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Characterisation of premature cell senescence in Alzheimer’s disease using single nuclear transcriptomics

Characterisation of premature cell senescence in Alzheimer’s disease using single nuclear transcriptomics
Characterisation of premature cell senescence in Alzheimer’s disease using single nuclear transcriptomics

Aging is associated with cell senescence and is the major risk factor for AD. We characterized premature cell senescence in postmortem brains from non-diseased controls (NDC) and donors with Alzheimer’s disease (AD) using imaging mass cytometry (IMC) and single nuclear RNA (snRNA) sequencing (> 200,000 nuclei). We found increases in numbers of glia immunostaining for galactosidase beta (> fourfold) and p16 INK4A (up to twofold) with AD relative to NDC. Increased glial expression of genes related to senescence was associated with greater β-amyloid load. Prematurely senescent microglia downregulated phagocytic pathways suggesting reduced capacity for β-amyloid clearance. Gene set enrichment and pseudo-time trajectories described extensive DNA double-strand breaks (DSBs), mitochondrial dysfunction and ER stress associated with increased β-amyloid leading to premature senescence in microglia. We replicated these observations with independent AD snRNA-seq datasets. Our results describe a burden of senescent glia with AD that is sufficiently high to contribute to disease progression. These findings support the hypothesis that microglia are a primary target for senolytic treatments in AD.

Aging, Alzheimer’s disease, Astrocyte, Cell stress, Glia, Image mass cytometry, Microglia, Neuron, Oligodendroglia, Senescence, Senolytics, Single cell transcriptomics
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Fancy, Nurun N.
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Smith, Amy M.
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Caramello, Alessia
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Tsartsalis, Stergios
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Davey, Karen
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Muirhead, Robert C.J.
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McGarry, Aisling
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Jenkyns, Marion H.
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Schneegans, Eleonore
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Chau, Vicky
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Thomas, Michael
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Boulger, Sam
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Dorcas Cheung, To Ka
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Adair, Emily
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Papageorgopoulou, Marianna
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Willumsen, Nanet
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Khozoie, Combiz
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Gomez-Nicola, Diego
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Jackson, Johanna S.
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Matthews, Paul M.
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Fancy, Nurun N.
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Smith, Amy M.
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Caramello, Alessia
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Tsartsalis, Stergios
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Davey, Karen
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Muirhead, Robert C.J.
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McGarry, Aisling
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Jenkyns, Marion H.
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Schneegans, Eleonore
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Chau, Vicky
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Thomas, Michael
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Boulger, Sam
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Dorcas Cheung, To Ka
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Adair, Emily
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Papageorgopoulou, Marianna
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Willumsen, Nanet
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Khozoie, Combiz
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Gomez-Nicola, Diego
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Jackson, Johanna S.
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Matthews, Paul M.
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Fancy, Nurun N., Smith, Amy M., Caramello, Alessia, Tsartsalis, Stergios, Davey, Karen, Muirhead, Robert C.J., McGarry, Aisling, Jenkyns, Marion H., Schneegans, Eleonore, Chau, Vicky, Thomas, Michael, Boulger, Sam, Dorcas Cheung, To Ka, Adair, Emily, Papageorgopoulou, Marianna, Willumsen, Nanet, Khozoie, Combiz, Gomez-Nicola, Diego, Jackson, Johanna S. and Matthews, Paul M. (2024) Characterisation of premature cell senescence in Alzheimer’s disease using single nuclear transcriptomics. Acta Neuropathologica, 147 (1), [78]. (doi:10.1007/s00401-024-02727-9).

Record type: Article

Abstract

Aging is associated with cell senescence and is the major risk factor for AD. We characterized premature cell senescence in postmortem brains from non-diseased controls (NDC) and donors with Alzheimer’s disease (AD) using imaging mass cytometry (IMC) and single nuclear RNA (snRNA) sequencing (> 200,000 nuclei). We found increases in numbers of glia immunostaining for galactosidase beta (> fourfold) and p16 INK4A (up to twofold) with AD relative to NDC. Increased glial expression of genes related to senescence was associated with greater β-amyloid load. Prematurely senescent microglia downregulated phagocytic pathways suggesting reduced capacity for β-amyloid clearance. Gene set enrichment and pseudo-time trajectories described extensive DNA double-strand breaks (DSBs), mitochondrial dysfunction and ER stress associated with increased β-amyloid leading to premature senescence in microglia. We replicated these observations with independent AD snRNA-seq datasets. Our results describe a burden of senescent glia with AD that is sufficiently high to contribute to disease progression. These findings support the hypothesis that microglia are a primary target for senolytic treatments in AD.

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Accepted/In Press date: 28 March 2024
Published date: 2 May 2024
Keywords: Aging, Alzheimer’s disease, Astrocyte, Cell stress, Glia, Image mass cytometry, Microglia, Neuron, Oligodendroglia, Senescence, Senolytics, Single cell transcriptomics

Identifiers

Local EPrints ID: 496040
URI: http://eprints.soton.ac.uk/id/eprint/496040
ISSN: 0001-6322
PURE UUID: 19c2f6c6-b1bb-44f3-9e5f-f59c2aeaa441
ORCID for Diego Gomez-Nicola: ORCID iD orcid.org/0000-0002-5316-2682

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Date deposited: 02 Dec 2024 17:34
Last modified: 03 Dec 2024 02:43

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Contributors

Author: Nurun N. Fancy
Author: Amy M. Smith
Author: Alessia Caramello
Author: Stergios Tsartsalis
Author: Karen Davey
Author: Robert C.J. Muirhead
Author: Aisling McGarry
Author: Marion H. Jenkyns
Author: Eleonore Schneegans
Author: Vicky Chau
Author: Michael Thomas
Author: Sam Boulger
Author: To Ka Dorcas Cheung
Author: Emily Adair
Author: Marianna Papageorgopoulou
Author: Nanet Willumsen
Author: Combiz Khozoie
Author: Johanna S. Jackson
Author: Paul M. Matthews

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