Downregulation of miR-139-5p contributes to the antiapoptotic effect of liraglutide on the diabetic rat pancreas and INS-1 cells by targeting IRS1

PLoS One. 2017 Mar 27;12(3):e0173576. doi: 10.1371/journal.pone.0173576. eCollection 2017.

Abstract

Liraglutide is administered as glucagon-like peptide-1 (GLP-1) receptor agonist for diabetic patients and can protect pancreatic β-cells by inhibiting their apoptosis. MicroRNA-139-5p (miRNA-139-5p) participates in the regulation of cancer cell apoptosis. However, it is not clear whether miR-139-5p contributes to the anti-apoptotic effect of liraglutide in β-cells. The objective of the present study was to investigate the role of miR-139-5p on apoptosis of pancreatic β-cells. MicroRNA levels in pancreatic tissue from diabetic rats and INS-1 cells treated with liraglutide were measured by real-time quantitative RT-PCR. The role of miR-139-5p on apoptosis was studied by transfecting INS-1 cells with miR-139-5p mimics. The mRNA and protein expression of the target gene, insulin receptor substrate-1 (IRS1), were measured by qRT-PCR and Western blot, respectively. Apoptosis in rat pancreatic tissue and INS-1 cells was detected by TUNEL and annexin V/propidium iodide costaining. Apoptosis of pancreatic tissue from diabetic rats and INS-1 cells was decreased by administration of liraglutide. The expression of miR-139-5p increased in the pancreas of diabetic rats and decreased with liraglutide treatment. Incubation with liraglutide (100 nM) for 48 h attenuated the expression of miR-139-5p and increased the mRNA and protein levels of IRS1. Direct regulatory effects of miR-139-5p on IRS1 were found by a dual-luciferase reporter assay. Transfection of INS-1 cells with miR-139-5p mimics led to decreases in the mRNA and protein expression of IRS1. In conclusion, our observations suggest that decreased miR-139-5p expression contributes to the anti-apoptotic effect of liraglutide on the diabetic rat pancreas and INS-1 cells by targeting IRS1.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Cell Line
  • Diabetes Mellitus, Experimental / drug therapy
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / pathology
  • Diabetes Mellitus, Experimental / therapy*
  • Down-Regulation
  • Genetic Therapy
  • Hypoglycemic Agents / therapeutic use*
  • Insulin Receptor Substrate Proteins / genetics*
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism
  • Insulin-Secreting Cells / pathology
  • Liraglutide / therapeutic use*
  • Male
  • MicroRNAs / genetics*
  • Pancreas / drug effects
  • Pancreas / metabolism
  • Pancreas / pathology
  • RNAi Therapeutics* / methods
  • Rats, Sprague-Dawley

Substances

  • Hypoglycemic Agents
  • Insulin Receptor Substrate Proteins
  • MIRN139 microRNA, rat
  • MicroRNAs
  • Liraglutide

Grants and funding

This study was supported by the Natural Science Foundation of Guangdong Province (S2012010009346); Chinese International Medical Foundation (201203). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.