Nonaggregated α-synuclein influences snare-dependent vesicle docking via membrane binding

Biochemistry

Volumn 53, Issue 24, 2014, Pages 3889-3896

  Lai, Ying ^a   Kim, Sunae ^a   Varkey, Jobin ^b,c   Lou, Xiaochu ^a   Song, Jae Kyun ^a   Diao, Jiajie ^d   Langen, Ralf ^c   Shin, Yeon Kyun ^a,e  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF RAJASTHAN   (India)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d XI'AN JIAOTONG UNIVERSITY   (China)

^e Korea Institute of Science and Technology   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES;

FLUORESCENCE METHOD; IN-VITRO ASSAYS; LIPOSOME FUSION; MEMBRANE BINDING; MEMBRANE FUSION; NEUROTRANSMITTER RELEASE; OVER-EXPRESSION; PARKINSON'S DISEASE;

NEUROPHYSIOLOGY;

ALPHA SYNUCLEIN; LIPOSOME; SNARE PROTEIN; SYNAPTOBREVIN 2;

ARTICLE; CONTROLLED STUDY; ENERGY TRANSFER; IN VITRO STUDY; LIPID BILAYER; MEMBRANE BINDING; MEMBRANE FUSION; MEMBRANE VESICLE; MOLECULAR DOCKING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SYNAPSE VESICLE;

ALPHA-SYNUCLEIN; BIOLOGICAL TRANSPORT; EXOCYTOSIS; MEMBRANE FUSION; MEMBRANE LIPIDS; SNARE PROTEINS; SYNAPTIC VESICLES; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84903164193     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5002536     Document Type: Article

References (53)

1. Choi et al. Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (10), 4087 - 4092
2. Choi, B. K., Choi, M. G., Kim, J. Y., Yang, Y., Lai, Y., Kweon, D. H., Lee, N. K., and Shin, Y. K. (2013) Large alpha-synuclein oligomers inhibit neuronal SNARE-mediated vesicle docking Proc. Natl. Acad. Sci. U. S. A. 110 (10) 4087-4092
3. Hardy, J. and Gwinn-Hardy, K. (1998) Genetic classification of primary neurodegenerative disease Science 282 (5391) 1075-1079
4. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) Alpha-synuclein in Lewy bodies Nature 388 (6645) 839-840
5. Shimohama, S., Sawada, H., Kitamura, Y., and Taniguchi, T. (2003) Disease model: Parkinson's disease Trends Mol. Med. 9 (8) 360-365
6. Lee, V. M. and Trojanowski, J. Q. (2006) Mechanisms of Parkinson's disease linked to pathological alpha-synuclein: new targets for drug discovery Neuron 52 (1) 33-38
7. Dev, K. K., Hofele, K., Barbieri, S., Buchman, V. L., and van der Putten, H. (2003) Part II: alpha-synuclein and its molecular pathophysiological role in neurodegenerative disease Neuropharmacology 45 (1) 14-44
8. Conway, K. A., Lee, S. J., Rochet, J. C., Ding, T. T., Harper, J. D., Williamson, R. E., and Lansbury, P. T., Jr. (2000) Accelerated oligomerization by Parkinson's disease linked alpha-synuclein mutants Ann. N. Y. Acad. Sci. 920, 42-45
9. 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 alpha-synuclein gene identified in families with Parkinson's disease Science 276 (5321) 2045-2047
10. Burre, J., Vivona, S., Diao, J., Sharma, M., Brunger, A. T., and Sudhof, T. C. (2013) Properties of native brain alpha-synuclein Nature 498 (7453) E4-6 discussion E6-7
11. Maroteaux, L., Campanelli, J. T., and Scheller, R. H. (1988) Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal J. Neurosci. 8 (8) 2804-2815
12. George, J. M., Jin, H., Woods, W. S., and Clayton, D. F. (1995) Characterization of a novel protein regulated during the critical period for song learning in the zebra finch Neuron 15 (2) 361-372
13. Steidl, J. V., Gomez-Isla, T., Mariash, A., Ashe, K. H., and Boland, L. M. (2003) Altered short-term hippocampal synaptic plasticity in mutant alpha-synuclein transgenic mice NeuroReport 14 (2) 219-223
14. Watson, J. B., Hatami, A., David, H., Masliah, E., Roberts, K., Evans, C. E., and Levine, M. S. (2009) Alterations in corticostriatal synaptic plasticity in mice overexpressing human alpha-synuclein Neuroscience 159 (2) 501-513
15. Cooper, A. A., Gitler, A. D., Cashikar, A., Haynes, C. M., Hill, K. J., Bhullar, B., Liu, K., Xu, K., Strathearn, K. E., Liu, F., Cao, S., Caldwell, K. A., Caldwell, G. A., Marsischky, G., Kolodner, R. D., Labaer, J., Rochet, J. C., Bonini, N. M., and Lindquist, S. (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models Science 313 (5785) 324-328
16. Gitler, A. D., Bevis, B. J., Shorter, J., Strathearn, K. E., Hamamichi, S., Su, L. J., Caldwell, K. A., Caldwell, G. A., Rochet, J. C., McCaffery, J. M., Barlowe, C., and Lindquist, S. (2008) The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis Proc. Natl. Acad. Sci. U. S. A. 105 (1) 145-150
17. Larsen, K. E., Schmitz, Y., Troyer, M. D., Mosharov, E., Dietrich, P., Quazi, A. Z., Savalle, M., Nemani, V., Chaudhry, F. A., Edwards, R. H., Stefanis, L., and Sulzer, D. (2006) Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis J. Neurosci. 26 (46) 11915-11922
18. Mosharov, E. V., Staal, R. G., Bove, J., Prou, D., Hananiya, A., Markov, D., Poulsen, N., Larsen, K. E., Moore, C. M., Troyer, M. D., Edwards, R. H., Przedborski, S., and Sulzer, D. (2006) Alpha-synuclein overexpression increases cytosolic catecholamine concentration J. Neurosci. 26 (36) 9304-9311
19. 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 (1) 66-79
20. 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., and Chandra, S. S. (2010) alphabetagamma-Synuclein triple knockout mice reveal age-dependent neuronal dysfunction Proc. Natl. Acad. Sci. U. S. A. 107 (45) 19573-19578
21. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution Nature 395 (6700) 347-353
22. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Sollner, T. H., and Rothman, J. E. (1998) SNAREpins: Minimal machinery for membrane fusion Cell 92 (6) 759-772
23. Brunger, A. T. (2005) Structure and function of SNARE and SNARE-interacting proteins Q. Rev. Biophys. 38 (1) 1-47
24. Jahn, R. and Scheller, R. H. (2006) SNAREs - engines for membrane fusion Nat. Rev. Mol. Cell Biol. 7 (9) 631-643
25. Poirier, M. A., Xiao, W., Macosko, J. C., Chan, C., Shin, Y. K., and Bennett, M. K. (1998) The synaptic SNARE complex is a parallel four-stranded helical bundle Nat. Struct. Biol. 5 (9) 765-769
26. Burre, J., Sharma, M., Tsetsenis, T., Buchman, V., Etherton, M. R., and Sudhof, T. C. (2010) Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro Science 329 (5999) 1663-1667
27. Chandra, S., Gallardo, G., Fernandez-Chacon, R., Schluter, O. M., and Sudhof, T. C. (2005) Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration Cell 123 (3) 383-396
28. Thayanidhi, N., Helm, J. R., Nycz, D. C., Bentley, M., Liang, Y., and Hay, J. C. (2010) Alpha-synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs Mol. Biol. Cell 21 (11) 1850-1863
29. DeWitt, D. C. and Rhoades, E. (2013) alpha-Synuclein Can Inhibit SNARE-Mediated Vesicle Fusion through Direct Interactions with Lipid Bilayers Biochemistry 52 (14) 2385-2387
30. Bodner, C. R., Maltsev, A. S., Dobson, C. M., and Bax, A. (2010) Differential phospholipid binding of alpha-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy Biochemistry 49 (5) 862-871
31. Scott, D. A., Tabarean, I., Tang, Y., Cartier, A., Masliah, E., and Roy, S. (2010) A pathologic cascade leading to synaptic dysfunction in alpha-synuclein-induced neurodegeneration J. Neurosci. 30 (24) 8083-8095
32. Brunger, A. T., Weninger, K., Bowen, M., and Chu, S. (2009) Single-Molecule Studies of the Neuronal SNARE Fusion Machinery Annu. Rev. Biochem. 78, 903-928
33. Diao, J., Ishitsuka, Y., and Bae, W. R. (2011) Single-molecule FRET study of SNARE-mediated membrane fusion Biosci. Rep. 31 (6) 457-463
34. Cypionka, A., Stein, A., Hernandez, J. M., Hippchen, H., Jahn, R., and Walla, P. J. (2009) Discrimination between docking and fusion of liposomes reconstituted with neuronal SNARE-proteins using FCS Proc. Natl. Acad. Sci. U. S. A. 106 (44) 18575-18580
35. Christensen, S. M., Mortensen, M. W., and Stamou, D. G. (2011) Single Vesicle Assaying of SNARE-Synaptotagmin-Driven Fusion Reveals Fast and Slow Modes of Both Docking and Fusion and Intrasample Heterogeneity Biophys. J. 100 (4) 957-967
36. Diao, J., Yoon, T. Y., Su, Z. L., Shin, Y. K., and Ha, T. (2009) C2AB: A Molecular Glue for Lipid Vesicles with a Negatively Charged Surface Langmuir 25 (13) 7177-7180
37. Smith, E. A. and Weisshaar, J. C. (2011) Docking, Not Fusion, as the Rate-Limiting Step in a SNARE-Driven Vesicle Fusion Assay Biophys. J. 100 (9) 2141-2150
38. Yoon, T. Y., Lu, X., Diao, J. J., Lee, S. M., Ha, T., and Shin, Y. K. (2008) Complexin and Ca(2+) stimulate SNARE-mediated membrane fusion Nat. Struct Mol. Biol. 15 (7) 707-713
39. Kyoung, M., Srivastava, A., Zhang, Y. X., Diao, J. J., Vrljic, M., Grob, P., Nogales, E., Chu, S., and Brunger, A. T. (2011) In vitro system capable of differentiating fast Ca(2+)-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release Proc. Natl. Acad. Sci. U. S. A. 108 (29) E304-E313
40. Karatekin, E., Di Giovanni, J., Iborra, C., Coleman, J., O'Shaughnessy, B., Seagar, M., and Rothman, J. E. (2010) A fast, single-vesicle fusion assay mimics physiological SNARE requirements Proc. Natl. Acad. Sci. U. S. A. 107 (8) 3517-3521
41. Domanska, M. K., Kiessling, V., Stein, A., Fasshauer, D., and Tamm, L. K. (2009) Single Vesicle Millisecond Fusion Kinetics Reveals Number of SNARE Complexes Optimal for Fast SNARE-mediated Membrane Fusion J. Biol. Chem. 284 (46) 32158-32166
42. Liu, T. T., Tucker, W. C., Bhalla, A., Chapman, E. R., and Weisshaar, J. C. (2005) SNARE-driven, 25-ms vesicle fusion in vitro Biophys. J. 89 (4) 2458-2472
43. Diao, J., Su, Z. L., Lu, X. B., Yoon, T. Y., Shin, Y. K., and Ha, T. (2010) Single-Vesicle Fusion Assay Reveals Munc18-1 Binding to the SNARE Core Is Sufficient for Stimulating Membrane Fusion ACS Chem. Neurosci. 1 (3) 168-174
44. Diao, J., Cipriano, D. J., Zhao, M., Zhang, Y., Shah, S., Padolina, M. S., Pfuetzner, R. A., and Brunger, A. T. (2013) Complexin-1 enhances the on-rate of vesicle docking via simultaneous SNARE and membrane interactions J. Am. Chem. Soc. 135 (41) 15274-15277
45. Lai, Y., Lou, X., Jho, Y., Yoon, T. Y., and Shin, Y. K. (2013) The synaptotagmin 1 linker may function as an electrostatic zipper that opens for docking but closes for fusion pore opening Biochem. J. 456 (1) 25-33
46. Diao, J. J., Zhao, M. L., Zhang, Y. X., Kyoung, M., and Brunger, A. T. (2013) Studying protein-reconstituted proteoliposome fusion with content indicators in vitro Bioessays 35 (7) 658-665
47. Diao, J., Su, Z. L., Ishitsuka, Y., Lu, B., Lee, K. S., Lai, Y., Shin, Y. K., and Ha, T. (2010) A single-vesicle content mixing assay for SNARE-mediated membrane fusion Nat. Commun. doi:10.1038/ncomms1054
48. Diao, J., Grob, P., Cipriano, D. J., Kyoung, M., Zhang, Y., Shah, S., Nguyen, A., Padolina, M., Srivastava, A., Vrljic, M., Shah, A., Nogales, E., Chu, S., and Brunger, A. T. (2012) Synaptic proteins promote acalcium-triggered fast transition from point contact to full fusion eLife 1, e00109
49. Lai, Y., Diao, J., Liu, Y., Ishitsuka, Y., Su, Z., Schulten, K., Ha, T., and Shin, Y. K. (2013) Fusion pore formation and expansion induced by Ca2+ and synaptotagmin 1 Proc. Natl. Acad. Sci. U. S. A. 110 (4) 1333-1338
50. Diao, J., Burre, J., Vivona, S., Cipriano, D. J., Sharma, M., Kyoung, M., Sudhof, T. C., and Brunger, A. T. (2013) Native alpha-synuclein induces clustering of synaptic-vesicle mimics via binding to phospholipids and synaptobrevin-2/VAMP2 eLife 2, e00592
51. Ferro-Novick, S. and Jahn, R. (1994) Vesicle fusion from yeast to man Nature 370 (6486) 191-193
52. Conway, K. A., Rochet, J. C., Bieganski, R. M., and Lansbury, P. T., Jr. (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct Science 294 (5545) 1346-1349
53. Lai, Y. and Shin, Y. K. (2012) The importance of an asymmetric distribution of acidic lipids for synaptotagmin 1 function as a Ca2+ sensor Biochem. J. 443 (1) 223-229