CD95-mediated apoptosis is impaired at receptor level by cellular FLICE-inhibitory protein (long form) in wild-type p53 human ovarian carcinoma

Clin Cancer Res. 2004 Aug 1;10(15):5202-14. doi: 10.1158/1078-0432.CCR-03-0537.

Abstract

Purpose: Ovarian carcinoma is a highly lethal malignancy that often becomes resistant to chemotherapy. Alterations in apoptotic signals and p53 status contribute to drug resistance, and CD95-mediated apoptosis is also deficient in resistant cells. We analyzed the mechanism of resistance to CD95-mediated apoptosis in ovarian carcinoma cell lines differing in p53 status.

Experimental design: CD95-mediated apoptosis was induced by agonistic anti-CD95 antibody, and the apoptotic cascade was monitored with biochemical and functional assays.

Results: CD95-mediated apoptosis was blocked in human ovarian cancer cells. In cell lines with wild-type p53, treatment with the protein synthesis inhibitor cycloheximide (CHX) together with anti-CD95 overcame the resistance, suggesting the presence of a labile inhibiting protein. Indeed, the labile protein cellular FLICE-inhibitory protein long form (c-FLIP(L)) was found to block caspase-8 recruitment to the death-inducing signaling complex (DISC), and sensitization of cells by CHX was due to c-FLIP(L) down-modulation at the DISC level. Down-regulation of c-FLIP(L) with antisense oligonucleotides increased CD95-mediated apoptosis as in cells sensitized by CHX, demonstrating the direct involvement of c-FLIP(L) in apoptosis resistance. Removal of c-FLIP(L) block at DISC level allowed full activation of the mitochondrial pathway and, eventually, apoptosis in wild-type p53 cells, whereas in cells with mutated p53, c-FLIP(L) involvement in CD95-mediated apoptosis resistance appeared to be irrelevant. Immunohistochemical analysis of an ovarian tumor tissue array revealed c-FLIP(L) expression in samples with no p53 accumulation (P = 0.034), and a significant (P = 0.037) inverse relationship between c-FLIP(L) and p53 expression levels was also observed in 27 epithelial ovarian cancer specimens with known p53 status.

Conclusion: The inhibitory protein c-FLIP(L) is involved in resistance to CD95-mediated apoptosis in ovarian carcinoma cells with wild-type p53.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis*
  • Blotting, Western
  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • Caspase 8
  • Caspases / metabolism
  • Cell Death
  • Cell Line, Tumor
  • Cycloheximide / pharmacology
  • Cytochromes c / metabolism
  • DNA Fragmentation
  • Down-Regulation
  • Drug Resistance
  • Enzyme Activation
  • Female
  • Flow Cytometry
  • Humans
  • Immunohistochemistry
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins / chemistry*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lymphocytes / metabolism
  • Mitochondria / metabolism
  • Oligonucleotides, Antisense / chemistry
  • Oligonucleotides, Antisense / pharmacology
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / pathology*
  • Protein Synthesis Inhibitors / pharmacology
  • Subcellular Fractions
  • Time Factors
  • Transfection
  • Tumor Suppressor Protein p53 / biosynthesis
  • Tumor Suppressor Protein p53 / metabolism*
  • fas Receptor / biosynthesis*

Substances

  • CASP8 and FADD-Like Apoptosis Regulating Protein
  • CFLAR protein, human
  • Intracellular Signaling Peptides and Proteins
  • Oligonucleotides, Antisense
  • Protein Synthesis Inhibitors
  • Tumor Suppressor Protein p53
  • fas Receptor
  • Cytochromes c
  • Cycloheximide
  • CASP8 protein, human
  • Caspase 8
  • Caspases