EphA2 stimulates VCAM-1 expression through calcium-dependent NFAT1 activity

Cell Signal. 2018 Sep:49:30-38. doi: 10.1016/j.cellsig.2018.05.008. Epub 2018 May 21.

Abstract

Endothelial cell activation by proinflammatory stimuli drives leukocyte recruitment through enhanced expression of counter-receptors such as vascular cell adhesion molecule-1 (VCAM-1). We previously demonstrated that activation of the receptor tyrosine kinase EphA2 with its ligand ephrin-A1 induces VCAM-1 expression. Here, we sought to characterize the proinflammatory signaling pathways involved. Analysis of over-represented transcription factors in ephrin-A1-induced genes identified multiple potential transcriptional regulators, including the Rel family members nuclear factor-κB (NF-κB/p65) and nuclear factor of activated T-cells (NFAT). While ephrin-A1 failed to induce endothelial NF-κB activation, NF-κB inhibitors prevented ephrin-A1-induced VCAM-1 expression, suggesting basal NF-κB activity is required. In contrast, ephrin-A1 induced a robust EphA2-dependent increase in NFAT activation, and mutation of the NF-κB/NFAT-binding sites in the VCAM-1 promoter blunted ephrin-A1-induced promoter activity. NFAT activation classically occurs through calcium-dependent calcineurin activation, and inhibiting NFAT signaling with calcineurin inhibitors (cyclosporine A, FK506) or direct NFAT inhibitors (A-285222) was sufficient to block ephrin-A1-induced VCAM-1 expression. Consistent with robust NFAT activation, ephrin-A1-induced an EphA2-dependent calcium influx in endothelial cells that was required for ephrin-A1-induced NFAT activation and VCAM-1 expression. This work provides the first data showing EphA2-dependent calcium influx and NFAT activation and identifies NFAT as a novel EphA2-dependent proinflammatory pathway in endothelial activation.

Keywords: Endothelial; Eph receptor; Ephrin; Inflammation; NFAT; VCAM-1.

MeSH terms

  • Calcium / metabolism*
  • Calcium Signaling / drug effects
  • Cell Line
  • Cell Nucleus / metabolism
  • Cyclosporine / pharmacology
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Ephrin-A2 / antagonists & inhibitors
  • Ephrin-A2 / genetics
  • Ephrin-A2 / metabolism*
  • Gene Expression Regulation / drug effects
  • Histone Deacetylases / metabolism
  • Humans
  • NF-kappa B / metabolism
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / metabolism*
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptor, EphA2
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Vascular Cell Adhesion Molecule-1 / metabolism*

Substances

  • EPHA2 protein, human
  • Ephrin-A2
  • NF-kappa B
  • NFATC Transcription Factors
  • NFATC2 protein, human
  • RNA, Small Interfering
  • Transcription Factors
  • Vascular Cell Adhesion Molecule-1
  • Cyclosporine
  • Receptor, EphA2
  • Histone Deacetylases
  • histone deacetylase 3
  • Calcium