Endothelial-like malignant glioma cells in dynamic three dimensional culture identifies a role for VEGF and FGFR in a tumor-derived angiogenic response

Oncotarget. 2015 Sep 8;6(26):22191-205. doi: 10.18632/oncotarget.4339.

Abstract

Aims: Recent studies have observed that cells from high-grade glial tumors are capable of assuming an endothelial phenotype and genotype, a process termed 'vasculogenic mimicry' (VM). Here we model and manipulate VM in dynamic 3-dimensional (3D) glioma cultures.

Methods: The Rotary Cell Culture System (RCCS) was used to derive large macroscopic glioma aggregates, which were sectioned for immunohistochemistry and RNA extracted prior to angiogenic array-PCR.

Results: A 3D cell culture induced microenvironment (containing only glial cells) is sufficient to promote expression of the endothelial markers CD105, CD31 and vWF in a proportion of glioma aggregates in vitro. Many pro-angiogenic genes were upregulated in glioma aggregates and in primary explants and glioma cells were capable of forming tubular-like 3D structures under endothelial-promoting conditions. Competitive inhibition of either vascular endothelial growth factor or fibroblast growth factor receptor was sufficient to impair VM and downregulate the tumor-derived angiogenic response, whilst impairing tumor cell derived tubule formation. Glioma xenografts using the same cells reveal tumor-derived vessel-like structures near necrotic areas, consistent with widespread tumor-derived endothelial expression in primary glioma tissue.

Conclusions: Our findings support studies indicating that tumor-derived endothelial cells arise in gliomas and describe a dynamic 3D culture as a bona fide model to interrogate the molecular basis of this phenomenon in vitro. Resistance to current anti-angiogenic therapies and the contribution of tumor derived endothelial cells to such resistance are amenable to study using the RCCS.

Keywords: angiogenesis; glioma; rotary cell culture system; tumor-derived endothelium; vasculogenic mimicry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Neoplasms / blood supply*
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Glioma / blood supply*
  • Glioma / metabolism
  • Glioma / pathology
  • Heterografts
  • Humans
  • Mice
  • Mice, Nude
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Pathologic / pathology
  • Receptors, Fibroblast Growth Factor / metabolism*
  • Vascular Endothelial Growth Factor A / metabolism*

Substances

  • Receptors, Fibroblast Growth Factor
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A