Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice

J Immunol. 2011 Feb 1;186(3):1666-1674. doi: 10.4049/jimmunol.1002194. Epub 2010 Dec 22.

Abstract

Staphylococcus aureus is a significant cause of hospital and community acquired pneumonia and causes secondary infection after influenza A. Recently, patients with hyper-IgE syndrome, who often present with S. aureus infections of the lung and skin, were found to have mutations in STAT3, required for Th17 immunity, suggesting a potential critical role for Th17 cells in S. aureus pneumonia. Indeed, IL-17R(-/-) and IL-22(-/-) mice displayed impaired bacterial clearance of S. aureus compared with that of wild-type mice. Mice challenged with influenza A PR/8/34 H1N1 and subsequently with S. aureus had increased inflammation and decreased clearance of both virus and bacteria. Coinfection resulted in greater type I and II IFN production in the lung compared with that with virus infection alone. Importantly, influenza A coinfection resulted in substantially decreased IL-17, IL-22, and IL-23 production after S. aureus infection. The decrease in S. aureus-induced IL-17, IL-22, and IL-23 was independent of type II IFN but required type I IFN production in influenza A-infected mice. Furthermore, overexpression of IL-23 in influenza A, S. aureus-coinfected mice rescued the induction of IL-17 and IL-22 and markedly improved bacterial clearance. These data indicate a novel mechanism by which influenza A-induced type I IFNs inhibit Th17 immunity and increase susceptibility to secondary bacterial pneumonia.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Genetic Predisposition to Disease
  • Humans
  • Influenza A Virus, H1N1 Subtype / immunology*
  • Interferon Type I / administration & dosage
  • Interferon Type I / biosynthesis
  • Interleukin-17 / antagonists & inhibitors*
  • Interleukin-17 / deficiency
  • Interleukin-17 / physiology*
  • Interleukin-22
  • Interleukin-23 / antagonists & inhibitors
  • Interleukins / antagonists & inhibitors
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Orthomyxoviridae Infections / genetics
  • Orthomyxoviridae Infections / immunology*
  • Orthomyxoviridae Infections / microbiology
  • Pneumonia, Bacterial / genetics
  • Pneumonia, Bacterial / immunology*
  • Pneumonia, Bacterial / virology
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Staphylococcal Infections / genetics
  • Staphylococcal Infections / immunology*
  • Staphylococcal Infections / virology
  • Staphylococcus aureus / immunology
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Helper-Inducer / metabolism
  • T-Lymphocytes, Helper-Inducer / virology

Substances

  • Il17a protein, mouse
  • Interferon Type I
  • Interleukin-17
  • Interleukin-23
  • Interleukins