ArticleAnnals of neurology2025
Mutations in the Key Autophagy Tethering Factor EPG5 Link Neurodevelopmental and Neurodegenerative Disorders Including Early-Onset Parkinsonism.
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4 citing papers in PubMed.
- Reply to: Data from the ROPAD study corroborate an association between ITSN1 loss-of-function variants and Parkinson's disease.NPJ Parkinson's disease · 2026Article
- Pathogenic variants in the autophagy-tethering factor EPG5 drive neurodegeneration through mitochondrial dysfunction and innate immune activation.Nature communications · 2026Article
- Pancreatic involvement inMolecular genetics and metabolism reports · 2025Article
- Pleiotropy and the Increasing Complexity of Parkinson's Disease Genetics.Annals of neurology · 2025Article
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141 authors.
Hormos Salimi DafsariDepartment of Pediatrics and Center for Rare Diseases, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.ORCID 0000-0003-3483-5009
Celine DeneubourgDepartment of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Kritarth SinghUCL Consortium for Mitochondrial Research and Department of Cell and Developmental Biology, University College London, London, UK.ORCID 0000-0003-4072-6888
Reza MaroofianDepartment of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0001-6763-1542
Zita SuprenantVici Syndrome Foundation, Inc, Silver Spring, Maryland, USA.
Ay Lin KhoRandall Center for Cell and Molecular Biophysics, Muscle Signaling Section, Faculty of Life Sciences and Medicine (FoLSM), King's College London, London, UK.
Neil J InghamWolfson Sensory Pain and Regeneration Centre, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Karen P SteelWolfson Sensory Pain and Regeneration Centre, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Preethi SheshadriUCL Consortium for Mitochondrial Research and Department of Cell and Developmental Biology, University College London, London, UK.
Franciska BaurDepartment of Pediatrics and Center for Rare Diseases, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Lea HentrichDepartment of Pediatrics and Center for Rare Diseases, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Birgit GerischMax Planck Institute for Biology of Aging and Cologne Excellence Cluster for Aging-associated Diseases, Cologne, Germany.
Mina ZamaniDepartment of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK.
Cesar AlvesDepartment of Radiology, Boston Children's Hospital, Boston, MA, USA.
Ata SiddiquiDepartment of Radiology, Guy's and Saint Thomas' Hospitals NHS Trust, London, UK.
Haidar S DafsariDepartment of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Mehri SalariFaculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
Anthony E LangEdmond J Safra Program in Parkinson's Disease, Krembil Brain Institute, University Health Network and the Department of Medicine, University of Toronto, Toronto, ON, Canada.
Michael HarrisVici Syndrome Foundation, Inc, Silver Spring, Maryland, USA.
Alice AbdelaleemDepartment of Neurology, Weill Cornell Medicine Qatar, Education City, Doha, Qatar.
Saeid SadeghianDepartment of Neurology, University of Minnesota, Minneapolis, Minnesota, USA.
Reza AzizimalamiriDepartment of Neurology, University of Minnesota, Minneapolis, Minnesota, USA.
Hamid GalehdariNarges Medical Genetics and Prenatal Diagnosis Laboratory, Ahvaz, Iran.
Gholamreza ShariatiNarges Medical Genetics and Prenatal Diagnosis Laboratory, Ahvaz, Iran.
Alireza SedaghatNarges Medical Genetics and Prenatal Diagnosis Laboratory, Ahvaz, Iran.
Jawaher ZeighamiFaculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
Daniel CalameDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, USA.ORCID 0000-0001-6860-372X
Dana MarafiDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, USA.ORCID 0000-0003-2233-3423
Ruizhi DuanDepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.
Adrian BoehnkeDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, USA.
Gary D ClarkDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, USA.
Jill A RosenfeldDepartment of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA.ORCID 0000-0001-5664-7987
Carrie A MohilaDepartment of Pathology, Department of Pathology and Immunology, Texas Children's Hospital, Baylor College of Medicine, Houston, TX, USA.
Dora SteelDevelopmental Neurosciences, Zayed Centre for Research into Rare Disease in Children, UCL GOS-Institute of Child Health, London, UK.
Saurabh ChopraIndraprastha Apollo Hospital, New Delhi, India.
Suvasini SharmaDepartment of Pediatrics, Lady Hardinge Medical College and Associated Kalawati Saran Children's Hospital, New Delhi, India.
Nicolai KohlschmidtInstitute for Clinical Genetics and Tumour Genetics, Bonn, Germany.
Steffi PatzerDepartment of Pediatrics, Krankenhaus St. Elisabeth und St. Barbara, Halle (Saale), Germany.
Afshin SaffariDivision of Child Neurology and Metabolic Medicine, Department of Pediatrics I, Center for Pediatrics and Adolescent Medicine, Medical Faculty Heidelberg, University Hospital Heidelberg, Heidelberg University, Heidelberg, Germany.
Darius Ebrahimi-FakhariMovement Disorders Program, Department of Neurology, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA.ORCID 0000-0002-0026-4714
Büşra Eser ÇavdartepeDepartment of Medical Genetics, Konya City Hospital, Konya, Turkey.
Irene J ChangDepartment of Pediatrics, Division of Medical Genetics, University of California at San Francisco, San Francisco, CA, USA.
Erika BeckmanDivision of Genetic Medicine, Department of Pediatrics, University of Washington, Seattle, WA, USA.
Renate PetersChristliches Kinderhospital Osnabrück, Osnabrück, Germany.
Andrew Paul FennellMonash Genetics, Monash Health, Melbourne, Vic, Australia.
Bernice LoResearch Branch, Sidra Medicine, Doha; College of Health and Life Sciences, Hamad Bin Khalifa University, Doha, Qatar.
Luisa AverdunkDepartment of General Pediatrics, Neonatology and Pediatric Cardiology, Medical Faculty, Heinrich-Heine-University, Düsseldorf, Germany.
Felix DistelmaierDepartment of General Pediatrics, Neonatology and Pediatric Cardiology, Medical Faculty, Heinrich-Heine-University, Düsseldorf, Germany.
Martina BaethmannDepartment of Pediatrics, Hospital Dritter Orden, Munich, Germany.
Frances ElmslieSt George's University Hospitals NHS Foundation Trust, London, UK.
Kairit JoostFaculty of Medicine, University of Tartu, Tartu, Estonia.
Sheela NampoothiriDepartment of Pediatric Genetics, Amrita Institute of Medical Sciences & Research Center, Cochin, India.
Dhanya YesodharanDepartment of Metabolic and Genetic Disorders, Ziv, Medical Center, Safed, Israel.
Hanna MandelDepartment of Metabolic and Genetic Disorders, Ziv, Medical Center, Safed, Israel.
Amy KimballHarvey Institute for Human Genetics, Greater Baltimore Medical Center, Baltimore, MD, USA.
Antonie D KlineHarvey Institute for Human Genetics, Greater Baltimore Medical Center, Baltimore, MD, USA.
Cyril MignotAPHP, Hôpital Pitié-Salpêtrière, Département de Génétique, Centre de Reference Déficience Intellectuelle de Causes Rares, GRC UPMC Déficience Intellectuelle et Autisme, Paris, France.
Boris KerenAPHP, Hôpital Pitié-Salpêtrière, Département de Génétique, Centre de Reference Déficience Intellectuelle de Causes Rares, GRC UPMC Déficience Intellectuelle et Autisme, Paris, France.
Vincent LaugelService de Pédiatrie, Centre Hospitalier Universitaire (CHU) de Strasbourg-Hautepierre, Strasbourg, France.
Katrin ÕunapDepartment of Clinical Genetics, Genetics and Personalized Medicine Clinic, Tartu University Hospital and Institute of Clinical Medicine, University of Tartu, Tartu, Estonia.
Kalpana DevadathanDepartment of Pediatric Neurology, Government Medical College, Thiruvananthapuram, India.
Frederique M C van BerkestijnDepartment of Pediatric Neurology, University Medical Center Utrecht, Utrecht, the Netherlands.
Arpana SilwalSt Bart's Health NHS Trust, London, UK.ORCID 0000-0002-0950-3101
Saskia KoeneDepartment of Clinical Genetics, Leiden University Medical Center, Leiden, the Netherlands.
Sumit VermaChildren's Healthcare of Atlanta, Emory University, Atlanta, GA, USA.ORCID 0000-0003-1992-4556
Mohammed Yousuf KarimDepartment of Pathology, Sidra Medicine, College of Medicine, Qatar University, Doha, Qatar.
Chahynez BoubidiDepartment of Pediatrics A, Hussein Dey University Hospital Center, University of Algiers 1, Algiers, Algeria.
Majid AzizDepartment of Pediatric Neurology, Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates.
Gehad ElGhazaliDepartment of Medical Microbiology and Immunology, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.
Lauren MattasStanford Children's Hospital, Palo Alto, CA, USA.
Mohammad MiryounesiDepartment of Medical Genetics, Faculty of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
Farzad Hashemi-GorjiGenomic Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.ORCID 0000-0002-9996-9406
Shahryar AlaviPalindrome, Isfahan, Iran.ORCID 0000-0002-3484-3423
Nayereh NouriKaryogen Lab, Isfahan, Iran.
Mehrdad NoruziniaDepartment of Laboratory Medicine and Pathology, University of Washington, Seattle, WA, USA.
Saeideh KavousiDepartment of Medical Genetics, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran.
Arveen KamathCardiff and Vale UHB-AWMGS, Cardiff, UK.
Sandeep JayawantOxford University Hospitals NHS Foundation Trust, Oxford, UK.
Russell SanetoNeuroscience Institute, Center for Integrated Brain Research, Department of Neurology/Division of Pediatric Neurology, Seattle Children's Hospital, Seattle, WA, USA.
Nourelhoda A HaridyDepartment of Neurology, Faculty of Medicine, Assiut University, Assiut, Egypt.
Pinar Ozkan KartDepartment of Pediatrics Neurology, Karadeniz Technical University, Trabzon, Turkey.
Ali CansuGenetics Department, Nantes University Hospital, Nantes, France.
Madeleine JoubertGenetics Department, Nantes University Hospital, Nantes, France.
Claire BeneteauGenetics Department, Nantes University Hospital, Nantes, France.
Kyra E StuurmanDepartment of Clinical Genetics, Erasmus MC University Medical Center, Rotterdam, the Netherlands.
Martina WilkeDepartment of Clinical Genetics, Erasmus MC University Medical Center, Rotterdam, the Netherlands.
Tahsin Stefan BarakatDepartment of Clinical Genetics, Erasmus MC University Medical Center, Rotterdam, the Netherlands.ORCID 0000-0003-1231-1562
Homa TajsharghiSchool of Health Science, Division Biomedicine and Translational Medicine, University of Skovde, Skovde, Sweden.ORCID 0000-0001-8854-5213
Annarita ScardamagliaDepartment of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK.
Sadeq VallianDepartment of Cell and Molecular Biology & Microbiology, Faculty of Science and Technology, University of Isfahan, Isfahan, Iran.
Semra HızFaculty of Medicine, Pediatric Neurology Department, Dokuz Eylül University, Izmir, Turkey.
Ali ShoeibiDepartment of Neurology, Mashhad University of Medical Sciences, Mashhad, Iran.
Reza BoostaniDepartment of Neurology, Mashhad University of Medical Sciences, Mashhad, Iran.
Narges HashemiDepartment of Pediatrics, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
Meisam BabaeiDepartment of Pediatrics, North Khorasan University of Medical Sciences, Bojnurd, Iran.
Norah Saleh AlsalehDepartment of Genetics and Precision Medicine, King Abdullah Specialized Children's Hospital, King Abdullah International Medical Research Center, Ministry of National Guard Health Affairs, Riyadh, Saudi Arabia.
Julie PorterDivision of Medical Genetics, Department of Pediatrics, University of Utah, Salt Lake City, UT, USA.
Tania Attié-BitachService de Médecine Génomique des Maladies Rares, Hôpital Necker-Enfants Malades, Paris, France.
Pauline MarzinService de Médecine Génomique des Maladies Rares, Hôpital Necker-Enfants Malades, Paris, France.
Dorota WicherDepartment of Medical Genetics, Children's Memorial Health Institute, Warsaw, Poland.
Jessica I GoldDivision of Medical Genetics, Department of Pediatrics, Cohen Children's Medical Center, New Hyde Park, NY, USA.
Elisabeth SchulerDivision of Child Neurology and Metabolic Medicine, Department of Pediatrics I, Center for Pediatrics and Adolescent Medicine, Medical Faculty Heidelberg, University Hospital Heidelberg, Heidelberg University, Heidelberg, Germany.
Amna KashgariDepartment of Clinical Genetics and Precision Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia.
Rakan F AlanaziDepartment of Clinical Genetics and Precision Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia.
Wafaa EyaidDepartment of Clinical Genetics and Precision Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia.
Marc EngelenAmsterdam Leukodystrophy Center, Department of Pediatric Neurology, Emma Children's Hospital, and Amsterdam Neuroscience, Cellular & Molecular Mechanisms, Amsterdam University Medical Center, University of Amsterdam, Amsterdam, the Netherlands.
Mirjam LangeveldDepartment of Endocrinology and Metabolism, Amsterdam UMC, Research Institute Gastroenterology, Endocrinology & Metabolism (AGEM), University of Amsterdam, Amsterdam, the Netherlands.
Burkhard StüveDepartment for Neuropediatrics, DRK Children's Hospital Siegen, Siegen, Germany.
Yun LiInstitute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany.
Gökhan YigitInstitute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany.
Bernd WollnikInstitute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany.
Mariana H G MonjeDepartment of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.ORCID 0000-0002-0730-4061
Dimitri KraincDepartment of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Niccolò E MencacciDepartment of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Somayeh BakhtiariPediatric Movement Disorders Program, Division of Pediatric Neurology, Barrow Neurological Institute, Phoenix Children's Hospital, Phoenix, AZ, USA.
Michael KruerPediatric Movement Disorders Program, Division of Pediatric Neurology, Barrow Neurological Institute, Phoenix Children's Hospital, Phoenix, AZ, USA.
Emanuela ArgilliDepartment of Neurology, University of California San Francisco Division of Hospital Medicine, San Francisco, CA, USA.
Elliott SherrDepartment of Neurology, University of California San Francisco Division of Hospital Medicine, San Francisco, CA, USA.
Yalda JamshidiMolecular and Clinical Sciences Institute, St. George's University of London, London, UK.
Ehsan Ghayoor KarimianiMolecular and Clinical Sciences Institute, St. George's University of London, London, UK.
Yiu Wing Sunny CheungLife Sciences Institute, Department of Biochemistry and Molecular Biology, The University of British Columbia, Vancouver, BC, Canada.
Ivan KarinFriedrich-Baur-Institute, Department of Neurology, LMU University Hospital, Ludwig-Maximilians-Universität München, Munich, Germany.
Giovanni ZifarelliCENTOGENE GmbH, Rostock, Germany.
Peter BauerCENTOGENE GmbH, Rostock, Germany.
Wendy K ChungDepartment of Pediatrics, Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.
James R LupskiDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, USA.
Manju A KurianDevelopmental Neurosciences, Zayed Centre for Research into Rare Disease in Children, UCL GOS-Institute of Child Health, London, UK.
Jörg DötschDepartment of Pediatrics and Center for Rare Diseases, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Jürgen-Christoph von Kleist-RetzowDepartment of Pediatrics and Center for Rare Diseases, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Thomas KlopstockFriedrich-Baur-Institute, Department of Neurology, LMU University Hospital, Ludwig-Maximilians-Universität München, Munich, Germany.
Matias WagnerInstitute of Human Genetics, School of Medicine and Health, Technische Universität München, Munich, Germany.ORCID 0000-0002-4454-8823
Calvin YipLife Sciences Institute, Department of Biochemistry and Molecular Biology, The University of British Columbia, Vancouver, BC, Canada.
Andreas RoosDepartment of Pediatric Neurology, Centre for Neuromuscular Disorders, Centre for Translational Neuro- and Behavioral Sciences, University Duisburg-Essen, Essen, Germany.
Rita CarsettiImmunology Research Area, B Cell Unit, Ospedale Pediatrico Bambino Gesù IRCCS, Rome, Italy.
Carlo Dionisi-ViciDivision of Metabolic Diseases and Hepatology, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
Mathias GautelRandall Center for Cell and Molecular Biophysics, Muscle Signaling Section, Faculty of Life Sciences and Medicine (FoLSM), King's College London, London, UK.
Michael R DuchenUCL Consortium for Mitochondrial Research and Department of Cell and Developmental Biology, University College London, London, UK.ORCID 0000-0003-2548-4294
Adam AntebiMax Planck Institute for Biology of Aging and Cologne Excellence Cluster for Aging-associated Diseases, Cologne, Germany.ORCID 0000-0002-7241-3029
Henry HouldenDepartment of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, UK.ORCID 0000-0002-2866-7777
Manolis FantoDepartment of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.ORCID 0000-0001-7807-2563
Heinz JungbluthDepartment of Pediatric Neurology, Evelina London Children's Hospital, Guy's & St Thomas NHS Foundation Trust, London, UK.ORCID 0000-0002-7159-3427
Funding
Frequency of variants of unknown significance by ancestry groups in the All of Us Research Program cohortU01HG011758 · NHGRI · BAYLOR COLLEGE OF MEDICINE · PI RICHARD A GIBBS, JAMES R. LUPSKI · 2021 to 2026
$13.8MSTRUCTURAL VARIATION IN NEUROLOGICAL DISEASER35NS105078 · NINDS · BAYLOR COLLEGE OF MEDICINE · PI LUPSKI, JAMES R. · 2018 to 2025
$6.0MGenomic analysis of the Multiplex, Autozygous Populations in Cerebral Palsy (MAP CP) cohort: a focused approach to a complex diseaseR01NS127108 · NINDS · UNIVERSITY OF ARIZONA · PI Michael C Kruer · 2023 to 2026
$2.6MUnderstanding the role of BORCS5 in neuronal lysosomal function and neurodegenerationK08NS131581 · NINDS · NORTHWESTERN UNIVERSITY AT CHICAGO · PI Niccolo E Mencacci · 2024 to 2026
$673kAction Medical Research GN2959Deutsche Forschungsgemeinschaft 413543196Estonian Research Competency Council PRG2040H2020 Marie Skłodowska-Curie Actions 765912 - DRIVE - H2020-MSCA-ITN-2017HORIZON EUROPE Framework Programme ERN-01-2016/739516Medizinische Fakultät, Universität zu Köln 243/2022Medizinische Fakultät, Universität zu Köln 371/2021NHGRI NIH HHS U01 HG011758NINDS NIH HHS K08 NS131581NINDS NIH HHS R01 NS127108NINDS NIH HHS R35 NS105078ZonMw 09150172110002
Abstract
objectiveAutophagy is a fundamental biological pathway with vital roles in intracellular homeostasis. During autophagy, defective cargoes including mitochondria are targeted to lysosomes for clearance and recycling. Recessive truncating variants in the autophagy gene EPG5 have been associated with Vici syndrome, a severe early-onset neurodevelopmental disorder with extensive multisystem involvement. Here, we aimed to delineate the extended, age-dependent EPG5-related disease spectrum.
methodsWe investigated clinical, radiological, and molecular features from the largest cohort of EPG5-related patients identified to date, complemented by experimental investigation of cellular and animal models of EPG5 defects.
resultsThrough worldwide collaboration, we identified 211 patients, 97 of them previously unpublished, with recessive EPG5 variants. The phenotypic spectrum ranged from antenatally lethal presentations to milder isolated neurodevelopmental disorders. A novel Epg5 knock-in mouse model of a recurrent EPG5 missense variant featured motor impairments and defective autophagy in brain areas particularly relevant for the neurological disorders in milder presentations. Novel age-dependent neurodegenerative manifestations in our cohort included adolescent-onset parkinsonism and dystonia with cognitive decline, and myoclonus. Radiological features suggested an emerging continuum with brain iron accumulation disorders. Patient fibroblasts showed defects in PINK1-Parkin-dependent mitophagic clearance and α-synuclein overexpression, indicating a cellular basis for the observed neurodegenerative phenotypes. In Caenorhabditis elegans, EPG5 knockdown caused motor impairments, defective mitophagic clearance, and changes in mitochondrial respiration comparable to observations in C. elegans knockdown of parkinsonism-related genes.
interpretationOur findings illustrate a lifetime neurological disease continuum associated with pathogenic EPG5 variants, linking neurodevelopmental and neurodegenerative disorders through the common denominator of defective autophagy. ANN NEUROL 2025;98:932-950.
Indexed as
AutophagyAutophagy-Related ProteinsMutationNeurodegenerative DiseasesNeurodevelopmental DisordersParkinsonian DisordersAdolescentAdultAge of OnsetAnimalsCaenorhabditis elegansChildChild, PreschoolCohort StudiesDisease Models, AnimalFemaleAutophagy-Related ProteinsEPG5 protein, humanVesicular Transport Proteins
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