Oncogenic RAS pathway activation promotes resistance to anti-VEGF therapy through G-CSF-induced neutrophil recruitment

Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6079-84. doi: 10.1073/pnas.1303302110. Epub 2013 Mar 25.

Abstract

Granulocyte-colony stimulating factor (G-CSF) promotes mobilization of CD11b(+)Gr1(+) myeloid cells and has been implicated in resistance to anti-VEGF therapy in mouse models. High G-CSF production has been associated with a poor prognosis in cancer patients. Here we show that activation of the RAS/MEK/ERK pathway regulates G-CSF expression through the Ets transcription factor. Several growth factors induced G-CSF expression by a MEK-dependent mechanism. Inhibition of G-CSF release with a MEK inhibitor markedly reduced G-CSF production in vitro and synergized with anti-VEGF antibodies to reduce CD11b(+)Ly6G(+) neutrophil mobilization and tumor growth and led to increased survival in animal models of cancer, including a genetically engineered mouse model of pancreatic adenocarcinoma. Analysis of biopsies from pancreatic cancer patients revealed increased phospho-MEK, G-CSF, and Ets expression and enhanced neutrophil recruitment compared with normal pancreata. These results provide insights into G-CSF regulation and on the mechanism of action of MEK inhibitors and point to unique anticancer strategies.

MeSH terms

  • Animals
  • Binding Sites
  • Cell Line, Tumor
  • Female
  • Granulocyte Colony-Stimulating Factor / metabolism*
  • Humans
  • MAP Kinase Signaling System*
  • Mice
  • Mice, Nude
  • Mice, Transgenic
  • Neoplasms / metabolism
  • Neovascularization, Pathologic
  • Neutrophil Infiltration
  • Neutrophils / cytology*
  • Protein-Tyrosine Kinases / metabolism
  • Proto-Oncogene Protein c-ets-2 / metabolism*
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / therapeutic use*

Substances

  • ETS2 protein, human
  • Proto-Oncogene Protein c-ets-2
  • Vascular Endothelial Growth Factor A
  • Granulocyte Colony-Stimulating Factor
  • Protein-Tyrosine Kinases