Three steps forward, two steps back: Mechanistic insights into the assembly and disassembly of the SNARE complex

Current Opinion in Chemical Biology

Volumn 29, Issue , 2015, Pages 66-71

  Bombardier, Jeffrey P ^a   Munson, Mary ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; N ETHYLMALEIMIDE SENSITIVE FACTOR; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNTAXIN;

CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; EXOCYTOSIS; HYSTERESIS; MEMBRANE FUSION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; REVIEW; SYNAPSE VESICLE; TRANSPORT VESICLE; ANIMAL; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; EXOCYTOSIS; HUMANS; MEMBRANE FUSION; PROTEIN MULTIMERIZATION; SNARE PROTEINS; TRANSPORT VESICLES;

EID: 84945298509     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.10.003     Document Type: Review

References (49)

1. Jahn R., Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012, 490:201-207.
2. Jahn R., Scheller R.H. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006, 7:631-643.
3. Rizo J., Sudhof T.C. The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices-guilty as charged?. Annu Rev Cell Dev Biol 2012, 28:279-308.
4. Sudhof T.C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 2013, 80:675-690.
5. Sudhof T.C. A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat Med 2013, 19:1227-1231.
6. Heider M.R., Munson M. Exorcising the exocyst complex. Traffic 2012, 13:898-907.
7. Hirokawa N., Niwa S., Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 2010, 68:610-638.
8. Martens S., McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol 2008, 9:543-556.
9. Munson M., Novick P. The exocyst defrocked, a framework of rods revealed. Nat Struct Mol Biol 2006, 13:577-581.
10. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009, 10:513-525.
11. Dubuke M.L., Maniatis S., Shaffer S.A., Munson M. The exocyst subunit Sec6 interacts with assembled exocytic SNARE complexes. J Biol Chem 2015, (in press).
12. Murthy M., Garza D., Scheller R.H., Schwarz T.L. Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 2003, 37:433-447.
13. Inoue M., Chang L., Hwang J., Chiang S.H., Saltiel A.R. The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 2003, 422:629-633.
14. Carr C.M., Rizo J. At the junction of SNARE and SM protein function. Curr Opin Cell Biol 2010, 22:488-495.
15. Yang X., Wang S., Sheng Y., Zhang M., Zou W., Wu L., Kang L., Rizo J., Zhang R., Xu T., et al. Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming. Nat Struct Mol Biol 2015, 22:547-554.
16. Fasshauer D., Otto H., Eliason W.K., Jahn R., Brunger A.T. Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation. J Biol Chem 1997, 272:28036-28041.
17. Stein A., Weber G., Wahl M.C., Jahn R. Helical extension of the neuronal SNARE complex into the membrane. Nature 2009, 460:525-528.
18. Hanson P.I., Roth R., Morisaki H., Jahn R., Heuser J.E. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 1997, 90:523-535.
19. Poirier M.A., Xiao W., Macosko J.C., Chan C., Shin Y.K., Bennett M.K. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat Struct Biol 1998, 5:765-769.
20. Sutton R.B., Fasshauer D., Jahn R., Brunger A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998, 395:347-353.
21. Lauer J.M., Dalal S., Marz K.E., Nonet M.L., Hanson P.I. SNARE complex zero layer residues are not critical for N-ethylmaleimide-sensitive factor-mediated disassembly. J Biol Chem 2006, 281:14823-14832.
22. Weber T., Zemelman B.V., McNew J.A., Westermann B., Gmachl M., Parlati F., Sollner T.H., Rothman J.E. SNAREpins: minimal machinery for membrane fusion. Cell 1998, 92:759-772.
23. Kweon D.H., Kim C.S., Shin Y.K. Regulation of neuronal SNARE assembly by the membrane. Nat Struct Biol 2003, 10:440-447.
24. Pobbati A.V., Stein A., Fasshauer D. N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 2006, 313:673-676.
25. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
26. Gao Y., Zorman S., Gundersen G., Xi Z., Ma L., Sirinakis G., Rothman J.E., Zhang Y. Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science 2012, 337:1340-1343.
27. Min D., Kim K., Hyeon C., Cho Y.H., Shin Y.K., Yoon T.Y. Mechanical unzipping and rezipping of a single SNARE complex reveals hysteresis as a force-generating mechanism. Nat Commun 2013, 4:1705.
28. Zorman S., Rebane A.A., Ma L., Yang G., Molski M.A., Coleman J., Pincet F., Rothman J.E., Zhang Y. Common intermediates and kinetics, but different energetics, in the assembly of SNARE proteins. Elife 2014, 3:e03348.
29. Schwartz M.L., Merz A.J. Capture and release of partially zipped trans-SNARE complexes on intact organelles. J Cell Biol 2009, 185:535-549.
30. Fasshauer D., Antonin W., Subramaniam V., Jahn R. SNARE assembly and disassembly exhibit a pronounced hysteresis. Nat Struct Biol 2002, 9:144-151.
31. Bowen M.E., Weninger K., Brunger A.T., Chu S. Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). Biophys J 2004, 87:3569-3584.
32. Liu T., Tucker W.C., Bhalla A., Chapman E.R., Weisshaar J.C. SNARE-driven, 25-millisecond vesicle fusion in vitro. Biophys J 2005, 89:2458-2472.
33. Domanska M.K., Kiessling V., Stein A., Fasshauer D., Tamm L.K. Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNARE-mediated membrane fusion. J Biol Chem 2009, 284:32158-32166.
34. Karatekin E., Di Giovanni J., Iborra C., Coleman J., O'Shaughnessy B., Seagar M., Rothman J.E. A fast, single-vesicle fusion assay mimics physiological SNARE requirements. Proc Natl Acad Sci U S A 2010, 107:3517-3521.
35. Nofal S., Becherer U., Hof D., Matti U., Rettig J. Primed vesicles can be distinguished from docked vesicles by analyzing their mobility. J Neurosci 2007, 27:1386-1395.
36. Heuser J.E., Reese T.S., Landis D.M. Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol 1974, 3:109-131.
37. Munson M. Synaptic-vesicle fusion: a need for speed. Nat Struct Mol Biol 2015, 22:509-511.
38. Giraudo C.G., Eng W.S., Melia T.J., Rothman J.E. A clamping mechanism involved in SNARE-dependent exocytosis. Science 2006, 313:676-680.
39. Kummel D., Krishnakumar S.S., Radoff D.T., Li F., Giraudo C.G., Pincet F., Rothman J.E., Reinisch K.M. Complexin cross-links prefusion SNAREs into a zigzag array. Nat Struct Mol Biol 2011, 18:927-933.
40. Brewer K.D., Bacaj T., Cavalli A., Camilloni C., Swarbrick J.D., Liu J., Zhou A., Zhou P., Barlow N., Xu J., et al. Dynamic binding mode of a Synaptotagmin-1-SNARE complex in solution. Nat Struct Mol Biol 2015, 22:555-564.
41. Krishnakumar S.S., Radoff D.T., Kummel D., Giraudo C.G., Li F., Khandan L., Baguley S.W., Coleman J., Reinisch K.M., Pincet F., et al. A conformational switch in complexin is required for synaptotagmin to trigger synaptic fusion. Nat Struct Mol Biol 2011, 18:934-940.
42. Trimbuch T., Xu J., Flaherty D., Tomchick D.R., Rizo J., Rosenmund C. Re-examining how complexin inhibits neurotransmitter release. Elife 2014, 3:e02391.
43. Ryu J.K., Min D., Rah S.H., Kim S.J., Park Y., Kim H., Hyeon C., Kim H.M., Jahn R., Yoon T.Y. Spring-loaded unraveling of a single SNARE complex by NSF in one round of ATP turnover. Science 2015, 347:1485-1489.
44. Zhao M., Wu S., Zhou Q., Vivona S., Cipriano D.J., Cheng Y., Brunger A.T. Mechanistic insights into the recycling machine of the SNARE complex. Nature 2015, 518:61-67.
45. Shah N., Colbert K.N., Enos M.D., Herschlag D., Weis W.I. Three alphaSNAP and 10 ATP molecules are used in SNARE complex disassembly by N-ethylmaleimide-sensitive factor (NSF). J Biol Chem 2015, 290:2175-2188.
46. Hayashi T., Yamasaki S., Nauenburg S., Binz T., Niemann H. Disassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro. EMBO J 1995, 14:2317-2325.
47. Littleton J.T., Barnard R.J., Titus S.A., Slind J., Chapman E.R., Ganetzky B. SNARE-complex disassembly by NSF follows synaptic-vesicle fusion. Proc Natl Acad Sci U S A 2001, 98:12233-12238.
48. Lobingier B.T., Nickerson D.P., Lo S.Y., Merz A.J. SM proteins Sly1 and Vps33 co-assemble with Sec17 and SNARE complexes to oppose SNARE disassembly by Sec18. Elife 2014, 3:e02272.
49. Zick M., Orr A., Schwartz M.L., Merz A.J., Wickner W.T. Sec17 can trigger fusion of trans-SNARE paired membranes without Sec18. Proc Natl Acad Sci U S A 2015, 112:E2290-E2297.