Excess of a Rassf1-targeting microRNA, miR-193a-3p, perturbs cell division fidelity

Br J Cancer. 2017 May 23;116(11):1451-1461. doi: 10.1038/bjc.2017.110. Epub 2017 Apr 27.

Abstract

Background: Several microRNA (miRNA) molecules have emerged as important post-transcriptional regulators of tumour suppressor and oncogene expression. Ras association domain family member 1 (RASSF1) is a critical tumour suppressor that controls multiple aspects of cell proliferation such as cell cycle, cell division and apoptosis. The expression of RASSF1 is lost in a variety of cancers due to the promoter hypermethylation.

Methods: miR-193a-3p was identified as a RASSF1-targeting miRNA by a dual screening approach. In cultured human cancer cells, immunoblotting, qRT-PCR, luciferase reporter assays, time-lapse microscopy and immunofluorescence methods were used to study the effects of excess miR-193a-3p on RASSF1 expression and cell division.

Results: Here, we report a new miRNA-mediated mechanism that regulates RASSF1 expression: miR-193a-3p binds directly to RASSF1-3'UTR and represses the mRNA and protein expression. In human cancer cells, excess of miR-193a-3p causes polyploidy through impairment of the Rassf1-Syntaxin 16 signalling pathway that is needed for completion of cytokinesis. In the next cell cycle the miR-193a-3p-overexpressing cells exhibit multipolar mitotic spindles, mitotic delay and elevated frequency of cell death.

Conclusions: Our results suggest that besides epigenetic regulation, altered expression of specific miRNAs may contribute to the loss of Rassf1 in cancer cells and cause cell division errors.

MeSH terms

  • 3' Untranslated Regions
  • Cell Death / genetics
  • Cell Division / genetics*
  • Cell Polarity / genetics
  • Cytokinesis / genetics
  • Down-Regulation
  • Gene Expression
  • Gene Expression Regulation, Neoplastic
  • HCT116 Cells
  • HeLa Cells
  • Humans
  • M Phase Cell Cycle Checkpoints / genetics
  • MicroRNAs / genetics*
  • RNA, Messenger / metabolism*
  • Signal Transduction / genetics
  • Syntaxin 16 / metabolism
  • Transfection
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism

Substances

  • 3' Untranslated Regions
  • MIRN193 microRNA, human
  • MicroRNAs
  • RASSF1 protein, human
  • RNA, Messenger
  • Syntaxin 16
  • Tumor Suppressor Proteins