Glioblastoma endothelium drives bevacizumab-induced infiltrative growth via modulation of PLXDC1

Int J Cancer. 2019 Mar 15;144(6):1331-1344. doi: 10.1002/ijc.31983. Epub 2018 Dec 16.

Abstract

Bevacizumab, a VEGF-targeting monoclonal antibody, may trigger an infiltrative growth pattern in glioblastoma. We investigated this pattern using both a human specimen and rat models. In the human specimen, a substantial fraction of infiltrating tumor cells were located along perivascular spaces in close relationship with endothelial cells. Brain xenografts of U87MG cells treated with bevacizumab were smaller than controls (p = 0.0055; Student t-test), however, bands of tumor cells spread through the brain farther than controls (p < 0.001; Student t-test). Infiltrating tumor Cells exhibited tropism for vascular structures and propensity to form tubules and niches with endothelial cells. Molecularly, bevacizumab triggered an epithelial to mesenchymal transition with over-expression of the receptor Plexin Domain Containing 1 (PLXDC1). These results were validated using brain xenografts of patient-derived glioma stem-like cells. Enforced expression of PLXDC1 in U87MG cells promoted brain infiltration along perivascular spaces. Importantly, PLXDC1 inhibition prevented perivascular infiltration and significantly increased the survival of bevacizumab-treated rats. Our study indicates that bevacizumab-induced brain infiltration is driven by vascular endothelium and depends on PLXDC1 activation of tumor cells.

Keywords: PLXDC1; antiangiogenic therapy; bevacizumab; brain infiltration; glioblastoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Antineoplastic Agents, Immunological / pharmacology*
  • Antineoplastic Agents, Immunological / therapeutic use
  • Bevacizumab / pharmacology*
  • Bevacizumab / therapeutic use
  • Brain / cytology
  • Brain / drug effects
  • Brain / pathology
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / mortality
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Coculture Techniques
  • Drug Resistance, Neoplasm
  • Endothelial Cells
  • Endothelium / cytology
  • Endothelium / drug effects*
  • Endothelium / pathology
  • Epithelial-Mesenchymal Transition / drug effects
  • Glioblastoma / drug therapy*
  • Glioblastoma / mortality
  • Glioblastoma / pathology
  • Humans
  • Male
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • RNA, Small Interfering / metabolism
  • Rats
  • Rats, Nude
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Survival Analysis
  • Treatment Outcome
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents, Immunological
  • Neoplasm Proteins
  • PLXDC1 protein, human
  • RNA, Small Interfering
  • Receptors, Cell Surface
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Bevacizumab