Conformational heterogeneity of α-synuclein in membrane

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 12, 2014, Pages 3107-3117

  Vermaas, Josh V ^a   Tajkhorshid, Emad ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

HMMM; Membrane binding; Molecular dynamics; Peripheral membrane protein; Synuclein

Indexed keywords

EID: 84925510085     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.08.012     Document Type: Article

References (75)

1. J. Burré, M. Sharma, T. Tsetsenis, V. Buchman, M.R. Etherton, T.C. Südhof, α- Synuclein promotes SNARE-complex assembly in vivo and in vitro, Science 329 (2010) 1663-1667.
2. J. Diao, J. Burré, S. Vivona, D.J. Cipriano, M. Sharma, M. Kyoung, T.C. Südhof, A.T. Brunger, Native α-synuclein induces clustering of synaptic-vesicle mimics via binding to phospholipids and synaptobrevin-2/VAMP2, eLife 2 (2013) e00592.
3. A.J. Lees, J. Hardy, T. Revesz, Parkinson's disease, Lancet 373 (2009) 13-19.
4. M.G. Spillantini, M.L. Schmidt, V.M.-Y. Lee, J.Q. Trojanowski, R. Jakes, M. Goedert, α-Synuclein in Lewy bodies, Nature 388 (1997) 839-840.
5. M.H. Polymeropoulous, C. Lavedan, E. Leroy, S.E. Ide, A. Deheija, A. Dutra, B. Pike, H. Root, J. Rubenstein, R. Boyer, E.S. Stenroos, S. Chandrasekharappa, A. Athanassiadou, T. Papapetropoulous, W.G. Johnson, A.M. Lazzarini, R.C. Duvosin, G.D. Iorio, L.I. Golbe, R.L. Nussbaum, Mutation in the α-synuclein gene identified in families with Parkinson's disease, Science 276 (1997) 2045-2047.
6. R. Krüger, W. Kuhn, T. Müller, D. Woitalla, M. Graeber, S. Kösel, H. Przuntek, J.T. Epplen, L. Schols, O. Riess, Ala SO Pro mutation in the gene encoding α-synuclein in Parkinson's disease, Nat. Genet. 18 (1998) 106-108.
7. J.J. Zarranz, J. Alegre, J.C. Gomez-Esteban, E. Lezcano, R. Ros, I. Ampuero, L. Vidal, J. Hoenicka, O. Rodriguez, B. Atares, V. Llorens, E.G. Tortosa, T. del Ser, D.G. Munoz, J. G. de Yebenes, The new mutation, E46K, or alpha-synuclein causes Parkinson and Lewy Body dementia, Ann. Neurol. 55 (2004) 164-173.
8. M.-C. Chartier-Harlin, J. Kachergus, C. Roumier, V. Mouroux, X. Douay, S. Lincoln, C. Levecque, L. Larvor, J. Andrieux, M. Hulihan, N. Waucquier, L. Defebvre, P. Amouyel, M. Farrer, A. Destée, α-Synuclein locus duplication as a cause of familial Parkinson's disease, Lancet 364 (2004) 1167-1169.
9. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, R. Nussbaum, S. Lincoln, A. Crawley, M. Hanson, D. Maraganore, C. Adler, M.R. Cookson, M. Muenter, M. Baptista, D. Miller, J. Blancato, J. Hardy, K. Gwinn-Hardy, α-Synuclein locus triplication causes Parkinson's disease, Science 302 (2003) 841.
10. I. Dikiy, D. Eliezer, Folding and misfolding of alpha-synuclein on membranes, Biochim. Biophys. Acta Biomembr. 1818 (2012) 1013-1018.
11. D. Boassa, M.L. Berlanga, M.A. Yang, M. Terada, J. Hu, E.A. Bushong, M. Hwang, E. Masliah, J.M. George, M.H. Ellisman, Mapping the subcellular distribution of α- synuclein in neurons using genetically encoded probes for correlated light and electron microscopy: implications for Parkinson's disease pathogenesis, J. Neurosci. 33 (2013) 2605-2615.
12. A. Iwai, E. Masliah, M. Yoshimoto, N. Ge, L. Flanagan, H.R. de Silva, A. Kittel, T. Saitoh, The precursor protein of non-Aβ component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system, Neuron 14 (1995) 467-475.
13. D.F. Clayton, J.M. George, The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease, Trends Neurosci. 21 (1998) 249-254.
14. C.G. Dudzik, E.D. Walter, B.S. Abrams, M.S. Jurica, G.L. Millhauser, Coordination of copper to the membrane-bound form of α-synuclein, Biochemistry 52 (2013) 53-60.
15. D.D.Murphy, S.M. Rueter, J.Q. Trojanowski, V.M. Lee, Synucleins are developmentally expressed, and α-Synuclin regulates the size of the presynaptic vesicular pool in primary hippocampal neurons, J. Neurosci. 20 (2000) 3214-3220.
16. D.E. Cabin, K. Shimazu, D. Murphy, N.B. Cole, W. Gottschalk, K.L. Mcllwain, B. Orrison, A. Chen, C.E. Ellis, R. Paylor, B. Lu, R.L. Nussbaum, Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking α-synuclein, J. Neurosci. 15 (2002) 8787-8807.
17. L. Yavich, H. Tanila, S. Vepsäläinen, P. Jäkälä, Role of α-synuclein in presynaptic dopamine recruitment, J. Neurosci. 8 (2004) 11165-11170.
18. S. Liu, I. Ninan, I. Antonova, F. Battaglia, F. Trinchese, A. Narasanna, N. Kolodilov, W. Dauer, R.D. Hawkins, O. Arancio, α-Synuclein produces a long-lasting increase in neurotransmitter release, EMBO J. 23 (2004) 4506-4516.
19. G. Rodriguez-Araujo, H. Nakagami, H. Hayashi, M. Mori, T. Shiuchi, Y. Minokoshi, Y. Nakaoka, Y. Takami, I. Komuro, R. Morishita, Y. Kaneda, Alpha-synuclein elicits glucose uptake and utilization in adipocytes through the Gab1/PI3K/Akt transduction pathway, Cell. Mol. Life Sci. 70 (2013) 1123-1133.
20. T.L. Yap, J.M. Gruschus, A. Velyati, W.Westbroek, E. Goldin, N. Moaven, E. Sidransky, J.C. Lee, α-Synuclein interacts with glucocerebrosidase providing a molecular link between Parkinson and Gaucher diseases, J. Biol. Chem. 286 (2011) 28080-28088.
21. B.-H. Ahn, H. Rhim, S.Y. Kim, Y.-M. Sung, M.-Y. Lee, J.-Y. Choi, B. Wolozin, J.-S. Chang, Y.H. Lee, T.K. Kwon, S.-H. Yoon, S.J. Hahn, M.-S. Kim, Y.-H. Jo, D.S. Min, α-Synuclein interacts with phospholipase D isozymes and inhibits pervanadate-induced phospholipase D activation in human embryonic kidney-293 cells, J. Biol. Chem. 277 (2002) 12334-12342.
22. E. Jo, J. McLaurin, C.M. Yip, P.S. George-Hyslop, P.E. Fraser, α-Synuclein membrane interactions and lipid specificity, J. Biol. Chem. 275 (2000) 34328-34334.
23. A.P. Pandey, F. Haque, J.-C. Rochet, J.S. Hovis, Clustering of α-synuclein on supported lipid bilayers: role of anionic lipid, protein, and divalent ion concentration, Biophys. J. 96 (2009) 540-551.
24. M. Necula, C.N. Chirita, J. Kuret, Rapid anionic micelle-mediated α-synuclein fibrillization in vitro, J. Biol. Chem. 278 (2003) 46674-46680.
25. E. Hellstrand, M. Grey, M.-L. Ainalem, J. Ankner, V.T. Forsyth, G. Fragneto, M. Haertlein, M.-T. Dauvergne, H. Nilsson, P. Brundin, S. Linse, T. Nylander, E. Sparr, Adsorption of α-synuclein to supported lipid bilayers: positioning and role of electrostatics, ACS Chem. Neurosci. 4 (2013) 1339-1351.
26. M. Grey, S. Linse, H.Nilsson, P. Brundin, E. Sparr, Membrane interaction of α-synuclin in different aggregation states, J. Park. Dis. 1 (2011) 359-371.
27. L. Tosatto, A.O. Andrighetti, N. Plotegher, V. Antonini, I. Tessari, L. Ricci, L. Bubacco, M. Dalla Serra, Alpha-synuclein pore forming activity upon membrane association, Biochim. Biophys. Acta Biomembr. 1818 (2012) 2876-2883.
28. I.F. Tsigelny, Y. Sharikov, W. Wrasidlo, T. Gonzalez, P.A. Desplats, L. Crews, B. Spencer, E. Masliah, Role of α-synuclein penetration into the membrane in the mechanisms of oligomer pore formation, FEBS J. 279 (2012) 1000-1013.
29. B. Winner, R. Jappelli, S.K. Maji, P.A. Desplats, L. Boyer, S. Aigner, C. Hetzer, T. Loher, M. Vilar, S. Campioni, C. Tzitzilonis, A. Soragni, S. Jessberger, H. Mira, A. Consiglio, E. Pham, E. Masliah, F.H. Gage, R. Riek, In vivo demonstration that α-synuclein oligomers are toxic, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 4194-4199.
30. M.J. Volles, S.-J. Lee, J.-C. Rochet, M.D. Shtilerman, T.T. Ding, J.C. Kessler, P.T. Lansbury Jr., Vesicle permeabilization by protofibrillar α-synuclein: implications for the pathogenesis and treatment of Parkinson's disease, Biochemistry 40 (2001) 7812-7819.
31. J. Wietek, I. Haralampiev, A. Amoussouvi, A. Herrmann, M. Stöckl, Membrane bound α-synuclein is fully embedded in the lipid bilayer while segments with higher flexibility remain, FEBS Lett. 587 (2013) 2572-2577.
32. T. Bartels, J.G. Choi, D.J. Selkoe, α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation, Nature 477 (2011) 107-110.
33. J.N. Rao, C.C. Jao, B.G. Hegde, R. Langen, T.S. Ulmer, A combinatorial NMR and EPR approach for evaluating the structural ensemble of partially folded proteins, J. Am. Chem. Soc. 132 (2010) 8657-8668.
34. M. Drescher, G. Veldhuis, B.D. van Rooijen, S. Milikisyants, V. Subramaniam, M. Huber, Antiparallel arrangement of the helices of vesicle-bound α-synuclein, J. Am. Chem. Soc. 130 (2008) 7796-7797.
35. T.S. Ulmer, A. Bax, N.B. Cole, R.L. Nussbaum, Structure and dynamics of micellebound human alpha-synuclein, J. Biol. Chem. 280 (2005) 9595-9603.
36. A.J. Trexler, E. Rhoades, α-Synuclein binds large unilamellar vesicles as an extended helix, Biochemistry 48 (2009) 2304-2306.
37. E.R. Georgieva, T.F. Ramlall, P.P. Borbat, J.H. Freed, D. Eliezer, Membrane-bound alpha-synuclein forms an extended helix: long-distance pulsed ESR measurements using vesicles, bicelles and rod-like micelles, J. Am. Chem. Soc. 130 (2008) 12856-12857.
38. C.C. Jao, B.G. Hegde, J. Chen, I.S. Haworth, R. Langen, Structure of membrane-bound α-synuclein from site-directed spin labeling and computational refinement, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 19666-19671.
39. C.C. Jao, A. Der-Sarkissian, J. Chen, R. Langen, Structure of membrane-bound α- synuclein studied by site-directed spin-labeling, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8331-8336.
40. P. Borbat, T.F. Ramlall, J.H. Freed, D. Eliezer, Inter-helix distances in lysophospholipid micelle-bound α-synuclein from pulsed ESR measurements, J. Am. Chem. Soc. 128 (2006) 10004-10005.
41. E.R. Middleton, E. Rhoades, Effects of curvature and composition on α-synuclein binding to lipid vesicles, Biophys. J. 99 (2010) 2279-2288.
42. M. Robotta, P. Braun, B. van Rooijen, V. Subramaniam, M. Huber, M. Drescher, Direct evidence of coexisting horseshoe and extended helix conformations of membranebound alpha-synuclein, Chem Phys Chem 12 (2011) 267-269.
43. E.R. Georgieva, T.F. Ramlall, P.P. Borbat, J.H. Freed, D. Eliezer, The lipid-binding domain of wild type and mutant α-synuclein: compactness and interconversion between the broken and extended helix forms, J. Biol. Chem. 285 (2010) 28261-28274.
44. S.B. Lokappa, T.S. Ulmer, Alpha-synuclein populates both elongated and broken helix states on small unilamellar vesicles, J. Biol. Chem. 286 (2011) 21450-21457.
45. G. Comellas, L.R. Lemkau, D.H. Zhou, J.M. George, C.M. Rienstra, Structural intermediates during α-synuclein fibrillogenesis on phospholipid vesicles, J. Am. Chem. Soc. 134 (2012) 5090-5099.
46. K. Vamvaca, M.J. Volles, P.T. Lansbury Jr., The first N-terminal amino acids of α-synuclein are essential for α-helical structure formation in vitro and membrane binding in yeast, J.Mol. Biol. 389 (2009) 413-424.
47. T. Bartels, L.S. Ahlstrom, A. Leftin, F. Kamp, C. Haass, M.F. Brown, K. Beyer, The N-terminus of the intrinsically disordered protein α-synuclein triggers membrane binding and helix folding, Biophys. J. 99 (2010) 2116-2124.
48. C.M. Pfefferkorn, F. Heinrich, A.J. Sodt, A.S. Maltsev, R.W. Pastor, J.C. Lee, Depth of α-synuclein in a bilayer determined by fluorescence, neutron reflectometry, and computation, Biophys. J. 102 (2012) 613-621.
49. A.S. Maltsev, J. Ying, A. Bax, Impact of N-terminal acetylation of α-synuclein on its random coil and lipid binding properties, Biochemistry 51 (2012) 5004-5013.
50. I. Dikiy, D. Eliezer, N-terminal acetylation stabilizes N-terminal helicity in lipid- And micelle-bound alpha-synuclein and increases its affinity for physiological membranes, J. Biol. Chem. 289 (2014) 3652-3665.
51. N. Lorenzen, L. Lemminger, J.N. Pedersen, S.r.B. Nielsen, D.E. Otzen, The N-terminus of α-synuclein is essential for both monomeric and oligomeric interactions with membranes, FEBS Lett. 588 (2014) 497-502.
52. J.D. Perlmutter, A.R. Braun, J.N. Sachs, Curvature dynamics of α-synuclein familial Parkinson disease mutants, J. Biol. Chem. 284 (2009) 7177-7189.
53. I.F. Tsigelny, P. Bar-On, Y. Sharikov, L. Crews, M. Hashimoto, M.A. Miller, S.H. Keller, O. Platoshyn, J.X.-J. Yuan, E. Masliah, Dynamics of α-synuclein aggregation and inhibition of pore-like oligomer development by β-synuclein, FEBS J. 274 (2007) 1862-1877.
54. A.R. Braun, E. Sevcsik, P. Chin, E. Rhoades, S. Tristram-Nagle, J.N. Sachs, α-Synuclein induces both positive mean curvature and negative Gaussian curvature in membranes, J. Am. Chem. Soc. 134 (2012) 2613-2620.
55. J.B. Klauda, B.R. Brooks, R.W. Pastor, Dynamical motions of lipids and a finite size effect in simulations of bilayers, J. Chem. Phys. 125 (2006) 144710.
56. J. Wohlert, O. Edholm, Dynamics in atomistic simulations of phospholipid membranes: nuclear magnetic resonance relaxation rates and lateral diffusion, J. Chem. Phys. 125 (2006) 204703.
57. S.J. Marrink, H.J. Risselada, S. Yefimov, D.P. Tieleman, A.H. de Vries, The MARTINI force field: coarse grained model for biomolecular simulations, J. Phys. Chem. B 111 (2007) 7812-7824.
58. P.S. Coppock, J.T. Kindt, Atomistic simulations of mixed-lipid bilayers in gel and fluid phases, Langmuir 25 (2009) 352-359.
59. Y.Z. Ohkubo, T.V. Pogorelov, M.J. Arcario, G.A. Christensen, E. Tajkhorshid, Accelerating membrane insertion of peripheral proteins with a novel membrane mimetic model, Biophys. J. 102 (2012) 2130-2139.
60. T.V. Pogorelov, J.V. Vermaas, M.J. Arcario, E. Tajkhorshid, Partitioning of amino acids into a model membrane: capturing the interface, J. Phys. Chem. B 118 (2014) 1481-1492.
61. J.V. Vermaas, E. Tajkhorshid, A microscopic view of phospholipid insertion into biological membranes, J. Phys. Chem. B 118 (2014) 1754-1764.
62. D. Eliezer, E. Kutluay, R. Bussell, G. Browne, Conformational properties of alphasynuclein in its free and lipid-associated states, J. Mol. Biol. 307 (2001) 1061-1073.
63. J.F. Nagle, S. Tristram-Nagle, Structure of lipid bilayers, Biochim. Biophys. Acta 1469 (2000) 159-195.
64. W. Humphrey, A. Dalke, K. Schulten, VMD - visual molecular dynamics, J. Mol. Graphics 14 (1996) 33-38.
65. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, K. Schulten, Scalable molecular dynamics with NAMD, J. Comput. Chem. 26 (2005) 1781-1802.
66. A.D. MacKerell Jr., M. Feig, C.L. Brooks III, Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations, J. Comput. Chem. 25 (2004) 1400-1415.
67. J.B. Klauda, R.M. Venable, J.A. Freites, J.W. O'Connor, D.J. Tobias, C. Mondragon- Ramirez, I. Vorobyov, A.D. MacKerell Jr., R.W. Pastor, Update of the CHARMM allatom additive force field for lipids: validation on six lipid types, J. Phys. Chem. B 114 (2010) 7830-7843.
68. T. Darden, D. York, L.G. Pedersen, Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems, J. Chem. Phys. 98 (1993) 10089-10092.
69. U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, L.G. Pedersen, A smooth particle mesh Ewald method, J. Chem. Phys. 103 (1995) 8577-8593.
70. G.J. Martyna, D.J. Tobias, M.L. Klein, Constant pressure molecular dynamics algorithms, J. Chem. Phys. 101 (1994) 4177-4189.
71. S.E. Feller, Y. Zhang, R.W. Pastor, B.R. Brooks, Constant pressuremolecular dynamics simulation: the Langevin piston method, J. Chem. Phys. 103 (1995) 4613-4621.
72. J.D. Hunter, Matplotlib: a 2D graphics environment, Comput. Sci. Eng. 9 (2007) 90-95.
73. F.B. Sheinerman, C.L. Brooks III, Calculations on folding of segment B1 of streptococcal protein G, J. Mol. Biol. 278 (1998) 439-456.
74. M. Krone, J.E. Stone, T. Ertl, K. Schulten, Fast visualization of Gaussian density surfaces for molecular dynamics and particle system trajectories, EuroVis - Short Papers 2012, 2012, pp. 67-71.
75. D. Frishman, P. Argos, Knowledge-based secondary structure assignment, Proteins 23 (1995) 566-579.