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.
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18 November 2002
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November 11 2002
B Cell–dependent T Cell Responses : IgM Antibodies Are Required to Elicit Contact Sensitivity
Ryohei F. Tsuji,
Ryohei F. Tsuji
1Noda Institute for Scientific Research, Chiba-ken 278, Japan
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Marian Szczepanik,
Marian Szczepanik
2Department of Immunology, Jagiellonian University College of Medicine, 31-008 Krakow, Poland
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Ivana Kawikova,
Ivana Kawikova
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Vipin Paliwal,
Vipin Paliwal
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Regis A. Campos,
Regis A. Campos
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Atsuko Itakura,
Atsuko Itakura
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Moe Akahira-Azuma,
Moe Akahira-Azuma
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Nicole Baumgarth,
Nicole Baumgarth
4Center for Comparative Medicine, University of California at Davis, Davis, CA 95616
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Leonore A. Herzenberg,
Leonore A. Herzenberg
5Department of Genetics, Beckman Center, Stanford University School of Medicine, Stanford, CA 94305
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Philip W. Askenase
Philip W. Askenase
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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Ryohei F. Tsuji
1Noda Institute for Scientific Research, Chiba-ken 278, Japan
Marian Szczepanik
2Department of Immunology, Jagiellonian University College of Medicine, 31-008 Krakow, Poland
Ivana Kawikova
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
Vipin Paliwal
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
Regis A. Campos
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
Atsuko Itakura
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
Moe Akahira-Azuma
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
Nicole Baumgarth
4Center for Comparative Medicine, University of California at Davis, Davis, CA 95616
Leonore A. Herzenberg
5Department of Genetics, Beckman Center, Stanford University School of Medicine, Stanford, CA 94305
Philip W. Askenase
3Section of Allergy and Clinical Immunology, Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520
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: [email protected]
L.A. Herzenberg and P.W. Askenase contributed equally to this work.
*
Abbreviations used in this paper: CS, contact sensitivity; DTH, delayed-type hypersensitivity; LNC, LN cell; OX, oxazolone (4-ethoxymethylene-2-phenyl-2-oxazolone-5-one); PCl, picryl chloride; TNP, trinitrophenol.
Received:
April 19 2002
Revision Received:
August 02 2002
Accepted:
September 06 2002
Online ISSN: 1540-9538
Print ISSN: 0022-1007
The Rockefeller University Press
2002
J Exp Med (2002) 196 (10): 1277–1290.
Article history
Received:
April 19 2002
Revision Received:
August 02 2002
Accepted:
September 06 2002
Citation
Ryohei F. Tsuji, Marian Szczepanik, Ivana Kawikova, Vipin Paliwal, Regis A. Campos, Atsuko Itakura, Moe Akahira-Azuma, Nicole Baumgarth, Leonore A. Herzenberg, Philip W. Askenase; B Cell–dependent T Cell Responses : IgM Antibodies Are Required to Elicit Contact Sensitivity . J Exp Med 18 November 2002; 196 (10): 1277–1290. doi: https://doi.org/10.1084/jem.20020649
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