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Antidepressant-like effect of ginsenoside Rb1 on potentiating synaptic plasticity via the miR-134-mediated BDNF

Guoli Wang¹, Tianyue An¹, Cong Lei¹

¹College of Pharmacy, Jinan University, Guangzhou, China.

Journal of Ginseng Research

|May 23, 2022

Abstract

Background:

Brain-derived neurotrophic factor (BDNF)-tropomyosin-related kinase B (TrkB) plays a critical role in the pathogenesis of depression by modulating synaptic structural remodeling and functional transmission. Previously, we have demonstrated that the ginsenoside Rb1 (Rb1) presents a novel antidepressant-like effect via BDNF-TrkB signaling in the hippocampus of chronic unpredictable mild stress (CUMS)-exposed mice. However, the underlying mechanism through which Rb1 counteracts stress-induced aberrant hippocampal synaptic plasticity via BDNF-TrkB signaling remains elusive.

Methods:

We focused on hippocampal microRNAs (miRNAs) that could directly bind to BDNF and are regulated by Rb1 to explore the possible synaptic plasticity-dependent mechanism of Rb1, which affords protection against CUMS-induced depression-like effects.

Results:

Herein, we observed that brain-specific miRNA-134 (miR-134) could directly bind to BDNF 3'UTR and was markedly downregulated by Rb1 in the hippocampus of CUMS-exposed mice. Furthermore, the hippocampus-targeted miR-134 overexpression substantially blocked the antidepressant-like effects of Rb1 during behavioral tests, attenuating the effects on neuronal nuclei-immunoreactive neurons, the density of dendritic spines, synaptic ultrastructure, long-term potentiation, and expression of synapse-associated proteins and BDNF-TrkB signaling proteins in the hippocampus of CUMS-exposed mice.

Conclusion:

These data provide strong evidence that Rb1 rescued CUMS-induced depression-like effects by modulating hippocampal synaptic plasticity via the miR-134-mediated BDNF signaling pathway.

Keywords:

AAV9, adeno-associated viral serotype 9 AKT, protein kinase B AMPAR, α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor ANOVA, analysis of variance BDNF, brain-derived neurotrophic factor BDNF–TrkB signaling CMC-Na, carboxymethyl cellulose sodium CREB, cAMP response element-binding protein CUMS, chronic unpredictable mild stress CaMKII, Ca2+/calmodulin-dependent protein kinase II DG, dentate gyrus Depression ERK1/2, extracellular regulatory protein kinase FST, forced swimming test GAP-43, growth-associated protein 43 GSK-3β, glycogen synthase kinase-3β Ginsenoside Rb1 GluR1, AMPAR subunit glutamate receptor 1 HFS, high-frequency stimulation IACUC, Institutional Animal Care and Use Committee ICR, Institute of Cancer Research LIMK1, LIM-kinase 1 LTD, long-term depression LTP, long-term potentiation MAP-2, microtubule-associated protein-2 MAPK, mitogen-activated protein kinase MDD, major depressive disorder NMDAR, N-methyl-D-aspartic acid receptor NR2A, NMDAR subunit 2A NR2B, NMDAR subunit 2B NeuN, neuronal nuclei OFT, open field test PI3K, phosphatidylinositol 3-kinase PSD, postsynaptic density PSD-95, postsynaptic density protein 95 Rb1, ginsenoside Rb1 SEM, standard error of the mean SPT, sucrose preference test Syn, synaptophysin Synaptic plasticity TST, tail suspension test TrkB, tropomyosin-related kinase B fEPSPs, field excitatory postsynaptic potentials i.g., intragastrically miR-134 miR-134, miRNA-134 miRNAs, microRNAs qRT-PCR, quantitative real-time PCR

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