High pressure induces superoxide production in isolated arteries via protein kinase C-dependent activation of NAD(P)H oxidase

Circulation. 2003 Sep 9;108(10):1253-8. doi: 10.1161/01.CIR.0000079165.84309.4D. Epub 2003 Jul 21.

Abstract

Background: Oxidative stress seems to be present in all forms of hypertension. Thus, we tested the hypothesis that high intraluminal pressure (Pi) itself, by activating vascular oxidases, elicits increased superoxide (O2*-) production interfering with flow-induced dilation.

Methods and results: Isolated, cannulated rat femoral arterial branches were exposed in vitro (for 30 minutes) to normal Pi (80 mm Hg) or high Pi (160 mm Hg). High Pi significantly increased vascular O2*- production (as measured by lucigenin chemiluminescence and ethidium bromide fluorescence) and impaired endothelium-dependent dilations to flow; these effects could be reversed by superoxide dismutase. Administration of the NAD(P)H oxidase inhibitor diphenyleneiodonium, apocynin, the protein kinase C (PKC) inhibitor chelerythrine or staurosporin or the removal of extracellular Ca2+ during high Pi treatment prevented the increases in O2*- production, whereas administration of losartan or captopril had no effect. High Pi resulted in significant increases in intracellular Ca2+ ([Ca2+]i) in the vascular wall (fura 2 fluorescence) and phosphorylation of PKCalpha (Western blotting). The PKC activator phorbol myristate acetate significantly increased vascular O2*- production, which was inhibited by superoxide dismutase, diphenyleneiodonium, chelerythrine, or removal of extracellular Ca2+. Both high Pi and phorbol myristate acetate increased the phosphorylation of the NAD(P)H oxidase subunit p47phox.

Conclusions: High Pi itself elicits arterial O2.- production, most likely by PKC-dependent activation of NAD(P)H oxidase, thus providing a potential explanation for the presence of oxidative stress and endothelial dysfunction in various forms of hypertension and the vasculoprotective effect of antihypertensive agents of different mechanisms of action.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Blood Flow Velocity / physiology
  • Blood Pressure
  • Calcium / metabolism
  • Calcium / pharmacology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism
  • Enzyme Activation / physiology
  • Enzyme Activators / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Femoral Artery / drug effects
  • Femoral Artery / physiopathology*
  • Fluorescent Dyes
  • Hypertension / physiopathology*
  • In Vitro Techniques
  • Male
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism
  • NADH, NADPH Oxidoreductases / antagonists & inhibitors
  • NADH, NADPH Oxidoreductases / metabolism*
  • NADPH Oxidases
  • Oxidoreductases / metabolism*
  • Phosphoproteins / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism*
  • Rats
  • Rats, Wistar
  • Superoxide Dismutase / pharmacology
  • Superoxides / metabolism*
  • Vasodilation / drug effects
  • Vasodilation / physiology

Substances

  • Enzyme Activators
  • Enzyme Inhibitors
  • Fluorescent Dyes
  • Phosphoproteins
  • Superoxides
  • Oxidoreductases
  • Superoxide Dismutase
  • NADH, NADPH Oxidoreductases
  • NADPH Oxidases
  • neutrophil cytosolic factor 1
  • Protein Kinase C
  • Calcium