A highly tilted membrane configuration for the prefusion state of synaptobrevin

Biophysical Journal

Volumn 107, Issue 9, 2014, Pages 2112-2121

  Blanchard, Andrew E ^a   Arcario, Mark J ^a   Schulten, Klaus ^a   Tajkhorshid, Emad ^a  

^a University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; PHOSPHATIDYLCHOLINE; SYNAPTOBREVIN;

AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; LIPID BILAYER; MOLECULAR DYNAMICS; MUTATION;

AMINO ACID SEQUENCE; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MUTATION; PHOSPHATIDYLCHOLINES; R-SNARE PROTEINS;

EID: 84908632323     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.09.013     Document Type: Article

References (43)

1. D. Fasshauer, and H. Otto A.T. Brünger Structural changes are associated with soluble n-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation J. Biol. Chem. 272 1997 28036 28041
2. T.C. Südhof The synaptic vesicle cycle Annu. Rev. Neurosci. 27 2004 509 547
3. A.T. Brunger Structure and function of SNARE and SNARE-interacting proteins Q. Rev. Biophys. 38 2005 1 47
4. R. Jahn, and R.H. Scheller SNAREs - engines for membrane fusion Nat. Rev. Mol. Cell Biol. 7 2006 631 643
5. T.C. Südhof, and J.E. Rothman Membrane fusion: grappling with SNARE and SM proteins Science 323 2009 474 477
6. S. Martens, and H.T. McMahon Mechanisms of membrane fusion: disparate players and common principles Nat. Rev. Mol. Cell Biol. 9 2008 543 556
7. R.B. Sutton, and D. Fasshauer A.T. Brunger Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution Nature 395 1998 347 353
8. A. Yersin, and H. Hirling S. Kasas Interactions between synaptic vesicle fusion proteins explored by atomic force microscopy Proc. Natl. Acad. Sci. USA 100 2003 8736 8741
9. Y.Z. Ohkubo, and T.V. Pogorelov E. Tajkhorshid Accelerating membrane insertion of peripheral proteins with a novel membrane mimetic model Biophys. J. 102 2012 2130 2139
10. A.T. Brunger, and K. Weninger S. Chu Single-molecule studies of the neuronal SNARE fusion machinery Annu. Rev. Biochem. 78 2009 903 928
11. A. Stein, and G. Weber R. Jahn Helical extension of the neuronal SNARE complex into the membrane Nature 460 2009 525 528
12. D.-H. Kweon, C.S. Kim, and Y.-K. Shin Regulation of neuronal SNARE assembly by the membrane Nat. Struct. Biol. 10 2003 440 447
13. J.A. McNew, and T. Weber J.E. Rothman The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion Mol. Cell 4 1999 415 421
14. T.C. Südhof, and M. Baumert R. Jahn A synaptic vesicle membrane protein is conserved from mammals to Drosophila Neuron 2 1989 1475 1481
15. M. Bowen, and A.T. Brunger Conformation of the synaptobrevin transmembrane domain Proc. Natl. Acad. Sci. USA 103 2006 8378 8383
16. M.-P. Durrieu, and P.J. Bond M. Baaden Coarse-grain simulations of the R-SNARE fusion protein in its membrane environment detect long-lived conformational sub-states ChemPhysChem 10 2009 1548 1552
17. D.-H. Kweon, C.S. Kim, and Y.-K. Shin Insertion of the membrane-proximal region of the neuronal SNARE coiled coil into the membrane J. Biol. Chem. 278 2003 12367 12373
18. A. Maximov, and J. Tang T.C. Südhof Complexin controls the force transfer from SNARE complexes to membranes in fusion Science 323 2009 516 521
19. E. Fdez, and M. Martínez-Salvador S. Hilfiker Transmembrane-domain determinants for SNARE-mediated membrane fusion J. Cell Sci. 123 2010 2473 2480
20. A.N. Ngatchou, and K. Kisler M. Lindau Role of the synaptobrevin C terminus in fusion pore formation Proc. Natl. Acad. Sci. USA 107 2010 18463 18468
21. J. Tong, and P.P. Borbat Y.-K. Shin A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol Proc. Natl. Acad. Sci. USA 106 2009 5141 5146
22. J.F. Ellena, and B. Liang L.K. Tamm Dynamic structure of lipid-bound synaptobrevin suggests a nucleation-propagation mechanism for trans-SNARE complex formation Proc. Natl. Acad. Sci. USA 106 2009 20306 20311
23. T.J. Siddiqui, and O. Vites D. Fasshauer Determinants of synaptobrevin regulation in membranes Mol. Biol. Cell 18 2007 2037 2046
24. M.J. Arcario, Y.Z. Ohkubo, and E. Tajkhorshid Capturing spontaneous partitioning of peripheral proteins using a biphasic membrane-mimetic model J. Phys. Chem. B 115 2011 7029 7037
25. L. Martínez, and R. Andrade J.M. Martínez PACKMOL: a package for building initial configurations for molecular dynamics simulations J. Comput. Chem. 30 2009 2157 2164
26. N. Kucerka, S. Tristram-Nagle, and J.F. Nagle Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains J. Membr. Biol. 208 2005 193 202
27. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
28. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802
29. A.D. MacKerell Jr., M. Feig, and C.L. Brooks 3rd Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
30. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
31. K. Vanommeslaeghe, and E. Hatcher A.D. MacKerell Jr. CHARMM general force field: a force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 31 2010 671 690
32. W.L. Jorgensen, and J. Chandrasekhar M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
33. G.J. Martyna, D.J. Tobias, and M.L. Klein Constant pressure molecular dynamics algorithms J. Chem. Phys. 101 1994 4177 4189
34. S.E. Feller, Y. Zhang, and R.W. Pastor Constant pressure molecular dynamics simulation: the Langevin piston method J. Chem. Phys. 103 1995 4613 4621
35. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
36. J. Åqvist A simple way to calculate the axis of an α-helix Comput. Chem. 10 1986 97 99
37. M.L. Nonet, and O. Saifee L. Wei Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants J. Neurosci. 18 1998 70 80
38. H.J. Risselada, C. Kutzner, and H. Grubmüller Caught in the act: visualization of SNARE-mediated fusion events in molecular detail ChemBioChem 12 2011 1049 1055
39. I. Martin, J. Ruysschaert, and R.M. Epand Role of the N-terminal peptides of viral envelope proteins in membrane fusion Adv. Drug Deliv. Rev. 38 1999 233 255
40. S. Légaré, and P. Lagüe The influenza fusion peptide promotes lipid polar head intrusion through hydrogen bonding with phosphates and N-terminal membrane insertion depth Proteins 82 2014 2118 2127
41. J.L. Baylon, and I.L. Lenov E. Tajkhorshid Characterizing the membrane-bound state of cytochrome P450 3A4: structure, depth of insertion, and orientation J. Am. Chem. Soc. 135 2013 8542 8551
42. M.J. Arcario, and E. Tajkhorshid Membrane-induced subdomain rearrangement of talin subdomains providing a molecular mechanism for inside-out integrin activation Biophys. J. 107 2014 2059 2069
43. M.B. Jackson SNARE complex zipping as a driving force in the dilation of proteinaceous fusion pores J. Membr. Biol. 235 2010 89 100