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Acta Neuropathol
Published

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

Authors

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

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 p16INK4A (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.

PMID:38695952 | DOI:10.1007/s00401-024-02727-9