J. Exp. Med., Volume 187, Number 7, April 6, 1998 1047-1056

/-T Cell Receptor (TCR)⁺CD4CD8 (NKT) Thymocytes Prevent Insulin-dependent Diabetes Mellitus in Nonobese Diabetic (NOD)/Lt Mice by the Influence of Interleukin (IL)-4 and/or IL-10

By Kirsten J.L. Hammond, Lynn D. Poulton, Linda J. Palmisano, Pablo A. Silveira, Dale I. Godfrey, and Alan G. Baxter

From the Autoimmunity Research Group, Centenary Institute of Cancer Medicine and Cell Biology, Newtown, New South Wales 2042, Australia

We have previously shown that nonobese diabetic (NOD) mice are selectively deficient in /-T cell receptor (TCR)⁺CD4CD8 NKT cells, a defect that may contribute to their susceptibility to the spontaneous development of insulin-dependent diabetes mellitus (IDDM). The role of NKT cells in protection from IDDM in NOD mice was studied by the infusion of thymocyte subsets into young female NOD mice. A single intravenous injection of 10⁶ CD4^/lowCD8 or CD4CD8 thymocytes from female (BALB/c × NOD)F1 donors protected intact NOD mice from the spontaneous onset of clinical IDDM. Insulitis was still present in some recipient mice, although the cell infiltrates were principally periductal and periislet, rather than the intraislet pattern characteristic of insulitis in unmanipulated NOD mice. Protection was not associated with the induction of "allogenic tolerance" or systemic autoimmunity. Accelerated IDDM occurs after injection of splenocytes from NOD donors into irradiated adult NOD recipients. When /-TCR⁺ and /-TCR subsets of CD4CD8 thymocytes were transferred with diabetogenic splenocytes and compared for their ability to prevent the development of IDDM in irradiated adult recipients, only the /-TCR⁺ population was protective, confirming that NKT cells were responsible for this activity. The protective effect in the induced model of IDDM was neutralized by anti-IL-4 and anti-IL-10 monoclonal antibodies in vivo, indicating a role for at least one of these cytokines in NKT cell-mediated protection. These results have significant implications for the pathogenesis and potential prevention of IDDM in humans.

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• Laloux, V., Beaudoin, L., Jeske, D., Carnaud, C., Lehuen, A. (2001). NK T Cell-Induced Protection Against Diabetes in V{{alpha}}14-J{{alpha}}281 Transgenic Nonobese Diabetic Mice Is Associated with a Th2 Shift Circumscribed Regionally to the Islets and Functionally to Islet Autoantigen. J. Immunol. 166: 3749-3756 [Abstract] [Full Text]  
• Fritz, R. B., Zhao, M.-L. (2001). Regulation of Experimental Autoimmune Encephalomyelitis in the C57BL/6J Mouse by NK1.1+, DX5+, {{alpha}}{{beta}}+ T Cells. J. Immunol. 166: 4209-4215 [Abstract] [Full Text]  
• Carnaud, C., Gombert, J.-M., Donnars, O., Garchon, H.-J., Herbelin, A. (2001). Protection Against Diabetes and Improved NK/NKT Cell Performance in NOD.NK1.1 Mice Congenic at the NK Complex. J. Immunol. 166: 2404-2411 [Abstract] [Full Text]  
• Seino, K.-i., Fukao, K., Muramoto, K., Yanagisawa, K., Takada, Y., Kakuta, S., Iwakura, Y., Van Kaer, L., Takeda, K., Nakayama, T., Taniguchi, M., Bashuda, H., Yagita, H., Okumura, K. (2001). Requirement for natural killer T (NKT) cells in the induction of allograft tolerance. Proc. Natl. Acad. Sci. USA 10.1073/pnas.041608298v1 [Abstract] [Full Text]  
• del C. Salamone, M., Rabinovich, G. A., Mendiguren, A. K., Salamone, G. V., Fainboim, L. (2001). Activation-induced expression of CD1d antigen on mature T cells. J. Leukoc. Biol. 69: 207-214 [Abstract] [Full Text]  
• Leite-de-Moraes, M. C., Hameg, A., Pacilio, M., Koezuka, Y., Taniguchi, M., Van Kaer, L., Schneider, E., Dy, M., Herbelin, A. (2001). IL-18 Enhances IL-4 Production by Ligand-Activated NKT Lymphocytes: A Pro-Th2 Effect of IL-18 Exerted Through NKT Cells. J. Immunol. 166: 945-951 [Abstract] [Full Text]  
• Kawakami, K., Kinjo, Y., Yara, S., Koguchi, Y., Uezu, K., Nakayama, T., Taniguchi, M., Saito, A. (2001). Activation of V{alpha}14+ Natural Killer T Cells by {alpha}-Galactosylceramide Results in Development of Th1 Response and Local Host Resistance in Mice Infected with Cryptococcus neoformans. Infect. Immun. 69: 213-220 [Abstract] [Full Text]  
• Sonoda, K.-H., Faunce, D. E., Taniguchi, M., Exley, M., Balk, S., Stein-Streilein, J. (2001). NK T Cell-Derived IL-10 Is Essential for the Differentiation of Antigen-Specific T Regulatory Cells in Systemic Tolerance. J. Immunol. 166: 42-50 [Abstract] [Full Text]  
• Pal, E., Tabira, T., Kawano, T., Taniguchi, M., Miyake, S., Yamamura, T. (2001). Costimulation-Dependent Modulation of Experimental Autoimmune Encephalomyelitis by Ligand Stimulation of V{{alpha}}14 NK T Cells. J. Immunol. 166: 662-668 [Abstract] [Full Text]  
• Araujo, L. M., Puel, A., Gouarin, C., Hameg, A., Mevel, J.-C., Koezuka, Y., Bach, J.-F., Mouton, D., Herbelin, A. (2000). NKT lymphocyte ontogeny and function are impaired in low antibody-producer Biozzi mice: gene mapping in the interval-specific congenic strains raised for immunomodulatory genes. Int Immunol 12: 1613-1622 [Abstract] [Full Text]  
• Yang, O. O., Racke, F. K., Nguyen, P. T., Gausling, R., Severino, M. E., Horton, H. F., Byrne, M. C., Strominger, J. L., Wilson, S. B. (2000). CD1d on Myeloid Dendritic Cells Stimulates Cytokine Secretion from and Cytolytic Activity of V{alpha}24J{alpha}Q T Cells: A Feedback Mechanism for Immune Regulation. J. Immunol. 165: 3756-3762 [Abstract] [Full Text]  
• ASSEMAN, C., FOWLER, S., POWRIE, F. (2000). Control of Experimental Inflammatory Bowel Disease by Regulatory T cells. Am. J. Respir. Crit. Care Med. 162: S185-189 [Abstract] [Full Text]  
• Matsuda, J. L., Naidenko, O. V., Gapin, L., Nakayama, T., Taniguchi, M., Wang, C.-R., Koezuka, Y., Kronenberg, M. (2000). Tracking the Response of Natural Killer T Cells to a Glycolipid Antigen Using CD1d Tetramers. JEM 192: 741-754 [Abstract] [Full Text]  
• MacDonald, H. R. (2000). CD1d-Glycolipid Tetramers: A New Tool to Monitor Natural Killer T Cells in Health and Disease. JEM 192: F15-F20 [Full Text]  
• Apostolou, I., Cumano, A., Gachelin, G., Kourilsky, P. (2000). Evidence for Two Subgroups of CD4-CD8- NKT Cells with Distinct TCR{alpha}{beta} Repertoires and Differential Distribution in Lymphoid Tissues. J. Immunol. 165: 2481-2490 [Abstract] [Full Text]  
• Gonzalez-Aseguinolaza, G., de Oliveira, C., Tomaska, M., Hong, S., Bruna-Romero, O., Nakayama, T., Taniguchi, M., Bendelac, A., Van Kaer, L., Koezuka, Y., Tsuji, M. (2000). alpha -Galactosylceramide-activated Valpha 14 natural killer T cells mediate protection against murine malaria. Proc. Natl. Acad. Sci. USA 97: 8461-8466 [Abstract] [Full Text]  
• Skold, M., Faizunnessa, N. N., Wang, C.-R., Cardell, S. (2000). CD1d-Specific NK1.1+ T Cells with a Transgenic Variant TCR. J. Immunol. 165: 168-174 [Abstract] [Full Text]  
• Joyce, S. (2000). Natural T cells: Cranking up the immune system by prompt cytokine secretion. Proc. Natl. Acad. Sci. USA 97: 6933-6935 [Full Text]  
• Wilson, S. B., Kent, S. C., Horton, H. F., Hill, A. A., Bollyky, P. L., Hafler, D. A., Strominger, J. L., Byrne, M. C. (2000). Multiple differences in gene expression in regulatory Valpha 24Jalpha Q T cells from identical twins discordant for type I diabetes. Proc. Natl. Acad. Sci. USA 10.1073/pnas.120161297v1 [Abstract] [Full Text]  
• Olivares-Villagomez, D., Wensky, A. K., Wang, Y., Lafaille, J. J. (2000). Repertoire Requirements of CD4+ T Cells That Prevent Spontaneous Autoimmune Encephalomyelitis. J. Immunol. 164: 5499-5507 [Abstract] [Full Text]  

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