Imbalanced mitochondrial dynamics contributes to the pathogenesis of X-linked adrenoleukodystrophy


Por: Launay N, Lopez-Erauskin J, Bianchi P, Guha S, Parameswaran J, Coppa A, Torreni L, Schlüter A, Fourcade S, Paredes-Fuentes AJ, Artuch-Iriberri R, Casasnovas C, Ruiz M and Pujol A

Publicada: 3 jun 2024 Ahead of Print: 1 may 2024
Resumen:
The peroxisomal disease adrenoleukodystrophy (X-ALD) is caused by loss of the transporter of very-long-chain fatty acids (VLCFAs), ABCD1. An excess of VLCFAs disrupts essential homeostatic functions crucial for axonal maintenance, including redox metabolism, glycolysis and mitochondrial respiration. As mitochondrial function and morphology are intertwined, we set out to investigate the role of mitochondrial dynamics in X-ALD models.Using quantitative 3D transmission electron microscopy, we revealed mitochondrial fragmentation in corticospinal axons in Abcd1- mice. In patient fibroblasts, an excess of VLCFAs triggers mitochondrial fragmentation through the redox-dependent phosphorylation of DRP1 (DRP1S616). The blockade of DRP1-driven fission by the peptide P110 effectively preserved mitochondrial morphology. Furthermore, mRNA inhibition of DRP1 not only prevented mitochondrial fragmentation but also protected axonal health in a Caenorhabditis elegans model of X-ALD, underscoring DRP1 as a potential therapeutic target.Elevated levels of circulating cell-free mtDNA in patients' CSF align this leukodystrophy with primary mitochondrial disorders. Our findings underscore the intricate interplay between peroxisomal dysfunction, mitochondrial dynamics and axonal integrity in X-ALD, shedding light on potential avenues for therapeutic intervention. Launay et al. identify abnormalities in mitochondrial dynamics, favouring increased mitochondrial fission, in models of the inherited neurodegenerative disorder, X-linked adrenoleukodystrophy. Targeting mitochondrial dynamics could be a new avenue for therapeutic intervention.

Filiaciones:
Launay N:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

Lopez-Erauskin J:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California at San Diego, La Jolla, CA 92093, USA

Bianchi P:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 Physiology and Immunology, Facultat de Medicina, Institut de Neurociències and Department of Cell Biology, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain

Guha S:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 Nautilus Biotechnology, San Carlos, CA 94070, USA

Parameswaran J:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 Department of Cell Biology, Emory University, Atlanta, GA 30322, USA

Coppa A:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

Torreni L:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 Programa de Doctorat en Biomedicina, Universitat de Barcelona, 08193 Barcelona, Spain

Schlüter A:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

Fourcade S:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

Paredes-Fuentes AJ:
 Division of Inborn Errors of Metabolism-IBC, Biochemistry and Molecular Genetics Department, Hospital Clínic de Barcelona, 08028 Barcelona, Spain

Artuch-Iriberri R:
 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

 Clinical Biochemistry Department, Institut de Recerca Sant Joan de Déu, Hospital Sant Joan de Déu, 08950 Barcelona, Spain

Casasnovas C:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

 Neuromuscular Unit, Neurology Department, Bellvitge University Hospital, Universitat de Barcelona, 08907 Lhospitalet de Llobregat, Barcelona, Spain

Ruiz M:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

Pujol A:
 Neurometabolic Diseases Laboratory, Institute of Neuropathology, IDIBELL, 08908 L'Hospitalet de Llobregat, Barcelona, Spain

 CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, ISCIII, 28029 Madrid, Spain

 Catalan Institution of Research and Advanced Studies (ICREA), 08010 Barcelona, Spain
ISSN: 00068950





BRAIN
Editorial
OXFORD UNIV PRESS, GREAT CLARENDON ST, OXFORD OX2 6DP, ENGLAND, Reino Unido
Tipo de documento: Article
Volumen: 147 Número: 6
Páginas: 2069-2084
WOS Id: 001226439900001
ID de PubMed: 38763511
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