Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids

Abstract Parkinson’s disease, an aging-associated neurodegenerative disorder, is characterised by nigrostriatal pathway dysfunction caused by the gradual loss of dopaminergic neurons in the substantia nigra pars compacta of the midbrain. Human in vitro models are enabling the study of the dopaminerg...

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Main Authors: Kyriaki Barmpa, Claudia Saraiva, Diego Lopez-Pigozzi, Gemma Gomez-Giro, Elisa Gabassi, Sarah Spitz, Konstanze Brandauer, Juan E. Rodriguez Gatica, Paul Antony, Graham Robertson, Rahman Sabahi-Kaviani, Alessandro Bellapianta, Florentia Papastefanaki, Regina Luttge, Ulrich Kubitscheck, Ahmad Salti, Peter Ertl, Mario Bortolozzi, Rebecca Matsas, Frank Edenhofer, Jens C. Schwamborn
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07273-4
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author Kyriaki Barmpa
Claudia Saraiva
Diego Lopez-Pigozzi
Gemma Gomez-Giro
Elisa Gabassi
Sarah Spitz
Konstanze Brandauer
Juan E. Rodriguez Gatica
Paul Antony
Graham Robertson
Rahman Sabahi-Kaviani
Alessandro Bellapianta
Florentia Papastefanaki
Regina Luttge
Ulrich Kubitscheck
Ahmad Salti
Peter Ertl
Mario Bortolozzi
Rebecca Matsas
Frank Edenhofer
Jens C. Schwamborn
author_facet Kyriaki Barmpa
Claudia Saraiva
Diego Lopez-Pigozzi
Gemma Gomez-Giro
Elisa Gabassi
Sarah Spitz
Konstanze Brandauer
Juan E. Rodriguez Gatica
Paul Antony
Graham Robertson
Rahman Sabahi-Kaviani
Alessandro Bellapianta
Florentia Papastefanaki
Regina Luttge
Ulrich Kubitscheck
Ahmad Salti
Peter Ertl
Mario Bortolozzi
Rebecca Matsas
Frank Edenhofer
Jens C. Schwamborn
author_sort Kyriaki Barmpa
collection DOAJ
description Abstract Parkinson’s disease, an aging-associated neurodegenerative disorder, is characterised by nigrostriatal pathway dysfunction caused by the gradual loss of dopaminergic neurons in the substantia nigra pars compacta of the midbrain. Human in vitro models are enabling the study of the dopaminergic neurons’ loss, but not the dysregulation within the dopaminergic network in the nigrostriatal pathway. Additionally, these models do not incorporate aging characteristics which potentially contribute to the development of Parkinson’s disease. Here we present a nigrostriatal pathway model based on midbrain-striatum assembloids with inducible aging. We show that these assembloids can develop characteristics of the nigrostriatal connectivity, with catecholamine release from the midbrain to the striatum and synapse formation between midbrain and striatal neurons. Moreover, Progerin-overexpressing assembloids acquire aging traits that lead to early neurodegenerative phenotypes. This model shall help to reveal the contribution of aging as well as nigrostriatal connectivity to the onset and progression of Parkinson’s disease.
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spelling doaj-art-01a3e63dcff24b67a4571fd2ecb5411b2024-11-24T12:39:07ZengNature PortfolioCommunications Biology2399-36422024-11-017111910.1038/s42003-024-07273-4Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloidsKyriaki Barmpa0Claudia Saraiva1Diego Lopez-Pigozzi2Gemma Gomez-Giro3Elisa Gabassi4Sarah Spitz5Konstanze Brandauer6Juan E. Rodriguez Gatica7Paul Antony8Graham Robertson9Rahman Sabahi-Kaviani10Alessandro Bellapianta11Florentia Papastefanaki12Regina Luttge13Ulrich Kubitscheck14Ahmad Salti15Peter Ertl16Mario Bortolozzi17Rebecca Matsas18Frank Edenhofer19Jens C. Schwamborn20Developmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgDevelopmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgDepartment of Physics and Astronomy “G. Galilei”, University of PaduaDevelopmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgGenomics, Stem Cell & Regenerative Medicine Group and CMBI, Institute of Molecular Biology, University of InnsbruckInstitute of Applied Synthetic Chemistry, Vienna University of TechnologyInstitute of Applied Synthetic Chemistry, Vienna University of TechnologyClausius Institute of Physical and Theoretical Chemistry, University of BonnDevelopmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgDevelopmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgEindhoven University of Technology, MicrosystemsJohannes Kepler University Linz, Kepler University Hospital, University Clinic for Ophthalmology and OptometryLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Hellenic Pasteur InstituteEindhoven University of Technology, MicrosystemsClausius Institute of Physical and Theoretical Chemistry, University of BonnGenomics, Stem Cell & Regenerative Medicine Group and CMBI, Institute of Molecular Biology, University of InnsbruckInstitute of Applied Synthetic Chemistry, Vienna University of TechnologyDepartment of Physics and Astronomy “G. Galilei”, University of PaduaLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Hellenic Pasteur InstituteGenomics, Stem Cell & Regenerative Medicine Group and CMBI, Institute of Molecular Biology, University of InnsbruckDevelopmental and Cellular Biology, Luxembourg Centre for Systems Biomedicine, University of LuxembourgAbstract Parkinson’s disease, an aging-associated neurodegenerative disorder, is characterised by nigrostriatal pathway dysfunction caused by the gradual loss of dopaminergic neurons in the substantia nigra pars compacta of the midbrain. Human in vitro models are enabling the study of the dopaminergic neurons’ loss, but not the dysregulation within the dopaminergic network in the nigrostriatal pathway. Additionally, these models do not incorporate aging characteristics which potentially contribute to the development of Parkinson’s disease. Here we present a nigrostriatal pathway model based on midbrain-striatum assembloids with inducible aging. We show that these assembloids can develop characteristics of the nigrostriatal connectivity, with catecholamine release from the midbrain to the striatum and synapse formation between midbrain and striatal neurons. Moreover, Progerin-overexpressing assembloids acquire aging traits that lead to early neurodegenerative phenotypes. This model shall help to reveal the contribution of aging as well as nigrostriatal connectivity to the onset and progression of Parkinson’s disease.https://doi.org/10.1038/s42003-024-07273-4
spellingShingle Kyriaki Barmpa
Claudia Saraiva
Diego Lopez-Pigozzi
Gemma Gomez-Giro
Elisa Gabassi
Sarah Spitz
Konstanze Brandauer
Juan E. Rodriguez Gatica
Paul Antony
Graham Robertson
Rahman Sabahi-Kaviani
Alessandro Bellapianta
Florentia Papastefanaki
Regina Luttge
Ulrich Kubitscheck
Ahmad Salti
Peter Ertl
Mario Bortolozzi
Rebecca Matsas
Frank Edenhofer
Jens C. Schwamborn
Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
Communications Biology
title Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
title_full Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
title_fullStr Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
title_full_unstemmed Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
title_short Modeling early phenotypes of Parkinson’s disease by age-induced midbrain-striatum assembloids
title_sort modeling early phenotypes of parkinson s disease by age induced midbrain striatum assembloids
url https://doi.org/10.1038/s42003-024-07273-4
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