The Journal of Experimental Medicine
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Published online 11 November 2002 doi:10.1084/jem.20020649
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© Rockefeller University Press, 0022-1007/2002/11/1277/ $5.00
The Journal of Experimental Medicine, Volume 196, Number 10, November 18, 2002 1277-1290

B Cell–dependent T Cell Responses : IgM Antibodies Are Required to Elicit Contact Sensitivity



Ryohei F. Tsuji1, Marian Szczepanik2, Ivana Kawikova3, Vipin Paliwal3, Regis A. Campos3, Atsuko Itakura3, Moe Akahira-Azuma3, Nicole Baumgarth4, Leonore A. Herzenberg5 and Philip W. Askenase3

1 Noda Institute for Scientific Research, Chiba-ken 278, Japan
2 Department of Immunology, Jagiellonian University College of Medicine, 31-008 Krakow, Poland
3 Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
4 Center for Comparative Medicine, University of California at Davis, Davis, CA 95616
5 Department of Genetics, Beckman Center, Stanford University School of Medicine, Stanford, CA 94305

Address correspondence to Philip W. Askenase, Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, 333 Cedar Street, P.O. Box 208013, New Haven, CT 06520. Phone: 203-785-4143; Fax: 203-785-3229; E-mail: philip.askenase{at}yale.edu

Contact sensitivity (CS) is a classic example of in vivo T cell immunity in which skin sensitization with reactive hapten leads to immunized T cells, which are then recruited locally to mediate antigen-specific inflammation after subsequent skin challenge. We have previously shown that T cell recruitment in CS is triggered by local activation of complement, which generates C5a that triggers C5a receptors most likely on mast cells. Here, we show that B-1 cell–derived antihapten IgM antibodies generated within 1 day (d) of immunization combine with local challenge antigen to activate complement to recruit the T cells. These findings overturn three widely accepted immune response paradigms by showing that (a) specific IgM antibodies are required to initiate CS, which is a classical model of T cell immunity thought exclusively due to T cells, (b) CS priming induces production of specific IgM antibodies within 1 d, although primary antibody responses typically begin by day 4, and (c) B-1 cells produce the 1-d IgM response to CS priming, although these cells generally are thought to be nonresponsive to antigenic stimulation. Coupled with previous evidence, our findings indicate that the elicitation of CS is initiated by rapidly formed IgM antibodies. The IgM and challenge antigen likely form local complexes that activate complement, generating C5a, leading to local vascular activation to recruit the antigen-primed effector T cells that mediate the CS response.

Key Words: T cell recruitment • complement C5 and C5a • skin immunity • IgM response • T and B cell interactions


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