SNARE and regulatory proteins induce local membrane protrusions to prime docked vesicles for fast calcium-triggered fusion

EMBO Reports

Volumn 15, Issue 3, 2014, Pages 308-314

  Bharat, Tanmay A M ^a,c   Malsam, Jörg ^b   Hagen, Wim J H ^a   Scheutzow, Andrea ^b   Söllner, Thomas H ^b   Briggs, John A G ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

cryo electron microscopy; cryo electron tomography; in vitro reconstitution; membrane curvature; SNARE mediated membrane fusion

Indexed keywords

CALCIUM; REGULATOR PROTEIN; SNARE PROTEIN; SYNAPTOTAGMIN I;

ARTICLE; CALCIUM TRANSPORT; CELL ENERGY; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; IN VITRO STUDY; MEMBRANE FUSION; MEMBRANE RECONSTITUTION; MOLECULAR DOCKING; PRIORITY JOURNAL; SYNAPSE VESICLE; SYNAPTIC MEMBRANE;

CALCIUM; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; MEMBRANE FUSION; MUNC18 PROTEINS; SYNAPTOTAGMIN I; UNILAMELLAR LIPOSOMES; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84898619506     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1002/embr.201337807     Document Type: Article

References (33)

1. Bruns D, Jahn R, (1995) Real-time measurement of transmitter release from single synaptic vesicles. Nature 377: 62-65
2. Sabatini BL, Regehr WG, (1996) Timing of neurotransmission at fast synapses in the mammalian brain. Nature 384: 170-172 (Pubitemid 26386472)
3. Rizo J, Rosenmund C, (2008) Synaptic vesicle fusion. Nat Struct Mol Biol 15: 665-674 (Pubitemid 351932007)
4. Südhof TC, (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547 (Pubitemid 39050412)
5. Sutton RB, Fasshauer D, Jahn R, Brunger AT, (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353 (Pubitemid 28450677)
6. Fasshauer D, Sutton RB, Brunger AT, Jahn R, (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci USA 95: 15781-15786 (Pubitemid 29018777)
7. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE, (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362: 318-324 (Pubitemid 23101303)
8. Stein A, Weber G, Wahl MC, Jahn R, (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460: 525-528
9. Gao Y, Zorman S, Gundersen G, Xi Z, Ma L, Sirinakis G, Rothman JE, Zhang Y, (2012) Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science 337: 1340-1343
10. Südhof TC, Rizo J, (2011) Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3: pii: a005637
11. Chapman ER, (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77: 615-641
12. Jahn R, Fasshauer D, (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490: 201-207
13. Martens S, McMahon HT, (2011) C2 domains and membrane fusion. Curr Top Membr 68: 141-159
14. 2+ -dependent release. EMBO J 31: 3270-3281
15. 2+ -dependent trans interaction with phospholipids. Nat Struct Mol Biol 14: 904-911 (Pubitemid 47525181)
16. de Wit H, Walter AM, Milosevic I, Gulyás-Kovács A, Riedel D, Sørensen JB, Verhage M, (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138: 935-946
17. Reist NE, Buchanan J, Li J, DiAntonio A, Buxton EM, Schwarz TL, (1998) Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila. J Neurosci 18: 7662-7673 (Pubitemid 28441008)
18. Wang Z, Liu H, Gu Y, Chapman ER, (2011) Reconstituted synaptotagmin I mediates vesicle docking, priming, and fusion. J Cell Biol 195: 1159-1170
19. Kim JY, Choi BK, Choi MG, Kim SA, Lai Y, Shin YK, Lee NK, (2012) Solution single-vesicle assay reveals PIP2-mediated sequential actions of synaptotagmin-1 on SNAREs. EMBO J 31: 2144-2155
20. Maximov A, Tang J, Yang X, Pang ZP, Südhof TC, (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323: 516-521
21. Kümmel D, Krishnakumar SS, Radoff DT, Li F, Giraudo CG, Pincet F, Rothman JE, Reinisch KM, (2011) Complexin cross-links prefusion SNAREs into a zigzag array. Nat Struct Mol Biol 18: 927-933
22. Xu Y, Su L, Rizo J, (2010) Binding of Munc18-1 to synaptobrevin and to the SNARE four-helix bundle. Biochemistry 49: 1568-1576
23. Parisotto D, Malsam J, Scheutzow A, Krause JM, Söllner TH, (2012) SNAREpin assembly by Munc18-1 requires previous vesicle docking by synaptotagmin 1. J Biol Chem 287: 31041-31049
24. 2+ -triggered vesicle fusion. Nat Struct Mol Biol 17: 325-331
25. Hernandez JM, Stein A, Behrmann E, Riedel D, Cypionka A, Farsi Z, Walla PJ, Raunser S, Jahn R, (2012) Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336: 1581-1584
26. Diao J, Grob P, Cipriano DJ, Kyoung M, Zhang Y, Shah S, Nguyen A, Padolina M, Srivastava A, Vrljic M, Shah A, Nogales E, Chu S, Brunger AT, (2012) Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion. Elife 1: e00109
27. Monck JR, Fernandez JM, (1992) The exocytotic fusion pore. J Cell Biol 119: 1395-1404 (Pubitemid 23006539)
28. Efrat A, Chernomordik LV, Kozlov MM, (2007) Point-like protrusion as a prestalk intermediate in membrane fusion pathway. Biophys J 92: L61-L63
29. Chernomordik LV, Kozlov MM, (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15: 675-683 (Pubitemid 351932010)
30. Kozlov MM, McMahon HT, Chernomordik LV, (2010) Protein-driven membrane stresses in fusion and fission. Trends Biochem Sci 35: 699-706
31. Mastronarde DN, (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51 (Pubitemid 41384176)
32. Kremer JR, Mastronarde DN, McIntosh JR, (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76 (Pubitemid 26093126)
33. Amat F, Castaño-Diez D, Lawrence A, Moussavi F, Winkler H, Horowitz M, (2010) Alignment of cryo-electron tomography datasets. Methods Enzymol 482: 343-367