Nitric oxide suppresses apoptosis via interrupting caspase activation and mitochondrial dysfunction in cultured hepatocytes

J Biol Chem. 1999 Jun 11;274(24):17325-33. doi: 10.1074/jbc.274.24.17325.

Abstract

Nitric oxide (NO) is a potent inhibitor of apoptosis in many cell types, including hepatocytes. We and others have described NO-dependent decreases in caspase activity in cells undergoing apoptosis. However, previous work has not determined whether NO disrupts the proteolytic processing and thus the activation of pro-caspases. Here we report that NO suppresses proteolytic processing and activation of multiple pro-caspases in intact cells, including caspase-3 and caspase-8. We found that both exogenous NO as well as endogenously produced NO via adenoviral inducible NO synthase gene transfer protected hepatocytes from tumor necrosid factor (TNF) alpha plus actinomycin D (TNFalpha/ActD)-induced apoptosis. Affinity labeling with biotin-VAD-fmk of all active caspase species in TNFalpha-mediated apoptosis identified four newly labeled spots (activated caspases) present exclusively in TNFalpha/ActD-treated cells. Both NO and the caspase inhibitor, Ac-DEVD-CHO, prevented the appearance of the four newly labeled spots or active caspases. Immunoanalysis of affinity labeled caspases demonstrated that caspase-3 was the major effector caspase. Western blot analysis also identified the activation of caspase-8 in the TNFalpha/ActD-treated cells, and the activation was suppressed by NO. Furthermore, NO inhibited several other events associated with caspase activation in cells, including release of cytochrome c from mitochondria, decrease in mitochondrial transmembrane potential, and cleavage of poly(ADP-ribose) polymerase in TNFalpha/ActD-treated cells. These findings indicate the involvement of multiple caspases in TNFalpha-mediated apoptosis in hepatocytes and establish the capacity of NO to inhibit not only active caspases but also caspase activation.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Caspase 3
  • Caspase 8
  • Caspase 9
  • Caspases / metabolism*
  • Cells, Cultured
  • Cytochrome c Group / metabolism
  • Dactinomycin / pharmacology
  • Enzyme Activation / drug effects
  • Liver / cytology
  • Liver / drug effects*
  • Male
  • Membrane Potentials / drug effects
  • Mitochondria / metabolism*
  • Nitric Oxide / pharmacology*
  • Nitric Oxide Synthase / metabolism
  • Nitric Oxide Synthase Type II
  • Protein Processing, Post-Translational
  • Rats
  • Rats, Sprague-Dawley
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Cytochrome c Group
  • Tumor Necrosis Factor-alpha
  • Dactinomycin
  • Nitric Oxide
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type II
  • Nos2 protein, rat
  • Casp3 protein, rat
  • Casp8 protein, rat
  • Casp9 protein, rat
  • Caspase 3
  • Caspase 8
  • Caspase 9
  • Caspases