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Cutaneous Immunization Rapidly Activates Liver Invariant V14 NKT Cells Stimulating B-1 B Cells to Initiate T Cell Recruitment for Elicitation of Contact Sensitivity

¹ Section of Allergy and Clinical Immunology, Department of Medicine, Yale University School of Medicine, New Haven, CT 06520
² Department of Human Developmental Biology, Jagiellonian University College of Medicine, 31-008 Krakow, Poland
³ Laboratório de Alergia e Imunologia Clínica e Experimental (LIM-56), Faculdade de Medicina da Universidade de São Paulo, 01246-000 São Paulo, Brasil
⁴ La Jolla Institute for Allergy and Immunology, San Diego, CA 92121

Address correspondence to Philip W. Askenase, Section of Allergy and Clinical Immunology, Dept. of Medicine, Yale University School of Medicine, 333 Cedar St., New Haven, CT 06520-8013. Phone: (203) 785-4143; Fax: (203) 785-3229; email: philip.askenase{at}yale.edu

T cell recruitment to elicit contact sensitivity (CS) requires a CS-initiating process mediated by B-1 cells that produce IgM, which activates complement to promote T cell passage into the tissues. We now show that V14i NKT cells induce B-1 cell activation likely by releasing IL-4 early postimmunization. The CS initiation process is absent in J18^-/- and CD1d^-/- NKT cell–deficient mice and is reconstituted by populations enriched for V14i NKT cells. Transfers are not effective if cells are derived from IL-4^-/- mice. Staining with specific tetramers directly showed that hepatic V14i NKT cells increase by 30 min and nearly double by 2 h postimmunization. Transfer of immune B-1 cells also reconstitutes CS responses in NKT cell–deficient mice. The B-1 cells act downstream of the V14i NKT cells to restore CS initiation. In addition, IL-4 given systemically to J18^-/- or CD1d^-/- NKT cell–deficient mice reconstitutes elicitation of CS. Further, splenocytes from immune J18^-/- mice produce less antigen (Ag)-specific IgM antibodies compared with sensitized WT mice. Together these findings indicate that very early after skin immunization V14i NKT cells are stimulated to produce IL-4, which activates B-1 cells to produce Ag-specific IgM, subsequently needed to recruit effector T cells for elicitation of CS responses.

Key Words: V14i NKT cells • B-1 cells • contact sensitivity • liver lymphocytes • IL-4

Abbreviations used in this paper: -GalCer, -galactosylceramide; CS, contact sensitivity; DTH, delayed-type hypersensitivity; LMNC, liver mononuclear cell; PCl, picryl-chloride (TNP-Cl).

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