High-dose bee venom exposure induces similar tolerogenic B-cell responses in allergic patients and healthy beekeepers

Allergy. 2017 Mar;72(3):407-415. doi: 10.1111/all.12966. Epub 2016 Jul 20.

Abstract

Background: The involvement of B cells in allergen tolerance induction remains largely unexplored. This study investigates the role of B cells in this process, by comparing B-cell responses in allergic patients before and during allergen immunotherapy (AIT) and naturally exposed healthy beekeepers before and during the beekeeping season.

Methods: Circulating B cells were characterized by flow cytometry. Phospholipase A2 (PLA)-specific B cells were identified using dual-color staining with fluorescently labeled PLA. Expression of regulatory B-cell-associated surface markers, interleukin-10, chemokine receptors, and immunoglobulin heavy-chain isotypes, was measured. Specific and total IgG1, IgG4, IgA, and IgE from plasma as well as culture supernatants of PLA-specific cells were measured by ELISA.

Results: Strikingly, similar responses were observed in allergic patients and beekeepers after venom exposure. Both groups showed increased frequencies of plasmablasts, PLA-specific memory B cells, and IL-10-secreting CD73- CD25+ CD71+ BR 1 cells. Phospholipase A2-specific IgG4-switched memory B cells expanded after bee venom exposure. Interestingly, PLA-specific B cells showed increased CCR5 expression after high-dose allergen exposure while CXCR4, CXCR5, CCR6, and CCR7 expression remained unaffected.

Conclusions: This study provides the first detailed characterization of allergen-specific B cells before and after bee venom tolerance induction. The observed B-cell responses in both venom immunotherapy-treated patients and naturally exposed beekeepers suggest a similar functional immunoregulatory role for B cells in allergen tolerance in both groups. These findings can be investigated in other AIT models to determine their potential as biomarkers of early and successful AIT responses.

Keywords: CCR5; IgG4; Regulatory B cells; allergen-specific immunotherapy; bee venom allergy; immune tolerance.

MeSH terms

  • Allergens / immunology*
  • B-Lymphocyte Subsets / immunology
  • B-Lymphocyte Subsets / metabolism
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Bee Venoms / immunology*
  • Biomarkers
  • Cytokines / biosynthesis
  • Desensitization, Immunologic / methods
  • Dose-Response Relationship, Immunologic*
  • Environmental Exposure / adverse effects*
  • Humans
  • Hypersensitivity / immunology*
  • Hypersensitivity / metabolism
  • Hypersensitivity / therapy
  • Immune Tolerance*
  • Immunoglobulin A / blood
  • Immunoglobulin A / immunology
  • Immunoglobulin E / blood
  • Immunoglobulin E / immunology
  • Immunoglobulin G / blood
  • Immunoglobulin G / immunology
  • Immunophenotyping
  • Lymphocyte Activation / immunology
  • Occupational Exposure
  • Phospholipases A2 / metabolism

Substances

  • Allergens
  • Bee Venoms
  • Biomarkers
  • Cytokines
  • Immunoglobulin A
  • Immunoglobulin G
  • Immunoglobulin E
  • Phospholipases A2