Peroxynitrite-Triggered Carbon Monoxide Donor Improves Ischemic Stroke Outcome by Inhibiting Neuronal Apoptosis and Ferroptosis

Mol Neurobiol. 2024 Dec;61(12):10629-10644. doi: 10.1007/s12035-024-04238-w. Epub 2024 May 20.

Abstract

Cerebral ischemia-reperfusion injury produces excessive reactive oxygen and nitrogen species, including superoxide, nitric oxide, and peroxynitrite (ONOO-). We recently developed a new ONOO--triggered metal-free carbon monoxide donor (PCOD585), exhibiting a notable neuroprotective outcome on the rat middle cerebral artery occlusion model and rendering an exciting intervention opportunity toward ischemia-induced brain injuries. However, its therapeutic mechanism still needs to be addressed. In the pharmacological study, we found PCOD585 inhibited neuronal Bcl2/Bax/caspase-3 apoptosis pathway in the peri-infarcted area of stroke by scavenging ONOO-. ONOO- scavenging further led to decreased Acyl-CoA synthetase long-chain family member 4 and increased glutathione peroxidase 4, to minimize lipoperoxidation. Additionally, the carbon monoxide release upon the ONOO- reaction with PCOD585 further inhibited the neuronal Iron-dependent ferroptosis associated with ischemia-reperfusion. Such a synergistic neuroprotective mechanism of PCOD585 yields as potent a neuroprotective effect as Edaravone. Additionally, PCOD585 penetrates the blood-brain barrier and reduces the degradation of zonula occludens-1 by inhibiting matrix metalloproteinase-9, thereby protecting the integrity of the blood-brain barrier. Our study provides a new perspective for developing multi-functional compounds to treat ischemic stroke.

Keywords: Anti-lipid peroxidation; Carbon monoxide; Ferroptosis; Iron homeostasis; Ischemic/reperfusion injury.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology
  • Carbon Monoxide* / metabolism
  • Carbon Monoxide* / pharmacology
  • Ferroptosis* / drug effects
  • Infarction, Middle Cerebral Artery / drug therapy
  • Infarction, Middle Cerebral Artery / pathology
  • Ischemic Stroke* / drug therapy
  • Ischemic Stroke* / metabolism
  • Ischemic Stroke* / pathology
  • Male
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Neurons* / pathology
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use
  • Peroxynitrous Acid* / metabolism
  • Rats
  • Rats, Sprague-Dawley*
  • Treatment Outcome

Substances

  • Peroxynitrous Acid
  • Carbon Monoxide
  • Neuroprotective Agents