Versican is produced by Trif- and type I interferon-dependent signaling in macrophages and contributes to fine control of innate immunity in lungs

Am J Physiol Lung Cell Mol Physiol. 2017 Dec 1;313(6):L1069-L1086. doi: 10.1152/ajplung.00353.2017. Epub 2017 Sep 14.

Abstract

Growing evidence suggests that versican is important in the innate immune response to lung infection. Our goal was to understand the regulation of macrophage-derived versican and the role it plays in innate immunity. We first defined the signaling events that regulate versican expression, using bone marrow-derived macrophages (BMDMs) from mice lacking specific Toll-like receptors (TLRs), TLR adaptor molecules, or the type I interferon receptor (IFNAR1). We show that LPS and polyinosinic-polycytidylic acid [poly(I:C)] trigger a signaling cascade involving TLR3 or TLR4, the Trif adaptor, type I interferons, and IFNAR1, leading to increased expression of versican by macrophages and implicating versican as an interferon-stimulated gene. The signaling events regulating versican are distinct from those for hyaluronan synthase 1 (HAS1) and syndecan-4 in macrophages. HAS1 expression requires TLR2 and MyD88. Syndecan-4 requires TLR2, TLR3, or TLR4 and both MyD88 and Trif. Neither HAS1 nor syndecan-4 is dependent on type I interferons. The importance of macrophage-derived versican in lungs was determined with LysM/Vcan-/- mice. These studies show increased recovery of inflammatory cells in the bronchoalveolar lavage fluid of poly(I:C)-treated LysM/Vcan-/- mice compared with control mice. IFN-β and IL-10, two important anti-inflammatory molecules, are significantly decreased in both poly(I:C)-treated BMDMs from LysM/Vcan-/- mice and bronchoalveolar lavage fluid from poly(I:C)-treated LysM/Vcan-/- mice compared with control mice. In short, type I interferon signaling regulates versican expression, and versican is necessary for type I interferon production. These findings suggest that macrophage-derived versican is an immunomodulatory molecule with anti-inflammatory properties in acute pulmonary inflammation.

Keywords: hyaluronan synthase 1; inflammation; type I interferons; versican, syndecan-4.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics
  • Adaptor Proteins, Vesicular Transport / immunology*
  • Animals
  • Hyaluronan Synthases / genetics
  • Hyaluronan Synthases / immunology
  • Immunity, Innate*
  • Interferon-beta / immunology*
  • Interleukin-10 / genetics
  • Interleukin-10 / immunology
  • Lipopolysaccharides / toxicity
  • Lung / immunology*
  • Macrophages, Alveolar / immunology*
  • Mice
  • Mice, Knockout
  • Receptor, Interferon alpha-beta / genetics
  • Receptor, Interferon alpha-beta / immunology
  • Syndecan-4 / genetics
  • Syndecan-4 / immunology
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / immunology
  • Versicans / genetics
  • Versicans / immunology*

Substances

  • Adaptor Proteins, Vesicular Transport
  • IL10 protein, mouse
  • Ifnar1 protein, mouse
  • Lipopolysaccharides
  • Sdc4 protein, mouse
  • Syndecan-4
  • TICAM-1 protein, mouse
  • Toll-Like Receptors
  • Vcan protein, mouse
  • lipopolysaccharide, Escherichia coli O111 B4
  • Versicans
  • Interleukin-10
  • Receptor, Interferon alpha-beta
  • Interferon-beta
  • Hyaluronan Synthases