MiR-199a-5p-containing macrophage-derived extracellular vesicles inhibit SMARCA4 and alleviate atherosclerosis by reducing endothelial cell pyroptosis

Cell Biol Toxicol. 2023 Jun;39(3):591-605. doi: 10.1007/s10565-022-09732-2. Epub 2022 Aug 5.

Abstract

Background: Endothelial cell disturbance underpins a role in pathogenesis of atherosclerosis. Notably, accumulating studies indicate the substantial role of microRNAs (miRs) in atherosclerosis, and miR-199a-5p dysregulation has been associated with atherosclerosis and other cardiovascular disorders. However, the effect of miR-199a-5p on the phenotypes of endothelial cells and atherosclerosis remains largely unknown.

Methods: ApoE-/- male mice were fed with high-fat diet for detection of inflammation and aorta plaque area. Extracellular vesicles (EVs) were separated from THP-1-derived macrophage (THP-1-DM) that was treated by oxidized low-density lipoprotein, followed by co-culture with human aortic endothelial cells (HAECs). Ectopic expression and downregulation of miR-199a-5p were done in THP-1-DM-derived EVs to assess pyroptosis and lactate dehydrogenase (LDH) of HAECs. Binding relationship between miR-199a-5p and SMARCA4 was evaluated by luciferase activity assay.

Results: EVs derived from ox-LDL-induced THP-1-DM expedited inflammation and aorta plaque area in atherosclerotic mice. Besides, miR-199a-5p expression was reduced in EVs from ox-LDL-induced THP-1-DM, and miR-199a-5p inhibition facilitated HAEC pyroptosis and LDH activity. Moreover, miR-199a-5p targeted and restricted SMARCA4, and then SMARCA4 activated the NF-κB pathway by increasing PODXL expression in HAECs.

Conclusion: EV-packaged inhibited miR-199a-5p from macrophages expedites endothelial cell pyroptosis and further accelerates atherosclerosis through the SMARCA4/PODXL/NF-κB axis, providing promising targets and strategies for the prevention and treatment of atherosclerosis.

Keywords: Atherosclerosis; Extracellular vesicles; Macrophage; NF-κB pathway; PODXL; Pyroptosis; SMARCA4; miR-199a-5p.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atherosclerosis* / genetics
  • Atherosclerosis* / metabolism
  • Atherosclerosis* / pathology
  • DNA Helicases / metabolism
  • DNA Helicases / pharmacology
  • Endothelial Cells / metabolism
  • Extracellular Vesicles*
  • Humans
  • Inflammation / metabolism
  • Macrophages / metabolism
  • Male
  • Mice
  • MicroRNAs* / metabolism
  • NF-kappa B / metabolism
  • Nuclear Proteins / metabolism
  • Pyroptosis
  • Signal Transduction
  • Transcription Factors / metabolism

Substances

  • DNA Helicases
  • MicroRNAs
  • NF-kappa B
  • Nuclear Proteins
  • SMARCA4 protein, human
  • Transcription Factors
  • Smarca4 protein, mouse