Endothelial cell-derived angiopoietin-2 is a therapeutic target in treatment-naive and bevacizumab-resistant glioblastoma

EMBO Mol Med. 2016 Jan 1;8(1):39-57. doi: 10.15252/emmm.201505505.

Abstract

Glioblastoma multiforme (GBM) is treated by surgical resection followed by radiochemotherapy. Bevacizumab is commonly deployed for anti-angiogenic therapy of recurrent GBM; however, innate immune cells have been identified as instigators of resistance to bevacizumab treatment. We identified angiopoietin-2 (Ang-2) as a potential target in both naive and bevacizumab-treated glioblastoma. Ang-2 expression was absent in normal human brain endothelium, while the highest Ang-2 levels were observed in bevacizumab-treated GBM. In a murine GBM model, VEGF blockade resulted in endothelial upregulation of Ang-2, whereas the combined inhibition of VEGF and Ang-2 leads to extended survival, decreased vascular permeability, depletion of tumor-associated macrophages, improved pericyte coverage, and increased numbers of intratumoral T lymphocytes. CD206(+) (M2-like) macrophages were identified as potential novel targets following anti-angiogenic therapy. Our findings imply a novel role for endothelial cells in therapy resistance and identify endothelial cell/myeloid cell crosstalk mediated by Ang-2 as a potential resistance mechanism. Therefore, combining VEGF blockade with inhibition of Ang-2 may potentially overcome resistance to bevacizumab therapy.

Keywords: anti‐angiogenic therapy; glioblastoma; macrophage polarization; therapy resistance; tumor angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiopoietin-2 / antagonists & inhibitors
  • Angiopoietin-2 / blood
  • Angiopoietin-2 / metabolism*
  • Animals
  • Bevacizumab / therapeutic use
  • Brain / metabolism
  • Brain / pathology
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / mortality
  • Brain Neoplasms / pathology*
  • Disease Models, Animal
  • Drug Resistance, Neoplasm
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Female
  • Glioblastoma / drug therapy
  • Glioblastoma / mortality
  • Glioblastoma / pathology*
  • Humans
  • Lectins, C-Type / metabolism
  • Macrophages / cytology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mannose Receptor
  • Mannose-Binding Lectins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neoplasm Grading
  • Receptors, Cell Surface / metabolism
  • Receptors, Vascular Endothelial Growth Factor / pharmacology
  • Receptors, Vascular Endothelial Growth Factor / therapeutic use
  • Recombinant Fusion Proteins / pharmacology
  • Recombinant Fusion Proteins / therapeutic use
  • Signal Transduction / drug effects
  • Up-Regulation / drug effects
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Angiopoietin-2
  • Lectins, C-Type
  • Mannose Receptor
  • Mannose-Binding Lectins
  • Receptors, Cell Surface
  • Recombinant Fusion Proteins
  • Vascular Endothelial Growth Factor A
  • aflibercept
  • Bevacizumab
  • Receptors, Vascular Endothelial Growth Factor
  • trebananib