Eosinophil-derived IFN-gamma induces airway hyperresponsiveness and lung inflammation in the absence of lymphocytes

J Allergy Clin Immunol. 2009 Sep;124(3):573-82, 582.e1-9. doi: 10.1016/j.jaci.2009.04.031. Epub 2009 Jun 21.

Abstract

Background: Eosinophils are key players in T(H)2-driven pathologies, such as allergic lung inflammation. After IL-5- and eotaxin-mediated tissue recruitment, they release several cytotoxic and inflammatory mediators. However, their exact contribution to asthma remains controversial. Indeed, in human subjects anti-IL-5 treatment inhibits eosinophilia but not antigen-induced airway hyperresponsiveness (AHR). Likewise, lung fibrosis is abrogated in 2 strains of eosinophil-deficient mice, whereas AHR is inhibited in only one of them. Finally, eosinophils have been shown to attract T(H)2 lymphocytes at the inflammatory site.

Objective: The ability of eosinophils to promote AHR and lung inflammation independently of lymphocytes was investigated.

Methods: Adoptive transfers of resting or activated eosinophils from IL-5 transgenic mice were performed into naive BALB/c mice, mice with severe combined immunodeficiency, and IFN-gamma-deficient BALB/c recipients.

Results: Adoptively transferred eosinophils induced lung inflammation, fibrosis, collagen deposition, and AHR not only in BALB/c mice but also in recipient mice with severe combined immunodeficiency. Surprisingly, IFN-gamma expression was increased in lungs from eosinophil-transferred animals. Furthermore, IFN-gamma neutralization in recipients partially inhibited eosinophil-induced AHR. Moreover, IFN-gamma-deficient eosinophils or eosinophils treated with a blocking anti-IFN-gamma receptor antibody failed to induce AHR in IFN-gamma-deficient recipients. Finally, in vitro and at low concentrations, IFN-gamma increased eosinophil peroxidase release, potentiated chemotaxis, and prolonged survival, suggesting the existence of an autocrine mechanism.

Conclusions: These results support the important and previously unsuspected contribution of eosinophils to lung inflammation independently of lymphocytes through production of IFN-gamma, the prototypical T(H)1 cytokine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Bronchial Hyperreactivity / etiology
  • Bronchial Hyperreactivity / immunology*
  • Bronchial Hyperreactivity / metabolism
  • Chemotaxis / immunology
  • Eosinophil Peroxidase / analysis
  • Eosinophils / immunology*
  • Eosinophils / metabolism
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism*
  • Interleukin-5 / immunology*
  • Interleukin-5 / metabolism
  • Lung / immunology
  • Lung / pathology
  • Lymphocytes / immunology*
  • Lymphocytes / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Mice, SCID
  • Mice, Transgenic
  • Pneumonia / etiology
  • Pneumonia / immunology*
  • Pneumonia / metabolism
  • Receptors, Interferon / immunology
  • Receptors, Interferon / metabolism

Substances

  • Interleukin-5
  • Receptors, Interferon
  • Interferon-gamma
  • Eosinophil Peroxidase