Disruption of the inhibitor of apoptosis protein survivin sensitizes Bcr-abl-positive cells to STI571-induced apoptosis

Cancer Res. 2005 Sep 15;65(18):8224-32. doi: 10.1158/0008-5472.CAN-05-0303.

Abstract

The Bcr-abl oncogene induces hematopoietic cell transformation and protects cells from apoptosis; however, the mechanisms whereby Bcr-abl blocks apoptosis are poorly defined. We examined whether the inhibitor of apoptosis protein (IAP) family, in particular survivin, are regulated by Bcr-abl. Overexpression of Bcr-abl in Mo7e or BaF3 hematopoietic cells elevated survivin mRNA and protein concomitant with a 4-fold increase in survivin promoter activity. The region of the survivin promoter responding to Bcr-abl was narrowed down to a 116 bp fragment between nucleotides -1,194 and -1,078. The IAP family member IAP-like protein-2 was also up-regulated by Bcr-abl. Disruption of Bcr-abl in Bcr-abl-transduced BaF3 cells by small interfering RNA resulted in 3- to 4-fold reduction in survivin protein confirming the link between Bcr-abl and survivin. Survivin disruption in Bcr-abl-transduced Mo7e cells, or in K562 cells that endogenously express Bcr-abl, by transfection with dominant-negative or antisense survivin constructs promoted apoptosis induced by the Bcr-abl tyrosine kinase inhibitor STI571, which was accompanied by caspase-dependent cleavage of Bcr-abl, mitochondrial membrane potential disruption, and enhanced mitochondrial cytochrome c release. Although ectopic survivin protected K562 cells from apoptosis induced by STI571, it did not protect cells from apoptosis induced either by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) or the combination of TRAIL plus Hemin. Our results identify a new signal pathway downstream of Bcr-abl, in addition to the Bcl-2 family involved in the antiapoptotic effects of Bcr-abl, and suggest that anti-survivin therapy may have utility in patients with chronic myelogenous leukemia.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects*
  • Apoptosis / genetics
  • Apoptosis Regulatory Proteins / pharmacology
  • Benzamides
  • Caspase 9
  • Caspases / metabolism
  • Cell Line, Tumor
  • Cytochromes c / metabolism
  • Fusion Proteins, bcr-abl / biosynthesis
  • Fusion Proteins, bcr-abl / genetics
  • Fusion Proteins, bcr-abl / physiology*
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / drug effects
  • Hematopoietic Stem Cells / physiology
  • Humans
  • Imatinib Mesylate
  • Inhibitor of Apoptosis Proteins
  • K562 Cells
  • Leukemia, Megakaryoblastic, Acute / drug therapy
  • Leukemia, Megakaryoblastic, Acute / genetics
  • Leukemia, Megakaryoblastic, Acute / metabolism
  • Leukemia, Megakaryoblastic, Acute / pathology
  • Membrane Glycoproteins / pharmacology
  • Mice
  • Microtubule-Associated Proteins / antagonists & inhibitors*
  • Microtubule-Associated Proteins / biosynthesis
  • Microtubule-Associated Proteins / genetics
  • Neoplasm Proteins / antagonists & inhibitors*
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Oligonucleotides, Antisense / genetics
  • Piperazines / pharmacology*
  • Pyrimidines / pharmacology*
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Signal Transduction
  • Survivin
  • TNF-Related Apoptosis-Inducing Ligand
  • Transduction, Genetic
  • Tumor Necrosis Factor-alpha / pharmacology
  • Up-Regulation

Substances

  • Antineoplastic Agents
  • Apoptosis Regulatory Proteins
  • BIRC5 protein, human
  • Benzamides
  • Inhibitor of Apoptosis Proteins
  • Membrane Glycoproteins
  • Microtubule-Associated Proteins
  • Neoplasm Proteins
  • Oligonucleotides, Antisense
  • Piperazines
  • Pyrimidines
  • RNA, Messenger
  • Survivin
  • TNF-Related Apoptosis-Inducing Ligand
  • TNFSF10 protein, human
  • Tnfsf10 protein, mouse
  • Tumor Necrosis Factor-alpha
  • Imatinib Mesylate
  • Cytochromes c
  • Fusion Proteins, bcr-abl
  • CASP9 protein, human
  • Casp9 protein, mouse
  • Caspase 9
  • Caspases