Inhibition of IGF-1R-dependent PI3K activation sensitizes colon cancer cells specifically to DR5-mediated apoptosis but not to rhTRAIL

Cell Oncol (Dordr). 2011 Jun;34(3):245-59. doi: 10.1007/s13402-011-0033-9. Epub 2011 Apr 30.

Abstract

Background: Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) initiates apoptosis in tumor cells upon binding to its cognate agonistic receptors, death receptors 4 and 5 (DR4 and DR5). The activity of the insulin-like growth factor 1 (IGF-1) survival pathway is often increased in cancer, influencing both cell proliferation and apoptosis. We hypothesized that inhibiting the IGF-1 receptor (IGF-1R) using NVP-AEW541, a small molecular weight tyrosine kinase inhibitor of the IGF-1R, could increase death receptor (DR)-mediated apoptosis in colon cancer cells.

Methods: The analyses were performed by caspase assay, flow cytometry, Western blotting, immunoprecipitation and fluorescent microscopy.

Results: Preincubation with NVP-AEW541 surprisingly decreased apoptosis induced by recombinant human TRAIL (rhTRAIL) or an agonistic DR4 antibody while sensitivity to an agonistic DR5 antibody was increased. NVP-AEW541 could inhibit IGF-1-induced activation of the phosphatidylinositol 3-kinase (PI3K) pathway. The effects of the PI3K inhibitor LY294002 on TRAIL-induced apoptosis were similar to those of NVP-AEW541, further supporting a role for IGF-1R-mediated activation of PI3K. We show that PI3K inhibition enhances DR5-mediated caspase 8 processing but also lowers DR4 membrane expression and DR4-mediated caspase 8 processing. Inhibition of PI3K reduced rhTRAIL sensitivity independently of the cell line preference for either DR4- or DR5-mediated apoptosis signaling.

Conclusions: Our study indicates that individual effects on DR4 and DR5 apoptosis signaling should be taken into consideration when combining DR-ligands with PI3K inhibition.

MeSH terms

  • Antibodies, Neoplasm / immunology
  • Apoptosis / drug effects*
  • CASP8 and FADD-Like Apoptosis Regulating Protein / metabolism
  • Caspase 8 / metabolism
  • Cell Line, Tumor
  • Colonic Neoplasms / enzymology
  • Colonic Neoplasms / pathology*
  • Death Domain Receptor Signaling Adaptor Proteins / metabolism
  • Enzyme Activation / drug effects
  • Humans
  • Models, Biological
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphoinositide-3 Kinase Inhibitors
  • Pyrimidines / pharmacology
  • Pyrroles / pharmacology
  • Receptor, IGF Type 1 / antagonists & inhibitors*
  • Receptor, IGF Type 1 / metabolism
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / immunology
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • Recombinant Proteins / pharmacology*
  • Signal Transduction / drug effects
  • TNF-Related Apoptosis-Inducing Ligand / pharmacology*

Substances

  • Antibodies, Neoplasm
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • CFLAR protein, human
  • Death Domain Receptor Signaling Adaptor Proteins
  • NVP-AEW541
  • Phosphoinositide-3 Kinase Inhibitors
  • Pyrimidines
  • Pyrroles
  • Receptors, TNF-Related Apoptosis-Inducing Ligand
  • Recombinant Proteins
  • TNF-Related Apoptosis-Inducing Ligand
  • Receptor, IGF Type 1
  • Caspase 8