A novel mechanism for imatinib mesylate-induced cell death of BCR-ABL-positive human leukemic cells: caspase-independent, necrosis-like programmed cell death mediated by serine protease activity

Blood. 2004 Mar 15;103(6):2299-307. doi: 10.1182/blood-2003-05-1605. Epub 2003 Nov 26.

Abstract

Caspase-independent programmed cell death can exhibit either an apoptosis-like or a necrosis-like morphology. The ABL kinase inhibitor, imatinib mesylate, has been reported to induce apoptosis of BCR-ABL-positive cells in a caspase-dependent fashion. We investigated whether caspases alone were the mediators of imatinib mesylate-induced cell death. In contrast to previous reports, we found that a broad caspase inhibitor, zVAD-fmk, failed to prevent the death of imatinib mesylate-treated BCR-ABL-positive human leukemic cells. Moreover, zVAD-fmk-preincubated, imatinib mesylate-treated cells exhibited a necrosis-like morphology characterized by cellular pyknosis, cytoplasmic vacuolization, and the absence of nuclear signs of apoptosis. These cells manifested a loss of the mitochondrial transmembrane potential, indicating the mitochondrial involvement in this caspase-independent necrosis. We excluded the participation of several mitochondrial factors possibly involved in caspase-independent cell death such as apoptosis-inducing factor, endonuclease G, and reactive oxygen species. However, we observed the mitochondrial release of the serine protease Omi/HtrA2 into the cytosol of the cells treated with imatinib mesylate or zVAD-fmk plus imatinib mesylate. Furthermore, serine protease inhibitors prevented the caspase-independent necrosis. Taken together, our results suggest that imatinib mesylate induces a caspase-independent, necrosis-like programmed cell death mediated by the serine protease activity of Omi/HtrA2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Chloromethyl Ketones / pharmacology
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects*
  • Apoptosis / physiology
  • Apoptosis Inducing Factor
  • Benzamides
  • Caspase 3
  • Caspase 9
  • Caspase Inhibitors
  • Caspases / metabolism
  • Cell Line, Tumor / cytology
  • Cell Line, Tumor / drug effects
  • Cell Line, Tumor / enzymology
  • Cell Nucleus / metabolism
  • Cysteine Proteinase Inhibitors / pharmacology
  • Flavoproteins / metabolism
  • Fusion Proteins, bcr-abl / metabolism
  • High-Temperature Requirement A Serine Peptidase 2
  • Humans
  • Imatinib Mesylate
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive*
  • Membrane Potentials / physiology
  • Membrane Proteins / metabolism
  • Mitochondria / physiology
  • Mitochondrial Proteins
  • Necrosis
  • Nucleosomes / metabolism
  • Piperazines / pharmacology*
  • Pyrimidines / pharmacology*
  • Reactive Oxygen Species / metabolism
  • Serine Endopeptidases / metabolism*

Substances

  • AIFM1 protein, human
  • Amino Acid Chloromethyl Ketones
  • Antineoplastic Agents
  • Apoptosis Inducing Factor
  • Benzamides
  • Caspase Inhibitors
  • Cysteine Proteinase Inhibitors
  • Flavoproteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Nucleosomes
  • Piperazines
  • Pyrimidines
  • Reactive Oxygen Species
  • benzyloxycarbonylvalyl-alanyl-aspartyl fluoromethyl ketone
  • trypsin-like serine protease
  • Imatinib Mesylate
  • Fusion Proteins, bcr-abl
  • Serine Endopeptidases
  • HTRA2 protein, human
  • High-Temperature Requirement A Serine Peptidase 2
  • CASP3 protein, human
  • CASP9 protein, human
  • Caspase 3
  • Caspase 9
  • Caspases