Influence of proinflammatory stimuli on the expression of vascular ribonuclease 1 in endothelial cells

FASEB J. 2014 Feb;28(2):752-60. doi: 10.1096/fj.13-238600. Epub 2013 Oct 30.

Abstract

Extracellular RNA (eRNA) released under injury or pathological conditions has been identified as a yet unrecognized vascular alarm signal to induce procoagulant, permeability-promoting, and proinflammatory activities. eRNA-induced functions were largely prevented by administration of RNase1 as a natural blood vessel-protective antagonist of eRNA. The aim of this study was to investigate the inflammatory regulation of endothelial cell RNase1, which is partly stored in Weibel-Palade bodies of these cells. Long-term treatment of human umbilical vein endothelial cells (HUVECs) with inflammatory agents like tumor necrosis factor α (TNF-α) or interleukin 1β (IL-1β), but not with eRNA, significantly decreased the release (34 ± 5%; 34 ± 7% of control) as well as the cellular expression (19.5 ± 5%; 33 ± 8% of control) of RNase1. Down-regulation of RNase1 by TNF-α stimulation or RNase1 siRNA knockdown increased the permeability of HUVEC monolayers, demonstrated by dearrangement of VE-cadherins at cell-cell borders. Mechanistically, cytokine-induced decrease of RNase1 expression did not involve the nuclear factor κ B (NFκB) signaling pathway but epigenic modifications. Since inhibition of histone deacetylases resulted in recovery of RNase1 expression and secretion after cytokine treatment, an acetylation-dependent process of RNase1 regulation is proposed. These results indicate that cytokine-mediated down-regulation of RNase1 in endothelial cells may aggravate eRNA-induced inflammatory activities and thereby disturbs the vascular homeostasis of the extracellular RNA/RNase system.

Keywords: extracellular RNA; tumor necrosis factor α, vascular homeostasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Human Umbilical Vein Endothelial Cells / drug effects*
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Interleukin-1 / pharmacology
  • Microscopy, Fluorescence
  • Ribonucleases / genetics
  • Ribonucleases / metabolism*
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Interleukin-1
  • Tumor Necrosis Factor-alpha
  • Ribonucleases