Clinico-Genetic, Imaging and Molecular Delineation of COQ8A-Ataxia: A Multicenter Study of 59 Patients.


Journal

Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449

Informations de publication

Date de publication:
08 2020
Historique:
received: 11 11 2019
revised: 16 04 2020
accepted: 17 04 2020
pubmed: 28 4 2020
medline: 15 12 2020
entrez: 28 4 2020
Statut: ppublish

Résumé

To foster trial-readiness of coenzyme Q8A (COQ8A)-ataxia, we map the clinicogenetic, molecular, and neuroimaging spectrum of COQ8A-ataxia in a large worldwide cohort, and provide first progression data, including treatment response to coenzyme Q10 (CoQ10). Cross-modal analysis of a multicenter cohort of 59 COQ8A patients, including genotype-phenotype correlations, 3D-protein modeling, in vitro mutation analyses, magnetic resonance imaging (MRI) markers, disease progression, and CoQ10 response data. Fifty-nine patients (39 novel) with 44 pathogenic COQ8A variants (18 novel) were identified. Missense variants demonstrated a pleiotropic range of detrimental effects upon protein modeling and in vitro analysis of purified variants. COQ8A-ataxia presented as variable multisystemic, early-onset cerebellar ataxia, with complicating features ranging from epilepsy (32%) and cognitive impairment (49%) to exercise intolerance (25%) and hyperkinetic movement disorders (41%), including dystonia and myoclonus as presenting symptoms. Multisystemic involvement was more prevalent in missense than biallelic loss-of-function variants (82-93% vs 53%; p = 0.029). Cerebellar atrophy was universal on MRI (100%), with cerebral atrophy or dentate and pontine T2 hyperintensities observed in 28%. Cross-sectional (n = 34) and longitudinal (n = 7) assessments consistently indicated mild-to-moderate progression of ataxia (SARA: 0.45/year). CoQ10 treatment led to improvement by clinical report in 14 of 30 patients, and by quantitative longitudinal assessments in 8 of 11 patients (SARA: -0.81/year). Explorative sample size calculations indicate that ≥48 patients per arm may suffice to demonstrate efficacy for interventions that reduce progression by 50%. This study provides a deeper understanding of the disease, and paves the way toward large-scale natural history studies and treatment trials in COQ8A-ataxia. ANN NEUROL 2020;88:251-263.

Identifiants

pubmed: 32337771
doi: 10.1002/ana.25751
pmc: PMC7877690
mid: NIHMS1646232
doi:

Substances chimiques

Ubiquinone 1339-63-5
ubiquinone 8 CQA993F7P8

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

251-263

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM131795
Pays : United States
Organisme : Wellcome Trust
ID : 201064/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N010035/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1000848
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N025431/2
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N025431/1
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : T32 GM008505
Pays : United States

Informations de copyright

© 2020 The Authors. Annals of Neurology published by Wiley Periodicals, Inc. on behalf of American Neurological Association.

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Auteurs

Andreas Traschütz (A)

Department of Neurodegenerative Diseases, Hertie-Institute for Clinical Brain Research and Center of Neurology, University of Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, Tübingen, Germany.

Tommaso Schirinzi (T)

Neurorehabilitation Unit, Department of Neurosciences, IRCCS Bambino Gesù Children Hospital, Rome, Italy.
Department of Systems Medicine, University of Roma Tor Vergata, Rome, Italy.

Lucia Laugwitz (L)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.
Department of Pediatric Neurology, University Children's Hospital, Tübingen, Germany.

Nathan H Murray (NH)

Morgridge Institute for Research, Madison, WI, USA.
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, USA.

Craig A Bingman (CA)

Morgridge Institute for Research, Madison, WI, USA.
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, USA.

Selina Reich (S)

Department of Neurodegenerative Diseases, Hertie-Institute for Clinical Brain Research and Center of Neurology, University of Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, Tübingen, Germany.

Jan Kern (J)

Department of Pediatric Neurology, University Children's Hospital, Tübingen, Germany.

Anna Heinzmann (A)

Brain and Spine Institute (ICM), Sorbonne Université, Pitié-Salpêtrière University Hospital, Paris, France.
AP-HP, Department of Genetics, Pitié-Salpêtrière University Hospital, Paris, France.

Gessica Vasco (G)

Neurorehabilitation Unit, Department of Neurosciences, IRCCS Bambino Gesù Children Hospital, Rome, Italy.

Enrico Bertini (E)

Unit of Neuromuscular and Neurodegenerative Diseases, Department of Neurosciences, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.

Ginevra Zanni (G)

Unit of Neuromuscular and Neurodegenerative Diseases, Department of Neurosciences, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.

Alexandra Durr (A)

Brain and Spine Institute (ICM), Sorbonne Université, Pitié-Salpêtrière University Hospital, Paris, France.
AP-HP, Department of Genetics, Pitié-Salpêtrière University Hospital, Paris, France.

Stefania Magri (S)

Unit of Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Franco Taroni (F)

Unit of Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Alessandro Malandrini (A)

Department of Medicine, Surgery, and Neurosciences, University of Siena, Unit of Neurology and Neurometabolic Disorders, Azienda Ospedaliera Universitaria Senese, Siena, Italy.

Jonathan Baets (J)

Neurogenetics Group, University of Antwerp, Antwerp, Belgium.
Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.
Department of Neurology, Antwerp University Hospital, Antwerp, Belgium.

Peter de Jonghe (P)

Neurogenetics Group, University of Antwerp, Antwerp, Belgium.
Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.
Department of Neurology, Antwerp University Hospital, Antwerp, Belgium.

Willem de Ridder (W)

Neurogenetics Group, University of Antwerp, Antwerp, Belgium.
Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.
Department of Neurology, Antwerp University Hospital, Antwerp, Belgium.

Matthieu Bereau (M)

Service de Neurologie, Université de Franche-Comté, CHRU de Besançon, Besançon, France.
Unité Extrapyramidale, Département des Neurosciences Cliniques, HUG, Faculté de Médecine, Université de Genève, Geneva, Switzerland.

Stephanie Demuth (S)

Praxis für Humangenetik Erfurt, Erfurt, Germany.

Christos Ganos (C)

Department of Neurology, Charité University Medicine Berlin, Berlin, Germany.

A Nazli Basak (AN)

Suna and Inan Kıraç Foundation, Neurodegeneration Research Laboratory, KUTTAM, Koç University School of Medicine, Istanbul, Turkey.

Hasmet Hanagasi (H)

Behavioural Neurology and Movement Disorders Unit, Department of Neurology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey.

Semra Hiz Kurul (SH)

Departments of Pediatric Neurology, Dokuz Eylül University Faculty of Medicine, İzmir, Turkey.

Benjamin Bender (B)

Department of Diagnostic and Interventional Neuroradiology, University of Tübingen, Tübingen, Germany.

Ludger Schöls (L)

Department of Neurodegenerative Diseases, Hertie-Institute for Clinical Brain Research and Center of Neurology, University of Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, Tübingen, Germany.

Ute Grasshoff (U)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.

Thomas Klopstock (T)

Department of Neurology, Friedrich-Baur-Institute, Ludwig-Maximilians University of Munich, Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Rita Horvath (R)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.
Institute of Genetic Medicine, Newcastle University, Newcastle, UK.

Bart van de Warrenburg (B)

Department of Neurology, Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands.

Lydie Burglen (L)

Centre de Référence Maladies Rares "Malformations et Maladies Congénitales du Cervelet", Paris-Lyon-Lille, France.
Département de Génétique et Embryologie Médicale, APHP, GHUEP, Hôpital Armand Trousseau, Paris, France.
Developmental Brain Disorders Laboratory, Imagine Institute, INSERM UMR 1163, Paris, France.

Christelle Rougeot (C)

Centre de Référence Maladies Rares "Malformations et Maladies Congénitales du Cervelet", Paris-Lyon-Lille, France.
Hôpital Femme Mère Enfant, Service de Neuropédiatrie, Bron, France.

Claire Ewenczyk (C)

Brain and Spine Institute (ICM), Sorbonne Université, Pitié-Salpêtrière University Hospital, Paris, France.
AP-HP, Department of Genetics, Pitié-Salpêtrière University Hospital, Paris, France.
Hôpitaux universitaires Pitié Salpêtrière - Charles Foix, Service de Génétique, Paris, France.

Michel Koenig (M)

EA7402 Institut Universitaire de Recherche Clinique, and Laboratoire de Génétique Moléculaire, CHU and Université de Montpellier, Montpellier, France.

Filippo M Santorelli (FM)

IRCCS Fondazione Stella Maris, Pisa, Italy.

Mathieu Anheim (M)

Service de Neurologie, Hôpitaux Universitaires de Strasbourg, Hôpital de Hautepierre, Strasbourg, France.
Fédération de Médecine Translationnelle de Strasbourg (FMTS), Université de Strasbourg, Strasbourg, France.
Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM-U964/CNRS-UMR7104/Université de Strasbourg, Illkirch, France.

Renato P Munhoz (RP)

Movement Disorders Centre, Toronto Western Hospital, University of Toronto, Krembil Research Institute, Toronto, Ontario, Canada.

Tobias Haack (T)

Institute of Medical Genetics and Applied Genomics, University of Tübingen, Tübingen, Germany.

Felix Distelmaier (F)

Department of General Pediatrics, Neonatology, and Pediatric Cardiology, University Children's Hospital Duesseldorf, Medical Faculty, Heinrich Heine University, Duesseldorf, Germany.

David J Pagliarini (DJ)

Morgridge Institute for Research, Madison, WI, USA.
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, USA.

Hélène Puccio (H)

Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, France.
INSERM, U1258, Illkirch, France.
CNRS, UMR7104, IIllkirch, France.
Université de Strasbourg, Strasbourg, France.

Matthis Synofzik (M)

Department of Neurodegenerative Diseases, Hertie-Institute for Clinical Brain Research and Center of Neurology, University of Tübingen, Tübingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), University of Tübingen, Tübingen, Germany.

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