Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context

Summary: Background: The APOE-ε4 genotype is the highest genetic risk factor for Alzheimer's disease (AD), and exercise training can reduce the risk of AD. Two early pathologies of AD are degradation of tight junctions between brain microvascular endothelial cells (BMEC) and brain glucose hypo...

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Main Authors: Callie M. Weber, Bilal Moiz, Gabriel S. Pena, Marzyeh Kheradmand, Brooke Wunderler, Claire Kettula, Gurneet S. Sangha, J. Carson Smith, Alisa Morss Clyne
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396424005231
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author Callie M. Weber
Bilal Moiz
Gabriel S. Pena
Marzyeh Kheradmand
Brooke Wunderler
Claire Kettula
Gurneet S. Sangha
J. Carson Smith
Alisa Morss Clyne
author_facet Callie M. Weber
Bilal Moiz
Gabriel S. Pena
Marzyeh Kheradmand
Brooke Wunderler
Claire Kettula
Gurneet S. Sangha
J. Carson Smith
Alisa Morss Clyne
author_sort Callie M. Weber
collection DOAJ
description Summary: Background: The APOE-ε4 genotype is the highest genetic risk factor for Alzheimer's disease (AD), and exercise training can reduce the risk of AD. Two early pathologies of AD are degradation of tight junctions between brain microvascular endothelial cells (BMEC) and brain glucose hypometabolism. Therefore, the objective of this work was to determine how the APOE-ε4 genotype and serum from exercise trained individuals impacts BMEC barrier function and metabolism. Methods: iPSC homozygous for the APOE-ε3 and APOE-ε4 alleles were differentiated to BMEC-like cells and used to measure barrier function and metabolism. To investigate exercise effects, serum was collected from older adults pre- and post- 6 months of exercise training (n = 9 participants per genotype). APOE-ε3 and APOE-ε4 BMEC were treated with genotype-matched serum, and then barrier function and metabolism were measured. Findings: APOE-ε4 genotype impaired BMEC barrier function and metabolism by reducing sirtuin 1 (SIRT1) levels by 27% (p = 0.0188) and baseline insulin signalling by 37% (p = 0.0186) compared to APOE-ε3 BMEC. Exercise-trained serum increased SIRT1 by 33% (p = 0.0043) in APOE-ε3 BMEC but decreased SIRT1 by 22% (p = 0.0004) in APOE ε4 BMEC. Interpretation: APOE-ε4 directly impairs glucose metabolism and barrier function. Serum from exercise trained individuals alters SIRT1 in a genotype-dependent manner but may require additional cues from exercise to decrease AD pathologies. Funding: Brain and Behaviour Initiative at the University of Maryland through the Seed Grant Program, NSF-GRFP DGE 1840340, Fischell Fellowship in Biomedical Engineering, NSF CBET-2211966 and DGE-1632976, National Niemann-Pick Disease Foundation, University of Maryland ASPIRE Program, NIH R01HL165193, R01HL140239-01, and R01AG057552.
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issn 2352-3964
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spelling doaj-art-c298ca863f584ab5aa90b4e6f09711172025-08-20T02:20:42ZengElsevierEBioMedicine2352-39642025-01-0111110548710.1016/j.ebiom.2024.105487Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in contextCallie M. Weber0Bilal Moiz1Gabriel S. Pena2Marzyeh Kheradmand3Brooke Wunderler4Claire Kettula5Gurneet S. Sangha6J. Carson Smith7Alisa Morss Clyne8Department of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Kinesiology, University of Maryland, College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United StatesDepartment of Kinesiology, University of Maryland, College Park, MD, 20742, United StatesDepartment of Bioengineering, University of Maryland; College Park, MD, 20742, United States; Corresponding author.Summary: Background: The APOE-ε4 genotype is the highest genetic risk factor for Alzheimer's disease (AD), and exercise training can reduce the risk of AD. Two early pathologies of AD are degradation of tight junctions between brain microvascular endothelial cells (BMEC) and brain glucose hypometabolism. Therefore, the objective of this work was to determine how the APOE-ε4 genotype and serum from exercise trained individuals impacts BMEC barrier function and metabolism. Methods: iPSC homozygous for the APOE-ε3 and APOE-ε4 alleles were differentiated to BMEC-like cells and used to measure barrier function and metabolism. To investigate exercise effects, serum was collected from older adults pre- and post- 6 months of exercise training (n = 9 participants per genotype). APOE-ε3 and APOE-ε4 BMEC were treated with genotype-matched serum, and then barrier function and metabolism were measured. Findings: APOE-ε4 genotype impaired BMEC barrier function and metabolism by reducing sirtuin 1 (SIRT1) levels by 27% (p = 0.0188) and baseline insulin signalling by 37% (p = 0.0186) compared to APOE-ε3 BMEC. Exercise-trained serum increased SIRT1 by 33% (p = 0.0043) in APOE-ε3 BMEC but decreased SIRT1 by 22% (p = 0.0004) in APOE ε4 BMEC. Interpretation: APOE-ε4 directly impairs glucose metabolism and barrier function. Serum from exercise trained individuals alters SIRT1 in a genotype-dependent manner but may require additional cues from exercise to decrease AD pathologies. Funding: Brain and Behaviour Initiative at the University of Maryland through the Seed Grant Program, NSF-GRFP DGE 1840340, Fischell Fellowship in Biomedical Engineering, NSF CBET-2211966 and DGE-1632976, National Niemann-Pick Disease Foundation, University of Maryland ASPIRE Program, NIH R01HL165193, R01HL140239-01, and R01AG057552.http://www.sciencedirect.com/science/article/pii/S2352396424005231Blood-brain barrierAlzheimer's diseaseGlucose metabolismAPOE genotypeExercise training
spellingShingle Callie M. Weber
Bilal Moiz
Gabriel S. Pena
Marzyeh Kheradmand
Brooke Wunderler
Claire Kettula
Gurneet S. Sangha
J. Carson Smith
Alisa Morss Clyne
Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
EBioMedicine
Blood-brain barrier
Alzheimer's disease
Glucose metabolism
APOE genotype
Exercise training
title Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
title_full Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
title_fullStr Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
title_full_unstemmed Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
title_short Impacts of APOE-ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismResearch in context
title_sort impacts of apoe ε4 and exercise training on brain microvascular endothelial cell barrier function and metabolismresearch in context
topic Blood-brain barrier
Alzheimer's disease
Glucose metabolism
APOE genotype
Exercise training
url http://www.sciencedirect.com/science/article/pii/S2352396424005231
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