MicroRNA-146a-5p-modified human umbilical cord mesenchymal stem cells enhance protection against diabetic nephropathy in rats through facilitating M2 macrophage polarization

Stem Cell Res Ther. 2022 Apr 27;13(1):171. doi: 10.1186/s13287-022-02855-7.

Abstract

Background: Diabetic nephropathy (DN) is a severe complication of diabetes mellitus and a common cause of end-stage renal disease (ESRD). Mesenchymal stem cells (MSCs) possess potent anti-inflammatory and immunomodulatory properties, which render them an attractive therapeutic tool for tissue damage and inflammation.

Methods: This study was designed to determine the protective effects and underlying mechanisms of human umbilical cord-derived MSCs (UC-MSCs) on streptozotocin-induced DN. Renal function and histological staining were used to evaluate kidney damage. RNA high-throughput sequencing on rat kidney and UCMSC-derived exosomes was used to identify the critical miRNAs. Co-cultivation of macrophage cell lines and UC-MSCs-derived conditional medium were used to assess the involvement of macrophage polarization signaling.

Results: UC-MSC administration significantly improved renal function, reduced the local and systemic inflammatory cytokine levels, and attenuated inflammatory cell infiltration into the kidney tissue in DN rats. Moreover, UC-MSCs shifted macrophage polarization from a pro-inflammatory M1 to an anti-inflammatory M2 phenotype. Mechanistically, miR-146a-5p was significantly downregulated and negatively correlated with renal injury in DN rats as determined through high-throughput RNA sequencing. Importantly, UC-MSCs-derived miR-146a-5p promoted M2 macrophage polarization by inhibiting tumor necrosis factor receptor-associated factor-6 (TRAF6)/signal transducer and activator of transcription (STAT1) signaling pathway. Furthermore, miR-146a-5p modification in UC-MSCs enhanced the efficacy of anti-inflammation and renal function improvement.

Conclusions: Collectively, our findings demonstrate that UC-MSCs-derived miR-146a-5p have the potential to restore renal function in DN rats through facilitating M2 macrophage polarization by targeting TRAF6. This would pave the way for the use of miRNA-modified cell therapy for kidney diseases.

Keywords: Diabetic nephropathy; Macrophage polarization; Mesenchymal stem cells; MicroRNAs.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / metabolism
  • Diabetes Mellitus* / metabolism
  • Diabetic Nephropathies* / genetics
  • Diabetic Nephropathies* / metabolism
  • Diabetic Nephropathies* / therapy
  • Female
  • Humans
  • Macrophages / metabolism
  • Male
  • Mesenchymal Stem Cells* / metabolism
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Rats
  • TNF Receptor-Associated Factor 6
  • Umbilical Cord / metabolism

Substances

  • Anti-Inflammatory Agents
  • MIRN146a microRNA, rat
  • MicroRNAs
  • TNF Receptor-Associated Factor 6