Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-alpha expression and myocardial depression

Circulation. 2005 Apr 5;111(13):1637-44. doi: 10.1161/01.CIR.0000160366.50210.E9. Epub 2005 Mar 28.

Abstract

Background: Lipopolysaccharide (LPS) induces cardiomyocyte tumor necrosis factor-alpha (TNF-alpha) production, which is responsible for myocardial depression during sepsis. The aim of this study was to investigate the role of gp91phox-containing NADH oxidase signaling in cardiomyocyte TNF-alpha expression and myocardial dysfunction induced by LPS.

Methods and results: In cultured mouse neonatal cardiomyocytes, LPS increased NADH oxidase (gp91phox subunit) expression and superoxide generation. Deficiency of gp91phox or inhibition of NADH oxidase blocked TNF-alpha expression stimulated by LPS. TNF-alpha induction was also inhibited by tempol, N-acetylcysteine, or 1,3-dimethyl-2-thiourea. NADH oxidase activation by LPS increased ERK1/2 and p38 phosphorylation, and inhibition of ERK1/2 and p38 phosphorylation blocked the effect of NADH oxidase on TNF-alpha expression. Isolated mouse hearts were perfused with LPS (5 microg/mL) alone or in the presence of apocynin for 1 hour. Myocardial TNF-alpha production was decreased in gp91phox-deficient or apocynin-treated hearts compared with those of wild type (P<0.05). To investigate the role of gp91phox-containing NADH oxidase in endotoxemia, mice were treated with LPS (4 mg/kg IP) for 4 and 24 hours, and their heart function was measured with a Langendorff system. Deficiency of gp91phox significantly attenuated LPS-induced myocardial depression (P<0.05).

Conclusions: gp91phox-Containing NADH oxidase is pivotal in LPS-induced TNF-alpha expression and cardiac depression. Effects of NADH oxidase activation are mediated by ERK1/2 and p38 MAPK pathway. The present results suggest that gp91phox-containing NADH oxidase may represent a potential therapeutic target for myocardial dysfunction in sepsis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cardiomyopathies / enzymology*
  • Cardiomyopathies / etiology
  • Cells, Cultured
  • Enzyme Activation
  • Gene Expression Regulation*
  • Heart
  • In Vitro Techniques
  • Lipopolysaccharides / pharmacology*
  • Membrane Glycoproteins / physiology
  • Mice
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Multienzyme Complexes / physiology*
  • Myocytes, Cardiac
  • NADH, NADPH Oxidoreductases / physiology*
  • NADPH Oxidase 2
  • NADPH Oxidases / physiology
  • Tumor Necrosis Factor-alpha / genetics*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Multienzyme Complexes
  • Tumor Necrosis Factor-alpha
  • NADH oxidase
  • NADH, NADPH Oxidoreductases
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases
  • Mitogen-Activated Protein Kinase 3
  • p38 Mitogen-Activated Protein Kinases