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Investigating the neuronal role of the proteasomal ATPase subunit gene PSMC5 in neurodevelopmental proteasomopathies

Title: Investigating the neuronal role of the proteasomal ATPase subunit gene PSMC5 in neurodevelopmental proteasomopathies
Authors: Küry,Sébastien; Stanton,Janelle E; van Woerden,Geeske M; Bosc-Rosati,Amélie; Hsieh,Tzung-Chien; Bray,Lise; Oloudé,Marielle; Rosenfelt,Cory; Scott-Boyer,Marie Pier; Most,Victoria; Wang,Tianyun; Papendorf,Jonas J; de Konink,Charlotte; Deb,Wallid; Vignard,Virginie; Studencka-Turski,Maja; Besnard,Thomas; Hajdukowicz,Anna M; Thiel,Franziska G; Wolfgramm,Sophie; Florenceau,Laëtitia; Cuinat,Silvestre; Marsac,Sylvain; Verrès,Yann; Dangoumau,Audrey; Poirier,Léa; Wentzensen,Ingrid M; Tuttle,Annabelle; Forster,Cara; Striesow,Johanna; Golnik,Richard; Ortiz,Damara; Jenkins,Laura; Rosenfeld,Jill A; Ziegler,Alban; Houdayer,Clara; Bonneau,Dominique; Torti,Erin; Begtrup,Amber; Monaghan,Kristin G; Mullegama,Sureni V; Volker-Touw,Catharina M L Nienke; van Gassen, Koen L I; Oegema, Renske; de Pagter, Mirjam S; Steindl,Katharina; Rauch,Anita; Ivanovski,Ivan; McDonald,Kimberly; Boothe,Emily; Dauber,Andrew; Baker,Janice; Fabie,Noelle Andrea V; Bernier,Raphael A; Turner,Tychele N; Srivastava,Siddharth; Dies,Kira A; Swanson,Lindsay C; Costin,Carrie; Abdulrazak,Alali; Jobling,Rebekah K; Pappas,John; Rabin,Rachel; Niyazov,Dmitriy; Chun-Hui Tsai,Anne; Kovak,Karen; Beck,David B; Malicdan,May Christine V; Adams,David R; Wolfe,Lynne; Ganetzky,Rebecca D; Muraresku,Colleen C; Babikyan,Davit; Sedláček,Zdeněk; Hančárová,Miroslava; Timberlake,Andrew T; Saif,Hind Al; Nestler,Berkley; King,Kayla; Hajianpour,M J; Costain,Gregory; Prendergast,D'Arcy; Li,Chumei; Geneviève,David; Vitobello,Antonio; Sorlin,Arthur; Philippe,Christophe; Harel,Tamar; Toker,Ori; Sabir,Ataf; Lim,Derek; Hamilton,Mark J; Bryson,Lisa J; Cleary,Elaine; Weber,Sacha; Hoffman,Trevor L; Cueto-González,Anna M; Tizzano,Eduardo F; Gómez-Andrés,David; Codina-Solà,Marta; Ververi,Athina; Pavlidou,Efterpi; Lambropoulos,Alexandros; Garganis,Kyriakos; Rio,Marlène; Levy,Jonathan; Langas,Sarah J; McRae,Anne M; Lessard,Mathieu K; D'Agostino,Maria Daniela; De Bie,Isabelle; Wegler,Meret; Abou Jamra,Rami; Kamphausen,Susanne B; Bothe,Viktoria; Potocki,Lorraine; Olinger,Eric; Sznajer,Yves; Wiame,Elsa; Thompson,Michelle L; Schroeder,Molly C; Gooch,Catherine; Smith,Raphael A; Pandya,Arti; Busch,Larissa M; Völker,Uwe; Hammer,Elke; Wende,Kristian; Cogné,Benjamin; Isidor,Bertrand; Meiler,Jens; Ripoll,Clémentine; Bigou,Stéphanie; Laumonnier,Frédéric; Hildebrand,Peter W; Eichler,Evan E; McWalter,Kirsty; Krawitz,Peter M; Roux-Dalvai,Florence; Elgersma,Ype; Marcoux,Julien; Bousquet,Marie-Pierre; Droit,Arnaud; Poschmann,Jeremie; Grabrucker,Andreas M; Bolduc,Francois V; Bézieau,Stéphane; Ebstein,Frédéric; Krüger,Elke; Genetica Sectie Genoomdiagnostiek; Child Health; Genetica Klinische Genetica; Brain
Publication Year: 2025
Subject Terms: ATPases Associated with Diverse Cellular Activities/genetics; Adenosine Triphosphatases/genetics; Animals; Child; Drosophila Proteins/genetics; Drosophila melanogaster; Female; Humans; Male; Mitochondria/metabolism; Neurodevelopmental Disorders/genetics; Neurons/metabolism; Proteasome Endopeptidase Complex/genetics; Journal Article
Description: Neurodevelopmental proteasomopathies are a group of disorders caused by variants in proteasome subunit genes, that disrupt protein homeostasis and brain development through poorly characterized mechanisms. Here, we report 26 distinct variants in PSMC5, encoding the AAA⁺ ATPase subunit PSMC5/RPT6, in individuals with syndromic neurodevelopmental conditions. Combining genetic, multi-omics and biochemical approaches across cellular models and Drosophila, we unveil the essential role of proteasomes in sustaining key cellular processes. Loss of PSMC5/RPT6 function impairs proteasome activity, leading to protein aggregation, disruption of mitochondrial homeostasis, and dysregulation of lipid metabolism and immune signaling. It also compromises synaptic balance, neuritogenesis, and neural progenitor cell stemness, causing deficits in higher-order functions, including learning and locomotion. Pharmacological targeting of integrated stress response kinases reveals a mechanistic link between proteotoxic stress and spontaneous type I interferon activation. These findings expand our understanding of proteasome-dependent quality control in neurodevelopment and suggest potential therapeutic strategies for neurodevelopmental proteasomopathies.
Document Type: article in journal/newspaper
File Description: application/pdf
Language: English
ISSN: 2041-1723
Relation: https://dspace.library.uu.nl/handle/1874/468525
Availability: https://dspace.library.uu.nl/handle/1874/468525
Rights: info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.372AE5CB
Database: BASE