An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans

doi:10.1084/jem.180.3.1097

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An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans

O Lantz and A Bendelac
Laboratory of Cellular and Molecular Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892.

The mouse thymus contains a mature T cell subset that is distinguishable from the mainstream thymocytes by several characteristics. It is restricted in its usage of T cell receptor (TCR) V beta genes to V beta 8, V beta 7, and V beta 2. Its surface phenotype is that of activated/memory cells. It carries the natural killer NK1.1 surface marker. Furthermore, though it consists entirely of CD4+ and CD4-8- cells, its selection in the thymus depends solely upon major histocompatibility complex (MHC) class I expression by cells of hematopoietic origin. Forced persistence of CD8, in fact, imparts negative selection. Here, we have studied the TCR repertoire of this subset and found that, whereas the beta chain V-D-J junctions are quite variable, a single invariant alpha chain V alpha 14-J281 is used by a majority of the TCRs. This surprisingly restricted usage of the V alpha 14-J281 alpha chain is dependent on MHC class I expression, but independent of the MHC haplotype. In humans, a similar unusual population including CD4-8- cells can also be found that uses a strikingly homologous, invariant alpha chain V alpha 24-JQ. Thus, this unique V alpha-J alpha combination has been conserved in both species, conferring specificity to some shared nonpolymorphic MHC class I/peptide self-ligand(s). This implies that the T cell subset that it defines has a specialized and important role, perhaps related to its unique ability to secrete a large set of lymphokines including interleukin 4, upon primary stimulation in vitro and in vivo.
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Elewaut, D., Shaikh, R. B., Hammond, K. J. L., De Winter, H., Leishman, A. J., Sidobre, S., Turovskaya, O., Prigozy, T. I., Ma, L., Banks, T. A., Lo, D., Ware, C. F., Cheroutre, H., Kronenberg, M. (2003). NIK-dependent RelB Activation Defines a Unique Signaling Pathway for the Development of V{alpha}14i NKT Cells. JEM 197: 1623-1633 [Abstract] [Full Text]
Stewart, T. J., Smyth, M. J., Fernando, G. J. P., Frazer, I. H., Leggatt, G. R. (2003). Inhibition of Early Tumor Growth Requires J{alpha}18-positive (Natural Killer T) Cells. Cancer Res. 63: 3058-3060 [Abstract] [Full Text]
Schumann, J., Voyle, R. B., Wei, B.-Y., MacDonald, H. R. (2003). Cutting Edge: Influence of the TCR V{beta} Domain on the Avidity of CD1d:{alpha}-Galactosylceramide Binding by Invariant V{alpha}14 NKT Cells. J. Immunol. 170: 5815-5819 [Abstract] [Full Text]
Faunce, D. E., Gamelli, R. L., Choudhry, M. A., Kovacs, E. J. (2003). A role for CD1d-restricted NKT cells in injury-associated T cell suppression. J. Leukoc. Biol. 73: 747-755 [Abstract] [Full Text]
Matsuki, N., Stanic, A. K., Embers, M. E., Van Kaer, L., Morel, L., Joyce, S. (2003). Genetic Dissection of V{alpha}14J{alpha}18 Natural T Cell Number and Function in Autoimmune-Prone Mice. J. Immunol. 170: 5429-5437 [Abstract] [Full Text]
Zhang, G., Nichols, R. D., Taniguchi, M., Nakayama, T., Parmely, M. J. (2003). Gamma Interferon Production by Hepatic NK T Cells during Escherichia coli Infection Is Resistant to the Inhibitory Effects of Oxidative Stress. Infect. Immun. 71: 2468-2477 [Abstract] [Full Text]
Cantu, C. III, Benlagha, K., Savage, P. B., Bendelac, A., Teyton, L. (2003). The Paradox of Immune Molecular Recognition of {alpha}-Galactosylceramide: Low Affinity, Low Specificity for CD1d, High Affinity for {alpha}{beta} TCRs. J. Immunol. 170: 4673-4682 [Abstract] [Full Text]
Chun, T., Page, M. J., Gapin, L., Matsuda, J. L., Xu, H., Nguyen, H., Kang, H.-S., Stanic, A. K., Joyce, S., Koltun, W. A., Chorney, M. J., Kronenberg, M., Wang, C.-R. (2003). CD1d-expressing Dendritic Cells but Not Thymic Epithelial Cells Can Mediate Negative Selection of NKT Cells. JEM 197: 907-918 [Abstract] [Full Text]
Capone, M., Cantarella, D., Schumann, J., Naidenko, O. V., Garavaglia, C., Beermann, F., Kronenberg, M., Dellabona, P., MacDonald, H. R., Casorati, G. (2003). Human Invariant V{alpha}24-J{alpha}Q TCR Supports the Development of CD1d-Dependent NK1.1+ and NK1.1- T Cells in Transgenic Mice. J. Immunol. 170: 2390-2398 [Abstract] [Full Text]
Rigby, S. M., Rouse, T., Field, E. H. (2003). Total lymphoid irradiation nonmyeloablative preconditioning enriches for IL-4-producing CD4+-TNK cells and skews differentiation of immunocompetent donor CD4+ cells. Blood 101: 2024-2032 [Abstract] [Full Text]
Inui, T., Nakagawa, R., Ohkura, S., Habu, Y., Koike, Y., Motoki, K., Kuranaga, N., Fukasawa, M., Shinomiya, N., Seki, S. (2002). Age-Associated Augmentation of the Synthetic Ligand- Mediated Function of Mouse NK1.1 Ag+ T Cells: Their Cytokine Production and Hepatotoxicity In Vivo and In Vitro. J. Immunol. 169: 6127-6132 [Abstract] [Full Text]
Boyer, O., Marodon, G., Cohen, J. L., Lejeune, L., Irinopoulou, T., Liblau, R., Bruneval, P., Klatzmann, D. (2002). Human CD4 Expression at the Late Single-Positive Stage of Thymic Development Supports T Cell Maturation and Peripheral Export in CD4-Deficient Mice. J. Immunol. 169: 4347-4353 [Abstract] [Full Text]
Oikawa, Y., Shimada, A., Yamada, S., Motohashi, Y., Nakagawa, Y., Irie, J.-i., Maruyama, T., Saruta, T. (2002). High Frequency of V{alpha}24+ V{beta}11+ T-Cells Observed in Type 1 Diabetes. Diabetes Care 25: 1818-1823 [Abstract] [Full Text]
Procopio, D. O., Almeida, I. C., Torrecilhas, A. C. T., Cardoso, J. E., Teyton, L., Travassos, L. R., Bendelac, A., Gazzinelli, R. T. (2002). Glycosylphosphatidylinositol-Anchored Mucin-Like Glycoproteins from Trypanosoma cruzi Bind to CD1d but Do Not Elicit Dominant Innate or Adaptive Immune Responses Via the CD1d/NKT Cell Pathway. J. Immunol. 169: 3926-3933 [Abstract] [Full Text]
Gadue, P., Stein, P. L. (2002). NK T Cell Precursors Exhibit Differential Cytokine Regulation and Require Itk for Efficient Maturation. J. Immunol. 169: 2397-2406 [Abstract] [Full Text]
Kikkawa, E., Yamashita, M., Kimura, M., Omori, M., Sugaya, K., Shimizu, C., Katsumoto, T., Ikekita, M., Taniguchi, M., Nakayama, T. (2002). Th1/Th2 cell differentiation of developing CD4 single-positive thymocytes. Int Immunol 14: 943-951 [Abstract] [Full Text]