The aggregation and fibrillation of α-synuclein

Accounts of Chemical Research

Volumn 39, Issue 9, 2006, Pages 628-634

  Fink, Anthony L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; BIOPOLYMER;

ATOMIC FORCE MICROSCOPY; CHEMISTRY; HUMAN; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION; PARKINSON DISEASE; PROTEIN CONFORMATION; REVIEW;

ALPHA-SYNUCLEIN; BIOPOLYMERS; HUMANS; KINETICS; MICROSCOPY, ATOMIC FORCE; OXIDATION-REDUCTION; PARKINSON DISEASE; PROTEIN CONFORMATION;

EID: 33749841522     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar050073t     Document Type: Review

References (70)

1. Trojanowski, J. Q.; Lee, V. M. Parkinson's Disease and Related Alpha-Synucleinopathies Are Brain Amyloidoses. Ann. N. Y. Acad. Sci. 2003, 991, 107-110.
2. Singleton, A. B.; Farrer, M.; Johnson, J.; Singleton, A.; Hague, S.; Kachergus, J.; Hulihan, M.; Peuralinna, T.; Dutra, A.; Nussbaum, R.; Lincoln, S.; Crawley, A.; Hanson, M.; Maraganore, D.; Adler, C.; Cookson, M. R.; Muenter, M.; Baptista, M.; Miller, D.; Blancato, J.; Hardy, J.; Gwinn-Hardy, K. Alpha-Synuclein Locus Triplication Causes Parkinson's Disease. Science 2003, 302, 841.
3. Polymeropoulos, M. H.; Lavedan, C.; Leroy, E.; Ide, S. E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; Stenroos, E. S.; Chandrasekharappa, S.; Athanassiadou, A.; Papapetropoulos, T.; Johnson, W. G.; Lazzarini, A. M.; Duvoisin, R. C.; Di Iorio, G.; Golbe, L. I.; Nussbaum, R. L. Mutation in the Alpha-Synuclein Gene Identified in Families With Parkinson's Disease. Science 1997, 276, 2045-2047.
4. Kruger, R.; Kuhn, W.; Muller, T.; Woitalla, D.; Graeber, M.; Kosel, S.; Przuntek, H.; Epplen, J. T.; Schols, L.; Riess, O. Ala30Pro Mutation in the Gene Encoding Alpha-Synuclein in Parkinson's Disease. Nat. Genet. 1998, 18, 106-108.
5. Zarranz, J. J.; Alegre, J.; Gomez-Esteban, J. C.; Lezcano, E.; Ros, R.; Ampuero, I.; Vidal, L.; Hoenicka, J.; Rodriguez, O.; Atares, B.; Llorens, V.; Gomez, T. E.; del Ser, T.; Munoz, D. G.; de Yebenes, J. G. The New Mutation, E46K, of Alpha-Synuclein Causes Parkinson and Lewy Body Dementia. Ann. Neurol. 2004, 55, 164-173.
6. Spillantini, M. G.; Crowther, R. A.; Jakes, R.; Hasegawa, M.; Goedert, M. Alpha-Synuclein in Filamentous Inclusions of Lewy Bodies From Parkinson's Disease and Dementia With Lewy Bodies. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 6469-6473.
7. Volles, M. J.; Lansbury, P. T., Jr. Vesicle Permeabilization by Protofibrillar Alpha-Synuclein Is Sensitive to Parkinson's Disease-Linked Mutations and Occurs by a Pore-Like Mechanism. Biochemistry 2002, 41, 4595-4602.
8. Uversky, V. N.; Gillespie, J. R.; Fink, A. L. Why Are "Natively Unfolded" Proteins Unstructured Under Physiologic Conditions? Proteins 2000, 41, 415-427.
9. Fink, A. L. Protein Aggregation: Folding Aggregates, Inclusion Bodies and Amyloid. Folding Des. 1998, 3, 9-15.
10. Uversky, V. N.; Fink, A. L. Conformational Constraints for Amyloid Fibrillation: the Importance of Being Unfolded. Biochim. Biophys. Acta 2004, 1698, 131-153.
11. Uversky, V. N.; Li, J.; Fink, A. L. Metal-Triggered Structural Transformations, Aggregation, and Fibrillation of Human Alpha-Synuclein. A Possible Molecular Link Between Parkinson's Disease and Heavy Metal Exposure. J. Biol. Chem. 2001, 276, 44284-44296.
12. Khurana, R.; Ionescu-Zanetti, C.; pope, M.; Li, J.; Nielson, L.; Ramirez-Alvarado, M.; Regan, L.; Fink, A. L.; Carter, S. A. A General Model for Amyloid Fibril Assembly Based on Morphological Studies Using Atomic Force Microscopy. Biophys. J. 2003, 85, 1135-1144.
13. Rochet, J. C.; Conway, K. A.; Lansbury, P. T., Jr. Inhibition of Fibrillization and Accumulation of Prefibrillar Oligomers in Mixtures of Human and Mouse Alpha-Synuclein. Biochemistry 2000, 39, 10619-10626.
14. Uversky, V. N.; Li, J.; Fink, A. L. Evidence for a Partially Folded Intermediate in Alpha-Synuclein Fibril Formation. J. Biol. Chem. 2001, 276, 10737-10744.
15. Wetzel, R. For Protein Misassembly, It's the "I" Decade. Cell 1996, 86, 699-702.
16. Munishkina, L. A.; Phelan, C.; Uversky, V. N.; Fink, A. L. Conformational Behavior and Aggregation of Alpha-Synuclein in Organic Solvents: Modeling the Effects of Membranes. Biochemistry 2003, 42, 2720-2730.
17. Munishkina, L. A.; Henriques, J.; Uversky, V. N.; Fink, A. L. Role of Protein-Water Interactions and Electrostatics in Alpha-Synuclein Fibril Formation. Biochemistry 2004, 43, 3289-3300.
18. Li, J.; Uversky, V. N.; Fink, A. L. Conformational Behavior of Human Alpha-Synuclein Is Modulated by Familial Parkinson's Disease Point Mutations A30P and A53T. Neurotoxicology 2002, 23, 553-567.
19. Conway, K. A.; Harper, J. D.; Lansbury, P. T. Accelerated in Vitro Fibril Formation by a Mutant a-Synuclein Linked to Early-Onset Parkinson Disease. Nat. Med. 1998, 4, 1318-1320.
20. Conway, K. A.; Lee, S. J.; Rochet, J. C.; Ding, T. T.; Harper, J. D.; Williamson, R. E.; Lansbury, P. T., Jr. Accelerated Oligomerization by Parkinson's Disease Linked Alpha-Synuclein Mutants. Ann. N. Y. Acad. Sci. 2000, 920, 42-45.
21. Greenbaum, E. A.; Graves, C. L.; Mishizen-Eberz, A. J.; Lupoli, M. A.; Lynch, D. R.; Englander, S. W.; Axelsen, P. H.; Giasson, B. I. The E46K Mutation in Alpha-Synuclein Increases Amyloid Fibril Formation. J. Biol. Chem. 2005, 280, 7800-7807.
22. Hokenson, M. J.; Uversky, V. N.; Goers, J.; Yamin, G.; Munishkina, L. A.; Fink, A. L. Role of Individual Methionines in the Fibrillation of Methionine-Oxidized Alpha-Synuclein. Biochemistry 2004, 43, 4621-4633.
23. Conway, K. A.; Lee, S. J.; Rochet, J. C.; Ding, T. T.; Williamson, R. E.; Lansbury, P. T., Jr. Acceleration of Oligomerization, Not Fibrillization, Is a Shared Property of Both Alpha-Synuclein Mutations Linked to Early-Onset Parkinson's Disease: Implications for Pathogenesis and Therapy. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 571-576.
24. Kaylor, J.; Bodner, N.; Edridge, S.; Yamin, G.; Hong, D. P.; Fink, A. L. Characterization of Oligomeric Intermediates in α-Synuclein Fibrillation: FRET Studies of Y125W/Y133F/Y136F α-Synuclein. J. Mol. Biol. 2005, 353, 357-372.
25. Volles, M. J.; Lee, S. J.; Rochet, J. C.; Shtilerman, M. D.; Ding, T. T.; Kessler, J. C.; Lansbury, P. T., Jr. Vesicle Permeabilization by Protofibrillar Alpha-Synuclein: Implications for the Pathogenesis and Treatment of Parkinson's Disease. Biochemistry 2001, 40, 7812-7819.
26. Lashuel, H. A.; Petre, B. M.; Wall, J.; Simon, M.; Nowak, R. J.; Walz, T.; Lansbury, P. T., Jr. Alpha-Synuclein, Especially the Parkinson's Disease-Associated Mutants, Forms Pore-Like Annular and Tubular Protofibrils. J. Mol. Biol. 2002, 322, 1089-1102.
27. Deleted in proof.
28. Deleted in proof.
29. Dusa, A.; Kaylor, J.; Edridge, S.; Bodner, N.; Fink, A. L. Characterization of Oligomers During α-Synuclein Aggregation Using Intrinsic Tryptophan Fluorescence. Biochemistry 2006, 45, 2752-2760.
30. Uversky, V. N.; Yamin, G.; Souillac, P. O.; Goers, J.; Glaser, C. B.; Fink, A. L. Methionine Oxidation Inhibits Fibrillation of Human Alpha-Synuclein in Vitro. FEBS Lett. 2002, 517, 239-244.
31. Glaser, C. B.; Yamin, G.; Uversky, V. N.; Fink, A. L. Methionine Oxidation, Alpha-Synuclein and Parkinson's Disease. Biochim. Biophys. Acta 2005, 1703, 157-169.
32. Yamin, G.; Uversky, V. N.; Fink, A. L. Nitration Inhibits Fibrillation of Human Alpha-Synuclein in Vitro by Formation of Soluble Oligomers. FEBS Lett. 2003, 542, 147-152.
33. Uversky, V. N.; Yamin, G.; Munishkina, L. A.; Karyomov, M. A.; Millet, I. S.; Doniach, S.; Lyubchenko;, Y. L.; Fink, A. L. Effects of Nitration on the Structure and Aggregation of α-Synuclein. Mol. Brain Res. 2005, 134, 84-102.
34. Li, J.; Zhu, M.; Rajamani, S.; Uversky, V. N.; Fink, A. L. Rifampicin Inhibits Alpha-Synuclein Fibrillation and Disaggregates Fibrils. Chem. Biol. 2004, 11, 1513-1521.
35. Zhu, M.; Rajamani, S.; Kaylor, J.; Han, S.; Zhou, F.; Fink, A. L. The Flavonoid Baicalein Inhibits Fibrillation of Alpha-Synuclein and Disaggregates Existing Fibrils. J. Biol. Chem. 2004, 279, 26846-26857.
36. Qin, Z.; Hu, D.-M.; Han, S.; Reaney, S. H.; Di Monte, D. A.; Fink, A. L. Effect of 4-Hydroxy-2-Nonenal Modification on α-Synuclein Aggregation. J. Biol. Chem., submitted for publication, 2006.
37. Zhu, M.; Fink, A. L. Lipid Binding Inhibits Alpha-Synuclein Fibril Formation. J. Biol. Chem. 2003, 278, 16873-16877.
38. Jo, E.; McLaurin, J.; Yip, C. M.; George-Hyslop, P.; Fraser, P. E. Alpha-Synuclein Membrane Interactions and Lipid Specificity. J. Biol. Chem. 2000, 275, 34328-34334.
39. Davidson, W. S.; Jonas, A.; Clayton, D. F.; George, J. M. Stabilization of Alpha-Synuclein Secondary Structure Upon Binding to Synthetic Membranes. J. Biol. Chem. 1998, 273, 9443-9449.
40. Zhu, M.; Li, J.; Fink, A. L. The Association of Alpha-Synuclein With Membranes Affects Bilayer Structure, Stability, and Fibril Formation. J. Biol. Chem. 2003, 278, 40186-40197.
41. Lashuel, H. A.; Hartley, D.; Petre, B. M.; Walz, T.; Lansbury, P. T., Jr. Neurodegenerative Disease: Amyloid Pores From Pathogenic Mutations. Nature 2002, 418, 291.
42. Dixon, C.; Mathias, N.; Zweig, R. M.; Davis, D. A.; Gross, D. S. α-Synuclein Targets the Plasma Membrane via the Secretory Pathway and Induces Toxicity in Yeast. Genetics 2005, 170, 47-59.
43. Jenner, P.; Dexter, D. T.; Sian, J.; Schapira, A. H.; Marsden, C. D. Oxidative Stress as a Cause of Migral Cell Death in Parkinson's Disease and Incidental Lewy Body Disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 1992, 32 Suppl, S82-S87.
44. Yamin, G.; Glaser, C. B.; Uversky, V. N.; Fink, A. L. Certain Metals Trigger Fibrillation of Methionine-Oxidized α-Synuclein. J. Biol. Chem. 2003, 278, 27630-27635.
45. Minton, A. P. The Influence of Macromolecular Crowding and Macromolecular Confinement on Biochemical Reactions in Physiological Media. J. Biol. Chem. 2001, 276, 10577-10580.
46. Uversky, V. N.; Cooper, M.; Bower, K. S.; Li, J.; Fink, A. L. Accelerated Alpha-Synuclein Fibrillation in Crowded Milieu. FEBS Lett. 2002, 515, 99-103.
47. Shtilerman, M. D.; Ding, T. T.; Lansbury, P. T., Jr. Molecular Crowding Accelerates Fibrillization of α-Synuclein: Could an Increase in the Cytoplasmic Protein Concentration Induce Parkinson's Disease? Biochemistry 2002, 41, 3855-3860.
48. Cooper, E. M.; Uversky, V. N.; Fink, A. L. The Effect of Macromolecular Crowding Agents on Alpha-Synuclein Fibrillation. Biophys. J. 2002, 82, 323A.
49. Munishkina, L. A.; Cooper, E. M.; Uversky, V. N.; Fink, A. L. The Effect of Macromolecular Crowding on Protein Aggregation and Amyloid Fibril Formation. J. Mol. Recognit. 2004, 17, 456-464.
50. Yamin, G.; Munishkina, L. A.; Karymov, M. A.; Lyubchenko, Y. L.; Uversky, V. N.; Fink, A. L. Forcing Nonamyloidogenic β-Synuclein To Fibrillate. Biochemistry 2005, 44, 9096-9107.
51. Uversky, V. N.; Li, J.; Fink, A. L. Pesticides Directly Accelerate the Rate of Alpha-Synuclein Fibril Formation: a Possible Factor in Parkinson's Disease. FEBS Lett. 2001, 500, 105-108.
52. Manning-Bog, A. B.; McCormack, A. L.; Li, J.; Uversky, V. N.; Fink, A. L.; Di Monte, D. A. The Herbicide Paraquat Causes Up-Regulation and Aggregation of Alpha-Synuclein in Mice. J. Biol. Chem. 2002, 277, 1641-1644.
53. Uversky, V. N.; Li, J.; Zhu, M.; Bower, K.; Fink, A. L. Synergistic Effects of Pesticides and Metals on the Fibrillation of Alpha-Synuclein: Implications for Parkinson's Disease. Neurotoxicology 2002, 23, 527-536.
54. Berg, D.; Gerlach, M.; Youdim, M. B.; Double, K. L.; Zecca, L.; Riederer, P.; Becker, G. Brain Iron Pathways and Their Relevance to Parkinson's Disease. J. Neurochem. 2001, 79, 225-236.
55. Paik, S. R.; Shin, H. J.; Lee, J. H.; Chang, C. S.; Kim, J. Copper(II)-Induced Self-Oligomerization of Alpha-Synuclein. Biochem. J. 1999, 340 (Part 3), 821-828.
56. Cohlberg, J. A.; Li, J.; Uversky, V. N.; Fink, A. L. Heparin and Other Glycosaminoglycans Stimulate the Formation of Amyloid Fibrils From α-Synuclein in Vitro. Biochemistry 2002, 41, 1502-1511.
57. Liu, I. H.; Uversky, V. N.; Munishkina, L. A.; Fink, A. L.; Halfter, W.; Cole, G. J. Agrin Binds α-Synuclein and Modulates α-Synuclein Fibrillation. Glycobiology 2005, 15, 1320-1331.
58. Goers, J.; Uversky, V. N.; Fink, A. L. Polycation-Induced Oligomerization and Accelerated Fibrillation of Human Alpha-Synuclein in Vitro. Protein Sci. 2003, 12, 702-707.
59. Antony, T.; Hoyer, W.; Cherny, D.; Heim, G.; Jovin, T. M.; Subramaniam, V. Cellular Polyamines Promote the Aggregation of Alpha-Synuclein. J. Biol. Chem. 2003, 278, 3235-3240.
60. Uversky, V. N.; Li, J.; Fink, A. L. Trimethylamine-N-Oxide-Induced Folding of Alpha-Synuclein. FEBS Lett. 2001, 509, 31-35.
61. Norris, E. H.; Giasson, B. I.; Ischiropoulos, H.; Lee, V. M. Effects of Oxidative and Nitrative Challenges on Alpha-Synuclein Fibrillogenesis Involve Distinct Mechanisms of Protein Modifications. J. Biol. Chem. 2003, 278, 27230-27240.
62. Giasson, B. I.; Duda, J. E.; Murray, I. V.; Chen, Q.; Souza, J. M.; Hurtig, H. I.; Ischiropoulos, H.; Trojanowski, J. Q.; Lee, V. M. Oxidative Damage Linked to Neurodegeneration by Selective Alpha-Synuclein Nitration in Synucleinopathy Lesions. Science 2000, 290, 985-989.
63. Ischiropoulos, H.; Beckman, J. S. Oxidative Stress and Nitration in Neurodegeneration: Cause, Effect, or Association? J. Clin. Invest. 2003, 111, 163-169.
64. Uversky, V. N.; Yamin, G.; Munishkina, L. A.; Karymov, M. A.; Millett, I. S.; Doniach, S.; Lyubchenko, Y. L.; Fink, A. L. Effects of Nitration on the Structure and Aggregation of Alpha-Synuclein. Brain Res. Mol. Brain Res. 2005, 134, 84-102.
65. Uversky, V. N.; Li, J.; Souillac, P. O.; Millett, I. S.; Doniach, S.; Jakes, R.; Goedert, M.; Fink, A. L. Biophysical Properties of the Synucleins and Their Propensities to Fibrillate: Inhibition of Alpha-Synuclein Assembly by Beta- and Gamma-Synucleins. J. Biol. Chem. 2002, 277, 11970-11978.
66. Hashimoto, M.; Rockenstein, E.; Mante, M.; Mallory, M.; Masliah, E. Beta-Synuclein Inhibits Alpha-Synuclein Aggregation: A Possible Role as an Anti-Parkinsonian Factor. Neuron 2001, 32, 213-223.
67. Norris, E. H.; Giasson, B. I.; Hodara, R.; Xu, S.; Trojanowski, J. Q.; Ischiropoulos, H.; Lee, V. M. Reversible Inhibition of α-Synuclein Fibrillization by Dopaminochrome-Mediated Conformational Alterations. J. Biol. Chem. 2005, 280, 21212-21219.
68. Li, H. T.; Lin, D. H.; Luo, X. Y.; Zhang, F.; Ji, L. N.; Du, H. N.; Song, G. Q.; Hu, J.; Zhou, J. W.; Hu, H. Y. Inhibition of Alpha-Synuclein Fibrillization by Dopamine Analogs Via Reaction With the Amino Groups of Alpha-Synuclein. FEBS J. 2005, 272, 3661-3672.
69. Conway, K. A.; Rochet, J. C.; Bieganski, R. M.; Lansbury, P. T., Jr. Kinetic Stabilization of the Alpha-Synuclein Protofibril by a Dopamine- Alpha-Synuclein Adduct. Science 2001, 294, 1346-1349.
70. Li, J.; Zhu, M.; Manning-Bog, A. B.; Di Monte, D. A.; Fink, A. L. Dopamine and L-Dopa Disaggregate Amyloid Fibrils: Implications for Parkinson's and Alzheimer's Disease. FASEB J. 2004, 18, 962-964.