Syndecan-1 Attenuates Lung Injury during Influenza Infection by Potentiating c-Met Signaling to Suppress Epithelial Apoptosis

Am J Respir Crit Care Med. 2016 Aug 1;194(3):333-44. doi: 10.1164/rccm.201509-1878OC.

Abstract

Rationale: Syndecan-1 is a cell surface heparan sulfate proteoglycan primarily expressed in the lung epithelium. Because the influenza virus is tropic to the airway epithelium, we investigated the role of syndecan-1 in influenza infection.

Objectives: To determine the mechanism by which syndecan-1 regulates the lung mucosal response to influenza infection.

Methods: Wild-type (WT) and Sdc1(-/-) mice were infected with a H1N1 virus (PR8) as an experimental model of influenza infection. Human and murine airway epithelial cell cultures were also infected with PR8 to study the mechanism by which syndecan-1 regulates the inflammatory response.

Measurement and main results: We found worsened outcomes and lung injury in Sdc1(-/-) mice compared with WT mice after influenza infection. Our data demonstrated that syndecan-1 suppresses bronchial epithelial apoptosis during influenza infection to limit widespread lung inflammation. Furthermore, we determined that syndecan-1 attenuated apoptosis by crosstalking with c-Met to potentiate its cytoprotective signals in airway epithelial cells during influenza infection.

Conclusions: Our work shows that cell-associated syndecan-1 has an important role in regulating lung injury. Our findings demonstrate a novel mechanism in which cell membrane-associated syndecan-1 regulates the innate immune response to influenza infection by facilitating cytoprotective signals through c-Met signaling to limit bronchial epithelial apoptosis, thereby attenuating lung injury and inflammation.

Keywords: c-Met; influenza; lung injury; proteoglycan; syndecan-1.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / immunology*
  • Disease Models, Animal
  • Epithelial Cells / immunology
  • Humans
  • Immunity, Innate / immunology
  • Influenza A Virus, H1N1 Subtype / immunology*
  • Lung / immunology
  • Lung Injury / immunology
  • Lung Injury / prevention & control*
  • Mice
  • Orthomyxoviridae Infections / immunology*
  • Proto-Oncogene Proteins c-met / genetics
  • Proto-Oncogene Proteins c-met / immunology*
  • Signal Transduction / immunology*
  • Syndecan-1 / immunology
  • Syndecan-1 / pharmacology*

Substances

  • Syndecan-1
  • Proto-Oncogene Proteins c-met