Identification of Bisindolylmaleimide IX as a potential agent to treat drug-resistant BCR-ABL positive leukemia

Oncotarget. 2016 Oct 25;7(43):69945-69960. doi: 10.18632/oncotarget.11566.

Abstract

Chronic myeloid leukemia (CML) treatment with BCR-ABL inhibitors is often hampered by development of drug resistance. In a screen for novel chemotherapeutic drug candidates with genotoxic activity, we identified a bisindolylmaleimide derivative, IX, as a small molecule compound with therapeutic potential against CML including drug-resistant CML. We show that Bisindolylmaleimide IX inhibits DNA topoisomerase, generates DNA breaks, activates the Atm-p53 and Atm-Chk2 pathways, and induces cell cycle arrest and cell death. Interestingly, Bisindolylmaleimide IX is highly effective in targeting cells positive for BCR-ABL. BCR-ABL positive cells display enhanced DNA damage and increased cell cycle arrest in response to Bisindolylmaleimide IX due to decreased expression of topoisomerases. Cells positive for BCR-ABL or drug-resistant T315I BCR-ABL also display increased cytotoxicity since Bisindolylmaleimide IX inhibits B-Raf and the downstream oncogene addiction pathway. Mouse cancer model experiments showed that Bisindolylmaleimide IX, at doses that show little side effect, was effective in treating leukemia-like disorders induced by BCR-ABL or T315I BCR-ABL, and prolonged the lifespan of these model mice. Thus, Bisindolylmaleimide IX presents a novel drug candidate to treat drug-resistant CML via activating BCR-ABL-dependent genotoxic stress response and inhibiting the oncogene addiction pathway activated by BCR-ABL.

Keywords: BCR-ABL; Bisindolylmaleimide IX; chronic myeloid leukemia (CML).

MeSH terms

  • Animals
  • Cell Cycle Checkpoints / drug effects
  • DNA Damage
  • Drug Resistance, Neoplasm
  • Fusion Proteins, bcr-abl / physiology
  • HCT116 Cells
  • Humans
  • Indoles / pharmacology
  • Indoles / therapeutic use*
  • K562 Cells
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / drug therapy*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / pathology
  • Male
  • Maleimides / pharmacology
  • Maleimides / therapeutic use*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins B-raf / physiology
  • Topoisomerase Inhibitors / pharmacology

Substances

  • Indoles
  • Maleimides
  • Topoisomerase Inhibitors
  • bisindolylmaleimide IX
  • Fusion Proteins, bcr-abl
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf