Translational therapies for multiple system atrophy: Bottlenecks and future directions
Open accessAbstract
Over the last decade a prominent amount of studies in preclinical transgenic models of multiple system atrophy (MSA) has been performed. These studies have helped understand mechanisms downstream to the α-synuclein oligodendroglial accumulation relevant to human MSA. However, the successful translation of the preclinical outcomes into a clinical trial has failed. Looking back, we can now identify possible confounders for the failure. Biomarkers of disease progression are mostly missing. Early diagnosis and initiation of therapeutic clinical trials is limited. The need of both proof-of-concept as well as clinically relevant preclinical study designs with clinically relevant timing and preclinical readouts is identified as a must in our translational efforts for MSA to date. Finally, improved clinical study designs with improved enrollment criteria, and measurement outcomes are warranted on the way to finding the successful therapeutic approach for MSA. This review provides an overview of experimental studies and clinical trials for MSA and the lessons learned over the last decade towards the identification of the cure for MSA.
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A phase II double-blind, placebo-controlled study on MSA patients found no difference in progression rates with fluoxetine.
“However, a phase II double-blind, placebo-controlled study on MSA patients found no difference in progression rates (NCT01146548).503”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [503]
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1 retracted
Masliah, E., Rockenstein, E. M., Mante, M., Crews, L. A., Spencer, B. J., Adame, A., Patrick, C., Trejo, M., Ubhi, K. K., Rohn, T. T., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019338 · Cited by 422 · see citing works
RetractedSecond consensus statement on the diagnosis of multiple system atrophy
Gilman, S., Wenning, G. K., Low, P. A., Brooks, D. J., Mathias, C. J., Trojanowski, J. Q., Wood, N. W., Colosimo, C., Dürr, A., Fowler, C. J., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000324625.00404.15 · Cited by 3,140 · see citing works
α-Synuclein strains cause distinct synucleinopathies after local and systemic administration
Peelaerts, W., Bousset, L., Van der Perren, A., Moskalyuk, A., Pulizzi, R., Giugliano, M., Van den Haute, C., Melki, R., & Baekelandt, V. (2015) · Nature · doi:10.1038/nature14547 · Cited by 1,130 · see citing works
Spillantini, M. G., Crowther, R. A., Jakes, R., Cairns, N. J., Lantos, P. L., & Goedert, M. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00504-7 · Cited by 1,026 · see citing works
Papp, M. I., Kahn, J. E., & Lantos, P. L. (1989) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(89)90219-0 · Cited by 991 · see citing works
Fanciulli, A., & Wenning, G. K. (2015) · New England Journal of Medicine · doi:10.1056/nejmra1311488 · Cited by 827 · see citing works
Toll‐like receptor 4 is required for α‐synuclein dependent activation of microglia and astroglia
Fellner, L., Irschick, R., Schanda, K., Reindl, M., Klimaschewski, L., Poewe, W., Wenning, G. K., & Stefanova, N. (2013) · Glia · doi:10.1002/glia.22437 · Cited by 697 · see citing works
Self-citationEvidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism
Prusiner, S. B., Woerman, A. L., Mordes, D. A., Watts, J. C., Rampersaud, R., Berry, D. B., Patel, S. S., Oehler, A., Lowe, J. K., Kravitz, S. N., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514475112 · Cited by 679 · see citing works
Wagner, J., Ryazanov, S., Leonov, A., Levin, J., Shi, S., Schmidt, F., Prix, C., Pan-Montojo, F. J., Bertsch, U., Mitteregger-Kretzschmar, G., et al. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1114-9 · Cited by 457 · see citing works
Transmission of multiple system atrophy prions to transgenic mice
Watts, J. C., Giles, K., Oehler, A., Middleton, L. T., Dexter, D. T., Gentleman, S., DeArmond, S. J., & Prusiner, S. B. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318268110 · Cited by 433 · see citing works
Mutations in COQ2 in Familial and Sporadic Multiple-System Atrophy
The Multiple-System Atrophy Research Collaboration (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1212115 · Cited by 342 · see citing works
Multiple system atrophy: A primary oligodendrogliopathy
Wenning, G. K., Stefanova, N., Jellinger, K. A., Poewe, W. H., & Schlossmacher, M. G. (2008) · Annals of Neurology · doi:10.1002/ana.21465 · Cited by 320 · see citing works
Self-citationYazawa, 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 · see citing works
Alpha‐synuclein transfers from neurons to oligodendrocytes
Reyes, J. F., Rey, N. L., Bousset, L., Melki, R., Brundin, P., & Angot, É. (2013) · Glia · doi:10.1002/glia.22611 · Cited by 278 · see citing works
Toll-Like Receptor 4 Promotes α-Synuclein Clearance and Survival of Nigral Dopaminergic Neurons
Stefanova, N., Fellner, L., Reindl, M., Masliah, E., Poewe, W., & Wenning, G. K. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.04.013 · Cited by 272 · see citing works
Self-citationShults, C. W., Rockenstein, E., Crews, L., Adame, A., Mante, M., Larrea, G., Hashimoto, M., Song, D., Iwatsubo, T., Tsuboi, K., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3527-05.2005 · Cited by 254 · see citing works
Trial watch: FDA-approved Toll-like receptor agonists for cancer therapy
Vacchelli, E., Galluzzi, L., Eggermont, A. M. M., Fridman, W. H., Galon, J., Sautès‐Fridman, C., Tartour, É., Zitvogel, L., & Kroemer, G. (2012) · OncoImmunology · doi:10.4161/onci.20931 · Cited by 242 · see citing works
Expanding the spectrum of neuronal pathology in multiple system atrophy
Cykowski, M. D., Coon, E. A., Powell, S. Z., Jenkins, S. M., Benarroch, E. E., Low, P. A., Schmeichel, A. M., & Parisi, J. E. (2015) · Brain · doi:10.1093/brain/awv114 · Cited by 241 · see citing works
A randomized trial of mesenchymal stem cells in multiple system atrophy
Lee, P. H., Lee, J. E., Kim, H., Song, S., Lee, H. S., Nam, H. S., Cheong, J., Jeong, Y., Park, H., Kim, D. J., et al. (2012) · Annals of Neurology · doi:10.1002/ana.23612 · Cited by 233 · see citing works
Lee, P. H., Kim, J., Bang, O., Ahn, Y., Joo, I., & Huh, K. H. (2007) · Clinical Pharmacology & Therapeutics · doi:10.1038/sj.clpt.6100386 · Cited by 217 · see citing works
Stefanova, N., Reindl, M., Neumann, M., Kahle, P. J., Poewe, W. H., & Wenning, G. K. (2007) · Movement Disorders · doi:10.1002/mds.21671 · Cited by 217 · see citing works
Self-citationStefanova, N., Reindl, M., Neumann, M., Haass, C., Poewe, W., Kahle, P. J., & Wenning, G. K. (2005) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)62307-3 · Cited by 208 · see citing works
Self-citationp25α Relocalizes in Oligodendroglia from Myelin to Cytoplasmic Inclusions in Multiple System Atrophy
Song, Y. J. C., Lundvig, D. M. S., Huang, Y. M., Gai, W., Blumbergs, P. C., Højrup, P., Otzen, D. E., Halliday, G. M., & Jensen, P. H. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.070201 · Cited by 201 · see citing works
Absence of α-synuclein mRNA expression in normal and multiple system atrophy oligodendroglia
Miller, D. W., Johnson, J. M., Solano, S. M., Hollingsworth, Z. R., Standaert, D. G., & Young, A. B. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0378-1 · Cited by 198 · see citing works
Alpha‐synuclein mRNA expression in oligodendrocytes in MSA
Asi, Y. T., Simpson, J. E., Heath, P. R., Wharton, S. B., Lees, A. J., Révész, T., Houlden, H., & Holton, J. L. (2014) · Glia · doi:10.1002/glia.22653 · Cited by 191 · see citing works
Dodel, R. C., Spottke, A. E., Gerhard, A., Reuß, A., Reinecker, S., Schimke, N., Trenkwalder, C., Sixel‐Döring, F., Herting, B., Kamm, C., et al. (2009) · Movement Disorders · doi:10.1002/mds.22732 · Cited by 187 · see citing works
A Novel “Molecular Tweezer” Inhibitor of α-Synuclein Neurotoxicity in Vitro and in Vivo
Prabhudesai, S., Sinha, S., Attar, A., Kotagiri, A., Fitzmaurice, A., Lakshmanan, R., Ivanova, M., Loo, J. A., Klärner, F., Schrader, T., et al. (2012) · Neurotherapeutics · doi:10.1007/s13311-012-0105-1 · Cited by 165 · see citing works
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 · see citing works
Self-citationA genome-wide association study in multiple system atrophy
Sailer, A., Scholz, S. W., Nalls, M. A., Schulte, C., Federoff, M., Price, T. R., Lees, A. J., Ross, O. A., Dickson, D. W., Mok, K. Y., et al. (2016) · Neurology · doi:10.1212/wnl.0000000000003221 · Cited by 161 · see citing works
Mandler, M., Valera, E., Rockenstein, E. M., Mante, M., Weninger, H., Patrick, C., Adame, A., Schmidhuber, S. M., Santic, R., Schneeberger, A., et al. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0008-9 · Cited by 148 · see citing works
Melki, R. (2015) · Journal of Parkinson s Disease · doi:10.3233/jpd-150543 · Cited by 147 · see citing works
Levin, J., Schmidt, F., Boehm, C., Prix, C., Bötzel, K., Ryazanov, S., Leonov, A., Griesinger, C., & Giese, A. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1265-3 · Cited by 132 · see citing works
Bassil, F., Fernagut, P., Bézard, E., Pruvost, A., Lesté-Lasserre, T., Hoang, Q. Q., Ringe, D., Petsko, G. A., & Meissner, W. G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1609291113 · Cited by 113 · see citing works
Stefanova, N., Georgievska, B., Eriksson, H., Poewe, W., & Wenning, G. K. (2012) · Neurotoxicity Research · doi:10.1007/s12640-011-9294-3 · Cited by 111 · see citing works
Self-citationLow, P. A., Robertson, D., Gilman, S., Kaufmann, H., Singer, W., Biaggioni, I., Freeman, R. L., Perlman, S., Hauser, R. A., Cheshire, W. P., et al. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70301-6 · Cited by 111 · see citing works
Ozawa, T., Okuizumi, K., Ikeuchi, T., Wakabayashi, K., Takahashi, H., & Tsuji, S. (2001) · Acta Neuropathologica · doi:10.1007/s004010100367 · Cited by 109 · see citing works
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 · see citing works
A study of five candidate genes in Parkinson’s disease and related neurodegenerative disorders
Nicholl, D. J., Bennett, P. R., Hiller, L., Bonifati, V., Vanacore, N., Fabbrini, G., Marconi, R., Colosimo, C., Lamberti, P., Stocchi, F., et al. (1999) · Neurology · doi:10.1212/wnl.53.7.1415 · Cited by 107 · see citing works
Rationally Designed TLR4 Ligands for Vaccine Adjuvant Discovery
Gregg, K. A., Harberts, E. M., Gardner, F. M., Pelletier, M. R., Cayatte, C., Yu, L., McCarthy, M. P., Marshall, J. D., & Ernst, R. K. (2017) · mBio · doi:10.1128/mbio.00492-17 · Cited by 103 · see citing works
Molecular Basis for Preventing α-Synuclein Aggregation by a Molecular Tweezer
Acharya, S., Safaie, B. M., Wongkongkathep, P., Ivanova, M. I., Attar, A., Klärner, F. G., Schrader, T. H., Loo, J. A., Bitan, G., & Lapidus, L. J. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.524520 · Cited by 97 · see citing works
Poewe, W. H., Seppi, K., Fitzer‐Attas, C. J., Wenning, G. K., Gilman, S., Low, P. A., Giladi, N., Barone, P., Sampaio, C., Eyal, E., et al. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70288-1 · Cited by 96 · see citing works
Animal models of multiple system atrophy
Stefanova, N., & Wenning, G. K. (2015) · Clinical Autonomic Research · doi:10.1007/s10286-014-0266-6 · Cited by 93 · see citing works
Self-citationMutant COQ2 in Multiple-System Atrophy
Jeon, B. S., Farrer, M. J., & Bortnick, S. (2014) · New England Journal of Medicine · doi:10.1056/nejmc1311763 · Cited by 92 · see citing works
Venezia, S., Refolo, V., Polissidis, A., Stefanis, L., Wenning, G. K., & Stefanova, N. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0195-7 · Cited by 92 · see citing works
Self-citationStemberger, S., Jamnig, A., Stefanova, N., Lepperdinger, G., Reindl, M., & Wenning, G. K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019808 · Cited by 90 · see citing works
Self-citationUbhi, K. K., Inglis, C. A., Mante, M., Patrick, C., Adame, A., Spencer, B. J., Rockenstein, E. M., May, V. E. L., Winkler, J., & Masliah, E. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.01.008 · Cited by 87 · see citing works
Rasagiline is neuroprotective in a transgenic model of multiple system atrophy
Stefanova, N., Poewe, W. H., & Wenning, G. K. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.11.022 · Cited by 87 · see citing works
Self-citationSchwarz, L., Goldbaum, O., Bergmann, M., Probst‐Cousin, S., & Richter‐Landsberg, C. (2012) · Journal of Molecular Neuroscience · doi:10.1007/s12031-012-9733-5 · Cited by 82 · see citing works
Ettle, B., Kerman, B. E., Valera, E., Gillmann, C., Schlachetzki, J. C. M., Reiprich, S., Büttner, C., Ekici, A. B., Reis, A., Wegner, M., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1572-y · Cited by 81 · see citing works
Stefanova, N., Kaufmann, W. A., Humpel, C., Poewe, W. H., & Wenning, G. K. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-0977-5 · Cited by 79 · see citing works
Self-citationSmoking habits in multiple system atrophy and progressive supranuclear palsy
Vanacore, N., Bonifati, V., Fabbrini, G., Colosimo, C., Marconi, R., Nicholl, D. J., Bonuccelli, U., Stocchi, F., Lamberti, P., Volpe, G., et al. (2000) · Neurology · doi:10.1212/wnl.54.1.114 · Cited by 79 · see citing works
Rifampicin reduces α-synuclein in a transgenic mouse model of multiple system atrophy
Ubhi, K. K., Rockenstein, E. M., Mante, M., Patrick, C., Adame, A., Thukral, M., Shults, C. W., & Masliah, E. (2008) · Neuroreport · doi:10.1097/wnr.0b013e32830b3661 · Cited by 78 · see citing works
Case–control study of multiple system atrophy
Vanacore, N., Bonifati, V., Fabbrini, G., Colosimo, C., Michele, G. D., Marconi, R., Stocchi, F., Nicholl, D. J., Bonuccelli, U., Mari, M. D., et al. (2004) · Movement Disorders · doi:10.1002/mds.20303 · Cited by 76 · 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
Bladder dysfunction in a transgenic mouse model of multiple system atrophy
Boudes, M., Uvin, P., Pinto, S., Voets, T., Fowler, C. J., Wenning, G. K., Ridder, D. J. M. K. D., & Stefanova, N. (2013) · Movement Disorders · doi:10.1002/mds.25336 · Cited by 65 · see citing works
Self-citationLangerveld, A. J., Mihalko, D., DeLong, C., Walburn, J., & Ide, C. F. (2007) · Movement Disorders · doi:10.1002/mds.21259 · Cited by 65 · see citing works
Lee, P. H., & Park, H. J. (2009) · Journal of Clinical Neurology · doi:10.3988/jcn.2009.5.1.1 · Cited by 65 · see citing works
Alteration of autophagosomal proteins in the brain of multiple system atrophy
Tanji, K., Odagiri, S., Maruyama, A., Mori, F., Kakita, A., Takahashi, H., & Wakabayashi, K. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.08.017 · Cited by 64 · see citing works
Epidemiological evidence on multiple system atrophy
Vanacore, N. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0380-7 · Cited by 62 · see citing works
A Molecular Tweezer Ameliorates Motor Deficits in Mice Overexpressing α-Synuclein
Richter, F., Subramaniam, S., Magen, I., Lee, P., Hayes, J., Attar, A., Zhu, C., Franich, N. R., Bove, N., Rosa, K. D. L., et al. (2017) · Neurotherapeutics · doi:10.1007/s13311-017-0544-9 · Cited by 57 · see citing works
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
Kuzdas-Wood, D., Stemberger, S., Gaburro, S., Stefanova, N., Singewald, N., & Wenning, G. K. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.02.002 · Cited by 55 · see citing works
Self-citationMechanism of Anti-α-Synuclein Immunotherapy
Lee, J. S., & Lee, S. (2016) · Journal of Movement Disorders · doi:10.14802/jmd.15059 · Cited by 52 · see citing works
Genome-wide estimate of the heritability of Multiple System Atrophy
Federoff, M., Price, T. R., Sailer, A., Scholz, S. W., Hernandez, D. G., Nicolas, A., Singleton, A., Nalls, M. A., & Houlden, H. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.11.005 · Cited by 51 · see citing works
Pukaß, K., Goldbaum, O., & Richter‐Landsberg, C. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13256 · Cited by 49 · see citing works
Analysis of COQ2gene in multiple system atrophy
Ogaki, K., Fujioka, S., Heckman, M. G., Rayaprolu, S., Soto‐Ortolaza, A. I., Labbé, C., Walton, R. L., Lorenzo‐Betancor, O., Wang, X., Asmann, Y. W., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-44 · Cited by 49 · see citing works
Attar, A., & Bitan, G. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990496 · Cited by 48 · see citing works
Mutation scanning of the COQ2 gene in ethnic Chinese patients with multiple-system atrophy
Chen, Y. P., Zhao, B., Cao, B., Song, W., Guo, X., Wei, Q., Yang, Y., Yuan, L. X., & Shang, H. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.09.010 · Cited by 48 · see citing works
Viral‐mediated oligodendroglial alpha‐synuclein expression models multiple system atrophy
Bassil, F., Guerin, P. A., Dutheil, N., Li, Q., Klugmann, M., Meissner, W. G., Bézard, E., & Fernagut, P. (2017) · Movement Disorders · doi:10.1002/mds.27041 · Cited by 48 · see citing works
Kaindlstorfer, C., Sommer, P., Georgievska, B., Mather, R. J., Kugler, A. R., Poewe, W. H., Wenning, G. K., & Stefanova, N. (2015) · Neurotoxicity Research · doi:10.1007/s12640-015-9547-7 · Cited by 47 · see citing works
Self-citationScreening of Toll-Like Receptors Expression in Multiple System Atrophy Brains
Brudek, T., Winge, K., Agander, T. K., & Pakkenberg, B. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1020-5 · Cited by 43 · see citing works
Multiple System Atrophy: Genetic or Epigenetic?
Sturm, E., & Stefanova, N. (2014) · Experimental Neurobiology · doi:10.5607/en.2014.23.4.277 · Cited by 36 · see citing works
Self-citationFernagut, P. O., Meissner, W. G., Biran, M., Fantin, M., Bassil, F., Franconi, J. M., & Tison, F. (2014) · Synapse · doi:10.1002/syn.21719 · Cited by 35 · cited 1× · see citing works
“…et al., 2005;Stefanova et al., 2007;Krismer et al., 2013;Boudes et al., 2013;Kuzdas et al., 2013;Stefanova et al., 2013;Flabeau et al., 2014;Fernagut et al., 2014;Bassil et al., 2017b;Mandel et al., 2017;Hartner et al., 2016;Stefanova et al., 2014) AC CE PT ED M AN US CR IPT improvement…”
Breathing variability and brainstem serotonergic loss in a genetic model of multiple system atrophy
Flabeau, O., Meissner, W. G., Ozier, A., Berger, P., Tison, F., & Fernagut, P. (2014) · Movement Disorders · doi:10.1002/mds.25804 · Cited by 34 · see citing works
Fellner, L., Kuzdas-Wood, D., Levin, J., Ryazanov, S., Leonov, A., Griesinger, C., Giese, A., Wenning, G. K., & Stefanova, N. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00099 · Cited by 29 · see citing works
Self-citationStriatal transplantation for multiple system atrophy — Are grafts affected by α-synucleinopathy?
Stefanova, N., Hainzer, M., Stemberger, S., Couillard‐Després, S., Aigner, L., Poewe, W. H., & Wenning, G. K. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.05.016 · Cited by 28 · see citing works
Self-citationQuinn, N. P., Barker, R. A., & Wenning, G. K. (2008) · Clinical Pharmacology & Therapeutics · doi:10.1038/sj.clpt.6100454 · Cited by 25 · see citing works
Intact Olfaction in a Mouse Model of Multiple System Atrophy
Krismer, F., Wenning, G. K., Li, Y., Poewe, W. H., & Stefanova, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064625 · Cited by 22 · see citing works
Self-citationHärtner, L., Keil, T. W. M., Kreuzer, M., Fritz, E., Wenning, G., Stefanova, N., & Fenzl, T. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00252 · Cited by 21 · see citing works
Self-citationSunwoo, M. K., Yun, H. J., Song, S., Ham, J. H., Hong, J. Y., Lee, J. E., Lee, H. S., Sohn, Y. H., Lee, J., & Lee, P. H. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00118 · Cited by 19 · see citing works
Neuroprotection by Epigenetic Modulation in a Transgenic Model of Multiple System Atrophy
Sturm, E., Fellner, L., Krismer, F., Poewe, W. H., Wenning, G. K., & Stefanova, N. (2016) · Neurotherapeutics · doi:10.1007/s13311-016-0447-1 · Cited by 17 · see citing works
Self-citationLow, P. A., & Gilman, S. (2012) · Annals of Neurology · doi:10.1002/ana.23655 · Cited by 11 · see citing works
Clinical trials for multiple system atrophy
Galpern, W. R. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70311-4 · Cited by 4 · see citing works
Solano (2000) · doi:10.1002/1531-8249(200002)47:2 · Cited by 3 · see citing works
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Gao, C., Jiang, J., Tan, Y., & Chen, S. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01588-0 · Cited by 1,616 · see citing works
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Meissner, W. G., Fernagut, P., Dehay, B., Péran, P., Traon, A. P., Foubert‐Samier, A., Cuina, M. L., Bézard, E., Tison, F., & Rascol, O. (2019) · Movement Disorders · doi:10.1002/mds.27894 · Cited by 93 · see citing works
Lemos, M., Venezia, S., Refolo, V., Heras‐Garvin, A., Schmidhuber, S. M., Giese, A., Leonov, A., Ryazanov, S., Griesinger, C., Galabova, G., et al. (2020) · Translational Neurodegeneration · doi:10.1186/s40035-020-00217-y · Cited by 38 · see citing works
Self-citationKallab, M., Herrera-Vaquero, M., Johannesson, M., Eriksson, F., Sigvardson, J., Poewe, W. H., Wenning, G. K., Nordström, E. K. L., & Stefanova, N. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00452 · Cited by 34 · see citing works
Self-citationSigns of early cellular dysfunction in multiple system atrophy
Herrera-Vaquero, M., Heras‐Garvin, A., Krismer, F., Deleanu, R., Boesch, S., Wenning, G. K., & Stefanova, N. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12661 · Cited by 30 · see citing works
Self-citationATH434 Reduces α‐Synuclein‐Related Neurodegeneration in a Murine Model of Multiple System Atrophy
Heras‐Garvin, A., Refolo, V., Schmidt, C., Malfertheiner, K., Wenning, G. K., BRADBURY, M. J., Stamler, D. A., & Stefanova, N. (2021) · Movement Disorders · doi:10.1002/mds.28714 · Cited by 27 · see citing works
Self-citationMultiple System Atrophy: Pathology, Pathogenesis, and Path Forward
Ndayisaba, A., Halliday, G. M., & Khurana, V. (2024) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-051122-104528 · Cited by 26 · see citing works
MSA: From basic mechanisms to experimental therapeutics
Heras‐Garvin, A., & Stefanova, N. (2020) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2020.01.010 · Cited by 20 · see citing works
Self-citationCurrent experimental disease-modifying therapeutics for multiple system atrophy
Lemos, M., Wenning, G. K., & Stefanova, N. (2021) · Journal of Neural Transmission · doi:10.1007/s00702-021-02406-z · Cited by 18 · see citing works
Self-citationProgress in the treatment of Parkinson-Plus syndromes
Olfati, N., Shoeibi, A., & Litvan, I. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.10.006 · Cited by 12 · see citing works
Boström, E., Bachhav, S. S., Xiong, H., Zadikoff, C., Li, Q., Cohen, E. B., Dreher, I., Torrång, A., Osswald, G., Moge, M., et al. (2024) · The Journal of Clinical Pharmacology · doi:10.1002/jcph.6103 · Cited by 7 · see citing works
Chang, C. C., Liu, J., Chen, B. C., Jiang, Z. S., Tu, C. T., Su, C. H., Yang, H. H., Liu, Z. Q., Deng, Y. C., Chen, C. Y., et al. (2020) · Cell Transplantation · doi:10.1177/0963689720960185 · Cited by 1 · see citing works
- Authors
- Stefanova, N.
- Affiliations
- Innsbruck Medical University (AT)
- Corresponding author
- Stefanova, Nadia
- ORCID
- Stefanova, Nadia
- Venue
- Autonomic Neuroscience
- Publisher
- Elsevier BV
- Published
- 2018-05
- Volume
- 211
- Pages
- 7-14
- ISSN
- 1566-0702 (ISSN-L)
- OpenAlex
- W2762041465
- Cited by
- 12
- References
- 84
- Citations by year
- 2024: 2 · 2023: 1 · 2021: 2 · 2020: 4 · 2019: 1 · 2018: 2
- FWCI
- 0.25
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Autonomic Neuroscience (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Austrian Science Fund (F4414)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- multiple system atrophy, alpha-synuclein, translational therapy, clinical trial design, disease biomarkers, early diagnosis, proof of concept, therapeutic target
- MeSH terms
- Animals, Clinical Trials as Topic, Disease Models, Animal, Humans, Disease Progression, Multiple System Atrophy, alpha-Synuclein, Translational Research, Biomedical
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