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Differential contribution of Nox1, Nox2 and Nox4 to kidney vascular oxidative stress and endothelial dysfunction in obesity

Redox Biol. 2020 Jan:28:101330. doi: 10.1016/j.redox.2019.101330. Epub 2019 Sep 20.

Abstract

Oxidative stress-associated endothelial dysfunction is a key pathogenic factor underlying the microvascular complications of metabolic disease. NADPH oxidase (Nox) is a major source of oxidative stress in diabetic nephropathy and chronic kidney disease, despite Nox4 and Nox2 have been identified as relevant sources of vasodilator endothelial H2O2.The present study was sought to investigate the role of Nox enzymes in renal vascular oxidative stress and endothelial dysfunction in a rat model of genetic obesity. Endothelial function was assessed in intrarenal arteries of obese Zucker rats (OZR) and their counterparts lean Zucker rats (LZR) mounted in microvascular myographs, and superoxide (O2.-) and H2O2 production were measured. Impaired endothelium-dependent relaxations to acetylcholine (ACh) were associated to augmented O2.- generation, but neither ROS scavengers nor the Nox inhibitor apocynin significantly improved these relaxant responses in renal arteries of OZR. Whereas NO contribution to endothelial relaxations was blunted, catalase-sensitive non-NO non-prostanoid relaxations were enhanced in obese rats. Interestingly, NADPH-dependent O2.- production was augmented while NADPH-dependent H2O2 generation was reduced, and cytosolic and mitochondrial SOD were up-regulated in kidney of obese rats. Nox4 was down-regulated in renal arteries and Nox4-dependent H2O2 generation and endothelial relaxation were reduced in OZR. Up-regulation of both Nox2 and Nox1 was associated with augmented O2.- production but reduced H2O2 generation and blunted endothelial Nox2-derived H2O2-mediated in obese rats. Moreover, increased Nox1-derived O2.- contributed to renal endothelial dysfunction in OZR. In summary, the current data support a main role for Nox1-derived O2.- in kidney vascular oxidative stress and renal endothelial dysfunction in obesity, while reduced endothelial Nox4 expression associated to decreased H2O2 generation and H2O2-mediated vasodilatation might hinder Nox4 protective renal effects thus contributing to kidney injury. This suggests that effective therapies to counteract oxidative stress and prevent microvascular complications must identify the specific Nox subunits involved in metabolic disease.

Keywords: Endothelial dysfunction; Nox1; Nox2; Nox4; Obesity; Oxidative stress; Renal arteries.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Disease Susceptibility
  • Endothelium, Vascular / metabolism*
  • Hydrogen Peroxide / metabolism
  • Immunohistochemistry
  • Kidney / metabolism
  • Kidney / pathology
  • Male
  • Metabolomics
  • Models, Biological
  • NADPH Oxidase 1 / genetics*
  • NADPH Oxidase 1 / metabolism
  • NADPH Oxidase 2 / genetics*
  • NADPH Oxidase 2 / metabolism
  • NADPH Oxidase 4 / genetics*
  • NADPH Oxidase 4 / metabolism
  • Obesity / etiology*
  • Obesity / metabolism*
  • Obesity / pathology
  • Oxidative Stress*
  • Rats
  • Reactive Oxygen Species / metabolism
  • Renal Artery / metabolism
  • Renal Artery / physiopathology
  • Superoxides / metabolism

Substances

  • Antioxidants
  • Reactive Oxygen Species
  • Superoxides
  • Hydrogen Peroxide
  • NADPH Oxidase 1
  • NADPH Oxidase 2
  • NADPH Oxidase 4