Oncogene AEG-1 promotes glioma-induced neurodegeneration by increasing glutamate excitotoxicity

Cancer Res. 2011 Oct 15;71(20):6514-23. doi: 10.1158/0008-5472.CAN-11-0782. Epub 2011 Aug 18.

Abstract

Aggressive tumor growth, diffuse tissue invasion, and neurodegeneration are hallmarks of malignant glioma. Although glutamate excitotoxicity is considered to play a key role in glioma-induced neurodegeneration, the mechanism(s) controlling this process is poorly understood. Astrocyte elevated gene-1 (AEG-1) is an oncogene that is overexpressed in several types of human cancers, including more than 90% of brain tumors. In addition, AEG-1 promotes gliomagenesis, particularly in the context of tumor growth and invasion, 2 primary characteristics of glioma. In the present study, we investigated the contribution of AEG-1 to glioma-induced neurodegeneration. Pearson correlation coefficient analysis in normal brain tissues and samples from glioma patients indicated a strong negative correlation between expression of AEG-1 and a primary glutamate transporter of astrocytes EAAT2. Gain- and loss-of-function studies in normal primary human fetal astrocytes and T98G glioblastoma multiforme cells revealed that AEG-1 repressed EAAT2 expression at a transcriptional level by inducing YY1 activity to inhibit CBP function as a coactivator on the EAAT2 promoter. In addition, AEG-1-mediated EAAT2 repression caused a reduction of glutamate uptake by glial cells, resulting in induction of neuronal cell death. These findings were also confirmed in samples from glioma patients showing that AEG-1 expression negatively correlated with NeuN expression. Taken together, our findings suggest that AEG-1 contributes to glioma-induced neurodegeneration, a hallmark of this fatal tumor, through regulation of EAAT2 expression.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Brain / metabolism
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • CREB-Binding Protein / metabolism
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Line, Tumor
  • Excitatory Amino Acid Transporter 2
  • Glioma / metabolism
  • Glioma / pathology*
  • Glutamate Plasma Membrane Transport Proteins / metabolism*
  • Glutamic Acid / metabolism*
  • Humans
  • Membrane Proteins
  • Nerve Degeneration / metabolism
  • Nerve Degeneration / pathology*
  • Oncogenes*
  • Promoter Regions, Genetic
  • RNA-Binding Proteins
  • Rats
  • YY1 Transcription Factor / metabolism

Substances

  • Cell Adhesion Molecules
  • Excitatory Amino Acid Transporter 2
  • Glutamate Plasma Membrane Transport Proteins
  • MTDH protein, human
  • Membrane Proteins
  • RNA-Binding Proteins
  • SLC1A2 protein, human
  • YY1 Transcription Factor
  • YY1 protein, human
  • Glutamic Acid
  • CREB-Binding Protein
  • CREBBP protein, human