Synergistic activity of the SRC family kinase inhibitor dasatinib and oxaliplatin in colon carcinoma cells is mediated by oxidative stress

Cancer Res. 2009 May 1;69(9):3842-9. doi: 10.1158/0008-5472.CAN-08-2246. Epub 2009 Apr 21.

Abstract

Chemotherapeutic regimens for the treatment of colorectal cancer generally include oxaliplatin, although inherent and acquired resistance is common. One potential mediator of oxaliplatin sensitivity is the nonreceptor protein tyrosine kinase, Src, the activity of which correlates with disease stage and patient survival. Therefore, we investigated the effects of Src inhibition using the tyrosine kinase inhibitor dasatinib on oxaliplatin sensitivity. We show that oxaliplatin acutely activates Src and that combination treatment with dasatinib is synergistic in a cell-line dependent manner, with the level of Src activation correlating with extent of synergy in a panel of six cell lines. Intracellular reactive oxygen species (ROS) are generated after oxaliplatin treatment, and ROS potently activates Src. Pretreatment with antioxidants inhibits oxaliplatin-induced Src activation. In oxaliplatin-resistant cell lines, Src activity is constitutively increased. In a mouse model of colorectal liver metastases, treatment with oxaliplatin also results in chronic Src activation. The combination of dasatinib and oxaliplatin results in significantly smaller tumors compared with single-agent treatment, corresponding with reduced proliferation and angiogenesis. Therefore, we conclude that oxaliplatin activates Src through a ROS-dependent mechanism. Src inhibition increases oxaliplatin activity both in vitro and in vivo. These results suggest that Src inhibitors combined with oxaliplatin may have efficacy in metastatic colon cancer and may provide the first indication of a molecular phenotype that might be susceptible to such combinations.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Apoptosis / drug effects
  • Cell Growth Processes / drug effects
  • Colonic Neoplasms / blood supply
  • Colonic Neoplasms / drug therapy*
  • Colonic Neoplasms / metabolism
  • Colonic Neoplasms / pathology
  • Dasatinib
  • Down-Regulation
  • Drug Synergism
  • HCT116 Cells
  • HT29 Cells
  • Humans
  • Liver Neoplasms, Experimental / drug therapy
  • Liver Neoplasms, Experimental / metabolism
  • Male
  • Mice
  • Mice, Nude
  • Neovascularization, Pathologic / drug therapy
  • Neovascularization, Pathologic / pathology
  • Organoplatinum Compounds / administration & dosage
  • Organoplatinum Compounds / pharmacology*
  • Oxaliplatin
  • Oxidative Stress / drug effects*
  • Protein Kinase Inhibitors / administration & dosage
  • Protein Kinase Inhibitors / pharmacology
  • Pyrimidines / administration & dosage
  • Pyrimidines / pharmacology*
  • Random Allocation
  • Reactive Oxygen Species / metabolism
  • Thiazoles / administration & dosage
  • Thiazoles / pharmacology*
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • src-Family Kinases / antagonists & inhibitors*
  • src-Family Kinases / metabolism

Substances

  • Organoplatinum Compounds
  • Protein Kinase Inhibitors
  • Pyrimidines
  • Reactive Oxygen Species
  • Thiazoles
  • Vascular Endothelial Growth Factor A
  • Oxaliplatin
  • src-Family Kinases
  • Dasatinib