Impact of the acidic C-terminal region comprising amino acids 109-140 on α-synuclein aggregation in vitro

Biochemistry

Volumn 43, Issue 51, 2004, Pages 16233-16242

  Hoyer, Wolfgang ^a   Cherny, Dmitry ^a,b   Subramaniam, Vinod ^a,c   Jovin, Thomas M ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^c UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; BINDING ENERGY; ELECTRON MICROSCOPY; FLUORESCENCE; IONIC STRENGTH; LIGHT SCATTERING; MORPHOLOGY; PROTEINS; TURBIDITY;

AGGREGATION KINETICS; BIOGENIC POLYAMINES; FLUORESCENCE MICROSCOPY; NEURODEGENERATIVE DISORDERS;

AMINO ACIDS;

ALANINE; ALPHA SYNUCLEIN; AMINO ACID; MAGNESIUM CHLORIDE; MUTANT PROTEIN; PROLINE; SPERMINE; THIOFLAVINE; THREONINE;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; HUMAN; IN VITRO STUDY; IONIC STRENGTH; LIGHT SCATTERING; MOLECULAR INTERACTION; MUTATION; PARKINSON DISEASE; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; TURBIDITY;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; HUMANS; KINETICS; MICROSCOPY, ELECTRON; MUTATION; NERVE TISSUE PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; SYNUCLEINS; TIME FACTORS;

EID: 8544264002     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048453u     Document Type: Article

References (57)

1. Goedert, M. (2001) Alpha-synuclein and neurodegenerative diseases, Nat. Rev. Neurosci. 2, 492-501.
2. Dev, K. K., Hofele, K., Barbieri, S., Buchman, V. L., and van der Putten, H. (2003) Part II: α-Synuclein and its molecular pathophysiological role in neurodegenerative disease, Neuropharmacology 45, 14-44.
3. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) α-Synuclein in Lewy bodies, Nature 388, 839-840.
4. Baba, M., Nakajo, S., Tu, P. H., Tomita, T., Nakaya, K., Lee, V. M., Trojanowski, J. Q., and Iwatsubo, T. (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies, Am. J. Pathol. 152, 879-884.
5. Wakabayashi, K., Yoshimoto, M., Tsuji, S., and Takahashi, H. (1998) α-Synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy, Neurosci. Lett. 249, 180-182.
6. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J. T., Schols, L., and Riess, O. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease, Nat. Genet. 18, 106-108.
7. 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., and Nussbaum, R. L. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease, Science 276, 2045-2047.
8. Weinreb, P. H., Zhen, W., Poon, A. W., Conway, K. A., and Lansbury, P. T., Jr. (1996) NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded, Biochemistry 35, 13709-13715.
9. Hashimoto, M., Hsu, L. J., Sisk, A., Xia, Y., Takeda, A., Sundsmo, M., and Masliah, E. (1998) Human recombinant NACP/α-synuclein is aggregated and fibrillated in vitro: Relevance for Lewy body disease, Brain. Res. 799, 301-306.
10. Giasson, B. I., Uryu, K., Trojanowski, J. Q., and Lee, V. M. (1999) Mutant and wild-type human α-synucleins assemble into elongated filaments with distinct morphologies in vitro, J. Biol. Chem. 274, 7619-7622.
11. Serpell, L. C., Berriman, J., Jakes, R., Goedert, M., and Crowther, R. A. (2000) Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation, Proc. Natl. Acad. Sci. U.S.A. 97, 4897-4902.
12. Conway, K. A., Harper, J. D., and Lansbury, P. T., Jr. (2000) Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid, Biochemistry 39, 2552-2563.
13. Wood, S. J., Wypych, J., Steavenson, S., Louis, J. C., Citron, M., and Biere, A. L. (1999) α-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease, J. Biol. Chem. 274, 19509-19512.
14. Fernández, C. O., Hoyer, W., Zweckstetter, M., Jares-Erijman, E. A., Subramaniam, V., Griesinger, C., and Jovin, T. M. (2004) NMR of α-synuclein-polyamine complexes elucidates the mechanism and kinetics of induced aggregation, EMBO J. 23, 2039-2046.
15. Hoyer, W., Antony, T., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2002) Dependence of α-synuclein aggregate morphology on solution conditions, J. Mol. Biol. 322, 383-393.
16. Uversky, V. N., Li, J., and Fink, A. L. (2001) Evidence for a partially folded intermediate in α-synuclein fibril formation, J. Biol. Chem. 276, 10737-10744.
17. Uversky, V. N., Li, J., and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein, J. Biol. Chem. 276, 44284-44296.
18. Paik, S. R., Shin, H. J., Lee, J. H., Chang, C. S., and Kim, J. (1999) Copper(II)-induced self-oligomerization of α-synuclein, Biochem. J. 340, 821-828.
19. 2+ binding to α-synuclein regulates ligand binding and oligomerization, J. Biol. Chem. 276, 22680-22684.
20. Kim, T. D., Paik, S. R., Yang, C. H., and Kim, J. (2000) Structural changes in α-synuclein affect its chaperone-like activity in vitro, Protein. Sci. 9, 2489-2496.
21. Antony, T., Hoyer, W., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2003) Cellular polyamines promote the aggregation of α-synuclein, J. Biol. Chem. 278, 3235-3240.
22. Goers, J., Uversky, V. N., and Fink, A. L. (2003) Polycation-induced oligomerization and accelerated fibrillation of human α-synuclein in vitro, Protein. Sci. 12, 702-707.
23. Conway, K. A., Lee, S. J., Rochet, J. C., Ding, T. T., Williamson, R. E., and Lansbury, P. T., Jr. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: Implications for pathogenesis and therapy, Proc. Natl. Acad. Sci. U.S.A. 97, 571-576.
24. Ding, T. T., Lee, S. J., Rochet, J. C., and Lansbury, P. T., Jr. (2002) Annular α-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes, Biochemistry 41, 10209-10217.
25. Lashuel, H. A., Petre, B. M., Wall, J., Simon, M., Nowak, R. J., Walz, T., and Lansbury, P. T., Jr. (2002) α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils, J. Mol. Biol. 322, 1089-1102.
26. Hoyer, W., Cherny, D., Subramaniam, V., and Jovin, T. M. (2004) Rapid self-assembly of α-synuclein observed by in situ atomic force microscopy, J. Mol. Biol. 340, 127-139.
27. Chandra, S., Chen, X., Rizo, J., Jahn, R., and Sudhof, T. C. (2003) A broken α-helix in folded α-synuclein, J. Biol. Chem. 278, 15313-15318.
28. Bussell, R., Jr., and Eliezer, D. (2003) A structural and functional role for 11-mer repeats in α-synuclein and other exchangeable lipid binding proteins, J. Mol. Biol. 329, 763-778.
29. Giasson, B. I., Murray, I. V., Trojanowski, J. Q., and Lee, V. M. (2001) A hydrophobic stretch of 12 amino acid residues in the middle of α-synuclein is essential for filament assembly, J. Biol. Chem. 276, 2380-2386.
30. Du, H. N., Tang, L., Luo, X. Y., Li, H. T., Hu, J., Zhou, J. W., and Hu, H. Y. (2003) A peptide motif consisting of glycine, alanine, and valine is required for the fibrillization and cytotoxicity of human α-synuclein, Biochemistry 42, 8870-8878.
31. Park, S. M., Jung, H. Y., Chung, K. C., Rhim, H., Park, J. H., and Kim, J. (2002) Stress-induced aggregation profiles of GST-α-synuclein fusion proteins: Role of the C-terminal acidic tail of α-synuclein in protein thermosolubility and stability, Biochemistry 41, 4137-4146.
32. Souza, J. M., Giasson, B. I., Lee, V. M., and Ischiropoulos, H. (2000) Chaperone-like activity of synucleins, FEBS Lett. 474, 116-119.
33. Park, S. M., Jung, H. Y., Kim, T. D., Park, J. H., Yang, C. H., and Kim, J. (2002) Distinct roles of the N-terminal-binding domain and the C-terminal-solubilizing domain of α-synuclein, a molecular chaperone, J. Biol. Chem. 277, 28512-28520.
34. Kim, T. D., Paik, S. R., and Yang, C. H. (2002) Structural and functional implications of C-terminal regions of α-synuclein, Biochemistry 41, 13782-13790.
35. Crowther, R. A., Jakes, R., Spillantini, M. G., and Goedert, M. (1998) Synthetic filaments assembled from C-terminally truncated α-synuclein, FEBS Lett. 436, 309-312.
36. Murray, I. V., Giasson, B. I., Quinn, S. M., Koppaka, V., Axelsen, P. H., Ischiropoulos, H., Trojanowski, J. Q., and Lee, V. M. (2003) Role of α-synuclein carboxy-terminus on fibril formation in vitro, Biochemistry 42, 8530-8540.
37. Fujiwara, H., Hasegawa, M., Dohmae, N., Kawashima, A., Masliah, E., Goldberg, M. S., Shen, J., Takio, K., and Iwatsubo, T. (2002) α-Synuclein is phosphorylated in synucleinopathy lesions, Nat. Cell. Biol. 4, 160-164.
38. Giasson, B. I., Duda, J. E., Murray, I. V., Chen, Q., Souza, J. M., Hurtig, H. I., Ischiropoulos, H., Trojanowski, J. Q., and Lee, V. M. (2000) Oxidative damage linked to neurodegeneration by selective α-synuclein nitration in synucleinopathy lesions, Science 290, 985-989.
39. Crowther, R. A., Daniel, S. E., and Goedert, M. (2000) Characterisation of isolated α-synuclein filaments from substantia nigra of Parkinson's disease brain, Neurosci. Lett. 292, 128-130.
40. Der-Sarkissian, A., Jao, C. C., Chen, J., and Langen, R. (2003) Structural organization of α-synuclein fibrils studied by site-directed spin labeling, J. Biol. Chem. 278, 37530-37535.
41. Miake, H., Mizusawa, H., Iwatsubo, T., and Hasegawa, M. (2002) Biochemical characterization of the core structure of α-synuclein filaments, J. Biol. Chem. 277, 19213-19219.
42. Conway, K. A., Harper, J. D., and Lansbury, P. T. (1998) Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson disease, Nat. Med. 4, 1318-1320.
43. Narhi, L., Wood, S. J., Steavenson, S., Jiang, Y., Wu, G. M., Anafi, D., Kaufman, S. A., Martin, F., Sitney, K., Denis, P., Louis, J. C., Wypych, J., Biere, A. L., and Citron, M. (1999) Both familial Parkinson's disease mutations accelerate α-synuclein aggregation, J. Biol. Chem. 274, 9843-9846.
44. Li, J., Uversky, V. N., and Fink, A. L. (2001) Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human α-synuclein, Biochemistry 40, 11604-11613.
45. Dawson, R. M. C., Elliott, D. C., Elliott, W. H., and Jones, K. M. (1986) Data for biochemical research, 3rd ed., Oxford Science Publications.
46. Dubochet, J., Ducommun, M., Zollinger, M., and Kellenberger, E. (1971) A new preparation method for dark-field electron microscopy of biomacromolecules, J. Ultrastruct. Res. 35, 147-167.
47. Chili, F., Calamai, M., Taddei, N., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases, Proc. Natl. Acad. Sci. U.S.A. 99, 16419-16426.
48. Chili, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Ralionalizalion of the effecls of mutations on peptide and protein aggregation rates, Nature 424, 805-808.
49. Schmittschmitt, J. P., and Schottz, J. M. (2003) The role of protein stability, solubility, and net charge in amyloid fibril formation, Protein Sci. 12, 2374-2378.
50. Chityi, F., Taddei, N., Baroni, F., Capanni, C., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Kinetic partitioning of protein folding and aggregation, Nat. Struct. Biol. 9, 137-143.
51. Pavlov, N. A., Cherny, D. I., Heim, G., Jovin, T. M., and Subramaniam, V. (2002) Amyloid fibrils from the mammalian protein prothymosin α, FEBS Lett. 517, 37-40.
52. Park, S. M., Ahn, K. J., Jung, H. Y., Park, J. H., and Kim, J. (2004) Effects of novel peptides derived from the acidic tail of synuclein (ATS) on the aggregation and stability of fusion proteins, Protein Eng. Des. Sel. 17, 251-260.
53. McLean, P. J., and Hyman, B. T. (2002) An alternatively spliced form of rodent α-synuclein forms intracellular inclusions in vitro: Role of the carboxy-terminus in α-synuclein aggregation, Neurosci. Lett. 323, 219-223.
54. Chou, P. Y., and Fasman, G. D. (1978) Empirical prediclions of protein conformation, Annu. Rev. Biochem. 47, 251-276.
55. Gomes-Trolin, C., Nygren, I., Aquilonius, S. M., and Askmark, H. (2002) Increased red blood cell polyamines in ALS and Parkinson's disease, Exp. Neurol. 177, 515-520.
56. Lai, B. C., Marion, S. A., Teschke, K., and Tsui, J. K. (2002) Occupational and environmental risk factors for Parkinson's disease, Parkinsonism Relat. Disord. 8, 297-309.
57. Wolozin, B., and Golts, N. (2002) Iron and Parkinson's disease, Neuroscientist 8, 22-32.