Endothelial cell respiration is affected by the oxygen tension during shear exposure: role of mitochondrial peroxynitrite

Am J Physiol Cell Physiol. 2008 Jul;295(1):C180-91. doi: 10.1152/ajpcell.00549.2007. Epub 2008 May 14.

Abstract

Cultured vascular endothelial cell (EC) exposure to steady laminar shear stress results in peroxynitrite (ONOO(-)) formation intramitochondrially and inactivation of the electron transport chain. We examined whether the "hyperoxic state" of 21% O(2), compared with more physiological O(2) tensions (Po(2)), increases the shear-induced nitric oxide (NO) synthesis and mitochondrial superoxide (O(2)(*-)) generation leading to ONOO(-) formation and suppression of respiration. Electron paramagnetic resonance oximetry was used to measure O(2) consumption rates of bovine aortic ECs sheared (10 dyn/cm(2), 30 min) at 5%, 10%, or 21% O(2) or left static at 5% or 21% O(2). Respiration was inhibited to a greater extent when ECs were sheared at 21% O(2) than at lower Po(2) or left static at different Po(2). Flow in the presence of an endothelial NO synthase (eNOS) inhibitor or a ONOO(-) scavenger abolished the inhibitory effect. EC transfection with an adenovirus that expresses manganese superoxide dismutase in mitochondria, and not a control virus, blocked the inhibitory effect. Intracellular and mitochondrial O(2)(*-) production was higher in ECs sheared at 21% than at 5% O(2), as determined by dihydroethidium and MitoSOX red fluorescence, respectively, and the latter was, at least in part, NO-dependent. Accumulation of NO metabolites in media of ECs sheared at 21% O(2) was modestly increased compared with ECs sheared at lower Po(2), suggesting that eNOS activity may be higher at 21% O(2). Hence, the hyperoxia of in vitro EC flow studies, via increased NO and mitochondrial O(2)(*-) production, leads to enhanced ONOO(-) formation intramitochondrially and suppression of respiration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aorta / cytology
  • Cattle
  • Cell Respiration
  • Cells, Cultured
  • Endothelial Cells / metabolism*
  • Endothelium, Vascular / metabolism
  • Mitochondria / metabolism*
  • Nitric Oxide / biosynthesis
  • Nitric Oxide Synthase Type III / metabolism
  • Oxygen / metabolism*
  • Oxygen Consumption
  • Partial Pressure
  • Peroxynitrous Acid / biosynthesis*
  • Phosphorylation
  • Reactive Oxygen Species / metabolism
  • Shear Strength
  • Stress, Mechanical
  • Superoxide Dismutase / metabolism
  • Superoxides / metabolism

Substances

  • Reactive Oxygen Species
  • Superoxides
  • Peroxynitrous Acid
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • Superoxide Dismutase
  • Oxygen