Sorafenib induces apoptosis specifically in cells expressing BCR/ABL by inhibiting its kinase activity to activate the intrinsic mitochondrial pathway

Cancer Res. 2009 May 1;69(9):3927-36. doi: 10.1158/0008-5472.CAN-08-2978. Epub 2009 Apr 14.

Abstract

Although the BCR/ABL tyrosine kinase inhibitor imatinib is highly effective for treatment of chronic myelogenous leukemia and Philadelphia chromosome-positive (Ph+) acute lymphoblastic leukemia, relapse with emerging imatinib resistance mutations in the BCR/ABL kinase domain poses a significant problem. Here, we show that the multikinase inhibitor sorafenib inhibits proliferation and induces apoptosis at much lower concentrations in Ton.B210 cells when driven by inducibly expressed BCR/ABL than when driven by interleukin-3. The increased sensitivity to sorafenib was also observed in cells inducibly expressing BCR/ABL with the imatinib-resistant E255K or T315I mutation. Sorafenib-induced apoptosis in these cells and Ph+ leukemic cells was synergistically enhanced by rottlerin, bortezomib, or ABT-737 and inhibited by the pan-caspase inhibitor BOC-d-fmk or the overexpression of Bcl-XL. It was further revealed that sorafenib activates Bax and caspase-3 and reduces mitochondrial membrane potential specifically in BCR/ABL-driven cells. Sorafenib also inhibited BCR/ABL-induced tyrosine phosphorylation of its cellular substrates and its autophosphorylation in Ton.B210. It was finally shown that sorafenib inhibits the kinase activity of BCR/ABL as well as its E255K and T315I mutants in in vitro kinase assays. These results indicate that sorafenib induces apoptosis of BCR/ABL-expressing cells, at least partly, by inhibiting BCR/ABL to activate the mitochondria-mediated apoptotic pathway. Thus, sorafenib may provide an effective therapeutic measure to treat Ph+ leukemias, particularly those expressing the T315I mutant, which is totally resistant to imatinib and the second generation BCR/ABL inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetophenones / administration & dosage
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Apoptosis / drug effects*
  • Apoptosis / physiology
  • Benzamides
  • Benzenesulfonates / administration & dosage
  • Benzenesulfonates / pharmacology*
  • Benzopyrans / administration & dosage
  • Biphenyl Compounds / administration & dosage
  • Boronic Acids / administration & dosage
  • Bortezomib
  • Caspases / metabolism
  • Drug Resistance, Neoplasm
  • Drug Synergism
  • Enzyme Activation / drug effects
  • Fusion Proteins, bcr-abl / antagonists & inhibitors*
  • Fusion Proteins, bcr-abl / biosynthesis
  • Fusion Proteins, bcr-abl / genetics
  • Humans
  • Imatinib Mesylate
  • Interleukin-3 / pharmacology
  • K562 Cells
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Mitochondria / drug effects*
  • Mitochondria / physiology
  • Mutation
  • Niacinamide / analogs & derivatives
  • Nitrophenols / administration & dosage
  • Phenylurea Compounds
  • Piperazines / administration & dosage
  • Piperazines / pharmacology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / drug therapy*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Protein Kinase Inhibitors / administration & dosage
  • Protein Kinase Inhibitors / pharmacology
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Protein-Tyrosine Kinases / biosynthesis
  • Pyrazines / administration & dosage
  • Pyridines / administration & dosage
  • Pyridines / pharmacology*
  • Pyrimidines / pharmacology
  • Sorafenib
  • Sulfonamides / administration & dosage

Substances

  • ABT-737
  • Acetophenones
  • Benzamides
  • Benzenesulfonates
  • Benzopyrans
  • Biphenyl Compounds
  • Boronic Acids
  • Interleukin-3
  • Nitrophenols
  • Phenylurea Compounds
  • Piperazines
  • Protein Kinase Inhibitors
  • Pyrazines
  • Pyridines
  • Pyrimidines
  • Sulfonamides
  • Niacinamide
  • Bortezomib
  • Imatinib Mesylate
  • Sorafenib
  • rottlerin
  • Protein-Tyrosine Kinases
  • Fusion Proteins, bcr-abl
  • Caspases