TrkB-containing exosomes promote the transfer of glioblastoma aggressiveness to YKL-40-inactivated glioblastoma cells

Oncotarget. 2016 Aug 2;7(31):50349-50364. doi: 10.18632/oncotarget.10387.

Abstract

The neurotrophin receptors are known to promote growth and proliferation of glioblastoma cells. Their functions in spreading glioblastoma cell aggressiveness to the microenvironment through exosome release from glioblastoma cells are unknown. Considering previous reports demonstrating that YKL-40 expression is associated with undifferentiated glioblastoma cancer stem cells, we used YKL-40-silenced cells to modulate the U87-MG differentiated state and their biological aggressiveness. Herein, we demonstrated a relationship between neurotrophin-receptors and YKL-40 expression in undifferentiated cells. Differential functions of cells and derived-exosomes were evidenced according to neurotrophin receptor content and differentiated cell state by comparison with control pLKO cells. YKL-40 silencing of glioblastoma cells impairs proliferation, neurosphere formation, and their ability to induce endothelial cell (HBMEC) migration. The modulation of differentiated cell state in YKL-40-silenced cells induces a decrease of TrkB, sortilin and p75NTR cellular expressions, associated with a low-aggressiveness phenotype. Interestingly, TrkB expressed in exosomes derived from control cells was undetectable in exosomes from YKL-40 -silenced cells. The transfer of TrkB-containing exosomes in YKL-40-silenced cells contributed to restore cell proliferation and promote endothelial cell activation. Interestingly, in U87 MG xenografted mice, TrkB-depleted exosomes from YKL-40-silenced cells inhibited tumor growth in vivo. These data highlight that TrkB-containing exosomes play a key role in the control of glioblastoma progression and aggressiveness. Furthermore, TrkB expression was detected in exosomes isolated from plasma of glioblastoma patients, suggesting that this receptor may be considered as a new biomarker for glioblastoma diagnosis.

Keywords: TrkB; exosomes; glioblastoma; neurotrophin receptors; undifferentiated cells.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / metabolism
  • Animals
  • Brain Neoplasms / metabolism*
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Chitinase-3-Like Protein 1 / metabolism*
  • Exosomes / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gene Silencing
  • Glioblastoma / metabolism*
  • HEK293 Cells
  • Humans
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Neoplasm Invasiveness
  • Neoplasm Transplantation
  • Receptor, Nerve Growth Factor / metabolism
  • Receptor, trkB / metabolism*
  • Receptors, Nerve Growth Factor / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • CHI3L1 protein, human
  • Chitinase-3-Like Protein 1
  • Membrane Glycoproteins
  • Receptor, Nerve Growth Factor
  • Receptors, Nerve Growth Factor
  • Receptor, trkB
  • tropomyosin-related kinase-B, human
  • sortilin