Mechanism of action of the multikinase inhibitor Foretinib

Cell Cycle. 2011 Dec 1;10(23):4138-48. doi: 10.4161/cc.10.23.18323. Epub 2011 Dec 1.

Abstract

Mitotic catastrophe (MC) is induced when stressed cells enter prematurely or inappropriately into mitosis and can be caused by ionizing radiation and anticancer drugs. Foretinib is a multikinase inhibitor whose mechanism of action is incompletely understood. We investigated here the effect of Foretinib on chronic myelogenous leukemia (CML) cell lines either sensitive (IM-S) or resistant (IM-R) to the tyrosine kinase inhibitor Imatinib. Foretinib decreased viability and clonogenic potential of IM-S and IM-R CML cells as well. Foretinib-treated cells exhibited increased size, spindle assembly checkpoint anomalies and enhanced ploidy that collectively evoked mitotic catastrophe (MC). Accordingly, Foretinib-stimulated CML cells displayed decreased expression of Cdk1, Cyclin B1 and Plk1. In addition, Foretinib triggered caspase-2 activation that precedes mitochondrial membrane permeabilization. Accordingly, z-VAD-fmk and a caspase-2 siRNA abolished Foretinib-mediated cell death but failed to affect MC, indicating that Foretinib-mediated apoptosis and MC are two independent events. Anisomycin, a JNK activator, impaired Foretinib-induced MC and inhibition or knockdown of JNK phenotyped its effect on MC. Moreover, we found that Foretinib acted as a potent inhibitor of JNK. Importantly, Foretinib exhibited no or very little effect on normal peripheral blood mononuclear cells, monocytes or melanocytes cells but efficiently inhibited the clonogenic potential of CD34+ cell from CML patients. Collectively, our data show that the multikinase inhibitor Foretinib induces MC in CML cells and other cell lines via JNK-dependent inhibition of Plk1 expression and triggered apoptosis by a caspase 2-mediated mechanism. This unusual mechanism of action may have important implications for the treatment of cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Chloromethyl Ketones / pharmacology
  • Anilides / pharmacology*
  • Anisomycin / pharmacology
  • Antigens, CD34 / metabolism
  • Antineoplastic Agents / pharmacology
  • Benzamides
  • CDC2 Protein Kinase / genetics
  • CDC2 Protein Kinase / metabolism
  • Caspase 2 / genetics
  • Caspase 2 / metabolism
  • Caspase Inhibitors
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cell Death*
  • Cell Size
  • Cell Survival
  • Cyclin B1 / genetics
  • Cyclin B1 / metabolism
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism
  • Enzyme Activation
  • Enzyme Assays
  • Humans
  • Imatinib Mesylate
  • K562 Cells / drug effects
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism
  • M Phase Cell Cycle Checkpoints
  • MAP Kinase Signaling System*
  • Melanocytes / drug effects
  • Melanocytes / metabolism
  • Mitosis / drug effects
  • Phenotype
  • Piperazines / pharmacology
  • Ploidies
  • Polo-Like Kinase 1
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Pyrimidines / pharmacology
  • Quinolines / pharmacology*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Transfection

Substances

  • Amino Acid Chloromethyl Ketones
  • Anilides
  • Antigens, CD34
  • Antineoplastic Agents
  • Benzamides
  • CCNB1 protein, human
  • Caspase Inhibitors
  • Cell Cycle Proteins
  • Cyclin B1
  • GSK 1363089
  • Piperazines
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Pyrimidines
  • Quinolines
  • RNA, Small Interfering
  • benzyloxycarbonylvalyl-alanyl-aspartyl fluoromethyl ketone
  • Anisomycin
  • Imatinib Mesylate
  • Protein Serine-Threonine Kinases
  • CDC2 Protein Kinase
  • CASP2 protein, human
  • Caspase 2
  • Cysteine Endopeptidases