Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease

Long noncoding RNA and microRNA are regulatory noncoding RNAs that are implicated in Alzheimer’s disease, but the role of long noncoding RNA-associated competitive endogenous RNA has not been fully elucidated. The long noncoding RNA growth arrest-specific 5 (GAS5) is a member of the 5′-terminal olig...

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Main Authors: Li Zeng, Kaiyue Zhao, Jianghong Liu, Mimin Liu, Zhongdi Cai, Ting Sun, Zhuorong Li, Rui Liu
Format: Article
Language:English
Published: Wolters Kluwer Medknow Publications 2026-01-01
Series:Neural Regeneration Research
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Online Access:https://journals.lww.com/10.4103/NRR.NRR-D-23-01273
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author Li Zeng
Kaiyue Zhao
Jianghong Liu
Mimin Liu
Zhongdi Cai
Ting Sun
Zhuorong Li
Rui Liu
author_facet Li Zeng
Kaiyue Zhao
Jianghong Liu
Mimin Liu
Zhongdi Cai
Ting Sun
Zhuorong Li
Rui Liu
author_sort Li Zeng
collection DOAJ
description Long noncoding RNA and microRNA are regulatory noncoding RNAs that are implicated in Alzheimer’s disease, but the role of long noncoding RNA-associated competitive endogenous RNA has not been fully elucidated. The long noncoding RNA growth arrest-specific 5 (GAS5) is a member of the 5′-terminal oligopyrimidine gene family that may be involved in neurological disorders, but its role in Alzheimer’s disease remains unclear. This study aimed to investigate the function of GAS5 and construct a GAS5-associated competitive endogenous RNA network comprising potential targets. RNA sequencing results showed that GAS5 was upregulated in five familial Alzheimer’s disease (5×FAD) mice, APPswe/PSEN1dE9 (APP/PS1) mice, Alzheimer’s disease-related APPswe cells, and serum from patients with Alzheimer’s disease. Functional experiments with targeted overexpression and silencing demonstrated that GAS5 played a role in cognitive dysfunction and multiple Alzheimer’s disease-associated pathologies, including tau hyperphosphorylation, amyloid-beta accumulation, and neuronal apoptosis. Mechanistic studies indicated that GAS5 acted as an endogenous sponge by competing for microRNA-23b-3p (miR-23b-3p) binding to regulate its targets glycogen synthase kinase 3beta (GSK-3β) and phosphatase and tensin homologue deleted on chromosome 10 (PTEN) expression in an Argonaute 2-induced RNA silencing complex (RISC)-dependent manner. GAS5 inhibited miR-23b-3p-mediated GSK-3β and PTEN cascades with a feedforward PTEN/protein kinase B (Akt)/GSK-3β linkage. Furthermore, recovery of GAS5/miR-23b-3p/GSK-3β/PTEN pathways relieved Alzheimer’s disease-like symptoms in vivo, indicated by the amelioration of spatial cognition, neuronal degeneration, amyloid-beta load, and tau phosphorylation. Together, these findings suggest that GAS5 promotes Alzheimer’s disease pathogenesis. This study establishes the functional convergence of the GAS5/miR-23b-3p/GSK-3β/PTEN pathway on multiple pathologies, suggesting a candidate therapeutic target in Alzheimer’s disease.
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spelling doaj-art-c337f78de84c4418b0991e50843eee672025-08-20T03:07:54ZengWolters Kluwer Medknow PublicationsNeural Regeneration Research1673-53741876-79582026-01-0121139240510.4103/NRR.NRR-D-23-01273Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s diseaseLi ZengKaiyue ZhaoJianghong LiuMimin LiuZhongdi CaiTing SunZhuorong LiRui LiuLong noncoding RNA and microRNA are regulatory noncoding RNAs that are implicated in Alzheimer’s disease, but the role of long noncoding RNA-associated competitive endogenous RNA has not been fully elucidated. The long noncoding RNA growth arrest-specific 5 (GAS5) is a member of the 5′-terminal oligopyrimidine gene family that may be involved in neurological disorders, but its role in Alzheimer’s disease remains unclear. This study aimed to investigate the function of GAS5 and construct a GAS5-associated competitive endogenous RNA network comprising potential targets. RNA sequencing results showed that GAS5 was upregulated in five familial Alzheimer’s disease (5×FAD) mice, APPswe/PSEN1dE9 (APP/PS1) mice, Alzheimer’s disease-related APPswe cells, and serum from patients with Alzheimer’s disease. Functional experiments with targeted overexpression and silencing demonstrated that GAS5 played a role in cognitive dysfunction and multiple Alzheimer’s disease-associated pathologies, including tau hyperphosphorylation, amyloid-beta accumulation, and neuronal apoptosis. Mechanistic studies indicated that GAS5 acted as an endogenous sponge by competing for microRNA-23b-3p (miR-23b-3p) binding to regulate its targets glycogen synthase kinase 3beta (GSK-3β) and phosphatase and tensin homologue deleted on chromosome 10 (PTEN) expression in an Argonaute 2-induced RNA silencing complex (RISC)-dependent manner. GAS5 inhibited miR-23b-3p-mediated GSK-3β and PTEN cascades with a feedforward PTEN/protein kinase B (Akt)/GSK-3β linkage. Furthermore, recovery of GAS5/miR-23b-3p/GSK-3β/PTEN pathways relieved Alzheimer’s disease-like symptoms in vivo, indicated by the amelioration of spatial cognition, neuronal degeneration, amyloid-beta load, and tau phosphorylation. Together, these findings suggest that GAS5 promotes Alzheimer’s disease pathogenesis. This study establishes the functional convergence of the GAS5/miR-23b-3p/GSK-3β/PTEN pathway on multiple pathologies, suggesting a candidate therapeutic target in Alzheimer’s disease.https://journals.lww.com/10.4103/NRR.NRR-D-23-01273alzheimer’s diseaseamyloid-beta peptide accumulationcognitive dysfunctioncompetitive endogenous rnaglycogen synthase kinase 3betalncrna growth arrest-specific 5microrna-23b-3pneuronal apoptosisphosphatase and tensin homologue deleted on chromosome 10tau phosphorylation
spellingShingle Li Zeng
Kaiyue Zhao
Jianghong Liu
Mimin Liu
Zhongdi Cai
Ting Sun
Zhuorong Li
Rui Liu
Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
Neural Regeneration Research
alzheimer’s disease
amyloid-beta peptide accumulation
cognitive dysfunction
competitive endogenous rna
glycogen synthase kinase 3beta
lncrna growth arrest-specific 5
microrna-23b-3p
neuronal apoptosis
phosphatase and tensin homologue deleted on chromosome 10
tau phosphorylation
title Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
title_full Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
title_fullStr Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
title_full_unstemmed Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
title_short Long noncoding RNA GAS5 acts as a competitive endogenous RNA to regulate GSK-3β and PTEN expression by sponging miR-23b-3p in Alzheimer’s disease
title_sort long noncoding rna gas5 acts as a competitive endogenous rna to regulate gsk 3β and pten expression by sponging mir 23b 3p in alzheimer s disease
topic alzheimer’s disease
amyloid-beta peptide accumulation
cognitive dysfunction
competitive endogenous rna
glycogen synthase kinase 3beta
lncrna growth arrest-specific 5
microrna-23b-3p
neuronal apoptosis
phosphatase and tensin homologue deleted on chromosome 10
tau phosphorylation
url https://journals.lww.com/10.4103/NRR.NRR-D-23-01273
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