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Amyloid-β oligomers induce synaptic damage via Tau-dependent microtubule severing by TTLL6 and spastin
Open accessAbstract
Mislocalization and aggregation of Aβ and Tau combined with loss of synapses and microtubules (MTs) are hallmarks of Alzheimer disease. We exposed mature primary neurons to Aβ oligomers and analysed changes in the Tau/MT system. MT breakdown occurs in dendrites invaded by Tau (Tau missorting) and is mediated by spastin, an MT-severing enzyme. Spastin is recruited by MT polyglutamylation, induced by Tau missorting triggered translocalization of TTLL6 (Tubulin-Tyrosine-Ligase-Like-6) into dendrites. Consequences are spine loss and mitochondria and neurofilament mislocalization. Missorted Tau is not axonally derived, as shown by axonal retention of photoconvertible Dendra2-Tau, but newly synthesized. Recovery from Aβ insult occurs after Aβ oligomers lose their toxicity and requires the kinase MARK (Microtubule-Affinity-Regulating-Kinase). In neurons derived from Tau-knockout mice, MTs and synapses are resistant to Aβ toxicity because TTLL6 mislocalization and MT polyglutamylation are prevented; hence no spastin recruitment and no MT breakdown occur, enabling faster recovery. Reintroduction of Tau re-establishes Aβ-induced toxicity in TauKO neurons, which requires phosphorylation of Tau's KXGS motifs. Transgenic mice overexpressing Tau show TTLL6 translocalization into dendrites and decreased MT stability. The results provide a rationale for MT stabilization as a therapeutic approach.
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“Thus, cultured neurons from tau knockout (Tau−/−) mice are not susceptible to Aβ-induced synaptic damage and neurotoxicity (Rapoport et al., 2002; Nussbaum et al., 2012; Zempel et al., 2013) or to Aβ-induced defects in axonal transport (Vossel et al., 2011).”
From Wild-Type, but Not Mutant N296H, Human Tau Restores Aβ-Mediated Inhibition of LTP in Tau−/− mice (2017) · cites this paper as Zempel et al., 2013
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“In primary neurons, we further observed that CIP2A promoted tau translocalization to dendrites and spines, which is considered to be the key event mediating the synaptic toxicity of tau (Pooler et al., 2014; Zempel et al., 2013).”
From CIP2A Causes Tau/APP Phosphorylation, Synaptopathy, and Memory Deficits in Alzheimer’s Disease (2018) · cites this paper as Zempel et al., 2013
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Metadata
- Authors
- Zempel, H., Luedtke, J., Kumar, Y., Biernat, J., Dawson, H., Mandelkow, E., & Mandelkow, E.
- Affiliations
- German Center for Neurodegenerative Diseases (DE)
- Duke Medical Center (US)
- Center of Advanced European Studies and Research (DE)
- Corresponding author
- Mandelkow, Eva‐Maria
- Venue
- The EMBO Journal
- Published
- 2013-09-24
- Volume
- 32
- Issue
- 22
- Pages
- 2920-2937
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC3831312
- OpenAlex
- W2122620510
- Cited by
- 283
- References
- 85
- Citations by year
- 2026: 15 · 2025: 18 · 2024: 23 · 2023: 15 · 2022: 24 · 2021: 17 · 2020: 25 · 2019: 16 · 2018: 22 · 2017: 18 · 2016: 34 · 2015: 26 · 2014: 26 · 2013: 3
- FWCI
- 20.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DZNE Pub (submittedVersion)
- Funders
- Wellcome Trust (089703)
- Deutsches Zentrum für Neurodegenerative Erkrankungen
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- amyloid-beta oligomers, tau protein, Alzheimer's disease, microtubule severing, spastin, synaptic damage, dendritic microtubules, MARK kinases, tau phosphorylation, synaptic loss, microtubule stabilization
- MeSH terms
- Spastin, Adenosine Triphosphatases, Animals, Cells, Cultured, Microtubules, Peptide Synthases, Synapses, Amyloid beta-Peptides, tau Proteins, Mice, Knockout, Glutamic Acid, Mice, Rats
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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