An axis involving SNAI1, microRNA-128 and SP1 modulates glioma progression

PLoS One. 2014 Jun 24;9(6):e98651. doi: 10.1371/journal.pone.0098651. eCollection 2014.

Abstract

Background: Glioblastoma is an extraordinarily aggressive disease that requires more effective therapeutic options. Snail family zinc finger 1, dysregulated in many neoplasms, has been reported to be involved in gliomas. However, the biological mechanisms underlying SNAI1 function in gliomas need further investigation.

Methods: Quantitative real-time PCR was used to measure microRNA-128 (miR-128) expression level and western blot was performed to detect protein expression in U87 and U251 cells and human brain tissues. Cell cycle, CCK-8, transwell and wound-healing assays were performed. Dual-luciferase reporter assay was used for identifying the mechanism of SNAI1 and miR-128b regulation. The mechanism of miR-128 targeting SP1 was also tested by luciferase reporter assay. Immunohistochemistry and in situ hybridisation staining were used for quantifying SNAI1, SP1 and miR-128 expression levels in human glioma samples.

Results: The Chinese Glioma Genome Atlas (CGGA) data revealed that SNAI1 was up-regulated in glioma and we confirmed the findings in normal and glioma tissues. SNAI1 depletion by shRNA retarded the cell cycle and suppressed proliferation and invasion in glioma cell lines. The CGGA data showed that the Pearson correlation index between SNAI1 and miR-128 was negatively correlated. SNAI1 suppressed miR-128b expression by binding to the miR-128b specific promoter motif, and miR-128 targeted SP1 via binding to the 3'-untranslated region of SP1. Moreover, introduction of miR-128 anti-sense oligonucleotide alleviated the cell cycle retardation, proliferation and invasion inhibition induced by SNAI1 shRNA. Immunohistochemistry and in situ hybridisation analysis of SNAI1, SP1 and miR-128 unraveled their expression levels and correlations in glioma samples.

Conclusions: We propose that the SNAI1/miR-128/SP1 axis, which plays a vital role in glioma progression, may come to be a clinically relevant therapeutic target.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Cell Cycle
  • Cell Line, Tumor
  • Cell Proliferation
  • Disease Progression
  • Glioblastoma / genetics
  • Glioblastoma / metabolism
  • Glioblastoma / pathology*
  • Humans
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Snail Family Transcription Factors
  • Sp1 Transcription Factor / genetics*
  • Sp1 Transcription Factor / metabolism
  • Transcription Factors / chemistry
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism*
  • Up-Regulation

Substances

  • MIRN128 microRNA, human
  • MicroRNAs
  • SNAI1 protein, human
  • Snail Family Transcription Factors
  • Sp1 Transcription Factor
  • SP1 protein, human
  • Transcription Factors

Grants and funding

This work was supported by grants from the National High Technology Research and Development Program of China (863) (2012AA02A508), International Cooperation Program (2012DFA30470), National Natural Science Foundation of China (91229121, 81272792, 81172389, 81372709, 81302185, 81101901, 81302184), Jiangsu Province's Key Provincial Talents Program (RC2011051), Jiangsu Province's Key Discipline of Medicine (XK201117), Jiangsu Provincial Special Program of Medical Science (BL2012028), and Program for Development of Innovative Research Team in the First Affiliated Hospital of NJMU, and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.