Anti-tumoral effects of miR-3189-3p in glioblastoma

J Biol Chem. 2015 Mar 27;290(13):8067-80. doi: 10.1074/jbc.M114.633081. Epub 2015 Feb 2.

Abstract

Glioblastoma is one of the most aggressive brain tumors. We have previously found up-regulation of growth differentiation factor 15 (GDF15) in glioblastoma cells treated with the anticancer agent fenofibrate. Sequence analysis of GDF15 revealed the presence of a microRNA, miR-3189, in the single intron. We then asked whether miR-3189 was expressed in clinical samples and whether it was functional in glioblastoma cells. We found that expression of miR-3189-3p was down-regulated in astrocytoma and glioblastoma clinical samples compared with control brain tissue. In vitro, the functionality of miR-3189-3p was tested by RNA-binding protein immunoprecipitation, and miR-3189-3p coimmunoprecipitated with Argonaute 2 together with two of its major predicted gene targets, the SF3B2 splicing factor and the guanine nucleotide exchange factor p63RhoGEF. Overexpression of miR-3189-3p resulted in a significant inhibition of cell proliferation and migration through direct targeting of SF3B2 and p63RhoGEF, respectively. Interestingly, miR-3189-3p levels were increased by treatment of glioblastoma cells with fenofibrate, a lipid-lowering drug with multiple anticancer activities. The attenuated expression of miR-3189-3p in clinical samples paralleled the elevated expression of SF3B2, which could contribute to the activation of SF3B2 growth-promoting pathways in these tumors. Finally, miR-3189-3p-mediated inhibition of tumor growth in vivo further supported the function of this microRNA as a tumor suppressor.

Keywords: Cell Migration; Cell Proliferation; Glioblastoma; MicroRNA (miRNA); Tumor Suppressor Gene.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • Binding Sites
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism*
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Female
  • Gene Expression
  • Gene Expression Regulation, Neoplastic
  • Genes, Tumor Suppressor
  • Glioblastoma / genetics
  • Glioblastoma / metabolism*
  • Glioblastoma / pathology
  • Growth Differentiation Factor 15 / genetics
  • Growth Differentiation Factor 15 / metabolism
  • Humans
  • Mice, Nude
  • MicroRNAs / genetics*
  • Neoplasm Transplantation
  • RNA Interference
  • RNA Splicing Factors
  • RNA-Binding Proteins / biosynthesis
  • RNA-Binding Proteins / genetics
  • Rho Guanine Nucleotide Exchange Factors / biosynthesis
  • Rho Guanine Nucleotide Exchange Factors / genetics

Substances

  • ARHGEF25 protein, human
  • GDF15 protein, human
  • Growth Differentiation Factor 15
  • MIRN3189 microRNA, human
  • MicroRNAs
  • RNA Splicing Factors
  • RNA-Binding Proteins
  • Rho Guanine Nucleotide Exchange Factors
  • SF3B2 protein, human