Molecular mechanisms of TNF-alpha-induced ceramide formation in human glioma cells: P53-mediated oxidant stress-dependent and -independent pathways

Cell Death Differ. 2004 Sep;11(9):997-1008. doi: 10.1038/sj.cdd.4401438.

Abstract

The present study was designed to examine the roles of p53, reactive oxygen species (ROS), and ceramide, and to determine their mutual relationships during tumor necrosis factor (TNF)-alpha-induced apoptosis of human glioma cells. In cells possessing wild-type p53, TNF-alpha stimulated ceramide formation via the activation of both neutral and acid sphingomyelinases (SMases), accompanied by superoxide anion (O2-*) production, and induced mitochondrial depolarization and cytochrome c release, whereas p53-deficient cells were partially resistant to TNF-alpha and lacked O2-* generation and neutral SMase activation. Restoration of functional p53 sensitized glioma cells expressing mutant p53 to TNF-alpha by accumulation of O2-*. z-IETD-fmk (benzyloxycarbonyl-Ile-Glu-Thr-Asp fluoromethyl ketone), but not z-DEVD-fmk (benzyloxycarbonyl-Asp-Glu-Val-Asp fluoromethyl ketone), blocked TNF-alpha-induced ceramide formation through both SMases as well as O2-* generation. Caspase-8 was processed by TNF-alpha regardless of p53 status of cells or the presence of antioxidants. Two separate signaling cascades, p53-mediated ROS-dependent and -independent pathways, both of which are initiated by caspase-8 activation, thus contribute to ceramide formation in TNF-alpha-induced apoptosis of human glioma cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • Blotting, Western
  • Brain Neoplasms / metabolism
  • Caspase 8
  • Caspases / metabolism
  • Cathepsin B / metabolism
  • Cathepsin B / pharmacology
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Ceramides / metabolism*
  • Chromatography, High Pressure Liquid
  • Cycloheximide / pharmacology
  • Cysteine Proteinase Inhibitors / pharmacology
  • Cytochromes c / metabolism
  • Cytosol / metabolism
  • Electrophoresis, Polyacrylamide Gel
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Glioma / metabolism*
  • Glutathione / metabolism
  • Humans
  • Macrolides / pharmacology
  • Microscopy, Fluorescence
  • Mitochondria / metabolism
  • Mitosis
  • Oligopeptides / pharmacology
  • Oncogene Proteins, Viral / metabolism
  • Oxidation-Reduction
  • Oxidative Stress
  • Oxygen / metabolism
  • Protein Synthesis Inhibitors / pharmacology
  • RNA, Small Interfering / metabolism
  • Reactive Oxygen Species
  • Recombinant Proteins / chemistry
  • Repressor Proteins / metabolism
  • Retroviridae
  • Signal Transduction
  • Temperature
  • Time Factors
  • Transfection
  • Tumor Necrosis Factor-alpha / metabolism*
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • Ceramides
  • Cysteine Proteinase Inhibitors
  • E6 protein, Human papillomavirus type 16
  • Enzyme Inhibitors
  • Macrolides
  • Oligopeptides
  • Oncogene Proteins, Viral
  • Protein Synthesis Inhibitors
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Recombinant Proteins
  • Repressor Proteins
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor Protein p53
  • benzoylcarbonyl-aspartyl-glutamyl-valyl-aspartyl-fluoromethyl ketone
  • benzyloxycarbonyl-isoleucyl-glutamyl-threonyl-aspartic acid fluoromethyl ketone
  • bafilomycin A1
  • Cytochromes c
  • Cycloheximide
  • CASP8 protein, human
  • Caspase 8
  • Caspases
  • Cathepsin B
  • Glutathione
  • Oxygen