Serum amyloid A promotes lung neutrophilia by increasing IL-17A levels in the mucosa and γδ T cells

Am J Respir Crit Care Med. 2013 Jul 15;188(2):179-86. doi: 10.1164/rccm.201211-2139OC.

Abstract

Rationale: Neutrophilic inflammation is an important pathologic feature of chronic obstructive pulmonary disease (COPD) and infectious exacerbations of COPD. Serum amyloid A (SAA) promotes neutrophilic inflammation by its interaction with lung mucosal ALX/FPR2 receptors. However, little is known about how this endogenous mediator regulates IL-17A immunity.

Objectives: To determine whether SAA causes neutrophilic inflammation by IL-17A-dependent mechanisms.

Methods: The relationship between SAA and neutrophils was investigated in lung sections from patients with COPD and a chronic mouse model of SAA exposure. A neutralizing antibody to IL-17A was used to block SAA responses in vivo, and a cell-sorting strategy was used to identify cellular sources.

Measurements and main results: SAA mRNA expression was positively associated with tissue neutrophils in COPD (P < 0.05). SAA predominately promoted expression of the TH17 polarizing cytokine IL-6, which was opposed by 15-epi-lipoxin A4, a counter-regulatory mediator, and ALX/FPR2 ligand. SAA-induced inflammation was markedly reduced by a neutralizing antibody to IL-17A in vivo. Cellular sources of IL-17A induced by SAA include CD4(+) T cells, γδ T cells, and an Epcam(+)CD45(-) population enriched for epithelial cells. SAA promotes expression of IL-17A in γδ T cells and this innate cell proportionally expressed higher levels of IL-17A transcript than CD4(+) T cells or epithelial cells.

Conclusions: The SAA-IL-17A axis represents an important innate defense network that may underlie persistent neutrophilic airway inflammation in COPD and modulating the ALX/FPR2 receptor represents a novel approach to targeting aberrant IL-17A-mediated lung immunity.

Publication types

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

MeSH terms

  • Animals
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cells, Cultured
  • Disease Models, Animal
  • Flow Cytometry
  • Humans
  • Immunity, Innate
  • Immunohistochemistry
  • Inflammation / immunology
  • Interleukin-17 / blood
  • Interleukin-17 / immunology*
  • Lung / cytology
  • Lung / immunology*
  • Mice
  • Neutrophil Infiltration / physiology
  • Neutrophils / immunology*
  • Neutrophils / pathology
  • Pulmonary Disease, Chronic Obstructive / blood
  • Pulmonary Disease, Chronic Obstructive / immunology*
  • Respiratory Mucosa / immunology
  • Serum Amyloid A Protein / analysis
  • Serum Amyloid A Protein / immunology*
  • T-Lymphocyte Subsets / immunology

Substances

  • Interleukin-17
  • Serum Amyloid A Protein