Home Candidate biomarkers of multiple system atrophy in cerebrospinal fluid
Article
Licensed
Unlicensed Requires Authentication

Candidate biomarkers of multiple system atrophy in cerebrospinal fluid

  • Feng Zhang

    Feng Zhang is a master’s candidate in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University, Dalian. His research interests include neurodegenerative diseases and movement disorders.

    , Jianwen Chen

    Jianwen Chen is a master’s candidate in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University, Dalian. Her research interests include neurodegenerative diseases and movement disorders.

    , Li Zhao

    Li Zhao received her MD in Dalian Medical University, Dalian. She is currently associate Professor in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University. Her research interests include neuropsychology, counseling and clinical neurology.

    and Chunbo Dong

    Chunbo Dong received her MD in Dalian Medical University, Dalian. She is currently Professor and Chair in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University. Her research interests include neurodegenerative diseases, neurological genetic diseases and movement disorders.

    EMAIL logo
Published/Copyright: May 27, 2014
Become an author with De Gruyter Brill

Abstract

Multiple system atrophy (MSA) is a neurodegenerative disease that presents as an autonomic dysfunction in combination with varying degrees of parkinsonism and cerebellar ataxia. It comprises a pathologically widespread neuronal loss accompanied by gliosis in the basal ganglia, cerebellum, pons, inferior olivary nuclei, and spinal cord. As a rapidly progressive disorder, MSA develops with autonomic dysfunction and mobility problems in several years. These autonomic and motor function impairments severely disrupt the patients’ daily lives. Currently, the therapeutic management of this disease is only symptomatic. An early and accurate diagnosis is helpful not only in the clinical field but also in the research for new therapies. The biomarkers in cerebrospinal fluid (CSF) and serum facilitate the differential diagnosis of MSA when the disease is difficult to recognize based on the clinical features or even presymptomatic. This review will summarize the biomarkers present in CSF that are potential candidates to accurately differentiate MSA from other similar neurodegenerative disorders.


Corresponding author: Chunbo Dong, Department of Neurology, The First Affiliated Hospital of Dalian Medical University, Dalian 116011, China, e-mail:
aFeng Zhang and Jianwen Chen contributed equally to this article.

About the authors

Feng Zhang

Feng Zhang is a master’s candidate in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University, Dalian. His research interests include neurodegenerative diseases and movement disorders.

Jianwen Chen

Jianwen Chen is a master’s candidate in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University, Dalian. Her research interests include neurodegenerative diseases and movement disorders.

Li Zhao

Li Zhao received her MD in Dalian Medical University, Dalian. She is currently associate Professor in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University. Her research interests include neuropsychology, counseling and clinical neurology.

Chunbo Dong

Chunbo Dong received her MD in Dalian Medical University, Dalian. She is currently Professor and Chair in the Department of Neurology of the First Affiliated Hospital of Dalian Medical University. Her research interests include neurodegenerative diseases, neurological genetic diseases and movement disorders.

References

Abdo, W.F., De Jong, D., Hendriks, J.C., Horstink, M.W., Kremer, B.P., Bloem, B.R., and Verbeek, M.M. (2004). Cerebrospinal fluid analysis differentiates multiple system atrophy from Parkinson’s disease. Mov. Disord. 19, 571–579.10.1002/mds.10714Search in Google Scholar

Abdo, W.F., Bloem, B.R., Van Geel, W.J., Esselink, R.A., and Verbeek, M.M. (2007a). CSF neurofilament light chain and tau differentiate multiple system atrophy from Parkinson’s disease. Neurobiol. Aging 28, 742–747.10.1016/j.neurobiolaging.2006.03.010Search in Google Scholar

Abdo, W.F., van de Warrenburg, B.P., Kremer, H.P., Bloem, B.R., and Verbeek, M.M. (2007b). CSF biomarker profiles do not differentiate between the cerebellar and parkinsonian phenotypes of multiple system atrophy. Parkinsonism Relat. Disord. 13, 480–482.10.1016/j.parkreldis.2007.02.002Search in Google Scholar

Abe, K., Hikita, T., Yokoe, M., Mihara, M., and Sakoda, S. (2006). The “cross” signs in patients with multiple system atrophy: a quantitative study. J. Neuroimaging 16, 73–77.10.1177/1051228405279988Search in Google Scholar

Aerts, M.B., Esselink, R.A., Abdo, W.F., Bloem, B.R., and Verbeek, M.M. (2012). CSF alpha-synuclein does not differentiate between parkinsonian disorders. Neurobiol. Aging 33, 430, e1–e3.Search in Google Scholar

Andreasen, N. and Blennow, K. (2002). Beta-amyloid (Abeta) protein in cerebrospinal fluid as a biomarker for Alzheimer’s disease. Peptides 23, 1205–1214.10.1016/S0196-9781(02)00056-6Search in Google Scholar

Arima, K., Murayama, S., Mukoyama, M., and Inose, T. (1992). Immunocytochemical and ultrastructural studies of neuronal and oligodendroglial cytoplasmic inclusions in multiple system atrophy. 1. Neuronal cytoplasmic inclusions. Acta Neuropathol. 83, 453–460. [PubMed: 1320321].10.1007/BF00310020Search in Google Scholar PubMed

Beyer, K. (2006). Alpha-synuclein structure, posttranslational modification and alternative splicing as aggregation enhancers. Acta Neuropathol. 112, 237–251.10.1007/s00401-006-0104-6Search in Google Scholar PubMed

Biomarkers Definitions Working Group (2001). Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin. Pharmacol. Ther. 69, 89–95.Search in Google Scholar

Blennow, K., Hampel, H., Weiner, M., and Zetterberg, H. (2010). Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat. Rev. Neurol. 6, 131–144.10.1038/nrneurol.2010.4Search in Google Scholar PubMed

Botez, M.I. and Young, S.N. (2001). Biogenic amine metabolites and thiamine in cerebrospinal fluid in heredo-degenerative ataxias. Can. J. Neurol. Sci. 28, 134–140.10.1017/S0317167100052811Search in Google Scholar PubMed

Brettschneider, J., Petzold, A., Süssmuth, S.D., Landwehrmeyer, G.B., Ludolph, A.C., Kassubek, J., and Tumani, H. (2006). Neurofilament heavy-chain NfH(SMI35) in cerebrospinal fluid supports the differential diagnosis of parkinsonian syndromes. Mov. Disord. 21, 2224–2227.10.1002/mds.21124Search in Google Scholar PubMed

Chen, H., Mosley, T.H., Alonso, A., and Huang, X. (2009). Plasma urate and Parkinson’s disease in the Atherosclerosis Risk in Communities (ARIC) study. Am. J. Epidemiol. 169, 1064–1069.10.1093/aje/kwp033Search in Google Scholar PubMed PubMed Central

Constantinescu, R., Zetterberg, H., Holmberg, B., and Rosengren, L. (2009). Levels of brain related proteins in cerebrospinal fluid: an aid in the differential diagnosis of parkinsonian disorders. Parkinsonism Relat. Disord. 15, 205–212.10.1016/j.parkreldis.2008.05.001Search in Google Scholar PubMed

Constantinescu, R., Rosengren, L., Johnels, B., Zetterberg, H., and Holmberg, B. (2010a). Consecutive analyses of cerebrospinal fluid axonal and glial markers in Parkinson’s disease and atypical parkinsonian disorders. Parkinsonism Relat. Disord. 16, 142–145.10.1016/j.parkreldis.2009.07.007Search in Google Scholar PubMed

Constantinescu, R., Andreasson, U., Li, S., Podust, V.N., Mattsson, N., Anckarsäter, R., Anckarsäter, H., Rosengren, L., Holmberg, B., Blennow, K., et al. (2010b). Proteomic profiling of cerebrospinal fluid in parkinsonian disorders. Parkinsonism Relat. Disord. 16, 545–549.10.1016/j.parkreldis.2010.06.011Search in Google Scholar PubMed

Constantinescu, R., Andreasson, U., Holmberg, B., and Zetterberg, H. (2013). Serum and cerebrospinal fluid urate levels in synucleinopathies versus tauopathies. Acta Neurol. Scand. 127, e8–e12.10.1111/ane.12012Search in Google Scholar PubMed

Dickson, D.W., Lin, W., Liu, W.K., and Yen, S.H. (1999). Multiple system atrophy: a sporadic synucleinopathy. Brain Pathol. 9, 721–732.10.1111/j.1750-3639.1999.tb00553.xSearch in Google Scholar PubMed PubMed Central

Foulds, P.G., Yokota, O., Thurston, A., Davidson, Y., Ahmed, Z., Holton, J., Thompson, J.C., Akiyama, H., Arai, T., Hasegawa, M., et al. (2012). Post mortem cerebrospinal fluid alpha-synuclein levels are raised in multiple system atrophy and distinguish this from the other alpha-synucleinopathies, Parkinson’s disease and dementia with Lewy bodies. Neurobiol. Dis. 45, 188–195.10.1016/j.nbd.2011.08.003Search in Google Scholar PubMed PubMed Central

Frohman, L.A., Downs, T.R., and Chomczynski, P. (1992). Regulation of growth hormone secretion. Front. Neuroendocrinol. 13, 344–405.Search in Google Scholar

Gardner, R.C. and Schmahmann, J.D. (2010). Arginine test is not reliable for diagnosing cerebellar multiple system atrophy. Ann. Neurol. 67, 404–408.Search in Google Scholar

George, S., Rey, N.L., Reichenbach, N., Steiner, J.A., and Brundin, P. (2013). Alpha-synuclein: the long distance runner. Brain Pathol. 23, 350–357.10.1111/bpa.12046Search in Google Scholar PubMed PubMed Central

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). Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71, 670–676.10.1212/01.wnl.0000324625.00404.15Search in Google Scholar PubMed PubMed Central

Goldstein, D.S., Holmes, C., and Sharabi, Y. (2012). Cerebrospinal fluid biomarkers of central catecholamine deficiency in Parkinson’s disease and other synucleinopathies. Brain 135, 1900–1913.10.1093/brain/aws055Search in Google Scholar PubMed PubMed Central

Hall, S., Ö hrfelt, A., Constantinescu, R., Andreasson, U., Surova, Y., Bostrom, F., Nilsson, C., Håkan, W., Decraemer, H., Någga, K., et al. (2012). Accuracy of a panel of 5 cerebrospinal fluid biomarkers in the differential diagnosis of patients with dementia and/or parkinsonian disorders. Arch. Neurol. 69, 1445–1452.10.1001/archneurol.2012.1654Search in Google Scholar

Hashimoto, M. and Masliah, E. (1999). Alpha-synuclein in Lewy body disease and Alzheimer’s disease. Brain Pathol. 9, 707–720.10.1111/j.1750-3639.1999.tb00552.xSearch in Google Scholar

Holmberg, B., Rosengren, L., Karlsson, J.E., and Johnels, B. (1998). Increased cerebrospinal fluid levels of neurofilament protein in progressive supranuclear palsy and multiple-system atrophy compared with Parkinson’s disease. Mov. Disord. 13, 70–77.10.1002/mds.870130116Search in Google Scholar

Holmberg, B., Johnels, B., Ingvarsson, P., Eriksson, B., and Rosengren, L. (2001). CSF-neurofilament and levodopa tests combined with discriminant analysis may contribute to the differential diagnosis of parkinsonian syndromes. Parkinsonism Relat. Disord. 8, 23–31.10.1016/S1353-8020(00)00083-3Search in Google Scholar

Holmberg, B., Johnels, B., Blennow, K., and Rosengren, L. (2003). Cerebrospinal fluid Abeta42 is reduced in multiple system atrophy but normal in Parkinson’s disease and progressive supranuclear palsy. Mov. Disord. 18, 186–190.10.1002/mds.10321Search in Google Scholar PubMed

Horimoto, Y., Aiba, I., Yasuda, T., Ohkawa, Y., Katayama, T., Yokokawa, Y., Goto, A., and Ito, Y. (2002). Longitudinal MRI study of multiple system atrophy – when do the findings appear, and what is the course? J. Neurol. 249, 847–854.10.1007/s00415-002-0734-0Search in Google Scholar PubMed

Ingram, G., Hakobyan, S., Hirst, C.L., Harris, C.L., Pickersgill, T.P., Cossburn, M.D., Loveless, S., Robertson, N.P., and Morgan, B.P. (2010). Complement regulator factor H as a serum biomarker of multiple sclerosis disease state. Brain 133, 1602–1611.10.1093/brain/awq085Search in Google Scholar PubMed

Ishigami, N., Tokuda, T., Ikegawa, M., Komori, M., Kasai, T., Kondo, T., Matsuyama, Y., Nirasawa, T., Thiele, H., Tashiro, K., et al. (2012). Cerebrospinal fluid proteomic patterns discriminate Parkinson’s disease and multiple system atrophy. Mov. Disord. 27, 851–857.10.1002/mds.24994Search in Google Scholar PubMed

Kaeser, S.A., Herzig, M.C., Coomaraswamy, J., Kilger, E., Selenica, M.L., Winkler, D.T., Staufenbiel, M., Levy, E., Grubb, A., and Jucker, M. (2007). Cystatin C modulates cerebral b-amyloidosis. Nat. Genet. 39, 1437–1439.10.1038/ng.2007.23Search in Google Scholar PubMed

Kanhai, D.A., de Kleijn, D.P., Kappelle, L.J., Uiterwaal, C.S., van der Graaf, Y., Pasterkamp, G., Geerlings, M.I., Visseren, F.L.; SMART Study Group. (2014). Extracellular vesicle protein levels are related to brain atrophy and cerebral white matter lesions in patients with manifest vascular disease: the SMART-MR study. BMJ Open 4, e003824.10.1136/bmjopen-2013-003824Search in Google Scholar PubMed PubMed Central

Kato, S., Nakamura, H., Hirano, A., Ito, H., Llena, J.F., and Yen, SH. (1991). Argyrophilic ubiquitinated cytoplasmic inclusions of Leu-7-positive glial cells in olivopontocerebellar atrophy (multiple system atrophy). Acta Neuropathol. 82, 488–493.10.1007/BF00293383Search in Google Scholar

Kim, S.Y., Buckwalter, M., Soreq, H., Vezzani, A., and Kaufer, D. (2012). Blood-brain barrier dysfunction-induced inflammatory signaling in brain pathology and epileptogenesis. Epilepsia 53, 37–44.10.1111/j.1528-1167.2012.03701.xSearch in Google Scholar

Kish, S.J., Robitaille, Y., Schut, L., el-Awar, M., Ball, M.J., and Shannak, K. (1992). Normal serotonin but elevated 5-hydroxyindoleacetic acid concentration in cerebellar cortex of patients with dominantly-inherited olivopontocerebellar atrophy. Neurosci. Lett. 144, 84–86.10.1016/0304-3940(92)90721-ISearch in Google Scholar

Lee, J.E., Song, S.K., Sohn, Y.H., and Lee, P.H. (2011). Uric acid as a potential disease modifier in patients with multiple system atrophy. Mov. Disord. 26, 1533–1536.10.1002/mds.23556Search in Google Scholar

Lee, J.E., Song, S.K., Hong, J.Y., Sunwoo, M.K., Park, H.J., Sohn, Y.H., and Lee, P.H. (2013). Changes in the blood-brain barrier status closely correlate with the rate of disease progression in patients with multiple system atrophy: a longitudinal study. Parkinsonism Relat. Disord. 19, 450–452.10.1016/j.parkreldis.2012.12.002Search in Google Scholar

Leonelli, M., Torrao, A.S., and Britto, L.R. (2009). Unconventional neurotransmitters, neurodegeneration and neuroprotection. Braz. J. Med. Biol. Res. 42, 68–75.10.1590/S0100-879X2009000100011Search in Google Scholar

Loddick, S.A. and Rothwell, N.J. (1999). Mechanisms of tumor necrosis factor alpha action on neurodegeneration: interaction with insulin-like growth factor-1. Proc. Natl. Acad. Sci. USA 96, 9449–9451.10.1073/pnas.96.17.9449Search in Google Scholar

Lyman, S.D. and Jacobsen, S.E. (1998). c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91, 1101–1134.10.1182/blood.V91.4.1101Search in Google Scholar

Mandelkow, E.M. and Mandelkow, E. (2012). Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb. Perspect. Med. 2, a006247.10.1101/cshperspect.a006247Search in Google Scholar

Mollenhauer, B., Locascio, J.J., Schulz-Schaeffer, W., Sixel-Döring, F., Trenkwalder, C., and Schlossmacher, M.G. (2011). Alpha-synuclein and tau concentrations in cerebrospinal fluid of patients presenting with parkinsonism: a cohort study. Lancet Neurol. 10, 230–240.10.1016/S1474-4422(11)70014-XSearch in Google Scholar

Muller, E.E., Locatelli, V., and Cocchi, D. (1999). Neuroendocrine control of growth hormone secretion. Physiol. Rev. 79, 511–607.10.1152/physrev.1999.79.2.511Search in Google Scholar

Nakazato, Y., Yamazaki, H., Hirato, J., Ishida, Y., and Yamaguchi, H. (1990). Oligodendroglial microtubular tangles in olivopontocerebellar atrophy. J. Neuropathol. Exp. Neurol. 49, 521–530.10.1097/00005072-199009000-00007Search in Google Scholar

Numao, A., Suzuki, K., Miyamoto, M., Miyamoto, T., and Hirata, K. (2014). Clinical correlates of serum insulin-like growth factor-1 in patients with Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. Parkinsonism Relat. Disord. 20, 212–216.10.1016/j.parkreldis.2013.11.005Search in Google Scholar

Otto, M., Esselmann, H., Schulz-Shaeffer, W., Neumann, M., Schröter, A., Ratzka, P., Cepek, L., Zerr, I., Steinacker, P., Windl, O., et al. (2000). Decreased beta-amyloid1-42 in cerebrospinal fluid of patients with Creutzfeldt-Jakob disease. Neurology 54, 1099–1102.10.1212/WNL.54.5.1099Search in Google Scholar

Oueslati, A., Fournier, M., and Lashuel, H.A. (2010). Role of post-translational modifications in modulating the structure, function and toxicity of a-synuclein: implications for Parkinson’s disease pathogenesis and therapies. Prog. Brain Res. 183, 115–145.10.1016/S0079-6123(10)83007-9Search in Google Scholar

Papp, M.I., Kahn, J.E., and Lantos, P.L. (1989). Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J. Neurol. Sci. 94, 79–100.10.1016/0022-510X(89)90219-0Search in Google Scholar

Pellecchia, M.T., Pivonello, R., Salvatore, E., Faggiano, A., Barone, P., De Michele, G., Lombardi, G., Colao, A., and Filla, A. (2005). Growth hormone response to arginine test distinguishes multiple system atrophy from Parkinson’s disease and idiopathic late-onset cerebellar ataxia. Clin. Endocrinol. (Oxf.) 62, 428–433.10.1111/j.1365-2265.2005.02237.xSearch in Google Scholar PubMed

Pellecchia, M.T., Pivonello, R., Colao,A., and Barone, P. (2006). Growth hormone stimulation tests in the differential diagnosis of Parkinson’s disease. Clin. Med. Res. 4, 322–325.10.3121/cmr.4.4.322Search in Google Scholar PubMed PubMed Central

Pellecchia, M.T., Longo, K., Manfredi, M., Lucetti, C., Cossu, G., Petrone, A., Marconi, R., Sensi, M., Epifanio, A., Eleopra, R., et al. (2008). The arginine growth hormone stimulation test in bradykinetic-rigid parkinsonisms. Mov. Disord. 23, 190–194.10.1002/mds.21700Search in Google Scholar PubMed

Pellecchia, M.T., Pivonello, R., Longo, K., Manfredi, M., Tessitore, A., Amboni, M., Pivonello, C., Rocco, M., Cozzolino, A., Colao, A., et al. (2010). Multiple system atrophy is associated with changes in peripheral insulin-like growth factor system. Mov. Disord. 25, 2621–2626.10.1002/mds.23320Search in Google Scholar PubMed

Perrot, R., Berges, R., Bocquet, A., and Eyer, J. (2008). Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Mol. Neurobiol. 38, 27–65.10.1007/s12035-008-8033-0Search in Google Scholar

Pfeiffer, R.F. (2007). Multiple system atrophy. Handb. Clin. Neurol. 84, 305–326.10.1016/S0072-9752(07)84046-2Search in Google Scholar

Qin, L., Wu, X., Block, M.L., Liu, Y., Breese, G.R., Hong, J.S., Knapp, D.J., and Crews, F.T. (2007). Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55, 453–462.10.1002/glia.20467Search in Google Scholar

Rehman, H.U. (2000). Progressive supranuclear palsy. Postgrad. Med. J. 76, 333–336.10.1136/pmj.76.896.333Search in Google Scholar

Saracchi, E., Fermi, S., and Brighina, L. (2014). Emerging candidate biomarkers for Parkinson’s disease: a review. Aging Dis. 5, 27–34.10.14336/ad.2014.050027Search in Google Scholar

Sastre, M., Calero, M., Pawlik, M., Mathews, P.M., Kumar, A., Danilov, V., Schmidt, S.D., Nixon, R.A., Frangione, B., and Levy, E. (2004). Binding of cystatin C to Alzheimer’s amyloid beta inhibits in vitro amyloid fibril formation. Neurobiol. Aging 25, 1033–1043.10.1016/j.neurobiolaging.2003.11.006Search in Google Scholar

Shi, M., Bradner, J., Hancock, A.M., Chung, K.A., Quinn, J.F., Peskind, E.R., Galasko, D., Jankovic, J., Zabetian, C.P., Kim, H.M., et al. (2011). Cerebrospinal fluid biomarkers for Parkinson disease diagnosis and progression. Ann. Neurol. 69, 570–580.10.1002/ana.22311Search in Google Scholar

Sjögren, M., Minthon, L., Davidsson, P., Granérus, A.-K., Clarberg, A., Vanderstichele, H., Vanmechelen, E., Wallin, A., and Blennow, K. (2000). CSF levels of tau, beta-amyloid(1-42) and GAP-43 in frontotemporal dementia, other types of dementia and normal aging. J. Neural Transm. 107, 563–579.10.1007/s007020070079Search in Google Scholar

Song, S.K., Lee, S.K., Lee, J.J., Lee, J.E., Choi, H.S., Sohn, Y.H., and Lee, P.H. (2011). Blood-brain barrier impairment is functionally correlated with clinical severity in patients of multiple system atrophy. Neurobiol. Aging 32, 2183–2189.10.1016/j.neurobiolaging.2009.12.017Search in Google Scholar

Stefanova, N., Reindl, M., Neumann, M., Haass, C., Poewe, W., Kahle, P.J., and Wenning, G.K. (2005). Oxidative stress in transgenic mice with oligodendroglial alpha-synuclein overexpression replicates the characteristic neuropathology of multiple system atrophy. Am. J. Pathol. 166, 869–876.10.1016/S0002-9440(10)62307-3Search in Google Scholar

Stefanova, N., Bücke, P., Duerr, S., and Wenning, G.K. (2009). Multiple system atrophy: an update. Lancet Neurol. 8, 1172–1178.10.1016/S1474-4422(09)70288-1Search in Google Scholar

Tamaoka, A., Kondo, T., Odaka, A., Sahara, N., Sawamura, N., Ozawa, K., Suzuki, N., Shoji, S., and Mori, H. (1994). Biochemical evidence for the long-tail form (Abeta1-42/43) of amyloid beta protein as a seed molecule in cerebral deposits of Alzheimer’s disease. Biochem. Biophys. Res. Commun. 205, 834–842.10.1006/bbrc.1994.2740Search in Google Scholar

Ubhi, K., Lee, P.H., Adame, A., Inglis, C., Mante, M., Rockenstein, E., Stefanova, N., Wenning, G.K., and Masliah E. (2009). Mitochondrial inhibitor 3-nitroproprionic acid enhances oxidative modification of alpha-synuclein in a transgenic mouse model of multiple system atrophy. J. Neurosci. Res. 87, 2728–2739.10.1002/jnr.22089Search in Google Scholar

Ubhi, K., Low, P., and Masliah, E. (2011). Multiple system atrophy: a clinical and neuropathological perspective. Trends Neurosci. 34, 581–590.10.1016/j.tins.2011.08.003Search in Google Scholar

Urban, M.J., Dobrowsky, R.T., and Blagg, B.S. (2012). Heat shock response and insulin-associated neurodegeneration. Trends Pharmacol. Sci. 33, 129–137.10.1016/j.tips.2011.11.001Search in Google Scholar

Verbeek, M.M., Abdo, W.F., De Jong, D., Horstink, M.W., Kremer, B.P., and Bloem, B.R. (2004). Cerebrospinal fluid Abeta42 levels in multiple system atrophy. Mov. Disord. 19, 238–240; author reply 240–241.Search in Google Scholar

Wang, Y., Hancock, A.M., Bradner, J., Chung, K.A., Quinn, J.F., Peskind, E.R., Galasko, D., Jankovic, J., Zabetian, C.P., Kim, H.M., et al. (2011). Complement 3 and factor H in human cerebrospinal fluid in Parkinson’s disease, Alzheimer’s disease, and multiple-system atrophy. Am. J. Pathol. 178, 1509–1516.10.1016/j.ajpath.2011.01.006Search in Google Scholar

Winquist, A., Steenland, K., and Shankar, A. (2010). Higher serum uric acid associated with decreased Parkinson’s disease prevalence in a large community-based survey. Mov. Disord. 25, 932–936.10.1002/mds.23070Search in Google Scholar

Wodnar-Filipowicz, A. (2003). Flt3 ligand: role in control of hematopoietic and immune functions of the bone marrow. News Physiol. Sci. 18, 247–251.10.1152/nips.01452.2003Search in Google Scholar

Wolburg, H. and Lippoldt, A. (2002). Tight junctions of the blood-brain barrier: development, composition and regulation. Vasc. Pharmacol. 38, 323–337.10.1016/S1537-1891(02)00200-8Search in Google Scholar

Yamamoto-Watanabe, Y., Watanabe, M., Jackson, M., Akimoto, H., Sugimoto, K., Yasujima, M., Wakasaya, Y., Matsubara, E., Kawarabayashi, T., Harigaya, Y., et al. (2010). Quantification of cystatin C in cerebrospinal fluid from various neurological disorders and correlation with G73A polymorphism in CST3. Brain Res. 1361, 140–145.10.1016/j.brainres.2010.09.033Search in Google Scholar PubMed

Zhang, K., Zeng, Y., Song, C., Fu, Y., and Wan, Q. (2010). The comparison of clonidine, arginine and both combined: a growth hormone stimulation test to differentiate multiple system atrophy from idiopathic Parkinson’s disease. J. Neurol. 257, 1486–1491.10.1007/s00415-010-5556-xSearch in Google Scholar PubMed

Received: 2014-3-12
Accepted: 2014-4-25
Published Online: 2014-5-27
Published in Print: 2014-10-1

©2014 by De Gruyter

Downloaded on 27.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2014-0023/html
Scroll to top button