The prion hypothesis in Parkinson's disease: Braak to the future

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Visanji, Naomi P ^a   Brooks, Patricia L ^b   Hazrati, Lili Naz ^b   Lang, Anthony E ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alpha synuclein; Braak staging; Parkinson's disease; Prion

Indexed keywords

EID: 85005896337     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-1-2     Document Type: Review

References (88)

1. Braak H, Del Tredici K, Rub U, de Vos RAI, Steur E, Braak E: Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003, 24: 197-211. 10.1016/S0197-4580(02)00065-9
2. Braak H, Rub U, Jansen Steur EN, Del Tredici K, de Vos RA: Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 2005, 64: 1404-1410. 10.1212/01.WNL.0000158422.41380.82
3. Braak H, Rub U, Gai WP, Del Tredici K: Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. Journal of Neural Transmission 2003, 110: 517-536. 10.1007/s00702-002-0808-2
4. Braak H, Braak E: Pathoanatomy of Parkinson's disease. Journal of Neurology 2000, 247: 3-10. 10.1007/s004150050002
5. Beach TG, Adler CH, Sue LI, Vedders L, Lue L, White Iii CL, Akiyama H, Caviness JN, Shill HA, Sabbagh MN, Walker DG: Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 2010, 119: 689-702. 10.1007/s00401-010-0664-3
6. Bloch A, Probst A, Bissig H, Adams H, Tolnay M: Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 2006, 32: 284-295. 10.1111/j.1365-2990.2006.00727.x
7. Dickson DW, Fujishiro H, DelleDonne A, Menke J, Ahmed Z, Klos KJ, Josephs KA, Frigerio R, Burnett M, Parisi JE, Ahlskog JE: Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol 2008, 115: 437-444. 10.1007/s00401-008-0345-7
8. Parkkinen L, Kauppinen T, Pirttila T, Autere JM, Alafuzoff I: alpha-Synuclein pathology does not predict extrapyramidal symptoms or dementia. Ann Neurol 2005, 57: 82-91. 10.1002/ana.20321
9. Hawkes CH, Del Tredici K, Braak H: Parkinson's disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 2007, 33: 599-614. 10.1111/j.1365-2990.2007.00874.x
10. Daniel SE, Hawkes CH: Preliminary diagnosis of Parkinson's disease by olfactory bulb pathology. Lancet 1992, 340: 186-186.
11. Pfeiffer RF: Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol 2003, 2: 107-116. 10.1016/S1474-4422(03)00307-7
12. 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
13. Braak H, de Vos RA, Bohl J, Del Tredici K: Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 2006, 396: 67-72. 10.1016/j.neulet.2005.11.012
14. Lebouvier T, Chaumette T, Damier P, Coron E, Touchefeu Y, Vrignaud S, Naveilhan P, Galmiche JP: Bruley des Varannes S, Derkinderen P, Neunlist M: Pathological lesions in colonic biopsies during Parkinson's disease. Gut 2008, 57: 1741-1743. 10.1136/gut.2008.162503
15. Lebouvier T, Neunlist M, Bruley des Varannes S, Coron E, Drouard A, N'Guyen JM, Chaumette T, Tasselli M, Paillusson S, Flamand M: Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS One 2010, 5: e12728. 10.1371/journal.pone.0012728
16. Shannon KM, Keshavarzian A, Mutlu E, Dodiya HB, Daian D, Jaglin JA, Kordower JH: Alpha-synuclein in colonic submucosa in early untreated Parkinson's disease. Mov Disord 2012, 27: 709-715. 10.1002/mds.23838
17. Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F: Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses. Acta Neuropathol 1988, 76: 217-221. 10.1007/BF00687767
18. Braak H, Del Tredici K: Poor and protracted myelination as a contributory factor to neurodegenerative disorders. Neurobiol Aging 2004, 25: 19-23. 10.1016/j.neurobiolaging.2003.04.001
19. Natale G, Ferrucci M, Lazzeri G, Paparelli A, Fornai F: Transmission of prions within the gut and towards the central nervous system. Prion 2011, 5: 142-149. 10.4161/pri.5.3.16328
20. Natale G, Pasquali L, Paparelli A, Fornai F: Parallel manifestations of neuropathologies in the enteric and central nervous systems. Neurogastroenterol Motil 2011, 23: 1056-1065. 10.1111/j.1365-2982.2011.01794.x
21. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW: Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nature medicine 2008, 14: 504-506. 10.1038/nm1747
22. Kordower JH, Chu Y, Hauser RA, Olanow CW, Freeman TB: Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov Disord 2008, 23: 2303-2306. 10.1002/mds.22369
23. Kurowska Z, Englund E, Widner H, Lindvall O, Li J-Y, Brundin P: Signs of Degeneration in 12-22-Year Old Grafts of Mesencephalic Dopamine Neurons in Patients with Parkinson's Disease. Journal of Parkinson's disease 2011, 1: 83-92.
24. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, Lashley T, Quinn NP, Rehncrona S, Bjorklund A: Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nature medicine 2008, 14: 501-503. 10.1038/nm1746
25. Olanow CW, Prusiner SB: Is Parkinson's disease a prion disorder? Proc Natl Acad Sci U S A 2009, 106: 12571-12572. 10.1073/pnas.0906759106
26. Lerner A, Bagic A: Olfactory pathogenesis of idiopathic Parkinson disease revisited. Mov Disord 2008, 23: 1076-1084. 10.1002/mds.22066
27. Aguzzi A, Rajendran L: The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009, 64: 783-790. 10.1016/j.neuron.2009.12.016
28. Brundin P, Melki R, Kopito R: Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 2010, 11: 301-307. 10.1038/nrm2873
29. Polymenidou M, Cleveland DW: The seeds of neurodegeneration: prion-like spreading in ALS. Cell 2011, 147: 498-508. 10.1016/j.cell.2011.10.011
30. Prusiner SB: Prions. Proceedings of the National Academy of Sciences of the United States of America 1998, 95: 13363-13383. 10.1073/pnas.95.23.13363
31. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE: Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proceedings of the National Academy of Sciences of the United States of America 1993, 90: 10962-10966. 10.1073/pnas.90.23.10962
32. Prusiner SB: Novel proteinaceous infectious particles cause scrapie. Science 1982, 216: 136-144. 10.1126/science.6801762
33. Serpell LC, Berriman J, Jakes R, Goedert M, Crowther RA: Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 2000, 97: 4897-4902. 10.1073/pnas.97.9.4897
34. Crowther RA, Daniel SE, Goedert M: Characterisation of isolated alpha-synuclein filaments from substantia nigra of Parkinson's disease brain. Neurosci Lett 2000, 292: 128-130. 10.1016/S0304-3940(00)01440-3
35. Biere AL, Wood SJ, Wypych J, Steavenson S, Jiang Y, Anafi D, Jacobsen FW, Jarosinski MA, Wu GM, Louis JC: Parkinson's disease-associated alpha-synuclein is more fibrillogenic than beta- and gamma-synuclein and cannot cross-seed its homologs. J Biol Chem 2000, 275: 34574-34579.
36. Wood SJ, Wypych J, Steavenson S, Louis JC, Citron M, Biere AL: alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J Biol Chem 1999, 274: 19509-19512. 10.1074/jbc.274.28.19509
37. Yonetani M, Nonaka T, Masuda M, Inukai Y, Oikawa T, Hisanaga S, Hasegawa M: Conversion of wild-type alpha-synuclein into mutant-type fibrils and its propagation in the presence of A30P mutant. J Biol Chem 2009, 284: 7940-7950. 10.1074/jbc.M807482200
38. Freundt EC, Maynard N, Clancy EK, Roy S, Bousset L, Sourigues Y, Covert M, Melki R, Kirkegaard K, Brahic M: Neuron-to-neuron transmission of alpha-synuclein fibrils through axonal transport. Ann Neurol 2012, 72: 517-524. 10.1002/ana.23747
39. Lee HJ, Patel S, Lee SJ: Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 2005, 25: 6016-6024. 10.1523/JNEUROSCI.0692-05.2005
40. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR, Lee SJ: Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 2008, 40: 1835-1849. 10.1016/j.biocel.2008.01.017
41. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM: Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proceedings of the National Academy of Sciences of the United States of America 2009, 106: 20051-20056.
42. Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G, Outeiro TF, Melki R, Kallunki P, Fog K: alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 2011, 121: 715-725. 10.1172/JCI43366
43. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, Spencer B, Masliah E, Lee SJ: Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proceedings of the National Academy of Sciences of the United States of America 2009, 106: 13010-13015. 10.1073/pnas.0903691106
44. Lee HJ, Kim C, Lee SJ: Alpha-synuclein stimulation of astrocytes: Potential role for neuroinflammation and neuroprotection. Oxid Med Cell Longev 2010, 3: 283-287. 10.4161/oxim.3.4.12809
45. Mougenot AL, Nicot S, Bencsik A, Morignat E, Verchere J, Lakhdar L, Legastelois S, Baron T: Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol Aging 2012, 33: 2225-2228. 10.1016/j.neurobiolaging.2011.06.022
46. Angot E, Steiner JA, Lema Tome CM, Ekstrom P, Mattsson B, Bjorklund A, Brundin P: Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo. PLoS One 2012, 7: e39465. 10.1371/journal.pone.0039465
47. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, Lee VM: Intracerebral inoculation of pathological alpha-synuclein initiates a rapidly progressive neurodegenerative alpha-synucleinopathy in mice. J Exp Med 2012, 209: 975-986. 10.1084/jem.20112457
48. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, Lee VM-Y: Pathological a-Synuclein Transmission Initiates Parkinson-like Neurodegeneration in Nontransgenic Mice. Science 2012, 338: 949-953. 10.1126/science.1227157
49. Hughes AJ, Daniel SE, Blankson S, Lees AJ: A clinicopathological study of 100 cases of Parkinson's Disease. Arch Neurol 1993, 50: 140-148. 10.1001/archneur.1993.00540020018011
50. Jellinger KA: A critical reappraisal of current staging of Lewy-related pathology in human brain. Acta Neuropathol 2008, 116: 1-16. 10.1007/s00401-008-0406-y
51. Parkkinen L, Pirttila 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
52. Zaccai J, Brayne C, McKeith I, Matthews F, Ince PG: Patterns and stages of alpha-synucleinopathy: Relevance in a population-based cohort. Neurology 2008, 70: 1042-1048. 10.1212/01.wnl.0000306697.48738.b6
53. Beach TG, Adler CH, Lue LF, Sue LI, Bachalakuri J, Henry-Watson J, Sasse J, Boyer S, Shirohi S, Brooks R: Unified staging system for Lewy body disorders: correlation with nigrostriatal degeneration, cognitive impairment and motor dysfunction. Acta Neuropathol 2009, 117: 613-634. 10.1007/s00401-009-0538-8
54. Del Tredici K, Braak H: Spinal cord lesions in sporadic Parkinson's disease. Acta Neuropathol 2012, 124: 643-664. 10.1007/s00401-012-1028-y
55. Attems J, Jellinger KA: The dorsal motor nucleus of the vagus is not an obligatory trigger site of Parkinson's disease. Neuropathol Appl Neurobiol 2008, 34: 466-467.
56. Kalaitzakis ME, Graeber MB, Gentleman SM, Pearce RKB: The dorsal motor nucleus of the vagus is not an obligatory trigger site of Parkinson's disease: a critical analysis of alpha-synuclein staging. Neuropathol Appl Neurobiol 2008, 34: 284-295. 10.1111/j.1365-2990.2007.00923.x
57. Kingsbury AE, Bandopadhyay R, Silveira-Moriyama L, Ayling H, Kallis C, Sterlacci W, Maeir H, Poewe W, Lees AJ: Brain stem pathology in Parkinson's disease: an evaluation of the Braak staging model. Mov Disord 2010, 25: 2508-2515. 10.1002/mds.23305
58. Sengoku R, Saito Y, Ikemura M, Hatsuta H, Sakiyama Y, Kanemaru K, Arai T, Sawabe M, Tanaka N, Mochizuki H: Incidence and extent of Lewy body-related alpha-synucleinopathy in aging human olfactory bulb. J Neuropathol Exp Neurol 2008, 67: 1072-1083. 10.1097/NEN.0b013e31818b4126
59. Silveira-Moriyama L, Holton JL, Kingsbury A, Ayling H, Petrie A, Sterlacci W, Poewe W, Maier H, Lees AJ, Revesz T: Regional differences in the severity of Lewy body pathology across the olfactory cortex. Neurosci Lett 2009, 453: 77-80. 10.1016/j.neulet.2009.02.006
60. Hubbard PS, Esiri MM, Reading M, McShane R, Nagy Z: Alpha-synuclein pathology in the olfactory pathways of dementia patients. J Anat 2007, 211: 117-124. 10.1111/j.1469-7580.2007.00748.x
61. Halliday G, Hely M, Reid W, Morris J: The progression of pathology in longitudinally followed patients with Parkinson's disease. Acta Neuropathol 2008, 115: 409-415. 10.1007/s00401-008-0344-8
62. Olanow CW, Perl DP, DeMartino GN, McNaught KS: Lewy-body formation is an aggresome-related process: a hypothesis. Lancet Neurol 2004, 3: 496-503. 10.1016/S1474-4422(04)00827-0
63. Kramer ML, Schulz-Schaeffer WJ: Presynaptic alpha-synuclein aggregates, not Lewy bodies, cause neurodegeneration in dementia with Lewy bodies. J Neurosci 2007, 27: 1405-1410. 10.1523/JNEUROSCI.4564-06.2007
64. Tanaka M, Kim YM, Lee G, Junn E, Iwatsubo T, Mouradian MM: Aggresomes formed by alpha-synuclein and synphilin-1 are cytoprotective. J Biol Chem 2004, 279: 4625-4631.
65. Terry RD: Do neuronal inclusions kill the cell? J Neural Transm Suppl 2000, 59: 91-93.
66. Gertz HJ, Siegers A, Kuchinke J: Stability of cell size and nucleolar size in Lewy body containing neurons of substantia nigra in Parkinson's disease. Brain Res 1994, 637: 339-341. 10.1016/0006-8993(94)91257-2
67. Saha AR, Ninkina NN, Hanger DP, Anderton BH, Davies AM, Buchman VL: Induction of neuronal death by alpha-synuclein. Eur J Neurosci 2000, 12: 3073-3077. 10.1046/j.1460-9568.2000.00210.x
68. Tompkins MM, Hill WD: Contribution of somal Lewy bodies to neuronal death. Brain Res 1997, 775: 24-29. 10.1016/S0006-8993(97)00874-3
69. Parkkinen L, O'Sullivan S, Collinsa C, Petriec A, Holtona J, Revesza T, Lees AJ: Disentangling the Relationship between Lewy Bodies and Nigral Neuronal Loss in Parkinson's Disease. Journal of Parkinson's Disease 2011, 1: 277-286.
70. Nakazato Y, Yamazaki H, Hirato J, Ishida Y, Yamaguchi H: Oligodendroglial microtubular tangles in olivopontocerebellar atrophy. J Neuropathol Exp Neurol 1990, 49: 521-530. 10.1097/00005072-199009000-00007
71. Papp MI, Kahn JE, Lantos PL: Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 1989, 94: 79-100. 10.1016/0022-510X(89)90219-0
72. Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H: Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 1998, 249: 180-182. 10.1016/S0304-3940(98)00407-8
73. Milber JM, Noorigian JV, Morley JF, Petrovitch H, White L, Ross GW, Duda JE: Lewy pathology is not the first sign of degeneration in vulnerable neurons in Parkinson disease. Neurology 2012, 79: 2307-2314. 10.1212/WNL.0b013e318278fe32
74. Pan-Montojo F, Anichtchik O, Dening Y, Knels L, Pursche S, Jung R, Jackson S, Gille G, Spillantini MG, Reichmann H, Funk RH: Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. Plos One 2010, 5: e8762. 10.1371/journal.pone.0008762
75. Orimo S, Takahashi A, Uchihara T, Mori F, Kakita A, Wakabayashi K, Takahashi H: Degeneration of cardiac sympathetic nerve begins in the early disease process of Parkinson's disease. Brain Pathol 2007, 17: 24-30. 10.1111/j.1750-3639.2006.00032.x
76. Kordower JH, Freeman TB, Snow BJ, Vingerhoets FJ, Mufson EJ, Sanberg PR, Hauser RA, Smith DA, Nauert GM, Perl DP: Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N Engl J Med 1995, 332: 1118-1124. 10.1056/NEJM199504273321702
77. Danzer KM, Krebs SK, Wolff M, Birk G, Hengerer B: Seeding induced by alpha-synuclein oligomers provides evidence for spreading of alpha-synuclein pathology. J Neurochem 2009, 111: 192-203. 10.1111/j.1471-4159.2009.06324.x
78. Kalia LV, Kalia SK, McLean PJ, Lozano AM, Lang AE: alpha-Synuclein oligomers and clinical implications for Parkinson disease. Ann Neurol In press
79. Mendez I, Vinuela A, Astradsson A, Mukhida K, Hallett P, Robertson H, Tierney T, Holness R, Dagher A, Trojanowski JQ, Isacson O: Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nature medicine 2008, 14: 507-509. 10.1038/nm1752
80. Farrer M, Chan P, Chen R, Tan L, Lincoln S, Hernandez D, Forno L, Gwinn-Hardy K, Petrucelli L, Hussey J: Lewy bodies and parkinsonism in families with parkin mutations. Ann Neurol 2001, 50: 293-300. 10.1002/ana.1132
81. Gasser T, Hardy J, Mizuno Y: Milestones in PD Genetics. Mov Disord. 2011, 26: 1042-1048.
82. Mori H, Kondo T, Yokochi M, Matsumine H, Nakagawa-Hattori Y, Miyake T, Suda K, Mizuno Y: Pathologic and biochemical studies of juvenile parkinsonism linked to chromosome 6q. Neurology 1998, 51: 890-892. 10.1212/WNL.51.3.890
83. Takahashi H, Ohama E, Suzuki S, Horikawa Y, Ishikawa A, Morita T, Tsuji S, Ikuta F: Familial juvenile parkinsonism: Clinical and pathological study in a family Neurology. 1994, 44: 437-441.
84. van de Warrenburg BPC, Lammens M, Lucking CB, Denefle P, Wesseling P, Booij J, Praamstra P, Quinn N, Brice A, Horstink M: Clinical and pathologic abnormalities in a family with parkinsonism and parkin gene mutations. Neurology 2001, 56: 555-557. 10.1212/WNL.56.4.555
85. Frost B, Diamond MI: Prion-like mechanisms in neurodegenerative diseases. Nature Reviews Neuroscience 2010, 11: 155-159.
86. Guest WC, Silverman JM, Pokrishevsky E, O'Neill MA, Grad LI, Cashman NR: Generalization of the prion hypothesis to other neurodegenerative diseases: an imperfect fit. J Toxicol Environ Health A 74: 1433-1459.
87. Kabanov AV, Gendelman HE: Nanomedicine in the diagnosis and therapy of neurodegenerative disorders. Prog Polym Sci 2007, 32: 1054-1082. 10.1016/j.progpolymsci.2007.05.014
88. Konno M, Hasegawa T, Baba T, Miura E, Sugeno N, Kikuchi A, Fiesel FC, Sasaki T, Aoki M, Itoyama Y, Takeda A: Suppression of dynamin GTPase decreases alpha-synuclein uptake by neuronal and oligodendroglial cells: a potent therapeutic target for synucleinopathy. Mol Neurodegener 2012, 7: 38. 10.1186/1750-1326-7-38