Activation of the JAK/STAT3 and PI3K/AKT pathways are crucial for IL-6 trans-signaling-mediated pro-inflammatory response in human vascular endothelial cells

Cell Commun Signal. 2018 Sep 5;16(1):55. doi: 10.1186/s12964-018-0268-4.

Abstract

Background: IL-6 classic signaling is linked to anti-inflammatory functions while the trans-signaling is associated with pro-inflammatory responses. Classic signaling is induced via membrane-bound IL-6 receptor (IL-6R) whereas trans-signaling requires prior binding of IL-6 to the soluble IL-6R. In both cases, association with the signal transducing gp130 receptor is compulsory. However, differences in the downstream signaling mechanisms of IL-6 classic- versus trans-signaling remains largely elusive.

Methods: In this study, we used flow cytometry, quantitative PCR, ELISA and immuno-blotting techniques to investigate IL-6 classic and trans-signaling mechanisms in Human Umbilical Vein Endothelial Cells (HUVECs).

Results: We show that both IL-6R and gp130 are expressed on the surface of human vascular endothelial cells, and that the expression is affected by pro-inflammatory stimuli. In contrast to IL-6 classic signaling, IL-6 trans-signaling induces the release of the pro-inflammatory chemokine Monocyte Chemoattractant Protein-1 (MCP-1) from human vascular endothelial cells. In addition, we reveal that the classic signaling induces activation of the JAK/STAT3 pathway while trans-signaling also activates the PI3K/AKT and the MEK/ERK pathways. Furthermore, we demonstrate that MCP-1 induction by IL-6 trans-signaling requires simultaneous activation of the JAK/STAT3 and PI3K/AKT pathways.

Conclusions: Collectively, our study reports molecular differences in IL-6 classic- and trans-signaling in human vascular endothelial cells; and elucidates the pathways which mediate MCP-1 induction by IL-6 trans-signaling.

Keywords: Endothelium; HUVECs; Interleukin-6 signaling; Monocyte chemoattractant Protein-1; Pro-inflammatory cytokines.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chemokine CCL2 / metabolism
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology*
  • Gene Expression Regulation
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-6 / metabolism*
  • Janus Kinases / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Proto-Oncogene Proteins c-akt / metabolism*
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction*

Substances

  • CCL2 protein, human
  • Chemokine CCL2
  • Interleukin-6
  • STAT3 Transcription Factor
  • Phosphatidylinositol 3-Kinases
  • Janus Kinases
  • Proto-Oncogene Proteins c-akt