Chelation of intracellular iron with the antifungal agent ciclopirox olamine induces cell death in leukemia and myeloma cells

Blood. 2009 Oct 1;114(14):3064-73. doi: 10.1182/blood-2009-03-209965. Epub 2009 Jul 9.

Abstract

Off-patent drugs with previously unrecognized anticancer activity could be rapidly repurposed for this new indication. To identify such compounds, we conducted 2 independent cell-based chemical screens and identified the antimicrobial ciclopirox olamine (CPX) in both screens. CPX decreased cell growth and viability of malignant leukemia, myeloma, and solid tumor cell lines as well as primary AML patient samples at low-micromolar concentrations that appear pharmacologically achievable. Furthermore, oral CPX decreased tumor weight and volume in 3 mouse models of leukemia by up to 65% compared with control without evidence of weight loss or gross organ toxicity. In addition, oral CPX prevented the engraftment of primary AML cells in nonobese diabetic/severe combined immunodeficiency mouse models, thereby establishing its ability to target leukemia stem cells. Mechanistically, CPX bound intracellular iron, and this intracellular iron chelation was functionally important for its cytotoxicity. By electron paramagnetic resonance, CPX inhibited the iron-dependent enzyme ribonucleotide reductase at concentrations associated with cell death. Thus, in summary, CPX has previously unrecognized anticancer activity at concentrations that are pharmacologically achievable. Therefore, CPX could be rapidly repurposed for the treatment of malignancies, including leukemia and myeloma.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antifungal Agents / pharmacology*
  • Antimetabolites, Antineoplastic / pharmacology
  • Apoptosis / drug effects*
  • Cells, Cultured
  • Ciclopirox
  • Cytarabine / pharmacology
  • Drug Synergism
  • Electron Spin Resonance Spectroscopy
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Humans
  • Immunoblotting
  • Inhibitor of Apoptosis Proteins
  • Iron / metabolism*
  • Iron Chelating Agents / pharmacology*
  • Leukemia, Myeloid, Acute / drug therapy
  • Leukemia, Myeloid, Acute / metabolism
  • Leukemia, Myeloid, Acute / pathology*
  • Luciferases / metabolism
  • Lung / cytology
  • Lung / drug effects
  • Lung / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Microtubule-Associated Proteins / genetics
  • Multiple Myeloma / drug therapy
  • Multiple Myeloma / metabolism
  • Multiple Myeloma / pathology*
  • Promoter Regions, Genetic
  • Pyridones / pharmacology*
  • Ribonucleotide Reductases / antagonists & inhibitors
  • Ribonucleotide Reductases / metabolism
  • Survivin

Substances

  • Antifungal Agents
  • Antimetabolites, Antineoplastic
  • BIRC5 protein, human
  • Inhibitor of Apoptosis Proteins
  • Iron Chelating Agents
  • Microtubule-Associated Proteins
  • Pyridones
  • Survivin
  • Cytarabine
  • Ciclopirox
  • Iron
  • Luciferases
  • Ribonucleotide Reductases