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Cited by 187Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchPrion Diseases and Protein Misfolding

From the prion-like propagation hypothesis to therapeutic strategies of anti-tau immunotherapy

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Colin, Morvane, Dujardin, Simon, Schraen-Maschke, Susanna, Meno-Tetang, Guy, Duyckaerts, Charles, Courade, Jean-Philippe, Buée, Luc·2020·Acta Neuropathologica
DOI 10.1007/s00401-019-02087-9PMC PMC6942016
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Abstract

The term “propagon” is used to define proteins that may transmit misfolding in vitro, in tissues or in organisms. Among propagons, misfolded tau is thought to be involved in the pathogenic mechanisms of various “tauopathies” that include Alzheimer's disease, progressive supranuclear palsy, and argyrophilic grain disease. Here, we review the available data in the literature and point out how the prion-like tau propagation has been extended from Alzheimer's disease to tauopathies. First, in Alzheimer’s disease, the progression of tau aggregation follows stereotypical anatomical stages which may be considered as spreading. The mechanisms of the propagation are now subject to intensive and controversial research. It has been shown that tau may be secreted in the interstitial fluid in an active manner as reflected by high and constant concentration of extracellular tau during Alzheimer’s pathology. Animal and cell models have been devised to mimic tau seeding and propagation, and despite their limitations, they have further supported to the prion-like propagation hypothesis. Finally, such new ways of thinking have led to different therapeutic strategies in anti-tau immunotherapy among tauopathies and have stimulated new clinical trials. However, it appears that the prion-like propagation hypothesis mainly relies on data obtained in Alzheimer’s disease. From this review, it appears that further studies are needed (1) to characterize extracellular tau species, (2) to find the right pathological tau species to target, (3) to follow in vivo tau pathology by brain imaging and biomarkers and (4) to interpret current clinical trial results aimed at reducing the progression of these pathologies. Such inputs will be essential to have a comprehensive view of these promising therapeutic strategies in tauopathies.

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  • Pathogenic forms of tau spread toxicity between cells through a prion-like mechanism involving seeded conformational change.

    “Pathogenic forms of tau spread toxicity between cells through a prion-like mechanism involving seeded conformational change (Colin et al. 2020, Frost et al. 2009).”

    From The Role of Retrotransposons and Endogenous Retroviruses in Age-Dependent Neurodegenerative Disorders (2024) · cites this paper as Colin et al. 2020

    The “Tau seeding” section says abnormal tau can convert normal proteins into a pathological form, and “Tau uptake/transfer” describes experimental cell-to-cell transfer and seeding in receiving cells. The paper supports prion-like propagation of tau pathology, but it does not establish that toxicity itself spreads between cells; it also notes that active cell-to-cell transfer has not been visualized in the human brain. The supplied passages have no page numbers. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Short fibrils and oligomers of tau can transfer from one neuron to another and spread pathology throughout the brain in a prion-like manner.

    “Over the past several years, it has become increasingly evident that short fibrils and oligomers of tau can transfer from one neuron to another and thereby spread pathology throughout the brain in a prion-like manner (4, 5, 6).”

    From MAP2 caps tau fibrils and inhibits aggregation (2023) · cites this paper as [6]

    The Tau uptake/transfer section reports cell-to-cell tau transfer in models and pathology appearing in distant, connected areas. It also describes experiments using oligomeric or fibrillar tau, but says those experiments bypass secretion from donor cells; the Tau secretion section says the propagative forms have not been identified. Thus the paper supports prion-like spread as a model, not the specific assertion that short fibrils and oligomers transfer between neurons and spread pathology throughout the brain. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

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Cited by

Sorted by citations

Authors
Colin, M., Dujardin, S., Schraen-Maschke, S., Meno-Tetang, G., Duyckaerts, C., Courade, J.-P., & Buée, L.
Affiliations
  • Inserm (FR)
  • Harvard University (US)
  • Centre National de la Recherche Scientifique (FR)
  • UCB Pharma (Belgium) (BE)
Corresponding author
  • Colin, Morvane
  • Buée, Luc
ORCID
Venue
Acta Neuropathologica
Publisher
Springer Science and Business Media LLC
Published
2019-11-04
Volume
139
Issue
1
Pages
3-25
ISSN
  • 0001-6322 (ISSN-L)
  • 1432-0533
DOI
10.1007/s00401-019-02087-9
PMC
PMC6942016
OpenAlex
W2989455730
Cited by
187
References
30
Citations by year
2026: 16 · 2025: 18 · 2024: 17 · 2023: 28 · 2022: 34 · 2021: 30 · 2020: 43
FWCI
3.15
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Neuropathologica (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Funders
  • Agence Nationale de la Recherche (ANR-14-CE13-0031, LabEx DISTALZ)
  • UCB
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Prion Diseases and Protein Misfolding
Keywords
tau propagation, prion-like propagation, tauopathy, Alzheimer's disease, progressive supranuclear palsy, argyrophilic grain disease, extracellular tau, tau seeding, tau aggregation, clinical trials, neuroimaging biomarkers
MeSH terms
Animals, Humans, Immunotherapy, Tauopathies, Proteostasis Deficiencies

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