The DOI matches its Crossref record.
The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology
Abstract
In this study a semiquantitative mapping of oligodendroglial cytoplasmic inclusions (GCIs), a feature of oligodendroglial degeneration in multiple system atrophy (MSA), was undertaken by means of a sensitive silver technique in 14 brains and 11 spinal cords of patients with various combinations of striatonigral degeneration, olivopontocerebellar atrophy and autonomic failure. The results show a system-bound extensive degeneration of interfascicular, perineuronal and perivascular oligodendrocytes. Oligodendroglial cytoplasmic inclusion-rich structures occur in the supra-segmental motor systems (primary motor and higher motor areas of cerebral cortex, 'pyramidal', 'extrapyramidal' and cortico-cerebellar systems), in the supraspinal autonomic systems and in their targets. In contrast, the visual and auditory pathways, olfactory structures, somatosensory systems, association and limbic cortical areas and subcortical limbic structures contain no or only a few GCIs. Comparison of the severity of oligodendroglial degeneration (GCI-density) with that of the neuronal alterations (neuronal cytoplasmic and nuclear inclusions, degenerated neuronal processes and loss of nerve cells) indicates a striking preponderance of oligodendroglial degeneration and that degeneration neither of axons, nor of neuronal cell bodies is a prerequisite of the development of GCIs. It also suggests that inclusion-bearing oligodendroglial degeneration may cause or contribute to the manifestation of clinical symptomatology in structures with GCI accumulation but without convincing neuronal alterations, i.e. cerebral motor cortical areas and reticular formation of the lower brainstem, both previously thought to be spared in MSA.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Moreover, the morphology of the GCIs (Fig. 3f, red channel) mimics the typical conical half-moon shape inclusions seen in the human disease [43].”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [43]
In the citing paper
“These inclusions were later described to be composed mainly of α-syn [43].”
From Novel oligodendroglial alpha synuclein viral vector models of multiple system atrophy: studies in rodents and nonhuman primates (2017) · cites this paper as [43]
Citations
Cited by
Sorted by citations
Bendor, J. T., Logan, T. P., & Edwards, R. H. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.004 · Cited by 825
Calabresi, P., Mechelli, A., Natale, G., Volpicelli‐Daley, L. A., Lazzaro, G. D., & Ghiglieri, V. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05672-9 · Cited by 930
“Neuronal cytoplasmic inclusions are also found, but with distinct distributions as compared to LB, being observed in the putamen, pontine nuclei, and inferior olivary nuclei [12].”
BackgroundMultiple system atrophy: A review of 203 pathologically proven cases
Wenning, G. K., Tison, F., Ben‐Shlomo, Y., Daniel, S. E., & Quinn, N. P. (1997) · Movement Disorders · doi:10.1002/mds.870120203 · Cited by 802
Progression and prognosis in multiple system atrophy
Watanabe, H., Saito, Y., Terao, S.-I., Ando, T., Kachi, T., Mukai, E., Aiba, I., Abe, Y., Tamakoshi, A., Doyu, M., et al. (2002) · Brain · doi:10.1093/brain/awf117 · Cited by 596
The cholinergic system and Parkinson disease
Bohnen, N. I., & Albin, R. L. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.048 · Cited by 607
“The pathology of MSA is distinct from PD and consists of neuronal loss in the substantia nigra, striatum, cerebellum, brainstem and spinal cord with argyrophilic and glial inclusions [100].”
BackgroundOzawa, T. (2004) · Brain · doi:10.1093/brain/awh303 · Cited by 515
“Papp and Lantos observed no direct correlation between the density of GCIs and the severity of neuronal loss in most anatomical sites, and they suggested that GCIs generally appear before neuronal cell loss (Papp and Lantos, 1994).”
BackgroundWenning, G. K., Colosimo, C., Geser, F., & Poewe, W. H. (2004) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00662-8 · Cited by 470
Neuropathology underlying clinical variability in patients with synucleinopathies
Halliday, G. M., Holton, J. L., Révész, T., & Dickson, D. W. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0852-9 · Cited by 447
“In early studies, no relationship was found between the density of GCIs and the severity of neuronal loss [134].”
BackgroundDifferential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis
Tang, C. C., Poston, K. L., Eckert, T., Feigin, A., Frucht, S. J., Gudesblatt, M., DHAWAN, V. M., LESSER, M. L., Vonsattel, J., Fahn, S., et al. (2010) · The Lancet Neurology · doi:10.1016/s1474-4422(10)70002-8 · Cited by 352
Neuropathology and molecular diagnosis of Synucleinopathies
Koga, S., Sekiya, H., Kondru, N., Ross, O. A., & Dickson, D. W. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00501-z · Cited by 347
“about whether MSA was a single disease, the discovery of argyrophilic glial cytoplasmic inclusions (GCI), also known as Papp-Lantos bodies [15, 16], in SND and OPCA provided strong evidence that they were part of a”
BackgroundYazawa, I., Giasson, B. I., Sasaki, R., Zhang, B., Joyce, S., Uryu, K., Trojanowski, J. Q., & Lee, V. M.-Y. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.032 · Cited by 301
The neuropathology, pathophysiology and genetics of multiple system atrophy
Ahmed, Z., Asi, Y. T., Sailer, A., Lees, A. J., Houlden, H., Révész, T., & Holton, J. L. (2011) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2011.01234.x · Cited by 275
Filamentous nerve cell inclusions in neurodegenerative diseases
Goedert, M., Spillantini, M. G., & Davies, S. W. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80090-1 · Cited by 261
Wenning, G. K. (2000) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.68.4.434 · Cited by 261
Stanković, I., Krismer, F., Ješić, A., Antonini, A., Benke, T., Brown, R. G., Burn, D. J., Holton, J. L., Kaufmann, H., Kostić, V., et al. (2014) · Movement Disorders · doi:10.1002/mds.25880 · Cited by 248
“Substantia nigra and putamen are mostly affected, and caudate nucleus and globus pallidus are also involved but to a lesser degree.(1,59) Cerebellar degeneration in MSA comprises severe loss of Purkinje cells and to lesser extent neurons in the dentate nucleus.”
BackgroundAntonini, A. (1997) · Brain · doi:10.1093/brain/120.12.2187 · Cited by 241
“…studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson’s disease Angelo Antonini,1 Klaus L. Leenders,2 Peter Vontobel,1 R. Paul Maguire,1 John Missimer,1 Maria Psylla1 and Ilonka Gu¨nther1 1PET Department, Paul Scherrer Institute,…”
BackgroundRockenstein, E. M., Nuber, S., Overk, C., Ubhi, K. K., Mante, M., Patrick, C., Adame, A., Trejo, M., Gerez, J., Picotti, P., et al. (2014) · Brain · doi:10.1093/brain/awu057 · Cited by 242
RetractedThe aetiology of sporadic adult‐onset ataxia
Abele, M., Bürk, K., Schöls, L. J., Schwartz, S., Besenthal, I., DICHGANS, J., Zühlke, C., Rieß, O., & Klockgether, T. (2002) · Brain · doi:10.1093/brain/awf107 · Cited by 233
“The ultrastructural hallmark of MSA is the presence of oligodendroglial cytoplasmic inclusions (Papp and Lantos, 1994).”
Braak, H., & Braak, E. (1998) · Journal of Neural Transmission · doi:10.1007/s007020050096 · Cited by 225
“…atrophy) usually exhibit a marked development of abnormal tau protein in both oligodendroglial cells and astrocytes (Papp et al., 1989; Horoupian, 1990; Nakazato et al., 1990; Yamada and McGeer, 1990; Yamada et al., 1992; Probst et al., 1993; Papp and Lantos, 1994; Iwatsubo et al., 1994).”
BackgroundWhat Is the Accuracy of the Clinical Diagnosis of Multiple System Atrophy?
Litvan, I. (1997) · Archives of Neurology · doi:10.1001/archneur.1997.00550200007003 · Cited by 211
Multiple System Atrophy: A Sporadic Synucleinopathy
Dickson, D. W., Lin, W.-L., Liu, W.-K., & Yen, S.-H. C. (1999) · Brain Pathology · doi:10.1111/j.1750-3639.1999.tb00553.x · Cited by 212
“The neuroanatomical distribution of the GCI follows the distribution of neurodegeneration (1, 21, 36, 49, 59).”
BackgroundMultiple System Atrophy: An Oligodendroglioneural Synucleinopathy
Jellinger, K. A. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170397 · Cited by 218
“formation [160, 283], while the branchimotor neu-”
Tong, J., Wong, H., Guttman, M., Ang, L. C., Forno, L. S., Shimadzu, M., Rajput, A. H., Muenter, M. D., Kish, S. J., Hornykiewicz, O., et al. (2009) · Brain · doi:10.1093/brain/awp282 · Cited by 210
Glia and alpha-synuclein in neurodegeneration: A complex interaction
Brück, D., Wenning, G. K., Stefanova, N., & Fellner, L. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.03.003 · Cited by 213
“GCIs have an extensive distribution throughout the CNS including areas such as pons, medulla, putamen, SN, cerebellum and preganglionic autonomic brain structures (Papp and Lantos, 1994; Nishie et al., 2004; Beyer and Ariza, 2007; Jellinger and Lantos, 2010).”
Neuropathology of autonomic dysfunction in synucleinopathies
Coon, E. A., Cutsforth‐Gregory, J. K., & Benarroch, E. E. (2018) · Movement Disorders · doi:10.1002/mds.27186 · Cited by 210
“Oligodendroglial cytoplasmic inclusions are the hallmark pathological feature of multiple system atrophy (MSA).(4,5) Pure autonomic failure (PAF) is characterized by predominantly peripheral accumulation of a-synuclein as neuronal cytoplasmic inclusions.”
BackgroundAlpha-synuclein and transgenic mouse models
Fernagut, P., & Chesselet, M. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.07.001 · Cited by 210
“Glial cytoplasmic inclusions in MSA are distributed in the cortico-striato-cortical loops, while neuronal inclusions are present mostly in the pontine nuclei (Papp and Lantos, 1994).”
BackgroundCognitive impairments in multiple system atrophy
Kawai, Y., Suenaga, M., Takeda, A., Ito, M., Watanabe, H., Tanaka, F., Kato, K., Fukatsu, H., Naganawa, S., Kato, T., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000310413.04462.6a · Cited by 187
Neuropathology of multiple system atrophy: New thoughts about pathogenesis
Jellinger, K. A. (2014) · Movement Disorders · doi:10.1002/mds.26052 · Cited by 181
“Of note, some regions such as motor cortex, although histologically unremarkable, have a high density of GCIs, indicating that neurodegeneration is not a prerequisite for developing GCIs.(80) Furthermore, the SN, despite severe neuronal loss, usually shows a relatively low density of GCIs, and the association between…”
BackgroundInfluentialBooij, J., Tissingh, G., Winogrodzka, A., & van Royen, E. A. (1999) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s002590050374 · Cited by 174
“Multiple system atrophy is neuropathologically characterised by neuronal degeneration and gliosis in the caudate and putamen, globus pallidus, brain stem, cerebellum and spinal cord [73, 74].”
BackgroundMicroglial Activation Parallels System Degeneration in Multiple System Atrophy
Ishizawa, K., Komori, T., Sasaki, S., Arai, N., Mizutani, T., & Hirose, T. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.1.43 · Cited by 172
“It was suggested that GCI formation may be an early event of the disease and that GCIs tend to be less prominent in severely affected areas or in cases of long-standing duration (25, 41, 42).”
BackgroundResultInfluentialBak, T. H., Crawford, L., Hearn, V., Mathuranath, P. S., & Hodges, J. R. (2005) · Neurocase · doi:10.1080/13554790590962997 · Cited by 173
“Cortical pathology is not considered to be a common feature (Papp and Lantos, 1994).”
BackgroundVoxel‐based morphometry detects cortical atrophy in the Parkinson variant of multiple system atrophy
Brenneis, C., Seppi, K., Schocke, M. F., Müller, J., Luginger, E., Bösch, S., Löscher, W. N., Büchel, C., Poewe, W., & Wenning, G. K. (2003) · Movement Disorders · doi:10.1002/mds.10502 · Cited by 167
Glial dysfunction in the pathogenesis of α-synucleinopathies: emerging concepts
Fellner, L., Jellinger, K. A., Wenning, G. K., & Stefanova, N. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0833-z · Cited by 162
“Their distribution in the CNS is extensive: GCIs occur in the pons, medulla, putamen, SN, cerebellum and preganglionic autonomic structures [17, 107, 158, 169].”
BackgroundOligodendroglia and Myelin in Neurodegenerative Diseases: More Than Just Bystanders?
Ettle, B., Schlachetzki, J. C. M., & Winkler, J. (2016) · Molecular Neurobiology · doi:10.1007/s12035-015-9205-3 · Cited by 160
“Moreover, GCI load increases with disease progression [104, 122, 125].”
BackgroundThe elimination of accumulated and aggregated proteins: A role for aggrephagy in neurodegeneration
Yamamoto, A., & Simonsen, A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.08.015 · Cited by 155
Duda, J. E., Giasson, B. I., Gur, T., Montine, T. J., Robertson, D., Biaggioni, I., Hurtig, H. I., Stern, M. B., Gollomp, S. M., Grossman, M., et al. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.9.830 · Cited by 150
“Significantly, one area that appears to distinguish a-syn immunolabeled from silverstained GCIs in the MSA brain is the hippocampal formation, since it was reported that this region was ‘‘free or nearly free’’ of silver-positive GCIs (42), while a-syn specific antibodies detected a high to moderate GCI density in the…”
BackgroundOverlap between neurodegenerative disorders
Armstrong, R. A., Lantos, P. L., & Cairns, N. J. (2005) · Neuropathology · doi:10.1111/j.1440-1789.2005.00605.x · Cited by 146
Self-citationInvolvement of vagal autonomic nuclei in multiple system atrophy and Lewy body disease
Benarroch, E. E., Schmeichel, A. M., Sandroni, P., Low, P. A., & Parisi, J. E. (2006) · Neurology · doi:10.1212/01.wnl.0000196638.98781.bb · Cited by 146
Cellular pathology in multiple system atrophy
Wakabayashi, K., & Takahashi, H. (2006) · Neuropathology · doi:10.1111/j.1440-1789.2006.00713.x · Cited by 147
Measuring brain stem and cerebellar damage in parkinsonian syndromes using diffusion tensor MRI
Blain, C. R. V., Barker, G. J., Jarosz, J., Coyle, N. A., Landau, S., Brown, R. G., Chaudhuri, К. R., Simmons, A., Jones, D. K., Williams, S., et al. (2006) · Neurology · doi:10.1212/01.wnl.0000249307.59950.f8 · Cited by 146
Papp–Lantos inclusions and the pathogenesis of multiple system atrophy: an update
Jellinger, K. A., & Lantos, P. L. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0672-3 · Cited by 152
“They are widely distributed in the cerebral white matter and occur in an anatomically selective manner, affecting the pons, medulla, putamen, substantia nigra pars compacta (SNPC), cerebellum, and preganglionic autonomic structures [73, 78, 83, 97].”
BackgroundSelf-citationCellular pathology of multiple system atrophy: a review.
Lantos, P. L., & Papp, M. I. (1994) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.2.129 · Cited by 143
Self-citationSpinocerebellar ataxia type 1 with multiple system degeneration and glial cytoplasmic inclusions
Gilman, S., Sima, A. A. F., Junck, L., Kluin, K., Koeppe, R., Lohman, M., & Little, R. J. A. (1996) · Annals of Neurology · doi:10.1002/ana.410390214 · Cited by 157
Araki, K., Yagi, N., Aoyama, K., Choong, C., Hayakawa, H., Fujimura, H., Nagai, Y., Goto, Y., & Mochizuki, H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1906124116 · Cited by 137
“Lewy bodies (LBs) of Parkinson’s disease (PD) (2, 3) or dementia with LBs (2, 3) and glial cytoplasmic inclusions (GCIs) of multiple system atrophy (4) are mainly composed of α-syn.”
BackgroundRobitaille, Y., Schut, L., & Kish, S. (2004) · Acta Neuropathologica · doi:10.1007/bf00318569 · Cited by 102
“The remaining formalin-fixed tissues were sampled according to the following protocol: (1) frontal lobe: two sections of the convexity, one section of orbitofrontal gyms with striatal (caudate and putamen) head; (2) temporal lobe: two sections through the anterior hippocampus and entorhinal gyms; (3) parietal lobe: on…”
MethodHorimoto, Y., Aiba, I., Yasuda, T., et al. (2002) · Journal of Neurology · doi:10.1007/s00415-002-0734-0 · Cited by 133
Immunotherapy for neurodegenerative diseases: Focus on α-synucleinopathies
Valera, E., & Masliah, E. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.01.013 · Cited by 132
“…neurodegenerative disorders are also associated with intracellular accumulation of α-syn, such as Multiple system atrophy (MSA) (Dickson et al., 1999; Papp & Lantos, 1994; Spillantini, 1999; Wakabayashi et al., 1998), AD (Hamilton, 2000; Iwai, 2000), and Gaucher disease (Mazzulli et al., 2011).”
BackgroundNot paralysis, but dystonia causes stridor in multiple system atrophy
Merlo, I. M., Occhini, A., Pacchetti, C., & Alfonsi, E. (2002) · Neurology · doi:10.1212/wnl.58.4.649 · Cited by 130
Recent advances in neuropathology, biomarkers and therapeutic approach of multiple system atrophy
Koga, S., & Dickson, D. W. (2017) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2017-315813 · Cited by 130
Paviour, D. C., Thornton, J. S., Lees, A. J., & Jäger, H. R. (2006) · Movement Disorders · doi:10.1002/mds.21204 · Cited by 129
Multiple system atrophy: cellular and molecular pathology
Burn, D. J., & Jaros, E. (2001) · Molecular Pathology · doi:10.1136/mp.54.6.419 · Cited by 126
Soliveri, P. (2000) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.69.3.313 · Cited by 123
Myelin Degeneration in Multiple System Atrophy Detected by Unique Antibodies
Matsuo, A., Akiguchi, I., Lee, G. C., McGeer, E. G., McGeer, P. L., & Kimura, J. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65617-9 · Cited by 125
“Motor cortex has been reported to be the most GCI-rich cerebral cortical area.(2,7,18,19) Ubiquinated neuronal inclusions have been found in the subiculum and CA1 of Ammon’s horn.”
BackgroundNishie, M., Mori, F., Yoshimoto, M., Takahashi, H., & Wakabayashi, K. (2004) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2004.00564.x · Cited by 123
Scherfler, C., Seppi, K., Donnemiller, E., Goebel, G., Brenneis, C., Virgolini, I. J., Wenning, G. K., & Poewe, W. H. (2005) · Brain · doi:10.1093/brain/awh485 · Cited by 120
“This would be in line with reported neuropathological findings in MSA-P patients, showing neuronal loss in brainstem areas containing DAT, SERT or NAT bearing neurons as the substantia nigra, the locus coeruleus and the raphe nuclei (Wenning et al., 1997, 2004; Papp and Lantos, 1994).”
ResultInoue, M., Yagishita, S., Ryo, M., Hasegawa, K., Amano, N., & Matsushita, M. (1997) · Acta Neuropathologica · doi:10.1007/s004010050655 · Cited by 117
“The putaminal lesions have been reported to be more severe in the dorsolateral than in frontomedial regions [14, 23 ] and to have a positive association between their neuronal loss and incidence of GCIs [19].”
BackgroundResultInfluentialKikuchi, A., Takeda, A., Okamura, N., Tashiro, M., Hasegawa, T., Furumoto, S., Kobayashi, M., Sugeno, N., Baba, T., Miki, Y., et al. (2010) · Brain · doi:10.1093/brain/awq091 · Cited by 113
“…anterior cingulate cortex, globus pallidus, primary motor cortex and substantia nigra, in which glial cytoplasmic inclusions were densely distributed (Papp and Lantos, 1994; Inoue et al., 1997; Wakabayashi and Takahashi, 2006) and large increases of -synuclein content were found (Tong et al.,…”
BackgroundMinnerop, M., Specht, K., Ruhlmann, J., Schimke, N., Abele, M., Weyer, A., Wüllner, U., & Klockgether, T. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.04.028 · Cited by 114
Olivopontocerebellar pathology in multiple system atrophy
Wenning, G. K., Tison, F., Elliott, L., Quinn, N. P., & Daniel, S. E. (1996) · Movement Disorders · doi:10.1002/mds.870110207 · Cited by 106
Insulin resistance and exendin-4 treatment for multiple system atrophy
Bassil, F., Canron, M., Vital, A., Bézard, E., Li, Y., Greig, N. H., Gulyani, S., Kapogiannis, D., Fernagut, P., & Meissner, W. G. (2017) · Brain · doi:10.1093/brain/awx044 · Cited by 108
Visuospatial functions in atypical parkinsonian syndromes
Bak, T. H. (2006) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.068239 · Cited by 106
Electrophysiologic patterns of oral-pharyngeal swallowing in parkinsonian syndromes
Alfonsi, E., Versino, M., Merlo, I. M., Pacchetti, C., Martignoni, E., Bertino, G., Moglia, A., Tassorelli, C., & Nappi, G. (2007) · Neurology · doi:10.1212/01.wnl.0000254478.46278.67 · Cited by 107
Irving, E. A., Yatsushiro, K., McCulloch, J., & Dewar, D. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199706000-00003 · Cited by 103
Holmberg, B., Johnels, B., Blennow, K., & Rosengren, L. (2002) · Movement Disorders · doi:10.1002/mds.10321 · Cited by 106
Cantone, M., Pino, G. D., Capone, F., Piombo, M., Chiarello, D., Cheeran, B., Pennisi, G., & Lazzaro, V. D. (2014) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.04.010 · Cited by 102
Araki, K., Yagi, N., Ikemoto, Y., Yagi, H., Choong, C., Hayakawa, H., Beck, G., Sumi, H., Fujimura, H., Moriwaki, T., et al. (2015) · Scientific Reports · doi:10.1038/srep17625 · Cited by 101
Differential diagnosis of parkinsonism with [18F]fluorodeoxyglucose and PET
Antonini, A., Kazumata, K., Feigin, A., Mandel, F. S., DHAWAN, V. M., Margouleff, C., & Eidelberg, D. (1998) · Movement Disorders · doi:10.1002/mds.870130212 · Cited by 98
Wenning, G. K., & Braune, S. (2001) · CNS Drugs · doi:10.2165/00023210-200115110-00003 · Cited by 102
Diagnóstico diferencial das demências
Neto, J. G., Tamelini, M. G., & Forlenza, O. V. (2005) · Archives of Clinical Psychiatry (São Paulo) · doi:10.1590/s0101-60832005000300004 · Cited by 112
Dementia with Grains (Argyrophilic Grain Disease)
Jellinger, K. A. (1998) · Brain Pathology · doi:10.1111/j.1750-3639.1998.tb00161.x · Cited by 98
“ably tau and aB crystallin positive and neurofilamentantibody negative (11, 37).”
BackgroundInvolvement of precerebellar nuclei in multiple system atrophy
Braak, H., Rüb, U., & Tredici, K. D. (2003) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.2003.00432.x · Cited by 93
Recent developments in multiple system atrophy
Wenning, G. K., & Stefanova, N. (2009) · Journal of Neurology · doi:10.1007/s00415-009-5173-8 · Cited by 92
Chrysostome, V., Tison, F., Yekhlef, F., Sourgen, C., Baldi, I., & Dartigues, J. (2004) · Neuroepidemiology · doi:10.1159/000078506 · Cited by 92
Animal models of multiple system atrophy
Stefanova, N., & Wenning, G. K. (2015) · Clinical Autonomic Research · doi:10.1007/s10286-014-0266-6 · Cited by 94
Ahmed, Z., Asi, Y. T., Lees, A. J., Révész, T., & Holton, J. L. (2012) · Brain Pathology · doi:10.1111/j.1750-3639.2012.00637.x · Cited by 96
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 93
Lyoo, C. H., Jeong, Y., Ryu, Y. H., Lee, S., Song, T., Lee, J. H., Rinne, J. O., & Lee, M. S. (2008) · Brain · doi:10.1093/brain/awm328 · Cited by 92
“Glial cytoplasmic inclusions (GCIs) were found in the frontal lobe, particularly in the supplementary motor, cingulate, primary motor and premotor cortices (Papp and Lantos, 1994).”
BackgroundResultInfluentialPatterns of abnormal motor cortex excitability in atypical parkinsonian syndromes
Kühn, A. A., Grosse, P., Holtz, K., Brown, P., Meyer, B.-U., & Kupsch, A. R. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.03.020 · Cited by 92
SLEEP AND DEGENERATIVE NEUROLOGIC DISORDERS
Chokroverty, S. (1996) · Neurologic Clinics · doi:10.1016/s0733-8619(05)70286-3 · Cited by 87
The morbid anatomy of dementia in Parkinson’s disease
Kalaitzakis, M. E., & Pearce, R. K. B. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0597-x · Cited by 90
“bodies in neurons and/or glial cells [46, 127] with the term encompassing diverse, but clinically overlapping entities, such as multiple system atrophy, PD, dementia with Lewy bodies (DLB), the LB variant of Alzheimer’s disease (LBVAD) and neurodegeneration with brain iron accumulation type 1 (NBIA I) [9, 13, 38, 45,…”
BackgroundStacpoole, S., Spitzer, S. O., Bilican, B., Compston, A., Káradóttir, R. T., Chandran, S., & Franklin, R. J. M. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.09.006 · Cited by 91
Meissner, W. G., Traon, A. P., Foubert‐Samier, A., et al. (2020) · Movement Disorders · doi:10.1002/mds.28218 · Cited by 88
Abnormalities of the nucleus and nuclear inclusions in neurodegenerative disease: a work in progress
Woulfe, J. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2006.00819.x · Cited by 89
Multiple system atrophy with remarkable frontal lobe atrophy
Konagaya, M., Sakai, M., Matsuoka, Y., Konagaya, Y., & Hashizume, Y. (1999) · Acta Neuropathologica · doi:10.1007/s004010051008 · Cited by 88
“In MSA, involvement of the cerebral hemisphere, which is considered to be most resistant reticular formation [2, 10 ], has been reported in only a few cases [5, 16].”
Backgroundα-Synuclein impairs oligodendrocyte progenitor maturation in multiple system atrophy
May, V. E. L., Ettle, B., Poehler, A.-M., Nuber, S., Ubhi, K. K., Rockenstein, E. M., Winner, B., Wegner, M., Masliah, E., & Winkler, J. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.02.028 · Cited by 85
“Additionally, post mortem studies indicate a correlation of GCI load with neuronal degeneration (Ozawa, et al., 2004, Papp and Lantos, 1994) for striatonigral, Neurobiol Aging.”
BackgroundStemberger, S., Poewe, W., Wenning, G. K., & Stefanova, N. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.05.008 · Cited by 83
Dying-back oligodendrogliopathy: A late sequel of myelin-associated glycoprotein deficiency
Lassmann, H., Bartsch, U., Montag, D., & Schachner, M. (1997) · Glia · doi:10.1002/(sici)1098-1136(199702)19:2 · Cited by 87
Hanna, P. A., Jankovic, J. J., & Kirkpatrick, J. B. (1999) · Archives of Neurology · doi:10.1001/archneur.56.1.90 · Cited by 82
Wakabayashi, K., Ikeuchi, T., Ishikawa, A., & Takahashi, H. (1998) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(98)00018-5 · Cited by 81
Benarroch, E. E. (2009) · Neurology · doi:10.1212/wnl.0b013e3181a6b123 · Cited by 81
Davies, S. W., Turmaine, M., Cozens, B. A., Raza, A. S., Mahal, A., Mangiarini, L., & Bates, G. P. (1999) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1999.0448 · Cited by 81
“…not to our knowledge been described in postmortem human HD, DRPLA, SBMA or SCA brain, although it is of interest that inclusions composed of a-synuclein have been reported in nuclei of oligodendrocytes in post-mortem brain in multiple system atrophy (Papp & Lantos 1994; Spillantini et al. 1998).”
Olfactory dysfunction in cerebellar ataxia and multiple system atrophy
Abele, M., Riet, A., Hummel, T. R., Klockgether, T., & W�llner, U. (2003) · Journal of Neurology · doi:10.1007/s00415-003-0248-4 · Cited by 81
Characteristics of the Dysarthria of Multiple System Atrophy
Kluin, K. J., Gilman, S., Lohman, M., & Junck, L. (1996) · Archives of Neurology · doi:10.1001/archneur.1996.00550060089021 · Cited by 80
Shiga, K., Yamada, K., Yoshikawa, K., Mizuno, T., Nishimura, T., & Nakagawa, M. (2005) · Journal of Neurology · doi:10.1007/s00415-005-0708-0 · Cited by 79
“The pallor of myelin, gliosis, and GCIs are also observed in internal capsule [12], possibly disrupting tissue integrity in that area.”
BackgroundPiao, Y.-S., Hayashi, S., Hasegawa, M., Wakabayashi, K., Yamada, M., Yoshimoto, M., Ishikawa, A., Iwatsubo, T., & Takahashi, H. (2001) · Acta Neuropathologica · doi:10.1007/s004010000292 · Cited by 78
“GCIs are present in oligodendroglial cells and widely distributed in the brains of affected patients [ 32 ].”
Ishizawa, K., Komori, T., Arai, N., Mizutani, T., & Hirose, T. (2008) · Neuropathology · doi:10.1111/j.1440-1789.2007.00855.x · Cited by 74
“The exact effect of GCIs or microglia on white matter and gray matter still remains to be understood in MSA.”
BackgroundInfluentialA novel grading scale for striatonigral degeneration (multiple system atrophy)
Wenning, G. K., Seppi, K., Tison, F., & Jellinger, K. A. (2002) · Journal of Neural Transmission · doi:10.1007/s007020200025 · Cited by 76
Tsuchiya, K., Ozawa, E., Haga, C., WATABIKI, S., Ikeda, M., Sano, M., Ooe, K., Taki, K., & Ikeda, K. (2000) · Acta Neuropathologica · doi:10.1007/s004010051173 · Cited by 73
Monza, D., Soliveri, P., Radice, D., Fetoni, V., Testa, D., Caffarra, P., CARACENI, T., & Girotti, F. (1998) · Archives of Neurology · doi:10.1001/archneur.55.3.372 · Cited by 72
“Direct cortical involvement has also been found in MSA: the premotor areas show neural and oligodendroglial, basophilic, argyrophil, cytoplasmic inclusions that are relatively specific for this disease and point to a cortical origin of the motor disorganization in MSA.(49)”
BackgroundInfluential
Metadata
- Authors
- Papp, M. I., & Lantos, P. L.
- Affiliations
- Semmelweis University (HU)
- Corresponding author
- Papp, M. I.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 1994
- Volume
- 117
- Issue
- 2
- Pages
- 235-243
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2148569529
- Cited by
- 389
- References
- 0
- Citations by year
- 2026: 8 · 2025: 12 · 2024: 5 · 2023: 7 · 2022: 10 · 2021: 16 · 2020: 19 · 2019: 10 · 2018: 10 · 2017: 15 · 2016: 4 · 2015: 12 · 2014: 20 · 2013: 12 · 2012: 10
- FWCI
- 8.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Clinical 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, oligodendrocyte degeneration, striatonigral degeneration, olivopontocerebellar atrophy, autonomic failure, motor cortex, reticular formation, brainstem, spinal cord, symptomatology, silver staining
- MeSH terms
- Aged, Atrophy, Autonomic Nervous System Diseases, Brain Diseases, Inclusion Bodies, Corpus Striatum, Female, Humans, Male, Middle Aged, Oligodendroglia, Olivopontocerebellar Atrophies, Substantia Nigra
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
