Ribotoxic stress sensitizes glioblastoma cells to death receptor induced apoptosis: requirements for c-Jun NH2-terminal kinase and Bim

Mol Cancer Res. 2007 Aug;5(8):783-92. doi: 10.1158/1541-7786.MCR-06-0433.

Abstract

A prominent feature of glioblastoma is its resistance to death receptor-mediated apoptosis. In this study, we explored the possibility of modulating death receptor-induced cell death with the c-Jun-NH2-terminal kinase (JNK) activator anisomycin. Anisomycin activates JNK by inactivating the ribosome and inducing "ribotoxic stress." We found that anisomycin and death receptor ligand anti-Fas antibody CH-11 or tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induce apoptosis in multiple human glioblastoma cell lines. For example, in U87 cells, anisomycin reduced the IC50 of CH-11 by more than 20-fold (from 500 to 25 ng/mL). Cell viability in response to anisomycin, CH-11, and their combination was 79%, 91%, and 28% (P<0.001), respectively. Anisomycin and TRAIL were found to be similarly synergistic in glioblastoma cells maintained as tumor xenografts. The potentiation of death receptor-dependent cell death by anisomycin was specific because emetine, another ribosome inhibitor that does not induce ribotoxic stress or activate JNK, did not have a similar effect. Synergistic cell death was predominantly apoptotic involving both extrinsic and intrinsic pathways. Expression of Fas, FasL, FLIP, and Fas-associated death domain (FADD) was not changed following treatment with anisomycin+CH-11. JNK was activated 10- to 22-fold by anisomycin+CH-11 in U87 cells. Inhibiting JNK activation with pharmacologic inhibitors of JNKK and JNK or with dominant negative mitogen-activated protein kinase (MAPK) kinase kinase 2 (MEKK2) significantly prevented cell death induced by the combination of anisomycin+CH-11. We further found that anisomycin+CH-11 up-regulated the proapoptotic protein Bim by approximately 14-fold. Simultaneously inhibiting Bim expression and JNK activation additively desensitized U87 cells to anisomycin+CH-11. These findings show that anisomycin-induced ribotoxic stress sensitizes glioblastoma cells to death receptor-induced apoptosis via a specific mechanism requiring both JNK activation and Bim induction.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anisomycin / pharmacology*
  • Antibodies / pharmacology*
  • Apoptosis / drug effects*
  • Apoptosis Regulatory Proteins / antagonists & inhibitors
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism*
  • Bcl-2-Like Protein 11
  • Blotting, Western
  • Caspases / metabolism
  • Cell Cycle / drug effects
  • Cell Proliferation / drug effects
  • Cytochromes c / metabolism
  • Drug Synergism
  • Fas Ligand Protein / metabolism
  • Flow Cytometry
  • Glioblastoma / drug therapy
  • Glioblastoma / metabolism
  • Glioblastoma / pathology*
  • Humans
  • JNK Mitogen-Activated Protein Kinases / genetics
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Oxidative Stress / drug effects
  • Oxidative Stress / physiology
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • RNA, Small Interfering / pharmacology
  • Receptors, Death Domain / metabolism
  • Ribosomes / drug effects*
  • TNF-Related Apoptosis-Inducing Ligand / metabolism
  • Tumor Cells, Cultured
  • fas Receptor / metabolism

Substances

  • Antibodies
  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • Bcl-2-Like Protein 11
  • CH-11 anti-fas antibody, human
  • FAS protein, human
  • Fas Ligand Protein
  • Membrane Proteins
  • Proto-Oncogene Proteins
  • RNA, Small Interfering
  • Receptors, Death Domain
  • TNF-Related Apoptosis-Inducing Ligand
  • fas Receptor
  • Anisomycin
  • Cytochromes c
  • JNK Mitogen-Activated Protein Kinases
  • Caspases