Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution (original) (raw)

References

  1. Südhof, T. The synaptic vesicle cycle: a cascade of protein–protein interactions. Nature 375, 645–653 (1995).
    Article ADS PubMed Google Scholar
  2. Hanson, P. I., Heuser, J. E. & Jahn, R. Neurotransmitter release — four years of SNARE complexes. Curr. Opin. Neurobiol. 7, 310–315 (1997).
    Article CAS PubMed Google Scholar
  3. Jahn, R. & Niemann, H. Molecular mechanisms of clostridial neurotoxins. Ann. NY Acad. Sci. 733, 245–255 (1994).
    Article ADS CAS PubMed Google Scholar
  4. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. Aprotein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418 (1993).
    Article PubMed Google Scholar
  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).
    Article PubMed Central Google Scholar
  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).
    Article Google Scholar
  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).
    CAS Google Scholar
  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).
    Article ADS CAS PubMed PubMed Central Google Scholar
  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).
    Article ADS CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article Google Scholar
  12. Hendrickson, W. A. Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254, 51–58 (1991).
    Article ADS CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  15. Harbury, P. B., Zhang, T., Kim, P. S. & Alber, T. Aswitch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401–1407 (1993).
    Article ADS CAS PubMed Google Scholar
  16. Lupas, A., van Dyke, M. & Stock, J. Predicting coiled coils from protein sequences. Science 252, 1162–1164 (1991).
    Article ADS CAS PubMed Google Scholar
  17. Crick, F. H. C. The packing of α-helices: simple coiled coils. Acta Crystallogr. 6, 689–697 (1953).
    Article CAS Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  19. Weimbs, T., Mostov, K. E., Low, S. H. & Hofmann, K. Amodel for structural similarity between different SNARE complexes based on sequence relationships. Trends Cell Biol. 8, 260–262 (1998).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  22. Fasshauer, D., Bruns, D., Shen, B., Jahn, R. & Brunger, A. T. Astructural change occurs upon binding of syntaxin to SNAP-25. J. Biol. Chem. 272, 4582–4590 (1997).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  24. Hayashi, T. et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051–5061 (1994).
    Article CAS PubMed PubMed Central Google Scholar
  25. Wimley, W. C. & White, S. H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3, 842–848 (1996).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article ADS CAS PubMed Google Scholar
  28. Caffrey, M. et al. Three-dimensional solution structure of the 44 kDa ectodomain of SIV gp41. EMBO J. 17, 4572–4584 (1998).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article ADS CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  31. Chan, D. C. & Kim, P. S. HIV entry and its inhibition. Cell 93, 681–684 (1998).
    Article CAS PubMed Google Scholar
  32. Bernard, A. & Payton, M. Fermentation and growth of Escherichia coli for optimal protein production. Curr. Protocol. Protein Sci. 5.3, 1–18 (1995).
    Google Scholar
  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).
    Article CAS PubMed Google Scholar
  34. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1998).
    Article Google Scholar
  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).
    Article CAS PubMed Google Scholar
  36. Bricogne, G. Bayesian statistical viewpoint on structure determination: basic concepts and examples. Methods Enzymol. 276, 361–423 (1997).
    Article CAS PubMed Google Scholar
  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).
    Article ADS Google Scholar
  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).
    Article ADS CAS PubMed Google Scholar
  39. Wang, B.-C. Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol. 115, 90–112 (1985).
    Article CAS PubMed Google Scholar
  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).
    Article Google Scholar
  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).
    Article PubMed Google Scholar
  42. Rice, L. M. & Brunger, A. T. Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins 19, 277–290 (1994).
    Article CAS PubMed Google Scholar
  43. Hendrickson, W. A. Stereochemically restrained refinement of macromolecular structures. Methods Enzymol. 115, 252–270 (1985).
    Article CAS PubMed Google Scholar
  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).
    Article Google Scholar
  46. Brunger, A. T. The free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472–474 (1992).
    Article ADS CAS PubMed Google Scholar
  47. Read, R. J. Model phases: probabilities and bias. Methods Enzymol. 277, 110–128 (1997).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  49. Esnouf, M. An extensively modified version of MOLSCRIPT that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model 15, 132–134 (1997).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  51. Malashkevich, V. N., Chan, D. C., Chutkowski, C. T. & Kim, P. Crystal structure of the simian immunodeficiency virus (SIV) gp41core: Conserved helical interactions underlie the broad inhibitory activity of gp41peptides. Proc. Natl Acad. Sci. USA 95, 9134–9139 (1998).
    Article ADS CAS PubMed PubMed Central Google Scholar

Download references