MiR-124 governs glioma growth and angiogenesis and enhances chemosensitivity by targeting R-Ras and N-Ras

Neuro Oncol. 2014 Oct;16(10):1341-53. doi: 10.1093/neuonc/nou084. Epub 2014 May 25.

Abstract

Background: Glioma is one of the most aggressive and lethal human brain tumors. Accumulating evidence shows that microRNAs play important roles in cancers, including glioma. Previous studies reported that miR-124 levels were downregulated in glioma specimens. Here, we further investigate the potential role of miR-124 in glioma.

Methods: The expression levels of miR-124 were detected in glioma specimens by quantitative reverse transcriptase PCR. The direct targets of miR-124 were identified by bioinformatics analysis and were further validated by immunoblotting and luciferase reporter assay. The effects of miR-124 on glioma cell proliferation and chemosensitivity to temozolomide were analyzed by Cell-Counting Kit 8 assay. Apoptosis was evaluated by fluorescence activated cell sorting analysis. A xenograft model was used to study the effect of miR-124 on tumor growth and angiogenesis.

Results: Expression levels of miR-124 were greatly downregulated in glioma specimens. related Ras viral oncogene homolog (R-Ras) and neuroblastoma Ras viral oncogene homolog (N-Ras) were identified as direct targets of miR-124. MiR-124 inhibited glioma cell growth, invasion, angiogenesis, and tumor growth and increased chemosensitivity to temozolomide treatment by negatively regulating the Ras family and its downstream signaling pathways: phosphatidylinositol-3 kinase/Akt and Raf/extracellular signal-regulated kinase 1/2. Furthermore, overexpression of R-Ras rescued the inhibitory effects of miR-124. Meanwhile, overexpression of R-Ras and N-Ras restored miR-124-inhibited vascular endothelial growth factor (VEGF) transcription activation. In clinical glioma specimens, protein levels of R-Ras and N-Ras were upregulated and inversely correlated with miR-124 expression levels.

Conclusions: Taken together, these results revealed that miR-124 levels in tumor tissues are associated with glioma occurrence, angiogenesis, and chemoresistance and that miR-124 may be used as a new diagnostic marker and therapeutic target for glioma in the future.

Keywords: N-Ras; R-Ras; carcinogenesis; glioma; miR-124.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Brain / blood supply
  • Brain Neoplasms / drug therapy*
  • Brain Neoplasms / metabolism*
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Dacarbazine / administration & dosage
  • Dacarbazine / analogs & derivatives
  • Genes, ras*
  • Glioma / drug therapy*
  • Glioma / metabolism*
  • Glioma / pathology
  • Humans
  • Male
  • Mice
  • Mice, Nude
  • MicroRNAs / metabolism*
  • Neoplasm Invasiveness / physiopathology
  • Neovascularization, Pathologic*
  • Signal Transduction
  • Temozolomide
  • ras Proteins / metabolism*

Substances

  • MIRN124 microRNA, human
  • MicroRNAs
  • Dacarbazine
  • RRAS protein, human
  • ras Proteins
  • Temozolomide