IL-4 Causes Hyperpermeability of Vascular Endothelial Cells through Wnt5A Signaling

PLoS One. 2016 May 23;11(5):e0156002. doi: 10.1371/journal.pone.0156002. eCollection 2016.

Abstract

Microvascular leakage due to endothelial barrier dysfunction is a prominent feature of T helper 2 (Th2) cytokine mediated allergic inflammation. Interleukin-4 (IL-4) is a potent Th2 cytokine, known to impair the barrier function of endothelial cells. However, the effectors mediating IL-4 induced cytoskeleton remodeling and consequent endothelial barrier dysfunction remain poorly defined. Here we have used whole genome transcriptome profiling and gene ontology analyses to identify the genes and processes regulated by IL-4 signaling in human coronary artery endothelial cells (HCAEC). The study revealed Wnt5A as an effector that can mediate actin cytoskeleton remodeling in IL-4 activated HCAEC through the regulation of LIM kinase (LIMK) and Cofilin (CFL). Following IL-4 treatment, LIMK and CFL were phosphorylated, thereby indicating the possibility of actin stress fiber formation. Imaging of actin showed the formation of stress fibers in IL-4 treated live HCAEC. Stress fiber formation was notably decreased in the presence of Wnt inhibitory factor 1 (WIF1). Non-invasive impedance measurements demonstrated that IL-4 increased the permeability and impaired the barrier function of HCAEC monolayers. Silencing Wnt5A significantly reduced permeability and improved the barrier function of HCAEC monolayers upon IL-4 treatment. Our study identifies Wnt5A as a novel marker of IL-4 activated vascular endothelium and demonstrates a critical role for Wnt5A in mediating IL-4 induced endothelial barrier dysfunction. Wnt5A could be a potential therapeutic target for reducing microvascular leakage and edema formation in Th2 driven inflammatory diseases.

MeSH terms

  • Capillary Permeability / drug effects*
  • Capillary Permeability / genetics
  • Cell Movement / drug effects
  • Cells, Cultured
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism
  • Gene Expression / drug effects
  • Humans
  • Inflammation / genetics
  • Inflammation / metabolism
  • Interleukin-4 / metabolism
  • Interleukin-4 / pharmacology*
  • RNA, Small Interfering / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Th2 Cells / metabolism
  • Wnt-5a Protein / physiology*

Substances

  • RNA, Small Interfering
  • WNT5A protein, human
  • Wnt-5a Protein
  • Interleukin-4

Grants and funding

GS received the following grants for this study: 1. Swiss National Science Foundation (No. 31-124861; http://www.snf.ch/en/Pages/default.aspx); 2. Novartis Stiftung für Biologisch-Medizinische Forschung (No. 12B35; http://www.stiftungmedbiol.novartis.com/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.