The mucosal adjuvant cholera toxin B instructs non-mucosal dendritic cells to promote IgA production via retinoic acid and TGF-β

PLoS One. 2013;8(3):e59822. doi: 10.1371/journal.pone.0059822. Epub 2013 Mar 20.

Abstract

It is currently unknown how mucosal adjuvants cause induction of secretory immunoglobulin A (IgA), and how T cell-dependent (TD) or -independent (TI) pathways might be involved. Mucosal dendritic cells (DCs) are the primary antigen presenting cells driving TI IgA synthesis, by producing a proliferation-inducing ligand (APRIL), B cell activating factor (BAFF), Retinoic Acid (RA), TGF-β or nitric oxide (NO). We hypothesized that the mucosal adjuvant Cholera Toxin subunit B (CTB) could imprint non-mucosal DCs to induce IgA synthesis, and studied the mechanism of its induction. In vitro, CTB-treated bone marrow derived DCs primed for IgA production by B cells without the help of T cells, yet required co-signaling by different Toll-like receptor (TLR) ligands acting via the MyD88 pathway. CTB-DC induced IgA production was blocked in vitro or in vivo when RA receptor antagonist, TGF-β signaling inhibitor or neutralizing anti-TGF-β was added, demonstrating the involvement of RA and TGF-β in promoting IgA responses. There was no major involvement for BAFF, APRIL or NO. This study highlights that synergism between CTB and MyD88-dependent TLR signals selectively imprints a TI IgA-inducing capacity in non-mucosal DCs, explaining how CTB acts as an IgA promoting adjuvant.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / pharmacology*
  • Analysis of Variance
  • Animals
  • B-Lymphocytes / metabolism
  • Cell Culture Techniques
  • Cholera Toxin / pharmacology*
  • DNA Primers / genetics
  • Dendritic Cells / metabolism*
  • Enzyme-Linked Immunosorbent Assay
  • Female
  • Immunoglobulin A / biosynthesis*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Myeloid Differentiation Factor 88 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Statistics, Nonparametric
  • Transforming Growth Factor beta / metabolism*
  • Tretinoin / metabolism*

Substances

  • Adjuvants, Immunologic
  • DNA Primers
  • Immunoglobulin A
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Transforming Growth Factor beta
  • Tretinoin
  • Cholera Toxin

Grants and funding

This work was supported by the Dutch Organization for Scientific Research (NWO), Grant No ZONMW 40-40100-94-9024 (HHS), STW 10725 (YZ and HHS), the Netherlands Asthma Foundation (NAF) Grant No 06.043 (AKG). BNL is a recipient of an Odysseus Grant of the Fonds Wetenschappelijk Onderzoek (FWO) Flanders, a European Research Council (ERC) grant of the EU, and of a Multidisciplinary Research Partnerships (MRP) grant of Ghent University (Group-ID consortium). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.