Tumour-infiltrating neutrophils counteract anti-VEGF therapy in metastatic colorectal cancer

Br J Cancer. 2019 Jan;120(1):69-78. doi: 10.1038/s41416-018-0198-3. Epub 2018 Oct 31.

Abstract

Background: Immune infiltration is implicated in the development of acquired resistance to anti-angiogenic cancer therapy. We therefore investigated the correlation between neutrophil infiltration in metastasis of colorectal cancer (CRC) patients and survival after treatment with bevacizumab. Our study identifies CD177+ tumour neutrophil infiltration as an adverse prognostic factor for bevacizumab treatment. We further demonstrate that a novel anti-VEGF/anti-Ang2 compound (BI-880) can overcome resistance to VEGF inhibition in experimental tumour models.

Methods: A total of 85 metastatic CRC patients were stratified into cohorts that had either received chemotherapy alone (n = 39) or combined with bevacizumab (n = 46). Tumour CD177+ neutrophil infiltration was correlated to clinical outcome. The impact of neutrophil infiltration on anti-VEGF or anti-VEGF/anti-Ang2 therapy was studied in both xenograft and syngeneic tumour models by immunohistochemistry.

Results: The survival of bevacizumab-treated CRC patients in the presence of CD177+ infiltrates was significantly reduced compared to patients harbouring CD177- metastases. BI-880 treatment reduced the development of hypoxia associated with bevacizumab treatment and improved vascular normalisation in xenografts. Furthermore, neutrophil depletion or BI-880 treatment restored treatment sensitivity in a syngeneic tumour model of anti-VEGF resistance.

Conclusions: Our findings implicate CD177 as a biomarker for bevacizumab and suggest VEGF/Ang2 inhibition as a strategy to overcome neutrophil associated resistance to anti-angiogenic treatment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Angiogenesis Inhibitors / administration & dosage
  • Animals
  • Antibodies, Monoclonal, Humanized / administration & dosage
  • Bevacizumab / administration & dosage
  • Biomarkers, Tumor / genetics
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / pathology
  • Drug Resistance, Neoplasm / genetics
  • Female
  • GPI-Linked Proteins / genetics
  • Humans
  • Isoantigens / genetics*
  • Male
  • Mice
  • Middle Aged
  • Neoplasm Metastasis
  • Neoplastic Stem Cells / drug effects
  • Neovascularization, Pathologic / drug therapy*
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / pathology
  • Neutrophils / drug effects
  • Receptors, Cell Surface / genetics*
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / genetics*
  • Vesicular Transport Proteins / genetics*
  • Xenograft Model Antitumor Assays

Substances

  • Angiogenesis Inhibitors
  • Antibodies, Monoclonal, Humanized
  • Biomarkers, Tumor
  • CD177 protein, human
  • GPI-Linked Proteins
  • Isoantigens
  • Receptors, Cell Surface
  • VEGFA protein, human
  • VPS51 protein, human
  • Vascular Endothelial Growth Factor A
  • Vesicular Transport Proteins
  • Bevacizumab