Hsp90 inhibitor geldanamycin attenuates the cytotoxicity of sunitinib in cardiomyocytes via inhibition of the autophagy pathway

Toxicol Appl Pharmacol. 2017 Aug 15:329:282-292. doi: 10.1016/j.taap.2017.06.015. Epub 2017 Jun 15.

Abstract

Sunitinib malate (sunitinib) is an orally available, multitargeted tyrosine kinase inhibitor with antitumor and antiangiogenic activities. Although sunitinib is effective for the treatment of patients with gastrointestinal stromal tumor, advanced renal cell carcinoma, or pancreatic neuroendocrine tumor, adverse cardiac events associated with sunitinib administration have been reported. Here, we examined the effect of geldanamycin, an inhibitor of heat shock protein (Hsp) 90, on sunitinib-induced cytotoxicity in cardiomyocytes. First, we found that treatment with geldanamycin or other Hsp90 inhibitors (tanespimycin, ganetespib, or BIIB021) significantly attenuated sunitinib-induced cytotoxicity in rat H9c2 cardiomyocytes, suggesting a drug-class effect of Hsp90 inhibitors. We then examined the mechanisms underlying sunitinib-induced cytotoxicity and found that sunitinib induced autophagy in H9c2 cells and that pretreatment with geldanamycin inhibited the induction of autophagy by promoting degradation of the autophagy-related proteins Atg7, Beclin-1, and ULK1. Pharmacological assessment with autophagy inhibitors confirmed that geldanamycin attenuated the cytotoxicity of sunitinib by interfering with autophagy. In addition, we found that the molecular chaperone Hsp70, which is induced by geldanamycin, was not involved in the attenuation of sunitinib-induced cytotoxicity. Finally, to provide more clinically relevant data, we confirmed that geldanamycin attenuated sunitinib-induced cytotoxicity in human induced pluripotent stem cell-derived cardiomyocytes. Together, these data suggest that geldanamycin attenuates sunitinib-induced cytotoxicity in cardiomyocytes by inhibiting the autophagy pathway. Thus, the further investigation of combination or sequential treatment with an Hsp90 inhibitor and sunitinib is warranted as a potential strategy of attenuating the cardiotoxicity associated with sunitinib administration in the clinical setting.

Keywords: Autophagy; Cardiotoxicity; Hsp90 inhibitor; Human induced pluripotent stem cell; Sunitinib.

MeSH terms

  • Animals
  • Antineoplastic Agents / toxicity*
  • Autophagy / drug effects*
  • Autophagy-Related Protein 7 / genetics
  • Autophagy-Related Protein 7 / metabolism
  • Autophagy-Related Protein-1 Homolog / genetics
  • Autophagy-Related Protein-1 Homolog / metabolism
  • Beclin-1 / genetics
  • Beclin-1 / metabolism
  • Benzoquinones / pharmacology*
  • Cardiotoxicity
  • Cell Differentiation
  • Cell Line
  • Cell Lineage
  • Cytoprotection
  • Dose-Response Relationship, Drug
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / metabolism
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors*
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Indoles / toxicity*
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology
  • Lactams, Macrocyclic / pharmacology*
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • Protein Kinase Inhibitors / toxicity*
  • Pyrroles / toxicity*
  • RNA Interference
  • Rats
  • Signal Transduction / drug effects
  • Sunitinib
  • Transfection

Substances

  • Antineoplastic Agents
  • Atg7 protein, rat
  • Beclin-1
  • Becn1 protein, rat
  • Benzoquinones
  • HSP70 Heat-Shock Proteins
  • HSP90 Heat-Shock Proteins
  • Hspa1a protein, rat
  • Indoles
  • Lactams, Macrocyclic
  • Protein Kinase Inhibitors
  • Pyrroles
  • Autophagy-Related Protein-1 Homolog
  • ULK1 protein, rat
  • Autophagy-Related Protein 7
  • Sunitinib
  • geldanamycin