Melatonin Ameliorates the Progression of Atherosclerosis via Mitophagy Activation and NLRP3 Inflammasome Inhibition

Oxid Med Cell Longev. 2018 Sep 4:2018:9286458. doi: 10.1155/2018/9286458. eCollection 2018.

Abstract

The NLRP3 (nucleotide-binding domain and leucine-rich repeat pyrin domain containing 3) inflammasome-mediated inflammatory responses are critically involved in the progression of atherosclerosis (AS), which is the essential cause for cardiovascular diseases. Melatonin has anti-inflammatory properties. However, little is known about the potential effects of melatonin in the pathological process of AS. Herein, we demonstrate that melatonin suppressed prolonged NLRP3 inflammasome activation in atherosclerotic lesions by reactive oxygen species (ROS) scavenging via mitophagy in macrophages. The atherosclerotic mouse model was induced with a high-fat diet using ApoE-/- mice. Melatonin treatment markedly attenuated AS plaque size and vulnerability. Furthermore, melatonin decreased NLRP3 inflammasome activation and the consequent IL-1β secretion within atherosclerotic lesions. Despite the unchanged protein expression, the silent information regulator 3 (Sirt3) activity was elevated in the atherosclerotic lesions in melatonin-treated mice. In ox-LDL-treated macrophages, melatonin attenuated the NLRP3 inflammasome activation and the inflammatory factors secretion, while this protective effect was abolished by either Sirt3 silence or autophagy inhibitor 3-MA. Mitochondrial ROS (mitoROS), which was a recognized inducer for NLRP3 inflammasome, was attenuated by melatonin through the induction of mitophagy. Both Sirt3-siRNA and autophagy inhibitor 3-MA partially abolished the beneficial effects of melatonin on mitoROS clearance and NLRP3 inflammasome activation, indicating the crucial role of Sirt3-mediated mitophagy. Furthermore, we demonstrated that melatonin protected against AS via the Sirt3/FOXO3a/Parkin signaling pathway. In conclusion, the current study demonstrated that melatonin prevented atherosclerotic progression, at least in part, via inducing mitophagy and attenuating NLRP3 inflammasome activation, which was mediated by the Sirt3/FOXO3a/Parkin signaling pathway. Collectively, our study provides insight into melatonin as a new target for therapeutic intervention for AS.

MeSH terms

  • Animals
  • Atherosclerosis / drug therapy*
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology*
  • Disease Progression*
  • Forkhead Box Protein O3 / metabolism
  • Free Radical Scavengers / metabolism
  • Inflammasomes / metabolism*
  • Lipoproteins, LDL / pharmacology
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / ultrastructure
  • Male
  • Melatonin / pharmacology
  • Melatonin / therapeutic use*
  • Mice
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondria / ultrastructure
  • Mitophagy*
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Plaque, Atherosclerotic / drug therapy
  • Plaque, Atherosclerotic / metabolism
  • Plaque, Atherosclerotic / pathology
  • RAW 264.7 Cells
  • Reactive Oxygen Species / metabolism
  • Sirtuin 3 / metabolism
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Forkhead Box Protein O3
  • FoxO3 protein, mouse
  • Free Radical Scavengers
  • Inflammasomes
  • Lipoproteins, LDL
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Reactive Oxygen Species
  • oxidized low density lipoprotein
  • Ubiquitin-Protein Ligases
  • parkin protein
  • Sirtuin 3
  • Melatonin