Structural role of compensatory amino acid replacements in the α-synuclein protein

Biochemistry

Volumn 50, Issue 32, 2011, Pages 6994-7001

  Losasso, Valeria ^a,b   Pietropaolo, Adriana ^c   Zannoni, Claudio ^d   Gustincich, Stefano ^a   Carloni, Paolo ^b  

^a SISSA   (Italy)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRIL FORMATION; HUMAN PROTEINS; INTRAMOLECULAR INTERACTIONS; NEURODEGENERATION; NUCLEAR MAGNETIC RESONANCE DATA; PARKINSON'S DISEASE; PHYSIOLOGICAL STRUCTURES; POINT MUTATIONS; STRUCTURAL INFORMATION; SYNUCLEIN; SYNUCLEIN PROTEINS; WILD TYPES; WILD-TYPE PROTEINS;

AMINO ACIDS; MAMMALS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; RESONANCE; STRUCTURE (COMPOSITION);

PROTEINS;

ALPHA SYNUCLEIN; COLLAGEN FIBRIL;

AMINO ACID SUBSTITUTION; AQUEOUS SOLUTION; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN STRUCTURE;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; ANIMALS; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

MUS; PRIMATES; RODENTIA;

EID: 80051521167     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2007564     Document Type: Article

References (66)

1. Shehadeh, L. A., Yu, K., Wang, L., Guevara, A., Singer, C., Vance, J., and Papapetropoulos, S. (2010) SRRM2, a potential blood biomarker revealing high alternative splicing in Parkinson's disease PLoS One 5, e9104
2. 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
3. Bonini, N. M. and Giasson, B. I. (2005) Snaring the function of α-synuclein Cell 123, 359-361
4. Lee, H. J., Choi, C., and Lee, S. J. (2002) Membrane-bound α-synuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form J. Biol. Chem. 277, 671-678 (Pubitemid 34952106)
5. Ulmer, T. S. and Bax, A. (2005) Comparison of structure and dynamics of micelle-bound human α-synuclein and Parkinson disease variants J. Biol. Chem. 280, 43179-43187 (Pubitemid 43049284)
6. Bertoncini, C. W., Jung, Y. S., Fernández, C. O., Hoyer, W., Griesinger, C., Jovin, T. M., and Zweckstetter, M. (2005) Release of long-range tertiary interactions potentiates aggregation of natively unstructured α-synuclein Proc. Natl. Acad. Sci. U.S.A. 102, 1430-1435 (Pubitemid 40209187)
7. Rasia, R. M., Bertoncini, C. W., Marsh, D., Hoyer, W., Cherny, D., Zweckstetter, M., Griesinger, C., Jovin, T. M., and Fernández, C. O. (2005) Structural characterization of copper(II) binding to α-synuclein: Insights into the bioinorganic chemistry of Parkinson's disease Proc. Natl. Acad. Sci. U.S.A. 102, 4294-4299 (Pubitemid 40397105)
8. Dedmon, M. M., Lindorff-Larsen, K., Christodoulou, J., Vendruscolo, M., and Dobson, C. M. (2005) Mapping long-range interactions in α-synuclein using spin-label and ensemble molecular dynamics simulations J. Am. Chem. Soc. 127, 476-477 (Pubitemid 40174345)
9. Hoyer, W., Cherny, D., Subramaniam, V., and Jovin, T. M. (2004) Impact of the acidic C-terminal region comprising amino acids 109-140 on α-synuclein aggregation in vitro Biochemistry 43, 16233-16242 (Pubitemid 40041036)
10. Hong, D. P., Xiong, W., Chang, J. Y., and Jiang, C. (2011) The role of the C-terminus of human α-synuclein: Intra-disulfide bonds between the C-terminus and other regions stabilize non-fibrillar monomeric isomers FEBS Lett. 585, 561-566
11. Eliezer, D., Kutluay, E., Bussell, R., and Browne, G. (2001) Conformational properties of α-synuclein in its free and lipid-associated states J. Mol. Biol. 307, 1961-1973
12. Maiti, N. C., Apetri, M. M., Zagorski, M. H., Carey, P. R., and Anderson, V. E. (2004) Raman spectroscopic characterization of secondary structure in natively unfolded protein: α-Synuclein J. Am. Chem. Soc. 126, 2399-2408 (Pubitemid 38295722)
13. Murray, I. V. J., Giasson, B. I., Quinn, S. M., Koppaka, V., Axelsen, P. H., Ischiropoulos, H., Trojanowsky, J. Q., and Lee, V. M. (2003) Role of α-synuclein carboxy-terminus on fibril formation in vitro Biochemistry 42, 8530-8540 (Pubitemid 36875420)
14. Bodles, A. M., Guthrie, D. J., Greer, B., and Irvine, G. B. (2001) Identification of the region of non-Aβ component (NAC) of Alzheimer's disease amyloid responsible for its aggregation and toxicity J. Neurochem. 78, 384-395 (Pubitemid 32664420)
15. 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
16. 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 (Pubitemid 37175274)
17. Del Mar, C., Greenbaum, E. A., Mayne, L., Englander, S. W., and Woods, V. L. (2005) Structure and properties of α-synuclein and other amyloids determined at the amino acid level Proc. Natl. Acad. Sci. U.S.A. 102, 15477-15482 (Pubitemid 41528082)
18. Waxman, E. A., Mazzulli, J. R., and Giasson, B. I. (2009) Characterization of hydrophobic residue requirements for α-synuclein fibrillization Biochemistry 48, 9427-9436
19. Shulman, J. M., De Jager, P. L., and Feany, M. B. (2011) Parkinson's disease: Genetics and pathogenesis Annu. Rev. Pathol. 6, 193-222
20. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kösel, S., Przuntek, H., Epplen, J. T., Schöls, L., and Riess, O. (1998) Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease Nat. Genet. 18, 106-108
21. 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 Tortosa, E., del Ser, T., Munoz, D. G., and de Yebenes, J. G. (2004) The new mutation, E46K, of α-synuclein causes Parkinson and Lewy-body dementia Ann. Neurol. 55, 164-173 (Pubitemid 38166992)
22. 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 (Pubitemid 27443610)
23. 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 (Pubitemid 28512115)
24. Fredenburg, R. A., Rospigliosi, C., Meray, R. K., Kessler, J. C., Lashuel, H. A., Eliezer, D., and Lansbury, P. T. (2007) The impact of the E46K mutation on the properties of α-synuclein in its monomeric and oligomeric states Biochemistry 46, 7107-1118
25. Heise, H., Celej, M. S., Becker, S., Riedel, D., Pelah, A., Kumar, A., Jovin, T. M., and Baldus, M. (2003) Solid-state NMR reveals structural differences between fibrils of wild-type and disease-related A53T mutant α-synuclein J. Mol. Biol. 380, 444-450
26. Suk, J. E., Lokappa, S. B., and Ulmer, T. S. (2010) The clustering and spatial arrangement of β-sheet sequence, but not order, govern α-synuclein fibrillogenesis Biochemistry 49, 1533-1540
27. Graham, D. R. and Sidhu, A. (2010) Mice expressing the A53T mutant form of human α-synuclein exhibit hyperactivity and reduced anxiety-like behavior J. Neurosci. Res. 88, 1777-1783
28. Giasson, B. I., Duda, J. E., Quinn, S. M., Zhang, B., Trojanowski, J. Q., and Lee, V. M. (2002) Neuronal α-synucleinopathy with severe movement disorder in mice expressing A53T human α-synuclein Neuron 34, 521-533 (Pubitemid 34628750)
29. Koprich, J. B., Johnston, T. H., Reyes, M. G., Sun, X., and Brotchie, J. M. (2010) Expression of human A53T α-synuclein in the rat substantia nigra using a novel AAV1/2 vector produces a rapidly evolving pathology with protein aggregation, dystrophic neurite architecture and nigrostriatal degeneration with potential to model the pathology of Parkinson's disease Mol. Neurodegener. 5, 43
30. Tsika, E., Moysidou, M., Guo, J., Cushman, M., Gannon, P., Sandaltzopoulos, R., Giasson, B. I., Krainc, D., Ischiropoulos, H., and Mazzulli, J. R. (2010) Distinct region-specific α-synuclein oligomers in A53T transgenic mice: Implications for neurodegeneration J. Neurosci. 30, 3409-3418
31. Gispert, S., Del Turco, D., Garrett, L., Chen, A., Bernard, D. J., Hamm-Clement, J., Korf, H. W., Deller, T., Braak, H., Auburger, G., and Nussbaum, R. L. (2003) Transgenic mice expressing mutant A53T human α-synuclein show neuronal dysfunction in the absence of aggregate formation Mol. Cell. Neurosci. 24, 419-429 (Pubitemid 37311305)
32. Kurz, A., Double, K. L., Lastres-Becker, I., Tozzi, A., Tantucci, M., Bockhart, V., Bonin, M., García-Arencibia, M., Nuber, S., Schlaudraff, F., Liss, B., Fernández-Ruiz, J., Gerlach, M., Wüllner, U., Lüddens, H., Calabresi, P., Auburger, G., and Gispert, S. (2010) A53T-α-synuclein overexpression impairs dopamine signaling and striatal synaptic plasticity in old mice PLoS One 5, e11464
33. Paleologou, K. E., Oueslati, A., Shakked, G., Rospigliosi, C. C., Kim, H. Y., Lamberto, G. R., Fernández, C. O., Schmid, A., Chegini, F., Gai, W. P., Chiappe, D., Moniatte, M., Schneider, B. L., Aebischer, P., Eliezer, D., Zweckstetter, M., Masliah, E., and Lashuel, H. A. (2010) Phosphorylation at S87 is enhanced in synucleinopathies, inhibits α-synuclein oligomerization, and influences synuclein-membrane interactions J. Neurosci. 30, 3184-3198
34. Bodner, C. R., Maltsev, A. S., Dobson, C. M., and Bax, A. (2010) Differential phospholipid binding of AS variants implicated in Parkinson's disease revealed by solution NMR spectroscopy Biochemistry 49, 862-871
35. Bussell, R. and Eliezer, D. (2001) Residual structure and dynamics in Parkinson's disease-associated mutants of α-synuclein J. Biol. Chem. 276, 45996-46003
36. Bertoncini, C. W., Fernández, C. O., Griesinger, C., Jovin, T. M., and Zweckstetter, M. (2005) Familial mutants of α-synuclein with increased neurotoxicity have a destabilized conformation J. Biol. Chem. 280, 30649-30652 (Pubitemid 41291792)
37. Lee, J. C., Langen, R., Hummel, P. A., Gray, H. B., and Winkler, J. R. (2004) α-Synuclein structures from fluorescence energy-transfer kinetics: Implications for the role of the protein in Parkinson's disease Proc. Natl. Acad. Sci. U.S.A. 101, 16466-16471 (Pubitemid 39557736)
38. Brucale, M., Sandal, M., Di Maio, S., Rampioni, A., Tessari, I., Tosatto, L., Bisaglia, M., Bubacco, L., and Samorì, B. (2009) Pathogenic mutations shift the equilibria of α-synuclein single molecules towards structured conformers ChemBioChem 10, 176-183
39. Perlmutter, J. D., Braun, A., and Sachs, J. N. (2009) Curvature dynamics of α-synuclein familial Parkinson disease mutants: Molecular simulations of the micelle- and bilayer-bound forms J. Biol. Chem. 284, 7177-7189
40. Mihajlovic, M. and Lazaridis, T. (2008) Membrane-bound structure and energetics of α-synuclein Proteins 70, 761-768
41. Bortolus, M., Tombolato, F., Tessari, I., Bisaglia, M., Mammi, S., Bubacco, L., Ferrarini, A., and Maniero, A. L. (2008) Broken helix in vesicle and micelle-bound α-synuclein: Insights from site-directed spin labeling-EPR experiments and MD simulations J. Am. Chem. Soc. 130, 6690-6691 (Pubitemid 351748389)
42. Wu, K. P., Kim, S., Fela, D. A., and Baum, J. (2008) Characterization of conformational and dynamic properties of natively unfolded human and mouse α-synuclein ensembles by NMR: Implications for aggregation J. Mol. Biol. 378, 1104-1115
43. Pietropaolo, A., Muccioli, L., Berardi, R., and Zannoni, C. (2008) A chirality index for investigating protein secondary structures and their time evolution Proteins 70, 667-677 (Pubitemid 351161929)
44. Pietropaolo, A., Muccioli, L., Zannoni, C., and Rizzarelli, E. (2009) Conformational preferences of the full chicken prion protein in solution and its differences with respect to mammals ChemPhysChem 10, 1500-1510
45. Micheletti, C., Seno, F., and Maritan, A. (2000) Recurrent oligomers in proteins: An optimal scheme reconciling accurate and concise backbone representations in automated folding and design studies Proteins 40, 662-674
46. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
47. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65, 712-725 (Pubitemid 44583220)
48. Aaqvist, J. (1990) Ion-water interaction potentials derived from free energy perturbation simulations J. Phys. Chem. 94, 8021-8024
49. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
50. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10093
51. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes J. Comput. Phys. 23, 327-341
52. Adelman, S. A. and Doll, J. D. (1976) Generalized Langevin equation approach for atom/solid surface scattering: General formulation for classical scattering off harmonic solids J. Chem. Phys. 64, 2375-2388
53. Feller, S. E., Zhang, Y., Pastor, R. W., and Brooks, B. R. (1995) Constant pressure molecular dynamics simulation: The Langevin piston method J. Chem. Phys. 103, 4613-4621
54. Phylips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
55. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14, 33-38 (Pubitemid 26152973)
56. Bulheller, B. M. and Hirst, J. D. (2009) DichroCalc: Circular and linear dichroism online Bioinformatics 25, 539-540
57. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260 (Pubitemid 32006234)
58. Glättli, A., Daura, X., Seebach, D., and van Gunsteren, W. F. (2002) Can one derive the conformational preference of a β-peptide from its CD spectrum? J. Am. Chem. Soc. 124, 12972-12978 (Pubitemid 35247108)
59. Teilum, K., Kragelund, B. B., and Poulsen, F. M. (2002) Transient structure formation in unfolded acyl-coenzyme A-binding protein observed by site-directed spin labelling J. Mol. Biol. 324, 349-357 (Pubitemid 35379033)
60. Futamura, N., Aluru, S., Ranjan, D., and Hariharan, B. (2002) Efficient parallel algorithms for solvent accessible surface area of proteins IEEE Transactions on Parallel Distributed Systems 13, 544-555 (Pubitemid 34835455)
61. Osipov, M. A., Pickup, B. T., and Dunmur, D. A. (1995) A new twist to molecular chirality: intrinsic chirality indices Mol. Phys. 84, 1193-1206
62. Solymosi, M., Low, R. J., Grayson, M., and Neal, M. P. (2002) A generalized scaling of a chiral index for molecules J. Chem. Phys. 116, 9875-9881 (Pubitemid 34690638)
63. Herrera, F. E., Chesi, A., Paleologou, K. E., Schmid, A., Munoz, A., Vendruscolo, M., Vendruscolo, M., Gustincich, S., Lashuel, H. A., and Carloni, P. (2008) Inhibition of α-synuclein fibrillization by dopamine is mediated by interactions with five C-terminal residues and with E83 in the NAC region PLoS One 3, e3394
64. Latawiec, D., Herrera, F. E., Bek, A., Losasso, V., Candotti, M., Benetti, F., Carlino, E., Kranjc, A., Lazzarino, M., Gustincich, S., Carloni, P., and Legname, G. (2010) Modulation of α-synuclein aggregation by dopamine analogs PLoS One 5, e9234
65. Sandal, M., Valle, F., Tessari, I., Mammi, S., Bergantino, E., Musiani, F., Brucale, M., Bubacco, L., and Samorì, B. (2008) Conformational equilibria in monomeric α-synuclein at the single-molecule level PLoS Biol. 6, 99-108
66. Wu, K. P., Weinstock, D. S., Narayanan, C., Levy, R. M., and Baum, J. B. (2009) Structural reorganization of α-synuclein at low pH observed by NMR and REMD simulations J. Mol. Biol. 391, 784-796