Glucocerebrosidase is imported into mitochondria and preserves complex I integrity and energy metabolism.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
06 04 2023
Historique:
received: 24 04 2022
accepted: 17 03 2023
medline: 10 4 2023
entrez: 6 4 2023
pubmed: 7 4 2023
Statut: epublish

Résumé

Mutations in GBA1, the gene encoding the lysosomal enzyme β-glucocerebrosidase (GCase), which cause Gaucher's disease, are the most frequent genetic risk factor for Parkinson's disease (PD). Here, we employ global proteomic and single-cell genomic approaches in stable cell lines as well as induced pluripotent stem cell (iPSC)-derived neurons and midbrain organoids to dissect the mechanisms underlying GCase-related neurodegeneration. We demonstrate that GCase can be imported from the cytosol into the mitochondria via recognition of internal mitochondrial targeting sequence-like signals. In mitochondria, GCase promotes the maintenance of mitochondrial complex I (CI) integrity and function. Furthermore, GCase interacts with the mitochondrial quality control proteins HSP60 and LONP1. Disease-associated mutations impair CI stability and function and enhance the interaction with the mitochondrial quality control machinery. These findings reveal a mitochondrial role of GCase and suggest that defective CI activity and energy metabolism may drive the pathogenesis of GCase-linked neurodegeneration.

Identifiants

pubmed: 37024507
doi: 10.1038/s41467-023-37454-4
pii: 10.1038/s41467-023-37454-4
pmc: PMC10079970
doi:

Substances chimiques

Glucosylceramidase EC 3.2.1.45
alpha-Synuclein 0
LONP1 protein, human EC 3.4.21.-
Mitochondrial Proteins 0
ATP-Dependent Proteases EC 3.4.21.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1930

Informations de copyright

© 2023. The Author(s).

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Auteurs

Pascale Baden (P)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Maria Jose Perez (MJ)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Hariam Raji (H)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Federico Bertoli (F)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Stefanie Kalb (S)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

María Illescas (M)

Instituto de Investigación Hospital 12 de Octubre (i + 12), Madrid, 28041, Spain.

Fokion Spanos (F)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Claudio Giuliano (C)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Unit of Cellular and Molecular Neurobiology, IRCCS Mondino Foundation, 27100, Pavia, Italy.

Alessandra Maria Calogero (AM)

Department of Biosciences, Center of Excellence on Neurodegenerative Diseases, Università degli Studi di Milano, Milan, Italy.

Marvin Oldrati (M)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.

Hannah Hebestreit (H)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Graziella Cappelletti (G)

Department of Biosciences, Center of Excellence on Neurodegenerative Diseases, Università degli Studi di Milano, Milan, Italy.

Kathrin Brockmann (K)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Thomas Gasser (T)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Anthony H V Schapira (AHV)

Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA.
Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, Royal Free Campus, London, NW3 2PF, UK.

Cristina Ugalde (C)

Instituto de Investigación Hospital 12 de Octubre (i + 12), Madrid, 28041, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), U723, Madrid, Spain.

Michela Deleidi (M)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany. michela.deleidi@institutimagine.org.
Department of Neurodegenerative Diseases, Center of Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany. michela.deleidi@institutimagine.org.
Aligning Science Across Parkinson's (ASAP) Collaborative Research Network, Chevy Chase, MD, 20815, USA. michela.deleidi@institutimagine.org.
Institut Imagine, INSERM UMR1163 Paris Cite' University, 24 boulevard du Montparnasse, 75015, Paris, France. michela.deleidi@institutimagine.org.

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