IL-1RA regulates immunopathogenesis during fungal-associated allergic airway inflammation

JCI Insight. 2019 Nov 1;4(21):e129055. doi: 10.1172/jci.insight.129055.

Abstract

Severe asthma with fungal sensitization (SAFS) defines a subset of human asthmatics with allergy to 1 or more fungal species and difficult-to-control asthma. We have previously reported that human asthmatics sensitized to fungi have worse lung function and a higher degree of atopy, which was associated with higher IL-1 receptor antagonist (IL-1RA) levels in bronchoalveolar lavage fluid. IL-1RA further demonstrated a significant negative association with bronchial hyperresponsiveness to methacholine. Here, we show that IL-1α and IL-1β are elevated in both bronchoalveolar lavage fluid and sputum from human asthmatics sensitized to fungi, implicating an association with IL-1α, IL-1β, or IL-1RA in fungal asthma severity. In an experimental model of fungal-associated allergic airway inflammation, we demonstrate that IL-1R1 signaling promotes type 1 (IFN-γ, CXCL9, CXCL10) and type 17 (IL-17A, IL-22) responses that were associated with neutrophilic inflammation and increased airway hyperreactivity. Each of these were exacerbated in the absence of IL-1RA. Administration of human recombinant IL-1RA (Kineret/anakinra) during fungal-associated allergic airway inflammation improved airway hyperreactivity and lowered type 1 and type 17 responses. Taken together, these data suggest that IL-1R1 signaling contributes to fungal asthma severity via immunopathogenic type 1 and type 17 responses and can be targeted for improving allergic asthma severity.

Keywords: Asthma; Immunology; Pulmonology.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Animals
  • Asthma / immunology*
  • Asthma / microbiology
  • Bronchial Hyperreactivity
  • Bronchoalveolar Lavage Fluid
  • Female
  • Fungi / pathogenicity*
  • Humans
  • Hypersensitivity / immunology*
  • Hypersensitivity / microbiology
  • Interleukin 1 Receptor Antagonist Protein / physiology*
  • Interleukin-1alpha / metabolism
  • Interleukin-1beta / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Signal Transduction
  • Sputum / metabolism

Substances

  • IL1A protein, human
  • IL1B protein, human
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-1alpha
  • Interleukin-1beta