Compound 4f, a novel brain-penetrant reversible monoacylglycerol inhibitor, ameliorates neuroinflammation, neuronal cell loss, and cognitive impairment in mice with kainic acid-induced neurodegeneration

PLoS One. 2024 Nov 21;19(11):e0312090. doi: 10.1371/journal.pone.0312090. eCollection 2024.

Abstract

Neuroinflammation, a hallmark of neurodegenerative diseases, is associated with neuronal cell loss and cognitive dysfunction. Monoacylglycerol lipase (MAGL) is involved in neuroinflammation in the brain via the degradation of endocannabinoid 2-arachidonoylglycerol to arachidonic acid, a precursor of some eicosanoids; therefore, MAGL inhibitors are expected to have anti-inflammatory effects. We recently developed a reversible, selective, central nervous system penetrant, and orally available MAGL inhibitor, compound 4f. Compound 4f (1 mg/kg) robustly increased 2-arachidonoylglycerol levels and decreased arachidonic acid levels in the mouse brain. To examine whether compound 4f can suppress neuroinflammation and neuronal cell loss, kainic acid (KA)-injected mice were used as a neuroinflammation model in this study. Compound 4f (1 mg/kg) significantly decreased the cytokine and chemokine expression levels and suppressed neuronal cell loss in the hippocampi of mice. Compound 4f also ameliorated cognitive impairment in KA-injected mice. The cannabinoid receptor 1 antagonist, AM251, and cannabinoid receptor 2 antagonist, AM630, partly blocked the neuroprotective effects of compound 4f in the hippocampi of KA-injected mice. Gene expression profiles and pathway analyses revealed that compound 4f reversed the KA-induced changes in the expression of genes related to inflammation and neurotransmission. These results indicate that the selective and reversible MAGL inhibitor, compound 4f, can be used as a potential therapeutic agent for the treatment of neurodegenerative diseases.

MeSH terms

  • Animals
  • Arachidonic Acids / metabolism
  • Brain / drug effects
  • Brain / metabolism
  • Brain / pathology
  • Cognitive Dysfunction* / chemically induced
  • Cognitive Dysfunction* / drug therapy
  • Cognitive Dysfunction* / metabolism
  • Cytokines / metabolism
  • Endocannabinoids / metabolism
  • Enzyme Inhibitors / pharmacology
  • Glycerides / metabolism
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Kainic Acid* / toxicity
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Monoacylglycerol Lipases* / antagonists & inhibitors
  • Monoacylglycerol Lipases* / metabolism
  • Neurodegenerative Diseases / chemically induced
  • Neurodegenerative Diseases / drug therapy
  • Neurodegenerative Diseases / metabolism
  • Neuroinflammatory Diseases* / drug therapy
  • Neuroinflammatory Diseases* / metabolism
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Neurons* / pathology
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use
  • Piperidines / pharmacology
  • Piperidines / therapeutic use

Substances

  • Kainic Acid
  • Monoacylglycerol Lipases
  • Arachidonic Acids
  • Glycerides
  • Endocannabinoids
  • glyceryl 2-arachidonate
  • Piperidines
  • Enzyme Inhibitors
  • Neuroprotective Agents
  • Cytokines

Grants and funding

This work was supported by Takeda Pharmaceutical Company Limited, which employed all authors, and received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. There was no additional external funding received for this study.