Neuropathology of multiple system atrophy: New thoughts about pathogenesis

Jellinger, Kurt A.

doi:10.1002/mds.26052

Cited by 181Parkinson's Disease Mechanisms and TreatmentsNeuroinflammation and Neurodegeneration MechanismsNeurological diseases and metabolism

Neuropathology of multiple system atrophy: New thoughts about pathogenesis

Jellinger, Kurt A.·2014·Movement Disorders

DOI 10.1002/mds.26052

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Abstract

Multiple system atrophy (MSA) is a fatal adult‐onset neurodegenerative disorder of uncertain etiology, clinically manifesting with autonomic failure associated with parkinsonism, cerebellar dysfunction, and pyramidal signs in variable combination. The pathological process affects central autonomic, striatonigral, and olivopontocerebellar systems. These show varying degrees of neurodegeneration and underlie the stratification of the heterogenous disorder into MSA‐P and MSA‐C clinical variants, which correlate to the morphologic phenotypes of striatonigral degeneration and olivopontocerebellar atrophy (MSA‐C). The lesions are not limited to these most consistently and severely affected systems but may involve many other parts of the central, peripheral, and autonomic nervous systems, underpinning the multisystem character of MSA. The histological core feature are glial cytoplasmic inclusions (GCIs, Papp‐Lantos bodies) in all types of oligodendroglia that contain aggregates of misfolded α‐Synuclein (α‐Syn). In addition to the ectopic appearance of α‐Syn in oligodendrocytes and other cells, oxidative stress, proteasomal and mitochondrial dysfunction, excitotoxiciy, neuroinflammation, metabolic changes, and energy failure are important contributors to the pathogenesis of MSA, as shown by various neurotoxic and transgenic animal models. Although the basic mechanisms of α‐Syn–triggered neurodegeneration are not completely understood, neuron‐to‐oligodendrocyte transfer of α‐Syn by prion‐like spreading, inducing oligodendroglial and myelin dysfunction associated with chronic neuroinflammation, are suggested finally to lead to a system‐specific pattern of neurodegeneration. © 2014 International Parkinson and Movement Disorder Society

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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 [28]
The model recapitulates early pathogenesis seen in MSA, as many of the pathological features induce dysfunction of the oligodendroglia-myelin-axon-neuron complex.
“Our model recapitulates early pathogenesis seen in MSA, as many of the pathological features induce dysfunction of the oligodendroglia-myelin-axon-neuron complex [28].”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [28]

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Tau protein in the glial cytoplasmic inclusions of multiple system atrophy can be distinguished from abnormal tau in Alzheimer's disease
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Multiple System Atrophy
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α-Synuclein Accumulates in Purkinje Cells in Lewy Body Disease but not in Multiple System Atrophy
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Protein Aggregation Mechanisms in Synucleinopathies: Commonalities and Differences
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α‐Synuclein mediates alterations in membrane conductance: a potential role for α‐synuclein oligomers in cell vulnerability
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Heredity in multiple system atrophy
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Gene expression changes in postmortem tissue from the rostral pons of multiple system atrophy patients
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Is there a risk of prion-like disease transmission by Alzheimer- or Parkinson-associated protein particles?
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Assessment of dementia in patients with multiple system atrophy
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Glucose metabolism in the cortical and subcortical brain structures in multiple system atrophy and Parkinson's disease: a positron emission tomographic study
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Striatal efferent involvement and its correlation to levodopa efficacy in patients with multiple system atrophy
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More frequent Lewy bodies but less frequent Alzheimer-type lesions in multiple system atrophy as compared to age-matched control brains
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Changes of unmyelinated nerve fibers in sural nerve in amyotrophic lateral sclerosis, Parkinson’s disease and multiple system atrophy
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Dopa resistance in multiple‐system atrophy: Loss of postsynaptic D2 receptors
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Molecular Pathological Classification of Neurodegenerative Diseases: Turning towards Precision Medicine
Kovács, G. G. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020189 · Cited by 322 · see citing works
Orthostatic Hypotension
Freeman, R. L., Abuzinadah, A. R., Gibbons, C. H., Jones, P. K., Miglis, M. G., & Sinn, D.-I. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.05.079 · Cited by 286 · see citing works
Initiation and propagation of α-synuclein aggregation in the nervous system
Hijaz, B. A., & Volpicelli‐Daley, L. A. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00368-6 · Cited by 267 · see citing works
18F-FDG PET in Parkinsonism: Differential Diagnosis and Evaluation of Cognitive Impairment
Meyer, P., Frings, L., Rücker, G., & Hellwig, S. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.186403 · Cited by 227 · see citing works
Orthostatic heart rate changes in patients with autonomic failure caused by neurodegenerative synucleinopathies
Norcliffe‐Kaufmann, L., Kaufmann, H., Palma, J., Shibao, C. A., Biaggioni, I., Peltier, A., Singer, W., Low, P. A., Goldstein, D. S., Gibbons, C. H., et al. (2018) · Annals of Neurology · doi:10.1002/ana.25170 · Cited by 243 · see citing works
Molecular pathology of neurodegenerative diseases: principles and practice
Kovács, G. G. (2019) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2019-205952 · Cited by 243 · see citing works
Multiple System Atrophy: An Oligodendroglioneural Synucleinopathy
Jellinger, K. A. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170397 · Cited by 209 · see citing works
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<i>APOE</i> genotype regulates pathology and disease progression in synucleinopathy
Davis, A. A., Inman, C. E., Wargel, Z. M., Dube, U., Freeberg, B. M., Galluppi, A., Haines, J. N., Dhavale, D. D., Miller, R., Choudhury, F. A., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aay3069 · Cited by 177 · see citing works
Alpha-synuclein research: defining strategic moves in the battle against Parkinson’s disease
Oliveira, L. M. A., Gasser, T., Edwards, R. H., Zweckstetter, M., Melki, R., Stefanis, L., Lashuel, H. A., Sulzer, D. L., Vekrellis, K., Halliday, G. M., et al. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00203-9 · Cited by 169 · see citing works
Beyond the synucleinopathies: alpha synuclein as a driving force in neurodegenerative comorbidities
Visanji, N. P., Lang, A. E., & Kovács, G. G. (2019) · Translational Neurodegeneration · doi:10.1186/s40035-019-0172-x · Cited by 99 · see citing works
Brain Iron Accumulation in Atypical Parkinsonian Syndromes: in vivo MRI Evidences for Distinctive Patterns
Lee, J., & Lee, M. S. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00074 · Cited by 95 · see citing works
Pushing Forward: Remyelination as the New Frontier in CNS Diseases
Kremer, D., Göttle, P., Hartung, H., & Küry, P. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.02.004 · Cited by 89 · see citing works
Understanding the pathogenesis of multiple system atrophy: state of the art and future perspectives
Compagnoni, G. M., & Fonzo, A. D. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0730-6 · Cited by 90 · see citing works
The Potential Role of Gut-Derived Inflammation in Multiple System Atrophy
Engen, P. A., Dodiya, H. B., Naqib, A. D., Forsyth, C. B., Green, S. J., Voigt, R. M., Kordower, J. H., Mutlu, E., Shannon, K. M., & Keshavarzian, A. (2017) · Journal of Parkinson s Disease · doi:10.3233/jpd-160991 · Cited by 84 · see citing works
Fluid biomarkers in multiple system atrophy: A review of the MSA Biomarker Initiative
Laurens, B., Constantinescu, R., Freeman, R. L., Gerhard, A., Jellinger, K. A., Jeromin, A., Krismer, F., Mollenhauer, B., Schlossmacher, M. G., Shaw, L. M. J., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.05.004 · Cited by 85 · see citing works
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An update on advances in magnetic resonance imaging of multiple system atrophy
Chelban, V., Bocchetta, M., Hassanein, S. M. A., Haridy, N. A., Houlden, H., & Rohrer, J. D. (2018) · Journal of Neurology · doi:10.1007/s00415-018-9121-3 · Cited by 84 · see citing works
Atypical parkinsonian syndromes: a general neurologist's perspective
Deutschländer, A., Ross, O. A., Dickson, D. W., & Wszołek, Z. K. (2017) · European Journal of Neurology · doi:10.1111/ene.13412 · Cited by 80 · see citing works
Default mode network links to visual hallucinations: A comparison between Parkinson's disease and multiple system atrophy
Franciotti, R., Pizzi, S. D., Perfetti, B., Tartaro, A., Bonanni, L., Thomas, A., Weis, L., Biundo, R., Antonini, A., & ONOFRJ, M. C. (2015) · Movement Disorders · doi:10.1002/mds.26285 · Cited by 79 · see citing works
Loss of substantia nigra hyperintensity on 7 Tesla MRI of Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy
Kim, J., Jeong, H.-J., Bae, Y. J., Park, S., Kim, E., Kang, S. Y., Oh, E., Kim, K. J., Jeon, B., Kim, S. E., et al. (2016) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2016.01.023 · Cited by 78 · see citing works
The Relevance of Iron in the Pathogenesis of Multiple System Atrophy: A Viewpoint
Kaindlstorfer, C., Jellinger, K. A., Eschlböck, S., Stefanova, N., Weiß, G., & Wenning, G. K. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-170601 · Cited by 71 · see citing works
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Metallothionein, Copper and Alpha-Synuclein in Alpha-Synucleinopathies
Okita, Y., Rcom-H'cheo-Gauthier, A. N., Goulding, M., Chung, R. S., Faller, P., & Pountney, D. L. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00114 · Cited by 71 · see citing works
Multiple system atrophy: pathogenic mechanisms and biomarkers
Jellinger, K. A., & Wenning, G. K. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1545-2 · Cited by 70 · see citing works
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High‐Contrast Imaging of α‐Synuclein Pathologies in Living Patients with Multiple System Atrophy
Matsuoka, K., Ono, M., Takado, Y., Hirata, K., Endo, H., Ohfusa, T., Kojima, T., Yamamoto, T., Onishi, T., Orihara, A., et al. (2022) · Movement Disorders · doi:10.1002/mds.29186 · Cited by 63 · see citing works
Mitochondrial Dysregulation and Impaired Autophagy in iPSC-Derived Dopaminergic Neurons of Multiple System Atrophy
Compagnoni, G. M., Kleiner, G., Samarani, M., Aureli, M., Faustini, G., Bellucci, A., Ronchi, D., Bordoni, A., Garbellini, M., Salani, S., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.09.007 · Cited by 62 · see citing works
Filamentous aggregations of phosphorylated α-synuclein in Schwann cells (Schwann cell cytoplasmic inclusions) in multiple system atrophy
Nakamura, K., Mori, F., Kon, T., Tanji, K., Miki, Y., Tomiyama, M., Kurotaki, H., Toyoshima, Y., Kakita, A., Takahashi, H., et al. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0208-0 · Cited by 60 · see citing works
Cerebellar resting-state functional connectivity in Parkinson's disease and multiple system atrophy: Characterization of abnormalities and potential for differential diagnosis at the single-patient level
Baggio, H. C., Abós, A., Segura, B., Campabadal, A., Uribe, C., Giraldo, D. M., Pérez‐Soriano, A., Muñoz, E., Compta, Y., Junqué, C., et al. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101720 · Cited by 60 · see citing works
Pathogenesis of Alzheimer's Disease: Role of Amyloid-beta and Hyperphosphorylated Tau Protein
Sajjad, R., Arif, R., Shah, A. A., Manzoor, I., & Mustafa, G. (2018) · Indian Journal of Pharmaceutical Sciences · doi:10.4172/pharmaceutical-sciences.1000397 · Cited by 57 · see citing works
Mechanisms of Neurodegeneration in Various Forms of Parkinsonism—Similarities and Differences
Koziorowski, D., Figura, M., Milanowski, Ł., Szlufik, S., Alster, P., Madetko‐Alster, N., & Friedman, A. (2021) · Cells · doi:10.3390/cells10030656 · Cited by 59 · see citing works
Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates
Mandel, R. J., Marmion, D. J., Kirik, D., Chu, Y., Heindel, C., McCown, T., Gray, S. J., & Kordower, J. H. (2017) · Acta Neuropathologica Communications · doi:10.1186/s40478-017-0451-7 · Cited by 56 · see citing works
MicroRNA-101 Modulates Autophagy and Oligodendroglial Alpha-Synuclein Accumulation in Multiple System Atrophy
Valera, E., Spencer, B., Mott, J., Trejo, M., Adame, A., Mante, M., Rockenstein, E., Troncoso, J. C., Beach, T. G., Masliah, E., et al. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00329 · Cited by 55 · see citing works
Review: Multiple system atrophy: emerging targets for interventional therapies
Stefanova, N., & Wenning, G. K. (2016) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12304 · Cited by 54 · see citing works
Neocortical Neuronal Loss in Patients with Multiple System Atrophy: A Stereological Study
Salvesen, L., Winge, K., Brudek, T., Agander, T. K., Løkkegaard, A., & Pakkenberg, B. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv228 · Cited by 53 · see citing works
Synucleinopathies: common features and hippocampal manifestations
Yang, W., & Yu, S. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2411-y · Cited by 49 · see citing works
Alterations of the Gut Microbiota in Multiple System Atrophy Patients
Wan, L., Zhou, X. M., Wang, C., Chen, Z., Peng, H., Hou, X., Peng, Y., Wang, P., Li, T., Yuan, H., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01102 · Cited by 49 · see citing works
Association of the COQ2 V393A variant with risk of multiple system atrophy in East Asians: a case–control study and meta-analysis of the literature
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Authors: Jellinger, K. A.
Affiliations: Institute of Clinical Neurobiology Vienna Austria
Corresponding author: Jellinger, Kurt A.
ORCID: Jellinger, Kurt A.
Venue: Movement Disorders
Publisher: Wiley
Published: 2014-10-09
Volume: 29
Issue: 14
Pages: 1720-1741
ISSN: 0885-3185 (ISSN-L)
1531-8257
DOI: 10.1002/mds.26052
OpenAlex: W1902295431
Cited by: 181
References: 288
Citations by year: 2026: 8 · 2025: 11 · 2024: 22 · 2023: 11 · 2022: 12 · 2021: 20 · 2020: 15 · 2019: 20 · 2018: 16 · 2017: 18 · 2016: 15 · 2015: 13
FWCI: 2.11
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Movement Disorders (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute
Topics: Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Neurology › Neurological diseases and metabolism
Keywords: multiple system atrophy, neuropathology, pathogenesis, glial cytoplasmic inclusions, alpha-synuclein, oligodendrocytes, autonomic failure, parkinsonism, cerebellar dysfunction, striatonigral degeneration, olivopontocerebellar atrophy, neuroinflammation, oxidative stress, mitochondrial dysfunction, prion-like spreading, neurodegeneration
MeSH terms: Animals, Humans, Nervous System Diseases, Neurons, Oligodendroglia, Shy-Drager Syndrome, Multiple System Atrophy, alpha-Synuclein

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Neuropathology of multiple system atrophy: New thoughts about pathogenesis

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