Defective macroautophagic turnover of brain lipids in the TgCRND8 Alzheimer mouse model: prevention by correcting lysosomal proteolytic deficits
Open accessAbstract
Autophagy, the major lysosomal pathway for the turnover of intracellular organelles is markedly impaired in neurons in Alzheimer's disease and Alzheimer mouse models. We have previously reported that severe lysosomal and amyloid neuropathology and associated cognitive deficits in the TgCRND8 Alzheimer mouse model can be ameliorated by restoring lysosomal proteolytic capacity and autophagy flux via genetic deletion of the lysosomal protease inhibitor, cystatin B. Here we present evidence that macroautophagy is a significant pathway for lipid turnover, which is defective in TgCRND8 brain where lipids accumulate as membranous structures and lipid droplets within giant neuronal autolysosomes. Levels of multiple lipid species including several sphingolipids (ceramide, ganglioside GM3, GM2, GM1, GD3 and GD1a), cardiolipin, cholesterol and cholesteryl esters are elevated in autophagic vacuole fractions and lysosomes isolated from TgCRND8 brain. Lipids are localized in autophagosomes and autolysosomes by double immunofluorescence analyses in wild-type mice and colocalization is increased in TgCRND8 mice where abnormally abundant GM2 ganglioside-positive granules are detected in neuronal lysosomes. Cystatin B deletion in TgCRND8 significantly reduces the number of GM2-positive granules and lowers the levels of GM2 and GM3 in lysosomes, decreases lipofuscin-related autofluorescence, and eliminates giant lipid-containing autolysosomes while increasing numbers of normal-sized autolysosomes/lysosomes with reduced content of undigested components. These findings have identified macroautophagy as a previously unappreciated route for delivering membrane lipids to lysosomes for turnover, a function that has so far been considered to be mediated exclusively through the endocytic pathway, and revealed that autophagic-lysosomal dysfunction in TgCRND8 brain impedes lysosomal turnover of lipids as well as proteins. The amelioration of lipid accumulation in TgCRND8 by removing cystatin B inhibition on lysosomal proteases suggests that enhancing lysosomal proteolysis improves the overall environment of the lysosome and its clearance functions, which may be possibly relevant to a broader range of lysosomal disorders beyond Alzheimer's disease.
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APP-βCTF has been previously linked to lysosomal dysfunction in AD models involving overexpressed forms of FAD-mutated APP with or without additional overexpression of other mutated human AD genes, and in iPSC generated Ts21 neurons.
“APP-CTF has also been previously linked to lysosomal dysfunction in AD models involving overexpressed forms of FAD-mutated APP with or without additional overexpression of other mutated human AD genes (Lauritzen et al., 2012(Lauritzen et al., , 2016;;Yang et al., 2014;Kaur et al., 2017;Bourgeois et al., 2018), and in iPSC generated Ts21 neurons (Hung and Livesey, 2018).”
From Lysosomal Dysfunction in Down Syndrome Is APP-Dependent and Mediated by APP-βCTF (C99) (2019) · cites this paper as Yang et al., 2014
The Introduction describes lysosomal dysfunction in TgCRND8 mice overexpressing FAD-mutated human APP. The section on prevention of lysosomal lipid accumulation discusses impaired lysosomal degradation and accumulation of APP-CTFs, but does not identify APP-βCTF specifically as a cause of that dysfunction. The Ts21-neuron clause is attributed to a different citation, not Yang et al. (LLM, conf=0.84)
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The Impact of ESCRT on Aβ1-42 Induced Membrane Lesions in a Yeast Model for Alzheimer’s Disease
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Lysosomal gene Hexb displays haploinsufficiency in a knock-in mouse model of Alzheimer’s disease
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- Authors
- Yang, D.-S., Stavrides, P., Saito, M., Kumar, A., Rodriguez-Navarro, J. A., Pawlik, M., Huo, C., Walkley, S. U., Saito, M., Cuervo, A. M., & Nixon, R. A.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- Albert Einstein College of Medicine (US)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-09-30
- Volume
- 137
- Issue
- 12
- Pages
- 3300-3318
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC4240291
- OpenAlex
- W1980912292
- Cited by
- 114
- References
- 104
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 6 · 2022: 11 · 2021: 11 · 2020: 9 · 2019: 10 · 2018: 8 · 2017: 17 · 2016: 18 · 2015: 7
- FWCI
- 10.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alzheimer's Association (IIRG-08-90771)
- University of Alberta
- Università di Bologna
- National Institutes of Health (UL1TR001073)
- National Institute on Alcohol Abuse and Alcoholism (R01AA015355, AA015355)
- National Institute on Aging (P30AG038072, P01AG017617)
- National Center for Advancing Translational Sciences
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD045561, P30HD071593)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Physiology › Lysosomal Storage Disorders Research
- Keywords
- macroautophagy, Alzheimer's disease, cystatin B, lysosomal proteolysis, GM2 ganglioside, GM3 ganglioside, sphingolipids, autolysosomes, lipid droplets, lipofuscin, lysosomal storage disease, autophagic flux
- MeSH terms
- Alzheimer Disease, Amyloid, Animals, Autophagy, Brain, Disease Models, Animal, Female, Lysosomes, Male, Mice, Transgenic, Neurons, Lipid Metabolism, Mice, Proteolysis
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.
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