α-Synuclein: The long distance runner

Brain Pathology

Volumn 23, Issue 3, 2013, Pages 350-357

  George, Sonia ^a   Rey, Nolwen L ^a   Reichenbach, Nicole ^a   Steiner, Jennifer A ^b   Brundin, Patrik ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

Synuclein; Lewy pathology; Parkinson's disease; prion disease; prion like aggregation; templated misfolding

Indexed keywords

ALPHA SYNUCLEIN;

CELL TRANSFER; CENTRAL NERVOUS SYSTEM; CONFERENCE PAPER; DISEASE SEVERITY; HUMAN; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PARKINSON DISEASE; PERIPHERAL NERVE; PRION; PROTEIN AGGREGATION;

ALGORITHMS; ALPHA-SYNUCLEIN; ANIMALS; AXONAL TRANSPORT; AXONS; CENTRAL NERVOUS SYSTEM; DIGESTIVE SYSTEM; DISEASE PROGRESSION; HUMANS; PARKINSON DISEASE; PRIONS;

EID: 84876240395     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12046     Document Type: Conference Paper

References (78)

1. Alvarez-Erviti L, Seow Y, Schapira AH, Gardiner C, Sargent IL, Wood MJ, Cooper JM, (2011) Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol Dis 42: 360-367.
2. Angot E, Steiner JA, Lema Tomé CM, Ekström P, Mattsson B, Björklund A, Brundin P, (2012) Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo. PLoS ONE 7: e39465.
3. Bae EJ, Lee HJ, Rockenstein E, Ho DH, Park EB, Yang NY, et al (2012) Antibody-aided clearance of extracellular-synuclein prevents cell-to-cell aggregate transmission. J Neurosci 32: 13454-13469.
4. Baltic S, Perovic M, Mladenovic A, Raicevic N, Ruzdijic S, Rakic L, Kanazir S, (2004) α-Synuclein is expressed in different tissues during human fetal development. J Mol Neurosci 22: 199-204.
5. Bartels T, Choi JG, Selkoe DJ, (2011) α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477: 107-110.
6. Braak H, Rüb U, Gai WP, Del Tredici K, (2003) Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110: 517-536.
7. Brundin P, Li JY, Holton JL, Lindvall O, Revesz T, (2008) Research in motion: the enigma of Parkinson's disease pathology spread. Nat Rev Neurosci 9: 741-745.
8. Burke RE, Dauer WT, Vonsattel JPG, (2008) A critical evaluation of the Braak staging scheme for Parkinson's disease. Ann Neurol 64: 485-491.
9. Burré J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Südhof TC, (2010) Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329: 1663-1667.
10. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, et al (2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364: 1167-1169.
11. Chaudhuri KR, Yates L, Martinez-Martin P, (2005) The non-motor symptom complex of Parkinson's disease: a comprehensive assessment is essential. Curr Neurol Neurosci Rep 5: 275-283.
12. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B, et al (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313: 324-328.
13. Danzer KM, Haasen D, Karow AR, Moussaud S, Habeck M, Giese A, et al (2007) Different species of alpha-synuclein oligomers induce calcium influx and seeding. J Neurosci 27: 9220-9232.
14. Danzer KM, Ruf WP, Putcha P, Joyner D, Hashimoto T, Glabe C, et al (2011) Heat-shock protein 70 modulates toxic extracellular α-synuclein oligomers and rescues trans-synaptic toxicity. FASEB J 25: 326-336.
15. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, Crews L, et al (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci U S A 106: 13010-13015.
16. Dunning CJR, Reyes JF, Steiner JA, Brundin P, (2012) Can Parkinson's disease pathology be propagated from one neuron to another? Prog Neurobiol 97: 205-219.
17. El-Agnaf OM, Salem SA, Paleologou KE, Cooper LJ, Fullwood NJ, Gibson MJ, et al (2003) Alpha-synuclein implicated in Parkinson's disease is present in extracellular biological fluids, including human plasma. FASEB J 17: 1945-1947.
18. Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH, et al (2010) Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 30: 6838-6851.
19. Fahn S, (2003) Description of Parkinson's disease as a clinical syndrome. Ann N Y Acad Sci 991: 1-14.
20. Fauvet B, Mbefo MK, Fares MB, Desobry C, Michael S, Ardah MT, et al (2012) α-Synuclein in the central nervous system and from erythrocytes, mammalian cells and E. coli exists predominantly as a disordered monomer. J Biol Chem 287: 15345-15364.
21. Freundt EC, Maynard N, Clancy EK, Roy S, Bousset L, Sourigues Y, et al (2012) Neuron-to-neuron transmission of α-synuclein fibrils through axonal transport. Ann Neurol 72: 517-524.
22. Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, Lee VM, (2002) Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron 34: 521-533.
23. Gitler AD, Bevis BJ, Shorter J, Strathearn KE, Hamamichi S, Su LJ, et al (2008) The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc Natl Acad Sci U S A 105: 145-150.
24. Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G, et al (2011) alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121: 715-725.
25. Hardy J, (2005) Expression of normal sequence pathogenic proteins for neurodegenerative disease contributes to disease risk: "permissive templating" as a general mechanism underlying neurodegeneration. Biochem Soc Trans 33: 578-581.
26. Hasegawa T, Konno M, Baba T, Sugeno N, Kikuchi A, Kobayashi M, et al (2011) The AAA-ATPase VPS4 regulates extracellular secretion and lysosomal targeting of α-synuclein. Plos ONE 6: e29460.
27. Hawkes CH, Del Tredici K, Braak H, (2007) Parkinson's disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 33: 599-614.
28. Hawkes CH, Del Tredici K, Braak H, (2009) Parkinson's disease: the dual hit theory revisited. Ann N Y Acad Sci 1170: 615-622.
29. Hirokawa N, (1997) The mechanisms of fast and slow transport in neurons: identification and characterization of the new kinesin superfamily motors. Curr Opin Neurobiol 7: 605-614.
30. Irizarry MC, Growdon W, Gomez-Isla T, Newell K, George JM, Clayton DF, Hyman BT, (1998) Nigral and cortical Lewy bodies and dystrophic nigral neurites in Parkinson's disease and cortical Lewy body disease contain alpha-synuclein immunoreactivity. J Neuropathol Exp Neurol 57: 334-337.
31. Irwin DJ, Abrams JY, Schonberger LB, Werber Leschek E, Mills JL, Lee VMY, Trojanowski JQ, (2013) Potential infectivity of neurodegenerative disease associated proteins. Arch Neurol. doi: 10.1001/jamaneurol.2013.1933.
32. Jang A, Lee HJ, Suk JE, Jung JW, Kim KP, Lee SJ, (2010) Non-classical exocytosis of alpha-synuclein is sensitive to folding states and promoted under stress conditions. J Neurochem 113: 1263-1274.
33. Jellinger KA, (2011) Neuropathology of sporadic Parkinson's disease: evaluation and changes of concepts. Mov Disord 27: 8-30.
34. Jellinger KA, (2009) Critical evaluation of the Braak staging scheme for Parkinson's disease. Ann Neurol 67: 550-550.
35. Jensen PH, Li JY, Dahlström A, Dotti CG, (2008) Axonal transport of synucleins is mediated by all rate components. Eur J Neurosci 11: 3369-3376.
36. Jensen PH, Nielsen MS, Jakes R, Dotti CG, Goedert M, (1998) Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J Biol Chem 273: 26292-26294.
37. Jo E, (2000) Alpha-synuclein membrane interactions and lipid specificity. J Biol Chem 275: 34328-34334.
38. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW, (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14: 504-506.
39. Kordower JH, Dodiya HB, Kordower AM, Terpstra B, Paumier K, Madhavan L, et al (2011) Transfer of host-derived α-synuclein to grafted dopaminergic neurons in rat. Neurobiol Dis 43: 552-557.
40. Kordower JH, Chu Y, Hauser RA, Olanow CW, Freeman TB, (2008) Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov Disord 23: 2303-2306.
41. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, et al (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18: 106-108.
42. Kurowska Z, Englund E, Widner H, Lindvall O, Li JY, Brundin P, (2011) Signs of degeneration in 12-22-year old grafts of mesencephalic dopamine neurons in patients with Parkinson's disease. J Park Dis 1: 83-92.
43. Lavedan C, Buchholtz S, Auburger G, Albin RL, Athanassiadou A, Blancato J, et al (1998) Absence of mutation in the beta- and gamma-synuclein genes in familial autosomal dominant Parkinson's disease. DNA Res 5: 401-402.
44. Lee HJ, Patel S, Lee SJ, (2005) Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 25: 6016-6024.
45. Lee H-J, Suk J-E, Bae E-J, Lee J-H, Paik SR, Lee S-J, (2008) Assembly-dependent endocytosis and clearance of extracellular α-synuclein. Int J Biochem Cell Biol 40: 1835-1849.
46. Lee H-J, Suk J-E, Bae E-J, Lee S-J, (2008) Clearance and deposition of extracellular α-synuclein aggregates in microglia. Biochem Biophys Res Commun 372: 423-428.
47. Lewis KA, Yaeger A, DeMartino GN, Thomas PJ, (2010) Accelerated formation of alpha-synuclein oligomers by concerted action of the 20S proteasome and familial Parkinson mutations. J Bioenerg Biomembr 42: 85-95.
48. Lewy FH, (1912) Paralysis agitans. I. Pathologische anatomie. In: Handbuch der Neurologie, Vol. 3., M Lewandowsky, G Abelsdorff, (eds), pp. 920-933. Springer-Verlag: Berlin.
49. Li JY, Englund E, Holton JL, Soulet D, Hagell P, Lees AJ, et al (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14: 501-503.
50. Li JY, Englund E, Widner H, Rehncrona S, Bjorklund A, Lindvall O, Brundin P, (2010) Characterization of Lewy body pathology in 12- and 16-year-old intrastriatal mesencephalic grafts surviving in a patient with Parkinson's disease. Mov Disord 25: 1091-1096.
51. Li J, Uversky VN, Fink AL, (2001) Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry 40: 11604-11613.
52. Li W, Hoffman PN, Stirling W, Price DL, Lee MK, (2004) Axonal transport of human alpha-synuclein slows with aging but is not affected by familial Parkinson's disease-linked mutations. J Neurochem 88: 401-410.
53. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, Lee VMY, (2012) Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338: 949-953.
54. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR, et al (2009) Exogenous α-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci U S A 106: 20051-20056.
55. Luk KC, Kehm VM, Zhang B, O'Brien P, Trojanowski JQ, Lee VMY, (2012) Intracerebral inoculation of pathological α-synuclein initiates a rapidly progressive neurodegenerative α-synucleinopathy in mice. J Exp Med 209: 975-986.
56. Maraganore DM, de Andrade M, Lesnick TG, Strain KJ, Farrer MJ, Rocca WA, et al (2005) High-resolution whole-genome association study of Parkinson disease. Am J Hum Genet 77: 685-693.
57. Maroteaux L, Campanelli JT, Scheller RH, (1988) Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J Neurosci 8: 2804-2815.
58. Mougenot AL, Nicot S, Bencsik A, Morignat E, Verchère J, Lakhdar L, et al (2012) Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol Aging 33: 2225-2228.
59. Narhi L, Wood SJ, Steavenson S, Jiang Y, Wu GM, Anafi D, et al (1999) Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J Biol Chem 274: 9843-9846.
60. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, et al (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65: 66-79.
61. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M, (2010) Seeded aggregation and toxicity of α-synuclein and tau: cellular models of neurodenegerative diseases. J Biol Chem 285: 34885-34898.
62. Olanow CW, Prusiner SB, (2009) Is Parkinson's disease a prion disorder? Proc Natl Acad Sci U S A 106: 12571-12572.
63. Paillusson S, Clairembault T, Biraud M, Neunlist M, Derkinderen P, (2012) Activity-dependent secretion of alpha-synuclein by enteric neurons. J Neurochem. doi: 10.1111/jnc.12131.
64. Pan-Montojo F, Anichtchik O, Dening Y, Knels L, Pursche S, Jung R, et al (2010) Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. Plos ONE 5: e8762.
65. Pan-Montojo F, Schwarz M, Winkler C, Arnhold M, O'Sullivan GA, Pal A, et al (2012) Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep 2: 898.
66. Parkkinen L, Pirttilä T, Alafuzoff I, (2008) Applicability of current staging/categorization of α-synuclein pathology and their clinical relevance. Acta Neuropathologica 115: 399-407.
67. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, et al (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
68. Serpell LC, Berriman J, Jakes R, Goedert M, Crowther RA, (2000) Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 97: 4897-4902.
69. Shah JV, Cleveland DW, (2002) Slow axonal transport: fast motors in the slow lane. Curr Opin Cell Biol 14: 58-62.
70. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, et al (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302: 841.
71. Soper JH, Kehm V, Burd CG, Bankaitis VA, Lee VMY, (2011) Aggregation of α-synuclein in S. cerevisiae is associated with defects in endosomal trafficking and phospholipid biosynthesis. J Mol Neurosci 43: 391-405.
72. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M, (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
73. Tang Y, Das U, Scott DA, Roy S, (2012) The slow axonal transport of alpha-synuclein-mechanistic commonalities amongst diverse cytosolic cargoes. Cytoskeleton 69: 506-513.
74. Uversky VN, Eliezer D, (2009) Biophysics of Parkinson's disease: structure and aggregation of alpha-synuclein. Curr Protein Pept Sci 10: 483-499.
75. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A, et al (2011) Exogenous α-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72: 57-71.
76. Wang W, Perovic I, Chittuluru J, Kaganovich A, Nguyen LT, Liao J, et al (2011) A soluble α-synuclein construct forms a dynamic tetramer. Proc Natl Acad Sci U S A 108: 17797-17802.
77. Waxman EA, Giasson BI, (2010) A novel, high-efficiency cellular model of fibrillar α-synuclein inclusions and the examination of mutations that inhibit amyloid formation. J Neurochem 113: 374-388.
78. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, et al (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173.