MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats

Abstract Major depressive disorder (MDD) is usually considered associate with immune inflammation and synaptic injury within specific brain regions. However, the molecular mechanisms underlying the neural deterioration resulting in depression remain unclear. Here, it is found that miR‐204‐5p is mark...

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Main Authors: Xiao Chen, Yeting Gan, Kaiqi Zhang, Yuhan Wu, Ye Li, Tian Lan, Xianghua Zhuang, Shihong Chen, Shuyan Yu
Format: Article
Language:English
Published: Wiley 2025-03-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202403080
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author Xiao Chen
Yeting Gan
Kaiqi Zhang
Yuhan Wu
Ye Li
Tian Lan
Xianghua Zhuang
Shihong Chen
Shuyan Yu
author_facet Xiao Chen
Yeting Gan
Kaiqi Zhang
Yuhan Wu
Ye Li
Tian Lan
Xianghua Zhuang
Shihong Chen
Shuyan Yu
author_sort Xiao Chen
collection DOAJ
description Abstract Major depressive disorder (MDD) is usually considered associate with immune inflammation and synaptic injury within specific brain regions. However, the molecular mechanisms underlying the neural deterioration resulting in depression remain unclear. Here, it is found that miR‐204‐5p is markedly downregulated in the ventromedial prefrontal cortex (vmPFC) in a chronic unpredictable mild stress (CUMS) induce rat model of depression. Knockdown of miR‐204‐5p in the vmPFC of normal rats results in depression and anxiety‐like behaviors accompanied with the activation of microglia, elevated levels of pro‐inflammatory cytokines, and increased numbers of neural apoptotic cells, effects which appear to be mediated by activation of the JAK2/STAT3 signaling pathway. Electrophysiological recordings further demonstrate that knockdown of miR‐204‐5p induces abnormal excitability of pyramidal neurons. In contrast, upregulation of miR‐204‐5p in the vmPFC of CUMS rats significantly causes inhibition of JAK2/STAT3 signaling pathway, improvements in neuronal impairments, and an abolition of the depression and anxiety‐like behaviors. Moreover, pharmacological blocking of the JAK2/STAT3 signaling pathway significantly ameliorates abnormal behaviors resulting from miR‐204‐5p deficiency within the vmPFC. Collectively, these results provide robust evidence that the miR‐204‐5p/JAK2/STAT3 pathway may critically involve in the pathogenesis of depression, which may serve as potentially critical therapeutic target in the treatment of MDD.
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spelling doaj-art-62371cc771d040faa02accf8b189a6f32025-08-20T03:10:53ZengWileyAdvanced Science2198-38442025-03-011210n/an/a10.1002/advs.202403080MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in RatsXiao Chen0Yeting Gan1Kaiqi Zhang2Yuhan Wu3Ye Li4Tian Lan5Xianghua Zhuang6Shihong Chen7Shuyan Yu8Key Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaDepartment of Endocrinology and Metabolism The Second Hospital of Shandong University Jinan Shandong 250033 ChinaDepartment of Endocrinology and Metabolism The Second Hospital of Shandong University Jinan Shandong 250033 ChinaKey Laboratory of Mental Disorders The Second Hospital of Shandong University School of Basic Medical Sciences Shandong University Jinan Shandong 250012 ChinaAbstract Major depressive disorder (MDD) is usually considered associate with immune inflammation and synaptic injury within specific brain regions. However, the molecular mechanisms underlying the neural deterioration resulting in depression remain unclear. Here, it is found that miR‐204‐5p is markedly downregulated in the ventromedial prefrontal cortex (vmPFC) in a chronic unpredictable mild stress (CUMS) induce rat model of depression. Knockdown of miR‐204‐5p in the vmPFC of normal rats results in depression and anxiety‐like behaviors accompanied with the activation of microglia, elevated levels of pro‐inflammatory cytokines, and increased numbers of neural apoptotic cells, effects which appear to be mediated by activation of the JAK2/STAT3 signaling pathway. Electrophysiological recordings further demonstrate that knockdown of miR‐204‐5p induces abnormal excitability of pyramidal neurons. In contrast, upregulation of miR‐204‐5p in the vmPFC of CUMS rats significantly causes inhibition of JAK2/STAT3 signaling pathway, improvements in neuronal impairments, and an abolition of the depression and anxiety‐like behaviors. Moreover, pharmacological blocking of the JAK2/STAT3 signaling pathway significantly ameliorates abnormal behaviors resulting from miR‐204‐5p deficiency within the vmPFC. Collectively, these results provide robust evidence that the miR‐204‐5p/JAK2/STAT3 pathway may critically involve in the pathogenesis of depression, which may serve as potentially critical therapeutic target in the treatment of MDD.https://doi.org/10.1002/advs.202403080JAK2/STAT3 signaling pathwayMDDmiR‐204‐5pneuroinflammationneuronal apoptosissynaptic plasticity
spellingShingle Xiao Chen
Yeting Gan
Kaiqi Zhang
Yuhan Wu
Ye Li
Tian Lan
Xianghua Zhuang
Shihong Chen
Shuyan Yu
MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
Advanced Science
JAK2/STAT3 signaling pathway
MDD
miR‐204‐5p
neuroinflammation
neuronal apoptosis
synaptic plasticity
title MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
title_full MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
title_fullStr MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
title_full_unstemmed MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
title_short MicroRNA‐204‐5p Deficiency within the vmPFC Region Contributes to Neuroinflammation and Behavioral Disorders via the JAK2/STAT3 Signaling Pathway in Rats
title_sort microrna 204 5p deficiency within the vmpfc region contributes to neuroinflammation and behavioral disorders via the jak2 stat3 signaling pathway in rats
topic JAK2/STAT3 signaling pathway
MDD
miR‐204‐5p
neuroinflammation
neuronal apoptosis
synaptic plasticity
url https://doi.org/10.1002/advs.202403080
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