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CD1d-Independent Developmental Acquisition of Prompt IL-4 Gene Inducibility in Thymus CD161(NK1)^–CD44^lowCD4⁺CD8^– T Cells Is Associated with Complementarity Determining Region 3-Diverse and Biased V2/V7/V8/V3.2 T Cell Receptor Usage¹

Yi-Ting Chen^* and John T. Kung^2,

^* Graduate Institute of Immunology, College of Medicine, National Taiwan University, Taipei, Taiwan; and Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan

Among Ag-inexperienced naive T cells, the CD1d-restricted NKT cell that uses invariant TCR--chain is the most widely studied cell capable of prompt IL-4 inducibility. We show in this study that thymus CD161^–CD44^lowCD4⁺CD8^– T cells promptly produce IL-4 upon TCR stimulation, a response that displays biased V(2/7/8) and V3.2 TCR usage. The association of V family bias and IL-4 inducibility in thymus CD161^–CD44^lowCD4⁺CD8^– T cells is found for B6, B10, BALB/c, CBA, B10.A(4R), and ICR mouse strains. Despite reduced IL-4 inducibility, there is a similarly biased V(2/7/8) TCR usage by IL-4 inducibility⁺ spleen CD161^–CD44^lowCD4⁺CD8^– T cells. Removal of -galacotosylceramide/CD1d-binding cells from CD161^–CD44^lowCD4⁺CD8^– thymocytes does not significantly affect their IL-4 inducibility. The development of thymus CD161^–CD44^lowCD4⁺CD8^– T cells endowed with IL-4 inducibility and their associated use of V(2/7/8) are ₂-microglobulin-, CD1d-, and p59^fyn-independent. Thymus CD161^–CD44^lowCD4⁺CD8^– T cells produce low and no IFN- inducibility in response to TCR stimulation and to IL-12 + IL-18, respectively, and they express diverse complementarity determining region 3 sequences for both TCR-- and --chains. Taken together, these results demonstrate the existence of a NKT cell distinct, TCR-repertoire diverse naive CD4⁺ T cell subset capable of prompt IL-4 inducibility. This subset has the potential to participate in immune response to a relatively large number of Ags. The more prevalent nature of this unique T cell subset in the thymus than the periphery implies roles it might play in intrathymic T cell development and may provide a framework upon which mechanisms of developmentally regulated IL-4 gene inducibility can be studied.

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