Features of alpha-synuclein that could explain the progression and irreversibility of Parkinson's disease

Frontiers in Neuroscience

Volumn 9, Issue FEB, 2015, Pages

  Gallegos, S ^a   Pacheco, C ^a   Peters, C ^a   Opazo, C ^b   Aguayo, Luis G ^a  

^a Laboratory of Neurophysiology Department of Physiology University od Concepcion   (Chile)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

Alpha synuclein; Neurodegeneration; Parkinson's disease; Toxicity; Transmission

Indexed keywords

ALPHA SYNUCLEIN; PROTEASOME;

APOPTOSIS; ARTICLE; BRAIN DEPTH STIMULATION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CYTOTOXICITY; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM STRESS; EXOSOME; GAMMA KNIFE RADIOSURGERY; HUMAN; LEWY BODY; MEMBRANE DAMAGE; NERVE CELL; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; OLIGOMERIZATION; OXIDATIVE STRESS; PALLIDOTOMY; PARKINSON DISEASE; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; THALAMOTOMY;

EID: 84924402070     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00059     Document Type: Article

References (76)

1. Aguayo, L. G., J. Parodi, F. J. Sepúlveda and C. Opazo (2009). "Pore-Forming Neurotoxin-Like Mechanism for Aß Oligomer-Induced Synaptic Failure." Pore-Forming Neurotoxin-Like Mechanism for Aß Oligomer-Induced Synaptic Failure: 13-21.
2. Ahn, K. J., S. R. Paik, K. C. Chung and J. Kim (2006). "Amino acid sequence motifs and mechanistic features of the membrane translocation of alpha-synuclein." Journal of Neurochemistry 97(1): 265279.
3. Alvarez-Erviti, L., Y. Seow, A. H. Schapira, C. Gardiner, I. L. Sargent, M. J. Wood and J. M. Cooper (2011). "Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission." Neurobiology of Disease 42(3): 360-367.
4. Angot, E. and P. Brundin (2009). "Dissecting the potential molecular mechanisms underlying a- synuclein cell-to-cell transfer in Parkinson's disease." Parkinsonism & Related Disorders 15: S143-147.
5. Angot, E., J. A. Steiner, C. M. Lema Tome, P. Ekstrom, B. Mattsson, A. Bjorklund and P. Brundin (2012). "Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo." PloS one 7(6): e39465.
6. Auluck, P. K., G. Caraveo and S. Lindquist (2010). "alpha-Synuclein: membrane interactions and toxicity in Parkinson's disease." Annual review of cell and developmental biology 26: 211-233.
7. Bellucci, A., M. Zaltieri, L. Navarria, J. Grigoletto, C. Missale and P. Spano (2012). "From a- synuclein to synaptic dysfunctions: new insights into the pathophysiology of Parkinson's disease." Brain research 1476: 183-202.
8. Bendor, J. T., T. P. Logan and R. H. Edwards (2013). "The function of a-synuclein." Neuron 79(6): 1044-1066.
9. Bisaglia, M., S. Mammi and L. Bubacco (2009). "Structural insights on physiological functions and pathological effects of alpha-synuclein." FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23(2): 329-340.
10. Brundin, P., J. Y. Li, J. L. Holton, O. Lindvall and T. Revesz (2008). "Research in motion: the enigma of Parkinson's disease pathology spread." Nature reviews. Neuroscience 9(10): 741-745.
11. Burre, J., M. Sharma, T. Tsetsenis, V. Buchman, M. R. Etherton and T. C. Sudhof (2010). "Alpha synuclein promotes SNARE-complex assembly in vivo and in vitro." Science (New York, N.Y.) 329(5999): 1663-1667.
12. Colla, E., P. Coune, Y. Liu, O. Pletnikova, J. C. Troncoso, T. Iwatsubo, B. L. Schneider and M. K. Lee (2012). "Endoplasmic reticulum stress is important for the manifestations of a-synucleinopathy in vivo." The Journal of neuroscience: the official journal of the Society for Neuroscience 32(10): 3306-3320.
13. Colla, E., P. H. Jensen, O. Pletnikova, J. C. Troncoso, C. Glabe and M. K. Lee (2012). "Accumulation of toxic a-synuclein oligomer within endoplasmic reticulum occurs in a- synucleinopathy in vivo." The Journal of neuroscience 32(10): 3301-3305.
14. Costanzo, M. and C. Zurzolo (2013). "The cell biology of prion-like spread of protein aggregates: mechanisms and implication in neurodegeneration." The Biochemical journal 452(1): 1-17.
15. Chandra, S., F. Fornai, H. B. Kwon, U. Yazdani, D. Atasoy, X. Liu, R. E. Hammer, G. Battaglia, D. C. German, P. E. Castillo and T. C. Sudhof (2004). "Double-knockout mice for a- and ß-synucleins: Effect on synaptic functions." Proceedings of the National Academy of Sciences of the United States of America 101(41): 14966-14971.
16. Danzer, K. M., D. Haasen, A. R. Karow, S. Moussaud, M. Habeck, A. Giese, H. Kretzschmar, B. Hengerer and M. Kostka (2007). "Different Species of -Synuclein Oligomers Induce Calcium Influx and Seeding." Journal of Neuroscience 27(34): 9220-9232.
17. Danzer, K. M., L. R. Kranich, W. P. Ruf, O. Cagsal-Getkin, A. R. Winslow, L. Zhu, C. R. Vanderburg and P. J. McLean (2012). "Exosomal cell-to-cell transmission of alpha synuclein oligomers." Molecular neurodegeneration 7: 42.
18. Danzer, K. M., S. K. Krebs, M. Wolff, G. Birk and B. Hengerer (2009). "Seeding induced by alpha synuclein oligomers provides evidence for spreading of alpha-synuclein pathology." Journal of neurochemistry 111(1): 192-203.
19. Deleersnijder, A., M. Gerard, Z. Debyser and V. Baekelandt (2013). "The remarkable conformational plasticity of alpha-synuclein: blessing or curse?" Trends in molecular medicine 19(6): 368-377.
20. Desplats, P. A., H. Lee, B. Eun-Jin, P. Christina, R. Edward, C. Leslie, S. Brian, M. Eliezer and L. Seung-Jae (2009). "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.
21. Doyle, K. M., D. Kennedy, A. M. Gorman, S. Gupta, S. J. Healy and A. Samali (2011). "Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders." Journal of cellular and molecular medicine 15(10): 2025-2039.
22. El-Agnaf, O. M., S. A. Salem, K. E. Paleologou, M. D. Curran, M. J. Gibson, J. A. Court, M. G. Schlossmacher and D. Allsop (2006). "Detection of oligomeric forms of a-synuclein protein in human plasma as a potential biomarker for Parkinson's disease." The FASEB Journal 20(3): 419-425.
23. Feng, L. R., H. J. Federoff, S. Vicini and K. A. Maguire-Zeiss (2010). "Alpha-synuclein mediates alterations in membrane conductance: a potential role for alpha-synuclein oligomers in cell vulnerability." The European journal of neuroscience 32(1): 10-17.
24. Freundt, E. C., N. Maynard, E. K. Clancy, S. Roy, L. Bousset, Y. Sourigues, M. Covert, R. Melki, K. Kirkegaard and M. Brahic (2012). "Neuron-to-neuron transmission of a-synuclein fibrils through axonal transport." Annals of neurology 72(4): 517-524.
25. Furukawa, K., M. Matsuzaki-Kobayashi, T. Hasegawa, A. Kikuchi, N. Sugeno, Y. Itoyama, Y. Wang, P. J. Yao, I. Bushlin and A. Takeda (2006). "Plasma membrane ion permeability induced by mutant a-synuclein contributes to the degeneration of neural cells." Journal of Neurochemistry 97(4): 1071-1077.
26. Greten-Harrison, B., M. Polydoro, M. Morimoto-Tomita, L. Diao, A. M. Williams, E. H. Nie, S. Makani, N. Tian, P. E. Castillo, V. L. Buchman and S. S. Chandra (2010). "aßγ-Synuclein triple knockout mice reveal age-dependent neuronal dysfunction." Proceedings of the National Academy of Sciences of the United States of America 107(45): 19573-19578.
27. Hansen, C., E. Angot, A. L. Bergstrom, J. A. Steiner, L. Pieri, G. Paul, T. F. Outeiro, R. Melki, P. Kallunki, K. Fog, J. Y. Li and P. Brundin (2011). "a-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells." The Journal of clinical investigation 121(2): 715-725.
28. Hara, S., S. Arawaka, H. Sato, Y. Machiya, C. Cui, A. Sasaki, S. Koyama and T. Kato (2013). "Serine 129 phosphorylation of membrane-associated a-synuclein modulates dopamine transporter function in a G protein-coupled receptor kinase-dependent manner." Molecular biology of the cell 24(11): 1649.
29. Irwin, D. J., V. M. Lee and J. Q. Trojanowski (2013). "Parkinson's disease dementia: convergence of a-synuclein, tau and amyloid-ß pathologies." Nature reviews. Neuroscience 14(9): 626-636.
30. Jain, N., K. Bhasne, M. Hemaswasthi and S. Mukhopadhyay (2013). "Structural and Dynamical Insights into the Membrane-Bound a-Synuclein." PLoS ONE 8(12): e83752.
31. Jang, A., H. Lee, J. Suk, J. Jung, K. Kim and S. Lee (2010). "Non-classical exocytosis of alpha synuclein is sensitive to folding states and promoted under stress conditions." Journal of neurochemistry.
32. Jang, H., J. Zheng and R. Nussinov (2007). "Models of ß-Amyloid Ion Channels in the Membrane Suggest That Channel Formation in the Bilayer Is a Dynamic Process." Biophysical Journal 93(6): 19381949.
33. Jankovic, J. (2008). "Parkinson's disease: clinical features and diagnosis." Journal of neurology, neurosurgery, and psychiatry 79(4): 368-376.
34. Jucker, M. and L. C. Walker (2013). "Self-propagation of pathogenic protein aggregates in neurodegenerative diseases." Nature 501(7465): 45-51.
35. Junn, E. and M. M. Mouradian (2002). "Human a-Synuclein over-expression increases intracellular reactive oxygen species levels and susceptibility to dopamine." Neuroscience Letters 320(3): 146150.
36. Kim, H. Y., M. K. Cho, A. Kumar, E. Maier, C. Siebenhaar, S. Becker, C. O. Fernandez, H. A. Lashuel, R. Benz, A. Lange and M. Zweckstetter (2009). "Structural properties of pore-forming oligomers of alpha-synuclein." Journal of the American Chemical Society 131(47): 17482-17489.
37. Kosten, J., A. Binolfi, M. Stuiver, S. Verzini, F. X. Theillet, B. Bekei, M. van Rossum and P. Selenko (2014). "Efficient Modification of Alpha-Synuclein Serine 129 by Protein Kinase CK1 Requires Phosphorylation of Tyrosine 125 as a Priming Event." ACS Chemical Neuroscience 5(12): 12031208.
38. Lashuel, H. A., C. R. Overk, A. Oueslati and E. Masliah (2013). "The many faces of a-synuclein: from structure and toxicity to therapeutic target." Nature reviews. Neuroscience 14(1): 38-48.
39. Lavedan, C. (1998). "The synuclein family." Genome research 8(9): 871-880.
40. Lee, C. and M.-H. H. Yu (2005). "Protein folding and diseases." Journal of biochemistry and molecular biology 38(3): 275-280.
41. Lee, H. J., E. D. Cho, K. W. Lee, J. H. Kim, S. G. Cho and S. J. Lee (2013). "Autophagic failure promotes the exocytosis and intercellular transfer of a-synuclein." Experimental & molecular medicine 45: e22.
42. Lee, H. J., S. Patel and S. J. Lee (2005). "Intravesicular Localization and Exocytosis of a-Synuclein and its Aggregates." The Journal of Neuroscience 25(25): 6016-6024.
43. Li, J. Y., E. Englund, J. L. Holton, D. Soulet, P. Hagell, A. J. Lees, T. Lashley, N. P. Quinn, S. Rehncrona, A. Bjorklund, H. Widner, T. Revesz, O. Lindvall and P. Brundin (2008). "Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation." Nature medicine 14(5): 501-503.
44. Luk, K. C., V. Kehm, J. Carroll, B. Zhang, P. O'Brien, J. Q. Trojanowski and V. M. Lee (2012). "Pathological a-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice." Science 338(6109): 949-953.
45. Luk, K. C., V. M. Kehm, B. Zhang, P. O'Brien, J. Q. Trojanowski and V. M. Lee (2012). "Intracerebral inoculation of pathological a-synuclein initiates a rapidly progressive neurodegenerative a-synucleinopathy in mice." The Journal of experimental medicine 209(5): 975-986.
46. Luk, K. C., C. Song, P. O'Brien, A. Stieber, J. R. Branch, K. R. Brunden, J. Q. Trojanowski and V. M. Lee (2009). "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 106(47): 20051-20056.
47. Masters, C. S., G.; Weiman, NA.; Multhaup, G.; McDonald, DL.; Beyreuther, K. (1985). "Amyloid plaque core protein in Alzheimer disease and Down syndrome." Proceedings of the National Academy of Sciences 82(12): 4245-4249.
48. Mercuri, N. B. and G. Bernardi (2005). "The 'magic' of -dopa: why is it the gold standard Parkinson's disease therapy?" Trends in Pharmacological Sciences 26(7): 341344.
49. Moreno-Gonzalez, I. and C. Soto (2011). "Misfolded protein aggregates: mechanisms, structures and potential for disease transmission." Seminars in cell & developmental biology 22(5): 482-487.
50. Munch, C. and A. Bertolotti (2012). "Propagation of the prion phenomenon: beyond the seeding principle." Journal of molecular biology 421(4-5): 491-498.
51. Obeso, J. A., M. C. Rodriguez-Oroz, C. G. Goetz, C. Marin, J. H. Kordower, M. Rodriguez, E. C.
52. Pacheco, C., C. Morales, AE. Ramirez, FJ. Muñoz, S. Gallegos, P. Caviedes, LG. Aguayo and C. Opazo (2015). "Extracellular a-synuclein oligomers alter synaptip transmission in brain neurons by perforating the neuronal plasma membrane." Journal of Neurochemistry in press.
53. Parihar, M. S., A. Parihar, M. Fujita, M. Hashimoto and P. Ghafourifar (2008). "Mitochondrial association of alpha-synuclein causes oxidative stress." Cellular and molecular life sciences: CMLS 65(7-8): 1272-1284.
54. Parihar, M. S., A. Parihar, M. Fujita, M. Hashimoto and P. Ghafourifar (2009). "Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells." The international journal of biochemistry & cell biology.
55. Parodi, J., F. J. Sepúlveda, J. Roa, C. Opazo, N. C. Inestrosa and L. G. Aguayo (2010). "Beta amyloid causes depletion of synaptic vesicles leading to neurotransmission failure." The Journal of biological chemistry 285(4): 2506-2514.
56. Plotegher, N., E. Greggio, M. Bisaglia and L. Bubacco (2014). "Biophysical groundwork as a hinge to unravel the biology of a-synuclein aggregation and toxicity." Quarterly Reviews of Biophysics 47(01): 148.
57. Ross, C. A. and M. A. Poirier (2004). "Protein aggregation and neurodegenerative disease." Nature Medicine 10 Suppl: S10-17.
58. Sato, H., T. Kato and S. Arawaka (2013). "The role of Ser129 phosphorylation of a-synuclein in neurodegeneration of Parkinson's disease: a review of in vivo models." Reviews in the Neurosciences 24(2): 115-123.
59. Schapira, A. H. (2009). "Neurobiology and treatment of Parkinson's disease." Trends in pharmacological sciences.
60. Schmidt, F., J. Levin, F. Kamp, H. Kretzschmar, A. Giese and K. Botzel (2012). "Single-channel electrophysiology reveals a distinct and uniform pore complex formed by a-synuclein oligomers in lipid membranes." PloS one 7(8): e42545.
61. Sepulveda, F. J., H. Fierro, E. Fernandez, C. Castillo, R. W. Peoples, C. Opazo and L. G. Aguayo (2014). "Nature of the neurotoxic membrane actions of amyloid-ß on hippocampal neurons in Alzheimer's disease." Neurobiology of Aging 35(3): 472481.
62. Sepulveda, F. J., J. Parodi, R. W. Peoples, C. Opazo and L. G. Aguayo (2010). "Synaptotoxicity of Alzheimer beta amyloid can be explained by its membrane perforating property." PLoS One 5(7): e11820.
63. Singh, N., V. Pillay and Y. E. Choonara (2007). "Advances in the treatment of Parkinson's disease." Progress in Neurobiology 81(1): 2944.
64. Smith, W. W., H. Jiang, Z. Pei, Y. Tanaka, H. Morita, A. Sawa, V. L. Dawson, T. M. Dawson and C. A. Ross (2005). "Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity." Human Molecular Genetics 14(24): 3801-3811.
65. Soto, C. (2003). "Unfolding the role of protein misfolding in neurodegenerative diseases." Nature Reviews Neuroscience 4(1): 49-60.
66. Soto, C. (2012). "Transmissible proteins: expanding the prion heresy." Cell 149(5): 968-977.
67. Soto, C. and N. Satani (2011). "The intricate mechanisms of neurodegeneration in prion diseases." Trends in Molecular Medicine 17(1): 1424.
68. Steiner, J. A., E. Angot and P. Brundin (2011). "A deadly spread: cellular mechanisms of a- synuclein transfer." Cell death and differentiation 18(9): 1425-1433.
69. Stockl, M. T., N. Zijlstra and V. Subramaniam (2013). "a-Synuclein oligomers: an amyloid pore? Insights into mechanisms of a-synuclein oligomer-lipid interactions." Molecular neurobiology 47(2): 613-621.
70. Tarazi, F. I., Z. T. Sahli, M. Wolny and S. A. Mousa (2014). "Emerging therapies for Parkinson's disease: From bench to bedside." Pharmacology & Therapeutics.
71. Tosatto, L., A. O. Andrighetti, N. Plotegher, V. Antonini, I. Tessari, L. Ricci, L. Bubacco and M. Dalla Serra (2012). "Alpha-synuclein pore forming activity upon membrane association." Biochimica et biophysica acta 1818(11): 2876-2883.
72. Tsigelny, I. F., P. Bar-On, Y. Sharikov, L. Crews, M. Hashimoto, M. A. Miller, S. H. Keller, O. Platoshyn, J. X. Yuan and E. Masliah (2007). "Dynamics of a-synuclein aggregation and inhibition of pore-like oligomer development by ß-synuclein." FEBS Journal 274(7): 18621877.
73. Tsigelny, I. F., Y. Sharikov, W. Wrasidlo, T. Gonzalez, P. A. Desplats, L. Crews, B. Spencer and E. Masliah (2012). "Role of a-synuclein penetration into the membrane in the mechanisms of oligomer pore formation." The FEBS journal 279(6): 1000-1013.
74. Ulmer, T. S., A. Bax, N. B. Cole and R. L. Nussbaum (2005). "Structure and Dynamics of Micelle bound Human a-Synuclein." Journal of Biological Chemistry 280(10): 9595-9603.
75. Volpicelli-Daley, L. A., K. C. Luk, T. P. Patel, S. A. Tanik, D. M. Riddle, A. Stieber, D. F. Meaney, J. Q. Trojanowski and V. M. Lee (2011). "Exogenous a-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death." Neuron 72(1): 57-71.
76. Walker, D. G., L. F. Lue, C. H. Adler, H. A. Shill, J. N. Caviness, M. N. Sabbagh, H. Akiyama, G. E. Serrano, L. I. Sue, T. G. Beach and C. Arizona Parkinson Disease (2013). "Changes in properties of serine 129 phosphorylated a-synuclein with progression of Lewy-type histopathology in human brains." Experimental neurology 240: 190-204.