Therapeutic efficacy of a synthetic epsin mimetic peptide in glioma tumor model: uncovering multiple mechanisms beyond the VEGF-associated tumor angiogenesis

J Neurooncol. 2018 May;138(1):17-27. doi: 10.1007/s11060-018-2766-z. Epub 2018 Jan 22.

Abstract

Binding of epsin ubiquitin-interacting motif (UIM) with ubiquitylated VEGFR2 is a critical mechanism for epsin-dependent VEGFR2 endocytosis and physiological angiogenesis. Deletion of epsins in vessel endothelium produces uncontrolled tumor angiogenesis and retards tumor growth in animal models. The aim of this study is to test the therapeutic efficacy and targeting specificity of a chemically-synthesized peptide, UPI, which compete for epsin binding sites in VEGFR2 and potentially inhibits Epsin-VEGFR2 interaction in vivo, in an attempt to reproduce an epsin-deficient phenotype in tumor angiogenesis. Our data show that UPI treatment significantly inhibits and shrinks tumor growth in GL261 glioma tumor model. UPI peptide specifically targets VEGFR2 signaling pathway revealed by genetic and biochemical approaches. Furthermore, we demonstrated that UPI peptide treatment caused serious thrombosis in tumor vessels and damages tumor cells after a long-term UPI peptide administration. Besides, we revealed that UPI peptides were unexpectedly targeted cancer cells and induced apoptosis. We conclude that UPI peptide is a potent inhibitor to glioma tumor growth through specific targeting of VEGFR2 signaling in the tumor vasculature and cancer cells, which may offer a potentially novel treatment for cancer patients who are resistant to current anti-VEGF therapies.

Keywords: Epsin; Glioma tumor therapy; Mimetic peptide; Tumor angiogenesis; UPI; VEGFR2 signaling.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / chemistry*
  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / therapeutic use*
  • Apoptosis / drug effects
  • Brain Neoplasms / diagnostic imaging
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / genetics
  • Brain Neoplasms / ultrastructure
  • Cell Line, Tumor
  • Disease Models, Animal
  • Endothelial Cells / drug effects
  • Endothelial Cells / ultrastructure
  • Glioma / diagnostic imaging
  • Glioma / drug therapy*
  • Glioma / genetics
  • Glioma / ultrastructure
  • In Situ Nick-End Labeling
  • Magnetic Resonance Imaging
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microscopy, Electron, Transmission
  • Neovascularization, Pathologic / drug therapy*
  • Platelet Endothelial Cell Adhesion Molecule-1 / metabolism
  • Thrombosis / drug therapy
  • Thrombosis / etiology
  • Time Factors
  • Up-Regulation / drug effects
  • Vascular Endothelial Growth Factor Receptor-2 / genetics
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism*

Substances

  • Adaptor Proteins, Vesicular Transport
  • Antineoplastic Agents
  • Platelet Endothelial Cell Adhesion Molecule-1
  • epsin
  • Kdr protein, mouse
  • Vascular Endothelial Growth Factor Receptor-2