Small molecules targeting histone demethylase genes (KDMs) inhibit growth of temozolomide-resistant glioblastoma cells

Oncotarget. 2017 May 23;8(21):34896-34910. doi: 10.18632/oncotarget.16820.

Abstract

In glioblastoma several histone demethylase genes (KDM) are overexpressed compared to normal brain tissue and the development of Temozolomide (TMZ) resistance is accompanied by the transient further increased expression of KDM5A and other KDMs following a mechanism that we defined as "epigenetic resilience". We hypothesized that targeting KDMs may kill the cells that survive the cytotoxic therapy.We determined the effect of JIB 04 and CPI-455, two KDM inhibitors, on glioblastoma cells and found that both molecules are more effective against TMZ-resistant rather than native cells.Because of its lower IC50, we focused on JIB 04 that targets KDM5A and other KDMs as well. We have shown that this molecule activates autophagic and apoptotic pathways, interferes with cell cycle progression, inhibits cell clonogenicity and dephosphorylates Akt thus inactivating a potent pro-survival pathway. We performed combination temozolomide/JIB 04 in vitro treatments showing that these two molecules, under certain conditions, have a strong synergic effect and we hypothesize that JIB 04 intercepts the cells that escape the G2 block exerted by TMZ. Finally we studied the permeability of JIB 04 across the blood-brain barrier and found that this molecule reaches bioactive concentration in the brain; furthermore a pilot in vivo experiment in an orthotopic GB xenograft model showed a trend toward longer survival in treated mice with an Hazard Ratio of 0.5.In conclusion we propose that the combination between cytotoxic drugs and molecules acting on the epigenetic landscape may offer the opportunity to develop new therapies for this invariably lethal disease.

Keywords: drug resistance; epigenetics; glioblastoma; histone demethylase; temozolomide.

MeSH terms

  • Aminopyridines / administration & dosage
  • Aminopyridines / pharmacology
  • Animals
  • Blood-Brain Barrier / drug effects
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Dacarbazine / administration & dosage
  • Dacarbazine / analogs & derivatives*
  • Dacarbazine / pharmacology
  • Drug Resistance, Neoplasm / drug effects*
  • Drug Synergism
  • Enzyme Inhibitors / administration & dosage*
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glioblastoma / drug therapy*
  • Glioblastoma / metabolism
  • Histone Demethylases / antagonists & inhibitors
  • Humans
  • Hydrazones / administration & dosage
  • Hydrazones / pharmacology
  • Mice
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • Retinoblastoma-Binding Protein 2 / antagonists & inhibitors
  • Retinoblastoma-Binding Protein 2 / genetics
  • Small Molecule Libraries / administration & dosage*
  • Small Molecule Libraries / pharmacology
  • Temozolomide
  • Xenograft Model Antitumor Assays

Substances

  • Aminopyridines
  • Enzyme Inhibitors
  • Hydrazones
  • JIB-04
  • Small Molecule Libraries
  • Dacarbazine
  • Histone Demethylases
  • KDM5A protein, human
  • Retinoblastoma-Binding Protein 2
  • Proto-Oncogene Proteins c-akt
  • Temozolomide