Augmented superoxide production by Nox2-containing NADPH oxidase causes cerebral artery dysfunction during hypercholesterolemia

Stroke. 2010 Apr;41(4):784-9. doi: 10.1161/STROKEAHA.109.575365. Epub 2010 Feb 18.

Abstract

Background and purpose: We tested the hypothesis that elevated superoxide production by Nox2-NADPH oxidase occurs in cerebral arteries during hypercholesterolemia and causes decreased nitric oxide function.

Methods: Wild-type (WT), apolipoprotein E-deficient (ApoE(-/-)) and Nox2(-/-)/ApoE(-/-) mice were fed a high-fat diet for 7 to 14 weeks. Basal superoxide production by cerebral arteries was measured using L-012 (100 micromol/L)-enhanced chemiluminescence. Nitric oxide function was assessed in isolated middle cerebral arteries through the constrictor response to N(omega)-nitro-L-arginine methyl ester (L-NAME; 100 micromol/L). Western blotting was used to measure protein expression of Nox2, p47phox, endothelial nitric oxide synthase, and superoxide dismutases (1-3).

Results: Morphology of cerebral arteries was similar in WT and ApoE(-/-) mice. In ApoE(-/-), but not Nox2(-/-)/ApoE(-/-) mice, superoxide production by cerebral arteries was approximately 50% greater than in WT mice (P<0.05). Moreover, the magnitude of L-NAME-induced contractions of isolated middle cerebral arteries from ApoE(-/-) mice was <50% of that in WT mice (P<0.05), whereas in Nox2(-/-)/ApoE(-/-) mice, the contractile response was comparable to WT responses. In the presence of the superoxide scavenger, tempol (1 mmol/L), L-NAME-induced contractions of middle cerebral arteries were similar between WT and ApoE(-/-) mice. Expression of p47phox was approximately 2-fold higher in ApoE(-/-) versus WT mice, whereas Nox2, endothelial nitric oxide synthase, and superoxide dismutase isoforms were unchanged.

Conclusions: Elevated superoxide production and reduced basal nitric oxide-mediated relaxation occur in cerebral arteries of hypercholesterolemic mice even in the absence of lesions. These changes appear to be exclusively due to increased activity of Nox2-NADPH oxidase, possibly through increased expression of its regulatory subunit p47phox.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / pharmacology
  • Aorta / anatomy & histology
  • Aorta / pathology
  • Apolipoproteins E / genetics
  • Apolipoproteins E / metabolism
  • Cerebral Arteries / anatomy & histology
  • Cerebral Arteries / drug effects
  • Cerebral Arteries / metabolism*
  • Cerebral Arteries / physiopathology*
  • Cholesterol / blood
  • Cyclic N-Oxides / pharmacology
  • Dietary Fats
  • Enzyme Inhibitors / pharmacology
  • Hypercholesterolemia* / metabolism
  • Hypercholesterolemia* / physiopathology
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Knockout
  • NADPH Oxidase 2
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism*
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide / metabolism
  • Spin Labels
  • Superoxides / metabolism*
  • Vasoconstriction / drug effects
  • Vasoconstriction / physiology

Substances

  • Antioxidants
  • Apolipoproteins E
  • Cyclic N-Oxides
  • Dietary Fats
  • Enzyme Inhibitors
  • Membrane Glycoproteins
  • Spin Labels
  • Superoxides
  • Nitric Oxide
  • Cholesterol
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases
  • tempol
  • NG-Nitroarginine Methyl Ester