Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways

Alzheimer’s disease (AD) is the most common form of dementia and a significant social and economic burden. Estrogens can exert neuroprotective effects and may contribute to the prevention, attenuation, or even delay in the onset of AD; however, long-term estrogen therapy is associated with harmful s...

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Main Authors: Qi Qiu, Xia Lei, Yueying Wang, Hui Xiong, Yanming Xu, Huifeng Sun, Hongdan Xu, Ning Zhang
Format: Article
Language:English
Published: Wiley 2023-01-01
Series:Behavioural Neurology
Online Access:http://dx.doi.org/10.1155/2023/1857330
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author Qi Qiu
Xia Lei
Yueying Wang
Hui Xiong
Yanming Xu
Huifeng Sun
Hongdan Xu
Ning Zhang
author_facet Qi Qiu
Xia Lei
Yueying Wang
Hui Xiong
Yanming Xu
Huifeng Sun
Hongdan Xu
Ning Zhang
author_sort Qi Qiu
collection DOAJ
description Alzheimer’s disease (AD) is the most common form of dementia and a significant social and economic burden. Estrogens can exert neuroprotective effects and may contribute to the prevention, attenuation, or even delay in the onset of AD; however, long-term estrogen therapy is associated with harmful side effects. Thus, estrogen alternatives are of interest for countering AD. Naringin, a phytoestrogen, is a key active ingredient in the traditional Chinese medicine Drynaria. Naringin is known to protect against nerve injury induced by amyloid beta-protein (Aβ) 25–35, but the underlying mechanisms of this protection are unclear. To investigate the mechanisms of naringin neuroprotection, we observed the protective effect on Aβ25–35-injured C57BL/6J mice’s learning and memory ability and hippocampal neurons. Then, an Aβ25–35 injury model was established with adrenal phaeochromocytoma (PC12) cells. We examined the effect of naringin treatment on Aβ25–35-injured PC12 cells and its relationship with estrogen receptor (ER), phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT), and glycogen synthase kinase (GSK)-3β signaling pathways. Estradiol (E2) was used as a positive control for neuroprotection. Naringin treatment resulted in improved learning and memory ability, the morphology of hippocampal neurons, increased cell viability, and reduced apoptosis. We next examined the expression of ERβ, p-AKT (Ser473, Thr308), AKT, p-GSK-3β (Ser9), GSK-3β, p-Tau (Thr231, Ser396), and Tau in PC12 cells treated with Aβ25–35 and either naringin or E2, with and without inhibitors of the ER, PI3K/AKT, and GSK-3β pathways. Our results demonstrated that naringin inhibits Aβ25–35-induced Tau hyperphosphorylation by modulating the ER, PI3K/AKT, and GSK-3β signaling pathways. Furthermore, the neuroprotective effects of naringin were comparable to those of E2 in all treatment groups. Thus, our results have furthered our understanding of naringin’s neuroprotective mechanisms and indicate that naringin may comprise a viable alternative to estrogen therapy.
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spelling doaj-art-ad2e52be97c647e7b17cfddc6d01f8572025-08-20T03:38:55ZengWileyBehavioural Neurology1875-85842023-01-01202310.1155/2023/1857330Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling PathwaysQi Qiu0Xia Lei1Yueying Wang2Hui Xiong3Yanming Xu4Huifeng Sun5Hongdan Xu6Ning Zhang7College of PharmacyCollege of JiamusiCollege of PharmacyCollege of PharmacyCollege of JiamusiCollege of PharmacyDepartment of PharmacyCollege of PharmacyAlzheimer’s disease (AD) is the most common form of dementia and a significant social and economic burden. Estrogens can exert neuroprotective effects and may contribute to the prevention, attenuation, or even delay in the onset of AD; however, long-term estrogen therapy is associated with harmful side effects. Thus, estrogen alternatives are of interest for countering AD. Naringin, a phytoestrogen, is a key active ingredient in the traditional Chinese medicine Drynaria. Naringin is known to protect against nerve injury induced by amyloid beta-protein (Aβ) 25–35, but the underlying mechanisms of this protection are unclear. To investigate the mechanisms of naringin neuroprotection, we observed the protective effect on Aβ25–35-injured C57BL/6J mice’s learning and memory ability and hippocampal neurons. Then, an Aβ25–35 injury model was established with adrenal phaeochromocytoma (PC12) cells. We examined the effect of naringin treatment on Aβ25–35-injured PC12 cells and its relationship with estrogen receptor (ER), phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT), and glycogen synthase kinase (GSK)-3β signaling pathways. Estradiol (E2) was used as a positive control for neuroprotection. Naringin treatment resulted in improved learning and memory ability, the morphology of hippocampal neurons, increased cell viability, and reduced apoptosis. We next examined the expression of ERβ, p-AKT (Ser473, Thr308), AKT, p-GSK-3β (Ser9), GSK-3β, p-Tau (Thr231, Ser396), and Tau in PC12 cells treated with Aβ25–35 and either naringin or E2, with and without inhibitors of the ER, PI3K/AKT, and GSK-3β pathways. Our results demonstrated that naringin inhibits Aβ25–35-induced Tau hyperphosphorylation by modulating the ER, PI3K/AKT, and GSK-3β signaling pathways. Furthermore, the neuroprotective effects of naringin were comparable to those of E2 in all treatment groups. Thus, our results have furthered our understanding of naringin’s neuroprotective mechanisms and indicate that naringin may comprise a viable alternative to estrogen therapy.http://dx.doi.org/10.1155/2023/1857330
spellingShingle Qi Qiu
Xia Lei
Yueying Wang
Hui Xiong
Yanming Xu
Huifeng Sun
Hongdan Xu
Ning Zhang
Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
Behavioural Neurology
title Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
title_full Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
title_fullStr Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
title_full_unstemmed Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
title_short Naringin Protects against Tau Hyperphosphorylation in Aβ25–35-Injured PC12 Cells through Modulation of ER, PI3K/AKT, and GSK-3β Signaling Pathways
title_sort naringin protects against tau hyperphosphorylation in aβ25 35 injured pc12 cells through modulation of er pi3k akt and gsk 3β signaling pathways
url http://dx.doi.org/10.1155/2023/1857330
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