An Update on CSF Biomarkers of Parkinson's Disease

Advances in Predictive, Preventive and Personalised Medicine

Volumn 3, Issue , 2013, Pages 161-184

  LeWitt, Peter A ^a,b   Huber, Bertraand R ^c   Zhang, Jing ^d  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Disease monitoring; Disease specific biomerker; Molecular mechanism; Neuroprotecton; Parkinson's disease; Person at risk; Personalized medicine; Population screening; Predictive diagnostics; Tailored treatment

Indexed keywords

3 O METHYLDOPA; 3 O METHYLDOPAMINE; 3, 4 DIHYDROXYPHENYLACETIC ACID; 4 AMINOBUTYRIC ACID; ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN [1-42]; BIOLOGICAL MARKER; CHOLECYSTOKININ; DOPAMINE; DOPAMINE 3 SULFATE; ENKEPHALIN; GLUTATHIONE; LEVODOPA; METAL ION; MISCELLANEOUS DRUGS AND AGENTS; NEUROTRANSMITTER; SOMATOSTATIN; TAU PROTEIN; UNCLASSIFIED DRUG;

CEREBROSPINAL FLUID; DISEASE DURATION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNOREACTIVITY; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; NERVE DEGENERATION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 84886377955     PISSN: 22113495     EISSN: 22113509     Source Type: Book Series    
DOI: 10.1007/978-94-007-5866-7_8     Document Type: Review

References (125)

1. Graeber MB (2009) Biomarkers for Parkinson's disease. Exp Neurol 216: 249-253.
2. Antoniades CA, Barker RA (2008) The search for biomarkers in Parkinson's disease: a critical review. Expert Rev Neurother 8: 1841-1852.
3. Sherer TB (2011) Biomarkers for Parkinson's disease. Sci Transl Med 3: 79ps14.
4. Chahine LM, Stern MB (2011) Diagnostic markers for Parkinson's disease. Curr Opin Neurol 24: 309-317.
5. Gerlach M, Maetzler W, Broich K, Hampel H, Rems L, Reum T, Riederer P, Stöffler A, Streffer J, Berg D (2012) Biomarker candidates of neurodegeneration in Parkinson's disease for the evaluation of disease-modifying therapeutics. J Neural Transm 119: 39-52.
6. Eckstein JW (2010) Biomarkers in Parkinson's disease: a venture capitalists's perspective. Biomark Med 4: 731-735.
7. LeWitt PA, Galloway MP (1990) Neurochemical markers of Parkinson's disease. In: Koller WC, Paulson G (eds) Therapy of Parkinson's disease. Marcel Dekker, New York, pp 63-93.
8. Hornykiewicz O (1998) Biochemical aspects of Parkinson's disease. Neurology 51(suppl 2): S2-S9.
9. Goldstein DS, Holmes C, Sharabi Y (2012) Cerebrospinal fluid biomarkers of central catecholamine deficiency in Parkinson's disease and other synucleinopathies. Brain 135: 1900-1913.
10. LeWitt PA, Galloway MP, Matson W, Milbury P, McDermott M, Srivastava DK, Oakes D (1992) Markers of dopamine metabolism in Parkinson's disease. Neurology 42: 2111-2117.
11. Parkinson Study Group (1995) CSF homovanillic acid in the DATATOP study on Parkinson's disease. Arch Neurol 52: 237-245.
12. Ruberg M, Javoy-Agid F, Hirsch E, Scatton B, LHeureux R, Hauw JJ, Duyckaerts C, Gray F, Morel-Maroger A, Rascol A, Serdaru M, Agid Y (1985) Dopaminergic and cholinergic lesions in progressive supranuclear palsy. Ann Neurol 18: 523-529.
13. Abdo WF, de Jong D, Hendriks JC, Horstink MW, Kremer BP, Bloem BR, Verbeek MM (2004) Cerebrospinal fluid analysis differentiates multiple system atrophy from Parkinson's disease. Mov Disord 19: 571-579.
14. Kanemaru K, Mitani K, Yamanouchi H (1998) Cerebrospinal fluid homovanillic acid levels are not reduced in early corticobasal degeneration. Neurosci Lett 245: 121-122.
15. Hildebrand J, Bourgeois F, Buyse M, Przedborski S, Goldman S (1990) Reproducibility of monoamine metabolite measurements in human cerebrospinal fluid. Acta Neurol Scand 81: 427-430.
16. Toghi H, Abe T, Takahashi S, Ueno M, Nozaki Y (1990) Cerebrospinal fluid dopamine, norepinephrine, and epinephrine concentrations correlated with clinical symptoms. Adv Neurol 53: 277-282.
17. Poseta JS, Parsons L, Engelland S, Kripke DF (2009) Circadian rhythm of CSF monoamines and hypocretin-1 in restless leg syndrome and Parkinson's disease. Sleep Med 10: 129-133.
18. Ishibashi K, Kanemaru K, Saito Y, Murayama S, Oda K, Ishiwata K, Mizusawa H, Ishii K (2010) Cerebropinal fluid metabolite and nigrostriatal dopaminergic function in Parkinson's disease. Acta Neurol Scand 122: 46-51.
19. Goldstein DS, Holmes C, Kopin IJ, Sharabi Y (2011) Intra-neuronal vesicular uptake of catecholamines is decreased in patients with Lewy body diseases. J Clin Invest 121: 3320-3330.
20. Loeffler DA, LeWitt PA, Juneau PL, Camp DM, DeMaggio AJ, Milbury P, Matson WR, Rathbone MP (1998) Altered guanosine and guanine concentrations in rabbit striatum following increased dopamine turnover. Brain Res Bull 45: 297-299.
21. Ascherio A, LeWitt PA, Xu K, Eberly S, Watts A, Matson WR, Marras C, Kieburtz K, Rudolph A, Bogdanov MB, Schwid SR, Tennis M, Tanner CM, Beal MF, Lang AE, Oakes D, Fahn S, Shoulson I, Schwarzschild MA; Parkinson Study Group DATATOP Investigators (2009) Urate as a predictor of the rate of clinical decline in Parkinson disease. Arch Neurol 66: 1460-1468.
22. LeWitt P, Schultz L, Auinger P, LuM; Parkinson Study Group DATATOP Investigators (2011) CSF xanthine, homovanillic acid, and their ratio as biomarkers of Parkinson's disease. Brain Res 1408: 88-97.
23. Mayeux R, Stern Y, Cote L, Williams JB (1984) Altered serotonin metabolism in depressed patients with Parkinson's disease. Neurology 34: 642-646.
24. Toghi H, Abe T, Takahashi S, Takahashi J, Hamato H (1993) Concentrations of serotonin and its related substances in the cerebrospinal fluid of Parkinsonian patients and their relations to the severity of symptoms. Neurosci Lett 150: 71-74.
25. LeWitt PA, Miller LP, Newman RP, Burns RS, Insel T, Levine RA, Lovenberg W, Calne DB (1984) Tyrosine hydroxylase cofactor (tetrahydrobiopterin) in Parkinsonism. Adv Neurol 40: 459-462.
26. Abe T, Isobe C, Murata T, Sato C, Toghi H (2003) Alteration of 8-hydroxyguanosine concentrations in the cerebrospinal fluid and serum from patients with Parkinson's disease. Neurosci Lett 336: 105-108.
27. Boll M-C, Alcaraz-Zubeldia M, Montes S, Rios C (2008) Free copper, ferroxidase and SOD1 activities, lipid peroxidation and NOx content in the CSF, a different marker profile in four neurodegenerative diseases. Neurochem Res 33: 1717-1723.
28. Konings CH, Kuiper MA, Teerlink T, Mulder C, Scheltens P, Wolters EC (1999) Normal cerebrospinal fluid glutathione concentrations in Parkinson's disease, Alzheimer's disease, and multiple system atrophy. J Neurol Sci 168: 112-115.
29. LeWitt PA, Lu M, Poisson L, Beach T, Adler C, Guo L (2011) PD biomarker search: metabolomic analysis of post-mortem CSF. Mov Disord 26(suppl 2): S193.
30. Maetzler W, Schmid SP, Wurster I, Liepelt I, Gaenslen A, Gasser T, Berg D (2011) Reduced but not oxidized cerebrospinal fluid glutathione levels are lowered in Lewy body diseases. Mov Disord 26: 176-181.
31. Buhmann C, Arlt S, Kontush A, Möller-Bertram T, Sperber S, Oechsner M, Stuerenburg HJ, Beisiegel U (2004) Plasma and CSF markers of oxidative stress are increased in Parkinson's disease and influenced by antiparkinsonian medication. Neurobiol Dis 15: 160-170.
32. Cheng F-C, Kuo J-S, Chia L-G, Dryhurst G (1996) Elevated 5-S-cysteinyldopamine/homovanillic acid ratio and reduced homovanillic acid in cerebrospinal fluid: possible markers for and potential insights into the pathophysiology of Parkinson's disease. J Neural Transm 103: 433-446.
33. Gjessing LR, Gjesdahl P, Dietrichson P, Presthuis J (1974) Free amino acids in the cerebrospinal fluid in old age and in Parkinson's disease. Eur Neurol 12: 33-37.
34. Araki K, Takino T, Ida S, Kuriyama K (1986) Alteration of amino acids in cerebrospinal fluid from patients with Parkinson's disease and spinocerebellar degeneration. Acta Neurol Scand 71: 105-110.
35. Manyam BV, Ferraro TN, Hare TA (1988) Cerebrospinal fluid amino compounds in Parkinson's disease: alterations due to carbidopa/levodopa. Arch Neurol 45: 48-50.
36. Molina JA, Jiménez-Jiménez FJ, Gomez P, Vargas C, Navarro JA, Ortí-Pareja M, Gasalla T, Benito-Léon J, Bermejo F, Arenas J (1997) Decreased cerebrospinal fluid levels of neutral and basic amino acids in patients with Parkinson's disease. J Neurol Sci 150: 123-127.
37. Hare TA, Beasley BL, Chambers RA, Boehme DH, Vogel WH (1973) GABA and amino acid levels in plasma and cerebrospinal fluid of patients with Parkinson's disease before and during treatment with L-DOPA. Clin Chim Acta 45: 273-280.
38. Mally J, Szalai G, Stone TW (1997) Changes in the concentration of amino acids in serum and cerebrospinal fluid of patients with Parkinson's disease. J Neurol Sci 151: 159-162.
39. Kornhuber J, Kornhuber ME, Hartmann GM, Kornhuber AW (1988) In vivo influences on CSF amino acids. Neurochem Int 12: 25-31.
40. Pall HS, Williams AC, Blake DR, Lunec J, Gutteridge JM, Hall M, Taylor A (1987) Raised cerebrospinal fluid copper concentration in Parkinson's disease. Lancet 2: 238-241.
41. Hozumi I, Hasegawa T, Honda A, Ozawa K, Hayashi Y, Hashimoto K, Yamada M, Koumura A, Sakurai T, Kimura A, Tanaka Y, Satoh M, Inuzuka T (2011) Patterns of levels of biological metals in CSF differ among neurodegenerative diseases. J Neurol Sci 2011(303): 95-99.
42. Alimonti A, Bocca B, Pino A, Ruggieri F, Forte G, Sancesario G (2007) Elemental profile of cerebrospinal fluid in patients with Parkinson's disease. J Trace Elem Med Biol 21: 234-241.
43. Bocca B, Alimonti A, Senofonte O, Pino A, Violante N, Petrucci F, Sancesario G, Forte G (2006) Metal changes in CSF and peripheral compartments of parkinsonian patients. J Neurol Sci 248: 23-30.
44. Lee PH, Lee G, PaikM-J (2008) Polyunsaturated fatty acid concentrations polyamine patterns in the cerebrospinal fluid of patients with Parkinson's disease and multiple system atrophy. Mov Disord 23: 309-310.
45. Paik M-J, Ahn Y-H, Lee PH, Kang H, Park CB, Choi S, Lee G (2010) Polyamine patterns in the cerebrospinal fluid of patients with Parkinson's disease and multiple system atrophy. Clin Chim Acta 411: 1532-1535.
46. Maruyama W, Abe T, Toghi H, Dostert P, Naoi M (1996) A dopaminergic neurotoxin, N-methyl(R)salsalinol, increases in parkinsonian CSF. Ann Neurol 40: 119-122.
47. Maruyama W, Abe T, Toghi H, Naoi M (1999) An endogenous MPTP-like dopaminergic neurotoxin, N-methyl(R)salsalinol, in the cerebrospinal fluid decreases with progression of Parkinson's disease. Neurosci Lett 262: 13-16.
48. Zhou G, Shoji H, Yamada S, Matsuishi T (1997) Decreased beta-phenylethylamine in CSF in Parkinson's disease. J Neurol Neurosurg Psychiatry 63: 754-758.
49. CaudleWM, Bammler TK, Lin Y, Pan S, Zhang J (2010) Using 'omics' to define pathogenesis and biomarkers of Parkinson's disease. Expert Rev Neurother 10: 925-942.
50. Cohen P (2000) The regulation of protein function by multisite phosphorylation-a 25 year update. Trends Biochem Sci 25: 596-601.
51. Silverberg GD, Mayo M, Saul T, Rubenstein E, McGuire D (2003) Alzheimer's disease, normal-pressure hydrocephalus, and senescent changes in CSF circulatory physiology: a hypothesis. Lancet Neurol 2: 506-511.
52. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Mutation in the '-synuclein gene Identified in families with Parkinson's disease. Science 276: 2045-2047.
53. Braak H, Braak E, Yilmazer D, Schultz C, de Vos RA, Jansen EN (1995) Nigral and extranigral pathology in Parkinson's disease. J Neural Transm Suppl 46: 15-31.
54. Forno LS (1996) Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 55: 259-272.
55. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD (1990) Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54: 823-827.
56. Schapira AH, Cooper JM, Dexter D, Jenner P, Clark JB, Marsden CD (1989) Mitochondrial complex I deficiency in Parkinson's disease. Lancet 333: 1269.
57. Devi L, Raghavendran V, Prabhu BM, Avadhani NG, Anandatheerthavarada HK (2008) Mitochondrial import and accumulation of '-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J Biol Chem 283: 9089-9100.
58. Su X, Maguire-Zeiss KA, Giuliano R, Prifti L, Venkatesh K, Federoff HJ (2008) Synuclein activates microglia in a model of Parkinson's disease. Neurobiol Aging 29: 1690-1701.
59. Zhang W, Wang T, Pei Z, Miller D, Wu X, Block M, Wilson B, Zhang W, Zhou Y, Hong J, Zhang J (2005) Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J 19: 533-542.
60. Aleyasin H, Rousseaux MW, Marcogliese PC, Hewitt SJ, Irrcher I, Joselin AP, Parsanejad M, Kim RH, Rizzu P, Callaghan SM, Slack RS, Mak TW, Park DS (2010) DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc Natl Acad Sci U S A 107: 3186-3191.
61. Duan X, Kelsen SG, Merali S (2008) Proteomic analysis of oxidative stress-responsive proteins in human pneumocytes: insight into the regulation of DJ-1 expression. J Proteome Res 7: 4955-4961.
62. Jin J, Li GJ, Davis J, Zhu D, Wang Y, Pan C, Zhang J (2007) Identification of novel proteins associated with both alpha-synuclein and DJ-1. Mol Cell Proteomics 6: 845-859.
63. Hong Z, Shi M, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Leverenz JB, Baird G, Montine TJ, Hancock AM, Hwang H, Pan C, Bradner J, Kang UJ, Jensen PH, Zhang J (2010) DJ-1 and alpha-synuclein in human cerebrospinal fluid as biomarkers of Parkinson's disease. Brain 133: 713-726.
64. Mollenhauer B, Locascio JJ, Schulz-Schaeffer W, Sixel-Döring F, Trenkwalder C, Schlossmacher MG (2011) '-Synuclein and tau concentrations in cerebrospinal fluid of patients presenting with parkinsonism: a cohort study. Lancet Neurol 10: 230-240.
65. Mollenhauer B, Cullen V, Kahn I, Krastins B, Outeiro TF, Pepivani I, Ng J, Schulz-Schaeffer W, Kretzschmar HA, McLean PJ, Trenkwalder C, Sarracino DA, Vonsattel JP, Locascio JJ, El-Agnaf OM, Schlossmacher MG (2008) Direct quantification of CSF alpha-synuclein by ELISA and first cross-sectional study in patients with neurodegeneration. Exp Neurol 213: 315-325.
66. Shi M, Bradner J, Hancock AM, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Kim HM, Leverenz JB, Montine TJ, Ginghina C, Kang UJ, Cain KC, Wang Y, Aasly J, Goldstein D, Zhang J (2011) Cerebrospinal fluid biomarkers for Parkinson disease diagnosis and progression. Ann Neurol 69: 570-580.
67. Ohrfelt A, Grognet P, Andreasen N, Wallin A, Vanmechelen E, Blennow K, Zetterberg H (2009) Cerebrospinal fluid alpha-synuclein in neurodegenerative disorders-a marker of synapse loss? Neurosci Lett 450: 332-335.
68. Borghi R, Marchese R, Negro A, Marinelli L, Forloni G, Zaccheo D, Abbruzzese G, Tabaton M (2000) Full length alpha-synuclein is present in cerebrospinal fluid from Parkinson's disease and normal subjects. Neurosci Lett 287: 65-67.
69. Mollenhauer B, El-Agnaf OM, Marcus K, Trenkwalder C, Schlossmacher MG (2010) Quantification of '-synuclein in cerebrospinal fluid as a biomarker candidate: review of the literature and considerations for future studies. Biomark Med 4: 683-699.
70. Park MJ, Cheon SM, Bae HR, Kim SH, Kim JW (2011) Elevated levels of '-synuclein oligomer in the cerebrospinal fluid of drug-naive patients with Parkinson's disease. J Clin Neurol 7: 215-222.
71. Wang Y, Shi M, Chung KA, Zabetian CP, Leverenz JB, Berg D, Srulijes K, Trojanowski JQ, Lee VM-Y, Siderowf AD, Hurtig H, Litvan I, SchiessMC, Peskind ER, Masuda M, Hasegawa M, Lin X, Pan C, Galasko D, Goldstein DS, Jensen PH, Yang H, Cain KC, Zhang J (2012) Phosphorylated '-synuclein in Parkinson's disease. Sci Transl Med 4(121): 121ra120.
72. Maita C, Tsuji S, Yabe I, Hamada S, Ogata A, Maita H, Iguchi-Ariga SM, Sasaki H, Ariga H (2008) Secretion of DJ-1 into the serum of patients with Parkinson's disease. Neurosci Lett 431: 86-89.
73. Waragai M, Wei J, Fujita M, Nakai M, Ho GJ, Masliah E, Akatsu H, Yamada T, Hashimoto M (2006) Increased level of DJ-1 in the cerebrospinal fluids of sporadic Parkinson's disease. Biochem Biophys Res Commun 345: 967-972.
74. Inden M, Kitamura Y, Takahashi K, Takata K, Ito N, Niwa R, Funayama R, Nishimura K, Taniguchi T, Honda T, Taira T, Ariga H (2011) Protection against dopaminergic neurodegeneration in Parkinson's disease-model animals by a modulator of the oxidized form of DJ-1, a wild-type of familial Parkinson's disease-linked PARK7. J Pharmacol Sci 2011(117): 189-203.
75. Saito Y, Hamakubo T, Yoshida Y, Ogawa Y, Hara Y, Fujimura H, Imai Y, Iwanari H, Mochizuki Y, Shichiri M, Nishio K, Kinumi T, Noguchi N, Kodama T, Niki E (2009) Preparation and application of monoclonal antibodies against oxidized DJ-1. Significant elevation of oxidized DJ-1 in erythrocytes of early-stage Parkinson disease patients. Neurosci Lett 465: 1-5.
76. Ren H, Fu K, Wang D, Mu C, Wang G (2011) Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL. J Biol Chem 286: 35308-35317.
77. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, Beecham GW, Wang L, Züchner S, Konidari I, Wang G, Singer C, Nahab F, Scott B, Stajich JM, Pericak-Vance M, Haines J, Vance JM, Martin ER (2010) Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 74: 97-109.
78. Hamza TH, Zabetian CP, Tenesa A, Laederach A, Montimurro J, Yearout D, Kay DM, Doheny KF, Paschall J, Pugh E, Kusel VI, Collura R, Roberts J, Griffith A, Samii A, Scott WK, Nutt J, Factor SA, Payami H (2010) Common genetic variation in the HLA region is associated with late-onset sporadic Parkinson's disease. Nat Genet 42: 781-785.
79. Pankratz N, Wilk JB, Latourelle JC, DeStefano AL, Halter C, Pugh EW, Doheny KF, Gusella JF, Nichols WC, Foroud T, Myers RH; PSG-PROGENI and GenePD Investigators, Coordinators and Molecular Genetic Laboratories (2009) Genomewide association study for susceptibility genes contributing to familial Parkinson disease. Hum Genet 124: 593-605.
80. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, Kubo M, Kawaguchi T, Tsunoda T, Watanabe M, Takeda A, Tomiyama H, Nakashima K, Hasegawa K, Obata F, Yoshikawa T, Kawakami H, Sakoda S, Yamamoto M, Hattori N, Murata M, Nakamura Y, Toda T (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 41: 1303-1307.
81. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D, Paisan-Ruiz C, Lichtner P, Scholz SW, Hernandez DG, Krüger R, Federoff M, Klein C, Goate A, Perlmutter J, Bonin M, Nalls MA, Illig T, Gieger C, Houlden H, Steffens M, Okun MS, Racette BA, Cookson MR, Foote KD, Fernandez HH, Traynor BJ, Schreiber S, Arepalli S, Zonozi R, Gwinn K, van der Brug M, Lopez G, Chanock SJ, Schatzkin A, Park Y, Hollenbeck A, Gao J, Huang X, Wood NW, Lorenz D, Deuschl G, Chen H, Riess O, Hardy JA, Singleton AB, Gasser T (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 41: 1308-1312.
82. Hampel H, Bürger K, Teipel SJ, Bokde AL, Zetterberg H, Blennow K (2008) Core candidate neurochemical and imaging biomarkers of Alzheimer's disease. Alzheimers Dement 4: 38-48.
83. Jellinger KA (2003) Neuropathological spectrum of synucleinopathies. Mov Disord 18(Suppl 6): S2-S12.
84. Litvan I, Halliday G, Hallett M, Goetz CG, Rocca W, Duyckaerts C, Ben-Shlomo Y, Dickson DW, Lang AE, Chesselet MF, Langston WJ, Di Monte DA, Gasser T, Hagg T, Hardy J, Jenner P, Melamed E, Myers RH, Parker D Jr, Price DL (2007) The etiopathogenesis of Parkinson disease and suggestions for future research. Part I. J Neuropathol Exp Neurol 66: 251-257.
85. Montine TJ, Shi M, Quinn JF, Peskind ER, Craft S, Ginghina C, Chung KA, Kim H, Galasko DR, Jankovic J, Zabetian CP, Leverenz JB, Zhang J (2010) CSF A"42 and tau in Parkinson's disease with cognitive impairment. Mov Disord 25: 2682-2685.
86. Aasly JO, Shi M, Sossi V, Stewart T, Johansen KK, Wszolek ZK, Uitti RJ, Hasegawa K, Yokoyama T, Zabetian CP, Kim HM, Leverenz JB, Ginghina C, Armaly J, Edwards KL, Snapinn KW, Stoessl AJ, Zhang J (2012) Cerebrospinal fluid amyloid " and tau in LRRK2 mutation carriers. Neurology 78: 55-61.
87. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T (1994) Interleukin-1", interleukin-6, epidermal growth factor and transforming growth factor-' are elevated in the brain from parkinsonian patients. Neurosci Lett 180: 147-150.
88. Mogi M, Harada M, Narabayashi H, Inagaki H, Minami M, Nagatsu T (1996) Interleukin (IL)-1", IL-2, IL-4, IL-6 and transforming growth factor-' levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease. Neurosci Lett 211: 13-16.
89. Mogi M, Harada M, Riederer P, Narabayashi H, Fujita K, Nagatsu T (1994) Tumor necrosis factor-' (TNF-') increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett 165: 208-210.
90. Nagatsu T, Mogi M, Ichinose H, Togari A (2000) Cytokines in Parkinson's disease. In: Mizuno Y, Calne DB, Horowski R, Poewe W, Riederer P, Youdim MBH (eds) Advances in Research on Neurodegeneration. Springer, Vienna, pp 143-151.
91. Pabon MM, Bachstetter AD, Hudson CE, Gemma C, Bickford PC (2011) CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J Neuroinflammation 8: 9.
92. Nilsson C, Lindvall-Axelsson M, Owman C (1992) Neuroendocrine regulatory mechanisms in the choroid-plexus cerebrospinal-fluid system. Brain Res Rev 17: 109-138.
93. Vigh B, Marzano e Silva MJ, Frank CL, Vincze C, Czirok SJ, Szabo A, Lukats A, Szel A (2004) The system of cerebrospinal fluid-contacting neurons: its supposed role in the nonsynaptic signal transmission of the brain. Histol Histopathol 19: 607-628.
94. Ly L, Wasinger VC (2011) Protein and peptide fractionation, enrichment and depletion: tools for the complex proteome. Proteomics 11: 513-534.
95. Domon B, Aebersold R (2006) Mass spectrometry and protein analysis. Science 312: 212-217.
96. Senko MW, Hendrickson CL, Emmett MR, Shi SDH, Marshall AG (1997) External accumulation of ions for enhanced electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. J Am Soc Mass Spectrom 8: 970-976.
97. Hardman M, Makarov AA (2003) Interfacing the Orbitrap mass analyzer to an electrospray ion source. Anal Chem 75: 1699-1705.
98. Medzihradszky KF, Campbell JM, Baldwin MA, Falick AM, Juhasz P, Vestal ML, Burlingame AL (2000) The characteristics of peptide collision-induced dissociation using a high-performance MALDI-TOF/TOF tandem mass spectrometer. Anal Chem 72: 552-558.
99. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM (1989) Electrospray ionization for mass spectrometry of large biomolecules. Science 246: 64-71.
100. Karas M, Hillenkamp F (1988) Laser desorption ionization of proteins with molecular masses exceeding 10, 000 daltons. Anal Chem 60: 2299-2301.
101. Syka JE, Coon JJ, Schroeder MJ, Shabanowitz J, Hunt DF (2004) Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Nat Acad Sci U S A 101: 9528-9533.
102. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494.
103. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17: 994-999.
104. Hsu JL, Huang SY, Chen SH (2006) Dimethyl multiplexed labeling combined with microcolumn separation and MS analysis for time course study in proteomics. Electrophoresis 27: 3652-3660.
105. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using aminereactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
106. Yao X, Afonso C, Fenselau C (2003) Dissection of proteolytic 18O labeling: endoproteasecatalyzed 16O-to-18O exchange of truncated peptide substrates. J Proteome Res 2: 147-152.
107. May D, Fitzgibbon M, Liu Y, Holzman T, Eng J, Kemp CJ, Whiteaker J, Paulovich A, McIntosh M (2007) A platform for accurate mass and time analyses of mass spectrometry data. J Proteome Res 6: 2685-2694.
108. Mueller LN, Rinner O, Schmidt A, Letarte S, Bodenmiller B, Brusniak MY, Vitek O, Aebersold R, Muller M (2007) SuperHirn-a novel tool for high resolution LC-MS-based peptide/protein profiling. Proteomics 7: 3470-3480.
109. Liu H, Sadygov RG, Yates JR 3rd (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76: 4193-4201.
110. Zybailov BL, Florens L, Washburn MP (2007) Quantitative shotgun proteomics using a protease with broad specificity and normalized spectral abundance factors. Mol Biosyst 3: 354-360.
111. Pan S, Rush J, Peskind ER, Galasko D, Chung K, Quinn J, Jankovic J, Leverenz JB, Zabetian C, Pan C, Wang Y, Oh JH, Gao J, Zhang J, Montine T, Zhang J (2008) Application of targeted quantitative proteomics analysis in human cerebrospinal fluid using a liquid chromatography matrix-assisted laser desorption/ionization time-of-flight tandem mass spectrometer (LC MALDI TOF/TOF) platform. J Proteome Res 7: 720-730.
112. Abdi F, Quinn JF, Jankovic J, McIntosh M, Leverenz JB, Peskind E, Nixon R, Nutt J, Chung K, Zabetian C, Samii A, Lin M, Hattan S, Pan C, Wang Y, Jin J, Zhu D, Li GJ, Liu Y, Waichunas D, Montine TJ, Zhang J (2006) Detection of biomarkers with a multiplex quantitative proteomic platform in cerebrospinal fluid of patients with neurodegenerative disorders. J Alzheimers Dis 9: 293-348.
113. Pan S, Zhu D, Quinn JF, Peskind ER, Montine TJ, Lin B, Goodlett DR, Taylor G, Eng J, Zhang J (2007) A combined dataset of human cerebrospinal fluid proteins identified by multidimensional chromatography and tandem mass spectrometry. Proteomics 7: 469-473.
114. Harrington M, Fonteh A, Oborina E, Liao P, Cowan R, McComb G, Chavez J, Rush J, Biringer R, Huhmer A (2009) The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid. Cerebrospinal Fluid Res 6: 10.
115. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation-association of plasma-membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420.
116. Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579.
117. Ecroyd H, Sarradin P, Dacheux JL, Gatti JL (2004) Compartmentalization of prion isoforms within the reproductive tract of the ram. Biol Reprod 71: 993-1001.
118. Vingtdeux V, Hamdane M, Loyens A, Gele P, Drobeck H, Begard S, Galas MC, Delacourte A, Beauvillain JC, Buee L, Sergeant N (2007) Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J Biol Chem 282(25): 18197-18205.
119. El-Agnaf OM, Salem SA, Paleologou KE, Cooper LJ, Fullwood NJ, Gibson MJ, Curran MD, Court JA, Mann DMA, Ikeda S, Cookson MR, Hardy J, Allsop D (2003) Alpha-synuclein implicated in Parkinson's disease is present in extracellular biological fluids, including human plasma. FASEB J 17: 1945-1947.
120. Liu J, Zhang JP, Shi M, Quinn T, Bradner J, Beyer R, Chen S, Zhang J (2009) Rab11a and HSP90 regulate recycling of extracellular alpha-synuclein. J Neurosci 29: 1480-1485.
121. Zhang J, Sokal I, Peskind ER, Quinn JF, Jankovic J, Kenney C, Chung KA, Millard SP, Nutt JG, Montine TJ (2008) CSF multianalyte profile distinguishes Alzheimer and Parkinson diseases. Am J Clin Pathol 129: 526-529.
122. Selvaraju S, El Rassi ZE (2012) Liquid-phase-based separation systems for depletion, prefractionation and enrichment of proteins in biological fluids and matrices for in-depth proteomics analysis-an update covering the period 2008-2011. Electrophoresis 33: 74-88.
123. Lehnert S, Jesse S, Rist W, Steinacker P, Soininen H, Herukka S-K, Tumani H, Lenter M, Oeckl P, Ferger B, Hengerer B, Otto M (2012) iTRAQ and multiple reaction monitoring as proteomic tools for biomarker search in cerebrospinal fluid of patients with Parkinson's disease dementia. Exp Neurol 234: 499-505.
124. Breen DP, Michell AW, Barker RA (2011) Parkinson's disease-the continuing search for biomarkers. Clin Chem Lab Med 49: 393-401.
125. Hughes AJ, Daniel SE, Ben-Shlomo Y, Lees AJ (2002) The accuracy of diagnosis of parkinsonian syndromes in a specialist movement disorder service. Brain 125: 861-870.