Perturbation of energy metabolism by fatty-acid derivative AIC-47 and imatinib in BCR-ABL-harboring leukemic cells

Cancer Lett. 2016 Feb 1;371(1):1-11. doi: 10.1016/j.canlet.2015.11.020. Epub 2015 Nov 23.

Abstract

In Ph-positive leukemia, imatinib brought marked clinical improvement; however, further improvement is needed to prevent relapse. Cancer cells efficiently use limited energy sources, and drugs targeting cellular metabolism improve the efficacy of therapy. In this study, we characterized the effects of novel anti-cancer fatty-acid derivative AIC-47 and imatinib, focusing on cancer-specific energy metabolism in chronic myeloid leukemia cells. AIC-47 and imatinib in combination exhibited a significant synergic cytotoxicity. Imatinib inhibited only the phosphorylation of BCR-ABL; whereas AIC-47 suppressed the expression of the protein itself. Both AIC-47 and imatinib modulated the expression of pyruvate kinase M (PKM) isoforms from PKM2 to PKM1 through the down-regulation of polypyrimidine tract-binding protein 1 (PTBP1). PTBP1 functions as alternative splicing repressor of PKM1, resulting in expression of PKM2, which is an inactive form of pyruvate kinase for the last step of glycolysis. Although inactivation of BCR-ABL by imatinib strongly suppressed glycolysis, compensatory fatty-acid oxidation (FAO) activation supported glucose-independent cell survival by up-regulating CPT1C, the rate-limiting FAO enzyme. In contrast, AIC-47 inhibited the expression of CPT1C and directly fatty-acid metabolism. These findings were also observed in the CD34(+) fraction of Ph-positive acute lymphoblastic leukemia cells. These results suggest that AIC-47 in combination with imatinib strengthened the attack on cancer energy metabolism, in terms of both glycolysis and compensatory activation of FAO.

Keywords: BCR-ABL; CPT1C; Fatty-acid oxidation; Imatinib; Warburg effect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, CD34 / metabolism
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Dose-Response Relationship, Drug
  • Drug Synergism
  • Energy Metabolism / drug effects*
  • Fatty Acids / pharmacology*
  • Fusion Proteins, bcr-abl / genetics
  • Fusion Proteins, bcr-abl / metabolism
  • Glycolysis / drug effects
  • Heterocyclic Compounds, 1-Ring / pharmacology*
  • Heterogeneous-Nuclear Ribonucleoproteins / genetics
  • Heterogeneous-Nuclear Ribonucleoproteins / metabolism
  • Humans
  • Imatinib Mesylate / pharmacology*
  • K562 Cells
  • Ketones / pharmacology*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / genetics
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / metabolism
  • Oxidation-Reduction
  • Polypyrimidine Tract-Binding Protein / genetics
  • Polypyrimidine Tract-Binding Protein / metabolism
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / drug therapy*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism
  • Protein Kinase Inhibitors / pharmacology*
  • Pyruvate Kinase / genetics
  • Pyruvate Kinase / metabolism
  • RNA Interference
  • Transfection

Substances

  • 1-(azocan-1-yl)dec-3-en-1one
  • Antigens, CD34
  • BCR-ABL1 fusion protein, human
  • Fatty Acids
  • Heterocyclic Compounds, 1-Ring
  • Heterogeneous-Nuclear Ribonucleoproteins
  • Ketones
  • MIRN124 microRNA, human
  • MicroRNAs
  • PTBP1 protein, human
  • Protein Kinase Inhibitors
  • Polypyrimidine Tract-Binding Protein
  • Imatinib Mesylate
  • Pyruvate Kinase
  • Fusion Proteins, bcr-abl