Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease

© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, p...

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Autores: García-Revilla, Juan, Boza-Serrano, Antonio, Jin, Yiyun, Vadukul, Devkee M., Soldán-Hidalgo, Jesús, Camprubí-Ferrer, Lluís, García-Cruzado, Marta, Martinsson, Isak, Klementieva, Oxana, Ruiz, Rocío, Aprile, Francesco A., Deierborg, Tomas, Venero, José L.
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/350461
Acesso em linha:http://hdl.handle.net/10261/350461
Access Level:acceso abierto
Palavra-chave:Parkinson’s disease (PD)
Galectin-3 (GAL3)
α-synuclein (αSYN)
Lewy body (LB)
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dc.title.none.fl_str_mv Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
title Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
spellingShingle Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
García-Revilla, Juan
Parkinson’s disease (PD)
Galectin-3 (GAL3)
α-synuclein (αSYN)
Lewy body (LB)
title_short Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
title_full Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
title_fullStr Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
title_full_unstemmed Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
title_sort Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s disease
dc.creator.none.fl_str_mv García-Revilla, Juan
Boza-Serrano, Antonio
Jin, Yiyun
Vadukul, Devkee M.
Soldán-Hidalgo, Jesús
Camprubí-Ferrer, Lluís
García-Cruzado, Marta
Martinsson, Isak
Klementieva, Oxana
Ruiz, Rocío
Aprile, Francesco A.
Deierborg, Tomas
Venero, José L.
author García-Revilla, Juan
author_facet García-Revilla, Juan
Boza-Serrano, Antonio
Jin, Yiyun
Vadukul, Devkee M.
Soldán-Hidalgo, Jesús
Camprubí-Ferrer, Lluís
García-Cruzado, Marta
Martinsson, Isak
Klementieva, Oxana
Ruiz, Rocío
Aprile, Francesco A.
Deierborg, Tomas
Venero, José L.
author_role author
author2 Boza-Serrano, Antonio
Jin, Yiyun
Vadukul, Devkee M.
Soldán-Hidalgo, Jesús
Camprubí-Ferrer, Lluís
García-Cruzado, Marta
Martinsson, Isak
Klementieva, Oxana
Ruiz, Rocío
Aprile, Francesco A.
Deierborg, Tomas
Venero, José L.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Michael J. Fox Foundation for Parkinson's Research
Lund University
Hospital Clínic de Barcelona
Institut d'Investigacions Biomèdiques August Pi i Sunyer
Universidad de Barcelona
Ministerio de Universidades (España)
European Commission
Dementia Association (Sweden)
Swedish Brain Foundation
Crafoord Foundation
Olle Engkvist Foundation
Gamla Tjänarinnor Foundation
Swedish Medical Research Council
Swedish Parkinson Foundation
Fredrik O Ingrid Thurings Foundation
Swedish National Association for Social and Mental Health
Swedish Research Council
Ministerio de Ciencia e Innovación (España)
Agencia Estatal de Investigación (España)
Junta de Andalucía
UK Research and Innovation
Alzheimer's Research UK
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Parkinson’s disease (PD)
Galectin-3 (GAL3)
α-synuclein (αSYN)
Lewy body (LB)
topic Parkinson’s disease (PD)
Galectin-3 (GAL3)
α-synuclein (αSYN)
Lewy body (LB)
description © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
publishDate 2023
dc.date.none.fl_str_mv 2023
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
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status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/350461
url http://hdl.handle.net/10261/350461
dc.language.none.fl_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-124096OB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1007/s00401-023-02585-x
https://doi.org/10.1007/s00401-023-02585-x

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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dc.publisher.none.fl_str_mv Springer Nature
publisher.none.fl_str_mv Springer Nature
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spelling Galectin-3 shapes toxic alpha-synuclein strains in Parkinson’s diseaseGarcía-Revilla, JuanBoza-Serrano, AntonioJin, YiyunVadukul, Devkee M.Soldán-Hidalgo, JesúsCamprubí-Ferrer, LluísGarcía-Cruzado, MartaMartinsson, IsakKlementieva, OxanaRuiz, RocíoAprile, Francesco A.Deierborg, TomasVenero, José L.Parkinson’s disease (PD)Galectin-3 (GAL3)α-synuclein (αSYN)Lewy body (LB)© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.Parkinson’s Disease (PD) is a neurodegenerative and progressive disorder characterised by intracytoplasmic inclusions called Lewy bodies (LB) and degeneration of dopaminergic neurons in the substantia nigra (SN). Aggregated α-synuclein (αSYN) is known to be the main component of the LB. It has also been reported to interact with several proteins and organelles. Galectin-3 (GAL3) is known to have a detrimental function in neurodegenerative diseases. It is a galactose-binding protein without known catalytic activity and is expressed mainly by activated microglial cells in the central nervous system (CNS). GAL3 has been previously found in the outer layer of the LB in post-mortem brains. However, the role of GAL3 in PD is yet to be elucidated. In post-mortem samples, we identified an association between GAL3 and LB in all the PD subjects studied. GAL3 was linked to less αSYN in the LB outer layer and other αSYN deposits, including pale bodies. GAL3 was also associated with disrupted lysosomes. In vitro studies demonstrate that exogenous recombinant Gal3 is internalised by neuronal cell lines and primary neurons where it interacts with endogenous αSyn fibrils. In addition, aggregation experiments show that Gal3 affects spatial propagation and the stability of pre-formed αSyn fibrils resulting in short, amorphous toxic strains. To further investigate these observations in vivo, we take advantage of WT and Gal3KO mice subjected to intranigral injection of adenovirus overexpressing human αSyn as a PD model. In line with our in vitro studies, under these conditions, genetic deletion of GAL3 leads to increased intracellular αSyn accumulation within dopaminergic neurons and remarkably preserved dopaminergic integrity and motor function. Overall, our data suggest a prominent role for GAL3 in the aggregation process of αSYN and LB formation, leading to the production of short species to the detriment of larger strains which triggers neuronal degeneration in a mouse model of PD.This work was supported by The Michael J. Fox Foundation For Parkinson's Research (Grant ID: 11902). DLB samples were kindly provided by Elisabet Englund (Lund University) and PD samples were obtained with the help of Raquel Sánchez-Valle (Hospital Clínic de Barcelona, IDIBAPS, Universitat de Barcelona). J.G-R is granted by Spanish Ministerio de Universidades/NexGenerationEU/Ayudas Margarita Salas (20117) and Swedish Demensfonden. The Strategic Research Area MultiPark (Multidisciplinary Research in neurodegenerative diseases) at Lund University, the Swedish Brain Foundation, Crafoord Foundation, Swedish Dementia Association, G&J Kock Foundation, Olle Engkvist Foundation, Gamla Tjänarinnor Foundation, the Swedish Medical Research Council, the Swedish Parkinson Foundation, the Swedish Parkinson Research Foundation the A.E. Berger Foundation, the Thurings Foundation, and the Swedish mental health foundation to T.D., I.M., and The Swedish Research Council (International postdoc, 2019-06333) to A.B-S. We also thank the Spanish Ministerio de Ciencia e Innovación/FEDER/UE/PID2021-124096OB-I00; the Spanish Junta de Andalucia/FEDER/EU P18-RT-1372, the Spanish FEDER I + D + i-USE US-1264806, and the Agencia Española de Investigación PID2021-124096OB-I00 to J.L.V, and R.R. We thank the Agencia Española de Investigación PID2021-124096OB-I00 and the Spanish Junta de Andalucia /FEDER/EU P18-RT-1372. FAA is grateful to UK Research and Innovation (Future Leaders Fellowship MR/S033947/1), Alzheimer’s Society, UK (Grant 511), and Alzheimer’s Research UK (ARUK-PG2019B-020) for the support.Open access funding provided by Lund University.Peer reviewedSpringer NatureMichael J. Fox Foundation for Parkinson's ResearchLund UniversityHospital Clínic de BarcelonaInstitut d'Investigacions Biomèdiques August Pi i SunyerUniversidad de BarcelonaMinisterio de Universidades (España)European CommissionDementia Association (Sweden)Swedish Brain FoundationCrafoord FoundationOlle Engkvist FoundationGamla Tjänarinnor FoundationSwedish Medical Research CouncilSwedish Parkinson FoundationFredrik O Ingrid Thurings FoundationSwedish National Association for Social and Mental HealthSwedish Research CouncilMinisterio de Ciencia e Innovación (España)Agencia Estatal de Investigación (España)Junta de AndalucíaUK Research and InnovationAlzheimer's Research UKConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/350461reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-124096OB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-124096OB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-124096OB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at https://doi.org/10.1007/s00401-023-02585-xhttps://doi.org/10.1007/s00401-023-02585-xSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3504612026-05-22T06:33:51Z
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