Bid-dependent generation of oxygen radicals promotes death receptor activation-induced apoptosis in murine hepatocytes

Hepatology. 2004 Aug;40(2):403-13. doi: 10.1002/hep.20310.

Abstract

Activation of tumor necrosis factor receptor 1 or Fas leads to the generation of reactive oxygen species, which are important to the cytotoxic effects of tumor necrosis factor alpha (TNF-alpha) or Fas ligand. However, how these radicals are generated following receptor ligation is not clear. Using primary hepatocytes, we found that TNF-alpha or anti-Fas antibody-induced burst of oxygen radicals was mainly derived from the mitochondria. We discovered that Bid--a pro-death Bcl-2 family protein activated by ligated death receptors--was the main intracellular molecule signaling the generation of the radicals by targeting to the mitochondria and that the majority of oxygen radical production was dependent on Bid. Reactive oxygen species contributed to cell death and caspase activation by promoting FLICE-inhibitory protein degradation and mitochondrial release of cytochrome c. For the latter part, the oxygen radicals did not affect Bak oligomerization but instead promoted mitochondrial cristae reorganization and membrane lipid peroxidation. Antioxidants could reverse these changes and therefore protect against TNF-alpha or anti-Fas-induced apoptosis. In conclusion, our studies established the signaling pathway from death receptor engagement to oxygen radical generation and determined the mechanism by which reactive oxygen species contributed to hepatocyte apoptosis following death receptor activation.

Publication types

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

MeSH terms

  • Animals
  • Antioxidants / pharmacology
  • Apoptosis / physiology*
  • BH3 Interacting Domain Death Agonist Protein
  • Carrier Proteins / physiology*
  • Caspase 3
  • Caspases / metabolism
  • Cytochromes c / antagonists & inhibitors
  • Cytochromes c / metabolism
  • Enzyme Activation / drug effects
  • Hepatocytes / drug effects
  • Hepatocytes / physiology*
  • Lipid Peroxidation / drug effects
  • Membrane Lipids / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria, Liver / physiology
  • Reactive Oxygen Species / metabolism*
  • Receptors, Tumor Necrosis Factor / metabolism*
  • Tumor Necrosis Factor-alpha / pharmacology
  • fas Receptor / metabolism

Substances

  • Antioxidants
  • BH3 Interacting Domain Death Agonist Protein
  • Bid protein, mouse
  • Carrier Proteins
  • Membrane Lipids
  • Reactive Oxygen Species
  • Receptors, Tumor Necrosis Factor
  • Tumor Necrosis Factor-alpha
  • fas Receptor
  • Cytochromes c
  • Casp3 protein, mouse
  • Caspase 3
  • Caspases