lncR-GAS5 upregulates the splicing factor SRSF10 to impair endothelial autophagy, leading to atherogenesis

Front Med. 2023 Apr;17(2):317-329. doi: 10.1007/s11684-022-0931-4. Epub 2023 Jan 16.

Abstract

Long noncoding RNAs (lncRNAs) play a critical role in the regulation of atherosclerosis. Here, we investigated the role of the lncRNA growth arrest-specific 5 (lncR-GAS5) in atherogenesis. We found that the enforced expression of lncR-GAS5 contributed to the development of atherosclerosis, which presented as increased plaque size and reduced collagen content. Moreover, impaired autophagy was observed, as shown by a decreased LC3II/LC3I protein ratio and an elevated P62 level in lncR-GAS5-overexpressing human aortic endothelial cells. By contrast, lncR-GAS5 knockdown promoted autophagy. Moreover, serine/arginine-rich splicing factor 10 (SRSF10) knockdown increased the LC3II/LC3I ratio and decreased the P62 level, thus enhancing the formation of autophagic vacuoles, autolysosomes, and autophagosomes. Mechanistically, lncR-GAS5 regulated the downstream splicing factor SRSF10 to impair autophagy in the endothelium, which was reversed by the knockdown of SRSF10. Further results revealed that overexpression of the lncR-GAS5-targeted gene miR-193-5p promoted autophagy and autophagic vacuole accumulation by repressing its direct target gene, SRSF10. Notably, miR-193-5p overexpression decreased plaque size and increased collagen content. Altogether, these findings demonstrate that lncR-GAS5 partially contributes to atherogenesis and plaque instability by impairing endothelial autophagy. In conclusion, lncR-GAS5 overexpression arrested endothelial autophagy through the miR-193-5p/SRSF10 signaling pathway. Thus, miR-193-5p/SRSF10 may serve as a novel treatment target for atherosclerosis.

Keywords: atherogenesis; autophagy; lncR-GAS5; miR-193-5p; splicing factor SRSF10.

MeSH terms

  • Atherosclerosis* / genetics
  • Autophagy / genetics
  • Cell Cycle Proteins / metabolism
  • Endothelial Cells / metabolism
  • Endothelium / metabolism
  • Humans
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • RNA Splicing Factors
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • Repressor Proteins / metabolism
  • Serine-Arginine Splicing Factors / genetics

Substances

  • Cell Cycle Proteins
  • GAS5 long non-coding RNA, human
  • MicroRNAs
  • Repressor Proteins
  • RNA Splicing Factors
  • Serine-Arginine Splicing Factors
  • SRSF10 protein, human
  • RNA, Long Noncoding