The Journal of Experimental Medicine
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© The Rockefeller University Press, 0022-1007/1999/1/103/ $5.00
The Journal of Experimental Medicine, Volume 189, Number 1, January 4, 1999 103-110

Articles

Distinct Subsets of CD1d-restricted T Cells Recognize Self-antigens Loaded in Different Cellular Compartments

Ya-Hui Chiu*, Jayanthi Jayawardena*, Angela Weiss*, Daniel Lee*, Se-Ho Park*, Alice Dautry-Varsat{ddagger}, and Albert Bendelac*

From the * Department of Molecular Biology, Princeton, New Jersey 08544; and the {ddagger} Institut Pasteur, Unite de Biologie des Interactions Cellulaires, 75724 Paris Cedex 15, France

Although recent studies have indicated that the major histocompatibility complex–like, β2-microglobulin–associated CD1 molecules might function to present a novel chemical class of antigens, lipids and glycolipids, to {alpha}/β T cells, little is known about the T cell subsets that interact with CD1. A subset of CD1d-autoreactive, natural killer (NK)1.1 receptor–expressing {alpha}/β T cells has recently been identified. These cells, which include both CD4–CD8– and CD4+ T cells, preferentially use an invariant V{alpha}14-J{alpha}281 T cell receptor (TCR) {alpha} chain paired with a Vβ8 TCR β chain in mice, or the homologous V{alpha}24-J{alpha}Q/Vβ11 in humans. This cell subset can explosively release key cytokines such as interleukin (IL)-4 and interferon (IFN)-{gamma} upon TCR engagement and may regulate a variety of infectious and autoimmune conditions. Here, we report the existence of a second subset of CD1d-restricted CD4+ T cells that do not express the NK1.1 receptor or the V{alpha}14 TCR. Like the V{alpha}14+ NK1.1+ T cells, these T cells exhibit a high frequency of autoreactivity to CD1d, use a restricted albeit distinct set of TCR gene families, and contribute to the early burst of IL-4 and IFN-{gamma} induced by intravenous injection of anti-CD3. However, the V{alpha}14+ NK1.1+ and V{alpha}14– NK1.1– T cells differ markedly in their requirements for self-antigen presentation. Antigen presentation to the V{alpha}14+ NK1.1+ cells requires endosomal targeting of CD1d through a tail-encoded tyrosine-based motif, whereas antigen presentation to the V{alpha}14– NK1.1– cells does not. These experiments suggest the existence of two phenotypically different subsets of CD1d-restricted T cells that survey self-antigens loaded in distinct cellular compartments.

Key Words: CD1 • self-antigen • endosome • interleukin 4 • interferon {gamma}

Address correspondence to Albert Bendelac, Department of Molecular Biology, Princeton, NJ 08544. Phone: 609-258-5454; Fax: 609-258-2205; E-mail: abendelac{at}molbio.princeton.edu

Abbreviations used: HPRT, hypoxanthine ribosyl transferase; mfi, mean fluorescent intensity; RT, reverse transcriptase.


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