Extracellular clusterin limits the uptake of α-synuclein fibrils by murine and human astrocytes.


Journal

Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785

Informations de publication

Date de publication:
03 2021
Historique:
received: 12 06 2020
revised: 23 09 2020
accepted: 29 09 2020
pubmed: 13 10 2020
medline: 14 1 2022
entrez: 12 10 2020
Statut: ppublish

Résumé

The progressive neuropathological damage seen in Parkinson's disease (PD) is thought to be related to the spreading of aggregated forms of α-synuclein. Clearance of extracellular α-synuclein released by degenerating neurons may be therefore a key mechanism to control the concentration of α-synuclein in the extracellular space. Several molecular chaperones control misfolded protein accumulation in the extracellular compartment. Among these, clusterin, a glycoprotein associated with Alzheimer's disease, binds α-synuclein aggregated species and is present in Lewy bodies, intraneuronal aggregates mainly composed by fibrillary α-synuclein. In this study, using murine primary astrocytes with clusterin genetic deletion, human-induced pluripotent stem cell (iPSC)-derived astrocytes with clusterin silencing and two animal models relevant for PD we explore how clusterin affects the clearance of α-synuclein aggregates by astrocytes. Our findings showed that astrocytes take up α-synuclein preformed fibrils (pffs) through dynamin-dependent endocytosis and that clusterin levels are modulated in the culture media of cells upon α-synuclein pffs exposure. Specifically, we found that clusterin interacts with α-synuclein pffs in the extracellular compartment and the clusterin/α-synuclein complex can be internalized by astrocytes. Mechanistically, using clusterin knock-out primary astrocytes and clusterin knock-down hiPSC-derived astrocytes we observed that clusterin limits the uptake of α-synuclein pffs by cells. Interestingly, we detected increased levels of clusterin in the adeno-associated virus- and the α-synuclein pffs- injected mouse model, suggesting a crucial role of this chaperone in the pathogenesis of PD. Overall, our observations indicate that clusterin can limit the uptake of extracellular α-synuclein aggregates by astrocytes and, hence, contribute to the spreading of Parkinson pathology.

Identifiants

pubmed: 33045109
doi: 10.1002/glia.23920
pmc: PMC7821254
doi:

Substances chimiques

Clusterin 0
alpha-Synuclein 0

Types de publication

Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

681-696

Informations de copyright

© 2020 The Authors. GLIA published by Wiley Periodicals LLC.

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Auteurs

Alice Filippini (A)

Unit of Biology and Genetics, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Veronica Mutti (V)

Unit of Pharmacology, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Gaia Faustini (G)

Unit of Pharmacology, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Francesca Longhena (F)

Unit of Pharmacology, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Ileana Ramazzina (I)

Department of Medicine and Surgery, University of Parma, Parma, Italy.

Federica Rizzi (F)

Department of Medicine and Surgery, University of Parma, Parma, Italy.

Alice Kaganovich (A)

Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

Dorien A Roosen (DA)

Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

Natalie Landeck (N)

Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

Megan Duffy (M)

Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

Isabella Tessari (I)

Department of Biology, University of Padova, Padova, Italy.

Federica Bono (F)

Laboratory of Personalized and Preventive Medicine, University of Brescia, Brescia, Italy.

Chiara Fiorentini (C)

Unit of Pharmacology, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Elisa Greggio (E)

Department of Biology, University of Padova, Padova, Italy.

Luigi Bubacco (L)

Department of Biology, University of Padova, Padova, Italy.

Arianna Bellucci (A)

Laboratory of Personalized and Preventive Medicine, University of Brescia, Brescia, Italy.

Mariacristina Missale (M)

Unit of Pharmacology, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Mark R Cookson (MR)

Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, Maryland, USA.

Massimo Gennarelli (M)

Unit of Biology and Genetics, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
Genetics Unit, IRCCS Istituto Centro S. Giovanni di Dio Fatebenefratelli, Brescia, Italy.

Isabella Russo (I)

Unit of Biology and Genetics, Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
Genetics Unit, IRCCS Istituto Centro S. Giovanni di Dio Fatebenefratelli, Brescia, Italy.

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Classifications MeSH