Mitochondrial matrix chaperone and c-myc inhibition causes enhanced lethality in glioblastoma

Oncotarget. 2017 Jun 6;8(23):37140-37153. doi: 10.18632/oncotarget.16202.

Abstract

Malignant gliomas display high levels of the transcription factor c-myc and organize a tumor specific chaperone network within mitochondria. Here, we show that c-myc along with mitochondrial chaperone inhibition displays massive tumor cell death. Inhibition of mitochondrial matrix chaperones and c-myc was established by utilizing genetic as well as pharmacological approaches. Bromodomain and extraterminal (BET) family protein inhibitors, JQ1 and OTX015, were used for c-myc inhibition. Gamitrinib was applied to interfere with mitochondrial matrix chaperones. A xenograft model was used to determine the in vivo efficacy. Combined inhibition of c-myc and mitochondrial matrix chaperones led to a synergistic reduction of cellular proliferation (CI values less than 1) in established glioblastoma, patient-derived xenograft and stem cell-like glioma cultures. The combinatorial treatment of BET inhibitors and Gamitrinib elicited massive apoptosis induction with dissipation of mitochondrial membrane potential and activation of caspases. Mechanistically, BET-inhibitors and Gamitrinib mediated a pronounced integrated stress response with a PERK-dependent up regulation of ATF4 and subsequent modulation of Bcl-2 family of proteins with down-regulation of Mcl-1 and its interacting partner, Usp9X, and an increase in pro-apoptotic Noxa. Blocking ATF4 by siRNA attenuated Gamitrinib/BET inhibitor mediated increase of Noxa. Knockdown of Noxa and Bak protected from the combinatorial treatment. Finally, the combination treatment of Gamitrinib and OTX015 led to a significantly stronger reduction of tumor growth as compared to single treatments in a xenograft model of human glioma without induction of toxicity. Thus, Gamitrinib in combination with BET-inhibitors should be considered for the development for clinical application.

Keywords: JQ1; OTX015; apoptosis; c-myc; gamitrinib.

MeSH terms

  • Acetanilides / pharmacology
  • Animals
  • Azepines / pharmacology
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Endoplasmic Reticulum Chaperone BiP
  • Glioblastoma / drug therapy
  • Glioblastoma / genetics
  • Glioblastoma / metabolism*
  • Guanidines / pharmacology
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Heterocyclic Compounds, 3-Ring / pharmacology
  • Humans
  • Lactams, Macrocyclic / pharmacology
  • Mice, Nude
  • Mitochondria / drug effects
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mitochondrial Proteins / antagonists & inhibitors
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Molecular Chaperones / antagonists & inhibitors
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism*
  • Proto-Oncogene Proteins c-myc / antagonists & inhibitors
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism*
  • RNA Interference
  • Triazoles / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • (+)-JQ1 compound
  • Acetanilides
  • Azepines
  • Endoplasmic Reticulum Chaperone BiP
  • Guanidines
  • Heat-Shock Proteins
  • Heterocyclic Compounds, 3-Ring
  • Lactams, Macrocyclic
  • Mitochondrial Proteins
  • Molecular Chaperones
  • OTX015
  • Proto-Oncogene Proteins c-myc
  • Triazoles
  • gamitrinib-G4