Dominant mutations in MIEF1 affect mitochondrial dynamics and cause a singular late onset optic neuropathy.


Journal

Molecular neurodegeneration
ISSN: 1750-1326
Titre abrégé: Mol Neurodegener
Pays: England
ID NLM: 101266600

Informations de publication

Date de publication:
25 02 2021
Historique:
received: 02 06 2020
accepted: 08 02 2021
entrez: 26 2 2021
pubmed: 27 2 2021
medline: 6 11 2021
Statut: epublish

Résumé

Inherited optic neuropathies are the most common mitochondrial diseases, leading to neurodegeneration involving the irreversible loss of retinal ganglion cells, optic nerve degeneration and central visual loss. Importantly, properly regulated mitochondrial dynamics are critical for maintaining cellular homeostasis, and are further regulated by MIEF1 (mitochondrial elongation factor 1) which encodes for MID51 (mitochondrial dynamics protein 51), an outer mitochondrial membrane protein that acts as an adaptor protein to regulate mitochondrial fission. However, dominant mutations in MIEF1 have not been previously linked to any human disease. Using targeted sequencing of genes involved in mitochondrial dynamics, we report the first heterozygous variants in MIEF1 linked to disease, which cause an unusual form of late-onset progressive optic neuropathy characterized by the initial loss of peripheral visual fields. Pathogenic MIEF1 variants linked to optic neuropathy do not disrupt MID51's localization to the outer mitochondrial membrane or its oligomerization, but rather, significantly disrupt mitochondrial network dynamics compared to wild-type MID51 in high spatial and temporal resolution confocal microscopy live imaging studies. Together, our study identifies dominant MIEF1 mutations as a cause for optic neuropathy and further highlights the important role of properly regulated mitochondrial dynamics in neurodegeneration.

Identifiants

pubmed: 33632269
doi: 10.1186/s13024-021-00431-w
pii: 10.1186/s13024-021-00431-w
pmc: PMC7905578
doi:

Substances chimiques

MIEF1 protein, human 0
Membrane Proteins 0
Mitochondrial Proteins 0
Peptide Elongation Factors 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

12

Subventions

Organisme : NINDS NIH HHS
ID : R00 NS109252
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS076054
Pays : United States
Organisme : NINDS NIH HHS
ID : K99 NS109252
Pays : United States

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Auteurs

Majida Charif (M)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France.
Genetics and Immuno-Cell Therapy Team, Mohammed First University, Oujda, Morocco.

Yvette C Wong (YC)

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

Soojin Kim (S)

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

Agnès Guichet (A)

Departments of Biochemistry and Genetics, University Hospital Angers, Angers, France.

Catherine Vignal (C)

Neuroophthalmology Department, Rothschild Ophthalmologic Foundation, Paris, France.

Xavier Zanlonghi (X)

Centre de Compétence Maladies Rares, Clinique Pluridisciplinaire Jules Verne, Nantes, France.

Philippe Bensaid (P)

Cabinet d'Ophtalmologie, Morlaix, France.

Vincent Procaccio (V)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France.
Departments of Biochemistry and Genetics, University Hospital Angers, Angers, France.

Dominique Bonneau (D)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France.
Departments of Biochemistry and Genetics, University Hospital Angers, Angers, France.

Patrizia Amati-Bonneau (P)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France.
Departments of Biochemistry and Genetics, University Hospital Angers, Angers, France.

Pascal Reynier (P)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France.
Departments of Biochemistry and Genetics, University Hospital Angers, Angers, France.

Dimitri Krainc (D)

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

Guy Lenaers (G)

Université d'Angers, MitoLab team, UMR CNRS 6015 - INSERM U1083, Unité MitoVasc, Angers, France. guy.lenaers@inserm.fr.

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Classifications MeSH