Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains

<h3>Background</h3><p dir="ltr">Alpha-synuclein (α-syn) aggregation into proteinaceous intraneuronal inclusions, called Lewy bodies (LBs), is the neuropathological hallmark of Parkinson’s disease (PD) and related synucleinopathies. However, the exact role of α-syn inclusi...

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Main Author: Morgan Bérard (12219298) (author)
Other Authors: Laura Martínez-Drudis (17460758) (author), Razan Sheta (3825544) (author), Omar M. A. El-Agnaf (8809331) (author), Abid Oueslati (816135) (author)
Published: 2023
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_version_ 1864513520759996416
author Morgan Bérard (12219298)
author2 Laura Martínez-Drudis (17460758)
Razan Sheta (3825544)
Omar M. A. El-Agnaf (8809331)
Abid Oueslati (816135)
author2_role author
author
author
author
author_facet Morgan Bérard (12219298)
Laura Martínez-Drudis (17460758)
Razan Sheta (3825544)
Omar M. A. El-Agnaf (8809331)
Abid Oueslati (816135)
author_role author
dc.creator.none.fl_str_mv Morgan Bérard (12219298)
Laura Martínez-Drudis (17460758)
Razan Sheta (3825544)
Omar M. A. El-Agnaf (8809331)
Abid Oueslati (816135)
dc.date.none.fl_str_mv 2023-11-27T09:00:00Z
dc.identifier.none.fl_str_mv 10.1186/s13024-023-00683-8
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Non-invasive_systemic_viral_delivery_of_human_alpha-synuclein_mimics_selective_and_progressive_neuropathology_of_Parkinson_s_disease_in_rodent_brains/26776462
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biomedical and clinical sciences
Clinical sciences
Neurosciences
Alpha-synuclein
Adeno-associated virus
AAV-PHP.eB
Neurodegeneration Parkinson’s
Disease Animal model
Systemic delivery .
PD-like symptoms
Genetic model of PD
Protein aggregation
dc.title.none.fl_str_mv Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <h3>Background</h3><p dir="ltr">Alpha-synuclein (α-syn) aggregation into proteinaceous intraneuronal inclusions, called Lewy bodies (LBs), is the neuropathological hallmark of Parkinson’s disease (PD) and related synucleinopathies. However, the exact role of α-syn inclusions in PD pathogenesis remains elusive. This lack of knowledge is mainly due to the absence of optimal α-syn-based animal models that recapitulate the different stages of neurodegeneration.</p><h3>Methods</h3><p dir="ltr">Here we describe a novel approach for a systemic delivery of viral particles carrying human α-syn allowing for a large-scale overexpression of this protein in the mouse brain. This approach is based on the use of a new generation of adeno-associated virus (AAV), AAV-PHP.eB, with an increased capacity to cross the blood-brain barrier, thus offering a viable tool for a non-invasive and large-scale gene delivery in the central nervous system.</p><h3>Results</h3><p dir="ltr">Using this model, we report that widespread overexpression of human α-syn induced selective degeneration of dopaminergic (DA) neurons, an exacerbated neuroinflammatory response in the substantia nigra and a progressive manifestation of PD-like motor impairments. Interestingly, biochemical analysis revealed the presence of insoluble α-syn oligomers in the midbrain. Together, our data demonstrate that a single non-invasive systemic delivery of viral particles overexpressing α-syn prompted selective and progressive neuropathology resembling the early stages of PD.</p><h3>Conclusions</h3><p dir="ltr">Our new in vivo model represents a valuable tool to study the role of α-syn in PD pathogenesis and in the selective vulnerability of nigral DA neurons; and offers the opportunity to test new strategies targeting α-syn toxicity for the development of disease-modifying therapies for PD and related disorders.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular Neurodegeneration<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1186/s13024-023-00683-8" target="_blank">https://dx.doi.org/10.1186/s13024-023-00683-8</a></p>
eu_rights_str_mv openAccess
id Manara2_a3fec7e95d3e0ea66ac8848d97653d5c
identifier_str_mv 10.1186/s13024-023-00683-8
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26776462
publishDate 2023
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repository_id_str
rights_invalid_str_mv CC BY 4.0
spelling Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brainsMorgan Bérard (12219298)Laura Martínez-Drudis (17460758)Razan Sheta (3825544)Omar M. A. El-Agnaf (8809331)Abid Oueslati (816135)Biomedical and clinical sciencesClinical sciencesNeurosciencesAlpha-synucleinAdeno-associated virusAAV-PHP.eBNeurodegeneration Parkinson’sDisease Animal modelSystemic delivery .PD-like symptomsGenetic model of PDProtein aggregation<h3>Background</h3><p dir="ltr">Alpha-synuclein (α-syn) aggregation into proteinaceous intraneuronal inclusions, called Lewy bodies (LBs), is the neuropathological hallmark of Parkinson’s disease (PD) and related synucleinopathies. However, the exact role of α-syn inclusions in PD pathogenesis remains elusive. This lack of knowledge is mainly due to the absence of optimal α-syn-based animal models that recapitulate the different stages of neurodegeneration.</p><h3>Methods</h3><p dir="ltr">Here we describe a novel approach for a systemic delivery of viral particles carrying human α-syn allowing for a large-scale overexpression of this protein in the mouse brain. This approach is based on the use of a new generation of adeno-associated virus (AAV), AAV-PHP.eB, with an increased capacity to cross the blood-brain barrier, thus offering a viable tool for a non-invasive and large-scale gene delivery in the central nervous system.</p><h3>Results</h3><p dir="ltr">Using this model, we report that widespread overexpression of human α-syn induced selective degeneration of dopaminergic (DA) neurons, an exacerbated neuroinflammatory response in the substantia nigra and a progressive manifestation of PD-like motor impairments. Interestingly, biochemical analysis revealed the presence of insoluble α-syn oligomers in the midbrain. Together, our data demonstrate that a single non-invasive systemic delivery of viral particles overexpressing α-syn prompted selective and progressive neuropathology resembling the early stages of PD.</p><h3>Conclusions</h3><p dir="ltr">Our new in vivo model represents a valuable tool to study the role of α-syn in PD pathogenesis and in the selective vulnerability of nigral DA neurons; and offers the opportunity to test new strategies targeting α-syn toxicity for the development of disease-modifying therapies for PD and related disorders.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular Neurodegeneration<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1186/s13024-023-00683-8" target="_blank">https://dx.doi.org/10.1186/s13024-023-00683-8</a></p>2023-11-27T09:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1186/s13024-023-00683-8https://figshare.com/articles/journal_contribution/Non-invasive_systemic_viral_delivery_of_human_alpha-synuclein_mimics_selective_and_progressive_neuropathology_of_Parkinson_s_disease_in_rodent_brains/26776462CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/267764622023-11-27T09:00:00Z
spellingShingle Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
Morgan Bérard (12219298)
Biomedical and clinical sciences
Clinical sciences
Neurosciences
Alpha-synuclein
Adeno-associated virus
AAV-PHP.eB
Neurodegeneration Parkinson’s
Disease Animal model
Systemic delivery .
PD-like symptoms
Genetic model of PD
Protein aggregation
status_str publishedVersion
title Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
title_full Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
title_fullStr Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
title_full_unstemmed Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
title_short Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
title_sort Non-invasive systemic viral delivery of human alpha-synuclein mimics selective and progressive neuropathology of Parkinson’s disease in rodent brains
topic Biomedical and clinical sciences
Clinical sciences
Neurosciences
Alpha-synuclein
Adeno-associated virus
AAV-PHP.eB
Neurodegeneration Parkinson’s
Disease Animal model
Systemic delivery .
PD-like symptoms
Genetic model of PD
Protein aggregation