A role for soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex dimerization during neurosecretion

Molecular Biology of the Cell

Volumn 19, Issue 8, 2008, Pages 3379-3389

  Fdez, Elena ^a   Jowitt, Thomas A ^b   Wang, Ming Chuan ^b   Rajebhosale, Manisha ^b   Foster, Keith ^c   Bella, Jordi ^b   Baldock, Clair ^b   Woodman, Philip G ^b   Hilfiker, Sabine ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c SYNTAXIN LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN; SNARE PROTEIN; SYNAPTOBREVIN 2;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOSOL; DIMERIZATION; HUMAN; HUMAN CELL; NEUROSECRETION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ANIMALS; BOTULINUM TOXINS; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; DIMERIZATION; EXOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; NEURONS; PC12 CELLS; RATS; SNARE PROTEINS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 53249129685     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-01-0010     Document Type: Article

References (55)

1. Antonin, W., Holroyd, C., Fasshauer, D., Pabst, S., Fischer von Mollard, G., and Jahn, R. (2000). A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 19, 6453-6464.
2. Bevan, S., and Wendon, L. M. (1984). A study of the action of tetanus toxin at rat soleus neuromuscular junctions. J. Physiol. 348, 1-17.
3. Bowen, M. E., Engelman, D. M., and Brunger, A. T. (2002). Mutational analysis of synaptobrevin transmembrane domain oligomerization. Biochemistry 41, 15861-15866.
4. Bowen, M. E., Weninger, K., Ernst, J., Chu, S., and Brunger, A. T. (2005). Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex. Biophys. J. 89, 690-702.
5. Chen, X., Tomchick, D. R., Kovrigin, E., Arac, D., Machius, M., Südhof, T. C., and Rizo, J. (2002). Three-dimensional structure of the complexin/SNARE complex. Neuron 33, 397-409.
6. Chilcote, T. J., Galli, T., Mundigl, O., Edelmann, L., McPherson, P. S., Takei, K., and De Camilli, P. (1995). Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC12 cells. J. Cell Biol. 129, 219-231.
7. Chin, D., and Means, A. R. (2000). Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10, 322.
8. Cull-Candy, S. G., Lundh, H., and Thesleff, S. (1976). Effects of botulinum toxin on neuromuscular transmission in the rat. J. Physiol. 260, 177-203.
9. 2+/calmodulin transfers the membrane-proximal lipid-binding domain of the v-SNARE synaptobrevin from cis to trans bilayers. Proc. Natl. Acad. Sci. USA 101, 1578-1583.
10. Ernst, J. A., and Brünger, A. T. (2003). High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex. J. Biol. Chem. 278, 8630-8636.
11. Fasshauer, D., Eliason, W. K., Brünger, A. T., and Jahn, R. (1998). Identification of a minimal core of the synaptic SNARE complex sufficient for reversible assembly and disassembly. Biochemistry 37, 10354-10362.
12. Fasshauer, D., Otto, H., Eliason, W. K., Jahn, R., and Brünger, A. T. (1997). Structural changes are associated with soluble N-ethylmaleimide- sensitive fusion protein attachment protein receptor complex formation. J. Biol. Chem. 272, 28036-28041.
13. Fiebig, K. M., Rice, L. M., Pollock, E., and Brünger, A. T. (1999). Folding intermediates of SNARE complex assembly. Nat. Struct. Biol. 6, 117-123.
14. Giraudo, C. G., Eng, W. S., Melia, T. J., and Rothman, J. E. (2006). A clamping mechanism involved in SNARE-dependent exocytosis. Science 313, 676-680.
15. 2+-triggered exocytosis. Science 304, 289-292.
16. Hanson, P. I., Roth, R., Morisaki, R., Jahn, R., and Heuser, J. E. (1997). Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523-536.
17. Hohl, T. M., Parlati, F., Wimmer, C., Rothman, J. E., Söllner, T. H., and Engelhardt, H. (1998). Arrangement of subunits in 20S particles consisting of NSF, SNAPs, and SNARE complexes. Mol. Cell 2, 539-548.
18. Hu, C., Ahmed, M., Melia, T. J., Söllner, T., Mayer, T., and Rothman, J. E. (2003). Fusion of cells by flipped SNAREs. Science 300, 1745-1749.
19. Hu, K., Carroll, J., Fedorovich, S., Rickman, C., Sukhodub, A., and Davletov, B. (2002). Vesicular restriction of synaptobrevin suggests a role for calcium in membrane fusion. Nature 415, 646-650.
20. Hua, Y., and Scheller, R. H. (2001). Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. USA 98, 8065-8070.
21. Jahn, R., and Scheller, R. H. (2006). SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643.
22. Keller, J. E., Cai, F., and Neale, E. A. (2004). Uptake of botulinum neurotoxin into cultured neurons. Biochemistry 43, 526-532.
23. Keller, J. E., and Neale, E. A. (2001). The role of the synaptic protein SNAP-25 in the potency of botulinum neurotoxin type A. J. Biol. Chem. 276, 13476-13482.
24. Kweon, D. H., Chen, Y., Zhang, F., Poirier, M., Kim, C. S., and Shin, Y. K. (2002). Probing domain swapping for the neuronal SNARE complex with electron paramagnetic resonance. Biochemistry 41, 5449-5452.
25. Kweon, D.-H., Kim, C. S., and Shin, Y.-K. (2003). Regulation of neuronal SNARE assembly by the membrane. Nat. Struct. Biol. 10, 440-447.
26. Laage, R., Rohde, J., Brosig, B., and Langosch, D. (2000). A conserved membrane-spanning amino acid motif drives homomeric and supports heteromeric assembly of presynaptic SNARE proteins. J. Biol. Chem. 275, 17481-17487.
27. Li, F., Pincet, F., Perez, E., Eng, W. S., Melia, T. J., Rothman, J. E., and Tareste, D. (2007). Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat. Struct. Mol. Biol. 14, 890-896.
28. 2+- triggered fusion and recycling of synaptic vesicles in vivo. J. Neurosci. 21, 1421-1433.
29. 2+- triggered vesicle exocytosis. Mol. Biol. Cell 18, 4957-4968.
30. Margittai, M., Fasshauer, D., Pabst, S., Jahn, R., and Langen, R. (2001). Homoand heterooligomeric SNARE complexes studied by site-directed spin labeling. J. Biol. Chem. 276, 13169-13177.
31. Montecucco, C., Schiavo, G., and Pantano, S. (2005). SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem. Sci. 30, 367.
32. Pobbati, A. V., Stein, A., and Fasshauer, D. (2006). N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313, 673-676.
33. Quetglas, S., Iborra, C., Sasakawa, N., De Haro, L., Kumakura, K., Sato, K., Leveque, C., and Seagar, M. (2002). Calmodulin and lipid binding to synaptobrevin regulates calcium-dependent exocytosis. EMBO J. 21, 3970-3979.
34. 2+-dependent regulation of synaptic SNARE complex assembly via a calmodulin-and phospholipid-binding domain of synaptobrevin. Proc. Natl. Acad. Sci. USA 97, 9695-9700.
35. Rhoads, A. R., and Friedberg, F. (1997). Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340.
36. Rickman, C., Hu, K., Carroll, J., and Davletov, B. (2005). Self-assembly of SNARE fusion proteins into star-shaped oligomers. Biochem. J. 388, 75-79.
37. Rickman, C., Jiménez, J. L., Graham, M. E., Archer, D. A., Soloviev, M., Burgoyne, R. D. and Davletov, B. (2006). Conserved prefusion protein assembly in regulated exocytosis. Mol. Biol. Cell 17, 283-294.
38. Rizo, J., Chen, X., and Arac, D. (2006). Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. Trends Cell Biol. 16, 339.
39. Roy, R., Laage, R., and Langosch, D. (2004). Synaptobrevin transmembrane domain dimerization-revisited. Biochemistry 43, 4964-4970.
40. Siddiqui, T. J., Vites, O., Stein, A., Heintzmann, R., Jahn, R., and Fasshauer, D. (2007). Determinants of synaptobrevin regulation in membranes. Mol. Biol. Cell 18, 2037-2046.
41. Sorensen, J. B., Wiederhold, K., Muller, E. M., Milosevic, I., Nagy, G., de Groot, B. L., Grubmuller, H., and Fasshauer, D. (2006). Sequential N- to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 25, 955-966.
42. Spotorno, B., Piccinini, L., Tassara, G., Ruggiero, C., Nardini, M., Molina, F., and Rocco, M. (1997). BEAMS (BEAds Modelling System): a set of computer programs for the generation, the visualization and the computation of the hydrodynamic and conformational properties of bead models of proteins. Eur. Biophys. J. 25, 373-384.
43. Stewart, B. A., Mohtashami, M., Trimble, W. S., and Boulianne, G. L. (2000). SNARE proteins contribute to calcium cooperativity of synaptic transmission. Proc. Natl. Acad. Sci. USA 97, 13955-13960.
44. Südhof, T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
45. 2+-dependent exocytosis in PC12 cells. J. Biol. Chem. 274, 18893-18901.
46. Sutton, J. M., Wayne, J., Scott-Tucker, A., O'Brien, S. M., Marks, P. M., Alexander, F. C., Shone, C. C., and Chaddock, J. A. (2005). Preparation of specifically activatable endopeptidase derivatives of Clostridium botulinum toxins type A, B, and C and their applications. Protein Expr. Purif. 40, 31-41.
47. Sutton, R. B., Fasshauer, D., Jahn, R., and Brünger, A. T. (1998). Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution. Nature 395, 347-353.
48. Svergun, D. I. (1999). Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886.
49. Svergun, D. I., Petoukhov, M. V., and Koch, M. H. (2001). Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80, 2946-2953.
50. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H., and Rothman, J. E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
51. Tang, J., Maximov, A., Shin, O., Dai, H., Rizo, J., and Südhof, T. C. (2006). A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187.
52. Tokumaru, H., Umayahara, K., Pellegrini, L., Ishizuka, T., Saisu, H., Betz, H., Augustine, G., and Abe, T. (2001). SNARE complex oligomerization by synaphin/complexin is essential for synaptic vesicle exocytosis. Cell 104, 421-432.
53. Vestergaard, B., Sanyal, S., Roessle, M., Mora, L., Buckingham, R. H., Kastrup, J. S., Gajhede, M., Svergun, D. I., and Ehrenberg, M. (2005). The SAXS solution structure of RF1 differs from its crystal structure and is similar to its ribosome bound cryo-EM structure. Mol. Cell 20, 929-938.
54. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., and Rothman, J. E. (1998). SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772.
55. Wojcik, S. M., and Brose, N. (2007). Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron 55, 11-24.