Transforming growth factor beta-dependent sequential activation of Smad, Bim, and caspase-9 mediates physiological apoptosis in gastric epithelial cells

Mol Cell Biol. 2005 Nov;25(22):10017-28. doi: 10.1128/MCB.25.22.10017-10028.2005.

Abstract

Transforming growth factor beta (TGF-beta) has been implicated in the maintenance of homeostasis in various organs, including the gastric epithelium. In particular, TGF-beta-induced signaling was shown to be required for the differentiation-associated physiological apoptosis of gastric epithelial cells, but its mechanism has not been well understood. In this study, the molecular mechanism of TGF-beta-induced apoptosis was analyzed in a human gastric epithelial cell line, SNU16, as an in vitro model. Expression of Smad7 and Bcl-X(L), but not viral FLIP, was shown to prevent TGF-beta-induced apoptosis, indicating an exclusive requirement of the activation of Smad signaling pathway and mitochondrial dysfunction followed by activation of caspase-9. In addition, treatment with TGF-beta induced binding of Bim, a proapoptotic Bcl-2 homology domain 3 (BH3)-only protein, to Bcl-X(L), which is dependent on the activation of Smad, and reduction in the expression of Bim by RNA interference decreased the sensitivity to TGF-beta-induced apoptosis. Moreover, we found abnormalities in the gastric epithelium of both Bim and caspase-9 knockout mice; these abnormalities were associated with a defect of physiological apoptosis in gastric epithelial cells. These results indicate for the first time that TGF-beta is involved in the physiological loss of gastric epithelial cells by activating apoptosis mediated by Smad, Bim, and caspase-9.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Animals, Newborn
  • Apoptosis Regulatory Proteins / metabolism*
  • Apoptosis*
  • Bcl-2-Like Protein 11
  • Blotting, Western
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • Caspase 9
  • Caspases / metabolism*
  • Cell Differentiation
  • Cell Line
  • Cell Line, Tumor
  • Crosses, Genetic
  • Cycloheximide / pharmacology
  • Epithelium / metabolism*
  • Female
  • Gastric Mucosa / metabolism*
  • Humans
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Male
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / metabolism
  • Protein Binding
  • Protein Conformation
  • Proto-Oncogene Proteins / metabolism*
  • RNA Interference
  • Sensitivity and Specificity
  • Signal Transduction
  • Smad Proteins / metabolism*
  • Smad7 Protein / metabolism
  • Time Factors
  • Transforming Growth Factor beta / metabolism*
  • Transforming Growth Factor beta1
  • bcl-X Protein / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • CFLAR protein, human
  • Cflar protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • Smad Proteins
  • Smad7 Protein
  • TGFB1 protein, human
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • bcl-X Protein
  • Adenosine Triphosphate
  • Cycloheximide
  • CASP9 protein, human
  • Casp9 protein, mouse
  • Caspase 9
  • Caspases