Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease

Abstract Background Alzheimer’s disease (AD) is a progressive neurodegenerative disorder characterized by the accumulation of amyloid-β plaques, tau hyperphosphorylation, and neuroinflammation. The choroid plexus (ChP), serving as the blood-cerebrospinal fluid-brain barrier, plays essential roles in...

Full description

Saved in:
Bibliographic Details
Main Authors: Zhong-Jiang Yan, Maosen Ye, Jiexi Li, Deng-Feng Zhang, Yong-Gang Yao
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Molecular Neurodegeneration
Subjects:
Online Access:https://doi.org/10.1186/s13024-025-00853-w
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850242995639549952
author Zhong-Jiang Yan
Maosen Ye
Jiexi Li
Deng-Feng Zhang
Yong-Gang Yao
author_facet Zhong-Jiang Yan
Maosen Ye
Jiexi Li
Deng-Feng Zhang
Yong-Gang Yao
author_sort Zhong-Jiang Yan
collection DOAJ
description Abstract Background Alzheimer’s disease (AD) is a progressive neurodegenerative disorder characterized by the accumulation of amyloid-β plaques, tau hyperphosphorylation, and neuroinflammation. The choroid plexus (ChP), serving as the blood-cerebrospinal fluid-brain barrier, plays essential roles in immune response to stress and brain homeostasis. However, the cellular and molecular contributions of the ChP to AD progression remain inadequately understood. Methods To elucidate the molecular abnormalities during the early stages of AD, we acquired single-cell transcription profiling of ChP from APP/PS1 mice with early-stage of Aβ pathology and litter-mate controls. The transcriptional alterations that occurred in each cell type were identified by differentially expressed genes, cell–cell communications and pseudotemporal trajectory analysis. The findings were subsequently validated by a series of in situ and in vitro assays. Results We constructed a comprehensive atlas of ChP at single-cell resolution and identified six major cell types and immune subclusters in male mice. The majority of dysregulated genes were found in the epithelial cells of APP/PS1 mice in comparison to wild-type (WT) mice, and most of these genes belonged to down-regulated module involved in mitochondrial respirasome assembly, cilium organization, and barrier integrity. The disruption of the epithelial barrier resulted in the downregulation of macrophage migration inhibitory factor (MIF) secretion in APP/PS1 mice, leading to macrophage activation and increased phagocytosis of Aβ. Concurrently, ligands (e.g., APOE) secreted by macrophages and other ChP cells facilitated the entry of lipids into ependymal cells, leading to lipid accumulation and the activation of microglia in the brain parenchyma in APP/PS1 mice compared to WT controls. Conclusions Taken together, these data profiled early transcriptional and cellular abnormalities of ChP within an AD mouse model, providing novel insights of cerebral vasculature into the pathobiology of AD.
format Article
id doaj-art-5b8a700b453e49d5bb56997eab9db51e
institution OA Journals
issn 1750-1326
language English
publishDate 2025-05-01
publisher BMC
record_format Article
series Molecular Neurodegeneration
spelling doaj-art-5b8a700b453e49d5bb56997eab9db51e2025-08-20T02:00:08ZengBMCMolecular Neurodegeneration1750-13262025-05-0120112110.1186/s13024-025-00853-wEarly transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s diseaseZhong-Jiang Yan0Maosen Ye1Jiexi Li2Deng-Feng Zhang3Yong-Gang Yao4State Key Laboratory of Genetic Evolution & Animal Models, Yunnan Key Laboratory of Animal Models and Human Disease Mechanisms, and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Genetic Evolution & Animal Models, Yunnan Key Laboratory of Animal Models and Human Disease Mechanisms, and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Genetic Evolution & Animal Models, Yunnan Key Laboratory of Animal Models and Human Disease Mechanisms, and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Genetic Evolution & Animal Models, Yunnan Key Laboratory of Animal Models and Human Disease Mechanisms, and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Genetic Evolution & Animal Models, Yunnan Key Laboratory of Animal Models and Human Disease Mechanisms, and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of SciencesAbstract Background Alzheimer’s disease (AD) is a progressive neurodegenerative disorder characterized by the accumulation of amyloid-β plaques, tau hyperphosphorylation, and neuroinflammation. The choroid plexus (ChP), serving as the blood-cerebrospinal fluid-brain barrier, plays essential roles in immune response to stress and brain homeostasis. However, the cellular and molecular contributions of the ChP to AD progression remain inadequately understood. Methods To elucidate the molecular abnormalities during the early stages of AD, we acquired single-cell transcription profiling of ChP from APP/PS1 mice with early-stage of Aβ pathology and litter-mate controls. The transcriptional alterations that occurred in each cell type were identified by differentially expressed genes, cell–cell communications and pseudotemporal trajectory analysis. The findings were subsequently validated by a series of in situ and in vitro assays. Results We constructed a comprehensive atlas of ChP at single-cell resolution and identified six major cell types and immune subclusters in male mice. The majority of dysregulated genes were found in the epithelial cells of APP/PS1 mice in comparison to wild-type (WT) mice, and most of these genes belonged to down-regulated module involved in mitochondrial respirasome assembly, cilium organization, and barrier integrity. The disruption of the epithelial barrier resulted in the downregulation of macrophage migration inhibitory factor (MIF) secretion in APP/PS1 mice, leading to macrophage activation and increased phagocytosis of Aβ. Concurrently, ligands (e.g., APOE) secreted by macrophages and other ChP cells facilitated the entry of lipids into ependymal cells, leading to lipid accumulation and the activation of microglia in the brain parenchyma in APP/PS1 mice compared to WT controls. Conclusions Taken together, these data profiled early transcriptional and cellular abnormalities of ChP within an AD mouse model, providing novel insights of cerebral vasculature into the pathobiology of AD.https://doi.org/10.1186/s13024-025-00853-wAlzheimer’s diseaseChoroid plexusSingle-cell transcriptomeLipid accumulationNeuroinflammation
spellingShingle Zhong-Jiang Yan
Maosen Ye
Jiexi Li
Deng-Feng Zhang
Yong-Gang Yao
Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
Molecular Neurodegeneration
Alzheimer’s disease
Choroid plexus
Single-cell transcriptome
Lipid accumulation
Neuroinflammation
title Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
title_full Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
title_fullStr Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
title_full_unstemmed Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
title_short Early transcriptional and cellular abnormalities in choroid plexus of a mouse model of Alzheimer’s disease
title_sort early transcriptional and cellular abnormalities in choroid plexus of a mouse model of alzheimer s disease
topic Alzheimer’s disease
Choroid plexus
Single-cell transcriptome
Lipid accumulation
Neuroinflammation
url https://doi.org/10.1186/s13024-025-00853-w
work_keys_str_mv AT zhongjiangyan earlytranscriptionalandcellularabnormalitiesinchoroidplexusofamousemodelofalzheimersdisease
AT maosenye earlytranscriptionalandcellularabnormalitiesinchoroidplexusofamousemodelofalzheimersdisease
AT jiexili earlytranscriptionalandcellularabnormalitiesinchoroidplexusofamousemodelofalzheimersdisease
AT dengfengzhang earlytranscriptionalandcellularabnormalitiesinchoroidplexusofamousemodelofalzheimersdisease
AT yonggangyao earlytranscriptionalandcellularabnormalitiesinchoroidplexusofamousemodelofalzheimersdisease