Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys

Background: Progressive neuronal death in monoaminergic nuclei and widespread accumulation of α-synuclein are neuropathological hallmarks of Parkinson's disease (PD). Given that α-synuclein may be an early mediator of the pathological cascade that ultimately leads to neurodegeneration, decrease...

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Autores: Alarcón-Arís, Diana, Pavia-Collado, Rubén, Miquel-Rio, Lluís, Coppola-Segovia, Valentín, Ferrés-Coy, Albert, Ruiz-Bronchal, Esther, Galofré, Mireia, Paz, Verónica, Campa, Leticia, Revilla, Raquel, Montefeltro, Andrés, Kordower, Jeffrey H., Vila, M., Artigas, Francesc, Bortolozzi, Analía
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/223696
Acceso en línea:http://hdl.handle.net/10261/223696
Access Level:acceso abierto
Palabra clave:α-Synuclein
Antisense oligonucleotides
Axonal neurodegeneration
Dopamine neurotransmission
Mouse and monkey models
Parkinson's disease
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spelling Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeysAlarcón-Arís, DianaPavia-Collado, RubénMiquel-Rio, LluísCoppola-Segovia, ValentínFerrés-Coy, AlbertRuiz-Bronchal, EstherGalofré, MireiaPaz, VerónicaCampa, LeticiaRevilla, RaquelMontefeltro, AndrésKordower, Jeffrey H.Vila, M.Artigas, FrancescBortolozzi, Analíaα-SynucleinAntisense oligonucleotidesAxonal neurodegenerationDopamine neurotransmissionMouse and monkey modelsParkinson's diseaseBackground: Progressive neuronal death in monoaminergic nuclei and widespread accumulation of α-synuclein are neuropathological hallmarks of Parkinson's disease (PD). Given that α-synuclein may be an early mediator of the pathological cascade that ultimately leads to neurodegeneration, decreased α-synuclein synthesis will abate neurotoxicity if delivered to the key affected neurons. Methods: We used a non-viral gene therapy based on a new indatraline-conjugated antisense oligonucleotide (IND-ASO) to disrupt the α-synuclein mRNA transcription selectively in monoamine neurons of a PD-like mouse model and elderly nonhuman primates. Molecular, cell biology, histological, neurochemical and behavioral assays were performed. Findings: Intracerebroventricular and intranasal IND-ASO administration for four weeks in a mouse model with AAV-mediated wild-type human α-synuclein overexpression in dopamine neurons prevented the synthesis and accumulation of α-synuclein in the connected brain regions, improving dopamine neurotransmission. Likewise, the four-week IND-ASO treatment led to decreased levels of endogenous α-synuclein protein in the midbrain monoamine nuclei of nonhuman primates, which are affected early in PD. Conclusions: : The inhibition of α-synuclein production in dopamine neurons and its accumulation in cortical/striatal projection areas may alleviate the early deficits of dopamine function, showing the high translational value of antisense oligonucleotides as a disease modifying therapy for PD and related synucleinopathies.Grants SAF2016-75797-R, RTC-2014-2812-1 and RTC-2015-3309-1, Ministry of Economy and Competitiveness (MINECO) and European Regional Development Fund (ERDF), UE; Grant ID 9238, Michael J. Fox Foundation; and Centres for Networked Biomedical Research on Mental Health (CIBERSAM), and on Neurodegenerative Diseases (CIBERNED).ElsevierMinisterio de Economía y Competitividad (España)European CommissionMichael J. Fox Foundation for Parkinson's ResearchCentro de Investigación Biomédica en Red Salud Mental (España)Centro Investigación Biomédica en Red Enfermedades Neurodegenerativas (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2020202020202020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/223696reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2016-75797-Rinfo:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/RTC-2014-2812-1info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/RTC-2015-3309-1http://dx.doi.org/10.1016/j.ebiom.2020.102944Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2236962026-05-22T06:33:51Z
dc.title.none.fl_str_mv Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
title Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
spellingShingle Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
Alarcón-Arís, Diana
α-Synuclein
Antisense oligonucleotides
Axonal neurodegeneration
Dopamine neurotransmission
Mouse and monkey models
Parkinson's disease
title_short Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
title_full Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
title_fullStr Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
title_full_unstemmed Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
title_sort Anti-α-synuclein ASO delivered to monoamine neurons prevents α-synuclein accumulation in a Parkinson's disease-like mouse model and in monkeys
dc.creator.none.fl_str_mv Alarcón-Arís, Diana
Pavia-Collado, Rubén
Miquel-Rio, Lluís
Coppola-Segovia, Valentín
Ferrés-Coy, Albert
Ruiz-Bronchal, Esther
Galofré, Mireia
Paz, Verónica
Campa, Leticia
Revilla, Raquel
Montefeltro, Andrés
Kordower, Jeffrey H.
Vila, M.
Artigas, Francesc
Bortolozzi, Analía
author Alarcón-Arís, Diana
author_facet Alarcón-Arís, Diana
Pavia-Collado, Rubén
Miquel-Rio, Lluís
Coppola-Segovia, Valentín
Ferrés-Coy, Albert
Ruiz-Bronchal, Esther
Galofré, Mireia
Paz, Verónica
Campa, Leticia
Revilla, Raquel
Montefeltro, Andrés
Kordower, Jeffrey H.
Vila, M.
Artigas, Francesc
Bortolozzi, Analía
author_role author
author2 Pavia-Collado, Rubén
Miquel-Rio, Lluís
Coppola-Segovia, Valentín
Ferrés-Coy, Albert
Ruiz-Bronchal, Esther
Galofré, Mireia
Paz, Verónica
Campa, Leticia
Revilla, Raquel
Montefeltro, Andrés
Kordower, Jeffrey H.
Vila, M.
Artigas, Francesc
Bortolozzi, Analía
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
European Commission
Michael J. Fox Foundation for Parkinson's Research
Centro de Investigación Biomédica en Red Salud Mental (España)
Centro Investigación Biomédica en Red Enfermedades Neurodegenerativas (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv α-Synuclein
Antisense oligonucleotides
Axonal neurodegeneration
Dopamine neurotransmission
Mouse and monkey models
Parkinson's disease
topic α-Synuclein
Antisense oligonucleotides
Axonal neurodegeneration
Dopamine neurotransmission
Mouse and monkey models
Parkinson's disease
description Background: Progressive neuronal death in monoaminergic nuclei and widespread accumulation of α-synuclein are neuropathological hallmarks of Parkinson's disease (PD). Given that α-synuclein may be an early mediator of the pathological cascade that ultimately leads to neurodegeneration, decreased α-synuclein synthesis will abate neurotoxicity if delivered to the key affected neurons. Methods: We used a non-viral gene therapy based on a new indatraline-conjugated antisense oligonucleotide (IND-ASO) to disrupt the α-synuclein mRNA transcription selectively in monoamine neurons of a PD-like mouse model and elderly nonhuman primates. Molecular, cell biology, histological, neurochemical and behavioral assays were performed. Findings: Intracerebroventricular and intranasal IND-ASO administration for four weeks in a mouse model with AAV-mediated wild-type human α-synuclein overexpression in dopamine neurons prevented the synthesis and accumulation of α-synuclein in the connected brain regions, improving dopamine neurotransmission. Likewise, the four-week IND-ASO treatment led to decreased levels of endogenous α-synuclein protein in the midbrain monoamine nuclei of nonhuman primates, which are affected early in PD. Conclusions: : The inhibition of α-synuclein production in dopamine neurons and its accumulation in cortical/striatal projection areas may alleviate the early deficits of dopamine function, showing the high translational value of antisense oligonucleotides as a disease modifying therapy for PD and related synucleinopathies.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/223696
url http://hdl.handle.net/10261/223696
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2016-75797-R
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/RTC-2014-2812-1
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/RTC-2015-3309-1
http://dx.doi.org/10.1016/j.ebiom.2020.102944

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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