The gain-of-function GLI1 transcription factor TGLI1 enhances expression of VEGF-C and TEM7 to promote glioblastoma angiogenesis

Oncotarget. 2015 Sep 8;6(26):22653-65. doi: 10.18632/oncotarget.4248.

Abstract

We recently discovered that truncated glioma-associated oncogene homolog 1 (TGLI1) is highly expressed in glioblastoma (GBM) and linked to increased GBM vascularity. The mechanisms underlying TGLI1-mediated angiogenesis are unclear. In this study, we compared TGLI1- with GLI1-expressing GBM xenografts for the expression profile of 84 angiogenesis-associated genes. The results showed that expression of six genes were upregulated and five were down-regulated in TGLI1-carrying tumors compared to those with GLI1. Vascular endothelial growth factor-C (VEGF-C) and tumor endothelial marker 7 (TEM7) were selected for further investigations because of their significant correlations with high vascularity in 135 patient GBMs. TGLI1 bound to both VEGF-C and TEM7 gene promoters. Conditioned medium from TGLI1-expressing GBM cells strongly induced tubule formation of brain microvascular endothelial cells, and the induction was prevented by VEGF-C/TEM7 knockdown. Immunohistochemical analysis of 122 gliomas showed that TGLI1 expression was positively correlated with VEGF-C, TEM7 and microvessel density. Analysis of NCBI Gene Expression Omnibus datasets with 161 malignant gliomas showed an inverse relationship between tumoral VEGF-C, TEM7 or microvessel density and patient survival. Together, our findings support an important role that TGLI1 plays in GBM angiogenesis and identify VEGF-C and TEM7 as novel TGLI1 target genes of importance to GBM vascularity.

Keywords: GLI1; TGLI1; VEGF-C; angiogenesis; glioblastoma.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain Neoplasms / blood supply*
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Cell Line, Tumor
  • Glioblastoma / blood supply*
  • Glioblastoma / genetics
  • Glioblastoma / metabolism
  • Heterografts
  • Humans
  • Immunohistochemistry
  • Mice
  • Mice, Nude
  • Neoplasm Proteins / biosynthesis*
  • Neoplasm Proteins / genetics
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Pathologic / pathology
  • Receptors, Cell Surface / biosynthesis*
  • Receptors, Cell Surface / genetics
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transfection
  • Up-Regulation
  • Vascular Endothelial Growth Factor C / biosynthesis*
  • Vascular Endothelial Growth Factor C / genetics
  • Zinc Finger Protein GLI1

Substances

  • GLI1 protein, human
  • Neoplasm Proteins
  • PLXDC1 protein, human
  • Receptors, Cell Surface
  • Transcription Factors
  • VEGFC protein, human
  • Vascular Endothelial Growth Factor C
  • Zinc Finger Protein GLI1