Antisense Bcl-xl down-regulation switches the response to topoisomerase I inhibition from senescence to apoptosis in colorectal cancer cells, enhancing global cytotoxicity

Clin Cancer Res. 2003 Jul;9(7):2856-65.

Abstract

Purpose: To identify determinants of the effect of antisense-mediated Bcl-xl down-regulation (Bcl-xl knockdown) on the response of colorectal cancer cells to SN38, the active metabolite of irinotecan, a topoisomerase I inhibitor licensed for colorectal cancer chemotherapy.

Experimental design: Using wild-type HCT116, p53 null, Bax null, or p21/WAF1 null isogenic derivatives, we measured expression of regulators of cellular response, and associated growth arrests or apoptosis, after SN38 treatment, with or without antisense-mediated Bcl-xl knockdown.

Results: A modified phosphorothioate antisense oligonucleotide (ISIS15999) reduced Bcl-xl protein expression by approximately 90%. SN38 induced p53, Bax, Bcl-xl, and p53-dependent p21/WAF1 protein accumulation. The Bax:Bcl-xl ratio changed little. In wild-type HCT116, but not in Bax null cells, Bcl-xl knockdown induced a shift in response from drug-induced senescence to apoptosis, and enhanced the global cytotoxicity of SN38. In p53 null or p21/WAF1 null cells marked apoptosis occurred after SN38 alone, and was additionally enhanced by Bcl-xl knockdown in p21/WAF1 null cells but not in p53 null cells.

Conclusions: Drug-induced senescence is associated with late relapse after therapy in transgenic models of cancer in vivo. We have shown that abolition of p21/WAF1-mediated drug-induced senescence or antisense-mediated Bcl-xl knockdown can both, independently, enhance the apoptotic response of colorectal cancer cells to SN38 in vitro. The growth arrest suppresses a p53-independent apoptotic pathway, whereas Bcl-xl induction suppresses a p53 and Bax-dependent apoptotic pathway. The combination of irinotecan and Bcl-xL antisense merits testing in models of colorectal cancer in vivo.

MeSH terms

  • Annexin A5 / pharmacology
  • Antineoplastic Agents, Phytogenic / pharmacology
  • Apoptosis*
  • Camptothecin / analogs & derivatives*
  • Camptothecin / pharmacology
  • Cell Cycle
  • Cell Division
  • Cell Line, Tumor
  • Cellular Senescence
  • Colorectal Neoplasms / pathology
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins / genetics
  • Dose-Response Relationship, Drug
  • Down-Regulation*
  • Enzyme Inhibitors / pharmacology
  • Fluorescent Dyes / pharmacology
  • Genes, p53 / genetics
  • Humans
  • Immunoblotting
  • Irinotecan
  • Oligonucleotides, Antisense / pharmacology*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins c-bcl-2 / genetics*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Time Factors
  • Topoisomerase I Inhibitors*
  • bcl-2-Associated X Protein
  • bcl-X Protein
  • beta-Galactosidase / metabolism

Substances

  • Annexin A5
  • Antineoplastic Agents, Phytogenic
  • BAX protein, human
  • BCL2L1 protein, human
  • CDKN1A protein, human
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • Enzyme Inhibitors
  • Fluorescent Dyes
  • Oligonucleotides, Antisense
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Topoisomerase I Inhibitors
  • bcl-2-Associated X Protein
  • bcl-X Protein
  • Irinotecan
  • beta-Galactosidase
  • Camptothecin