Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy

Abstract Multiple system atrophy (MSA) is a neurodegenerative disorder characterized by parkinsonism, cerebellar dysfunction, and autonomic failure. Key pathological features of MSA include the formation of glial cytoplasmic inclusions (GCIs) in oligodendrocytes (OLs), myelin loss, and neuroinflamma...

Full description

Saved in:
Bibliographic Details
Main Authors: Sam Chi-Hao Liu, Koping Chang, Meng-Ling Chen, Ming-Che Kuo, Teh-Cheng Wang, Ruey-Meei Wu
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Acta Neuropathologica Communications
Subjects:
Online Access:https://doi.org/10.1186/s40478-025-02014-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850190827112890368
author Sam Chi-Hao Liu
Koping Chang
Meng-Ling Chen
Ming-Che Kuo
Teh-Cheng Wang
Ruey-Meei Wu
author_facet Sam Chi-Hao Liu
Koping Chang
Meng-Ling Chen
Ming-Che Kuo
Teh-Cheng Wang
Ruey-Meei Wu
author_sort Sam Chi-Hao Liu
collection DOAJ
description Abstract Multiple system atrophy (MSA) is a neurodegenerative disorder characterized by parkinsonism, cerebellar dysfunction, and autonomic failure. Key pathological features of MSA include the formation of glial cytoplasmic inclusions (GCIs) in oligodendrocytes (OLs), myelin loss, and neuroinflammation. Although both inflammation and myelination are known to be critical in MSA, the roles of myelin proteins and their relationship with inflammation have often been overlooked. In this study, we injected AAV-Olig001 vectors carrying either human SNCA (AAV-hSNCA) or eGFP (AAV-eGFP) into the striatum of TgM83 transgenic mice, which express the A53T mutant form of human alpha-synuclein (αSyn), as well as into wild-type (WT) mice. We then assessed myelin protein expression and inflammatory responses. TgM83 mice injected with AAV-hSNCA exhibited demyelination, increased activation of microglia and astrocytes, and altered cytokine and chemokine profiles (including IL-1α, IL-10, IL-12(p40), CCL2, CCL3, CCL4, and CCL5), compared to both WT mice and TgM83 mice injected with AAV-eGFP. Interestingly, myelin basic protein (MBP) levels were significantly elevated around the injection site in TgM83 mice injected with AAV-hSNCA. Notably, we observed a positive correlation between MBP expression and inflammatory markers, as indicated by Iba1 and GFAP staining. These findings suggest that hSNCA overexpression is associated with increased MBP levels and enhanced inflammatory responses, implicating that MBP and myelination processes may play previously underappreciated roles in the pathogenesis of MSA.
format Article
id doaj-art-c0c17fb35122482884d4f7d587ff7fb1
institution OA Journals
issn 2051-5960
language English
publishDate 2025-05-01
publisher BMC
record_format Article
series Acta Neuropathologica Communications
spelling doaj-art-c0c17fb35122482884d4f7d587ff7fb12025-08-20T02:15:08ZengBMCActa Neuropathologica Communications2051-59602025-05-0113111810.1186/s40478-025-02014-yOligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophySam Chi-Hao Liu0Koping Chang1Meng-Ling Chen2Ming-Che Kuo3Teh-Cheng Wang4Ruey-Meei Wu5Department of Neurology, National Taiwan University College of MedicineDepartment of Pathology, National Taiwan University HospitalDepartment of Neurology, National Taiwan University College of MedicineDepartment of Neurology, National Taiwan University College of MedicineDepartment of Neurology, National Taiwan University College of MedicineDepartment of Neurology, National Taiwan University College of MedicineAbstract Multiple system atrophy (MSA) is a neurodegenerative disorder characterized by parkinsonism, cerebellar dysfunction, and autonomic failure. Key pathological features of MSA include the formation of glial cytoplasmic inclusions (GCIs) in oligodendrocytes (OLs), myelin loss, and neuroinflammation. Although both inflammation and myelination are known to be critical in MSA, the roles of myelin proteins and their relationship with inflammation have often been overlooked. In this study, we injected AAV-Olig001 vectors carrying either human SNCA (AAV-hSNCA) or eGFP (AAV-eGFP) into the striatum of TgM83 transgenic mice, which express the A53T mutant form of human alpha-synuclein (αSyn), as well as into wild-type (WT) mice. We then assessed myelin protein expression and inflammatory responses. TgM83 mice injected with AAV-hSNCA exhibited demyelination, increased activation of microglia and astrocytes, and altered cytokine and chemokine profiles (including IL-1α, IL-10, IL-12(p40), CCL2, CCL3, CCL4, and CCL5), compared to both WT mice and TgM83 mice injected with AAV-eGFP. Interestingly, myelin basic protein (MBP) levels were significantly elevated around the injection site in TgM83 mice injected with AAV-hSNCA. Notably, we observed a positive correlation between MBP expression and inflammatory markers, as indicated by Iba1 and GFAP staining. These findings suggest that hSNCA overexpression is associated with increased MBP levels and enhanced inflammatory responses, implicating that MBP and myelination processes may play previously underappreciated roles in the pathogenesis of MSA.https://doi.org/10.1186/s40478-025-02014-yMBPAAVOlig001TgM83 miceAlpha-synucleinopathyInflammation responsesMSA
spellingShingle Sam Chi-Hao Liu
Koping Chang
Meng-Ling Chen
Ming-Che Kuo
Teh-Cheng Wang
Ruey-Meei Wu
Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
Acta Neuropathologica Communications
MBP
AAVOlig001
TgM83 mice
Alpha-synucleinopathy
Inflammation responses
MSA
title Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
title_full Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
title_fullStr Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
title_full_unstemmed Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
title_short Oligodendrocyte-specific overexpression of human alpha-synuclein results in elevated MBP levels and inflammatory responses in TgM83 mice, mimicking the pathological features of multiple system atrophy
title_sort oligodendrocyte specific overexpression of human alpha synuclein results in elevated mbp levels and inflammatory responses in tgm83 mice mimicking the pathological features of multiple system atrophy
topic MBP
AAVOlig001
TgM83 mice
Alpha-synucleinopathy
Inflammation responses
MSA
url https://doi.org/10.1186/s40478-025-02014-y
work_keys_str_mv AT samchihaoliu oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy
AT kopingchang oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy
AT menglingchen oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy
AT mingchekuo oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy
AT tehchengwang oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy
AT rueymeeiwu oligodendrocytespecificoverexpressionofhumanalphasynucleinresultsinelevatedmbplevelsandinflammatoryresponsesintgm83micemimickingthepathologicalfeaturesofmultiplesystematrophy