CD23 provides a noninflammatory pathway for IgE-allergen complexes

J Allergy Clin Immunol. 2020 Jan;145(1):301-311.e4. doi: 10.1016/j.jaci.2019.07.045. Epub 2019 Aug 19.

Abstract

Background: Type I hypersensitivity is mediated by allergen-specific IgE, which sensitizes the high-affinity IgE receptor FcεRI on mast cells and basophils and drives allergic inflammation upon secondary allergen contact. CD23/FcεRII, the low-affinity receptor for IgE, is constitutively expressed on B cells and has been shown to regulate immune responses. Simultaneous binding of IgE to FcεRI and CD23 is blocked by reciprocal allosteric inhibition, suggesting that the 2 receptors exert distinct roles in IgE handling.

Objective: We aimed to study how free IgE versus precomplexed IgE-allergen immune complexes (IgE-ICs) target the 2 IgE receptors FcεRI and CD23, and we investigated the functional implications of the 2 pathways.

Methods: We performed binding and activation assays with human cells in vitro and IgE pharmacokinetics and anaphylaxis experiments in vivo.

Results: We demonstrate that FcεRI preferentially binds free IgE and CD23 preferentially binds IgE-ICs. We further show that those different binding properties directly translate to distinct biological functions: free IgE initiated allergic inflammation through FcεRI on allergic effector cells, while IgE-ICs were noninflammatory because of reduced FcεRI binding and enhanced CD23-dependent serum clearance.

Conclusion: We propose that IgE-ICs are noninflammatory through reduced engagement by FcεRI but increased targeting of the CD23 pathway.

Keywords: CD23; FcεRI; IgE clearance; IgE sensitization; IgE-allergen complex; inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allergens / genetics
  • Allergens / immunology*
  • Anaphylaxis / genetics
  • Anaphylaxis / immunology*
  • Anaphylaxis / pathology
  • Animals
  • Antigen-Antibody Complex / genetics
  • Antigen-Antibody Complex / immunology*
  • Humans
  • Immunoglobulin E / immunology*
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology*
  • Mice
  • Mice, Knockout
  • Receptors, IgE / genetics
  • Receptors, IgE / immunology*
  • Signal Transduction / genetics
  • Signal Transduction / immunology*

Substances

  • Allergens
  • Antigen-Antibody Complex
  • FCER2 protein, human
  • Lectins, C-Type
  • Receptors, IgE
  • Immunoglobulin E