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Upregulation of APP endocytosis by neuronal aging drives amyloid-dependent synapse loss

Burrinha, Tatiana, Martinsson, Isak, Gomes, Ricardo, Terrasso, Ana Paula, Gouras, Gunnar K., Almeida, Cláudia Guimas·2021·Journal of Cell Science
DOI 10.1242/jcs.255752
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Abstract

Neuronal aging increases the risk of late-onset Alzheimer's disease. During normal aging, synapses decline, and β-amyloid (Aβ) accumulates intraneuronally. However, little is known about the underlying cell biological mechanisms. We studied neuronal aging using normal-aged brain and aged mouse primary neurons that accumulate lysosomal lipofuscin and show synapse loss. We identified the upregulation of amyloid precursor protein (APP) endocytosis as a neuronal aging mechanism that potentiates APP processing and Aβ production in vitro and in vivo. The increased APP endocytosis may contribute to the early endosome enlargement observed in the aged brain. Mechanistically, we showed that clathrin-dependent APP endocytosis requires F-actin and that clathrin and endocytic F-actin increase with neuronal aging. Finally, Aβ production inhibition reverts synaptic decline in aged neurons, whereas Aβ accumulation, promoted by endocytosis upregulation in younger neurons, recapitulates aging-related synapse decline. Overall, we identify APP endocytosis upregulation as a potential mechanism of neuronal aging and, thus, a novel target to prevent late-onset Alzheimer's disease. This article has an associated First Person interview with the first author of the paper.

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Metadata

Authors
Burrinha, T., Martinsson, I., Gomes, R., Terrasso, A. P., Gouras, G. K., & Almeida, C. G.
Affiliations
  • iNOVA4Health, Chronic Diseases Research Center (CEDOC), NOVA Medical School (NMS), Universidade Nova de Lisboa, 1169-056 Lisboa, Portugal
  • Experimental Dementia Research Unit, Lund University, 22184 Lund, Sweden
ORCID
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2021-05-01
Volume
134
Issue
9
ISSN
  • 0021-9533
  • 1477-9137
DOI
10.1242/jcs.255752
Cited by
64
References
31
Language
en
Licence
www.biologists.com/user-licence-1-1/ (vor)
Funders
  • FP7 People: Marie-Curie Actions (PCIG–GA–2012–334366–trafficinAD)
  • Fundação para a Ciência e a Tecnologia (UID/Multi/04462/2019-FCT/MCTES/ PT2020 SFRH/BD/52473/2014 CEECIND/00410/2017 SFRH/BD/131513/2017)
  • Maratona da Saúde-2016
  • Alzheimer's Association (AARG-19-618007)
  • European Regional Development Fund (PPBI-POCI-01-0145-FEDER-022122)
  • Horizon 2020 Framework Programme (GA811087-Lysocil)
  • Vetenskapsrådet

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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