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

Publication date

2025-11-26

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

Editors

Advisors

Supervisors

Document Type

Article

Collections

Open Access logo

License

cc_by

Abstract

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.

Keywords

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

Citation

Küry, S, Stanton, J E, van Woerden, G M, Bosc-Rosati, A, Hsieh, T-C, Bray, L, Oloudé, M, Rosenfelt, C, Scott-Boyer, M P, Most, V, Wang, T, Papendorf, J J, de Konink, C, Deb, W, Vignard, V, Studencka-Turski, M, Besnard, T, Hajdukowicz, A M, Thiel, F G, Wolfgramm, S, Florenceau, L, Cuinat, S, Marsac, S, Verrès, Y, Dangoumau, A, Poirier, L, Wentzensen, I M, Tuttle, A, Forster, C, Striesow, J, Golnik, R, Ortiz, D, Jenkins, L, Rosenfeld, J A, Ziegler, A, Houdayer, C, Bonneau, D, Torti, E, Begtrup, A, Monaghan, K G, Mullegama, S V, Volker-Touw, C M L N, van Gassen, K L I, Oegema, R, de Pagter, M S, Steindl, K, Rauch, A, Ivanovski, I, McDonald, K, Boothe, E, Dauber, A, Baker, J, Fabie, N A V, Bernier, R A, Turner, T N, Srivastava, S, Dies, K A, Swanson, L C, Costin, C, Abdulrazak, A, Jobling, R K, Pappas, J, Rabin, R, Niyazov, D, Chun-Hui Tsai, A, Kovak, K, Beck, D B, Malicdan, M C V, Adams, D R, Wolfe, L, Ganetzky, R D, Muraresku, C C, Babikyan, D, Sedláček, Z, Hančárová, M, Timberlake, A T, Saif, H A, Nestler, B, King, K, Hajianpour, M J, Costain, G, Prendergast, DA, Li, C, Geneviève, D, Vitobello, A, Sorlin, A, Philippe, C, Harel, T, Toker, O, Sabir, A, Lim, D, Hamilton, M J, Bryson, L J, Cleary, E, Weber, S, Hoffman, T L, Cueto-González, A M, Tizzano, E F, Gómez-Andrés, D, Codina-Solà, M, Ververi, A, Pavlidou, E, Lambropoulos, A, Garganis, K, Rio, M, Levy, J, Langas, S J, McRae, A M, Lessard, M K, D'Agostino, M D, De Bie, I, Wegler, M, Abou Jamra, R, Kamphausen, S B, Bothe, V, Potocki, L, Olinger, E, Sznajer, Y, Wiame, E, Thompson, M L, Schroeder, M C, Gooch, C, Smith, R A, Pandya, A, Busch, L M, Völker, U, Hammer, E, Wende, K, Cogné, B, Isidor, B, Meiler, J, Ripoll, C, Bigou, S, Laumonnier, F, Hildebrand, P W, Eichler, E E, McWalter, K, Krawitz, P M, Roux-Dalvai, F, Elgersma, Y, Marcoux, J, Bousquet, M-P, Droit, A, Poschmann, J, Grabrucker, A M, Bolduc, F V, Bézieau, S, Ebstein, F & Krüger, E 2025, 'Investigating the neuronal role of the proteasomal ATPase subunit gene PSMC5 in neurodevelopmental proteasomopathies', Nature Communications, vol. 16, no. 1, 10545, pp. 10545. https://doi.org/10.1038/s41467-025-65556-8