Bi-allelic LETM1 variants perturb mitochondrial ion homeostasis leading to a clinical spectrum with predominant nervous system involvement.


Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
01 09 2022
Historique:
received: 27 03 2022
accepted: 01 07 2022
entrez: 2 9 2022
pubmed: 3 9 2022
medline: 9 9 2022
Statut: ppublish

Résumé

Leucine zipper-EF-hand containing transmembrane protein 1 (LETM1) encodes an inner mitochondrial membrane protein with an osmoregulatory function controlling mitochondrial volume and ion homeostasis. The putative association of LETM1 with a human disease was initially suggested in Wolf-Hirschhorn syndrome, a disorder that results from de novo monoallelic deletion of chromosome 4p16.3, a region encompassing LETM1. Utilizing exome sequencing and international gene-matching efforts, we have identified 18 affected individuals from 11 unrelated families harboring ultra-rare bi-allelic missense and loss-of-function LETM1 variants and clinical presentations highly suggestive of mitochondrial disease. These manifested as a spectrum of predominantly infantile-onset (14/18, 78%) and variably progressive neurological, metabolic, and dysmorphic symptoms, plus multiple organ dysfunction associated with neurodegeneration. The common features included respiratory chain complex deficiencies (100%), global developmental delay (94%), optic atrophy (83%), sensorineural hearing loss (78%), and cerebellar ataxia (78%) followed by epilepsy (67%), spasticity (53%), and myopathy (50%). Other features included bilateral cataracts (42%), cardiomyopathy (36%), and diabetes (27%). To better understand the pathogenic mechanism of the identified LETM1 variants, we performed biochemical and morphological studies on mitochondrial K

Identifiants

pubmed: 36055214
pii: S0002-9297(22)00311-1
doi: 10.1016/j.ajhg.2022.07.007
pmc: PMC9502063
pii:
doi:

Substances chimiques

Calcium-Binding Proteins 0
LETM1 protein, human 0
Membrane Proteins 0
Mitochondrial Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1692-1712

Subventions

Organisme : Medical Research Council
ID : MC_PC_13029/2
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S005021/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S01165X/1
Pays : United Kingdom
Organisme : Austrian Science Fund FWF
ID : P 31471
Pays : Austria
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Rauan Kaiyrzhanov (R)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Sami E M Mohammed (SEM)

Department of Biomedical Sciences, Institute of Physiology, Pathophysiology and Biophysics, University of Veterinary Medicine Vienna, Vienna 1210, Austria.

Reza Maroofian (R)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Ralf A Husain (RA)

Department of Neuropediatrics, Jena University Hospital, Jena 07747, Germany; Center for Rare Diseases, Jena University Hospital, Jena 07747, Germany.

Alessia Catania (A)

Unit of Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20126, Italy.

Alessandra Torraco (A)

Unit of Muscular and Neurodegenerative Disorders, Laboratory of Molecular Medicine, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

Ahmad Alahmad (A)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE2 4HH, UK; Kuwait Medical Genetics Centre, Al-Sabah Medical Area 80901, Kuwait.

Marina Dutra-Clarke (M)

Division of Medical Genetics, Department of Pediatrics, David Geffen School of Medicine, the University of California at Los Angeles, Los Angeles, CA 90095, USA.

Sabine Grønborg (S)

Center for Rare Diseases, Department of Pediatrics and Department of Genetics, Copenhagen University Hospital Rigshospitalet, Blegdamsvej 9, Copenhagen 2100, Denmark.

Annapurna Sudarsanam (A)

West Midlands Regional Genetics Service, Birmingham Women's and Children's Hospital, Birmingham B15 2TG, UK.

Julie Vogt (J)

West Midlands Regional Genetics Service, Birmingham Women's and Children's Hospital, Birmingham B15 2TG, UK.

Filippo Arrigoni (F)

Paediatric Radiology and Neuroradiology Department, V. Buzzi Children's Hospital, Milan 20154, Italy.

Julia Baptista (J)

Peninsula Medical School, Faculty of Health, University of Plymouth, Plymouth PL4 8AA, UK.

Shahzad Haider (S)

Paediatrics Wah Medical College NUMS, Wah Cantonment, Punjab 44000, Pakistan.

René G Feichtinger (RG)

University Children's Hospital, Salzburger Landeskliniken (SALK) and Paracelsus Medical University (PMU), Salzburg 5020, Austria.

Paolo Bernardi (P)

Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58/B, Padova 35131, Italy.

Alessandra Zulian (A)

Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58/B, Padova 35131, Italy.

Mirjana Gusic (M)

Institute of Neurogenomics, Helmholtz Zentrum München, Neuherberg 85764, Germany; DZHK (German Centre for Cardiovascular Research), Partner Site Munich Heart Alliance, Munich 81675, Germany; Institute of Human Genetics, Technical University of Munich, Munich 81675, Germany.

Stephanie Efthymiou (S)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Renkui Bai (R)

GeneDx Inc, Gaithersburg, MD 20877, USA.

Farah Bibi (F)

Institute of Biochemistry and Biotechnology, Pir Mehar Ali Shah Arid Agriculture University, Rawalpindi 44000, Pakistan.

Alejandro Horga (A)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK; Neuromuscular Diseases Unit, Department of Neurology, Hospital Clinico San Carlos and San Carlos Health Research Institute (IdISSC), Madrid 28040, Spain.

Julian A Martinez-Agosto (JA)

Department of Human Genetics, Division of Medical Genetics, Department of Pediatrics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095, USA.

Amanda Lam (A)

Neurometabolic Unit, National Hospital for Neurology and Neurosurgery, London, UK; Department of Chemical Pathology, Great Ormond Street Hospital, WC1N 3BG London, UK.

Andreea Manole (A)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Diego-Perez Rodriguez (DP)

Department of Clinical Movement Neurosciences, Royal Free Campus, University College of London, Queen Square Institute of Neurology, London WC1N 3BG, UK.

Romina Durigon (R)

Department of Clinical Movement Neurosciences, Royal Free Campus, University College of London, Queen Square Institute of Neurology, London WC1N 3BG, UK.

Angela Pyle (A)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE2 4HH, UK.

Buthaina Albash (B)

Kuwait Medical Genetics Centre, Al-Sabah Medical Area 80901, Kuwait.

Carlo Dionisi-Vici (C)

Division of Metabolism, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

David Murphy (D)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Diego Martinelli (D)

Division of Metabolism, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

Enrico Bugiardini (E)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Katrina Allis (K)

GeneDx Inc, Gaithersburg, MD 20877, USA.

Costanza Lamperti (C)

Unit of Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20126, Italy.

Siegfried Reipert (S)

Core Facility of Cell Imaging and Ultrastructure Research, University of Vienna, Djerassiplatz 1, 1030 Wien, Austria.

Lotte Risom (L)

Department of Genetics, Copenhagen University Hospital Rigshospitalet Blegdamsvej, Copenhagen 2100, Denmark.

Lucia Laugwitz (L)

Institute of Medical Genetics and Applied Genomics, University of Tuebingen, 72076 Tübingen, Germany; Department of Neuropediatrics, Developmental Neurology and Social Pediatrics, University of Tübingen, Tübingen 72076, Germany.

Michela Di Nottia (M)

Unit of Muscular and Neurodegenerative Disorders, Laboratory of Molecular Medicine, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

Robert McFarland (R)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE2 4HH, UK; NHS Highly Specialised Service for Rare Mitochondrial Disorders, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne NE1 4LP, UK.

Laura Vilarinho (L)

Unit of Neonatal Screening, Metabolism and Genetics, Department of Human Genetics, National Institute of Health Dr Ricardo Jorge, Porto 4000-055, Portugal.

Michael Hanna (M)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK.

Holger Prokisch (H)

Institute of Neurogenomics, Helmholtz Zentrum München, Neuherberg 85764, Germany; Institute of Human Genetics, Technical University of Munich, Munich 81675, Germany.

Johannes A Mayr (JA)

University Children's Hospital, Salzburger Landeskliniken (SALK) and Paracelsus Medical University (PMU), Salzburg 5020, Austria.

Enrico Silvio Bertini (ES)

Unit of Muscular and Neurodegenerative Disorders, Laboratory of Molecular Medicine, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

Daniele Ghezzi (D)

Unit of Medical Genetics and Neurogenetics, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20126, Italy; Department of Pathophysiology and Transplantation, University of Milan, Milan 20122, Italy.

Elsebet Østergaard (E)

Department of Genetics, Copenhagen University Hospital Rigshospitalet Blegdamsvej, Copenhagen 2100, Denmark; Institute for Clinical Medicine, University of Copenhagen, Copenhagen 2200, Denmark.

Saskia B Wortmann (SB)

University Children's Hospital, Salzburger Landeskliniken (SALK) and Paracelsus Medical University (PMU), Salzburg 5020, Austria; Institute of Neurogenomics, Helmholtz Zentrum München, Neuherberg 85764, Germany; Institute of Human Genetics, Technical University of Munich, Munich 81675, Germany; Radboud Center for Mitochondrial Medicine, Department of Pediatrics, Amalia Children's Hospital, Radboudumc, Nijmegen 6525 EZ, the Netherlands.

Rosalba Carrozzo (R)

Unit of Muscular and Neurodegenerative Disorders, Laboratory of Molecular Medicine, Bambino Gesù Children's Hospital, IRCCS, Rome 00146, Italy.

Tobias B Haack (TB)

Department of Neuropediatrics, Developmental Neurology and Social Pediatrics, University of Tübingen, Tübingen 72076, Germany; Centre for Rare Diseases, University of Tuebingen, Tübingen 72076, Germany.

Robert W Taylor (RW)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE2 4HH, UK; NHS Highly Specialised Service for Rare Mitochondrial Disorders, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne NE1 4LP, UK.

Antonella Spinazzola (A)

Department of Clinical Movement Neurosciences, Royal Free Campus, University College of London, Queen Square Institute of Neurology, London WC1N 3BG, UK.

Karin Nowikovsky (K)

Department of Biomedical Sciences, Institute of Physiology, Pathophysiology and Biophysics, University of Veterinary Medicine Vienna, Vienna 1210, Austria; Department of Internal Medicine I, ASCTR and Comprehensive Cancer Center, Medical University of Vienna, Vienna 1090, Austria. Electronic address: karin.nowikovsky@vetmeduni.ac.at.

Henry Houlden (H)

Department of Neuromuscular Diseases, University College London, Queen Square, Institute of Neurology, London WC1N 3BG, UK. Electronic address: h.houlden@ucl.ac.uk.

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