Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects

J Clin Invest. 2004 Aug;114(3):379-88. doi: 10.1172/JCI21102.

Abstract

Mutant isoforms of the KIT or PDGF receptors expressed by gastrointestinal stromal tumors (GISTs) are considered the therapeutic targets for STI571 (imatinib mesylate; Gleevec), a specific inhibitor of these tyrosine kinase receptors. Case reports of clinical efficacy of Gleevec in GISTs lacking the typical receptor mutations prompted a search for an alternate mode of action. Here we show that Gleevec can act on host DCs to promote NK cell activation. DC-mediated NK cell activation was triggered in vitro and in vivo by treatment of DCs with Gleevec as well as by a loss-of-function mutation of KIT. Therefore, tumors that are refractory to the antiproliferative effects of Gleevec in vitro responded to Gleevec in vivo in an NK cell-dependent manner. Longitudinal studies of Gleevec-treated GIST patients revealed a therapy-induced increase in IFN-gamma production by NK cells, correlating with an enhanced antitumor response. These data point to a novel mode of antitumor action for Gleevec.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Benzamides
  • Case-Control Studies
  • Coculture Techniques
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Enzyme Inhibitors / pharmacology*
  • Female
  • Gastrointestinal Neoplasms / drug therapy
  • Gastrointestinal Neoplasms / genetics
  • Gastrointestinal Neoplasms / metabolism
  • Gastrointestinal Neoplasms / pathology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Imatinib Mesylate
  • Interferon-gamma / drug effects
  • Interferon-gamma / metabolism
  • Killer Cells, Natural / metabolism*
  • Leukocytes, Mononuclear / metabolism
  • Longitudinal Studies
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, SCID
  • Mutation
  • Neutrophil Activation / drug effects
  • Piperazines / pharmacology
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-kit / drug effects
  • Proto-Oncogene Proteins c-kit / genetics*
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Pyrimidines / pharmacology
  • Receptor Protein-Tyrosine Kinases / drug effects
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Receptors, Platelet-Derived Growth Factor / drug effects
  • Receptors, Platelet-Derived Growth Factor / genetics
  • Receptors, Platelet-Derived Growth Factor / metabolism
  • Stromal Cells / drug effects

Substances

  • Antineoplastic Agents
  • Benzamides
  • Enzyme Inhibitors
  • Piperazines
  • Pyrimidines
  • Interferon-gamma
  • Imatinib Mesylate
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-kit
  • Receptor Protein-Tyrosine Kinases
  • Receptors, Platelet-Derived Growth Factor