Exosomes regulate SIRT3-related autophagy by delivering miR-421 to regulate macrophage polarization and participate in OSA-related NAFLD

J Transl Med. 2024 May 19;22(1):475. doi: 10.1186/s12967-024-05283-8.

Abstract

Purpose: To analyze the role of and mechanism underlying obstructive sleep apnea (OSA)-derived exosomes in inducing non-alcoholic fatty liver (NAFLD).

Methods: The role of OSA-derived exosomes was analyzed in inducing hepatocyte fat accumulation in mice models both in vivo and in vitro.

Results: OSA-derived exosomes caused fat accumulation and macrophage activation in the liver tissue. These exosomes promoted fat accumulation; steatosis was more noticeable in the presence of macrophages. Macrophages could internalize OSA-derived exosomes, which promoted macrophage polarization to the M1 type. Moreover, it inhibited sirtuin-3 (SIRT3)/AMP-activated protein kinase (AMPK) and autophagy and promoted the activation of nucleotide-binding domain, leucine-rich-containing family, pyrin domain-containing-3 (NLRP3) inflammasomes. The use of 3-methyladenine (3-MA) to inhibit autophagy blocked NLRP3 inflammasome activation and inhibited the M1 polarization of macrophages. miR-421 targeting inhibited SIRT3 protein expression in the macrophages. miR-421 was significantly increased in OSA-derived exosomes. Additionally, miR-421 levels were increased in OSA + NAFLD mice- and patient-derived exosomes. In the liver tissues of OSA and OSA + NAFLD mice, miR-421 displayed similar co-localization with the macrophages. Intermittent hypoxia-induced hepatocytes deliver miR-421 to the macrophages via exosomes to inhibit SIRT3, thereby participating in macrophage M1 polarization. After OSA and NAFLD modeling in miR-421-/- mice, liver steatosis and M1 polarization were significantly reduced. Additionally, in the case of miR-421 knockout, the inhibitory effects of OSA-derived exosomes on SIRT3 and autophagy were significantly alleviated. Furthermore, their effects on liver steatosis and macrophage M1 polarization were significantly reduced.

Conclusions: OSA promotes the delivery of miR-421 from the hepatocytes to macrophages. Additionally, it promotes M1 polarization by regulating the SIRT3/AMPK-autophagy pathway, thereby causing NAFLD.

Keywords: Autophagy; Exosomes; Macrophages; Non-alcoholic fatty liver; Obstructive sleep apnea; SIRT3/AMPK; miR-421.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Autophagy*
  • Base Sequence
  • Cell Polarity*
  • Exosomes* / metabolism
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Humans
  • Inflammasomes / metabolism
  • Liver / metabolism
  • Liver / pathology
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Non-alcoholic Fatty Liver Disease* / complications
  • Non-alcoholic Fatty Liver Disease* / metabolism
  • Non-alcoholic Fatty Liver Disease* / pathology
  • Sirtuin 3* / genetics
  • Sirtuin 3* / metabolism
  • Sleep Apnea, Obstructive* / complications
  • Sleep Apnea, Obstructive* / metabolism

Substances

  • AMP-Activated Protein Kinases
  • Inflammasomes
  • MicroRNAs
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Sirtuin 3