EZH2 Modifies Sunitinib Resistance in Renal Cell Carcinoma by Kinome Reprogramming

Cancer Res. 2017 Dec 1;77(23):6651-6666. doi: 10.1158/0008-5472.CAN-17-0899. Epub 2017 Oct 4.

Abstract

Acquired and intrinsic resistance to receptor tyrosine kinase inhibitors (RTKi) represents a major hurdle in improving the management of clear cell renal cell carcinoma (ccRCC). Recent reports suggest that drug resistance is driven by tumor adaptation via epigenetic mechanisms that activate alternative survival pathways. The histone methyl transferase EZH2 is frequently altered in many cancers, including ccRCC. To evaluate its role in ccRCC resistance to RTKi, we established and characterized a spontaneously metastatic, patient-derived xenograft model that is intrinsically resistant to the RTKi sunitinib, but not to the VEGF therapeutic antibody bevacizumab. Sunitinib maintained its antiangiogenic and antimetastatic activity but lost its direct antitumor effects due to kinome reprogramming, which resulted in suppression of proapoptotic and cell-cycle-regulatory target genes. Modulating EZH2 expression or activity suppressed phosphorylation of certain RTKs, restoring the antitumor effects of sunitinib in models of acquired or intrinsically resistant ccRCC. Overall, our results highlight EZH2 as a rational target for therapeutic intervention in sunitinib-resistant ccRCC as well as a predictive marker for RTKi response in this disease. Cancer Res; 77(23); 6651-66. ©2017 AACR.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Bevacizumab / pharmacology
  • Carcinoma, Renal Cell / drug therapy*
  • Carcinoma, Renal Cell / pathology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / physiology*
  • Enhancer of Zeste Homolog 2 Protein / antagonists & inhibitors*
  • Enhancer of Zeste Homolog 2 Protein / genetics
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Female
  • Humans
  • Indoles / pharmacology*
  • Kidney Neoplasms / drug therapy*
  • Kidney Neoplasms / pathology
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / secondary
  • Mice
  • Mice, Inbred ICR
  • Mice, SCID
  • Neovascularization, Pathologic / drug therapy
  • Phosphorylation
  • Pyrroles / pharmacology*
  • Receptor Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Sunitinib
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Indoles
  • Pyrroles
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Bevacizumab
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Receptor Protein-Tyrosine Kinases
  • Sunitinib