SNAREs: Could they be the answer to an energy landscape riddle in exocytosis?

TheScientificWorldJournal

Volumn 10, Issue , 2010, Pages 1258-1268

  Liu, Wei ^a   Parpura, Vladimir ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

Atomic force microscopy; Free energy; Isothermal titration calorimetry; Secretory vesicle fusion; SNARE; Surface force apparatus; Theoretical modeling

Indexed keywords

SNARE PROTEIN;

ATOMIC FORCE MICROSCOPY; BIOPHYSICS; CELL MEMBRANE; CELL ORGANELLE; ENERGY; EXOCYTOSIS; ISOTHERMAL TITRATION CALORIMETRY; LIPID BILAYER; MEMBRANE FUSION; MODEL; MOLECULAR DOCKING; MOLECULAR INTERACTION; NEUROSCIENCE; SECRETORY VESICLE; SHORT SURVEY; TEMPERATURE; CALORIMETRY; PHYSIOLOGY; REVIEW; THEORETICAL MODEL;

CALORIMETRY; EXOCYTOSIS; MEMBRANE FUSION; MODELS, THEORETICAL; SNARE PROTEINS;

EID: 77955861788     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2010.137     Document Type: Short Survey

References (38)

1. Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
2. 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, 347-353. (Pubitemid 28450677)
3. Otto, H., Hanson, P.I., and Jahn, R. (1997) Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl. Acad. Sci. U. S. A. 94, 6197-6201. (Pubitemid 27270661)
4. Yang, B., Gonzalez, L., Jr., Prekeris, R., Steegmaier, M., Advani, R.J., and Scheller, R.H. (1999) SNARE interactions are not selective. Implications for membrane fusion specificity. J. Biol. Chem. 274, 5649-5653. (Pubitemid 29109216)
5. Pobbati, A.V., Stein, A., and Fasshauer, D. (2006) N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313, 673-676. (Pubitemid 44201146)
6. 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.
7. Fasshauer, D., Antonin, W., Subramaniam, V., and Jahn, R. (2002) SNARE assembly and disassembly exhibit a pronounced hysteresis. Nat. Struct. Biol. 9, 144-151. (Pubitemid 34132418)
8. Rizo, J. and Rosenmund, C. (2008) Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674.
9. Liu, W. and Parpura, V. (2009) Energetics of (dis)assembly of the ternary SNARE complex. Front. Neuroenergetics 1, 5.
10. Markin, V.S. and Albanesi, J.P. (2002) Membrane fusion: stalk model revisited. Biophys. J. 82, 693-712.
11. Chernomordik, L.V. and Kozlov, M.M. (2005) Membrane hemifusion: crossing a chasm in two leaps. Cell 123, 375-382.
12. Cohen, F.S. and Melikyan, G.B. (2004) The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199, 1-14.
13. Marrink, S.J. and Mark, A.E. (2003) The mechanism of vesicle fusion as revealed by molecular dynamics simulations. J. Am. Chem. Soc. 125, 11144-11145.
14. Kasson, P.M., Kelley, N.W., Singhal, N., Vrljic, M., Brunger, A.T., and Pande, V.S. (2006) Ensemble molecular dynamics yields submillisecond kinetics and intermediates of membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 103, 11916-11921. (Pubitemid 44215786)
15. Katsov, K., Muller, M., and Schick, M. (2006) Field theoretic study of bilayer membrane fusion: II. Mechanism of a stalk-hole complex. Biophys. J. 90, 915-926.
16. 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. (Pubitemid 47525184)
17. Liu, W., Montana, V., Mohideen, U., and Parpura, V. (2009) Single molecule measurements of interaction free energies between the proteins within binary and ternary SNARE complexes. J. Nanoneurosci. 1, 120-129.
18. Wiederhold, K. and Fasshauer, D. (2009) Is assembly of the SNARE complex enough to fuel membrane fusion? J. Biol. Chem. 284, 13143-13152.
19. Liu, W., Montana, V., Bai, J., Chapman, E.R., Mohideen, U., and Parpura, V. (2006) Single molecule mechanical probing of the SNARE protein interactions. Biophys. J. 91, 744-758.
20. Montana, V., Liu, W., Mohideen, U., and Parpura, V. (2009) Single molecule measurements of mechanical interactions within ternary SNARE complexes and dynamics of their disassembly: SNAP25 vs. SNAP23. J. Physiol. 587, 1943-1960.
21. Montana, V., Liu, W., Mohideen, U., and Parpura, V. (2008) Single molecule probing of exocytotic protein interactions using force spectroscopy. Croat. Chem. Acta 81, 31-40.
22. Parpura, V. and Mohideen, U. (2008) Molecular form follows function: (un)snaring the SNAREs. Trends Neurosci. 31, 435-443.
23. Liu, W. and Parpura, V. (2009) Single molecule probing of SNARE proteins by atomic force microscopy. Ann. N. Y. Acad. Sci. 1152, 113-120.
24. Hanson, P.I., Roth, R., Morisaki, H., 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, 523-535. (Pubitemid 27347242)
25. Lin, R.C. and Scheller, R.H. (1997) Structural organization of the synaptic exocytosis core complex. Neuron 19, 1087-1094. (Pubitemid 27512368)
26. Bowen, M.E., Weninger, K., Brunger, A.T., and Chu, S. (2004) Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). Biophys. J. 87, 3569-3584.
27. Schwesinger, F., Ros, R., Strunz, T., Anselmetti, D., Guntherodt, H.J., Honegger, A., Jermutus, L., Tiefenauer, L., and Pluckthun, A. (2000) Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc. Natl. Acad. Sci. U. S. A. 97, 9972-9977.
28. Weninger, K., Bowen, M.E., Chu, S., and Brunger, A.T. (2003) Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. Proc. Natl. Acad. Sci. U. S. A. 100, 14800-14805. (Pubitemid 37517971)
29. Weninger, K., Bowen, M.E., Choi, U.B., Chu, S., and Brunger, A.T. (2008) Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex. Structure 16, 308-320. (Pubitemid 351222650)
30. Rizo, J. and Dai, H. (2007) How much can SNAREs flex their muscles? Nat. Struct. Mol. Biol. 14, 880-882. (Pubitemid 47525166)
31. Chernomordik, L.V. and Kozlov, M.M. (2008) Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675-683.
32. van den Bogaart, G., Holt, M.G., Bunt, G., Riedel, D., Wouters, F.S., and Jahn, R. (2010) One SNARE complex is sufficient for membrane fusion. Nat. Struct. Mol. Biol. 17, 358-364.
33. Ellena, J.F., Liang, B., Wiktor, M., Stein, A., Cafiso, D.S., Jahn, R., and Tamm, L.K. (2009) Dynamic structure of lipid-bound synaptobrevin suggests a nucleation-propagation mechanism for trans-SNARE complex formation. Proc. Natl. Acad. Sci. U. S. A. 106, 20306-20311.
34. Stein, A., Weber, G., Wahl, M.C., and Jahn, R. (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460, 525-528.
35. Verhage, M. and Sorensen, J.B. (2008) Vesicle docking in regulated exocytosis. Traffic 9, 1414-1424.
36. Rosenmund, C. and Stevens, C.F. (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197-1207. (Pubitemid 26227241)
37. Darios, F., Wasser, C., Shakirzyanova, A., Giniatullin, A., Goodman, K., Munoz-Bravo, J.L., Raingo, J., Jorgacevski, J., Kreft, M., Zorec, R., Rosa, J.M., Gandia, L., Gutierrez, L.M., Binz, T., Giniatullin, R., Kavalali, E.T., and Davletov, B. (2009) Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron 62, 683-694.
38. Sudhof, T.C. and Rothman, J.E. (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.