Sunitinib dose escalation overcomes transient resistance in clear cell renal cell carcinoma and is associated with epigenetic modifications

Mol Cancer Ther. 2015 Feb;14(2):513-22. doi: 10.1158/1535-7163.MCT-14-0208. Epub 2014 Dec 17.

Abstract

Sunitinib is considered a first-line therapeutic option for patients with advanced clear cell renal cell carcinoma (ccRCC). Despite sunitinib's clinical efficacy, patients eventually develop drug resistance and disease progression. Herein, we tested the hypothesis whether initial sunitinib resistance may be transient and could be overcome by dose increase. In selected patients initially treated with 50 mg sunitinib and presenting with minimal toxicities, sunitinib dose was escalated to 62.5 mg and/or 75 mg at the time of tumor progression. Mice bearing two different patient-derived ccRCC xenografts (PDX) were treated 5 days per week with a dose-escalation schema (40-60-80 mg/kg sunitinib). Tumor tissues were collected before dose increments for immunohistochemistry analyses and drug levels. Selected intrapatient sunitinib dose escalation was safe and several patients had added progression-free survival. In parallel, our preclinical results showed that PDXs, although initially responsive to sunitinib at 40 mg/kg, eventually developed resistance. When the dose was incrementally increased, again we observed tumor response to sunitinib. A resistant phenotype was associated with transient increase of tumor vasculature despite intratumor sunitinib accumulation at higher dose. In addition, we observed associated changes in the expression of the methyltransferase EZH2 and histone marks at the time of resistance. Furthermore, specific EZH2 inhibition resulted in increased in vitro antitumor effect of sunitinib. Overall, our results suggest that initial sunitinib-induced resistance may be overcome, in part, by increasing the dose, and highlight the potential role of epigenetic changes associated with sunitinib resistance that can represent new targets for therapeutic intervention.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Renal Cell / blood supply
  • Carcinoma, Renal Cell / drug therapy*
  • Carcinoma, Renal Cell / genetics*
  • Carcinoma, Renal Cell / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Disease Progression
  • Dose-Response Relationship, Drug
  • Drug Resistance, Neoplasm* / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Enhancer of Zeste Homolog 2 Protein
  • Epigenesis, Genetic* / drug effects
  • Humans
  • Immunohistochemistry
  • Indoles / blood
  • Indoles / pharmacology
  • Indoles / therapeutic use*
  • Kidney Neoplasms / blood supply
  • Kidney Neoplasms / drug therapy*
  • Kidney Neoplasms / genetics*
  • Kidney Neoplasms / pathology
  • Mice, SCID
  • Microvessels / drug effects
  • Microvessels / pathology
  • Polycomb Repressive Complex 2 / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • Pyrroles / blood
  • Pyrroles / pharmacology
  • Pyrroles / therapeutic use*
  • Sunitinib
  • Treatment Outcome
  • Xenograft Model Antitumor Assays

Substances

  • Indoles
  • Protein Kinase Inhibitors
  • Pyrroles
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2
  • Sunitinib