Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution

Nature

Volumn 395, Issue 6700, 1998, Pages 347-353

  Sutton, R Bryan ^a   Fasshauer, Dirk ^b   Jahn, Reinhard ^b   Brunger, Axel T ^a  

^a YALE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 41; HEMAGGLUTININ; MEMBRANE PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

CRYSTAL STRUCTURE; EXOCYTOSIS; MEMBRANE FUSION; MEMBRANE VESICLE; NEUROTRANSMISSION; PRIORITY JOURNAL; REVIEW; SYNAPSE;

ANTIGENS, SURFACE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; EXOCYTOSIS; MACROMOLECULAR SUBSTANCES; MEMBRANE FUSION; MEMBRANE PROTEINS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; NEUROTOXINS; PROTEIN BINDING; PROTEIN CONFORMATION; R-SNARE PROTEINS; RECOMBINANT PROTEINS; SNARE PROTEINS; SYNAPTIC VESICLES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNTAXIN 1; VESICULAR TRANSPORT PROTEINS;

EID: 3543096759     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/26412     Document Type: Review

References (51)

1. Südhof, T. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653 (1995).
2. Hanson, P. I., Heuser, J. E. & Jahn, R. Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol. 7, 310-315 (1997).
3. Jahn, R. & Niemann, H. Molecular mechanisms of clostridial neurotoxins. Ann. NY Acad. Sci. 733, 245-255 (1994).
4. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418 (1993).
5. Hayashi, T., Yamasaki, S., Nauenburg, S., Binz, T. & Niemann, H. Disassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro. EMBO J. 14(10), 2317-2325 (1995).
6. Fasshauer, D., Otto, H., Eliason, W. K., Jahn, R. & Brunger, A. T. Structural changes are associated with SNARE-complex formation. J. Biol. Chem. 242, 28036-28041 (1997).
7. Nichols, B. J., Ungerman, C., Pelham, H. R. B., Wickner, W. T. & Haas, A. Homotypic vacuolar fusion mediated by t-and v-SNAREs. Proc. Natl Acad. Sci. USA 387, 199-202 (1997).
8. Otto, H., Hanson, P. I. & Jahn, R. Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl Acad. Sci. USA 94, 6197-6201 (1997).
9. Block, M. R., Glick, B. S., Wilcox, C. A., Wieland, F. T. & Rothman, J. E. Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc. Natl Acad. Sci. USA 85, 7852-7856 (1988).
10. Hanson, P. I., Otto, H., Barton, N. & Jahn, R. The N-ethylmaleimide-sensitive fusion protein and α-SNAP induce a conformational change in syntaxin. J. Biol. Chem. 270, 16955-16961 (1995).
11. Fasshauer, D., Eliason, W. K., Brunger, A. T. & Jahn, R. Identification of a minimal core of the synaptic SNARE-complex sufficient for reversible assembly and disassembly. Biochemsitry 37, 10345-10353 (1998).
12. Hendrickson, W. A. Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254, 51-58 (1991).
13. Hanson, P. I., Roth, R., Morisaki, H., Jahn, R. & Heuser, J. E. Structure and conformational changes in NSF and its membrane receptor complex visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523-525 (1997).
14. Oyler, G. A. et al. The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell. Biol. 109, 3039-3052 (1989).
15. Harbury, P. B., Zhang, T., Kim, P. S. & Alber, T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401-1407 (1993).
16. Lupas, A., van Dyke, M. & Stock, J. Predicting coiled coils from protein sequences. Science 252, 1162-1164 (1991).
17. Crick, F. H. C. The packing of α-helices: simple coiled coils. Acta Crystallogr. 6, 689-697 (1953).
18. Wolf, E., Kim, P. S. & Berger, B. MultiCoil: a program for predicting two-and three-stranded coiled coils. Protein Sci. 6, 1179-1189 (1997).
19. Weimbs, T., Mostov, K. E., Low, S. H. & Hofmann, K. A model for structural similarity between different SNARE complexes based on sequence relationships. Trends Cell Biol. 8, 260-262 (1998).
20. Hao, J. C., Salem, N., Peng, X. R., Kelly, R. B. & Bennett, M. K. Effect of mutations in vesicle-associated membrane protein (VAMP) on the assembly of multimeric protein complexes. J. Neurosci. 17, 1596-1603 (1997).
21. Saifee, O., Wei, L. & Nonet, M. L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol. Biol. Cell 9, 1235-1239 (1998).
22. Fasshauer, D., Bruns, D., Shen, B., Jahn, R. & Brunger, A. T. A structural change occurs upon binding of syntaxin to SNAP-25. J. Biol. Chem. 272, 4582-4590 (1997).
23. Kee, Y., Lin, R. C., Hsu, S. C. & Scheller, R. H. Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation. Neuron 14, 991-998 (1995).
24. Hayashi, T. et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061 (1994).
25. Wimley, W. C. & White, S. H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3, 842-848 (1996).
26. Chan, D. c., Fass, D., Berger, J. M. & Kim, P. S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89, 263-273 (1997).
27. Weissenhorn, W., Dessen, A., Harrison, S. C., Skehel, J. J. & Wiley, D. C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387, 426-430 (1997).
28. Caffrey, M. et al. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17, 4572-4584 (1998).
29. Wilson, I. A., Skehel, J. J. & Wiley, D. C. Structure of the haemagglutinin membrane glycoprotein influenza virus at 3 Å resolution. Nature 289, 366-373 (1981).
30. Rice, L. M., Brennwald, P. & Brunger, A. T. Formation of a yeast SNARE complex is accompanied by significant structural changes. FEBS Lett. 415, 49-55 (1997).
31. Chan, D. C. & Kim, P. S. HIV entry and its inhibition. Cell 93, 681-684 (1998).
32. Bernard, A. & Payton, M. Fermentation and growth of Escherichia coli for optimal protein production. Curr. Protocol. Protein Sci. 5.3, 1-18 (1995).
33. Leahy, D. J., Erickson, H. P., Aukhil, I., Joshi, P. & Hendrickson, W. A. Crystallization of a fragment of human fibronectin: introduction of methionine by site-directed mutagenesis to allow phasing via selenomethionine. Proteins 19, 48-54 (1994).
34. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1998).
35. Brunger, A. T. et al. Crystallography & NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
36. Bricogne, G. Bayesian statistical viewpoint on structure determination: basic concepts and examples. Methods Enzymol. 276, 361-423 (1997).
37. Phillips, J. C. & Hodgson, K. O. The use of anomalous scattering effects to phase diffraction patterns from macromolecules. Acta Crystallogr, A 36, 856-864 (1980).
38. Burling, F. T., Weis, W. I., Flaherty, K. M. & Brunger, A. T. Direct observation of protein solvation and discrete disorder with experimental crystallographic phases. Science 271, 72-77 (1996).
39. Wang, B.-C. Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol. 115, 90-112 (1985).
40. Zhang, K. Y. J. & Main, P. Histogram matching as a new density modification technique for phase refinement and extension of protein molecules. Acta Crystallogr. A 46, 41-46 (1990).
41. Jones, T. A., Zou, J. Y., Cowan, S. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
42. Rice, L. M. & Brunger, A. T. Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins 19, 277-290 (1994).
43. Hendrickson, W. A. Stereochemically restrained refinement of macromolecular structures. Methods Enzymol. 115, 252-270 (1985).
44. Pannu, N. S., Murshudov, G. N., Dodson, E. J. & Read, R. J. Incorporation of prior phase information strengthens maximum likelihood structural refinement. Acta Crystallogr. D (in the press).
45. Read, R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A 42, 140-149 (1986).
46. Brunger, A. T. The free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-474 (1992).
47. Read, R. J. Model phases: probabilities and bias. Methods Enzymol. 277, 110-128 (1997).
48. Nicholls, A., Sharp, K. A. & Honig, B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296 (1991).
49. Esnouf, M. An extensively modified version of MOLSCRIPT that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model 15, 132-134 (1997).
50. Jorgensen, W. L. & Rives, J. T. The OPLS potential functions for protein energy minimizations for crystals of cyclic peptide and crambin. J. Am. Chem. Soc. 110, 1657-1666 (1988).
51. 41 peptides. Proc. Natl Acad. Sci. USA 95, 9134-9139 (1998).