H2 O2 -induced microvessel barrier dysfunction: the interplay between reactive oxygen species, nitric oxide, and peroxynitrite

Physiol Rep. 2019 Aug;7(16):10.14814/phy2.14206. doi: 10.14814/phy2.14206.

Abstract

Elevated H2 O2 is implicated in many cardiovascular diseases. We previously demonstrated that H2 O2 -induced endothelial nitric oxide synthase (eNOS) activation and excessive NO production contribute to vascular cell injury and increases in microvessel permeability. However, the mechanisms of excessive NO-mediated vascular injury and hyperpermeability remain unknown. This study aims to examine the functional role of NO-derived peroxynitrite (ONOO- ) in H2 O2 -induced vascular barrier dysfunction by elucidating the interrelationships between H2 O2 -induced NO, superoxide, ONOO- , and changes in endothelial [Ca2+ ]i and microvessel permeability. Experiments were conducted on intact rat mesenteric venules. Microvessel permeability was determined by measuring hydraulic conductivity (Lp). Endothelial [Ca2+ ]i , NO, and O2- were assessed with fluorescence imaging. Perfusion of vessels with H2 O2 (10 µmol/L) induced marked productions of NO and O2- , resulting in extensive protein tyrosine nitration, a biomarker of ONOO- . The formation of ONOO- was abolished by inhibition of NOS with NG -Methyl-L-arginine. Blocking NO production or scavenging ONOO- by uric acid prevented H2 O2 -induced increases in endothelial [Ca2+ ]i and Lp. Additionally, the application of exogenous ONOO- to microvessels induced delayed and progressive increases in endothelial [Ca2+ ]i and microvessel Lp, a pattern similar to that observed in H2 O2 -perfused vessels. Importantly, ONOO- caused further activation of eNOS with amplified NO production. We conclude that the augmentation of NO-derived ONOO- is essential for H2 O2 -induced endothelial Ca2+ overload and progressively increased microvessel permeability, which is achieved by self-promoted amplifications of NO-dependent signaling cascades. This novel mechanism provides new insight into the reactive oxygen and/or reactive nitrogen species-mediated vascular dysfunction in cardiovascular diseases.

Keywords: Endothelial [Ca2+]i; H2O2; microvessel permeability; nitric oxide; peroxynitrite.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Capillary Permeability / drug effects*
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism
  • Female
  • Hydrogen Peroxide / metabolism
  • Hydrogen Peroxide / toxicity*
  • Microvessels / drug effects
  • Microvessels / metabolism
  • Nitric Oxide / metabolism*
  • Nitric Oxide / toxicity
  • Peroxynitrous Acid / metabolism*
  • Peroxynitrous Acid / toxicity
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Reactive Oxygen Species / toxicity*

Substances

  • Reactive Oxygen Species
  • Peroxynitrous Acid
  • Nitric Oxide
  • Hydrogen Peroxide