Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels

Circulation. 2003 Oct 21;108(16):2000-6. doi: 10.1161/01.CIR.0000092948.04444.C7. Epub 2003 Sep 29.

Abstract

Background: Although abnormal L-arginine NO signaling contributes to endothelial dysfunction in the aging cardiovascular system, the biochemical mechanisms remain controversial. L-arginine, the NO synthase (NOS) precursor, is also a substrate for arginase. We tested the hypotheses that arginase reciprocally regulates NOS by modulating L-arginine bioavailability and that arginase is upregulated in aging vasculature, contributing to depressed endothelial function.

Methods and results: Inhibition of arginase with (S)-(2-boronoethyl)-L-cysteine, HCl (BEC) produced vasodilation in aortic rings from young (Y) adult rats (maximum effect, 46.4+/-9.4% at 10(-5) mol/L, P<0.01). Similar vasorelaxation was elicited with the additional arginase inhibitors N-hydroxy-nor-L-arginine (nor-NOHA) and difluoromethylornithine (DFMO). This effect required intact endothelium and was prevented by 1H-oxadiazole quinoxalin-1-one (P<0.05 and P<0.001, respectively), a soluble guanylyl cyclase inhibitor. DFMO-elicited vasodilation was greater in old (O) compared with Y rat aortic rings (60+/-6% versus 39+/-6%, P<0.05). In addition, BEC restored depressed L-arginine (10(-4) mol/L)-dependent vasorelaxant responses in O rings to those of Y. Arginase activity and expression were increased in O rings, whereas NOS activity and cyclic GMP levels were decreased. BEC and DFMO suppressed arginase activity and restored NOS activity and cyclic GMP levels in O vessels to those of Y.

Conclusions: These findings demonstrate that arginase modulates NOS activity, likely by regulating intracellular L-arginine availability. Arginase upregulation contributes to endothelial dysfunction of aging and may therefore be a therapeutic target.

Publication types

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

MeSH terms

  • Aging / metabolism*
  • Aging / pathology
  • Animals
  • Arginase / antagonists & inhibitors
  • Arginase / metabolism*
  • Arginine / pharmacology
  • Blood Vessels / enzymology
  • Blood Vessels / pathology
  • Blood Vessels / physiopathology*
  • Cyclic GMP / metabolism
  • Disease Models, Animal
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / pathology
  • Endothelium, Vascular / physiopathology*
  • Enzyme Inhibitors / pharmacology
  • Guanylate Cyclase
  • In Vitro Techniques
  • Nitric Oxide Synthase / metabolism*
  • Rats
  • Rats, Wistar
  • Receptors, Cytoplasmic and Nuclear / antagonists & inhibitors
  • Soluble Guanylyl Cyclase
  • Vasodilation / drug effects
  • Vasodilator Agents / pharmacology

Substances

  • Enzyme Inhibitors
  • Receptors, Cytoplasmic and Nuclear
  • Vasodilator Agents
  • Arginine
  • Nitric Oxide Synthase
  • Arginase
  • Guanylate Cyclase
  • Soluble Guanylyl Cyclase
  • Cyclic GMP