Original Article

CD1-reactive Natural Killer T Cells Are Required for Development of Systemic Tolerance through an Immune-Privileged Site

Correspondence to: Joan Stein-Streilein, Schepens Eye Research Institute, 20 Staniford St., Boston, MA 02114. Tel:617-912-7494 Fax:617-912-0105 E-mail:jstein{at}vision.eri.harvard.edu.

Systemic tolerance can be elicited by introducing antigen into an immune-privileged site, such as the eye, or directly into the blood. Both routes of immunization result in a selective deficiency of systemic delayed type hypersensitivity. Although the experimental animal model of anterior chamber–associated immune deviation (ACAID) occurs in most mouse strains, ACAID cannot be induced in several mutant mouse strains that are coincidentally deficient in natural killer T (NKT) cells. Therefore, this model for immune-privileged site–mediated tolerance provided us with an excellent format for studying the role of NKT cells in the development of tolerance. The following data show that CD1-reactive NKT cells are required for the development of systemic tolerance induced via the eye as follows: (a) CD1 knockout mice were unable to develop ACAID unless they were reconstituted with NKT cells together with CD1⁺ antigen-presenting cells; (b) specific antibody depletion of NKT cells in vivo abrogated the development of ACAID; and (c) anti-CD1 monoclonal antibody treatment of wild-type mice prevented ACAID development. Significantly, CD1-reactive NKT cells were not required for intravenously induced systemic tolerance, thereby establishing that different mechanisms mediate development of tolerance to antigens inoculated by these routes. A critical role for NKT cells in the development of systemic tolerance associated with an immune-privileged site suggests a mechanism involving NKT cells in self-tolerance and their defects in autoimmunity.

Key Words: innate immunity , immune deviation , anterior chamber–associated immune deviation , autoimmunity , i.v. tolerance

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• Skelsey, M. E., Mellon, J., Niederkorn, J. Y. (2001). {{gamma}}{{delta}}T Cells Are Needed for Ocular Immune Privilege and Corneal Graft Survival. J. Immunol. 166: 4327-4333 [Abstract] [Full Text]  
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• 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]  
• Faunce, D. E., Sonoda, K.-H., Stein-Streilein, J. (2001). MIP-2 Recruits NKT Cells to the Spleen During Tolerance Induction. J. Immunol. 166: 313-321 [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]  
• van der Vliet, H. J. J., Nishi, N., de Gruijl, T. D., von Blomberg, B. M. E., van den Eertwegh, A. J. M., Pinedo, H. M., Giaccone, G., Scheper, R. J. (2000). Human natural killer T cells acquire a memory-activated phenotype before birth. Blood 95: 2440-2442 [Abstract] [Full Text]  
• Hong, S., Van Kaer, L. (1999). Immune Privilege: Keeping an Eye on Natural Killer T Cells. JEM 190: 1197-1200 [Full Text]  
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• 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 98: 13838-13843 [Abstract] [Full Text]  
• Pellicci, D. G., Hammond, K. J.L., Uldrich, A. P., Baxter, A. G., Smyth, M. J., Godfrey, D. I. (2002). A Natural Killer T (NKT) Cell Developmental Pathway Involving a Thymus-dependent NK1.1-CD4+ CD1d-dependent Precursor Stage. JEM 195: 835-844 [Abstract] [Full Text]  
• Motsinger, A., Haas, D. W., Stanic, A. K., Van Kaer, L., Joyce, S., Unutmaz, D. (2002). CD1d-restricted Human Natural Killer T Cells Are Highly Susceptible to Human Immunodeficiency Virus 1 Infection. JEM 195: 869-879 [Abstract] [Full Text]  

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