Architecture of the Synaptophysin/Synaptobrevin Complex: Structural Evidence for an Entropic Clustering Function at the Synapse

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Adams, Daniel J ^a   Arthur, Christopher P ^a,c   Stowell, Michael H B ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b University of Colorado at Boulder   (United States)

^c Thermo Fisher Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BINDING; SYNAPTOBREVIN 2; SYNAPTOPHYSIN;

AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; COMPUTER SIMULATION; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN CONFORMATION; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; SYNAPSE; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; COMPUTER SIMULATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; SYNAPTOPHYSIN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84940855905     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13659     Document Type: Article

References (47)

1. Walch-Solimena, C. et al. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. The Journal of cell biology 128, 637-645 (1995).
2. Milnerwood, A. J., Raymond, L. A. Early synaptic pathophysiology in neurodegeneration: insights from Huntington's disease. Trends in neurosciences 33, 513-523, doi: 10.1016/j.tins.2010.08.002 (2010).
3. van Spronsen, M., Hoogenraad, C. C. Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10, 207-214, doi: 10.1007/s11910-010-0104-8 (2010).
4. Tackenberg, C., Brandt, R. Divergent pathways mediate spine alterations and cell death induced by amyloid-beta, wild-type tau, and R406W tau. The Journal of neuroscience: the official journal of the Society for Neuroscience 29, 14439-14450, doi: 10.1523/JNEUROSCI.3590-09.2009 (2009).
5. Jahn, R., Schiebler, W., Ouimet, C., Greengard, P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. P Natl Acad Sci USA 82, 4137-4141 (1985).
6. Wiedenmann, B., Franke, W. W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41, 1017-1028 (1985).
7. Janz, R. et al. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24, 687-700 (1999).
8. Spiwoks-Becker, I. et al. Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107, 127-142 (2001).
9. Kwon, S. E., Chapman, E. R. Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 70, 847-854, doi: 10.1016/j.neuron.2011.04.001 (2011).
10. Schmitt, U., Tanimoto, N., Seeliger, M., Schaeffel, F., Leube, R. E. Detection of behavioral alterations and learning deficits in mice lacking synaptophysin. Neuroscience 162, 234-243, doi: 10.1016/j.neuroscience.2009.04.046 (2009).
11. Lin, J. Y. et al. Optogenetic inhibition of synaptic release with chromophore-assisted light inactivation (CALI). Neuron 79, 241-253, doi: 10.1016/j.neuron.2013.05.022 (2013).
12. Johnston, P. A., Jahn, R., Sudhof, T. C. Transmembrane topography and evolutionary conservation of synaptophysin. The Journal of biological chemistry 264, 1268-1273 (1989).
13. Arthur, C. P., Stowell, M. H. Structure of synaptophysin: a hexameric MARVEL-domain channel protein. Structure 15, 707-714 (2007).
14. Takamori, S. et al. Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (2006).
15. Thomas, L. et al. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242, 1050-1053 (1988).
16. Gincel, D., Shoshan-Barmatz, V. The synaptic vesicle protein synaptophysin: purification and characterization of its channel activity. Biophys J 83, 3223-3229 (2002).
17. Marqueze-Pouey, B., Wisden, W., Malosio, M. L., Betz, H. Differential expression of synaptophysin and synaptoporin mRNAs in the postnatal rat central nervous system. The Journal of neuroscience: the official journal of the Society for Neuroscience 11, 3388-3397 (1991).
18. Abraham, C. et al. Synaptic tetraspan vesicle membrane proteins are conserved but not needed for synaptogenesis and neuronal function in Caenorhabditis elegans. Proc Natl Acad Sci USA 103, 8227-8232 (2006).
19. Eshkind, L. G., Leube, R. E. Mice lacking synaptophysin reproduce and form typical synaptic vesicles. Cell Tissue Res 282, 423-433 (1995).
20. Leube, R. E. Expression of the synaptophysin gene family is not restricted to neuronal and neuroendocrine differentiation in rat and human. Differentiation 56, 163-171 (1994).
21. Thiele, C., Hannah, M. J., Fahrenholz, F., Huttner, W. B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nature cell biology 2, 42-49, doi: 10.1038/71366 (2000).
22. Edelmann, L., Hanson, P. I., Chapman, E. R., Jahn, R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. The EMBO journal 14, 224-231 (1995).
23. Gordon, S. L., Leube, R. E., Cousin, M. A. Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. The Journal of neuroscience: the official journal of the Society for Neuroscience 31, 14032-14036, doi: 10.1523/JNEUROSCI.3162-11.2011 (2011).
24. Tong, J., Borbat, P. P., Freed, J. H., Shin, Y. K. A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. P Natl Acad Sci USA 106, 5141-5146, doi: 10.1073/pnas.0813138106 (2009).
25. Laage, R., Langosch, D. Dimerization of the synaptic vesicle protein synaptobrevin (vesicle-associated membrane protein) II depends on specific residues within the transmembrane segment. Eur J Biochem 249, 540-546 (1997).
26. Maeda, S. et al. Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature 458, 597-602, doi: 10.1038/nature07869 (2009).
27. Ellena, J. F. et al. Dynamic structure of lipid-bound synaptobrevin suggests a nucleation-propagation mechanism for trans-SNARE complex formation. P Natl Acad Sci USA 106, 20306-20311, doi: 10.1073/pnas.0908317106 (2009).
28. Tarpey, P. S. et al. A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation. Nat Genet 41, 535-543, doi: 10.1038/ng.367 (2009).
29. Gordon, S. L., Cousin, M. A. X-linked intellectual disability-associated mutations in synaptophysin disrupt synaptobrevin II retrieval. The Journal of neuroscience: the official journal of the Society for Neuroscience 33, 13695-13700, doi: 10.1523/JNEUROSCI.0636-13.2013 (2013).
30. Cho, W. J., Jeremic, A., Jin, H., Ren, G., Jena, B. P. Neuronal fusion pore assembly requires membrane cholesterol. Cell biology international 31, 1301-1308, doi: 10.1016/j.cellbi.2007.06.011 (2007).
31. Murray, D. H., Tamm, L. K. Molecular mechanism of cholesterol-and polyphosphoinositide-mediated syntaxin clustering. Biochemistry 50, 9014-9022, doi: 10.1021/bi201307u (2011).
32. Sieber, J. J. et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317, 1072-1076, doi: 10.1126/science.1141727 (2007).
33. Galli, T., McPherson, P. S., De Camilli, P. The V0 sector of the V-ATPase, synaptobrevin, and synaptophysin are associated on synaptic vesicles in a Triton X-100-resistant, freeze-thawing sensitive, complex. The Journal of biological chemistry 271, 2193-2198 (1996).
34. Kiessling, V. et al. Rapid fusion of synaptic vesicles with reconstituted target SNARE membranes. Biophysical journal 104, 1950-1958, doi: 10.1016/j.bpj.2013.03.038 (2013).
35. van den Bogaart, G. et al. One SNARE complex is sufficient for membrane fusion. Nat Struct Mol Biol 17, 358-364, doi: 10.1038/nsmb.1748 (2010).
36. Domanska, M. K., Kiessling, V., Stein, A., Fasshauer, D., Tamm, L. K. Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNARE-mediated membrane fusion. The Journal of biological chemistry 284, 32158-32166, doi: 10.1074/jbc.M109.047381 (2009).
37. Karatekin, E. et al. A fast, single-vesicle fusion assay mimics physiological SNARE requirements. P Natl Acad Sci USA 107, 3517-3521, doi: 10.1073/pnas.0914723107 (2010).
38. Mohrmann, R., de Wit, H., Verhage, M., Neher, E., Sorensen, J. B. Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 330, 502-505, doi: 10.1126/science.1193134 (2010).
39. Zampighi, G. A. et al. Conical electron tomography of a chemical synapse: vesicles docked to the active zone are hemi-fused. Biophysical journal 91, 2910-2918, doi: 10.1529/biophysj.106.084814 (2006).
40. Szule, J. A. et al. Regulation of synaptic vesicle docking by different classes of macromolecules in active zone material. PLoS One 7, e33333, doi: 10.1371/journal.pone.0033333 (2012).
41. Gincel, D., Shoshan-Barmatz, V. The synaptic vesicle protein synaptophysin: purification and characterization of its channel activity. Biophysical journal 83, 3223-3229, doi: 10.1016/S0006-3495(02)75324-1 (2002).
42. He, L., Wu, X. S., Mohan, R., Wu, L. G. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 444, 102-105 (2006).
43. Sabatini, B. L., Regehr, W. G. Timing of neurotransmission at fast synapses in the mammalian brain. Nature 384, 170-172, doi: 10.1038/384170a0 (1996).
44. Fukuda, M. Vesicle-associated membrane protein-2/synaptobrevin binding to synaptotagmin I promotes O-glycosylation of synaptotagmin I. J Biol Chem 277, 30351-30358 (2002).
45. Smith, P. K. et al. Measurement of Protein Using Bicinchoninic Acid. Analytical Biochemistry 150, 76-85, doi: 10.1016/0003-2697(85)90442-7 (1985).
46. Hoenger, A., Aebi, U. 3-D Reconstructions from Ice-Embedded and Negatively Stained Biomacromolecular Assemblies: A Critical Comparison. Journal of Structural Biology 117, 99-116 (1996).
47. Ludtke, S. J., Baldwin, P. R., Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82-97 (1999).