The Innate Immune Protein S100A9 Protects from T-Helper Cell Type 2-mediated Allergic Airway Inflammation

Am J Respir Cell Mol Biol. 2019 Oct;61(4):459-468. doi: 10.1165/rcmb.2018-0217OC.

Abstract

Calprotectin is a heterodimer of the proteins S100A8 and S100A9, and it is an abundant innate immune protein associated with inflammation. In humans, calprotectin transcription and protein abundance are associated with asthma and disease severity. However, mechanistic studies in experimental asthma models have been inconclusive, identifying both protective and pathogenic effects of calprotectin. To clarify the role of calprotectin in asthma, calprotectin-deficient S100A9-/- and wild-type (WT) C57BL/6 mice were compared in a murine model of allergic airway inflammation. Mice were intranasally challenged with extracts of the clinically relevant allergen, Alternaria alternata (Alt Ext), or PBS every third day over 9 days. On Day 10, BAL fluid and lung tissue homogenates were harvested and allergic airway inflammation was assessed. Alt Ext challenge induced release of S100A8/S100A9 to the alveolar space and increased protein expression in the alveolar epithelium of WT mice. Compared with WT mice, S100A9-/- mice displayed significantly enhanced allergic airway inflammation, including production of IL-13, CCL11, CCL24, serum IgE, eosinophil recruitment, and airway resistance and elastance. In response to Alt Ext, S100A9-/- mice accumulated significantly more IL-13+IL-5+CD4+ T-helper type 2 cells. S100A9-/- mice also accumulated a significantly lower proportion of CD4+ T regulatory (Treg) cells in the lung that had significantly lower expression of CD25. Calprotectin enhanced WT Treg cell suppressive activity in vitro. Therefore, this study identifies a role for the innate immune protein, S100A9, in protection from CD4+ T-helper type 2 cell hyperinflammation in response to Alt Ext. This protection is mediated, at least in part, by CD4+ Treg cell function.

Keywords: CD4+ T cells; S100A9; allergic airway inflammation; calprotectin; knockout mouse.

Publication types

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

MeSH terms

  • Adaptive Immunity
  • Allergens / toxicity
  • Alternaria / immunology
  • Alveolitis, Extrinsic Allergic / etiology
  • Alveolitis, Extrinsic Allergic / immunology*
  • Alveolitis, Extrinsic Allergic / pathology
  • Animals
  • Bronchial Hyperreactivity / etiology
  • Bronchial Hyperreactivity / immunology
  • Bronchial Hyperreactivity / pathology
  • Bronchoalveolar Lavage Fluid / chemistry
  • Calgranulin A / biosynthesis
  • Calgranulin A / genetics
  • Calgranulin B / genetics
  • Calgranulin B / physiology*
  • Cytokines / metabolism
  • Forkhead Transcription Factors / biosynthesis
  • Forkhead Transcription Factors / genetics
  • Immunoglobulin E / immunology
  • Inflammation
  • Leukocyte L1 Antigen Complex / physiology*
  • Lung / immunology*
  • Lung / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pulmonary Eosinophilia / etiology
  • Pulmonary Eosinophilia / immunology
  • Pulmonary Eosinophilia / pathology
  • Specific Pathogen-Free Organisms
  • T-Lymphocytes, Regulatory / immunology*
  • Th2 Cells / immunology*

Substances

  • Allergens
  • Calgranulin A
  • Calgranulin B
  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Leukocyte L1 Antigen Complex
  • S100A9 protein, mouse
  • S100a8 protein, mouse
  • Immunoglobulin E