Cited by 104Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsPharmacological Receptor Mechanisms and Effects

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Widespread cell stress and mitochondrial dysfunction occur in patients with early Alzheimer’s disease

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Venkataraman, Ashwin V., Mansur, Ayla, Rizzo, Gaia, Bishop, Courtney, Lewis, Yvonne, Kocagoncu, Ece, Lingford-Hughes, Anne, Huiban, Mickael, Passchier, Jan, Rowe, James B., Tsukada, Hideo, Brooks, David J., Martarello, Laurent, Comley, Robert A., Chen, Laigao, Schwarz, Adam J., Hargreaves, Richard, Gunn, Roger N., Rabiner, Eugenii A., Matthews, Paul M.·2022·Science Translational Medicine

DOI 10.1126/scitranslmed.abk1051

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Abstract

Abstract Cell stress and impaired oxidative phosphorylation are central to mechanisms of synaptic loss and neurodegeneration in the cellular pathology of Alzheimer’s disease (AD). We quantified the in vivo density of the endoplasmic reticulum stress marker, the sigma 1 receptor (S1R) using [ 11 C]SA4503 PET, as well as that of mitochondrial complex I (MC1) with [ 18 F]BCPP-EF and the pre-synaptic vesicular protein SV2A with [ 11 C]UCB-J in 12 patients with early AD and in 16 cognitively normal controls. We integrated these molecular measures with assessments of regional brain volumes and brain perfusion (CBF) measured with MRI arterial spin labelling. 8 AD patients were followed longitudinally to estimate rates of change with disease progression over 12-18 months. The AD patients showed widespread increases in S1R (≤ 27%) and regional decreases in MC1 (≥ -28%), SV2A (≥ -25%), brain volume (≥ -23%), and CBF (≥ -26%). [ 18 F]BCPP-EF PET MC1 density (≥ -12%) and brain volumes (≥ -5%) were further reduced at follow up in brain regions consistent with the differences between AD patients and controls at baseline. Exploratory analyses showing associations of MC1, SV2A and S1R density with cognitive changes at baseline and longitudinally with AD, but not in controls, suggested a loss of metabolic functional reserve with disease. Our study thus provides novel in vivo evidence for widespread cellular stress and bioenergetic abnormalities in early AD and that they may be clinically meaningful.

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Additional file 3 of Mitovesicles secreted into the extracellular space of brains with mitochondrial dysfunction impair synaptic plasticity
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Additional file 4 of Mitovesicles secreted into the extracellular space of brains with mitochondrial dysfunction impair synaptic plasticity
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Additional file 1 of Mitovesicles secreted into the extracellular space of brains with mitochondrial dysfunction impair synaptic plasticity
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Additional file 2 of Mitovesicles secreted into the extracellular space of brains with mitochondrial dysfunction impair synaptic plasticity
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Authors: Venkataraman, A. V., Mansur, A., Rizzo, G., Bishop, C., Lewis, Y., Kocagoncu, E., Lingford-Hughes, A., Huiban, M., Passchier, J., Rowe, J. B., Tsukada, H., Brooks, D. J., Martarello, L., Comley, R. A., Chen, L., Schwarz, A. J., Hargreaves, R., Gunn, R. N., Rabiner, E. A., & Matthews, P. M.
Affiliations: UK Dementia Research Institute (GB)
Invicro (United Kingdom) (GB)
University of Cambridge, Cambridge CB2 2QQ, UK.
Imperial College London (GB)
Invicro LLC, London W12 0NN, UK.
University of Cambridge (GB)
Hamamatsu Photonics (Japan) (JP)
Aarhus University (DK)
Biogen (United States) (US)
AbbVie (United States) (US)
Pfizer (United States) (US)
Takeda Pharmaceuticals Ltd, Cambridge, MA 02139, USA.
Bristol-Myers Squibb (United States) (US)
King's College London (GB)
Corresponding author: Matthews, Paul M.
ORCID: Venkataraman, Ashwin V.
Mansur, Ayla
Rizzo, Gaia
Bishop, Courtney
Lewis, Yvonne
Kocagoncu, Ece
Lingford-Hughes, Anne
Passchier, Jan
Rowe, James B.
Tsukada, Hideo
Brooks, David J.
Comley, Robert A.
Chen, Laigao
Schwarz, Adam J.
Gunn, Roger N.
Rabiner, Eugenii A.
Matthews, Paul M.
Venue: Science Translational Medicine
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2022-08-17
Volume: 14
Issue: 658
Pages: eabk1051-eabk1051
ISSN: 1946-6234 (ISSN-L)
1946-6242
DOI: 10.1126/scitranslmed.abk1051
OpenAlex: W4292266434
Cited by: 101
References: 64
Citations by year: 2026: 21 · 2025: 28 · 2024: 32 · 2023: 17 · 2022: 2
FWCI: 13.26
Type: journal article
Language: en
Open access: green
doi.org
Licence: cc-by-nc-nd
Locations: Science Translational Medicine (publishedVersion)
medRxiv (acceptedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
Spiral (Imperial College London) (submittedVersion)
Funders: Alzheimer's Society
National Institute for Health and Care Research (BRC1215-20014, NIHR-INF-0507, CL-2022-17-003)
Department of Health and Social Care
Imperial College London
UK Dementia Research Institute
Medical Research Council (MR/N029941/1, MR/L023784/2, SUAG/051 G101400, G101400, BRC-1215-20014, MR/T033371/1)
NIHR Cambridge Biomedical Research Centre ((BRC-1215-20014))
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacological Receptor Mechanisms and Effects
Keywords: early Alzheimer's disease, endoplasmic reticulum stress, sigma-1 receptor, mitochondrial complex I, oxidative phosphorylation, mitochondrial dysfunction, SV2A, presynaptic dysfunction, brain atrophy, cerebral blood flow, disease progression, pharmacodynamic biomarkers, cognitive decline
MeSH terms: Alzheimer Disease, Brain, Cerebrovascular Circulation, Humans, Magnetic Resonance Imaging, Mitochondria, Biomarkers, Positron-Emission Tomography

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Widespread cell stress and mitochondrial dysfunction occur in patients with early Alzheimer’s disease

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