TLR3 activation augments matrix metalloproteinase production through reactive nitrogen species generation in human lung fibroblasts

J Immunol. 2014 Jun 1;192(11):4977-88. doi: 10.4049/jimmunol.1302919. Epub 2014 Apr 23.

Abstract

Viral infection often triggers asthma exacerbation and contributes to airway remodeling. Cell signaling in viral infection is mainly mediated through TLR3. Many mediators are involved in airway remodeling, but matrix metalloproteinases (MMPs) are key players in this process in asthma. However, the role of TLR3 activation in production of MMPs is unknown. In this study, we examined the effects of polyinosinic-polycytidylic acid [poly(I:C)], a ligand for TLR3, on production of MMPs in human lung fibroblasts, with a focus on nitrosative stress in TLR3 modulation of MMP production. After lung fibroblasts were treated with poly(I:C), production of MMP-1, -2, and -9 and inducible NO synthase (iNOS) was assessed. The roles of NF-κB and IFN regulatory factor-3 (IRF-3) in the poly(I:C)-mediated production of MMPs and the responsiveness to poly(I:C) of normal lung fibroblasts and asthmatic lung fibroblasts were also investigated. Poly(I:C) augmented production of MMPs and iNOS in fibroblasts, and an iNOS inhibitor diminished this production of MMPs. Poly(I:C) stimulated translocation of NF-κB and IRF-3 into the nucleus in fibroblasts and inhibition of NF-κB or IRF-3 abrogated the poly(I:C)-induced increase in both iNOS expression and release of MMPs. Poly(I:C)-induced production of iNOS and MMPs was greater in asthmatic fibroblasts than in normal fibroblasts. We conclude that viral infection may induce nitrosative stress and subsequent MMP production via NF-κB- and IRF-3-dependent pathways, thus potentiating viral-induced airway remodeling in asthmatic airways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Airway Remodeling / genetics
  • Airway Remodeling / immunology
  • Asthma / genetics
  • Asthma / immunology*
  • Asthma / pathology
  • Cell Line, Tumor
  • Collagenases / genetics
  • Collagenases / immunology*
  • Fibroblasts / immunology*
  • Fibroblasts / pathology
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Enzymologic / immunology
  • Humans
  • Interferon Inducers / pharmacology
  • Interferon Regulatory Factor-3 / genetics
  • Interferon Regulatory Factor-3 / immunology
  • Lung / cytology
  • Lung / immunology*
  • Lung / pathology
  • Lung / virology
  • Nitric Oxide / genetics
  • Nitric Oxide / immunology*
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / immunology
  • Poly I-C / pharmacology
  • Toll-Like Receptor 3 / agonists
  • Toll-Like Receptor 3 / genetics
  • Toll-Like Receptor 3 / immunology*
  • Virus Diseases / genetics
  • Virus Diseases / immunology*
  • Virus Diseases / pathology

Substances

  • IRF3 protein, human
  • Interferon Inducers
  • Interferon Regulatory Factor-3
  • TLR3 protein, human
  • Toll-Like Receptor 3
  • Nitric Oxide
  • NOS2 protein, human
  • Nitric Oxide Synthase Type II
  • Collagenases
  • Poly I-C