Allergic conversion of protective mucosal immunity against nasal bacteria in patients with chronic rhinosinusitis with nasal polyposis

J Allergy Clin Immunol. 2019 Mar;143(3):1163-1175.e15. doi: 10.1016/j.jaci.2018.07.006. Epub 2018 Jul 25.

Abstract

Background: Chronic rhinosinusitis with nasal polyposis (CRSwNP) is characterized by eosinophilic inflammation and polyposis at the nose and paranasal sinus and a high concentration of IgE in nasal polyps (NPs). The causative antigen and pathogenesis of CRSwNP remain unknown.

Objective: We aimed to identify reactive allergens of IgE antibodies produced locally in NPs of patients with CRSwNP. We also attempted to unravel the differentiation pathway of IgE-producing B cells in NPs.

Methods: IgE reactivity of patients with CRSwNP was investigated by characterizing single cell-derived mAbs. T-cell response against identified allergens was investigated in vitro. NP-infiltrating lymphocytes were characterized by using flow cytometry. Immunoglobulins expressed in NPs were analyzed by using high-throughput DNA sequencing for immunoglobulin.

Results: About 20% of isolated IgE antibodies derived from NP-residing plasmablasts specifically recognized surface determinants of nasal bacteria, such as Staphylococcus aureus, Streptococcus pyogenes, and Haemophilus influenzae. A TH2 response against S pyogenes was observed in patients with CRSwNP. Flow cytometric analysis revealed sizable germinal center B-like cell and plasmablast subsets expressing IgE on the cell surface in NPs. High-throughput DNA sequencing immunoglobulin analysis highlighted the clonal connectivity of IgE with IgG and IgA1. The Iε-Cα1 circle transcript was detected in NPs.

Conclusions: In patients with CRSwNP, nasal bacteria-reactive B cells differentiate into IgE-producing B cells through IgG/IgA1-IgE class switching, suggesting that allergic conversion of the mucosal response against nasal bacteria underlies disease pathogenesis.

Keywords: Chronic rhinosinusitis with nasal polyposis; IgE; T(H)2 inflammation; high-throughput immunoglobulin analysis; human mAb.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Antibodies, Monoclonal / pharmacology
  • B-Lymphocytes / immunology*
  • Bacteria / immunology*
  • Cells, Cultured
  • Chronic Disease
  • Eosinophilia / immunology
  • Eosinophilia / microbiology
  • Female
  • Humans
  • Immunity, Mucosal*
  • Immunoglobulin E / immunology*
  • Male
  • Middle Aged
  • Nasal Mucosa / immunology
  • Nasal Mucosa / microbiology
  • Nasal Polyps / immunology*
  • Nasal Polyps / microbiology
  • Rhinitis / immunology*
  • Rhinitis / microbiology
  • Sinusitis / immunology*
  • Sinusitis / microbiology
  • Young Adult

Substances

  • Antibodies, Monoclonal
  • Immunoglobulin E