Double-Stranded RNA Interacts With Toll-Like Receptor 3 in Driving the Acute Inflammatory Response Following Lung Contusion

Crit Care Med. 2016 Nov;44(11):e1054-e1066. doi: 10.1097/CCM.0000000000001879.

Abstract

Objectives: Lung contusion is a major risk factor for the development of acute respiratory distress syndrome. We set to determine the role of toll-like receptor 3 and the binding of double-stranded RNA in the pathogenesis of sterile injury following lung contusion.

Design: Toll-like receptor 3 expression was analyzed in postmortem lung samples from patients with lung contusion. Unilateral lung contusion was induced in toll-like receptor 3 (-/-), TIR-domain-containing adapter-inducing interferon-β (-/-), and wild-type mice. Subsequently, lung injury and inflammation were evaluated. Apoptotic indices, phagocytic activity, and phenotypic characterization of the macrophages were determined. Double-stranded RNA in bronchoalveolar lavage and serum samples following lung contusion was measured. A toll-like receptor 3/double-stranded RNA ligand inhibitor was injected into wild-type mice prior to lung contusion.

Measurements and main results: Toll-like receptor 3 expression was higher in patients and wild-type mice with lung contusion. The degree of lung injury, inflammation, and macrophage apoptosis was reduced in toll-like receptor 3 (-/-), TIR-domain-containing adapter-inducing interferon-β (-/-), and wild-type mice with toll-like receptor 3 antibody neutralization. Alveolar macrophages from toll-like receptor 3 (-/-) mice had a lower early apoptotic index, a predominant M2 phenotype and increased surface translocation of toll-like receptor 3 from the endosome to the surface. When compared with viral activation pathways, lung injury in lung contusion demonstrated increased p38 mitogen-activated protein kinases, extracellular signal-regulated kinase 1/2 phosphorylation with inflammasome activation without a corresponding increase in nuclear factor-κB or type-1 interferon production. Additionally, pretreatment with toll-like receptor 3/double-stranded RNA ligand inhibitor led to a reduction in injury, inflammation, and macrophage apoptosis.

Conclusions: We conclude that the interaction of double-stranded RNA from injured cells with toll-like receptor 3 drives the acute inflammatory response following lung contusion.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / physiology
  • Albumins / metabolism
  • Animals
  • Apoptosis
  • Bronchoalveolar Lavage Fluid
  • Contusions / metabolism*
  • Contusions / pathology
  • Cytokines / metabolism
  • Epithelial Cells / pathology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Humans
  • Inflammasomes / metabolism
  • Lung / metabolism
  • Lung / pathology
  • Lung Injury / metabolism*
  • Lung Injury / pathology
  • Lymphocytes / pathology
  • Macrophages, Alveolar / pathology
  • Mice
  • Myeloid Differentiation Factor 88 / metabolism
  • Phosphorylation
  • RNA, Double-Stranded / metabolism*
  • Toll-Like Receptor 3 / metabolism*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • Albumins
  • Cytokines
  • Inflammasomes
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • RNA, Double-Stranded
  • TICAM-1 protein, mouse
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases