α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model

Abstract Understanding the progression of α‐synuclein pathology in neurodegenerative diseases such as Parkinson's disease (PD) is a longstanding challenge. Here, a novel midbrain–hindbrain‐assembloid model that recapitulates the spread of α‐synuclein pathology observed in PD patients, akin to B...

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Main Authors: Gemma Gomez‐Giro, Daniela Frangenberg, Daniela Vega, Alise Zagare, Kyriaki Barmpa, Paul M. A. Antony, Graham Robertson, Rahman Sabahi‐Kaviani, Kristian Haendler, Nathalie Kruse, Florentia Papastefanaki, Rebecca Matsas, Malte Spielmann, Regina Luttge, Jens C. Schwamborn
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202409040
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author Gemma Gomez‐Giro
Daniela Frangenberg
Daniela Vega
Alise Zagare
Kyriaki Barmpa
Paul M. A. Antony
Graham Robertson
Rahman Sabahi‐Kaviani
Kristian Haendler
Nathalie Kruse
Florentia Papastefanaki
Rebecca Matsas
Malte Spielmann
Regina Luttge
Jens C. Schwamborn
author_facet Gemma Gomez‐Giro
Daniela Frangenberg
Daniela Vega
Alise Zagare
Kyriaki Barmpa
Paul M. A. Antony
Graham Robertson
Rahman Sabahi‐Kaviani
Kristian Haendler
Nathalie Kruse
Florentia Papastefanaki
Rebecca Matsas
Malte Spielmann
Regina Luttge
Jens C. Schwamborn
author_sort Gemma Gomez‐Giro
collection DOAJ
description Abstract Understanding the progression of α‐synuclein pathology in neurodegenerative diseases such as Parkinson's disease (PD) is a longstanding challenge. Here, a novel midbrain–hindbrain‐assembloid model that recapitulates the spread of α‐synuclein pathology observed in PD patients, akin to Braak's hypothesis, is presented. Initially, the presence α‐synuclein pathology is demonstrated in the hindbrain organoids. Subsequently, sophisticated tissue engineering methods are employed to create midbrain–hindbrain assembloids. These assembloids allow investigation and description of the spreading of α‐synuclein pathology, as it progresses from the hindbrain components to the midbrain regions within the integrated structure. It is observed that an increase in α‐synuclein in the hindbrain can induce transfer of the pathology into the healthy midbrain, as well as cause changes at the synapse level. The presented model constitutes a robust in vitro platform for investigating the mechanisms underlying α‐synuclein spreading and disease progression, and holding potential for the screening of prospective therapeutics targeting the pathological propagation in PD and related synucleinopathies.
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spelling doaj-art-ff038201aa6d49a2a01f2cf86e2b3f432025-08-20T02:34:43ZengWileyAdvanced Science2198-38442025-05-011220n/an/a10.1002/advs.202409040α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid ModelGemma Gomez‐Giro0Daniela Frangenberg1Daniela Vega2Alise Zagare3Kyriaki Barmpa4Paul M. A. Antony5Graham Robertson6Rahman Sabahi‐Kaviani7Kristian Haendler8Nathalie Kruse9Florentia Papastefanaki10Rebecca Matsas11Malte Spielmann12Regina Luttge13Jens C. Schwamborn14Developmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgBioimaging Platform Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgDepartment of Mechanical Engineering Eindhoven University of Technology (TUE) Eindhoven 5612 AE The NetherlandsInstitute of Human Genetics Universitätsklinikum Schleswig–Holstein (UKSH) 23538 Lübeck GermanyInstitute of Human Genetics Universitätsklinikum Schleswig–Holstein (UKSH) 23538 Lübeck GermanyHuman Embryonic and Induced Pluripotent Stem Cell Unit Hellenic Pasteur Institute Athens 11521 GreeceHuman Embryonic and Induced Pluripotent Stem Cell Unit Hellenic Pasteur Institute Athens 11521 GreeceInstitute of Human Genetics Universitätsklinikum Schleswig–Holstein (UKSH) 23538 Lübeck GermanyDepartment of Mechanical Engineering Eindhoven University of Technology (TUE) Eindhoven 5612 AE The NetherlandsDevelopmental and Cellular Biology Luxembourg Centre for Systems Biomedicine University of Luxembourg Belvaux L‐4367 LuxembourgAbstract Understanding the progression of α‐synuclein pathology in neurodegenerative diseases such as Parkinson's disease (PD) is a longstanding challenge. Here, a novel midbrain–hindbrain‐assembloid model that recapitulates the spread of α‐synuclein pathology observed in PD patients, akin to Braak's hypothesis, is presented. Initially, the presence α‐synuclein pathology is demonstrated in the hindbrain organoids. Subsequently, sophisticated tissue engineering methods are employed to create midbrain–hindbrain assembloids. These assembloids allow investigation and description of the spreading of α‐synuclein pathology, as it progresses from the hindbrain components to the midbrain regions within the integrated structure. It is observed that an increase in α‐synuclein in the hindbrain can induce transfer of the pathology into the healthy midbrain, as well as cause changes at the synapse level. The presented model constitutes a robust in vitro platform for investigating the mechanisms underlying α‐synuclein spreading and disease progression, and holding potential for the screening of prospective therapeutics targeting the pathological propagation in PD and related synucleinopathies.https://doi.org/10.1002/advs.202409040α‐synucleinbrain organoidin vitro disease modelingParkinson's disease
spellingShingle Gemma Gomez‐Giro
Daniela Frangenberg
Daniela Vega
Alise Zagare
Kyriaki Barmpa
Paul M. A. Antony
Graham Robertson
Rahman Sabahi‐Kaviani
Kristian Haendler
Nathalie Kruse
Florentia Papastefanaki
Rebecca Matsas
Malte Spielmann
Regina Luttge
Jens C. Schwamborn
α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
Advanced Science
α‐synuclein
brain organoid
in vitro disease modeling
Parkinson's disease
title α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
title_full α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
title_fullStr α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
title_full_unstemmed α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
title_short α‐Synuclein Pathology Spreads in a Midbrain–Hindbrain Assembloid Model
title_sort α synuclein pathology spreads in a midbrain hindbrain assembloid model
topic α‐synuclein
brain organoid
in vitro disease modeling
Parkinson's disease
url https://doi.org/10.1002/advs.202409040
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