Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology

Abstract Background Choroid plexus (CP) or blood-cerebrospinal fluid-barrier (BCSFB) is a unique functional tissue which lines the brain’s fluid-filled ventricles, with a crucial role in CSF production and clearance. BCSFB dysfunction is thought to contribute to toxic protein build-up in neurodegene...

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Main Authors: Charith Perera, Renata Cruz, Noam Shemesh, Tânia Carvalho, David L. Thomas, Jack Wells, Andrada Ianuș
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Fluids and Barriers of the CNS
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Online Access:https://doi.org/10.1186/s12987-024-00597-7
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author Charith Perera
Renata Cruz
Noam Shemesh
Tânia Carvalho
David L. Thomas
Jack Wells
Andrada Ianuș
author_facet Charith Perera
Renata Cruz
Noam Shemesh
Tânia Carvalho
David L. Thomas
Jack Wells
Andrada Ianuș
author_sort Charith Perera
collection DOAJ
description Abstract Background Choroid plexus (CP) or blood-cerebrospinal fluid-barrier (BCSFB) is a unique functional tissue which lines the brain’s fluid-filled ventricles, with a crucial role in CSF production and clearance. BCSFB dysfunction is thought to contribute to toxic protein build-up in neurodegenerative disorders, including Alzheimer’s disease (AD). However, the dynamics of this process remain unknown, mainly due to the paucity of in-vivo methods for assessing CP function. Methods We harness recent developments in Arterial Spin Labelling MRI to measure water delivery across the BCSFB as a proxy for CP function, as well as cerebral blood flow (CBF), at different stages of AD in the widely used triple transgenic mouse model (3xTg), with ages between 8 and 32 weeks. We further compared the MRI results with Y-maze behaviour testing, and histologically validated the expected pathological changes, which recapitulate both amyloid and tau deposition. Results Total BCSFB-mediated water delivery is significantly higher in 3xTg mice (> 50%) from 8 weeks (preclinical stage), an increase which is not explained by differences in ventricular volumes, while tissue parameters such as CBF and T1 are not different between groups at all ages. Behaviour differences between the groups were observed starting at 20 weeks, especially in terms of locomotion, with 3xTg animals showing a significantly smaller number of arm entries in the Y-maze. Conclusions Our work strongly suggests the involvement of CP in the early stages of AD, before the onset of symptoms and behavioural changes, providing a potential biomarker of pathology.
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spelling doaj-art-bc70a9c3a0384b53aa0d7cdbc0be1eab2024-12-08T12:41:40ZengBMCFluids and Barriers of the CNS2045-81182024-12-0121111510.1186/s12987-024-00597-7Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathologyCharith Perera0Renata Cruz1Noam Shemesh2Tânia Carvalho3David L. Thomas4Jack Wells5Andrada Ianuș6UCL Centre for Advanced Biomedical Imaging, Division of Medicine, University College LondonChampalimaud Research, Champalimaud FoundationChampalimaud Research, Champalimaud FoundationChampalimaud Research, Champalimaud FoundationNeuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, UCL Queen Square Institute of NeurologyUCL Centre for Advanced Biomedical Imaging, Division of Medicine, University College LondonChampalimaud Research, Champalimaud FoundationAbstract Background Choroid plexus (CP) or blood-cerebrospinal fluid-barrier (BCSFB) is a unique functional tissue which lines the brain’s fluid-filled ventricles, with a crucial role in CSF production and clearance. BCSFB dysfunction is thought to contribute to toxic protein build-up in neurodegenerative disorders, including Alzheimer’s disease (AD). However, the dynamics of this process remain unknown, mainly due to the paucity of in-vivo methods for assessing CP function. Methods We harness recent developments in Arterial Spin Labelling MRI to measure water delivery across the BCSFB as a proxy for CP function, as well as cerebral blood flow (CBF), at different stages of AD in the widely used triple transgenic mouse model (3xTg), with ages between 8 and 32 weeks. We further compared the MRI results with Y-maze behaviour testing, and histologically validated the expected pathological changes, which recapitulate both amyloid and tau deposition. Results Total BCSFB-mediated water delivery is significantly higher in 3xTg mice (> 50%) from 8 weeks (preclinical stage), an increase which is not explained by differences in ventricular volumes, while tissue parameters such as CBF and T1 are not different between groups at all ages. Behaviour differences between the groups were observed starting at 20 weeks, especially in terms of locomotion, with 3xTg animals showing a significantly smaller number of arm entries in the Y-maze. Conclusions Our work strongly suggests the involvement of CP in the early stages of AD, before the onset of symptoms and behavioural changes, providing a potential biomarker of pathology.https://doi.org/10.1186/s12987-024-00597-7Alzheimer’s diseaseChoroid plexusBlood CSF barrierBrain perfusionArterial spin labelling MRI3xTg mouse model
spellingShingle Charith Perera
Renata Cruz
Noam Shemesh
Tânia Carvalho
David L. Thomas
Jack Wells
Andrada Ianuș
Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
Fluids and Barriers of the CNS
Alzheimer’s disease
Choroid plexus
Blood CSF barrier
Brain perfusion
Arterial spin labelling MRI
3xTg mouse model
title Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
title_full Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
title_fullStr Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
title_full_unstemmed Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
title_short Non-invasive MRI of blood-cerebrospinal fluid-barrier function in a mouse model of Alzheimer’s disease: a potential biomarker of early pathology
title_sort non invasive mri of blood cerebrospinal fluid barrier function in a mouse model of alzheimer s disease a potential biomarker of early pathology
topic Alzheimer’s disease
Choroid plexus
Blood CSF barrier
Brain perfusion
Arterial spin labelling MRI
3xTg mouse model
url https://doi.org/10.1186/s12987-024-00597-7
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