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A Becn1 mutation mediates hyperactive autophagic sequestration of amyloid oligomers and improved cognition in Alzheimer's disease
Open accessAbstract
Impairment of the autophagy pathway has been observed during the pathogenesis of Alzheimer's disease (AD), a neurodegenerative disorder characterized by abnormal deposition of extracellular and intracellular amyloid β (Aβ) peptides. Yet the role of autophagy in Aβ production and AD progression is complex. To study whether increased basal autophagy plays a beneficial role in Aβ clearance and cognitive improvement, we developed a novel genetic model to hyperactivate autophagy in vivo. We found that knock-in of a point mutation F121A in the essential autophagy gene Beclin 1/Becn1 in mice significantly reduces the interaction of BECN1 with its inhibitor BCL2, and thus leads to constitutively active autophagy even under non-autophagy-inducing conditions in multiple tissues, including brain. Becn1F121A-mediated autophagy hyperactivation significantly decreases amyloid accumulation, prevents cognitive decline, and restores survival in AD mouse models. Using an immunoisolation method, we found biochemically that Aβ oligomers are autophagic substrates and sequestered inside autophagosomes in the brain of autophagy-hyperactive AD mice. In addition to genetic activation of autophagy by Becn1 gain-of-function, we also found that ML246, a small-molecule autophagy inducer, as well as voluntary exercise, a physiological autophagy inducer, exert similar Becn1-dependent protective effects on Aβ removal and memory in AD mice. Taken together, these results demonstrate that genetically disrupting BECN1-BCL2 binding hyperactivates autophagy in vivo, which sequestrates amyloid oligomers and prevents AD progression. The study establishes new approaches to activate autophagy in the brain, and reveals the important function of Becn1-mediated autophagy hyperactivation in the prevention of AD.
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“Evidence indicates that Aβ peptides can accumulate intracellularly while their extracellular release decreases when autophagy is impaired [85, 93].”
From Senescence-related impairment of autophagy induces toxic intraneuronal amyloid-β accumulation in a mouse model of amyloid pathology (2023) · cites this paper as [93]
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Metadata
- Authors
- Rocchi, A., Yamamoto, S., Ting, T., Fan, Y., Sadleir, K., Wang, Y., Zhang, W., Huang, S., Levine, B., Vassar, R., & He, C.
- Affiliations
- Northwestern University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- He, Congcong
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-08-14
- Volume
- 13
- Issue
- 8
- Pages
- e1006962
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC5570506
- OpenAlex
- W2749882665
- Cited by
- 166
- References
- 65
- Citations by year
- 2026: 11 · 2025: 24 · 2024: 12 · 2023: 21 · 2022: 24 · 2021: 29 · 2020: 19 · 2019: 10 · 2018: 16
- FWCI
- 9.10
- Type
- journal article
- Language
- en
- Update notices
- new_version (2017-08-24)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Cancer Prevention and Research Institute of Texas (RP120718)
- Northwestern University (AG13854)
- Northeast Normal University
- National Institutes of Health (U19AI199725, 5r01gm078555-08, AG13854, RO1 CA109618)
- University of North Carolina at Chapel Hill
- Fundamental Research Funds for the Central Universities (2412017FZ018)
- National Institute on Aging (AG13854, R01AG030142, R01AG022560, P30AG013854)
- National Cancer Institute (R01CA109618)
- National Institute of General Medical Sciences (R01 GM-078555)
- National Institute of Allergy and Infectious Diseases (U19AI109725, T32AI007163)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, autophagy, Beclin-1, Bcl-2, amyloid-beta oligomers, autophagosomes, cognitive decline, voluntary exercise, autophagy inducers, genetic mouse models
- MeSH terms
- Beclin-1, Alzheimer Disease, Animals, Autophagy, Cognition, Disease Models, Animal, HeLa Cells, Humans, Male, Memory, Mice, Inbred C57BL, Neurons, Amyloid beta-Peptides, Point Mutation, Sequence Analysis, DNA, Proto-Oncogene Proteins c-bcl-2, In Situ Nick-End Labeling, Mice, Gene Knock-In Techniques, HEK293 Cells
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