Monomeric synucleins generate membrane curvature

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1829-1840

  Westphal, Christopher H ^a,b   Chandra, Sreeganga S ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC; ENDOPHILIN; GAIN INSIGHT; KNOCK OUTS; MEMBRANE BINDING; MEMBRANE CURVATURE; MOLECULAR FUNCTION; N-TERMINALS; PARKINSON DISEASE; PHYSIOLOGICAL FUNCTIONS; PRESYNAPTIC; SYNAPTIC PROTEINS; SYNAPTIC VESICLE; SYNUCLEIN; VESICLE TRAFFICKING;

DISEASES; MEMBRANES; MOLECULAR BIOLOGY; PROTEIN FOLDING;

PROTEINS;

ALPHA SYNUCLEIN; BETA SYNUCLEIN; CELL PROTEIN; ENDOPHILIN; ENDOPHILIN A1; GAMMA SYNUCLEIN; MUTANT PROTEIN; SYNAPTIC PROTEIN; SYNUCLEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE INSERTION; HUMAN; MASS SPECTROMETRY; MEMBRANE BIOLOGY; MEMBRANE CURVATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEOMICS; REGULATORY MECHANISM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALPHA-SYNUCLEIN; ANIMALS; BETA-SYNUCLEIN; BRAIN CHEMISTRY; CELL MEMBRANE; CELL SHAPE; GAMMA-SYNUCLEIN; GENE EXPRESSION REGULATION; HUMANS; LIPOSOMES; MICE; MICE, KNOCKOUT; PARKINSON DISEASE; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEOMICS; RECOMBINANT FUSION PROTEINS; SYNAPTIC VESICLES;

EID: 84872744821     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.418871     Document Type: Article

References (67)

1. 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
2. Krüger, R., Kuhn, W., Müller, T., Woitalla, D., Graeber, M., Kösel, S., Przuntek, H., Epplen, J. T., Schöls, L., and Riess, O. (1998) A30P mutation in the gene encoding α-synuclein in Parkinson's disease. Nat. Genet. 18, 106-108
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., and Nussbaum, R. L. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047 (Pubitemid 27443610)
4. Zarranz, J. J., Alegre, J., Gómez-Esteban, J. C., Lezcano, E., Ros, R., Ampuero, I., Vidal, L., Hoenicka, J., Rodriguez, O., Atarés, B., Llorens, V., Gomez Tortosa, E., del Ser, T., Muñoz, 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)
5. Símon-Sánchez, J., Schulte, C., Bras, J. M., Sharma, M., Gibbs, J. R., Berg, D., Paisan-Ruiz, C., Lichtner, P., Scholz, S. W., Hernandez, D. G., Krüger, R., Federoff, M., Klein, C., Goate, A., Perlmutter, J., Bonin, M., Nalls, M. A., Illig, T., Gieger, C., Houlden, H., Steffens, M., Okun, M. S., Racette, B. A., Cookson, M. R., Foote, K. D., Fernandez, H. H., Traynor, B. J., Schreiber, S., Arepalli, S., Zonozi, R., Gwinn, K., van der Brug, M., Lopez, G., Chanock, S. J., Schatzkin, A., Park, Y., Hollenbeck, A., Gao, J., Huang, X., Wood, N. W., Lorenz, D., Deuschl, G., Chen, H., Riess, O., Hardy, J. A., Singleton, A. B., and Gasser, T. (2009) Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat. Genet. 41, 1308-1312
6. Satake, W., Nakabayashi, Y., Mizuta, I., Hirota, Y., Ito, C., Kubo, M., Kawaguchi, T., Tsunoda, T., Watanabe, M., Takeda, A., Tomiyama, H., Nakashima, K., Hasegawa, K., Obata, F., Yoshikawa, T., Kawakami, H., Sakoda, S., Yamamoto, M., Hattori, N., Murata, M., Nakamura, Y., and Toda, T. (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat. Genet. 41, 1303-1307
7. Murphy, D. D., Rueter, S. M., Trojanowski, J. Q., and Lee, V. M. (2000) Synucleins are developmentally expressed, and α-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 20, 3214-3220 (Pubitemid 30263139)
8. Cabin, D. E., Shimazu, K., Murphy, D., Cole, N. B., Gottschalk, W., McIlwain, K. L., Orrison, B., Chen, A., Ellis, C. E., Paylor, R., Lu, B., and Nussbaum, R. L. (2002) Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking α-synuclein. J. Neurosci. 22, 8797-8807 (Pubitemid 35379049)
9. Anwar, S., Peters, O., Millership, S., Ninkina, N., Doig, N., Connor-Robson, N., Threlfell, S., Kooner, G., Deacon, R. M., Bannerman, D. M., Bolam, J. P., Chandra, S. S., Cragg, S. J., Wade-Martins, R., and Buchman, V. L. (2011) Functional alterations to the nigrostriatal system in mice lacking all three members of the synuclein family. J. Neurosci. 31, 7264-7274
10. Ben Gedalya, T., Loeb, V., Israeli, E., Altschuler, Y., Selkoe, D. J., and Sharon, R. (2009) α-Synuclein and polyunsaturated fatty acids promote clathrin-mediated endocytosis and synaptic vesicle recycling. Traffic 10, 218-234
11. Burré, J., Sharma, M., Tsetsenis, T., Buchman, V., Etherton, M. R., and Südhof, T. C. (2010) α-Synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663-1667
12. Greten-Harrison, B., Polydoro, M., Morimoto-Tomita, M., Diao, L., Williams, A. M., Nie, E. H, Makani, S., Tian, N., Castillo, P. E., Buchman, V. L., Südhof, T. C., and Chandra, S. S. (2010) α-Synuclein triple knockout mice reveal age-dependent neuronal dysfunction. Proc. Natl. Acad. Sci. U.S.A. 107, 19573-19578
13. Nemani, V. M., Lu, W., Berge, V., Nakamura, K., Onoa, B., Lee, M. K., Chaudhry, F. A., Nicoll, R. A., and Edwards, R. H. (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65, 66-79
14. Gaugler, M. N., Genc, O., Bobela, W., Mohanna, S., Ardah, M. T., El-Agnaf, O. M., Cantoni, M., Bensadoun, J. C., Schneggenburger, R., Knott, G. W., Aebischer, P., and Schneider, B. L. (2012) Nigrostriatal overabundance of α-synuclein leads to decreased vesicle density and deficits in dopamine release that correlate with reduced motor activity. Acta Neuropathol. 123, 653-669
15. Davidson, W. S., Jonas, A., Clayton, D. F., and George, J. M. (1998) Stabilization of α-Synuclein in secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273, 9443-9449 (Pubitemid 28183026)
16. Bartels, T., Choi, J. G., and Selkoe, D. J. (2011) α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477, 107-110
17. Wang, W., Perovic, I., Chittuluru, J., Kaganovich, A., Nguyen, L. T., Liao, J., Auclair, J. R., Johnson, D., Landeru, A., Simorellis, A. K., Ju, S., Cookson, M. R., Asturias, F.J., Agar, J. N., Webb, B. N, Kang, C., Ringe, D., Petsko, G. A., Pochapsky, T. C., Hoang, Q. Q. (2011) A soluble α-synuclein construct forms a dynamic tetramer. Proc. Natl. Acad. Sci. U.S.A. 108, 17797-17802
18. Chandra, S., Chen, X., Rizo, J., Jahn, R., and Südhof, T. C. (2003) A broken α-helix in folded α-synuclein. J. Biol. Chem. 278, 15313-15318
19. Jao, C. C., Der-Sarkissian, A., Chen, J., and Langen, R. (2004) Structure of membrane-boundα-synuclein studied by site-directed spin labeling. Proc. Natl. Acad. Sci. U.S.A. 101, 8331-8336 (Pubitemid 38736575)
20. Ulmer, T. S., Bax, A., Cole, N. B., and Nussbaum, R. L. (2005) Structure and dynamics of micelle-bound human α-synuclein. J. Biol. Chem. 280, 9595-9603 (Pubitemid 40409655)
21. Ferreon, A. C., Gambin, Y., Lemke, E. A., and Deniz, A. A. (2009) Interplay of α-synuclein binding and conformational switching probed by singlemolecule fluorescence. Proc. Natl. Acad. Sci. U.S.A. 106, 5645-5650
22. Jao, C. C., Hegde, B. G., Chen, J., Haworth, I. S., and Langen, R. (2008) Structure of membrane-bound α-synuclein from site-directed spin labeling and computational refinement. Proc. Natl. Acad. Sci. U.S.A. 105, 19666-19671
23. Middleton, E. R., and Rhoades, E. (2010) Effects of curvature and composition on α-synuclein binding to lipid vesicles. Biophys. J. 99, 2279-2288
24. Clayton, D. F., and George, J. M. (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 58, 120-129 (Pubitemid 29463698)
25. Varkey, J., Isas, J. M., Mizuno, N., Jensen, M. B., Bhatia, V. K., Jao, C. C., Petrlova, J., Voss, J. C., Stamou, D. G., Steven, A. C., and Langen, R. (2010) Membrane curvature induction and tubulation are common features of synucleins and apolipoproteins. J. Biol. Chem. 285, 32486-32493
26. Pandey A. P., Haque, F., Rochet J. C., Hovis J. S. (2011) α-Synucleininduced tubule formation in lipid bilayers. J. Phys. Chem. B 115, 5886-5893
27. Mizuno, N., Varkey, J., Kegulian, N. C., Hegde, B. G., Cheng, N., Langen, R., Steven, A. C. (2012) Remodeling of lipid vesicles into cylindrical micelles byα-synuclein in an extendedα-helical conformation. J. Biol. Chem. 287, 29301-29311
28. Chandra, S., Gallardo, G., Fernández-Chacón, R., Schlüter, O. M., and Südhof, T. C. (2005) α-Synuclein cooperates with CSPα in preventing neurodegeneration. Cell 123, 383-396 (Pubitemid 41546670)
29. Huttner, W. B., Schiebler, W., Greengard, P., and De Camilli, P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374-1388 (Pubitemid 13029640)
30. Wu, T. L. (2006) Two dimensional difference gel electrophoresis. New Emerging Proteomics Techniques 328, 71-96
31. Zhang, Y. Q., Henderson, M. X., Colangelo, C. M., Ginsberg, S. D., Bruce, C., Wu, T., and Chandra, S. S. (2012) Identification of CSPα clients reveals a role in dynamin 1 regulation. Neuron 74, 136-150
32. Dávalos, A., Fernández-Hernando, C., Sowa, G., Derakhshan, B., Lin, M. I., Lee, J. Y., Zhao, H., Luo, R., Colangelo, C., and Sessa, W. C. (2010) Quantitative proteomics of caveolin-1-regulated proteins: characterization of polymerase I and transcript release factor/CAVIN-1 in endothelial cells. Mol. Cell Proteomics 9, 2109-2124
33. Shilov, I. V., Seymour, S. L., Patel, A. A., Loboda, A., Tang, W. H., Keating, S. P., Hunter, C. L., Nuwaysir, L. M., and Schaeffer, D. A. (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell Proteomics 6, 1638-1655 (Pubitemid 47506173)
34. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K., and De Camilli, P. (2001) Generation of high curvature membranes mediated by directed endophilin bilayer interactions. J. Cell Biol. 155, 193-200 (Pubitemid 34289294)
35. Takei, K., Slepnev, V. I., Haucke, V., and De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39 (Pubitemid 129495007)
36. Itoh, T., Erdmann, K. S., Roux, A., Habermann, B., Werner, H., and De Camilli, P. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (Pubitemid 41724107)
37. Tannu, N. S., and Hemby, S. E. (2006) Methods for proteomics in neuroscience. Prog Brain Res. 158, 41-82
38. Gallop, J. L., Jao, C. C., Kent, H. M., Butler, P. J., Evans, P. R., Langen, R., and McMahon, H. T. (2006) Mechanism of endophilin N-BAR domainmediated membrane curvature. EMBO J. 25, 2898-2910 (Pubitemid 43980396)
39. Haucke, V., Neher, E., and Sigrist, S. J. (2011) Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat. Rev. Neurosci. 12, 127-138
40. Hosaka, M., Hammer, R. E., and Südhof, T. C. (1999) A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24, 377-387 (Pubitemid 29508411)
41. Oling, F., Santos, J. S., Govorukhina, N., Mazères-Dubut, C., Bergsma-Schutter, W., Oostergetel, G., Keegstra, W., Lambert, O., Lewit-Bentley, A., and Brisson, A. (2000) Structure of membrane-bound annexin A5 trimers: A hybrid cryo-EM-X-ray crystallography study. J. Mol. Biol. 304, 561-573 (Pubitemid 32006190)
42. Henne, W. M., Kent, H. M., Ford, M. G., Hegde, B. G., Daumke, O., Butler, P. J., Mittal, R., Langen, R., Evans, P. R., and McMahon, H. T. (2007) Structure and analysis of FCHo2 F-BAR domain: A dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852 (Pubitemid 47042426)
43. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366
44. Mim, C., Cui, H., Gawronski-Salerno, J. A., Frost, A., Lyman, E., Voth, G. A., and Unger, V. M. (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137-145
45. Drin, G., and Antonny, B. (2010) Amphipathic helices and membrane curvature. FEBS Lett. 584, 1840-1847
46. Sorre, B., Callan-Jones, A., Manzi, J., Goud, B., Prost, J., Bassereau, P., and Roux, A. (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl. Acad. Sci. U.S.A. 109, 173-178
47. Nakajo, S., Tsukada, K., Kameyama, H., Furuyama, Y., and Nakaya, K. (1996) Distribution of phosphoneuroprotein 14 (PNP 14) in vertebrates: its levels as determined by enzyme immunoassay. Brain Res. 741, 180-184 (Pubitemid 26426314)
48. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Groønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S. A., Rammner, B., Gräter, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., Heuser, J., Wieland, F., and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (Pubitemid 44716256)
49. Jahn, R., and Südhof, T. C. (1993) Synaptic vesicle traffic: rush hour in the nerve terminal. J. Neurochem. 61, 12-21 (Pubitemid 23175879)
50. Fernandez-Busnadiego, R., Schrod, N., Kochovski, Z., Asano, S., Vanhecke, D., Baumeister, W., and Lucic, V. (2011) Insights into the molecular organization of the neuron by cryo-electron tomography. J. Electron Microsc. 60, S137-S148
51. Abeliovich, A., Schmitz, Y., Fariñas, I., Choi-Lundberg, D., Ho, W. H., Castillo, P. E., Shinsky, N., Verdugo, J. M., Armanini, M., Ryan, A., Hynes, M., Phillips, H., Sulzer, D., and Rosenthal, A. (2000) Mice lacking α-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239-252 (Pubitemid 30316525)
52. Farrer, M., Kachergus, J., Forno, L., Lincoln, S., Wang, D. S., Hulihan, M., Maraganore, D., Gwinn-Hardy, K., Wszolek, Z., Dickson, D., Langston, J. W. (2004) Comparison of kindreds with parkinsonism and α-synuclein genomic multiplications. Ann. Neurol. 55, 174-179 (Pubitemid 38166993)
53. Miller, D. W., Hague, S. M., Clarimon, J., Baptista, M., Gwinn-Hardy, K., Cookson, M. R., Singleton, A. B. (2004) α-Synuclein in blood and brain from familial Parkinson disease with SNCA locus triplication. Neurology 62, 1835-1838 (Pubitemid 38661745)
54. Jensen, P. H., Nielsen, M. S., Jakes, R., Dotti, C. G., and Goedert, M. (1998) Binding of α-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J. Biol. Chem. 273, 26292-26294 (Pubitemid 28471629)
55. Jo, E., Fuller, N., Rand, R. P., St George-Hyslop, P., and Fraser, P. E. (2002) Defective membrane interactions of familial Parkinson's disease mutant A30P α-synuclein. J. Mol. Biol. 315, 799-807 (Pubitemid 34729327)
56. Choi, W., Zibaee, S., Jakes, R., Serpell, L. C., Davletov, B., Crowther, R. A., Goedert, M. (2004) Mutation E46K increases phospholipid binding and assembly into filaments of human α-synuclein. FEBS Lett. 576, 363-368 (Pubitemid 39388629)
57. Yoon, Y., Tong, J., Lee, P. J., Albanese, A., Bhardwaj, N., Källberg, M., Digman, M. A., Lu, H., Gratton, E., Shin, Y. K., and Cho, W. (2010) Molecular basis of the potent membrane-remodeling activity of the epsin 1 N-terminal homology domain. J. Biol. Chem. 285, 531-540
58. Sung, Y. H., and Eliezer, D. (2006) Secondary structure and dynamics of micelle bound α-and α-synuclein. Protein Sci. 15, 1162-1174
59. Pranke, I. M., Morello, V., Bigay, J., Gibson, K., Verbavatz, J. M., Antonny, B., and Jackson, C. L. (2011) α-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding. J. Cell Biol. 194, 89-103
60. Drescher, M., Huber, M., and Subramaniam, V. (2012) Hunting the chameleon: structural conformations of the intrinsically disordered protein α-synuclein. Chembiochem 13, 761-768
61. Fauvet, B., Mbefo, M. K., Fares, M. B., Desobry, C., Michael, S., Ardah, M. T., Tsika, E., Coune, P., Prudent, M., Lion, N., Eliezer, D., Moore, D. J., Schneider, B., Aebischer, P., El-Agnaf, O. M., Masliah, E., and Lashuel, H. A. (2012)α-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer. J. Biol. Chem. 287, 15345-15364
62. + sensor for spontaneous neurotransmitter release. Science 327, 1614-1618
63. Hui, E., Johnson, C. P., Yao, J., Dunning, F. M., and Chapman, E. R. (2009) Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2α)-regulated fusion. Cell 138, 709-721
64. McMahon, H. T., Kozlov, M. M., and Martens, S. (2010) Membrane curvature in synaptic vesicle fusion and beyond. Cell 140, 601-605
65. Di Paolo, G., and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (Pubitemid 44564702)
66. Blondeau, F., Ritter, B., Allaire, P. D., Wasiak, S., Girard, M., Hussain, N. K., Angers, A., Legendre-Guillemin, V., Roy, L., Boismenu, D., Kearney, R. E., Bell, A. W., Bergeron, J. J., and McPherson, P. S. (2004) Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. U.S.A. 101, 3833-3838 (Pubitemid 38381064)
67. 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)