Th2 cytokines impair innate immune responses to rhinovirus in respiratory epithelial cells

Allergy. 2015 Aug;70(8):910-20. doi: 10.1111/all.12627. Epub 2015 Apr 24.

Abstract

Background: Asthma and other Th2 inflammatory conditions have been associated with increased susceptibility to viral infections. The mechanisms by which Th2 cytokines can influence immune responses to infections are largely unknown.

Methods: We measured the effects of Th2 cytokines (IL-4 and IL-13) on bronchial epithelial cell innate immune antiviral responses by assessing interferon (IFN-β and IFN-λ1) induction following rhinovirus (RV)-16 infection. We also investigated the modulatory effects of Th2 cytokines on Toll-like receptor 3 (TLR3), interferon-responsive factor 3 (IRF3) and nuclear factor (NF)-kB, that is key molecules and transcription factors involved in the rhinovirus-induced interferon production and inflammatory cascade. Pharmacological and redox modulation of these pathways was also assessed.

Results: Th2 cytokines impaired RV-16-induced interferon production, increased rhinovirus replication and impaired TLR3 expression in bronchial epithelial cells. These results were replicated in vivo: we found increased IL-4 mRNA levels in nasal epithelial cells from nasal brushing of atopic rhinitis patients and a parallel reduction in TLR3 expression and increased RV-16 replication compared to nonatopic subjects. Mechanistically, Th2 cytokines impaired RV-16-induced activation of IRF3, but had no effects on RV-16-induced NF-kB activation in bronchial epithelial cell cultures. N-acetylcysteine and phosphoinositide 3-kinase (PI3K) inhibitor restored the inhibitory effects of Th2 cytokines over RV-16-induced activation of IRF3.

Conclusions: IL-4 and IL-13, through inhibition of TLR3 expression and signalling (IRF3), impair immune response to RV-16 infection. These data suggest that Th2 conditions increase susceptibility to infections and identify pharmacological approaches with potential to restore impaired immune response in these conditions.

Keywords: Th2 inflammation; asthma; innate immunity; interferon; virus.

MeSH terms

  • Asthma / immunology
  • Asthma / metabolism
  • Bronchi / cytology
  • Cells, Cultured
  • Cytokines / immunology
  • Cytokines / metabolism*
  • Disease Susceptibility
  • Enzyme-Linked Immunosorbent Assay
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism
  • Humans
  • Immunity, Innate / immunology*
  • Interleukin-13 / immunology
  • Interleukin-13 / metabolism
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Real-Time Polymerase Chain Reaction
  • Respiratory Mucosa / immunology
  • Respiratory Mucosa / metabolism
  • Rhinovirus / immunology*
  • Th2 Cells / immunology
  • Th2 Cells / metabolism
  • Toll-Like Receptor 3 / immunology
  • Toll-Like Receptor 3 / metabolism*

Substances

  • Cytokines
  • Interleukin-13
  • NF-kappa B
  • Toll-Like Receptor 3
  • Interleukin-4