High Cholesterol Obviates a Prolonged Hemifusion Intermediate in Fast SNARE-Mediated Membrane Fusion

Biophysical Journal

Volumn 109, Issue 2, 2015, Pages 319-329

  Kreutzberger, Alex J B ^a   Kiessling, Volker ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; CHOLESTEROL; LIPID BILAYER; SNARE PROTEIN; SYNAPTOBREVIN 2;

ANIMAL; BRAIN; COMPARATIVE STUDY; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; LIPID BILAYER; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY; PIG; RAT; TIME FACTOR;

ALPHA-TOCOPHEROL; ANIMALS; BRAIN; CHOLESTEROL; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; LIPID BILAYERS; MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; RATS; SNARE PROTEINS; SWINE; TIME FACTORS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84937553937     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.06.022     Document Type: Article

References (76)

1. L.K. Tamm, J. Crane, and V. Kiessling Membrane fusion: a structural perspective on the interplay of lipids and proteins Curr. Opin. Struct. Biol. 13 2003 453 466
2. S. Martens, and H.T. McMahon Mechanisms of membrane fusion: disparate players and common principles Nat. Rev. Mol. Cell Biol. 9 2008 543 556
3. L.V. Chernomordik, and M.M. Kozlov Mechanics of membrane fusion Nat. Struct. Mol. Biol. 15 2008 675 683
4. J.E. Rothman The principle of membrane fusion in the cell (Nobel lecture) Angew. Chem. Int. Ed. Engl. 53 2014 12676 12694
5. A.T. Brunger Structure and function of SNARE and SNARE-interacting proteins Q. Rev. Biophys. 38 2005 1 47
6. J. Rizo, and C. Rosenmund Synaptic vesicle fusion Nat. Struct. Mol. Biol. 15 2008 665 674
7. R. Jahn, and D. Fasshauer Molecular machines governing exocytosis of synaptic vesicles Nature 490 2012 201 207
8. T.C. Südhof Neurotransmitter release: the last millisecond in the life of a synaptic vesicle Neuron 80 2013 675 690
9. T. Weber, and B.V. Zemelman J.E. Rothman SNAREpins: minimal machinery for membrane fusion Cell 92 1998 759 772
10. C.G. Schuette, and K. Hatsuzawa R. Jahn Determinants of liposome fusion mediated by synaptic SNARE proteins Proc. Natl. Acad. Sci. USA 101 2004 2858 2863
11. O. Zamir, and M.P. Charlton Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions J. Physiol. 571 2006 83 99
12. C.R. Wasser, and M. Ertunc E.T. Kavalali Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling J. Physiol. 579 2007 413 429
13. A. Linetti, and A. Fratangeli P. Rosa Cholesterol reduction impairs exocytosis of synaptic vesicles J. Cell Sci. 123 2010 595 605
14. M.A. Churchward, and T. Rogasevskaia J.R. Coorssen Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion J. Cell Sci. 118 2005 4833 4848
15. M.A. Churchward, and T. Rogasevskaia J.R. Coorssen Specific lipids supply critical negative spontaneous curvature - an essential component of native Ca2+-triggered membrane fusion Biophys. J. 94 2008 3976 3986
16. M.A. Churchward, and J.R. Coorssen Cholesterol, regulated exocytosis and the physiological fusion machine Biochem. J. 423 2009 1 14
17. L.H. Chamberlain, R.D. Burgoyne, and G.W. Gould SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis Proc. Natl. Acad. Sci. USA 98 2001 5619 5624
18. T. Lang, and D. Bruns R. Jahn SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis EMBO J. 20 2001 2202 2213
19. E. Taverna, and E. Saba P. Rosa Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes J. Biol. Chem. 279 2004 5127 5134
20. C. Salaün, G.W. Gould, and L.H. Chamberlain Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells J. Biol. Chem. 280 2005 19449 19453
21. C. Salaün, G.W. Gould, and L.H. Chamberlain The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells. Regulation by distinct cysteine-rich domains J. Biol. Chem. 280 2005 1236 1240
22. C. Gil, and A. Soler-Jover J. Aguilera Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes Biochem. Biophys. Res. Commun. 329 2005 117 124
23. T. Lang SNARE proteins and 'membrane rafts' J. Physiol. 585 2007 693 698
24. E. Taverna, and E. Saba P. Rosa Localization of synaptic proteins involved in neurosecretion in different membrane microdomains J. Neurochem. 100 2007 664 677
25. G. van den Bogaart, T. Lang, and R. Jahn Microdomains of SNARE proteins in the plasma membrane Curr. Top. Membr. 72 2013 193 230
26. D.H. Murray, and L.K. Tamm Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol Biochemistry 48 2009 4617 4625
27. D.H. Murray, and L.K. Tamm Molecular mechanism of cholesterol- and polyphosphoinositide-mediated syntaxin clustering Biochemistry 50 2011 9014 9022
28. J.W. Deutsch, and R.B. Kelly Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion Biochemistry 20 1981 378 385
29. C. Thiele, and M.J. Hannah W.B. Huttner Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles Nat. Cell Biol. 2 2000 42 49
30. S. Takamori, and M. Holt R. Jahn Molecular anatomy of a trafficking organelle Cell 127 2006 831 846
31. J. Chang, and S.A. Kim Y.K. Shin Fusion step-specific influence of cholesterol on SNARE-mediated membrane fusion Biophys. J. 96 2009 1839 1846
32. 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
33. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
34. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nat. Rev. Mol. Cell Biol. 11 2010 688 699
35. P.L. Yeagle Lanosterol and cholesterol have different effects on phospholipid acyl chain ordering Biochim. Biophys. Acta 815 1985 33 36
36. M.B. Sankaram, and T.E. Thompson Modulation of phospholipid acyl chain order by cholesterol. A solid-state 2H nuclear magnetic resonance study Biochemistry 29 1990 10676 10684
37. D.J. Recktenwald, and H.M. McConnell Phase equilibria in binary mixtures of phosphatidylcholine and cholesterol Biochemistry 20 1981 4505 4510
38. J.R. Coorssen, and R.P. Rand Effects of cholesterol on the structural transitions induced by diacylglycerol in phosphatidylcholine and phosphatidylethanolamine bilayer systems Biochem. Cell Biol. 68 1990 65 69
39. Z. Chen, and R.P. Rand The influence of cholesterol on phospholipid membrane curvature and bending elasticity Biophys. J. 73 1997 267 276
40. W. Wang, L. Yang, and H.W. Huang Evidence of cholesterol accumulated in high curvature regions: implication to the curvature elastic energy for lipid mixtures Biophys. J. 92 2007 2819 2830
41. M.E. Bowen, and K. Weninger S. Chu Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs) Biophys. J. 87 2004 3569 3584
42. T. Liu, and W.C. Tucker J.C. Weisshaar SNARE-driven, 25-millisecond vesicle fusion in vitro Biophys. J. 89 2005 2458 2472
43. T.Y. Yoon, and B. Okumus T. Ha Multiple intermediates in SNARE-induced membrane fusion Proc. Natl. Acad. Sci. USA 103 2006 19731 19736
44. M.K. Domanska, and V. Kiessling L.K. Tamm Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNARE-mediated membrane fusion J. Biol. Chem. 284 2009 32158 32166
45. V. Kiessling, B. Liang, and L.K. Tamm Reconstituting SNARE-mediated membrane fusion at the single liposome level Methods Cell Biol. 128 2015 339 363
46. A.T. Brunger, D.J. Cipriano, and J. Diao Towards reconstitution of membrane fusion mediated by SNAREs and other synaptic proteins Crit. Rev. Biochem. Mol. Biol. 2015 10.3109/10409238.2015.1023252 Published online March 19, 2015
47. M.K. Domanska, V. Kiessling, and L.K. Tamm Docking and fast fusion of synaptobrevin vesicles depends on the lipid compositions of the vesicle and the acceptor SNARE complex-containing target membrane Biophys. J. 99 2010 2936 2946
48. J.M. Hernandez, and A.J. Kreutzberger R. Jahn Variable cooperativity in SNARE-mediated membrane fusion Proc. Natl. Acad. Sci. USA 111 2014 12037 12042
49. D. Fasshauer, and W. Antonin R. Jahn Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties J. Biol. Chem. 274 1999 15440 15446
50. D. Fasshauer, and M. Margittai A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly J. Biol. Chem. 279 2004 7613 7621
51. A. Stein, and A. Radhakrishnan R. Jahn Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids Nat. Struct. Mol. Biol. 14 2007 904 911
52. V. Kiessling, and S. Ahmed L.K. Tamm Rapid fusion of synaptic vesicles with reconstituted target SNARE membranes Biophys. J. 104 2013 1950 1958
53. M.L. Wagner, and L.K. Tamm Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers Biophys. J. 81 2001 266 275
54. M.L. Wagner, and L.K. Tamm Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker Biophys. J. 79 2000 1400 1414
55. E. Kalb, S. Frey, and L.K. Tamm Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers Biochim. Biophys. Acta 1103 1992 307 316
56. J.M. Hernandez, and A. Stein R. Jahn Membrane fusion intermediates via directional and full assembly of the SNARE complex Science 336 2012 1581 1584
57. V. Kiessling, J.M. Crane, and L.K. Tamm Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking Biophys. J. 91 2006 3313 3326
58. G.R. Bartlett Phosphorus assay in column chromatography J. Biol. Chem. 234 1959 466 468
59. A. Pokorny, T.H. Birkbeck, and P.F. Almeida Mechanism and kinetics of delta-lysin interaction with phospholipid vesicles Biochemistry 41 2002 11044 11056
60. V. Kiessling, M.K. Domanska, and L.K. Tamm Single SNARE-mediated vesicle fusion observed in vitro by polarized TIRFM Biophys. J. 99 2010 4047 4055
61. T. Wang, and E.A. Smith J.C. Weisshaar Lipid mixing and content release in single-vesicle, SNARE-driven fusion assay with 1-5 ms resolution Biophys. J. 96 2009 4122 4131
62. R.J. Rawle, and B. van Lengerich S.G. Boxer Vesicle fusion observed by content transfer across a tethered lipid bilayer Biophys J 101 2011 L37 L39
63. B. van Lengerich, R.J. Rawle, P.M. Bendix, and S.G. Boxer Individual vesicle fusion events mediated by lipid-anchored DNA Biophys J 105 2013 409 419
64. A. Bradford, and J. Atkinson R.P. Rand The effect of vitamin E on the structure of membrane lipid assemblies J. Lipid Res. 44 2003 1940 1945
65. D. Mitter, and C. Reisinger G. Ahnert-Hilger The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content J. Neurochem. 84 2003 35 42
66. W.B. Huttner, and A. Schmidt Lipids, lipid modification and lipid-protein interaction in membrane budding and fission - insights from the roles of endophilin A1 and synaptophysin in synaptic vesicle endocytosis Curr. Opin. Neurobiol. 10 2000 543 551
67. C. Wan, and V. Kiessling L.K. Tamm Partitioning of synaptotagmin I C2 domains between liquid-ordered and liquid-disordered inner leaflet lipid phases Biochemistry 50 2011 2478 2485
68. J.H. Lv, L. He, and S.F. Sui Lipid rafts association of synaptotagmin I on synaptic vesicles Biochemistry (Mosc.) 73 2008 283 288
69. N. Kato, M. Nakanishi, and N. Hirashima Cholesterol depletion inhibits store-operated calcium currents and exocytotic membrane fusion in RBL-2H3 cells Biochemistry 42 2003 11808 11814
70. B. Liang, and D. Dawidowski D.S. Cafiso The SNARE motif of synaptobrevin exhibits an aqueous-interfacial partitioning that is modulated by membrane curvature Biochemistry 53 2014 1485 1494
71. B. Liang, V. Kiessling, and L.K. Tamm Prefusion structure of syntaxin-1A suggests pathway for folding into neuronal trans-SNARE complex fusion intermediate Proc. Natl. Acad. Sci. USA 110 2013 19384 19389
72. L. Yang, and H.W. Huang Observation of a membrane fusion intermediate structure Science 297 2002 1877 1879
73. S. Aeffner, and T. Reusch T. Salditt Energetics of stalk intermediates in membrane fusion are controlled by lipid composition Proc. Natl. Acad. Sci. USA 109 2012 E1609 E1618
74. L.V. Chernomordik, and M.M. Kozlov Membrane hemifusion: crossing a chasm in two leaps Cell 123 2005 375 382
75. J. Otterstrom, and A.M. van Oijen Visualization of membrane fusion, one particle at a time Biochemistry 52 2013 1654 1668
76. M. Kyoung, and A. Srivastava A.T. Brunger In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release Proc. Natl. Acad. Sci. USA 108 2011 E304 E313