Living Neurons with Tau Filaments Aberrantly Expose Phosphatidylserine and Are Phagocytosed by Microglia
Open accessAbstract
Tau protein forms insoluble filamentous inclusions that are closely associated with nerve cell death in many neurodegenerative diseases. How neurons die in these tauopathies is unclear. We report that living neurons with tau inclusions from P301S-tau mice expose abnormally high amounts of phosphatidylserine because of the production of reactive oxygen species (ROS). Consequently, co-cultured phagocytes (BV2 cells or primary microglia) identify and phagocytose the living neurons, thereby engulfing insoluble tau inclusions. To facilitate engulfment, neurons induce contacting microglia to secrete the opsonin milk-fat-globule EGF-factor-8 (MFGE8) and nitric oxide (NO), whereas neurons with tau inclusions are rescued when MFGE8 or NO production is prevented. MFGE8 expression is elevated in transgenic P301S-tau mouse brains with tau inclusions and in tau inclusion-rich brain regions of several human tauopathies, indicating shared mechanisms of disease. Preventing phagocytosis of living neurons will preserve them for treatments that inhibit tau aggregation and toxicity.
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Microglia can phagocytose tau-laden synapses or entire neurons, promoting neurodegeneration and memory loss.
“Microglia can phagocytose tau-laden synapses or entire neurons [36, 75], promoting neurodegeneration and memory loss.”
From Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function (2022) · cites this paper as [36]
The Results section (‘Phagocytes Engulf Neurons with Tau Inclusions that Expose PS’; page not provided) reports that microglia phagocytose neurons with tau inclusions, causing neuronal loss. The Discussion links this process to neurodegeneration. Our copy does not show phagocytosis of tau-laden synapses or establish that this process causes memory loss. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMicroglia can internalise aggregated or hyperphosphorylated tau for degradation, but can also release incompletely degraded forms into extracellular space, promoting tau spread.
“human and microglia can internalise aggregated or hyperphosphorylated tau for protein degradation, they can also release incompletely degraded or un-neutralised forms back it into the extracellular space, promoting the spread of tau [12, 32, 36, 108, 153]”
From Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function (2022) · cites this paper as [36]
The Results section, “Insoluble Tau Inclusions Are Transferred into Microglia after Phagocytosis” (page unavailable), shows that microglia engulf neurons containing insoluble tau aggregates. The Introduction mentions a possible role for microglial phagocytosis in tau spreading, but the paper does not establish tau degradation or the release of incompletely degraded tau into extracellular space. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMicroglia can phagocytize live neurons containing tau inclusions in addition to free extracellular tau.
“Notably, microglia can even phagocytize live neurons containing tau inclusions in addition to free extracellular tau.391”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [391]
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- Authors
- Brelstaff, J., Tolkovsky, A. M., Ghetti, B., Goedert, M., & Spillantini, M. G.
- Affiliations
- University of Cambridge (GB)
- Indiana University Indianapolis (US)
- MRC Laboratory of Molecular Biology (GB)
- Corresponding author
- Tolkovsky, Aviva M.
- Spillantini, Maria Grazia
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2018-08
- Volume
- 24
- Issue
- 8
- Pages
- 1939-1948.e4
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC6161320
- OpenAlex
- W2888349482
- Cited by
- 195
- References
- 54
- Citations by year
- 2026: 14 · 2025: 22 · 2024: 27 · 2023: 24 · 2022: 19 · 2021: 42 · 2020: 30 · 2019: 15 · 2018: 2
- FWCI
- 15.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion, cc-by)
- PubMed Central (acceptedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Alzheimer’s Research UK (P30-AG010133)
- Eberhard Karls Universität Tübingen (NC/L000741/1)
- National Institutes of Health (MC_U105184291)
- Université de Recherche Paris Sciences et Lettres
- Wellcome Trust (100574/Z/12/Z)
- National Centre for the Replacement Refinement and Reduction of Animals in Research (PG2011-20)
- UCLH Biomedical Research Centre
- National Institute for Health and Care Research
- Medical Research Council
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- tau filaments, tauopathy, phosphatidylserine exposure, microglial phagocytosis, reactive oxygen species, MFG-E8, nitric oxide, opsonization, neuronal cell death, neurodegeneration, tau aggregation
- MeSH terms
- Animals, Humans, Neurons, Phagocytosis, Phosphatidylserines, tau Proteins, Microglia, Mice
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