Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice

Abstract A variety of pathophysiological mechanisms are implicated in Huntington's disease (HD). Among them, reduced cholesterol biosynthesis has been detected in the HD mouse brain from pre‐symptomatic stages, leading to diminished cholesterol synthesis, particularly in the striatum. In additi...

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Main Authors: Giulia Birolini, Marta Valenza, Eleonora Di Paolo, Elena Vezzoli, Francesca Talpo, Claudia Maniezzi, Claudio Caccia, Valerio Leoni, Franco Taroni, Vittoria D Bocchi, Paola Conforti, Elisa Sogne, Lara Petricca, Cristina Cariulo, Margherita Verani, Andrea Caricasole, Andrea Falqui, Gerardo Biella, Elena Cattaneo
Format: Article
Language:English
Published: Springer Nature 2020-09-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202012519
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author Giulia Birolini
Marta Valenza
Eleonora Di Paolo
Elena Vezzoli
Francesca Talpo
Claudia Maniezzi
Claudio Caccia
Valerio Leoni
Franco Taroni
Vittoria D Bocchi
Paola Conforti
Elisa Sogne
Lara Petricca
Cristina Cariulo
Margherita Verani
Andrea Caricasole
Andrea Falqui
Gerardo Biella
Elena Cattaneo
author_facet Giulia Birolini
Marta Valenza
Eleonora Di Paolo
Elena Vezzoli
Francesca Talpo
Claudia Maniezzi
Claudio Caccia
Valerio Leoni
Franco Taroni
Vittoria D Bocchi
Paola Conforti
Elisa Sogne
Lara Petricca
Cristina Cariulo
Margherita Verani
Andrea Caricasole
Andrea Falqui
Gerardo Biella
Elena Cattaneo
author_sort Giulia Birolini
collection DOAJ
description Abstract A variety of pathophysiological mechanisms are implicated in Huntington's disease (HD). Among them, reduced cholesterol biosynthesis has been detected in the HD mouse brain from pre‐symptomatic stages, leading to diminished cholesterol synthesis, particularly in the striatum. In addition, systemic injection of cholesterol‐loaded brain‐permeable nanoparticles ameliorates synaptic and cognitive function in a transgenic mouse model of HD. To identify an appropriate treatment regimen and gain mechanistic insights into the beneficial activity of exogenous cholesterol in the HD brain, we employed osmotic mini‐pumps to infuse three escalating doses of cholesterol directly into the striatum of HD mice in a continuous and rate‐controlled manner. All tested doses prevented cognitive decline, while amelioration of disease‐related motor defects was dose‐dependent. In parallel, we found morphological and functional recovery of synaptic transmission involving both excitatory and inhibitory synapses of striatal medium spiny neurons. The treatment also enhanced endogenous cholesterol biosynthesis and clearance of mutant Huntingtin aggregates. These results indicate that cholesterol infusion to the striatum can exert a dose‐dependent, disease‐modifying effect and may be therapeutically relevant in HD.
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institution Kabale University
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publishDate 2020-09-01
publisher Springer Nature
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spelling doaj-art-89f06c9b7c8d4934b2e0285e4e423d492025-08-20T04:02:55ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842020-09-01121012010.15252/emmm.202012519Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease miceGiulia Birolini0Marta Valenza1Eleonora Di Paolo2Elena Vezzoli3Francesca Talpo4Claudia Maniezzi5Claudio Caccia6Valerio Leoni7Franco Taroni8Vittoria D Bocchi9Paola Conforti10Elisa Sogne11Lara Petricca12Cristina Cariulo13Margherita Verani14Andrea Caricasole15Andrea Falqui16Gerardo Biella17Elena Cattaneo18Department of Biosciences, University of MilanDepartment of Biosciences, University of MilanDepartment of Biosciences, University of MilanDepartment of Biosciences, University of MilanDepartment of Biology and Biotechnologies, University of PaviaDepartment of Biology and Biotechnologies, University of PaviaUnit of Medical Genetics and Neurogenetics, Fondazione I.R.C.C.S. Istituto Neurologico Carlo BestaSchool of Medicine and Surgery, Monza and Laboratory of Clinical Pathology, Hospital of Desio, ASST‐Monza, University of Milano‐BicoccaUnit of Medical Genetics and Neurogenetics, Fondazione I.R.C.C.S. Istituto Neurologico Carlo BestaDepartment of Biosciences, University of MilanDepartment of Biosciences, University of MilanBiological and Environmental Science & Engineering (BESE) Division, NABLA Lab, King Abdullah University of Science and Technology (KAUST)Neuroscience Unit, Translational and Discovery Research Department, IRBM S.p.ANeuroscience Unit, Translational and Discovery Research Department, IRBM S.p.ANeuroscience Unit, Translational and Discovery Research Department, IRBM S.p.ANeuroscience Unit, Translational and Discovery Research Department, IRBM S.p.ABiological and Environmental Science & Engineering (BESE) Division, NABLA Lab, King Abdullah University of Science and Technology (KAUST)Department of Biology and Biotechnologies, University of PaviaDepartment of Biosciences, University of MilanAbstract A variety of pathophysiological mechanisms are implicated in Huntington's disease (HD). Among them, reduced cholesterol biosynthesis has been detected in the HD mouse brain from pre‐symptomatic stages, leading to diminished cholesterol synthesis, particularly in the striatum. In addition, systemic injection of cholesterol‐loaded brain‐permeable nanoparticles ameliorates synaptic and cognitive function in a transgenic mouse model of HD. To identify an appropriate treatment regimen and gain mechanistic insights into the beneficial activity of exogenous cholesterol in the HD brain, we employed osmotic mini‐pumps to infuse three escalating doses of cholesterol directly into the striatum of HD mice in a continuous and rate‐controlled manner. All tested doses prevented cognitive decline, while amelioration of disease‐related motor defects was dose‐dependent. In parallel, we found morphological and functional recovery of synaptic transmission involving both excitatory and inhibitory synapses of striatal medium spiny neurons. The treatment also enhanced endogenous cholesterol biosynthesis and clearance of mutant Huntingtin aggregates. These results indicate that cholesterol infusion to the striatum can exert a dose‐dependent, disease‐modifying effect and may be therapeutically relevant in HD.https://doi.org/10.15252/emmm.202012519aggregatesbehaviorcholesterolHuntington's diseasesynapses
spellingShingle Giulia Birolini
Marta Valenza
Eleonora Di Paolo
Elena Vezzoli
Francesca Talpo
Claudia Maniezzi
Claudio Caccia
Valerio Leoni
Franco Taroni
Vittoria D Bocchi
Paola Conforti
Elisa Sogne
Lara Petricca
Cristina Cariulo
Margherita Verani
Andrea Caricasole
Andrea Falqui
Gerardo Biella
Elena Cattaneo
Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
EMBO Molecular Medicine
aggregates
behavior
cholesterol
Huntington's disease
synapses
title Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
title_full Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
title_fullStr Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
title_full_unstemmed Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
title_short Striatal infusion of cholesterol promotes dose‐dependent behavioral benefits and exerts disease‐modifying effects in Huntington's disease mice
title_sort striatal infusion of cholesterol promotes dose dependent behavioral benefits and exerts disease modifying effects in huntington s disease mice
topic aggregates
behavior
cholesterol
Huntington's disease
synapses
url https://doi.org/10.15252/emmm.202012519
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