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Lewy pathology formation in patient-derived GBA1 Parkinson's disease midbrain organoids

Title: Lewy pathology formation in patient-derived GBA1 Parkinson's disease midbrain organoids
Authors: Frattini, Emanuele; Faustini, Gaia; Lopez, Gianluca; Carsana, Emma Veronica; Tosi, Mattia; Trezzi, Ilaria; Magni, Manuela; Soldà, Giulia; Straniero, Letizia; Facchi, Daniele; Samarani, Maura; Martá-Ariza, Mitchell; De Luca, Chiara Maria Giulia; Vezzoli, Elena; Pittaro, Alessandra; Stepanyan, Astghik; Silipigni, Rosamaria; Rosety, Isabel; Schwamborn, Jens C; Sardi, Sergio Pablo; Moda, Fabio; Corti, Stefania; Comi, Giacomo P; Blandini, Fabio; Tritsch, Nicolas X; Bortolozzi, Mario; Ferrero, Stefano; Cribiù, Fulvia Milena; Wisniewski, Thomas; Asselta, Rosanna; Aureli, Massimo; Bellucci, Arianna; Di Fonzo, Alessio
Contributors: Frattini Emanuele; Faustini Gaia; Lopez Gianluca; Carsana Emma Veronica; Tosi Mattia; Trezzi Ilaria; Magni Manuela; Soldà, Giulia; Straniero Letizia; Facchi Daniele; Samarani Maura; Martá-Ariza Mitchell; De Luca Chiara Maria Giulia; Vezzoli Elena; Pittaro Alessandra; Stepanyan Astghik; Silipigni Rosamaria; Rosety Isabel; Schwamborn Jens C; Sardi Sergio Pablo; Moda Fabio; Corti Stefania; Comi Giacomo P; Blandini Fabio; Tritsch Nicolas X; Bortolozzi Mario; Ferrero Stefano; Cribiù, Fulvia Milena; Wisniewski Thoma; Asselta Rosanna; Aureli Massimo; Bellucci Arianna; Di Fonzo Alessio
Publication Year: 2025
Collection: Università degli Studi di Brescia: OPENBS - Open Archive UniBS
Subject Terms: GBA1; Lewy bodie; Parkinson’s disease; ambroxol; glucocerebrosidase; midbrain organoids
Description: Fibrillary aggregation of α-synuclein in Lewy body inclusions and nigrostriatal dopaminergic neuron degeneration define Parkinson’s disease neuropathology. Mutations in GBA1, encoding glucocerebrosidase, are the most frequent genetic risk factor for Parkinson’s disease. However, the lack of reliable experimental models able to reproduce key neuropathological signatures has hampered clarification of the link between mutant glucocerebrosidase and Parkinson’s disease pathology. Here, we describe an innovative protocol for the generation of human induced pluripotent stem cell-derived midbrain organoids containing dopaminergic neurons with nigral identity that reproduce characteristics of advanced maturation. When applied to patients with GBA1-related Parkinson’s disease, this method enabled the differentiation of midbrain organoids recapitulating dopaminergic neuron loss and fundamental features of Lewy pathology observed in human brains, including the generation of α-synuclein fibrillary aggregates with seeding activity that also propagate pathology in healthy control organoids. Concurrently, we found that the retention of mutant glucocerebrosidase in the endoplasmic reticulum and increased levels of its substrate, glucosylceramide, are determinants of α-synuclein aggregation into Lewy body-like inclusions, and the reduction of glucocerebrosidase activity accelerated α-synuclein pathology by promoting fibrillary α-synuclein deposition. Finally, we demonstrated the efficacy of ambroxol and GZ667161 (two modulators of the glucocerebrosidase pathway in clinical development for the treatment of GBA1-related Parkinson’s disease) in reducing α-synuclein pathology in this model, supporting the use of midbrain organoids as a relevant preclinical platform for investigational drug screening.
Document Type: article in journal/newspaper
Language: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/39570889; info:eu-repo/semantics/altIdentifier/wos/WOS:001436835800001; volume:148; issue:4; firstpage:1242; lastpage:1257; numberofpages:16; journal:BRAIN; https://hdl.handle.net/11379/631187; https://academic.oup.com/brain/article/148/4/1242/7906568?login=true
DOI: 10.1093/brain/awae365
Availability: https://hdl.handle.net/11379/631187; https://doi.org/10.1093/brain/awae365; https://academic.oup.com/brain/article/148/4/1242/7906568?login=true
Rights: info:eu-repo/semantics/openAccess ; license:PUBBLICO - Pubblico con Copyright ; license uri:iris.PUB02
Accession Number: edsbas.1EFA8B15
Database: BASE