Inhibition of nuclear factor kappaB and phosphatidylinositol 3-kinase/Akt is essential for massive hepatocyte apoptosis induced by tumor necrosis factor alpha in mice

Liver Int. 2003 Oct;23(5):386-96. doi: 10.1034/j.1478-3231.2003.00867.x.

Abstract

Background/aims: Tumor necrosis factor (TNF)-alpha itself does not induce liver injury in normal mice or hepatocytes. Rather, this event, especially in vitro, is explained by the fact that the TNF-alpha/TNF receptor system not only triggers downstream signals leading to apoptosis but also induces an antiapoptotic pathway through the activation of nuclear factor (NF)-kappaB. The aim of this study was to determine whether inhibition of antiapoptotic pathways influences the susceptibility of mice to TNF-alpha. Here, we focused on the roles of NF-kappaB and phosphatidylinositol 3-kinase (PI3K)-regulated serine/threonine kinase Akt.

Methods: TNF-alpha was administered to BALB/c mice after treatment with an adenovirus expressing a mutant form IkappaBalpha (Ad5IkappaB), the PI3K inhibitor wortmannin, or both. Liver injury was assessed biochemically and histologically. The expression of Bcl-2 family members and caspase activity were examined.

Results: In the mice livers, treatment with Ad5IkappaB or the wortmannin suppressed the activation of NF-kappaB or Akt, respectively. Suppression of either NF-kappaB or Akt showed a slight increase in transaminase levels and focal liver cell death after TNF-alpha administration. However, in mice treated with both Ad5IkappaB and wortmannin, TNF-alpha administration resulted in massive hepatocyte apoptosis and hemorrhagic liver destruction in mice. The combination of Ad5IkappaB, wortmannin, and TNF-alpha markedly increased the activation of caspase-3 and -9, and activated caspase-8 to a lesser degree, suggesting that TNF-alpha-induced hepatocyte apoptosis is dependent on type II cell death signaling pathway, probably through the mitochondria. Inhibition of the NF-kappaB and PI3K/Akt pathways had no effect on expression of Bcl-2 families.

Conclusion: The inducible activation of NF-kappaB and constitutive activation of Akt regulate hepatocyte survival against TNF-alpha, which occurs independent of Bcl-2 families.

MeSH terms

  • Androstadienes / pharmacology
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Apoptosis / physiology*
  • BH3 Interacting Domain Death Agonist Protein
  • Carrier Proteins / genetics
  • Caspase Inhibitors
  • Caspases / metabolism
  • Enzyme Inhibitors / pharmacology
  • Hepatocytes / cytology*
  • Hepatocytes / enzymology
  • I-kappa B Proteins / genetics
  • I-kappa B Proteins / pharmacology
  • In Vitro Techniques
  • Liver Failure / chemically induced
  • Liver Failure / drug therapy*
  • Liver Failure / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Minor Histocompatibility Antigens
  • Myeloid Cell Leukemia Sequence 1 Protein
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / antagonists & inhibitors*
  • NF-kappa B / metabolism
  • Neoplasm Proteins / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors*
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Specific Pathogen-Free Organisms
  • Tumor Necrosis Factor-alpha / pharmacology
  • Wortmannin
  • bcl-2-Associated X Protein
  • bcl-Associated Death Protein
  • bcl-X Protein

Substances

  • Androstadienes
  • Antineoplastic Agents
  • BCL2-related protein A1
  • BH3 Interacting Domain Death Agonist Protein
  • Bad protein, mouse
  • Bcl2l1 protein, mouse
  • Bid protein, mouse
  • Carrier Proteins
  • Caspase Inhibitors
  • Enzyme Inhibitors
  • I-kappa B Proteins
  • Minor Histocompatibility Antigens
  • Myeloid Cell Leukemia Sequence 1 Protein
  • NF-kappa B
  • Neoplasm Proteins
  • Nfkbia protein, mouse
  • Phosphoinositide-3 Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Tumor Necrosis Factor-alpha
  • bcl-2-Associated X Protein
  • bcl-Associated Death Protein
  • bcl-X Protein
  • NF-KappaB Inhibitor alpha
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Caspases
  • Wortmannin