Authors

Hormos Salimi Dafsari
Celine Deneubourg
Kritarth Singh
Reza Maroofian
Zita Suprenant
Ay Lin Kho
Neil J Ingham
Karen P Steel
Preethi Sheshadri
Franciska Baur
Lea Hentrich
Birgit Gerisch
Mina Zamani
Cesar Alves
Ata Siddiqui
Haidar S Dafsari
Mehri Salari
Anthony E Lang
Michael Harris
Alice Abdelaleem
Saeid Sadeghian
Reza Azizimalamiri
Hamid Galehdari
Gholamreza Shariati
Alireza Sedaghat
Jawaher Zeighami
Daniel Calame
Dana Marafi
Ruizhi Duan
Adrian Boehnke
Gary D Clark
Jill A Rosenfeld
Carrie A Mohila
Dora Steel
Saurabh Chopra
Suvasini Sharma
Nicolai Kohlschmidt
Steffi Patzer
Afshin Saffari
Darius Ebrahimi-Fakhari
Büşra Eser Çavdartepe
Irene J Chang
Erika Beckman
Renate Peters
Andrew Paul Fennell
Bernice Lo
Luisa Averdunk
Felix Distelmaier
Martina Baethmann
Frances Elmslie
Kairit Joost
Sheela Nampoothiri
Dhanya Yesodharan
Hanna Mandel
Amy Kimball
Antonie D Kline
Cyril Mignot
Boris Keren
Vincent Laugel
Katrin Õunap
Kalpana Devadathan
Frederique M C van Berkestijn
Arpana Silwal
Saskia Koene
Sumit Verma
Mohammed Yousuf Karim
Chahynez Boubidi
Majid Aziz
Gehad ElGhazali
Lauren Mattas
Mohammad Miryounesi
Farzad Hashemi-Gorji
Shahryar Alavi
Nayereh Nouri
Mehrdad Noruzinia
Saeideh Kavousi
Arveen Kamath
Sandeep Jayawant
Russell Saneto
Nourelhoda A Haridy
Pinar Ozkan Kart
Ali Cansu
Madeleine Joubert
Claire Beneteau
Kyra E Stuurman
Martina Wilke
Tahsin Stefan Barakat
Homa Tajsharghi
Annarita Scardamaglia
Sadeq Vallian
Semra Hız
Ali Shoeibi
Reza Boostani
Narges Hashemi
Meisam Babaei
Norah Saleh Alsaleh
Julie Porter
Tania Attié-Bitach
Pauline Marzin
Dorota Wicher
Jessica I Gold
Elisabeth Schuler
Amna Kashgari
Rakan F Alanazi
Wafaa Eyaid
Marc Engelen
Mirjam Langeveld
Burkhard Stüve
Yun Li
Gökhan Yigit
Bernd Wollnik
Mariana H G Monje
Dimitri Krainc
Niccolò E Mencacci
Somayeh Bakhtiari
Michael Kruer
Emanuela Argilli
Elliott Sherr
Yalda Jamshidi
Ehsan Ghayoor Karimiani
Yiu Wing Sunny Cheung
Ivan Karin
Giovanni Zifarelli
Peter Bauer
Wendy K Chung
James R Lupski
Manju A Kurian
Jörg Dötsch
Jürgen-Christoph von Kleist-Retzow
Thomas Klopstock
Matias Wagner
Calvin Yip
Andreas Roos
Rita Carsetti
Carlo Dionisi-Vici
Mathias Gautel
Michael R Duchen
Adam Antebi
Henry Houlden
Manolis Fanto
Heinz Jungbluth

Language

English

Publication Date

11-1-2025

Journal

Annals of Neurology

DOI

10.1002/ana.78013

PMID

41053928

PMCID

PMC12577676

PubMedCentral® Posted Date

10-6-2025

PubMedCentral® Full Text Version

Post-print

Abstract

Objective: Autophagy 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.

Methods: We 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.

Results: Through 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.

Interpretation: Our findings illustrate a lifetime neurological disease continuum associated with pathogenic EPG5 variants, linking neurodevelopmental and neurodegenerative disorders through the common denominator of defective autophagy.

Keywords

Humans, Animals, Female, Mice, Male, Autophagy, Mutation, Parkinsonian Disorders, Adolescent, Neurodevelopmental Disorders, Child, Adult, Neurodegenerative Diseases, Caenorhabditis elegans, Autophagy-Related Proteins, Cohort Studies, Age of Onset, Young Adult, Vesicular Transport Proteins, Child, Preschool, Disease Models, Animal

Published Open-Access

yes

Share

COinS
 
 

To view the content in your browser, please download Adobe Reader or, alternately,
you may Download the file to your hard drive.

NOTE: The latest versions of Adobe Reader do not support viewing PDF files within Firefox on Mac OS and if you are using a modern (Intel) Mac, there is no official plugin for viewing PDF files within the browser window.