Matrine alleviates neurobehavioral alterations via modulation of JNK-mediated caspase-3 and BDNF/VEGF signaling in a mouse model of burn injury

Psychopharmacology (Berl). 2020 Aug;237(8):2327-2343. doi: 10.1007/s00213-020-05537-5. Epub 2020 May 12.

Abstract

Rationale: The c-Jun N-terminal kinase (JNK) pathway and neurotrophic factor dysregulation play a critical role in the pathogenesis of neurobehavioral disorders (anxiety and depression). Targeting the JNK pathway and BDNF/VEGF signaling may signify a new avenue for the treatment of neurobehavioral disorders.

Objectives: The present study investigated the effect of matrine (Mat) against anxiety- and depressive-like emotional status in an acute mouse model of burn injury and explores its underlying mechanism.

Methods: In the mouse model of thermal injury, anxiety- and depression-related behaviors were evaluated using the elevated plus-maze test, the light-dark box test, the open-field test, the forced swimming test, and the tail suspension test. The JNK/caspase-3 and BDNF/VEGF proteins were determined by immunohistochemistry. Additionally, proinflammatory cytokine, antioxidant, nitric oxide, and corticosterone levels were also measured.

Results: The results showed that treatment with Mat significantly improves anxiety- and depressive-like behaviors. It remarkably reduced the levels of proinflammatory cytokines, malondialdehyde, and nitric oxide in the hippocampus and prefrontal cortex of a mouse brain. It considerably improved burn-induced alteration in the antioxidant status, corticosterone, and BDNF/VEGF. It also inhibited burn-induced apoptotic signaling by downregulating the expression of JNK/caspase-3. Similarly, it prevented DNA damage and histopathological changes in the dentate gyrus of the hippocampus. Furthermore, molecular docking results showed that Mat possess better binding affinity for JNK/caspase-3 and BDNF/VEGF proteins.

Conclusions: These findings provide convincing evidence that Mat improves anxiety- and depressive-like emotional status through modulation of JNK-mediated inflammatory, oxidative stress, apoptotic, and BDNF/VEGF signaling in an acute mouse model of burn injury.

Keywords: BDNF/VEGF; Burn; JNK; Mat; Neurobehavioral disorders.

MeSH terms

  • Alkaloids / metabolism*
  • Alkaloids / pharmacology
  • Alkaloids / therapeutic use
  • Animals
  • Anti-Anxiety Agents / metabolism
  • Anti-Anxiety Agents / pharmacology
  • Anti-Anxiety Agents / therapeutic use
  • Anxiety / drug therapy
  • Anxiety / metabolism
  • Brain-Derived Neurotrophic Factor / antagonists & inhibitors
  • Brain-Derived Neurotrophic Factor / metabolism*
  • Burns / drug therapy
  • Burns / metabolism*
  • Caspase 3 / metabolism*
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology*
  • Male
  • Matrines
  • Maze Learning / drug effects
  • Maze Learning / physiology
  • Mice
  • Molecular Docking Simulation / methods
  • Oxidative Stress / drug effects
  • Oxidative Stress / physiology
  • Quinolizines / metabolism*
  • Quinolizines / pharmacology
  • Quinolizines / therapeutic use
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Vascular Endothelial Growth Factor A / metabolism*

Substances

  • Alkaloids
  • Anti-Anxiety Agents
  • Bdnf protein, mouse
  • Brain-Derived Neurotrophic Factor
  • Quinolizines
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Caspase 3
  • Matrines