Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system

Circulation. 1999 Apr 20;99(15):2027-33. doi: 10.1161/01.cir.99.15.2027.

Abstract

Background: Angiotensin II activates NAD(P)H-dependent oxidases via AT1-receptor stimulation, the most important vascular source of superoxide (O2*-). The AT1 receptor is upregulated in vitro by low-density lipoprotein. The present study was designed to test whether hypercholesterolemia is associated with increased NAD(P)H-dependent vascular O2*- production and whether AT1-receptor blockade may inhibit this oxidase and in parallel improve endothelial dysfunction.

Methods and results: Vascular responses were determined by isometric tension studies, and relative rates of vascular O2*- production were determined by use of chemiluminescence with lucigenin, a cypridina luciferin analogue, and electron spin resonance studies. AT1-receptor mRNA was quantified by Northern analysis, and AT1-receptor density was measured by radioligand binding assays. Hypercholesterolemia was associated with impaired endothelium-dependent vasodilation and increased O2*- production in intact vessels. In vessel homogenates, we found a significant activation of NADH-driven O2*- production in both models of hyperlipidemia. Treatment of cholesterol-fed animals with the AT1-receptor antagonist Bay 10-6734 improved endothelial dysfunction, normalized vascular O2*- and NADH-oxidase activity, decreased macrophage infiltration, and reduced early plaque formation. In the setting of hypercholesterolemia, the aortic AT1 receptor mRNA was upregulated to 166+/-11%, accompanied by a comparable increase in AT1-receptor density.

Conclusions: Hypercholesterolemia is associated with AT1-receptor upregulation, endothelial dysfunction, and increased NADH-dependent vascular O2*- production. The improvement of endothelial dysfunction, inhibition of the oxidase, and reduction of early plaque formation by an AT1-receptor antagonist suggests a crucial role of angiotensin II-mediated O2*- production in the early stage of atherosclerosis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Acridines / analysis
  • Amlodipine / pharmacology
  • Amlodipine / therapeutic use
  • Angiotensin Receptor Antagonists*
  • Angiotensin-Converting Enzyme Inhibitors / pharmacology
  • Animals
  • Antihypertensive Agents / pharmacology
  • Antihypertensive Agents / therapeutic use
  • Arteriosclerosis / enzymology*
  • Arteriosclerosis / etiology
  • Arteriosclerosis / physiopathology
  • Diet, Atherogenic
  • Dihydropyridines / pharmacology
  • Electron Spin Resonance Spectroscopy
  • Hypercholesterolemia / complications
  • Hypercholesterolemia / drug therapy
  • Hypercholesterolemia / enzymology*
  • Hypercholesterolemia / genetics
  • Lipids / blood
  • Luminescent Measurements
  • Macrophages / pathology
  • Male
  • Multienzyme Complexes / metabolism*
  • NADH, NADPH Oxidoreductases / metabolism*
  • Phenylephrine / pharmacology
  • Rabbits
  • Receptor, Angiotensin, Type 1
  • Receptor, Angiotensin, Type 2
  • Receptors, Angiotensin / biosynthesis
  • Receptors, Angiotensin / physiology
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • Renin-Angiotensin System / physiology*
  • Superoxides / metabolism*
  • Tetrazoles / pharmacology
  • Up-Regulation
  • Vasoconstriction / drug effects
  • Vasoconstrictor Agents / pharmacology
  • Vasodilation / drug effects
  • Vasodilator Agents / pharmacology
  • Vasodilator Agents / therapeutic use

Substances

  • Acridines
  • Angiotensin Receptor Antagonists
  • Angiotensin-Converting Enzyme Inhibitors
  • Antihypertensive Agents
  • Dihydropyridines
  • Lipids
  • Multienzyme Complexes
  • Receptor, Angiotensin, Type 1
  • Receptor, Angiotensin, Type 2
  • Receptors, Angiotensin
  • Receptors, LDL
  • Tetrazoles
  • Vasoconstrictor Agents
  • Vasodilator Agents
  • Superoxides
  • Amlodipine
  • Phenylephrine
  • 10,10'-dimethyl-9,9'-biacridinium
  • embusartan
  • NADH oxidase
  • NADH, NADPH Oxidoreductases
  • Acetylcholine