu, and P. Santamaria. 1996. Major histocompatibility complex class I-restricted infiltration and destruction of pancreatic islets by NOD mouse-derived beta cell cytotoxic CD8+ T cell clones in vivo. Diabetes. 45:1121-1131.
10. 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.
11. Verdaguer, J., J.W. Yoon, N. Averil, T. Utsugi, B.J. Park, and P. Santamaria. 1996. Acceleration of diabetes in NOD mice expressing beta cell-cytotoxic T cell-derived TCRβ transgene. J. Immunol. 157:4726-4735.
12. Katz, J.D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulin-dependent diabetes. Science. 268:1185-1190.
13. Kolb, H., G. Kantwerk, U. Treichel, T. Kurner, U. Kiesel, T. Hoppe, and V. Kolb-Bachofen. 1986. Prospective analysis of islet lesions in BB rats. Diabetologia. 29(Suppl. 1):A559.
14. Lee, K.U., M.K. Kim, K. Amano, C.Y. Pak, M.A. Jaworski, J.G. Mehta, and J.W. Yoon. 1989. Preferential infiltration of macrophages during early stages of insulitis in diabetes-prone BB rats. Diabetes. 37:1053-1058.
15. Voorbij, H.A.M., P.H.M. Jeucken, P.J. Kabel, M. DeHaan, and H.A. Drexhage. 1989. Dendritic cells and scavenger macrophages in pancreatic islets of prediabetic BB rats. Diabetes. 38:1623-1629.
16. Walker, R., A.J. Bone, A. Cooke, and J.D. Baird. 1988. Distinct macrophage subpopulations in pancreas of prediabetic BB/E rats: possible role for macrophages in pathogenesis of IDDM. Diabetes. 37:1301-1304.
17. Jasen, A., R. Homo-Delarche, H. Hooijkaas, P.J. Leenen, M. Dardenne, and H.A. Drexhage. 1994. Immunohistochemical characterization of monocyte-macrophages and dendritic cells involved in the initiation of insulitis and beta-cell destruction in NOD mice. Diabetes. 43:667-675.
18. Amano, K., and J.W. Yoon. 1990. Studies on autoimmunity for initiation of beta-cell destruction. V. Decrease of macrophage dependent T-effector cells and natural killer cytotoxicity in silica-treated BB rats. Diabetes. 39:590-596.
19. Lee, K.U., K. Amano, and J.W. Yoon. 1988. Evidence for initial involvement of macrophage in development of insulitis in NOD mice. Diabetes. 37:989-991.
20. Oschilewski, U., U. Kiesel, and H. Kolb. 1985. Administration of silica prevents diabetes in BB rats. Diabetes. 34:197-199.
21. Lee, K.U., C.Y. Pak, K. Amano, and J.W. Yoon. 1988. Prevention of lymphocytic thyroiditis and insulitis in diabetes-prone BB rats by the depletion of macrophages. Diabetologia. 31:400-402.
22. van Rooijen, N., and A. Sanders. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods. 174:83-93.
23. Chung, Y.H., H.S. Jun, Y. Kang, K. Hirasawa, B.R. Lee, N. Van Rooijen, and J.W. Yoon. 1997. Role of macrophages and macrophage-derived cytokines in the pathogenesis of Kilham rat virus-induced diabetes in diabetes-resistant BB rats J. Immunol. 159:466-471.
24. Kawamura, T., M. Nagata, T. Utsugi, and J.W. Yoon. 1993. Prevention of autoimmune type I diabetes by CD4+ suppressor T cells in superantigen-treated nonobese diabetic mice. J. Immunol. 151:4362-4370.
25. Yoon, J.W., P.R. McClintock, T. Onodera, and A.L. Not-\ kins. 1980. Virus-induced diabetes mellitus. XVIII. Inhibition by a nondiabetogenic variant of encephalomyocarditis virus. J. Exp. Med. 152:878-892.
26. Yoon, J.W., M.M. Rodriguez, C. Currier, and A. Notkins. 1982. Long-term complications of virus-induced diabetes mellitus in mice. Nature. 296:566-569.
27. Utsugi, T., M. Nagata, T. Kawamura, and J.W. Yoon. 1994. Prevention of recurrent diabetes in syngeneic islet-transplanted NOD mice by transfusion of autoreactive T lymphocytes. Transplantation. 57:1799-1804.
28. Han, H.S., H.S. Jun, T. Utsugi, and J.W. Yoon. 1996. A new type of CD4+ suppressor T cell completely prevents spontaneous autoimmune diabetes and recurrent diabetes in syngeneic islet-transplanted NOD mice. J. Autoimmunity. 9:331-339.
29. Naito, M., N. Hirotaka, S. Kawano, H. Umezu, H. Zhu, H. Moriyama, T. Yamomoto, H. Takatsuka, and Y. Takei. 1996. Liposome-encapsulated dichloro-methylene diphosphonate induces macrophage apoptosis in vivo and in vitro. J. Leukocyte Biol. 60:337-344.
30. van Rooijen, N., A.M. Sanders, and T.K. van den Berg. 1996. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J. Immunol. Methods. 193:93-99.
31. Szabo, S.J., A.S. Dighe, U. Gubler, and K.M. Murphy. 1997. Regulation of the IL-12R β2 subunit expression in developing Th1 and Th2 cells. J. Exp. Med. 185:817-824.
32. Bretscher, P. 1992. The two-signal model of lymphocyte activation twenty-one years later. Immunol. Today. 13:74-76.
33. Kurrer, M.O., S.V. Pakala, H.L. Hanson, and J.D. Katz. 1997. β cell apoptosis in T cell-mediated autoimmune diabetes. Proc. Natl. Acad. Sci. USA. 94:213-218.
34. van Rooijen, N., J. Bakker, and A.M. Sanders. 1997. Transient suppression of macrophage functions by liposome-encapsulated drugs. Trends Biotechnol. 15:178-185.
35. van Rooijen, N., and A.M. Sanders. 1997. Elimination, blocking, and activation of macrophages: three of a kind? J. Leukocyte Biol. 62:702-709.
36. van Rooijen, N., and R. van Nieuwmegen. 1984. Elimination of phagocytic cells in the spleen after intravenous injection of liposome encapsulated dichloromethylene diphosphonate. An enzyme histochemical study. Cell Tissue Res. 238:355-358.
37. van Rooijen, N., R. van Nieuwmegen, and E.W.A. Kamperdijk. 1985. Elimination of phagocytic cells in the spleen after intravenous injection of liposome encapsulated dichloromethylene diphosphonate. Ultra-structural aspects of elimination of marginal zone macrophages. Virchows Arch. B Cell Pathol. 49:375-383.
38. 2MDP-liposome-mediated macrophage depletion. J. Immunol. Methods. 134:153-161.
39. Claassen, I., N. van Rooijen, and E. Claassen. 1995. A new method for removal of mononuclear phagocytes from heterogeneous cell populations in vitro, using the liposome-mediated 'suicide' technique. Blood. 86:183-192.
40. + T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today. 16:34-38.
41. Zipris, D., D.L. Greiner, S. Malkani, B. Whalen, J.P. Mordes, and A.A. Rossini. 1996. Cytokine gene expression in islets and thyroids of BB rats: IFN-γ and IL-12p40 mRNA increase with age in both diabetic and insulin-treated nondiabetic BB rats J. Immunol. 156:1315-1321.
42. Rabinovitch, A. 1994. Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM: therapeutic intervention by immunostimulation? Diabetes. 43:613-621.
43. Fox, C.J., and J.S. Danska. 1997. IL-4 expression at the onset of islet inflammation predicts nondestructive insulitis in non-obese diabetic mice. J. Immunol. 158:2414-2424.
44. Cameron, M.J., G.A. Arreaza, P. Zucker, S.W. Chensue, R.M. Strieter, S. Chakrabart, and T.L. Delovitch. 1997. 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.
45. Trinchieri, G. 1993. Interleukin-12 and its role in the generation of Th1 cells. Immunol. Today. 14:335-337.
46. Kennedy, M.K., K.S. Picha, K.D. Shanebeck, D.M. Anderson, and K.H. Grabstein. 1994. Interleukin-12 regulates the proliferation of Th1, but not Th2 or Th0 clones. Eur.J. Immunol. 24:2271-2278.
47. Pankewycz, O.G., J.X. Guan, and J.F. Benedict. 1995. Cytokines as mediators of autoimmune diabetes and diabetic complications. Endocrinol. Rev. 16:164-176.
48. Mandrup-Poulsen, T., K. Bendtzen, C. Dinarello, and J. Nerup. 1987. Human tumor-necrosis factor potentiates human interleukin 1-mediated rat pancreatic beta cell-cytotoxicity. J. Immunol. 139:4077-4082.
49. Appels, B., V. Burkart, M. Kantwerk-Funke, J. Funda, V. Kolb-Bachofen, and H. Kolb. 1989. Spontaneous cytotoxicity of macrophages against pancreatic islet cells. J. Immunol. 142:3803-3808.
50. Pukel, C., H. Baquerizo, and A. Rabinovitch. 1988. Destruction of rat islet cell monolayers by cytokines. Synergistic interactions of interferon-gamma, tumor necrosis factor, lymphotoxin, and interleukin-1. Diabetes. 37:133-136.
51. Faust, A., R. Kleemann, H. Rothe, and H. Kolb. 1996. Role of macrophages and cytokines in β-cell death. In Lessons from Animal Diabetes VI. E. Shafrir, editor. Birkhäuser, Cambridge, Massachusetts. 47-56.
52. Asayama, K., N.W. Kooy, and I.M. Burr. 1986. Effect of vitamin E deficiency and selenium deficiency on insulin secretory reserve and free radical scavenging systems in islets; decrease of islet manganosuperoxide dismutase. J. Lab. Clin. Med. 107:4559-4564.
53. Malaisse, W.J., F. Malaisse-Lagae, A. Sener, and D.G. Pipeleers. 1982. Determinants of the selective toxicity of alloxan to the pancreatic β cell. Proc. Natl. Acad. Sci. USA. 79:927-930.
54. Corbett, J.A., and M.L. McDaniel. 1992. Does nitric oxide mediate autoimmune destruction of β cells? Possible therapeutic interventions in IDDM. Diabetes. 41:897-903.
55. Hirasawa, K., H.S. Jun, K. Maeda, Y. Kawaguchi, S. Itagaki, T. Mikami, H.S. Back, K. Doi, and J.W. Yoon. 1997. Possible role of macrophage-derived soluble mediators in the pathogenesis of EMC virus-induced diabetes in mice. J. Virol. 71:4024-4031.
56. Unuaue, E.R. Antigen-presenting function of the macrophage. 1984. Annu. Rev. Immunol. 2:395-428.
57. Unuaue, E.R., and P.M. Allen. 1987. The basis for the immunoregulatory role of macrophages and other accessory cells. Science. 236:551-557.
58. Kagi, D., B. Odermatt, P. Seiler, R.M. Zinkernagel, T.W. Mak, and H. Hengartner. 1997. Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice. J. Exp. Med. 186:989-997.
59. 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.
60. Chervonsky, A.V., Y. Wang, F.S. Wong, I. Visintin, R.A. Flavell, C.A. Janeway, Jr., and L. Matis. 1997. The role of Fas in autoimmune diabetes. Cell. 89:17-24.