TNF-alpha/cycloheximide-induced apoptosis in intestinal epithelial cells requires Rac1-regulated reactive oxygen species

Am J Physiol Gastrointest Liver Physiol. 2008 Apr;294(4):G928-37. doi: 10.1152/ajpgi.00219.2007. Epub 2008 Jan 24.

Abstract

Previously we have shown that both Rac1 and c-Jun NH(2)-terminal kinase (JNK1/2) are key proapoptotic molecules in tumor necrosis factor (TNF)-alpha/cycloheximide (CHX)-induced apoptosis in intestinal epithelial cells, whereas the role of reactive oxygen species (ROS) in apoptosis is unclear. The present studies tested the hypothesis that Rac1-mediated ROS production is involved in TNF-alpha-induced apoptosis. In this study, we showed that TNF-alpha/CHX-induced ROS production and hydrogen peroxide (H(2)O(2))-induced oxidative stress increased apoptosis. Inhibition of Rac1 by a specific inhibitor NSC23766 prevented TNF-alpha-induced ROS production. The antioxidant, N-acetylcysteine (NAC), or rotenone (Rot), the mitochondrial electron transport chain inhibitor, attenuated mitochondrial ROS production and apoptosis. Rot also prevented JNK1/2 activation during apoptosis. Inhibition of Rac1 by expression of dominant negative Rac1 decreased TNF-alpha-induced mitochondrial ROS production. Moreover, TNF-alpha-induced cytosolic ROS production was inhibited by Rac1 inhibition, diphenyleneiodonium (DPI, an inhibitor of NADPH oxidase), and NAC. In addition, DPI inhibited TNF-alpha-induced apoptosis as judged by morphological changes, DNA fragmentation, and JNK1/2 activation. Mitochondrial membrane potential change is Rac1 or cytosolic ROS dependent. Lastly, all ROS inhibitors inhibited caspase-3 activity. Thus these results indicate that TNF-alpha-induced apoptosis requires Rac1-dependent ROS production in intestinal epithelial cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / pharmacology
  • Aminoquinolines / pharmacology
  • Animals
  • Antioxidants / pharmacology
  • Apoptosis / drug effects*
  • Caspase 3 / metabolism
  • Cell Line
  • Cycloheximide / pharmacology*
  • Cytosol / metabolism
  • Dose-Response Relationship, Drug
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Epithelial Cells / drug effects*
  • Epithelial Cells / enzymology
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Hydrogen Peroxide / pharmacology
  • Intestinal Mucosa / drug effects*
  • Intestinal Mucosa / enzymology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Membrane Potential, Mitochondrial / drug effects
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitogen-Activated Protein Kinase 8 / metabolism
  • Mitogen-Activated Protein Kinase 9 / metabolism
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / metabolism
  • Onium Compounds / pharmacology
  • Oxidants / pharmacology
  • Oxidative Stress / drug effects*
  • Pyrimidines / pharmacology
  • Rats
  • Reactive Oxygen Species / metabolism*
  • Rotenone / pharmacology
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / metabolism*
  • Uncoupling Agents / pharmacology
  • rac1 GTP-Binding Protein / antagonists & inhibitors
  • rac1 GTP-Binding Protein / genetics
  • rac1 GTP-Binding Protein / metabolism*

Substances

  • Aminoquinolines
  • Antioxidants
  • Enzyme Inhibitors
  • NSC 23766
  • Onium Compounds
  • Oxidants
  • Pyrimidines
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • Uncoupling Agents
  • Rotenone
  • diphenyleneiodonium
  • Cycloheximide
  • Hydrogen Peroxide
  • NADPH Oxidases
  • Mitogen-Activated Protein Kinase 9
  • Mitogen-Activated Protein Kinase 8
  • Caspase 3
  • Rac1 protein, rat
  • rac1 GTP-Binding Protein
  • Acetylcysteine