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

Author

Listed:
  • Sébastien Küry

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Janelle E. Stanton

    (University of Limerick, Bernal Institute
    University of Limerick, Department of Biological Sciences)

  • Geeske M. van Woerden

    (Erasmus Medical Center, Department of Clinical Genetics
    Erasmus Medical Center, ENCORE Center of Expertise for Neurodevelopmental Disorders
    Erasmus Medical Center, Department of Neuroscience)

  • Amélie Bosc-Rosati

    (Université de Toulouse (UT), Institut de Pharmacologie et de Biologie Structurale (IPBS)
    Infrastructure Nationale de Protéomique, ProFI, UAR)

  • Tzung-Chien Hsieh

    (Rheinische Friedrich-Wilhelms-Universität Bonn, Institute for Genomic Statistics and Bioinformatics, University Hospital Bonn)

  • Lise Bray

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Marielle Oloudé

    (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology)

  • Cory Rosenfelt

    (University of Alberta, Department of Pediatrics)

  • Marie Pier Scott-Boyer

    (Centre de recherche du CHU de Québec-Université Laval)

  • Victoria Most

    (Leipzig University, Institute for Drug Discovery, Medical Faculty)

  • Tianyun Wang

    (Peking University Health Science Center, Department of Medical Genetics, Center for Medical Genetics
    Peking University; Key Laboratory for Neuroscience, Ministry of Education of China & National Health Commission of China, Neuroscience Research Institute
    Peking University Health Science Center, Autism Research Center)

  • Jonas J. Papendorf

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

  • Charlotte de Konink

    (Erasmus Medical Center, ENCORE Center of Expertise for Neurodevelopmental Disorders
    Erasmus Medical Center, Department of Neuroscience)

  • Wallid Deb

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Virginie Vignard

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Maja Studencka-Turski

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

  • Thomas Besnard

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Anna M. Hajdukowicz

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

  • Franziska G. Thiel

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

  • Sophie Wolfgramm

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

  • Laëtitia Florenceau

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Silvestre Cuinat

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Sylvain Marsac

    (Nantes Université, CHU Nantes, Service de Génétique Médicale)

  • Yann Verrès

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Audrey Dangoumau

    (Université de Tours, INSERM, Imaging Brain & Neuropsychiatry iBraiN U1253)

  • Léa Poirier

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Ingrid M. Wentzensen

    (GeneDx, LLC)

  • Annabelle Tuttle

    (GeneDx, LLC)

  • Cara Forster

    (Loyola University Chicago)

  • Johanna Striesow

    (Leibniz Institute for Plasma Science and Technology (INP))

  • Richard Golnik

    (Universität Leipzig, Department of Computer Science and Interdisciplinary Center for Bioinformatics, Bioinformatics Group)

  • Damara Ortiz

    (UPMC Children’s Hospital of Pittsburgh, One Children’s Hospital Drive)

  • Laura Jenkins

    (UPMC Children’s Hospital of Pittsburgh, One Children’s Hospital Drive)

  • Jill A. Rosenfeld

    (Baylor College of Medicine, Department of Molecular and Human Genetics
    Baylor Genetics Laboratory)

  • Alban Ziegler

    (University Hospital of Toulouse, Department of Medical Genetics)

  • Clara Houdayer

    (Service de Génétique médicale, CHU Angers)

  • Dominique Bonneau

    (Service de Génétique médicale, CHU Angers
    Angers University, Mitovasc, UMR CNRS 6015, INSERM U1083)

  • Erin Torti

    (GeneDx, LLC)

  • Amber Begtrup

    (GeneDx, LLC)

  • Kristin G. Monaghan

    (GeneDx, LLC)

  • Sureni V. Mullegama

    (GeneDx, LLC)

  • Catharina M. L. Nienke Volker-Touw

    (Utrecht University, Department of Genetics, University Medical Centre Utrecht)

  • Koen L. I. van Gassen

    (Utrecht University, Department of Genetics, University Medical Centre Utrecht)

  • Renske Oegema

    (Utrecht University, Department of Genetics, University Medical Centre Utrecht)

  • Mirjam S. de Pagter

    (Utrecht University, Department of Genetics, University Medical Centre Utrecht)

  • Katharina Steindl

    (University of Zürich, Institute of Medical Genetics)

  • Anita Rauch

    (University of Zürich, Institute of Medical Genetics
    University Children’s Hospital Zurich
    University of Zurich Research Priority Program ITINERARE: Innovative Therapies in Rare Diseases
    University of Zurich Research Priority Program AdaBD: Adaptive Brain Circuits in Development and Learning)

  • Ivan Ivanovski

    (University of Zürich, Institute of Medical Genetics)

  • Kimberly McDonald

    (University of Louisville School of Medicine, Norton Children’s Medical Group)

  • Emily Boothe

    (University of Mississippi Medical Center)

  • Andrew Dauber

    (The George Washington University School of Medicine and Health Sciences, Division of Endocrinology, Children’s National Hospital and Department of Pediatrics)

  • Janice Baker

    (Children’s Minnesota, Department of Medical Genetics and Genomics)

  • Noelle Andrea V. Fabie

    (Children’s Minnesota, Department of Medical Genetics and Genomics)

  • Raphael A. Bernier

    (University of Washington, Department of Psychiatry & Behavioral Sciences, Center on Human Development and Disability)

  • Tychele N. Turner

    (Washington University School of Medicine, Department of Genetics)

  • Siddharth Srivastava

    (Boston Children’s Hospital, Rosamund Stone Zander Translational Neuroscience Center, Department of Neurology)

  • Kira A. Dies

    (Boston Children’s Hospital, Rosamund Stone Zander Translational Neuroscience Center, Department of Neurology)

  • Lindsay C. Swanson

    (Boston Children’s Hospital, Rosamund Stone Zander Translational Neuroscience Center, Department of Neurology)

  • Carrie Costin

    (Akron Children’s Hospital, One Perkins Square, Department of Genetics)

  • Alali Abdulrazak

    (West Virginia University School of Medicine, One Medical Center Drive, Division of Genetics, Department of Pediatrics)

  • Rebekah K. Jobling

    (The Hospital for Sick Children, Division of Clinical and Metabolic Genetics)

  • John Pappas

    (NYU Grossman School of Medicine, Clinical Genetic Services, Department of Pediatrics
    NYU Orthopedic Hospital, Clinical Genetics)

  • Rachel Rabin

    (NYU Grossman School of Medicine, Clinical Genetic Services, Department of Pediatrics)

  • Dmitriy Niyazov

    (Duke University School of Medicine, Division of Medical Genetics, Department of Pediatrics)

  • Anne Chun-Hui Tsai

    (University of Illinois, Department of Pediatrics, College of Medicine)

  • Karen Kovak

    (Oregon Health and Sciences University, OHSU, Department of Molecular and Medical Genetics)

  • David B. Beck

    (New York University Grossman School of Medicine, Division of Rheumatology, Department of Medicine
    New York University Grossman School of Medicine, Center for Human Genetics and Genomics)

  • May Christine V. Malicdan

    (National Human Genome Research Institute, NIH, Medical Genetics Branch
    National Human Genome Research Institute, NIH, National Institutes of Health Undiagnosed Diseases Program)

  • David R. Adams

    (National Human Genome Research Institute, NIH, National Institutes of Health Undiagnosed Diseases Program)

  • Lynne Wolfe

    (National Human Genome Research Institute, NIH, National Institutes of Health Undiagnosed Diseases Program)

  • Rebecca D. Ganetzky

    (Children’s Hospital of Philadelphia, Mitochondrial Medicine Program, Division of Human Genetics
    Perelman School of Medicine, Department of Pediatrics, University of Pennsylvania)

  • Colleen C. Muraresku

    (Children’s Hospital of Philadelphia, Mitochondrial Medicine Program, Division of Human Genetics)

  • Davit Babikyan

    (Yerevan State Medical University after Mkhitar Heratsi, Department of Medical Genetics
    Center of Medical Genetics and Primary Health Care, Laboratory of Molecular Genetics)

  • Zdeněk Sedláček

    (Charles University 2nd Faculty of Medicine and University Hospital Motol, Department of Biology and Medical Genetics)

  • Miroslava Hančárová

    (Charles University 2nd Faculty of Medicine and University Hospital Motol, Department of Biology and Medical Genetics)

  • Andrew T. Timberlake

    (NYU Langone Medical Center, Wyss Department of Plastic Surgery)

  • Hind Al Saif

    (Virginia Commonwealth University School of Medicine, Department of Human and Molecular Genetics, Division of Clinical Genetics
    Virginia Commonwealth University School of Medicine, Department of Pediatrics, Division of Clinical Genetics)

  • Berkley Nestler

    (Virginia Commonwealth University School of Medicine, Department of Human and Molecular Genetics, Division of Clinical Genetics)

  • Kayla King

    (Virginia Commonwealth University School of Medicine, Department of Human and Molecular Genetics, Division of Clinical Genetics)

  • MJ Hajianpour

    (Albany Medical College, Division of Medical Genetics and Genomics, Department of Pediatrics)

  • Gregory Costain

    (The Hospital for Sick Children, Division of Clinical and Metabolic Genetics
    University of Toronto, Department of Molecular Genetics
    SickKids Research Institute, Program in Genetics and Genome Biology)

  • D’Arcy Prendergast

    (The Hospital for Sick Children, Division of Clinical and Metabolic Genetics
    University of Toronto, Department of Paediatrics, Temerty Faculty of Medicine)

  • Chumei Li

    (McMaster University Medical Center)

  • David Geneviève

    (Hôpital Arnaud de Villeneuve, Université Montpellier, Inserm U 1183, Centre de référence maladies rares anomalies du développement, Service de génétique médicale)

  • Antonio Vitobello

    (Université de Bourgogne Franche Comté, UMR 1231 GAD, Inserm
    CHU Dijon Bourgogne, Unité Fonctionnelle Innovation en Diagnostic Génomique des Maladies Rares, Fédération Hospitalo-Universitaire-TRANSLAD)

  • Arthur Sorlin

    (Université de Bourgogne Franche Comté, UMR 1231 GAD, Inserm
    CHU Dijon Bourgogne, Unité Fonctionnelle Innovation en Diagnostic Génomique des Maladies Rares, Fédération Hospitalo-Universitaire-TRANSLAD
    Centre Hospitalier Universitaire de Dijon, Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l’interrégion Est et FHU TRANSLAD)

  • Christophe Philippe

    (Université de Bourgogne Franche Comté, UMR 1231 GAD, Inserm
    CHU Dijon Bourgogne, Unité Fonctionnelle Innovation en Diagnostic Génomique des Maladies Rares, Fédération Hospitalo-Universitaire-TRANSLAD)

  • Tamar Harel

    (Hadassah Medical Organization, Department of Genetics
    Hebrew University of Jerusalem, Faculty of Medicine)

  • Ori Toker

    (Hebrew University of Jerusalem, Department of Pediatrics, Allergy and Clinical Immunology Unit, Shaare Zedek Medical Center, Faculty of Medicine)

  • Ataf Sabir

    (Birmingham Women’s and Children’s NHS Foundation Trust, Clinical Genetics Department
    University of Birmingham, Institute of Cancer and Genomic Sciences)

  • Derek Lim

    (Birmingham Women’s and Children’s NHS Foundation Trust, Clinical Genetics Department
    University of Birmingham, Institute of Cancer and Genomic Sciences)

  • Mark J. Hamilton

    (Queen Elizabeth University Hospital, West of Scotland Clinical Genetics Service)

  • Lisa J. Bryson

    (Queen Elizabeth University Hospital, West of Scotland Clinical Genetics Service)

  • Elaine Cleary

    (Western General Hospital, South East Scotland Genetics Service
    University of Edinburgh, Centre for Clinical Brain Sciences
    University of Edinburgh, UK Dementia Research Institute at University of Edinburgh)

  • Sacha Weber

    (Sorbonne Université, Service de Génétique Médicale, Hôpital Armand-Trousseau, APHP)

  • Trevor L. Hoffman

    (Southern California Kaiser Permanente Medical Group, Department of Genetics)

  • Anna M. Cueto-González

    (Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Department of Clinical and Molecular Genetics
    Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Medicine Genetics Group, Vall d’Hebron Institut de Recerca (VHIR))

  • Eduardo F. Tizzano

    (Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Department of Clinical and Molecular Genetics
    Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Medicine Genetics Group, Vall d’Hebron Institut de Recerca (VHIR))

  • David Gómez-Andrés

    (Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Pediatric Neurology, Vall d’Hebron Institut de Recerca (VHIR))

  • Marta Codina-Solà

    (Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Department of Clinical and Molecular Genetics
    Vall d’Hebron Hospital Universitari, Vall d’Hebron Barcelona Hospital Campus, Medicine Genetics Group, Vall d’Hebron Institut de Recerca (VHIR))

  • Athina Ververi

    (‘Papageorgiou’ General Hospital, Department of Genetics for Rare Diseases)

  • Efterpi Pavlidou

    (University Hospital of Ioannina, Department of Speech and Language Therapy)

  • Alexandros Lambropoulos

    (Aristotle University of Thessaloniki, ‘Papageorgiou’ General Hospital, Genetic Unit, 1st Department of Obstetrics and Gynecology, School of Medicine)

  • Kyriakos Garganis

    (St Luke’s Hospital, Epilepsy Unit)

  • Marlène Rio

    (Hôpital Necker-Enfants Malades, AP-HP, Service de Médecine Génomique des Maladies Rares)

  • Jonathan Levy

    (APHP-Robert Debré University Hospital, Department of Genetics
    Multi-site medical biology laboratory SeqOIA—FMG2025)

  • Sarah J. Langas

    (Ann & Robert H. Lurie Children’s Hospital of Chicago, Division of Genetics, Genomics and Metabolism
    Northwestern University Feinberg School of Medicine, Department of Pediatrics)

  • Anne M. McRae

    (Ann & Robert H. Lurie Children’s Hospital of Chicago, Division of Genetics, Genomics and Metabolism)

  • Mathieu K. Lessard

    (McGill University, Division of Medical Genetics, Department of Specialised Medicine, McGill University Health Centre, Department of Human Genetics)

  • Maria Daniela D’Agostino

    (McGill University, Division of Medical Genetics, Department of Specialised Medicine, McGill University Health Centre, Department of Human Genetics)

  • Isabelle De Bie

    (McGill University, Division of Medical Genetics, Department of Specialised Medicine, McGill University Health Centre, Department of Human Genetics)

  • Meret Wegler

    (University of Leipzig Medical Center, Institute of Human Genetics)

  • Rami Abou Jamra

    (University of Leipzig Medical Center, Institute of Human Genetics)

  • Susanne B. Kamphausen

    (University Hospital Magdeburg, Institute of Human Genetics, University Hospital Magdeburg)

  • Viktoria Bothe

    (University of Leipzig Medical Center, Institute of Human Genetics)

  • Lorraine Potocki

    (Baylor College of Medicine, Department of Molecular and Human Genetics
    Texas Children’s Hospital)

  • Eric Olinger

    (Cliniques Universitaires Saint-Luc, UCLouvain, Center for Human Genetics)

  • Yves Sznajer

    (Cliniques Universitaires Saint-Luc, UCLouvain, Center for Human Genetics)

  • Elsa Wiame

    (Cliniques Universitaires Saint-Luc, UCLouvain, Center for Human Genetics)

  • Michelle L. Thompson

    (Washington University School of Medicine in Saint Louis, Department of Pathology and Immunology, Division of Laboratory and Genomic Medicine)

  • Molly C. Schroeder

    (Washington University School of Medicine in Saint Louis, Department of Pathology and Immunology, Division of Laboratory and Genomic Medicine
    Washington University School of Medicine, Department of Pediatrics)

  • Catherine Gooch

    (Washington University in St Louis, Department of Pediatrics, Division of Genetics and Genomic Medicine)

  • Raphael A. Smith

    (University of North Carolina Health, Department of Pediatrics, Division of Genetics and Metabolism)

  • Arti Pandya

    (University of North Carolina Health, Department of Pediatrics, Division of Genetics and Metabolism)

  • Larissa M. Busch

    (Abteilung für Funktionelle Genomforschung, Universitätsmedizin Greifswald, Interfakultäres Institut für Genetik und Funktionelle Genomforschung)

  • Uwe Völker

    (Abteilung für Funktionelle Genomforschung, Universitätsmedizin Greifswald, Interfakultäres Institut für Genetik und Funktionelle Genomforschung)

  • Elke Hammer

    (Abteilung für Funktionelle Genomforschung, Universitätsmedizin Greifswald, Interfakultäres Institut für Genetik und Funktionelle Genomforschung)

  • Kristian Wende

    (Leibniz Institute for Plasma Science and Technology (INP))

  • Benjamin Cogné

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Bertrand Isidor

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Jens Meiler

    (Leipzig University, Institute for Drug Discovery, Medical Faculty
    Vanderbilt University, Department of Chemistry, Department of Pharmacology, Center for Structural Biology, Institute of Chemical Biology, Center for Applied Artificial Intelligence in Protein Dynamics)

  • Clémentine Ripoll

    (Hôpital de la Pitié Salpêtrière, ICV-iPS core facility, Sorbonne Université, Institut du Cerveau—Paris Brain Institute—ICM, Inserm, CNRS, APHP)

  • Stéphanie Bigou

    (Hôpital de la Pitié Salpêtrière, ICV-iPS core facility, Sorbonne Université, Institut du Cerveau—Paris Brain Institute—ICM, Inserm, CNRS, APHP)

  • Frédéric Laumonnier

    (Université de Tours, INSERM, Imaging Brain & Neuropsychiatry iBraiN U1253
    Centre Hospitalier Régional Universitaire, Service de Génétique)

  • Peter W. Hildebrand

    (Universität Leipzig, Medizinische Fakultät, Institut für Medizinische Physik und Biophysik
    Institute of Medical Physics and Biophysics, Charité Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
    Berlin Institute of Health)

  • Evan E. Eichler

    (University of Washington School of Medicine, Department of Genome Sciences
    University of Washington, Howard Hughes Medical Institute)

  • Kirsty McWalter

    (GeneDx, LLC)

  • Peter M. Krawitz

    (Rheinische Friedrich-Wilhelms-Universität Bonn, Institute for Genomic Statistics and Bioinformatics, University Hospital Bonn)

  • Florence Roux-Dalvai

    (Centre de recherche du CHU de Québec-Université Laval)

  • Ype Elgersma

    (Erasmus Medical Center, Department of Clinical Genetics
    Erasmus Medical Center, ENCORE Center of Expertise for Neurodevelopmental Disorders)

  • Julien Marcoux

    (Université de Toulouse (UT), Institut de Pharmacologie et de Biologie Structurale (IPBS)
    Infrastructure Nationale de Protéomique, ProFI, UAR)

  • Marie-Pierre Bousquet

    (Université de Toulouse (UT), Institut de Pharmacologie et de Biologie Structurale (IPBS)
    Infrastructure Nationale de Protéomique, ProFI, UAR)

  • Arnaud Droit

    (Centre de recherche du CHU de Québec-Université Laval
    Université Laval, 2325 rue de l’Université, Département de médecine moléculaire, Faculté de médecine)

  • Jeremie Poschmann

    (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology)

  • Andreas M. Grabrucker

    (University of Limerick, Bernal Institute
    University of Limerick, Department of Biological Sciences
    University of Limerick, Health Research Institute (HRI))

  • Francois V. Bolduc

    (University of Alberta, Department of Pediatrics
    University of Alberta, Neuroscience and Mental Health Institute
    University of Alberta, Department of Medical Genetics)

  • Stéphane Bézieau

    (Nantes Université, CHU Nantes, Service de Génétique Médicale
    Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Frédéric Ebstein

    (Nantes Université, CHU Nantes, CNRS, INSERM, l’institut du thorax)

  • Elke Krüger

    (Institut für Medizinische Biochemie und Molekularbiologie, Universitätsmedizin Greifswald)

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.

Suggested Citation

  • Sébastien Küry & Janelle E. Stanton & Geeske M. van Woerden & Amélie Bosc-Rosati & Tzung-Chien Hsieh & Lise Bray & Marielle Oloudé & Cory Rosenfelt & Marie Pier Scott-Boyer & Victoria Most & Tianyun W, 2025. "Investigating the neuronal role of the proteasomal ATPase subunit gene PSMC5 in neurodevelopmental proteasomopathies," Nature Communications, Nature, vol. 16(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-65556-8
    DOI: 10.1038/s41467-025-65556-8
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