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B lymphocytes promote expansion of regulatory T cells in oral tolerance: powerful induction by antigen coupled to cholera toxin B subunit.

Journal article
Authors Jia-Bin Sun
Carl-Fredrik Flach
Cecil Czerkinsky
Jan Holmgren
Published in Journal of immunology (Baltimore, Md. : 1950)
Volume 181
Issue 12
Pages 8278-87
ISSN 1550-6606
Publication year 2008
Published at Institute of Biomedicine, Department of Microbiology and Immunology
Pages 8278-87
Language en
Links www.jimmunol.org/content/181/12/827...
Keywords oral tolerance, B cell, sublingual, mouse, cholera toxin B subunit, ovalbumin
Subject categories Immunology in the medical area

Abstract

Mucosal administration of Ag conjugated to cholera toxin B subunit (CTB) can efficiently induce peripheral immunologic tolerance, so-called oral tolerance, associated with development of Foxp3(+)CD25(+)CD4(+) regulatory T (Treg) cells. Using an established sublingual tolerization regimen with Ag(OVA)/CTB conjugate, wherein CTB mediates Ag uptake and presentation by most B lymphocytes irrespective of their Ag specificity, we have assessed the importance of B cells for induction of Ag-specific Treg cells and oral tolerance. We found that Treg cells are reduced in microMT(-/-) B cell-deficient mice compared with wild-type (WT) mice. After sublingual Ag/CTB treatment, Treg cells increased much more in WT than in microMT(-/-) mice; however, adoptive transfer of B cells before treatment normalized Treg cell development and functional oral tolerance. B cells from OVA/CTB-treated mice expressed more IL-10 and less CD86 than control B cells. Adoptive transfer of these cells before parenteral immunization with OVA led to efficient suppression of proliferation and to induction of apoptotic depletion of Ag-specific CD25(-)CD4(+) effector T cells associated with the expansion of Treg cells. However, also OVA/CTB-treated microMT(-/-) mice could suppress the immune response to parenteral immunization with OVA, which was associated with a strong increase in Foxp3(-)CD4(+) T cells expressing LAP/TGF-beta. Our results indicate that mucosal tolerance comprises at least two separate pathways: one being B cell dependent and associated with expansion of Treg cells and Treg-mediated suppression and depletion of effector T cells, and one being B cell independent and associated with development of Foxp3(-)LAP(+)TGF-beta(+) regulatory T cells.

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