Pathogenic Variants in the Myosin Chaperone UNC-45B Cause Progressive Myopathy with Eccentric Cores.


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:
03 12 2020
Historique:
received: 15 06 2020
accepted: 03 11 2020
pubmed: 21 11 2020
medline: 13 1 2021
entrez: 20 11 2020
Statut: ppublish

Résumé

The myosin-directed chaperone UNC-45B is essential for sarcomeric organization and muscle function from Caenorhabditis elegans to humans. The pathological impact of UNC-45B in muscle disease remained elusive. We report ten individuals with bi-allelic variants in UNC45B who exhibit childhood-onset progressive muscle weakness. We identified a common UNC45B variant that acts as a complex hypomorph splice variant. Purified UNC-45B mutants showed changes in folding and solubility. In situ localization studies further demonstrated reduced expression of mutant UNC-45B in muscle combined with abnormal localization away from the A-band towards the Z-disk of the sarcomere. The physiological relevance of these observations was investigated in C. elegans by transgenic expression of conserved UNC-45 missense variants, which showed impaired myosin binding for one and defective muscle function for three. Together, our results demonstrate that UNC-45B impairment manifests as a chaperonopathy with progressive muscle pathology, which discovers the previously unknown conserved role of UNC-45B in myofibrillar organization.

Identifiants

pubmed: 33217308
pii: S0002-9297(20)30399-2
doi: 10.1016/j.ajhg.2020.11.002
pmc: PMC7820787
pii:
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0
Molecular Chaperones 0
UNC45B protein, human 0
unc-45 protein, C elegans 0
Myosins EC 3.6.4.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1078-1095

Informations de copyright

Copyright © 2020. Published by Elsevier Inc.

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Auteurs

Sandra Donkervoort (S)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Carl E Kutzner (CE)

Institute for Genetics and Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany.

Ying Hu (Y)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Xavière Lornage (X)

Institut de Génétique et de Biologie Moléculaire et Cellulaire, INSERM U1258, CNRS UMR7104, Université de Strasbourg, BP 10142, 67404 Illkirch, France.

John Rendu (J)

Centre Hospitalier Universitaire de Grenoble Alpes, Biochimie Génétique et Moléculaire, Grenoble 38000, France; Grenoble Institut des Neurosciences-INSERM U1216 UGA, Grenoble 38000, France.

Tanya Stojkovic (T)

Centre de Référence des Maladies Neuromusculaires Nord/Est/Ile de France, Institut de Myologie, GHU La Pitié-Salpêtrière, Sorbonne Université, AP-HP, 75013 Paris, France.

Jonathan Baets (J)

Faculty of Medicine, University of Antwerp, 2610 Antwerp, Belgium; Laboratory of Neuromuscular Pathology, Institute Born-Bunge, University of Antwerp, 2610 Antwerp, Belgium; Neuromuscular Reference Centre, Department of Neurology, Antwerp University Hospital, 2650 Antwerp, Belgium.

Sarah B Neuhaus (SB)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Jantima Tanboon (J)

Department of Pathology, Faculty of Medicine, Siriraj Hospital, Mahidol University, 10700 Bangkok, Thailand; Department of Neuromuscular Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 187-8502 Tokyo, Japan.

Reza Maroofian (R)

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

Véronique Bolduc (V)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Magdalena Mroczek (M)

John Walton Muscular Dystrophy Research Centre, Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne NE1 3BZ, UK.

Stefan Conijn (S)

Department of Physiology, Amsterdam UMC (location VUmc), 1081 HZ Amsterdam, the Netherlands.

Nancy L Kuntz (NL)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA.

Ana Töpf (A)

John Walton Muscular Dystrophy Research Centre, Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne NE1 3BZ, UK.

Soledad Monges (S)

Servicio de Neurología y Servicio de Patologia, Hospital de Pediatría Garrahan, C1245 AAM Buenos Aires, Argentina.

Fabiana Lubieniecki (F)

Servicio de Neurología y Servicio de Patologia, Hospital de Pediatría Garrahan, C1245 AAM Buenos Aires, Argentina.

Riley M McCarty (RM)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Katherine R Chao (KR)

Center for Mendelian Genomics, Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Serena Governali (S)

Department of Physiology, Amsterdam UMC (location VUmc), 1081 HZ Amsterdam, the Netherlands.

Johann Böhm (J)

Institut de Génétique et de Biologie Moléculaire et Cellulaire, INSERM U1258, CNRS UMR7104, Université de Strasbourg, BP 10142, 67404 Illkirch, France.

Kanokwan Boonyapisit (K)

Department of Medicine, Faculty of Medicine, Siriraj Hospital, Mahidol, University, 10700 Bangkok, Thailand.

Edoardo Malfatti (E)

Neurology Department, Raymond-Poincaré teaching hospital, centre de référence des maladies neuromusculaires Nord/Est/Ile-de-France, AP-HP, 92380 Garches, France.

Tumtip Sangruchi (T)

Department of Pathology, Faculty of Medicine, Siriraj Hospital, Mahidol University, 10700 Bangkok, Thailand.

Iren Horkayne-Szakaly (I)

Joint Pathology Center, Defense Health Agency, Silver Spring, MD 20910, USA.

Carola Hedberg-Oldfors (C)

Department of Laboratory Medicine, Sahlgrenska Academy, University of Gothenburg, 405 30 Gothenburg, Sweden.

Stephanie Efthymiou (S)

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

Satoru Noguchi (S)

Department of Neuromuscular Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 187-8502 Tokyo, Japan; Department of Genome Medicine Development, Medical Genome Center, National Center of Neurology and Psychiatry, 187-8551 Tokyo, Japan.

Sarah Djeddi (S)

Institut de Génétique et de Biologie Moléculaire et Cellulaire, INSERM U1258, CNRS UMR7104, Université de Strasbourg, BP 10142, 67404 Illkirch, France.

Aritoshi Iida (A)

Department of Clinical Genome Analysis, Medical Genome Center, National Center of Neurology and Psychiatry, 187-8551 Tokyo, Japan.

Gabriella di Rosa (G)

Division of Child Neurology and Psychiatry, Department of the Adult and Developmental Age Human Pathology, University of Messina, Messina 98125, Italy.

Chiara Fiorillo (C)

Pediatric Neurology and Muscular Diseases Unit, G. Gaslini Institute, 16147 Genoa, Italy; Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132 Genoa, Italy.

Vincenzo Salpietro (V)

Pediatric Neurology and Muscular Diseases Unit, G. Gaslini Institute, 16147 Genoa, Italy; Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University of Genoa, 16132 Genoa, Italy.

Niklas Darin (N)

Department of Pediatrics, Institute of Clinical Sciences, Sahlgrenska Academy at University of Gothenburg, 41650 Gothenburg, Sweden.

Julien Fauré (J)

Centre Hospitalier Universitaire de Grenoble Alpes, Biochimie Génétique et Moléculaire, Grenoble 38000, France; Grenoble Institut des Neurosciences-INSERM U1216 UGA, Grenoble 38000, France.

Henry Houlden (H)

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

Anders Oldfors (A)

Department of Laboratory Medicine, Sahlgrenska Academy, University of Gothenburg, 405 30 Gothenburg, Sweden.

Ichizo Nishino (I)

Department of Neuromuscular Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 187-8502 Tokyo, Japan; Department of Genome Medicine Development, Medical Genome Center, National Center of Neurology and Psychiatry, 187-8551 Tokyo, Japan; Department of Clinical Genome Analysis, Medical Genome Center, National Center of Neurology and Psychiatry, 187-8551 Tokyo, Japan.

Willem de Ridder (W)

Faculty of Medicine, University of Antwerp, 2610 Antwerp, Belgium; Laboratory of Neuromuscular Pathology, Institute Born-Bunge, University of Antwerp, 2610 Antwerp, Belgium; Neuromuscular Reference Centre, Department of Neurology, Antwerp University Hospital, 2650 Antwerp, Belgium.

Volker Straub (V)

John Walton Muscular Dystrophy Research Centre, Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne NE1 3BZ, UK; Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne NE7 7DN, UK.

Wojciech Pokrzywa (W)

Laboratory of Protein Metabolism in Development and Aging, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland.

Jocelyn Laporte (J)

Institut de Génétique et de Biologie Moléculaire et Cellulaire, INSERM U1258, CNRS UMR7104, Université de Strasbourg, BP 10142, 67404 Illkirch, France.

A Reghan Foley (AR)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA.

Norma B Romero (NB)

Centre de Référence des Maladies Neuromusculaires Nord/Est/Ile de France, Institut de Myologie, GHU La Pitié-Salpêtrière, Sorbonne Université, AP-HP, 75013 Paris, France; Université Sorbonne, UPMC Univ Paris 06, INSERM UMRS974, CNRS FRE3617, Center for Research in Myology, GH Pitié-Salpêtrière, 75651 Paris, France; Neuromuscular Morphology Unit, Myology Institute, GHU Pitié-Salpêtrière, 75013 Paris, France.

Coen Ottenheijm (C)

Department of Physiology, Amsterdam UMC (location VUmc), 1081 HZ Amsterdam, the Netherlands; Department of Cellular and Molecular Medicine, University of Arizona, Tucson, AZ 85718, USA.

Thorsten Hoppe (T)

Institute for Genetics and Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, 50931 Cologne, Germany; Center for Molecular Medicine Cologne, University of Cologne, 50931 Cologne, Germany. Electronic address: thorsten.hoppe@uni-koeln.de.

Carsten G Bönnemann (CG)

Neuromuscular and Neurogenetic Disorders of Childhood Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: carsten.bonnemann@nih.gov.

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