Nitric oxide increases toxicity of hydrogen peroxide against rat liver endothelial cells and hepatocytes by inhibition of hydrogen peroxide degradation

Am J Physiol Cell Physiol. 2007 Apr;292(4):C1440-9. doi: 10.1152/ajpcell.00366.2006. Epub 2006 Dec 27.

Abstract

Nitric oxide (NO) and hydrogen peroxide (H(2)O(2)) show cooperativity in their cytotoxic action. The present study was performed to decipher the mechanisms underlying this phenomenon. In cultured liver endothelial cells and in cultured, glutathione-depleted hepatocytes, the combined exposure to NO (released by spermine NONOate, 1 mM) and H(2)O(2) (released by glucose oxidase) induced cell injury that was far higher than the injury elicited by NO or H(2)O(2) alone. In both cell types, the addition of the NO donor increased H(2)O(2) steady-state levels, although with different kinetics: in hepatocytes, the increase in H(2)O(2) levels was already evident at early time points while in liver endothelial cells it became evident after > or =2 h of incubation. NO exposure inhibited H(2)O(2) degradation, assessed after addition of 50 microM, 200 microM, or 4 mM authentic H(2)O(2), significantly in both cell types. However, again, early and delayed inhibition was observed. The late inhibition of H(2)O(2) degradation in endothelial cells was paralleled by a decrease in glutathione peroxidase activity. Glutathione peroxidase inactivation was prevented by hypoxia or by ascorbate, suggesting inactivation by reactive nitrogen oxide species (NO(x)). Early inhibition of H(2)O(2) degradation by NO, in contrast, could be mimicked by the catalase inhibitor azide. Together, these results suggest that the cooperative effect of NO and H(2)O(2) is due to inhibition of H(2)O(2) degradation by NO, namely to inhibition of catalase by NO itself (predominant in hepatocytes) and/or to inhibition of glutathione peroxidase by NO(x) (prevailing in endothelial cells).

MeSH terms

  • Animals
  • Ascorbic Acid / pharmacology
  • Catalase / antagonists & inhibitors
  • Catalase / metabolism
  • Cell Hypoxia
  • Cell Survival
  • Cells, Cultured
  • Endothelial Cells / drug effects
  • Endothelial Cells / physiology*
  • Enzyme Activation
  • Glutathione Peroxidase / antagonists & inhibitors
  • Hepatocytes / drug effects
  • Hepatocytes / physiology*
  • Hydrogen Peroxide / metabolism*
  • Hydrogen Peroxide / pharmacology
  • Liver / cytology
  • Male
  • Nitric Oxide / physiology*
  • Nitric Oxide Donors / pharmacology
  • Rats
  • Rats, Wistar
  • Reactive Nitrogen Species / metabolism
  • Spermine / analogs & derivatives
  • Spermine / pharmacology

Substances

  • Nitric Oxide Donors
  • Reactive Nitrogen Species
  • spermine nitric oxide complex
  • Spermine
  • Nitric Oxide
  • Hydrogen Peroxide
  • Catalase
  • Glutathione Peroxidase
  • Ascorbic Acid