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CYP46A1 gene therapy deciphers the role of brain cholesterol metabolism in Huntington's disease.
Kacher, Radhia; Lamazière, Antonin; Heck, Nicolas; Kappes, Vincent; Mounier, Coline; Despres, Gaëtan; Dembitskaya, Yulia; Perrin, Elodie; Christaller, Wilhelm; Sasidharan Nair, Satish; Messent, Valérie; Cartier, Nathalie; Vanhoutte, Peter; Venance, Laurent; Saudou, Frédéric; Néri, Christian; Caboche, Jocelyne; Betuing, Sandrine.
Afiliación
  • Kacher R; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Lamazière A; LBM, CNRS UMR7203/INSERM U1157, Sorbonne Université, Faculté de Médecine, AP-HP, Hôpital Saint Antoine, Département PM2, Paris, France.
  • Heck N; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Kappes V; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Mounier C; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Despres G; LBM, CNRS UMR7203/INSERM U1157, Sorbonne Université, Faculté de Médecine, AP-HP, Hôpital Saint Antoine, Département PM2, Paris, France.
  • Dembitskaya Y; Center for Interdisciplinary Research in Biology, College de France, CNRS UMR7241/INSERM U1050, MemoLife Labex Paris, France.
  • Perrin E; Center for Interdisciplinary Research in Biology, College de France, CNRS UMR7241/INSERM U1050, MemoLife Labex Paris, France.
  • Christaller W; Université Grenoble Alpes, Grenoble Institut des Neurosciences, INSERM U1216, CHU Grenoble Alpes, 38000 Grenoble, France.
  • Sasidharan Nair S; Sorbonne Université, Centre National de la Recherche Scientifique, Research Unit Biology of Adaptation and Aging (B2A), Team Compensation in Neurodegenerative and Aging (Brain-C), F-75252, Paris, France.
  • Messent V; Neuroplasticity of Reproductive Behaviors, Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine, Institut de Biologie Paris Seine, Faculté des Sciences et Ingénierie, INSERM/UMR-S 1130, CNRS/UMR 8246, 75005 Paris, France.
  • Cartier N; Biotherapies for neurodegenerative diseases, Institut du Cerveau et de la Moelle (ICM) INSERM Sorbonne Université, Paris, France.
  • Vanhoutte P; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Venance L; Center for Interdisciplinary Research in Biology, College de France, CNRS UMR7241/INSERM U1050, MemoLife Labex Paris, France.
  • Saudou F; Université Grenoble Alpes, Grenoble Institut des Neurosciences, INSERM U1216, CHU Grenoble Alpes, 38000 Grenoble, France.
  • Néri C; Sorbonne Université, Centre National de la Recherche Scientifique, Research Unit Biology of Adaptation and Aging (B2A), Team Compensation in Neurodegenerative and Aging (Brain-C), F-75252, Paris, France.
  • Caboche J; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
  • Betuing S; Neuroscience Paris Seine, Institut de Biologie Paris-Seine, CNRS UMR 8246/INSERM U1130., Sorbonne Université, Paris, France.
Brain ; 142(8): 2432-2450, 2019 08 01.
Article en En | MEDLINE | ID: mdl-31286142
Dysfunctions in brain cholesterol homeostasis have been extensively related to brain disorders. The main pathway for brain cholesterol elimination is its hydroxylation into 24S-hydroxycholesterol by the cholesterol 24-hydrolase, CYP46A1. Increasing evidence suggests that CYP46A1 has a role in the pathogenesis and progression of neurodegenerative disorders, and that increasing its levels in the brain is neuroprotective. However, the mechanisms underlying this neuroprotection remain to be fully understood. Huntington's disease is a fatal autosomal dominant neurodegenerative disease caused by an abnormal CAG expansion in huntingtin's gene. Among the multiple cellular and molecular dysfunctions caused by this mutation, altered brain cholesterol homeostasis has been described in patients and animal models as a critical event in Huntington's disease. Here, we demonstrate that a gene therapy approach based on the delivery of CYP46A1, the rate-limiting enzyme for cholesterol degradation in the brain, has a long-lasting neuroprotective effect in Huntington's disease and counteracts multiple detrimental effects of the mutated huntingtin. In zQ175 Huntington's disease knock-in mice, CYP46A1 prevented neuronal dysfunctions and restored cholesterol homeostasis. These events were associated to a specific striatal transcriptomic signature that compensates for multiple mHTT-induced dysfunctions. We thus explored the mechanisms for these compensations and showed an improvement of synaptic activity and connectivity along with the stimulation of the proteasome and autophagy machineries, which participate to the clearance of mutant huntingtin (mHTT) aggregates. Furthermore, BDNF vesicle axonal transport and TrkB endosome trafficking were restored in a cellular model of Huntington's disease. These results highlight the large-scale beneficial effect of restoring cholesterol homeostasis in neurodegenerative diseases and give new opportunities for developing innovative disease-modifying strategies in Huntington's disease.
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Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Encéfalo / Terapia Genética / Colesterol / Enfermedad de Huntington / Fármacos Neuroprotectores / Colesterol 24-Hidroxilasa / Vectores Genéticos Tipo de estudio: Prognostic_studies Límite: Animals / Humans Idioma: En Revista: Brain Año: 2019 Tipo del documento: Article País de afiliación: Francia Pais de publicación: Reino Unido

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Encéfalo / Terapia Genética / Colesterol / Enfermedad de Huntington / Fármacos Neuroprotectores / Colesterol 24-Hidroxilasa / Vectores Genéticos Tipo de estudio: Prognostic_studies Límite: Animals / Humans Idioma: En Revista: Brain Año: 2019 Tipo del documento: Article País de afiliación: Francia Pais de publicación: Reino Unido