The HDAC inhibitor AR42 interacts with pazopanib to kill trametinib/dabrafenib-resistant melanoma cells in vitro and in vivo

Oncotarget. 2017 Mar 7;8(10):16367-16386. doi: 10.18632/oncotarget.14829.

Abstract

Studies focused on the killing of activated B-RAF melanoma cells by the histone deacetylase (HDAC) inhibitor AR42. Compared to other tumor cell lines, PDX melanoma isolates were significantly more sensitive to AR42-induced killing. AR42 and the multi-kinase inhibitor pazopanib interacted to activate: an eIF2α-Beclin1 pathway causing autophagosome formation; an eIF2α-DR4/DR5/CD95 pathway; and an eIF2α-dependent reduction in the expression of c-FLIP-s, MCL-1 and BCL-XL. AR42 did not alter basal chaperone activity but increased the ability of pazopanib to inhibit HSP90, HSP70 and GRP78. AR42 and pazopanib caused HSP90/HSP70 dissociation from RAF-1 and B-RAF that resulted in reduced 'RAF' expression. The drug combination activated a DNA-damage-ATM-AMPK pathway that was associated with: NFκB activation; reduced mTOR S2448 and ULK-1 S757 phosphorylation; and increased ULK-1 S317 and ATG13 S318 phosphorylation. Knock down of PERK, eIF2α, Beclin1, ATG5 or AMPKα, or expression of IκB S32A S36A, ca-mTOR or TRX, reduced cell killing. AR42, via lysosomal degradation, reduced the protein expression of HDACs 2/5/6/10/11. In vivo, a 3-day exposure of dabrafenib/trametinib resistant melanoma cells to the AR42 pazopanib combination reduced tumor growth and enhanced survival from ~25 to ~40 days. Tumor cells that had adapted through therapy exhibited elevated HGF expression and the c-MET inhibitor crizotinib enhanced AR42 pazopanib lethality in this evolved drug-resistant population.

Keywords: ER stress; autophagy; chaperone; death receptor.

MeSH terms

  • Angiogenesis Inhibitors / administration & dosage
  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Autophagosomes / drug effects
  • Autophagosomes / metabolism
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm / drug effects
  • Drug Synergism
  • Endoplasmic Reticulum Chaperone BiP
  • Eukaryotic Initiation Factor-2 / genetics
  • Eukaryotic Initiation Factor-2 / metabolism
  • Histone Deacetylase 6
  • Histone Deacetylase Inhibitors / administration & dosage
  • Histone Deacetylase Inhibitors / pharmacology
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Humans
  • Imidazoles / pharmacology*
  • Indazoles
  • Kaplan-Meier Estimate
  • Male
  • Melanoma / drug therapy*
  • Melanoma / genetics
  • Melanoma / metabolism
  • Mice, Nude
  • Microscopy, Fluorescence
  • Oximes / pharmacology*
  • Phenylbutyrates / administration & dosage
  • Phenylbutyrates / pharmacology*
  • Pyridones / pharmacology*
  • Pyrimidines / administration & dosage
  • Pyrimidines / pharmacology*
  • Pyrimidinones / pharmacology*
  • RNA Interference
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Sulfonamides / administration & dosage
  • Sulfonamides / pharmacology*
  • Xenograft Model Antitumor Assays

Substances

  • Angiogenesis Inhibitors
  • Endoplasmic Reticulum Chaperone BiP
  • Eukaryotic Initiation Factor-2
  • HSPA5 protein, human
  • Histone Deacetylase Inhibitors
  • Hspa5 protein, mouse
  • Imidazoles
  • Indazoles
  • OSU-HDAC42 compound
  • Oximes
  • Phenylbutyrates
  • Pyridones
  • Pyrimidines
  • Pyrimidinones
  • Sulfonamides
  • trametinib
  • pazopanib
  • HDAC6 protein, human
  • Histone Deacetylase 6
  • Histone Deacetylases
  • dabrafenib