Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice

Abstract Background Neuroinflammation is closely associated with the pathological progression of Alzheimer's disease (AD). The α1-adrenergic receptor (ADRA1), a G protein-coupled receptor, has been identified as a critical therapeutic target in inflammatory disorders. However, its precise mecha...

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Main Authors: Bo Li, Li Wang, Yan Xiao, Zhi Tang, Yang Wang, Ting Sun, Xiaolan Qi
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Journal of Neuroinflammation
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Online Access:https://doi.org/10.1186/s12974-025-03506-3
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author Bo Li
Li Wang
Yan Xiao
Zhi Tang
Yang Wang
Ting Sun
Xiaolan Qi
author_facet Bo Li
Li Wang
Yan Xiao
Zhi Tang
Yang Wang
Ting Sun
Xiaolan Qi
author_sort Bo Li
collection DOAJ
description Abstract Background Neuroinflammation is closely associated with the pathological progression of Alzheimer's disease (AD). The α1-adrenergic receptor (ADRA1), a G protein-coupled receptor, has been identified as a critical therapeutic target in inflammatory disorders. However, its precise mechanistic role in AD pathogenesis remains unclear. Methods To investigate ADRA1's role in AD, we employed 3xTg-AD and wild-type (WT) mice, modulating neuronal ADRA1 expression via intracerebroventricular delivery of adeno-associated viruses. Cognitive function, tau pathology, neuronal morphology, and activation of the STING/NF-κB/NLRP3 signaling pathway were evaluated using behavioral tests, Western blot, Golgi-Cox staining, immunohistochemistry, and immunofluorescence. In vitro AD models were established using Aβ42 oligomer-stimulated SH-SY5Y cells and primary murine neurons, along with SH-SY5Y cells transfected with full-length human tau (SH-SY5Y/htau). Pharmacological antagonists, inhibitors, lentiviral transduction, co-immunoprecipitation, and calcium flux assays were utilized to dissect ADRA1-mediated molecular mechanisms in tauopathy and neuroinflammation. Results Hippocampal ADRA1 expression was significantly elevated in 10-month-old 3xTg-AD mice. Neuronal ADRA1 knockdown suppressed STING/NF-κB/NLRP3 pathway activation, ameliorated tauopathy and neuroinflammation, restored neuronal structure/function, and improved cognitive deficits in 3xTg-AD mice. Conversely, ADRA1 overexpression in C57/BL6 mice induced tauopathy, neuroinflammation, and cognitive impairment. Mechanistically, ADRA1 interacts with CXCR4 to form heterodimers, triggering cytoplasmic Ca2⁺ overload and subsequent STING/NF-κB/NLRP3 pathway activation. Conclusions ADRA1 critically mediates tauopathy and neuroinflammation through STING/NF-κB/NLRP3 signaling. These results identify ADRA1 as a promising therapeutic target for AD prevention and treatment. Graphical Abstract
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spelling doaj-art-bff0a1f35d6f47ecbb644b2e53a1294d2025-08-20T04:03:02ZengBMCJournal of Neuroinflammation1742-20942025-07-0122112510.1186/s12974-025-03506-3Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease miceBo Li0Li Wang1Yan Xiao2Zhi Tang3Yang Wang4Ting Sun5Xiaolan Qi6Key Laboratory of Endemic and Ethnic Diseases, Ministry of Education and Key Laboratory of Medical Molecular Biology of Guizhou Province, Key Laboratory of Molecular Biology of Guizhou Medical UniversityKey Laboratory of Endemic and Ethnic Diseases, Ministry of Education and Key Laboratory of Medical Molecular Biology of Guizhou Province, Key Laboratory of Molecular Biology of Guizhou Medical UniversityKey Laboratory of Endemic and Ethnic Diseases, Ministry of Education and Key Laboratory of Medical Molecular Biology of Guizhou Province, Key Laboratory of Molecular Biology of Guizhou Medical UniversityKey Laboratory of Endemic and Ethnic Diseases, Ministry of Education and Key Laboratory of Medical Molecular Biology of Guizhou Province, Key Laboratory of Molecular Biology of Guizhou Medical UniversityThe Department of Imaging, Affiliated Hospital of Guizhou Medical UniversitySchool of Nursing, Guizhou Medical UniversityKey Laboratory of Endemic and Ethnic Diseases, Ministry of Education and Key Laboratory of Medical Molecular Biology of Guizhou Province, Key Laboratory of Molecular Biology of Guizhou Medical UniversityAbstract Background Neuroinflammation is closely associated with the pathological progression of Alzheimer's disease (AD). The α1-adrenergic receptor (ADRA1), a G protein-coupled receptor, has been identified as a critical therapeutic target in inflammatory disorders. However, its precise mechanistic role in AD pathogenesis remains unclear. Methods To investigate ADRA1's role in AD, we employed 3xTg-AD and wild-type (WT) mice, modulating neuronal ADRA1 expression via intracerebroventricular delivery of adeno-associated viruses. Cognitive function, tau pathology, neuronal morphology, and activation of the STING/NF-κB/NLRP3 signaling pathway were evaluated using behavioral tests, Western blot, Golgi-Cox staining, immunohistochemistry, and immunofluorescence. In vitro AD models were established using Aβ42 oligomer-stimulated SH-SY5Y cells and primary murine neurons, along with SH-SY5Y cells transfected with full-length human tau (SH-SY5Y/htau). Pharmacological antagonists, inhibitors, lentiviral transduction, co-immunoprecipitation, and calcium flux assays were utilized to dissect ADRA1-mediated molecular mechanisms in tauopathy and neuroinflammation. Results Hippocampal ADRA1 expression was significantly elevated in 10-month-old 3xTg-AD mice. Neuronal ADRA1 knockdown suppressed STING/NF-κB/NLRP3 pathway activation, ameliorated tauopathy and neuroinflammation, restored neuronal structure/function, and improved cognitive deficits in 3xTg-AD mice. Conversely, ADRA1 overexpression in C57/BL6 mice induced tauopathy, neuroinflammation, and cognitive impairment. Mechanistically, ADRA1 interacts with CXCR4 to form heterodimers, triggering cytoplasmic Ca2⁺ overload and subsequent STING/NF-κB/NLRP3 pathway activation. Conclusions ADRA1 critically mediates tauopathy and neuroinflammation through STING/NF-κB/NLRP3 signaling. These results identify ADRA1 as a promising therapeutic target for AD prevention and treatment. Graphical Abstracthttps://doi.org/10.1186/s12974-025-03506-3ADRA1CXCR4StingTau proteinNeuroinflammationAlzheimer’s disease
spellingShingle Bo Li
Li Wang
Yan Xiao
Zhi Tang
Yang Wang
Ting Sun
Xiaolan Qi
Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
Journal of Neuroinflammation
ADRA1
CXCR4
Sting
Tau protein
Neuroinflammation
Alzheimer’s disease
title Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
title_full Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
title_fullStr Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
title_full_unstemmed Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
title_short Modulation of neuronal α1-adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the STING/NF-κB/NLRP3 signaling pathway in Alzheimer’s disease mice
title_sort modulation of neuronal α1 adrenergic receptor reduces tauopathy and neuroinflammation by inhibiting the sting nf κb nlrp3 signaling pathway in alzheimer s disease mice
topic ADRA1
CXCR4
Sting
Tau protein
Neuroinflammation
Alzheimer’s disease
url https://doi.org/10.1186/s12974-025-03506-3
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