Upregulation of endothelial cell-derived exosomal microRNA-125b-5p protects from sepsis-induced acute lung injury by inhibiting topoisomerase II alpha

Inflamm Res. 2021 Feb;70(2):205-216. doi: 10.1007/s00011-020-01415-0. Epub 2021 Jan 2.

Abstract

Objective: Emerging evidence has revealed that exosomal microRNAs (miRNAs) are implicated in human diseases. However, role of exosomal miR-125b-5p in sepsis-induced acute lung injury (ALI) remains further explored. We focused on the effect of exosomal miR-125b-5p on ALI progression via targeting topoisomerase II alpha (TOP2A).

Methods: The ALI mouse models were established by cecal ligation and perforation, which were then treated with miR-125b-5p agomir or overexpressed TOP2A. Next, the pathological structure of ALI mouse lung tissues were observed, miR-125b-5p, TOP2A and vascular endothelial growth factor (VEGF) expression was determined, and the lung water content, inflammatory response, protein content in bronchoalveolar lavage fluid (BALF) and cell apoptosis in ALI mouse lung tissues were assessed. Exosomes were extracted from endothelial cells (ECs) and identified, which were then injected into the modeled mice to observe their roles in ALI. The targeting relationship between miR-125b-5p and TOP2A was confirmed.

Results: MiR-125b-5p was downregulated while TOP2A was upregulated in ALI mice. MiR-125b-5p elevation or ECs-derived exosomes promoted VEGF expression, improved pathological changes and restrained lung water content, inflammatory response, protein content in BALF and cell apoptosis in lung tissues ALI mice. TOP2A overexpression reversed the repressive role of miR-125b-5p upregulation in ALI, while downregulated miR-125b-5p abrogated the effect of ECs-derived exosomes on ALI. TOP2A was confirmed as a direct target gene of miR-125b-5p.

Conclusion: Our study indicates that ECs-derived exosomes overexpressed miR-125b-5p to protect from sepsis-induced ALI by inhibiting TOP2A, which may contribute to ALI therapeutic strategies.

Keywords: Endothelial cells-derived exosome; MicroRNA-125b-5p; Sepsis-induced acute lung injury; Topoisomerase II alpha; Vascular endothelial growth factor.

MeSH terms

  • Acute Lung Injury / etiology
  • Acute Lung Injury / genetics*
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Animals
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cell Line
  • Cytokines / metabolism
  • DNA Topoisomerases, Type II / genetics*
  • DNA Topoisomerases, Type II / metabolism
  • Down-Regulation
  • Endothelial Cells*
  • Exosomes*
  • Female
  • Lung / metabolism
  • Lung / pathology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs*
  • Sepsis / complications
  • Sepsis / genetics*
  • Sepsis / metabolism
  • Sepsis / pathology
  • Up-Regulation
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Cytokines
  • MicroRNAs
  • Mirn125 microRNA, mouse
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • DNA Topoisomerases, Type II