Melatonin Reduces Mito-Inflammation in Ischaemic Hippocampal HT22 Cells and Modulates the cGAS-STING Cytosolic DNA Sensing Pathway and FGF21 Release

J Cell Mol Med. 2024 Dec;28(24):e70285. doi: 10.1111/jcmm.70285.

Abstract

Mitochondrial dysfunction is a key event in many pathological conditions, including neurodegenerative processes. When mitochondria are damaged, they release damage-associated molecular patterns (DAMPs) that activate mito-inflammation. The present study assessed mito-inflammation after in vitro oxygen-glucose deprivation as a representation of ischaemia, followed by reoxygenation (OGD/R) of HT22 cells and modulation of the inflammatory response by melatonin. We observed that melatonin prevented mitochondrial structural damage and dysfunction caused by OGD/R. Melatonin reduced oxidative damage and preserved the enzymatic activity for complexes I, III and IV, encoded by mitochondrial DNA, which were reduced by OGD/R. No effect was observed on complex II activity encoded by nuclear DNA. The release of mtDNA into the cytosol was also prevented with a consequent reduction of the cGAS-STING pathway and IFNβ and IL-6 production. Interestingly, melatonin also increased the early release of the fibroblast growth factor-21 (FGF-21), a mitokine secreted in response to mitochondrial stress. These data indicate that melatonin reduces mito-inflammation and modulates FGF-21 release, further highlighting the key role of this molecule in preserving mitochondrial integrity in OGD/R deprivation-type ischaemic brain injury.

Keywords: FGF‐21; HT22; melatonin; mito‐inflammation; mtDNA; oxygen–glucose deprivation.

MeSH terms

  • Animals
  • Brain Ischemia / drug therapy
  • Brain Ischemia / metabolism
  • Brain Ischemia / pathology
  • Cell Line
  • Cytosol* / drug effects
  • Cytosol* / metabolism
  • DNA, Mitochondrial* / metabolism
  • Fibroblast Growth Factors* / metabolism
  • Hippocampus* / drug effects
  • Hippocampus* / metabolism
  • Hippocampus* / pathology
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Interleukin-6 / metabolism
  • Ischemia / metabolism
  • Melatonin* / pharmacology
  • Membrane Proteins* / metabolism
  • Mice
  • Mitochondria* / drug effects
  • Mitochondria* / metabolism
  • Nucleotidyltransferases* / metabolism
  • Oxidative Stress / drug effects
  • Signal Transduction* / drug effects

Substances

  • Melatonin
  • Membrane Proteins
  • Nucleotidyltransferases
  • DNA, Mitochondrial
  • Fibroblast Growth Factors
  • cGAS protein, mouse
  • fibroblast growth factor 21
  • Sting1 protein, mouse
  • Interleukin-6