Paeoniflorin exerts antidepressant-like effects through enhancing neuronal FGF-2 by microglial inactivation

J Ethnopharmacol. 2021 Jun 28:274:114046. doi: 10.1016/j.jep.2021.114046. Epub 2021 Mar 20.

Abstract

Ethnopharmacological relevance Paeonia lactiflora is a famous Traditional Chinese medicine widely used for immunological regulation. Paeoniflorin, the main component of Paeonia lactiflora, exerts neuroprotective and antidepressant-like effects in rodents.

Aim of the study: Fibroblast growth factor 2 (FGF-2) is essentially required in the central nervous system as it acts as both a neurotrophic factor and an anti-inflammatory factor participating in the regulation of proliferation, differentiation and apoptosis of neurons in the brain. However, it is unclear whether paeoniflorin could exert antidepressant effects via regulating FGF-2.

Materials and methods: In the present study, the effects of paeoniflorin were evaluated in depressive mice induced by the endotoxin lipopolysaccharide (LPS) injection.

Results: The results showed that paeoniflorin markedly increased sucrose preference and reduced immobility time in LPS mice, indicating antidepressant effects. Consistent with the results from molecular docking showing paeoniflorin antagonizes TLR4, NF-κB and NLRP3, the biochemical analysis also indicated paeoniflorin inhibited TLR4/NF-κB/NLRP3 signaling, decreased proinflammatory cytokine levels and microglial activation in the hippocampus of LPS induced mice. In addition, the levels of neuronal FGF-2 and the density of dendritic spine were improved by paeoniflorin. More importantly, the FGFR1 inhibitor SU5402 prevented the antidepressant effects of paeoniflorin and blocked the neuroinflammatory and neurogenic regulatory effects of paeoniflorin, indicating that FGF-2/FGFR1 activation was required for the effects of paeoniflorin.

Conclusion: Taken together, the results demonstrate that paeoniflorin exhibits neuroprotective and antidepressant effects in mice, which may be mediated by activating neuronal FGF-2/FGFR1 signaling via the inhibition of microglial activation in the hippocampus.

Keywords: Antidepressant; FGF-2; Microglia; Neuroinflammation; Paeoniflorin.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Anti-Inflammatory Agents / therapeutic use*
  • Antidepressive Agents / pharmacology
  • Antidepressive Agents / therapeutic use*
  • Calcium-Binding Proteins / metabolism
  • Cyclooxygenase 2 / metabolism
  • Cytokines / metabolism
  • Depression / chemically induced
  • Depression / drug therapy*
  • Depression / metabolism
  • Fibroblast Growth Factor 2 / metabolism
  • Glucosides / pharmacology
  • Glucosides / therapeutic use*
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Lipopolysaccharides
  • Lymphocyte Antigen 96 / metabolism
  • Male
  • Mice
  • Mice, Inbred ICR
  • Microfilament Proteins / metabolism
  • Microglia / drug effects
  • Molecular Docking Simulation
  • Monoterpenes / pharmacology
  • Monoterpenes / therapeutic use*
  • NF-kappa B / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Neurons / drug effects
  • Neurons / metabolism
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use*
  • Toll-Like Receptor 4 / metabolism

Substances

  • Aif1 protein, mouse
  • Anti-Inflammatory Agents
  • Antidepressive Agents
  • Calcium-Binding Proteins
  • Cytokines
  • Glucosides
  • Lipopolysaccharides
  • Lymphocyte Antigen 96
  • Microfilament Proteins
  • Monoterpenes
  • NF-kappa B
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Neuroprotective Agents
  • Toll-Like Receptor 4
  • Fibroblast Growth Factor 2
  • peoniflorin
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2