Neurodegeneration in a Transgenic Mouse Model of Multiple System Atrophy Is Associated with Altered Expression of Oligodendroglial-Derived Neurotrophic Factors
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Multiple system atrophy (MSA) is a neurodegenerative disorder characterized by striatonigral degeneration and olivo-pontocerebellar atrophy. Neuronal degeneration is accompanied by primarily oligodendrocytic accumulation of α-synuclein (αsyn) as opposed to the neuronal inclusions more commonly found in other α-synucleinopathies such as Parkinson's disease. It is unclear how αsyn accumulation in oligodendrocytes may lead to the extensive neurodegeneration observed in MSA; we hypothesize that the altered expression of oligodendrocyte-derived neurotrophic factors by αsyn may be involved. In this context, the expression of a number neurotrophic factors reportedly expressed by oligodendrocytes [glial-derived neurotrophic factor (GDNF), brain-derived neurotrophic factor (BDNF), and insulin-like growth factor 1 (IGF-1), as well as basic fibroblast growth factor 2 (bFGF2), reportedly astrocyte derived] were examined in transgenic mouse models expressing human αsyn (hαsyn) under the control of either neuronal (PDGFβ or mThy1) or oligodendrocytic (MBP) promoters. Although protein levels of BDNF and IGF-1 were altered in all the αsyn transgenic mice regardless of promoter type, a specific decrease in GDNF protein expression was observed in the MBP-hαsyn transgenic mice. Intracerebroventricular infusion of GDNF improved behavioral deficits and ameliorated neurodegenerative pathology in the MBP-hαsyn transgenic mice. Consistent with the studies in the MBP-hαsyn transgenic mice, analysis of GDNF expression levels in human MSA samples demonstrated a decrease in the white frontal cortex and to a lesser degree in the cerebellum compared with controls. These results suggest a mechanism in which αsyn expression in oligodendrocytes impacts on the trophic support provided by these cells for neurons, perhaps contributing to neurodegeneration.
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In MSA, in addition to GCIs, myelin degeneration, axonal damage, loss of neurotrophic support, neuronal loss, astrogliosis and microglial activation are pathological events seen in multiple regions of the central nervous system.
“The precise pathogenesis of MSA remains largely unknown, however, evidence from human postmortem cases and experimental models suggest that, in addition to GCIs, myelin degeneration, axonal damage, loss of neurotrophic support, neuronal loss, astrogliosis and microglial activation are pathological events seen in multiple regions of the central nervous system (CNS) [28, 56].”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [56]
The Introduction (page not provided) describes GCIs, myelin loss, neuronal loss across several CNS regions, astrogliosis and microgliosis in MSA. The Results report reduced GDNF in human MSA tissue, consistent with diminished neurotrophic support, but the Discussion presents disruption of neurotrophic support as a possibility. The passages do not establish axonal damage, so the full list is not supported by this source. (LLM, conf=0.86)
Experimental — accuracy not yet measuredDecreased neurotrophic support of oligodendroglia, as shown by reductions of glial derived neurotrophic factor expression levels, occurs in MSA transgenic mice and human MSA samples.
“Moreover, decreased neurotrophic support of oligodendroglia, as shown by reductions of glial derived neurotrophic factor expression levels in MSA tg mice and human MSA samples [56], furthers the idea that oligodendrocyte dysfunction is an early pathological event leading to secondary neurodegeneration related to retrograde axonal disease.”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [56]
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Self-citationGDNF, A Neuron-Derived Factor Upregulated in Glial Cells during Disease
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Immunotherapy for neurodegenerative diseases: Focus on α-synucleinopathies
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Self-citationInsulin resistance and exendin-4 treatment for multiple system atrophy
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T cell infiltration in both human multiple system atrophy and a novel mouse model of the disease
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Immunotherapies for Aging-Related Neurodegenerative Diseases—Emerging Perspectives and New Targets
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Self-citationAnimal models of multiple system atrophy
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Self-citationWidespread micro-RNA dysregulation in Multiple System Atrophy: disease-related alteration in miR-96
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Self-citationAn emerging role of dysfunctional axon-oligodendrocyte coupling in neurodegenerative diseases
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The neuropathology of multiple system atrophy and its therapeutic implications
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Gliotoxicity and Glioprotection: the Dual Role of Glial Cells
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Self-citationNeurons and Glia Interplay in α-Synucleinopathies
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Self-citationExtracellular Alpha-Synuclein: Mechanisms for Glial Cell Internalization and Activation
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Exploring Myelin Dysfunction in Multiple System Atrophy
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Self-citationRetractedTargeting α‐synuclein: Therapeutic options
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Self-citationRetractedOligodendrocytes in neurodegenerative diseases
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New insights into atypical parkinsonism
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Cross-examining candidate genes implicated in multiple system atrophy
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Self-citationFAS-Dependent Cell Death in α-Synuclein Transgenic Oligodendrocyte Models of Multiple System Atrophy
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Glia: an emerging target for neurological disease therapy
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An update on the cerebellar subtype of multiple system atrophy
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Mini Review: Effect of GLP-1 Receptor Agonists and SGLT-2 Inhibitors on the Growth Hormone/IGF Axis
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Oligodendrocyte-specific ATF4 inactivation does not influence the development of EAE
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“Multiple system atrophy: experimental models and reality”.
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Self-citationMSA: From basic mechanisms to experimental therapeutics
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- Authors
- Ubhi, K., Rockenstein, E., Mante, M., Inglis, C., Adame, A., Patrick, C., Whitney, K., & Masliah, E.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Masliah, Eliezer
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-05-05
- Volume
- 30
- Issue
- 18
- Pages
- 6236-6246
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2896284
- OpenAlex
- W2004154235
- Cited by
- 147
- References
- 74
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 8 · 2021: 9 · 2020: 12 · 2019: 12 · 2018: 8 · 2017: 14 · 2016: 9 · 2015: 10 · 2014: 17 · 2013: 17 · 2012: 10
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (AG‐022074, AG‐18440, NS044233, AG10435)
- National Institute on Aging (P01AG010435, R37AG018440, R01AG018440, AG022074, AG 18440, P01AG022074, AG10435)
- National Institute of Neurological Disorders and Stroke (P01NS044233, NS-044233)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- multiple system atrophy, alpha-synuclein, oligodendrocytes, neurotrophic factors, glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor, insulin-like growth factor I, basic fibroblast growth factor, neurodegeneration, striatonigral degeneration, transgenic mouse model, intracerebroventricular infusion, white matter
- MeSH terms
- Aged, Animals, Behavior, Animal, Brain, Disease Models, Animal, Female, Humans, Injections, Intraventricular, Male, Mice, Transgenic, Nerve Degeneration, Nerve Fibers, Myelinated, Nerve Growth Factors, Neurons, Oligodendroglia, Promoter Regions, Genetic, Mice, Knockout, Multiple System Atrophy, Glial Cell Line-Derived Neurotrophic Factor, Mice, alpha-Synuclein
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