GM-CSF treatment prevents respiratory syncytial virus-induced pulmonary exacerbation responses in postallergic mice by stimulating alveolar macrophage maturation

J Allergy Clin Immunol. 2016 Mar;137(3):700-9.e9. doi: 10.1016/j.jaci.2015.09.031. Epub 2015 Nov 10.

Abstract

Background: Human respiratory syncytial virus (RSV) is a frequent cause of asthma exacerbations, yet the susceptibility of asthmatic patients to RSV is poorly understood.

Objective: We sought to address the contribution of resident alveolar macrophages (rAMs) to susceptibility to RSV infection in mice that recovered from allergic airway eosinophilia.

Methods: Mice were infected with RSV virus after clearance of allergic airway inflammation (AAI). The contribution of post-AAI rAMs was studied in vivo by means of clodronate liposome-mediated depletion, adoptive transfer, and treatment with recombinant cytokines before RSV infection.

Results: After clearing the allergic bronchial inflammation, post-AAI mice had bronchial hyperreactivity and increased inflammatory cell influx when infected with RSV compared with nonallergic mice, whereas viral clearance was comparable in both mouse groups. Post-AAI rAMs were necessary and sufficient for mediating these proinflammatory effects. In post-AAI mice the residing CD11c(hi) autofluorescent rAM population did not upregulate the terminal differentiation marker sialic acid-binding immunoglobulin-like lectin F and overproduced TNF and IL-6 through increased nuclear factor κB nuclear translocation. In line with these results, post-AAI lungs had reduced levels of the rAM maturation cytokine GM-CSF. Intratracheal administration of GM-CSF induced final rAM maturation in post-AAI mice and prevented the increased susceptibility to RSV-induced hyperreactivity and inflammation.

Conclusion: Defective production of GM-CSF leads to insufficient post-AAI rAM maturation in mice that recovered from an AAI, causing increased susceptibility to RSV-induced immunopathology. Promoting the differentiation of post-AAI rAMs might be a therapeutic option for preventing RSV-induced exacerbations in human asthmatic patients.

Keywords: Allergic asthma; GM-CSF; alveolar macrophage; respiratory syncytial virus–induced exacerbation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Allergens / immunology
  • Animals
  • Asthma / complications*
  • Asthma / immunology
  • Asthma / metabolism
  • Asthma / pathology
  • Asthma / therapy
  • Bronchoalveolar Lavage Fluid
  • Cytokines / metabolism
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Granulocyte-Macrophage Colony-Stimulating Factor / pharmacology*
  • Humans
  • Immunophenotyping
  • Inflammation Mediators / metabolism
  • Lung / immunology
  • Lung / metabolism
  • Lung / pathology
  • Lung / virology
  • Macrophages, Alveolar / drug effects*
  • Macrophages, Alveolar / immunology
  • Macrophages, Alveolar / metabolism
  • Mice
  • NF-kappa B / metabolism
  • Phenotype
  • Respiratory Syncytial Virus Infections / complications*
  • Respiratory Syncytial Virus Infections / immunology
  • Respiratory Syncytial Virus Infections / metabolism
  • Respiratory Syncytial Virus Infections / pathology
  • Respiratory Syncytial Virus, Human*

Substances

  • Allergens
  • Cytokines
  • Inflammation Mediators
  • NF-kappa B
  • Granulocyte-Macrophage Colony-Stimulating Factor