Premotor biomarkers for Parkinson's disease - a promising direction of research

Translational Neurodegeneration

Volumn 1, Issue , 2012, Pages

  Haas, Brian R ^a   Stewart, Tessandra H ^a   Zhang, Jing ^a  

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

Author keywords

synuclein; Biochemical markers; Clinical biomarkers; CSF; DJ 1; GBA; LRRK2; Neuroimaging; parkin; Parkinson's disease; Premotor

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN[1-42]; BIOLOGICAL MARKER; DJ 1 PROTEIN; GLUCOSYLCERAMIDASE; LEUCINE RICH REPEAT KINASE 2; PARKIN; TAU PROTEIN; URIC ACID;

BEHAVIOR DISORDER; BIOCHEMISTRY; DISEASE ASSOCIATION; DISEASE MARKER; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE; GENE MUTATION; GENETIC ASSOCIATION; GENETIC MARKER; GLUCOCEREBROSIDASE GENE; HETEROZYGOTE; HUMAN; INTESTINE FUNCTION DISORDER; LEUCINE REPEAT KINASE 2 GENE; MOTOR DYSFUNCTION; NEUROIMAGING; NONHUMAN; OLFACTORY NERVE DISEASE; OXIDATIVE STRESS; PARKIN GENE; PARKINSON DISEASE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN EXPRESSION; REM SLEEP; REVIEW;

EID: 84881124213     PISSN: None     EISSN: 20479158     Source Type: Journal    
DOI: 10.1186/2047-9158-1-11     Document Type: Review

References (144)

1. Thomas B, Beal MF. Parkinson's disease. Hum Mol Genet 2007, 16:R183-194. Spec No. 2. England, 10.1093/hmg/ddm159, 17911161.
2. Cookson MR. The biochemistry of Parkinson's disease. Annu Rev Biochem 2005, 74:29-52. 10.1146/annurev.biochem.74.082803.133400, 15952880.
3. Robinson P. Understanding the molecular basis of Parkinson's disease, identification of biomarkers and routes to therapy. Expert Rev Proteomics 2010, 7:565-578. 10.1586/epr.10.40, 20653510.
4. Morgan JC, Mehta SH, Sethi KD. Biomarkers in Parkinson's disease. Curr Neurol Neurosci Rep 2010, 10:423-430. 10.1007/s11910-010-0144-0, 20809400.
5. Fahn S, Oakes D, Shoulson I, Kieburtz K, Rudolph A, Lang A, Olanow CW, Tanner C, Marek K. Levodopa and the progression of Parkinson's disease. In N Engl J Med 2004, 351:2498-2508. United States: 2004 Massachusetts Medical Society.
6. Meara J, Bhowmick BK, Hobson P. Accuracy of diagnosis in patients with presumed Parkinson's disease. Age Ageing 1999, 28:99-102. 10.1093/ageing/28.2.99, 10350403.
7. Shults CW. Lewy bodies. Proc Natl Acad Sci USA 2006, 103:1661-1668. 10.1073/pnas.0509567103, 1413649, 16449387.
8. Fearnley JM, Lees AJ. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114(Pt 5):2283-2301.
9. Bohnen NI, Albin RL, Koeppe RA, Wernette KA, Kilbourn MR, Minoshima S, Frey KA. Positron emission tomography of monoaminergic vesicular binding in aging and Parkinson disease. J Cereb Blood Flow Metab 2006, 26:1198-1212.
10. Ferrer I, Martinez A, Blanco R, Dalfó E, Carmona M. Neuropathology of sporadic Parkinson disease before the appearance of parkinsonism: preclinical Parkinson disease. J Neural Transm 2011, 118:821-839. 10.1007/s00702-010-0482-8, 20862500.
11. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 1973, 20:415-455. 10.1016/0022-510X(73)90175-5, 4272516.
12. Kish SJ, Shannak K, Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 1988, 318:876-880. 10.1056/NEJM198804073181402, 3352672.
13. Hornykiewicz O. Biochemical aspects of Parkinson's disease. Neurology 1998, 51:S2-9.
14. Downing GJ, . National Institutes of Health (U.S.), United States Food and Drug Administration.: Biomarkers and surrogate endpoints : clinical research and applications : proceedings of the NIH-FDA conference held on 15-16 April 1999 in Bethesda, Maryland, USA 2000, Elsevier, Amsterdam, 1, National Institutes of Health (U.S.), United States.
15. Breen DP, Michell AW, Barker RA. Parkinson's disease - the continuing search for biomarkers. Clin Chem Lab Med 2011, 49:393-401.
16. Olson EJ, Boeve BF, Silber MH. Rapid eye movement sleep behaviour disorder: demographic, clinical and laboratory findings in 93 cases. Brain 2000, 123(Pt 2):331-339.
17. Savica R, Rocca WA, Ahlskog JE. When does Parkinson disease start?. Arch Neurol 2010, 67:798-801. 10.1001/archneurol.2010.135, 20625084.
18. Monderer R, Thorpy M. Sleep disorders and daytime sleepiness in Parkinson's disease. Curr Neurol Neurosci Rep 2009, 9:173-180. 10.1007/s11910-009-0026-5, 19268041.
19. Postuma RB, Gagnon JF, Vendette M, Fantini ML, Massicotte-Marquez J, Montplaisir J. Quantifying the risk of neurodegenerative disease in idiopathic REM sleep behavior disorder. Neurology 2009, 72:1296-1300. 2828948, 19109537.
20. Wu Y, Le W, Jankovic J. Preclinical biomarkers of Parkinson disease. Arch Neurol 2011, 68:22-30. 10.1001/archneurol.2010.321, 21220674.
21. Postuma RB, Gagnon JF, Rompré S, Montplaisir JY. Severity of REM atonia loss in idiopathic REM sleep behavior disorder predicts Parkinson disease. Neurology 2010, 74:239-244. 10.1212/WNL.0b013e3181ca0166, 2872606, 20083800.
22. Mostile G, Jankovic J. Treatment of dysautonomia associated with Parkinson's disease. Parkinsonism Relat Disord 2009, 15(Suppl 3):S224-232.
23. Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, Curb JD, Grandinetti A, Blanchette PL, Popper JS, Ross GW. Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 2001, 57:456-462. 10.1212/WNL.57.3.456, 11502913.
24. Savica R, Carlin JM, Grossardt BR, Bower JH, Ahlskog JE, Maraganore DM, Bharucha AE, Rocca WA. Medical records documentation of constipation preceding Parkinson disease: A case-control study. Neurology 2009, 73:1752-1758. 10.1212/WNL.0b013e3181c34af5, 2788809, 19933976.
25. Ponsen MM, Stoffers D, Booij J, van Eck-Smit BL, Wolters E, Berendse HW. Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Ann Neurol 2004, 56:173-181. 10.1002/ana.20160, 15293269.
26. Doty RL, Bromley SM, Stern MB. Olfactory testing as an aid in the diagnosis of Parkinson's disease: development of optimal discrimination criteria. Neurodegeneration 1995, 4:93-97. 10.1006/neur.1995.0011, 7600189.
27. Silveira-Moriyama L, Petrie A, Williams DR, Evans A, Katzenschlager R, Barbosa ER, Lees AJ. The use of a color coded probability scale to interpret smell tests in suspected parkinsonism. Mov Disord 2009, 24:1144-1153. 10.1002/mds.22494, 19370732.
28. Müller A, Reichmann H, Livermore A, Hummel T. Olfactory function in idiopathic Parkinson's disease (IPD): results from cross-sectional studies in IPD patients and long-term follow-up of de-novo IPD patients. J Neural Transm 2002, 109:805-811. 10.1007/s007020200067, 12111470.
29. Herting B, Schulze S, Reichmann H, Haehner A, Hummel T. A longitudinal study of olfactory function in patients with idiopathic Parkinson's disease. J Neurol 2008, 255:367-370. 10.1007/s00415-008-0665-5, 18343969.
30. McKinnon J, Evidente V, Driver-Dunckley E, Premkumar A, Hentz J, Shill H, Sabbagh M, Caviness J, Connor D, Adler C. Olfaction in the elderly: a cross-sectional analysis comparing Parkinson's disease with controls and other disorders. Int J Neurosci 2010, 120:36-39. 10.3109/00207450903428954, 20128670.
31. Oka H, Toyoda C, Yogo M, Mochio S. Olfactory dysfunction and cardiovascular dysautonomia in Parkinson's disease. J Neurol 2010, 257:969-976. 10.1007/s00415-009-5447-1, 20119648.
32. Ponsen MM, Stoffers D, Wolters E, Booij J, Berendse HW. Olfactory testing combined with dopamine transporter imaging as a method to detect prodromal Parkinson's disease. J Neurol Neurosurg Psychiatry 2010, 81:396-399. 10.1136/jnnp.2009.183715, 19965851.
33. Siderowf A, Newberg A, Chou KL, Lloyd M, Colcher A, Hurtig HI, Stern MB, Doty RL, Mozley PD, Wintering N, et al. [99mTc]TRODAT-1 SPECT imaging correlates with odor identification in early Parkinson disease. Neurology 2005, 64:1716-1720. 10.1212/01.WNL.0000161874.52302.5D, 15911797.
34. Deeb J, Shah M, Muhammed N, Gunasekera R, Gannon K, Findley LJ, Hawkes CH. A basic smell test is as sensitive as a dopamine transporter scan: comparison of olfaction, taste and DaTSCAN in the diagnosis of Parkinson's disease. QJM 2010, 103:941-952. 10.1093/qjmed/hcq142, 20736182.
35. Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR. Association of olfactory dysfunction with risk for future Parkinson's disease. Ann Neurol 2008, 63:167-173. 10.1002/ana.21291, 18067173.
36. Berendse HW, Ponsen MM. Diagnosing premotor Parkinson's disease using a two-step approach combining olfactory testing and DAT SPECT imaging. Parkinsonism Relat Disord 2009, 15(Suppl 3):S26-30.
37. Aarsland D, Brønnick K, Alves G, Tysnes OB, Pedersen KF, Ehrt U, Larsen JP. The spectrum of neuropsychiatric symptoms in patients with early untreated Parkinson's disease. J Neurol Neurosurg Psychiatry 2009, 80:928-930. 10.1136/jnnp.2008.166959, 19608786.
38. Ravina B, Camicioli R, Como PG, Marsh L, Jankovic J, Weintraub D, Elm J. The impact of depressive symptoms in early Parkinson disease. Neurology 2007, 69:342-347. 10.1212/01.wnl.0000268695.63392.10, 2031220, 17581943.
39. Ravina B, Elm J, Camicioli R, Como PG, Marsh L, Jankovic J, Weintraub D. The course of depressive symptoms in early Parkinson's disease. Mov Disord 2009, 24:1306-1311. 10.1002/mds.22572, 2788307, 19412939.
40. Dooneief G, Mirabello E, Bell K, Marder K, Stern Y, Mayeux R. An estimate of the incidence of depression in idiopathic Parkinson's disease. Arch Neurol 1992, 49:305-307. 10.1001/archneur.1992.00530270125028, 1536634.
41. Tandberg E, Larsen JP, Aarsland D, Cummings JL. The occurrence of depression in Parkinson's disease. A community-based study. Arch Neurol 1996, 53:175-179. 10.1001/archneur.1996.00550020087019, 8639068.
42. Shiba M, Bower JH, Maraganore DM, McDonnell SK, Peterson BJ, Ahlskog JE, Schaid DJ, Rocca WA. Anxiety disorders and depressive disorders preceding Parkinson's disease: a case-control study. Mov Disord 2000, 15:669-677. 10.1002/1531-8257(200007)15:4<669::AID-MDS1011>3.0.CO;2-5, 10928577.
43. Bower JH, Grossardt BR, Maraganore DM, Ahlskog JE, Colligan RC, Geda YE, Therneau TM, Rocca WA. Anxious personality predicts an increased risk of Parkinson's disease. Mov Disord 2010, 25:2105-2113. 10.1002/mds.23230, 3089895, 20669309.
44. Abe N, Fujii T, Hirayama K, Takeda A, Hosokai Y, Ishioka T, Nishio Y, Suzuki K, Itoyama Y, Takahashi S, et al. Do parkinsonian patients have trouble telling lies? The neurobiological basis of deceptive behaviour. Brain 2009, 132:1386-1395. 10.1093/brain/awp052, 2677797, 19339257.
45. Ishihara L, Brayne C. What is the evidence for a premorbid parkinsonian personality: a systematic review. Mov Disord 2006, 21:1066-1072. 10.1002/mds.20980, 16755553.
46. Macías Y, Benito-León J, Louis ED, Cano-Vindel A. Anger in Parkinson's disease: a case-control study. Mov Disord 2008, 23:195-199. 10.1002/mds.21758, 18044696.
47. Evans AH, Lawrence AD, Potts J, MacGregor L, Katzenschlager R, Shaw K, Zijlmans J, Lees AJ. Relationship between impulsive sensation seeking traits, smoking, alcohol and caffeine intake, and Parkinson's disease. J Neurol Neurosurg Psychiatry 2006, 77:317-321. 2077692, 16484638.
48. Jellinger KA, Paulus W. Clinico-pathological correlations in Parkinson's disease. Clin Neurol Neurosurg 1992, 94(Suppl):S86-88.
49. Feldmann A, Illes Z, Kosztolanyi P, Illes E, Mike A, Kover F, Balas I, Kovacs N, Nagy F. Morphometric changes of gray matter in Parkinson's disease with depression: a voxel-based morphometry study. Mov Disord 2008, 23:42-46. 10.1002/mds.21765, 17973326.
50. Blonder LX, Slevin JT. Emotional dysfunction in Parkinson's disease. Behav Neurol 2011, 24:201-217. 3177157, 21876260.
51. Parkkinen L, Pirttilä T, Alafuzoff I. Applicability of current staging/categorization of alpha-synuclein pathology and their clinical relevance. Acta Neuropathol 2008, 115:399-407. 10.1007/s00401-008-0346-6, 2270355, 18297293.
52. Tan SK, Hartung H, Sharp T, Temel Y. Serotonin-dependent depression in Parkinson's disease: a role for the subthalamic nucleus?. Neuropharmacology 2011, 61:387-399. 10.1016/j.neuropharm.2011.01.006, 21251918.
53. Shi M, Caudle WM, Zhang J. Biomarker discovery in neurodegenerative diseases: a proteomic approach. Neurobiol Dis 2009, 35:157-164. 10.1016/j.nbd.2008.09.004, 2939006, 18938247.
54. Caudle WM, Bammler TK, Lin Y, Pan S, Zhang J. Using 'omics' to define pathogenesis and biomarkers of Parkinson's disease. Expert Rev Neurother 2010, 10:925-942. 10.1586/ern.10.54, 2913169, 20518609.
55. Hong Z, Shi M, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Leverenz JB, Baird G, et al. DJ-1 and alpha-synuclein in human cerebrospinal fluid as biomarkers of Parkinson's disease. Brain 2010, 133:713-726. 10.1093/brain/awq008, 2842513, 20157014.
56. Mollenhauer B, Locascio JJ, Schulz-Schaeffer W, Sixel-Döring F, Trenkwalder C, Schlossmacher MG. α-Synuclein and tau concentrations in cerebrospinal fluid of patients presenting with parkinsonism: a cohort study. Lancet Neurol 2011, 10:230-240. 10.1016/S1474-4422(11)70014-X, 21317042.
57. Tokuda T, Salem SA, Allsop D, Mizuno T, Nakagawa M, Qureshi MM, Locascio JJ, Schlossmacher MG, El-Agnaf OM. Decreased alpha-synuclein in cerebrospinal fluid of aged individuals and subjects with Parkinson's disease. Biochem Biophys Res Commun 2006, 349:162-166. 10.1016/j.bbrc.2006.08.024, 16930553.
58. Mollenhauer B, Cullen V, Kahn I, Krastins B, Outeiro TF, Pepivani I, Ng J, Schulz-Schaeffer W, Kretzschmar HA, McLean PJ, et al. Direct quantification of CSF alpha-synuclein by ELISA and first cross-sectional study in patients with neurodegeneration. Exp Neurol 2008, 213:315-325. 10.1016/j.expneurol.2008.06.004, 18625222.
59. Shi M, Bradner J, Hancock AM, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Kim HM, et al. Cerebrospinal fluid biomarkers for Parkinson disease diagnosis and progression. Ann Neurol 2011, 69:570-580. 10.1002/ana.22311, 3117674, 21400565.
60. Ohrfelt A, Grognet P, Andreasen N, Wallin A, Vanmechelen E, Blennow K, Zetterberg H. Cerebrospinal fluid alpha-synuclein in neurodegenerative disorders-a marker of synapse loss?. Neurosci Lett 2009, 450:332-335. 10.1016/j.neulet.2008.11.015, 19022350.
61. Borghi R, Marchese R, Negro A, Marinelli L, Forloni G, Zaccheo D, Abbruzzese G, Tabaton M. Full length alpha-synuclein is present in cerebrospinal fluid from Parkinson's disease and normal subjects. Neurosci Lett 2000, 287:65-67. 10.1016/S0304-3940(00)01153-8, 10841992.
62. Mollenhauer B, El-Agnaf OM, Marcus K, Trenkwalder C, Schlossmacher MG. Quantification of α-synuclein in cerebrospinal fluid as a biomarker candidate: review of the literature and considerations for future studies. Biomark Med 2010, 4:683-699. 10.2217/bmm.10.90, 20945981.
63. Li QX, Mok SS, Laughton KM, McLean CA, Cappai R, Masters CL, Culvenor JG, Horne MK. Plasma alpha-synuclein is decreased in subjects with Parkinson's disease. Exp Neurol 2007, 204:583-588. 10.1016/j.expneurol.2006.12.006, 17258710.
64. Lee PH, Lee G, Park HJ, Bang OY, Joo IS, Huh K. The plasma alpha-synuclein levels in patients with Parkinson's disease and multiple system atrophy. J Neural Transm 2006, 113:1435-1439. 10.1007/s00702-005-0427-9, 16465458.
65. El-Agnaf OM, Salem SA, Paleologou KE, Curran MD, Gibson MJ, Court JA, Schlossmacher MG, Allsop D. Detection of oligomeric forms of alpha-synuclein protein in human plasma as a potential biomarker for Parkinson's disease. FASEB J 2006, 20:419-425. 10.1096/fj.03-1449com, 16507759.
66. Duran R, Barrero FJ, Morales B, Luna JD, Ramirez M, Vives F. Plasma alpha-synuclein in patients with Parkinson's disease with and without treatment. Mov Disord 2010, 25:489-493. 10.1002/mds.22928, 20063406.
67. Yanamandra K, Gruden MA, Casaite V, Meskys R, Forsgren L, Morozova-Roche LA. α-synuclein reactive antibodies as diagnostic biomarkers in blood sera of Parkinson's disease patients. PLoS One 2011, 6:e18513. 10.1371/journal.pone.0018513, 3081826, 21541339.
68. Shi M, Zabetian CP, Hancock AM, Ginghina C, Hong Z, Yearout D, Chung KA, Quinn JF, Peskind ER, Galasko D, et al. Significance and confounders of peripheral DJ-1 and alpha-synuclein in Parkinson's disease. Neurosci Lett 2010, 480:78-82. 10.1016/j.neulet.2010.06.009, 2943649, 20540987.
69. Hoepken HH, Gispert S, Azizov M, Klinkenberg M, Ricciardi F, Kurz A, Morales-Gordo B, Bonin M, Riess O, Gasser T, et al. Parkinson patient fibroblasts show increased alpha-synuclein expression. Exp Neurol 2008, 212:307-313. 10.1016/j.expneurol.2008.04.004, 18511044.
70. Edwards LL, Pfeiffer RF, Quigley EM, Hofman R, Balluff M. Gastrointestinal symptoms in Parkinson's disease. Mov Disord 1991, 6:151-156. 10.1002/mds.870060211, 2057006.
71. Del Tredici K, Hawkes CH, Ghebremedhin E, Braak H. Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson's disease. Acta Neuropathol 2010, 119:703-713. 10.1007/s00401-010-0665-2, 20229352.
72. Proctor GB, Carpenter GH. Regulation of salivary gland function by autonomic nerves. Auton Neurosci 2007, 133:3-18. 10.1016/j.autneu.2006.10.006, 17157080.
73. Devic I, Hwang H, Edgar JS, Izutsu K, Presland R, Pan C, Goodlett DR, Wang Y, Armaly J, Tumas V, et al. Salivary α-synuclein and DJ-1: potential biomarkers for Parkinson's disease. Brain 2011, 134:e178. 10.1093/brain/awr015, 3122368, 21349902.
74. Sato S, Mizuno Y, Hattori N. Urinary 8-hydroxydeoxyguanosine levels as a biomarker for progression of Parkinson disease. Neurology 2005, 64:1081-1083. 10.1212/01.WNL.0000154597.24838.6B, 15781836.
75. Cipriani S, Chen X, Schwarzschild MA. Urate: a novel biomarker of Parkinson's disease risk, diagnosis and prognosis. Biomark Med 2010, 4:701-712. 10.2217/bmm.10.94, 3049925, 20945982.
76. de Lau LM, Koudstaal PJ, Hofman A, Breteler MM. Serum uric acid levels and the risk of Parkinson disease. Ann Neurol 2005, 58:797-800. 10.1002/ana.20663, 16240356.
77. Weisskopf MG, O'Reilly E, Chen H, Schwarzschild MA, Ascherio A. Plasma urate and risk of Parkinson's disease. Am J Epidemiol 2007, 166:561-567. 10.1093/aje/kwm127, 2391073, 17584757.
78. Chen H, Mosley TH, Alonso A, Huang X. Plasma urate and Parkinson's disease in the Atherosclerosis Risk in Communities (ARIC) study. Am J Epidemiol 2009, 169:1064-1069. 10.1093/aje/kwp033, 2727240, 19299404.
79. Schwarzschild MA, Schwid SR, Marek K, Watts A, Lang AE, Oakes D, Shoulson I, Ascherio A, Hyson C, Gorbold E, et al. Serum urate as a predictor of clinical and radiographic progression in Parkinson disease. Arch Neurol 2008, 65:716-723. 10.1001/archneur.2008.65.6.nct70003, 2574855, 18413464.
80. Aleyasin H, Rousseaux MW, Marcogliese PC, Hewitt SJ, Irrcher I, Joselin AP, Parsanejad M, Kim RH, Rizzu P, Callaghan SM, et al. DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc Natl Acad Sci USA 2010, 107:3186-3191. 10.1073/pnas.0914876107, 2840364, 20133695.
81. Duan X, Kelsen SG, Merali S. Proteomic analysis of oxidative stress-responsive proteins in human pneumocytes: insight into the regulation of DJ-1 expression. J Proteome Res 2008, 7:4955-4961. 10.1021/pr800295j, 18817430.
82. Jin J, Li GJ, Davis J, Zhu D, Wang Y, Pan C, Zhang J. Identification of novel proteins associated with both alpha-synuclein and DJ-1. Mol Cell Proteomics 2007, 6:845-859. 10.1074/mcp.M600182-MCP200, 16854843.
83. Maita C, Tsuji S, Yabe I, Hamada S, Ogata A, Maita H, Iguchi-Ariga SM, Sasaki H, Ariga H. Secretion of DJ-1 into the serum of patients with Parkinson's disease. Neurosci Lett 2008, 431:86-89. 10.1016/j.neulet.2007.11.027, 18162323.
84. Waragai M, Nakai M, Wei J, Fujita M, Mizuno H, Ho G, Masliah E, Akatsu H, Yokochi F, Hashimoto M. Plasma levels of DJ-1 as a possible marker for progression of sporadic Parkinson's disease. Neurosci Lett 2007, 425:18-22. 10.1016/j.neulet.2007.08.010, 17720313.
85. Waragai M, Wei J, Fujita M, Nakai M, Ho GJ, Masliah E, Akatsu H, Yamada T, Hashimoto M. Increased level of DJ-1 in the cerebrospinal fluids of sporadic Parkinson's disease. Biochem Biophys Res Commun 2006, 345:967-972. 10.1016/j.bbrc.2006.05.011, 16707095.
86. Inden M, Kitamura Y, Takahashi K, Takata K, Ito N, Niwa R, Funayama R, Nishimura K, Taniguchi T, Honda T, et al. 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. 10.1254/jphs.11151FP, 22041943.
87. Saito Y, Hamakubo T, Yoshida Y, Ogawa Y, Hara Y, Fujimura H, Imai Y, Iwanari H, Mochizuki Y, Shichiri M, et al. 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 2009, 465:1-5. 10.1016/j.neulet.2009.08.074, 19733211.
88. Ren H, Fu K, Wang D, Mu C, Wang G. Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL. J Biol Chem 2011, 286:35308-35317. 10.1074/jbc.M110.207134, 21852238.
89. Mehta SH, Morgan JC, Sethi KD. Neuroimaging and transcranial ultrasonography in Parkinson's disease. Curr Neurol Neurosci Rep 2008, 8:297-303. 10.1007/s11910-008-0046-6, 18590613.
90. Booij J, Korn P, Linszen DH, van Royen EA. Assessment of endogenous dopamine release by methylphenidate challenge using iodine-123 iodobenzamide single-photon emission tomography. Eur J Nucl Med 1997, 24:674-677.
91. Marek K, Jennings D. Can we image premotor Parkinson disease?. Neurology 2009, 72:S21-26. 10.1212/WNL.0b013e318198df97, 19221310.
92. Panzacchi A, Moresco RM, Garibotto V, Antonini A, Gobbo C, Isaias IU, Goldwurm S, Bonaldi L, Carpinelli A, Pezzoli G, et al. A voxel-based PET study of dopamine transporters in Parkinson's disease: relevance of age at onset. Neurobiol Dis 2008, 31:102-109. 10.1016/j.nbd.2008.03.012, 18502656.
93. Schwingenschuh P, Ruge D, Edwards MJ, Terranova C, Katschnig P, Carrillo F, Silveira-Moriyama L, Schneider SA, Kägi G, Palomar FJ, et al. Distinguishing SWEDDs patients with asymmetric resting tremor from Parkinson's disease: a clinical and electrophysiological study. Mov Disord 2010, 25:560-569. 10.1002/mds.23019, 2996567, 20131394.
94. Hu MT, Taylor-Robinson SD, Chaudhuri KR, Bell JD, Labbé C, Cunningham VJ, Koepp MJ, Hammers A, Morris RG, Turjanski N, Brooks DJ. Cortical dysfunction in non-demented Parkinson's disease patients: a combined (31)P-MRS and (18)FDG-PET study. Brain 2000, 123(Pt 2):340-352.
95. Hilker R, Schweitzer K, Coburger S, Ghaemi M, Weisenbach S, Jacobs AH, Rudolf J, Herholz K, Heiss WD. Nonlinear progression of Parkinson disease as determined by serial positron emission tomographic imaging of striatal fluorodopa F 18 activity. Arch Neurol 2005, 62:378-382. 10.1001/archneur.62.3.378, 15767502.
96. Stoessl AJ. Positron emission tomography in premotor Parkinson's disease. Parkinsonism Relat Disord 2007, 13(Suppl 3):S421-424.
97. Hu MT, White SJ, Chaudhuri KR, Morris RG, Bydder GM, Brooks DJ. Correlating rates of cerebral atrophy in Parkinson's disease with measures of cognitive decline. J Neural Transm 2001, 108:571-580. 10.1007/s007020170057, 11459077.
98. Martin WR, Wieler M, Gee M. Midbrain iron content in early Parkinson disease: a potential biomarker of disease status. Neurology 2008, 70:1411-1417. 10.1212/01.wnl.0000286384.31050.b5, 18172063.
99. Vaillancourt DE, Spraker MB, Prodoehl J, Abraham I, Corcos DM, Zhou XJ, Comella CL, Little DM. High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 2009, 72:1378-1384. 10.1212/01.wnl.0000340982.01727.6e, 2677508, 19129507.
100. Péran P, Cherubini A, Assogna F, Piras F, Quattrocchi C, Peppe A, Celsis P, Rascol O, Démonet JF, Stefani A, et al. Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 2010, 133:3423-3433. 10.1093/brain/awq212, 20736190.
101. Wild EJ, Fox NC. Serial volumetric MRI in Parkinsonian disorders. Mov Disord 2009, 24(Suppl 2):S691-698.
102. Hampe C, Ardila-Osorio H, Fournier M, Brice A, Corti O. Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum Mol Genet 2006, 15:2059-2075. 10.1093/hmg/ddl131, 16714300.
103. Veeriah S, Taylor BS, Meng S, Fang F, Yilmaz E, Vivanco I, Janakiraman M, Schultz N, Hanrahan AJ, Pao W, et al. Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 2010, 42:77-82. 10.1038/ng.491, 19946270.
104. Sutherland G, Mellick G, Sue C, Chan DK, Rowe D, Silburn P, Halliday G. A functional polymorphism in the parkin gene promoter affects the age of onset of Parkinson's disease. Neurosci Lett 2007, 414:170-173. 10.1016/j.neulet.2006.12.051, 17280783.
105. Hruska KS, LaMarca ME, Scott CR, Sidransky E. Gaucher disease: mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum Mutat 2008, 29:567-583. 10.1002/humu.20676, 18338393.
106. Westbroek W, Gustafson AM, Sidransky E. Exploring the link between glucocerebrosidase mutations and parkinsonism. Trends Mol Med 2011, 17:485-493. 10.1016/j.molmed.2011.05.003, 3351003, 21723784.
107. Neudorfer O, Giladi N, Elstein D, Abrahamov A, Turezkite T, Aghai E, Reches A, Bembi B, Zimran A. Occurrence of Parkinson's syndrome in type I Gaucher disease. QJM 1996, 89:691-694. 10.1093/qjmed/89.9.691, 8917744.
108. Aharon-Peretz J, Rosenbaum H, Gershoni-Baruch R. Mutations in the glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N Engl J Med 2004, 351:1972-1977. 10.1056/NEJMoa033277, 15525722.
109. Zimran A, Neudorfer O, Elstein D. The glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N Engl J Med 2005, 352:728-731. author reply 728-731.
110. De Marco EV, Annesi G, Tarantino P, Rocca FE, Provenzano G, Civitelli D, Cirò Candiano IC, Annesi F, Carrideo S, Condino F, et al. Glucocerebrosidase gene mutations are associated with Parkinson's disease in southern Italy. Mov Disord 2008, 23:460-463. 10.1002/mds.21892, 18074383.
111. Mao XY, Burgunder JM, Zhang ZJ, An XK, Zhang JH, Yang Y, Li T, Wang YC, Chang XL, Peng R. Association between GBA L444P mutation and sporadic Parkinson's disease from Mainland China. Neurosci Lett 2010, 469:256-259. 10.1016/j.neulet.2009.12.007, 20004703.
112. Sun QY, Guo JF, Wang L, Yu RH, Zuo X, Yao LY, Pan Q, Xia K, Tang BS. Glucocerebrosidase gene L444P mutation is a risk factor for Parkinson's disease in Chinese population. Mov Disord 2010, 25:1005-1011. 10.1002/mds.23009, 20131388.
113. Lesage S, Condroyer C, Hecham N, Anheim M, Belarbi S, Lohman E, Viallet F, Pollak P, Abada M, Dürr A, et al. Mutations in the glucocerebrosidase gene confer a risk for Parkinson disease in North Africa. Neurology 2011, 76:301-303. 10.1212/WNL.0b013e318207b01e, 21242499.
114. Neumann J, Bras J, Deas E, O'Sullivan SS, Parkkinen L, Lachmann RH, Li A, Holton J, Guerreiro R, Paudel R, et al. Glucocerebrosidase mutations in clinical and pathologically proven Parkinson's disease. Brain 2009, 132:1783-1794. 10.1093/brain/awp044, 2702833, 19286695.
115. Lesage S, Anheim M, Condroyer C, Pollak P, Durif F, Dupuits C, Viallet F, Lohmann E, Corvol JC, Honoré A, et al. Large-scale screening of the Gaucher's disease-related glucocerebrosidase gene in Europeans with Parkinson's disease. Hum Mol Genet 2011, 20:202-210. 10.1093/hmg/ddq454, 20947659.
116. Goker-Alpan O, Lopez G, Vithayathil J, Davis J, Hallett M, Sidransky E. The spectrum of parkinsonian manifestations associated with glucocerebrosidase mutations. Arch Neurol 2008, 65:1353-1357. 10.1001/archneur.65.10.1353, 2629407, 18852351.
117. Mata IF, Samii A, Schneer SH, Roberts JW, Griffith A, Leis BC, Schellenberg GD, Sidransky E, Bird TD, Leverenz JB, et al. Glucocerebrosidase gene mutations: a risk factor for Lewy body disorders. Arch Neurol 2008, 65:379-382. 10.1001/archneurol.2007.68, 2826203, 18332251.
118. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, Barbosa ER, Bar-Shira A, Berg D, Bras J, Brice A, et al. Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 2009, 361:1651-1661. 10.1056/NEJMoa0901281, 2856322, 19846850.
119. Goker-Alpan O, Stubblefield BK, Giasson BI, Sidransky E. Glucocerebrosidase is present in α-synuclein inclusions in Lewy body disorders. Acta Neuropathol 2010, 120:641-649. 10.1007/s00401-010-0741-7, 3352317, 20838799.
120. Cullen V, Sardi SP, Ng J, Xu YH, Sun Y, Tomlinson JJ, Kolodziej P, Kahn I, Saftig P, Woulfe J, et al. Acid β-glucosidase mutants linked to Gaucher disease, Parkinson disease, and Lewy body dementia alter α-synuclein processing. Ann Neurol 2011, 69:940-953. 10.1002/ana.22400, 21472771.
121. Yap TL, Gruschus JM, Velayati A, Westbroek W, Goldin E, Moaven N, Sidransky E, Lee JC. Alpha-synuclein interacts with Glucocerebrosidase providing a molecular link between Parkinson and Gaucher diseases. J Biol Chem 2011, 286:28080-28088. 10.1074/jbc.M111.237859, 21653695.
122. Lesage S, Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum Mol Genet 2009, 18:R48-59. 10.1093/hmg/ddp012, 19297401.
123. Dächsel JC, Farrer MJ. LRRK2 and Parkinson disease. Arch Neurol 2010, 67:542-547.
124. Kumari U, Tan EK. LRRK2 in Parkinson's disease: genetic and clinical studies from patients. FEBS J 2009, 276:6455-6463. 10.1111/j.1742-4658.2009.07344.x, 19804413.
125. Westermann B, Wattendorf E, Schwerdtfeger U, Husner A, Fuhr P, Gratzl O, Hummel T, Bilecen D, Welge-Lüssen A. Functional imaging of the cerebral olfactory system in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 2008, 79:19-24. 10.1136/jnnp.2006.113860, 17519323.
126. Ozelius LJ, Senthil G, Saunders-Pullman R, Ohmann E, Deligtisch A, Tagliati M, Hunt AL, Klein C, Henick B, Hailpern SM, et al. LRRK2 G2019S as a cause of Parkinson's disease in Ashkenazi Jews. N Engl J Med 2006, 354:424-425. 10.1056/NEJMc055509, 16436782.
127. Lesage S, Dürr A, Tazir M, Lohmann E, Leutenegger AL, Janin S, Pollak P, Brice A. Group FPsDGS: LRRK2 G2019S as a cause of Parkinson's disease in North African Arabs. N Engl J Med 2006, 354:422-423. 10.1056/NEJMc055540, 16436781.
128. Anand VS, Reichling LJ, Lipinski K, Stochaj W, Duan W, Kelleher K, Pungaliya P, Brown EL, Reinhart PH, Somberg R, et al. Investigation of leucine-rich repeat kinase 2: enzymological properties and novel assays. FEBS J 2009, 276:466-478. 10.1111/j.1742-4658.2008.06789.x, 19076219.
129. Li X, Patel JC, Wang J, Avshalumov MV, Nicholson C, Buxbaum JD, Elder GA, Rice ME, Yue Z. Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson's disease mutation G2019S. J Neurosci 2010, 30:1788-1797. 10.1523/JNEUROSCI.5604-09.2010, 2858426, 20130188.
130. Qing H, Wong W, McGeer EG, McGeer PL. Lrrk2 phosphorylates alpha synuclein at serine 129: Parkinson disease implications. Biochem Biophys Res Commun 2009, 387:149-152. 10.1016/j.bbrc.2009.06.142, 19576176.
131. Shi M, Furay AR, Sossi V, Aasly JO, Armaly J, Wang Y, Wszolek ZK, Uitti RJ, Hasegawa K, Yokoyama T, et al. DJ-1 and αSYN in LRRK2 CSF do not correlate with striatal dopaminergic function. Neurobiol Aging 2011, : .
132. Aasly JO, Shi M, Sossi V, Stewart T, Johansen KK, Wszolek ZK, Uitti RJ, Hasegawa K, Yokoyama T, Zabetian CP, et al. Cerebrospinal fluid amyloid β and tau in LRRK2 mutation carriers. Neurology 2011, : .
133. Johansen KK, Wang L, Aasly JO, White LR, Matson WR, Henchcliffe C, Beal MF, Bogdanov M. Metabolomic profiling in LRRK2-related Parkinson's disease. PLoS One 2009, 4:e7551. 10.1371/journal.pone.0007551, 2761616, 19847307.
134. Mirelman A, Gurevich T, Giladi N, Bar-Shira A, Orr-Urtreger A, Hausdorff JM. Gait alterations in healthy carriers of the LRRK2 G2019S mutation. Ann Neurol 2011, 69:193-197. 10.1002/ana.22165, 21280089.
135. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, Kubo M, Kawaguchi T, Tsunoda T, Watanabe M, Takeda A, et al. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 2009, 41:1303-1307. 10.1038/ng.485, 19915576.
136. Do CB, Tung JY, Dorfman E, Kiefer AK, Drabant EM, Francke U, Mountain JL, Goldman SM, Tanner CM, Langston JW, et al. Web-based genome-wide association study identifies two novel loci and a substantial genetic component for Parkinson's disease. PLoS Genet 2011, 7:e1002141. 10.1371/journal.pgen.1002141, 3121750, 21738487.
137. Nalls MA, Plagnol V, Hernandez DG, Sharma M, Sheerin UM, Saad M, Simón-Sánchez J, Schulte C, Lesage S, Sveinbjörnsdóttir S, et al. Imputation of sequence variants for identification of genetic risks for Parkinson's disease: a meta-analysis of genome-wide association studies. Lancet 2011, 377:641-649.
138. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, Beecham GW, Wang L, Züchner S, Konidari I, Wang G, et al. Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 2010, 74:97-109. 10.1111/j.1469-1809.2009.00560.x, 2853717, 20070850.
139. Maraganore DM, de Andrade M, Lesnick TG, Strain KJ, Farrer MJ, Rocca WA, Pant PV, Frazer KA, Cox DR, Ballinger DG. High-resolution whole-genome association study of Parkinson disease. Am J Hum Genet 2005, 77:685-693. 10.1086/496902, 1271381, 16252231.
140. Fung HC, Scholz S, Matarin M, Simón-Sánchez J, Hernandez D, Britton A, Gibbs JR, Langefeld C, Stiegert ML, Schymick J, et al. Genome-wide genotyping in Parkinson's disease and neurologically normal controls: first stage analysis and public release of data. Lancet Neurol 2006, 5:911-916. 10.1016/S1474-4422(06)70578-6, 17052657.
141. Pankratz N, Wilk JB, Latourelle JC, DeStefano AL, Halter C, Pugh EW, Doheny KF, Gusella JF, Nichols WC, Foroud T, et al. Genomewide association study for susceptibility genes contributing to familial Parkinson disease. Hum Genet 2009, 124:593-605. 10.1007/s00439-008-0582-9, 2627511, 18985386.
142. Rhodes SL, Sinsheimer JS, Bordelon Y, Bronstein JM, Ritz B. Replication of GWAS associations for GAK and MAPT in Parkinson's disease. Ann Hum Genet 2011, 75:195-200. 3074465, 21058943.
143. Trotta L, Guella I, Soldà G, Sironi F, Tesei S, Canesi M, Pezzoli G, Goldwurm S, Duga S, Asselta R. SNCA and MAPT genes: Independent and joint effects in Parkinson disease in the Italian population. Parkinsonism Relat Disord 2011, : .
144. Toledo JB, Brettschneider J, Grossman M, Arnold SE, Hu WT, Xie SX, Lee VM, Shaw LM, Trojanowski JQ. CSF biomarkers cutoffs: the importance of coincident neuropathological diseases. Acta Neuropathol 2012, : .