J. Exp. Med., Volume 189, Number 7, April 5, 1999 1121-1128

The Natural Killer T (NKT) Cell Ligand -Galactosylceramide Demonstrates Its Immunopotentiating Effect by Inducing Interleukin (IL)-12 Production by Dendritic Cells and IL-12 Receptor Expression on NKT Cells

By Hidemitsu Kitamura,^*§ Kenji Iwakabe, Takashi Yahata, Shin-ichiro Nishimura,^§ Akio Ohta,^* Yasushi Ohmi,^* Marimo Sato,^* Kazuyoshi Takeda, Ko Okumura, Luc Van Kaer,^¶ Tetsu Kawano,^** Masaru Taniguchi,^** and Takashi Nishimura^*

From the ^* Section of Genetic Engineering, Research Center for Genetic Engineering and Cell Transplantation, and  Department of Immunology, Tokai University School of Medicine, Isehara 259-1193,  Japan; the ^§ Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan; the  Department of Immunology, Juntendo University School of Medicine, Tokyo 113-0033,  Japan; the ^¶ Howard Hughes Medical Institute, Department of Microbiology and Immunology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232; and ^** Core Research for Evolutional Science and Technology (CREST) Project and Department of Molecular Immunology, Graduate School of Medicine, Chiba University, Chiba 260-8670,  Japan

The natural killer T (NKT) cell ligand -galactosylceramide (-GalCer) exhibits profound antitumor activities in vivo that resemble interleukin (IL)-12-mediated antitumor activities. Because of these similarities between the activities of -GalCer and IL-12, we investigated the involvement of IL-12 in the activation of NKT cells by -GalCer. We first established, using purified subsets of various lymphocyte populations, that -GalCer selectively activates NKT cells for production of interferon (IFN)-. Production of IFN- by NKT cells in response to -GalCer required IL-12 produced by dendritic cells (DCs) and direct contact between NKT cells and DCs through CD40/CD40 ligand interactions. Moreover, -GalCer strongly induced the expression of IL-12 receptor on NKT cells from wild-type but not CD1^/ or V14^/ mice. This effect of -GalCer required the production of IFN- by NKT cells and production of IL-12 by DCs. Finally, we showed that treatment of mice with suboptimal doses of -GalCer together with suboptimal doses of IL-12 resulted in strongly enhanced natural killing activity and IFN- production. Collectively, these findings indicate an important role for DC-produced IL-12 in the activation of NKT cells by -GalCer and suggest that NKT cells may be able to condition DCs for subsequent immune responses. Our results also suggest a novel approach for immunotherapy of cancer.

natural killer T cells;  dendritic cells;  -galactosylceramide;  interleukin 12;  interleukin 12 receptor

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• Laloux, V., Beaudoin, L., Ronet, C., Lehuen, A. (2002). Phenotypic and Functional Differences Between NKT Cells Colonizing Splanchnic and Peripheral Lymph Nodes. J. Immunol. 168: 3251-3258 [Abstract] [Full Text]  
• Gumperz, J. E., Miyake, S., Yamamura, T., Brenner, M. B. (2002). Functionally Distinct Subsets of CD1d-restricted Natural Killer T Cells Revealed by CD1d Tetramer Staining. JEM 195: 625-636 [Abstract] [Full Text]  
• Bendelac, A., Medzhitov, R. (2002). Adjuvants of Immunity: Harnessing Innate Immunity to Promote Adaptive Immunity. JEM 195: F19-F23 [Full Text]  
• Smyth, M. J., Crowe, N. Y., Pellicci, D. G., Kyparissoudis, K., Kelly, J. M., Takeda, K., Yagita, H., Godfrey, D. I. (2002). Sequential production of interferon-gamma by NK1.1+ T cells and natural killer cells is essential for the antimetastatic effect of alpha -galactosylceramide. Blood 99: 1259-1266 [Abstract] [Full Text]  
• Mempel, M., Ronet, C., Suarez, F., Gilleron, M., Puzo, G., Van Kaer, L., Lehuen, A., Kourilsky, P., Gachelin, G. (2002). Natural Killer T Cells Restricted by the Monomorphic MHC Class 1b CD1d1 Molecules Behave Like Inflammatory Cells. J. Immunol. 168: 365-371 [Abstract] [Full Text]  
• Jahng, A. W., Maricic, I., Pedersen, B., Burdin, N., Naidenko, O., Kronenberg, M., Koezuka, Y., Kumar, V. (2001). Activation of Natural Killer T Cells Potentiates or Prevents Experimental Autoimmune Encephalomyelitis. JEM 194: 1789-1799 [Abstract] [Full Text]  
• Singh, A. K., Wilson, M. T., Hong, S., Olivares-Villagomez, D., Du, C., Stanic, A. K., Joyce, S., Sriram, S., Koezuka, Y., Van Kaer, L. (2001). Natural Killer T Cell Activation Protects Mice Against Experimental Autoimmune Encephalomyelitis. JEM 194: 1801-1811 [Abstract] [Full Text]  
• Kawakami, K., Kinjo, Y., Uezu, K., Yara, S., Miyagi, K., Koguchi, Y., Nakayama, T., Taniguchi, M., Saito, A. (2001). Monocyte Chemoattractant Protein-1-Dependent Increase of V{alpha}14 NKT Cells in Lungs and Their Roles in Th1 Response and Host Defense in Cryptococcal Infection. J. Immunol. 167: 6525-6532 [Abstract] [Full Text]  
• Naumov, Y. N., Bahjat, K. S., Gausling, R., Abraham, R., Exley, M. A., Koezuka, Y., Balk, S. B., Strominger, J. L., Clare-Salzer, M., Wilson, S. B. (2001). Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc. Natl. Acad. Sci. USA 10.1073/pnas.251531798v1 [Abstract] [Full Text]  
• Ikarashi, Y., Mikami, R., Bendelac, A., Terme, M., Chaput, N., Terada, M., Tursz, T., Angevin, E., Lemonnier, F. A., Wakasugi, H., Zitvogel, L. (2001). Dendritic Cell Maturation Overrules H-2D-mediated Natural Killer T (NKT) Cell Inhibition: Critical Role for B7 in CD1d-dependent NKT Cell Interferon {gamma} Production. JEM 194: 1179-1186 [Abstract] [Full Text]  
• Maeda, M., Lohwasser, S., Yamamura, T., Takei, F. (2001). Regulation of NKT Cells by Ly49: Analysis of Primary NKT Cells and Generation of NKT Cell Line. J. Immunol. 167: 4180-4186 [Abstract] [Full Text]  
• Sato, M., Chamoto, K., Tsuji, T., Iwakura, Y., Togashi, Y., Koda, T., Nishimura, T. (2001). Th1 Cytokine-Conditioned Bone Marrow-Derived Dendritic Cells Can Bypass the Requirement for Th Functions During the Generation of CD8+ CTL. J. Immunol. 167: 3687-3691 [Abstract] [Full Text]  
• Muhammad Ali Tahir, S., Cheng, O., Shaulov, A., Koezuka, Y., Bubley, G. J., Wilson, S. B., Balk, S. P., Exley, M. A. (2001). Loss of IFN-{gamma} Production by Invariant NK T Cells in Advanced Cancer. J. Immunol. 167: 4046-4050 [Abstract] [Full Text]  
• Metelitsa, L. S., Naidenko, O. V., Kant, A., Wu, H.-W., Loza, M. J., Perussia, B., Kronenberg, M., Seeger, R. C. (2001). Human NKT Cells Mediate Antitumor Cytotoxicity Directly by Recognizing Target Cell CD1d with Bound Ligand or Indirectly by Producing IL-2 to Activate NK Cells. J. Immunol. 167: 3114-3122 [Abstract] [Full Text]  
• Wang, B., Geng, Y.-B., Wang, C.-R. (2001). CD1-restricted NK T Cells Protect Nonobese Diabetic Mice from Developing Diabetes. JEM 194: 313-320 [Abstract] [Full Text]  
• Trobonjaca, Z., Leithauser, F., Moller, P., Schirmbeck, R., Reimann, J. (2001). Activating Immunity in the Liver. I. Liver Dendritic Cells (but Not Hepatocytes) Are Potent Activators of IFN-{gamma} Release by Liver NKT Cells. J. Immunol. 167: 1413-1422 [Abstract] [Full Text]  
• Hayakawa, Y., Takeda, K., Yagita, H., Van Kaer, L., Saiki, I., Okumura, K. (2001). Differential Regulation of Th1 and Th2 Functions of NKT Cells by CD28 and CD40 Costimulatory Pathways. J. Immunol. 166: 6012-6018 [Abstract] [Full Text]  
• Exley, M. A., Bigley, N. J., Cheng, O., Tahir, S. M. A., Smiley, S. T., Carter, Q. L., Stills, H. F., Grusby, M. J., Koezuka, Y., Taniguchi, M., Balk, S. P. (2001). CD1d-reactive T-cell activation leads to amelioration of disease caused by diabetogenic encephalomyocarditis virus. J. Leukoc. Biol. 69: 713-718 [Abstract] [Full Text]  
• Trobonjaca, Z., Leithauser, F., Moller, P., Bluethmann, H., Koezuka, Y., MacDonald, H. R., Reimann, J. (2001). MHC-II-Independent CD4+ T Cells Induce Colitis in Immunodeficient RAG-/- Hosts. J. Immunol. 166: 3804-3812 [Abstract] [Full Text]  
• Smyth, M. J., Cretney, E., Takeda, K., Wiltrout, R. H., Sedger, L. M., Kayagaki, N., Yagita, H., Okumura, K. (2001). Tumor Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL) Contributes to Interferon {{gamma}}-dependent Natural Killer Cell Protection from Tumor Metastasis. JEM 193: 661-670 [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]  
• 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]  

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