The peroxynitrite donor 3-morpholinosydnonimine activates Nrf2 and the UPR leading to a cytoprotective response in endothelial cells

Cell Signal. 2012 Jan;24(1):199-213. doi: 10.1016/j.cellsig.2011.09.002. Epub 2011 Sep 14.

Abstract

Endothelial dysfunction is associated with the formation of peroxynitrite, described to be toxic. Recent data also suggests that peroxynitrite is able to activate the protective Nrf2 pathway and/or the unfolded protein response (UPR). The aim of our work was to study the response of human endothelial cells to 3-morpholinosydnonimine (SIN-1), a peroxynitrite donor, and to highlight the possible protective roles of Nrf2 or the UPR pathway in this response. Immortal and primary human umbilical vein endothelial cells were exposed to SIN-1. SIN-1 incubation led to Nrf2 activation and to the overexpression of Nrf2-regulated genes, heme oxygenase-1 (HO-1) and NAD(P)H quinone oxidoreductase 1. We also demonstrated that this defensive response protected cells against cell death induced by serum starvation, by reducing apoptosis (monitored by caspase-3 activity and DNA fragmentation) and favoring autophagosome formation, as evidenced by LC3-II accumulation. Interestingly, we observed an activation of the UPR, with a rapid and significant overexpression of CHOP in serum starved cells stimulated with SIN-1. While siRNA mediated knockdown of CHOP had no effect on DNA fragmentation, the invalidation of Nrf2 or HO-1 by siRNA strongly increased DNA fragmentation, but also reinforced the SIN-1-induced LC3-II accumulation. This study shows that peroxynitrite, at least at sublethal concentrations and within a narrow concentration range, could exert protective effects on endothelial cells by modulating the balance between autophagy and apoptosis, through Nrf2-dependent pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Autophagy
  • Cell Line
  • Cell Nucleus / metabolism
  • Cell Survival
  • Cytoprotection*
  • DNA Fragmentation
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism
  • Humans
  • Molsidomine / analogs & derivatives*
  • Molsidomine / pharmacology
  • NAD(P)H Dehydrogenase (Quinone) / genetics
  • NAD(P)H Dehydrogenase (Quinone) / metabolism
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism*
  • Oxidants / pharmacology*
  • Peroxynitrous Acid / pharmacology*
  • Protein Transport / drug effects
  • RNA Interference
  • Signal Transduction
  • Transcription Factor CHOP / genetics
  • Transcription Factor CHOP / metabolism
  • Transcription, Genetic
  • Unfolded Protein Response*

Substances

  • DDIT3 protein, human
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Oxidants
  • Peroxynitrous Acid
  • Transcription Factor CHOP
  • linsidomine
  • Molsidomine
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • NAD(P)H Dehydrogenase (Quinone)
  • NQO1 protein, human