The proto-oncogene c-Fos transcriptionally regulates VEGF production during peritoneal inflammation

Kidney Int. 2013 Dec;84(6):1119-28. doi: 10.1038/ki.2013.217. Epub 2013 Jun 12.

Abstract

Vascular endothelial growth factor (VEGF) and transforming growth factor-β1 (TGF-β1) are key mediators of adverse peritoneal membrane remodeling in peritoneal dialysis eventually leading to ultrafiltration failure. Both are pleiotropic growth factors with cell type-dependent regulation of expression and biological effects. Here we studied regulation of TGF-β1-induced VEGF expression in human peritoneal mesothelial cells in the absence or presence of proinflammatory stimuli, tumor necrosis factor-α (TNF-α) or interleukin-1β (IL-1β). Quiescent human peritoneal mesothelial cells secreted only trace amounts of VEGF. Stimulation with TGF-β1 resulted in time- and dose-dependent increases in VEGF mRNA expression and protein release. TNF-α and IL-1β alone had minimal effects but acted in synergy with TGF-β1. Combined stimulation led to induction of transcription factor c-Fos and activation of the VEGF promoter region with high-affinity binding sites for c-Fos. Inhibition of c-Fos by small interfering RNA interference or by pharmacological blockade with SR-11302 decreased VEGF promoter activity and downregulated its expression and release. Exposure of human peritoneal mesothelial cells to dialysate effluent containing increased levels of TGF-β1, TNF-α, and IL-1β obtained during peritonitis resulted in a dose-dependent VEGF induction that was significantly attenuated by SR-11302. Thus, dialysate TGF-β1, IL-1β, and TNF-α act through c-Fos to synergistically upregulate VEGF production in peritoneal mesothelium and may represent an important regulatory link between inflammation and angiogenesis in the peritoneal membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Cells, Cultured
  • Dialysis Solutions / metabolism
  • Dialysis Solutions / therapeutic use
  • Epithelial Cells / drug effects
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism*
  • Humans
  • Inflammation Mediators / metabolism
  • Interleukin-1beta / metabolism
  • Peritoneum / drug effects
  • Peritoneum / immunology
  • Peritoneum / metabolism*
  • Peritonitis / genetics
  • Peritonitis / immunology
  • Peritonitis / metabolism*
  • Peritonitis / therapy
  • Promoter Regions, Genetic
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-fos / antagonists & inhibitors
  • Proto-Oncogene Proteins c-fos / metabolism*
  • RNA Interference
  • RNA, Messenger / metabolism
  • Time Factors
  • Transcription, Genetic*
  • Transfection
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Up-Regulation
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism*

Substances

  • Dialysis Solutions
  • Inflammation Mediators
  • Interleukin-1beta
  • MAS1 protein, human
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-fos
  • RNA, Messenger
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A