Studying protein-reconstituted proteoliposome fusion with content indicators in vitro

BioEssays

Volumn 35, Issue 7, 2013, Pages 658-665

  Diao, Jiajie ^a,b   Zhao, Minglei ^a   Zhang, Yunxiang ^a   Kyoung, Minjoung ^a   Brunger, Axel T ^a  

^a STANFORD UNIVERSITY   (United States)

^b XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Content mixing; Membrane fusion; Proteoliposome; Single molecule; SNARE

Indexed keywords

CALCIUM ION; COMPLEXIN; PROTEIN; PROTEOLIPOSOME; SNARE PROTEIN; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN 1A; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ARTICLE; AUTOMATION; COMPUTER PROGRAM; CRYOELECTRON MICROSCOPY; IN VITRO STUDY; LIPID VESICLE; MEMBRANE FUSION; MOLECULAR DOCKING; PROTEIN LIPID INTERACTION; QUANTITATIVE ANALYSIS;

CALCIUM; CRYOELECTRON MICROSCOPY; EVALUATION STUDIES AS TOPIC; LIPIDS; MEMBRANE FUSION; MODELS, MOLECULAR; PROTEOLIPIDS; SNARE PROTEINS; SOFTWARE;

EID: 84879148115     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300010     Document Type: Article

References (58)

1. Sudhof TC, Rothman JE. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-7.
2. Struck DK, Hoekstra D, Pagano RE. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20: 4093-9.
3. Weber T, Zemelman BV, McNew JA, Westermann B, et al. 1998. SNAREpins: minimal machinery for membrane fusion. Cell 92: 759-72.
4. Bowen ME, Weninger K, Brunger AT, 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: 3569-84.
5. Kyoung M, Srivastava A, Zhang YX, Diao JJ, et al. 2011. In vitro system capable of differentiating fast Ca(2 +)-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc Natl Acad Sci USA 108: E304-13.
6. Floyd DL, Ragains JR, Skehel JJ, Harrison SC, et al. 2008. Single-particle kinetics of influenza virus membrane fusion. Proc Natl Acad Sci USA 105: 15382-7.
7. Jun Y, Wickner W. 2007. Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc Natl Acad Sci USA 104: 13010-5.
8. Diao J, Grob P, Cipriano DJ, Kyoung M, et al. 2012. Synaptic proteins promote calcium-triggered fast transition from point contact to full fusion. eLife 1: e00109.
9. Cypionka A, Stein A, Hernandez JM, Hippchen H, et al. 2009. Discrimination between docking and fusion of liposomes reconstituted with neuronal SNARE-proteins using FCS. Proc Natl Acad Sci USA 106: 18575-80.
10. Diao J, Ishitsuka Y, Bae WR. 2011. Single-molecule FRET study of SNARE-mediated membrane fusion. Biosci Rep 31: 457-63.
11. Diao J, Su ZL, Lu XB, Yoon TY, et al. 2010. Single-vesicle fusion assay reveals Munc 18-1 binding to the SNARE core is sufficient for stimulating membrane fusion. ACS Chem Neurosci 1: 168-74.
12. Yoon TY, Lu X, Diao JJ, Lee SM, et al. 2008. Complexin and Ca(2 +) stimulate SNARE-mediated membrane fusion. Nat Struct Mol Biol 15: 707-13.
13. Kyoung M, Zhang Y, Diao J, Chu S, et al. 2012. Studying calcium-triggered vesicle fusion in a single vesicle-vesicle content and lipid-mixing system. Nat Protoc 8: 1-16.
14. Kim JY, Choi BK, Choi MG, Kim SA, et al. 2012. Solution single-vesicle assay reveals PIP2-mediated sequential actions of synaptotagmin-1 on SNAREs. EMBO J 31: 2144-55.
15. Chan YHM, van Lengerich B, Boxer SG. 2009. Effects of linker sequences on vesicle fusion mediated by lipid-anchored DNA oligonucleotides. Proc Natl Acad Sci USA 106: 979-84.
16. Sorensen JB. 2009. Conflicting views on the membrane fusion machinery and the fusion pore. Annu Rev Cell Dev Bi 25: 513-37.
17. Schneggenburger R, Neher E. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889-93.
18. Wang Z, Liu H, Gu Y, Chapman ER. 2011. Reconstituted synaptotagmin I mediates vesicle docking, priming, and fusion. J Cell Biol 195: 1159-70.
19. van den Bogaart G, Thutupalli S, Risselada JH, Meyenberg K, et al. 2011. Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat Struct Mol Biol 18: 805-12.
20. Lee HK, Yang Y, Su ZL, Hyeon C, et al. 2010. Dynamic Ca(2 +)-dependent stimulation of vesicle fusion by membrane-anchored Synaptotagmin 1. Science 328: 760-3.
21. Diao J, Ishitsuka Y, Lee H, Joo C, et al. 2012. A single vesicle-vesicle fusion assay for in vitro studies of SNAREs and accessory proteins. Nat Protoc 7: 921-34.
22. Diao J, Su ZL, Ishitsuka Y, Lu B, et al. 2010. A single-vesicle content mixing assay for SNARE-mediated membrane fusion. Nat Commun 1: 54.
23. Lai Y, Diao J, Liu Y, Ishitsuka Y, et al. 2013. Fusion pore formation and expansion induced by Ca2+ and synaptotagmin 1. Proc Natl Acad Sci USA 110: 1333-8.
24. Shi L, Shen QT, Kiel A, Wang J, et al. 2012. SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335: 1355-9.
25. Ma C, Su L, Seven AB, Xu Y, et al. 2013. Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science 339: 421-5.
26. Zucchi PC, Zick M. 2011. Membrane fusion catalyzed by a Rab, SNAREs, and SNARE chaperones is accompanied by enhanced permeability to small molecules and by lysis. Mol Biol Cell 22: 4635-46.
27. Joo C, Balci H, Ishitsuka Y, Buranachai C, et al. 2008. Advances in single-molecule fluorescence methods for molecular biology. Annu Rev Biochem 77: 51-76.
28. Wang YZ. 1995. Jump and sharp cusp detection by wavelets. Biometrika 82: 385-97.
29. Rudin LI, Osher S, Fatemi E. 1992. Nonlinear total variation based noise removal algorithms. Physica D 60: 259-68.
30. Lin DC, Dimitriadis EK, Horkay F. 2007. Robust strategies for automated AFM force curve analysis - I. Non-adhesive indentation of soft, inhomogeneous materials. J Biomech Eng-T ASME 129: 430-40.
31. Wald A, Wolfowitz J. 1940. On a test whether two samples are from the same population. Ann Math Stat 11: 147-62.
32. Diao J, Burre J, Vivona S, Cipriano DJ, et al. 2013. Native α-synuclein induces clustering of synaptic vesicle mimics via binding to phospholipids and synaptobrevin-2/VAMP2. eLife 2: e00592.
33. Marshall RA, Aitken CE, Dorywalska M, Puglisi JD. 2008. Translation at the single-molecule level. Annu Rev Biochem 77: 177-203.
34. Gray EG, Whittaker VP. 1962. Isolation of nerve endings from brain - an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat 96: 79-88.
35. Whittaker VP, Gray EG. 1962. The synapse: biology and morphology. Brit Med Bull 18: 223-8.
36. Whittaker VP, Michaelson IA, Kirkland RJ. 1964. Separation of synaptic vesicles from nerve-ending particles (synaptosomes). Biochem J 90: 293-303.
37. Baumert M, Maycox PR, Navone F, Decamilli P, et al. 1989. Synaptobrevin - an integral membrane-protein of 18000 Daltons present in small synaptic vesicles of rat-brain. EMBO J 8: 379-84.
38. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4: 391-5.
39. Groffen AJ, Martens S, Arazola RD, Cornelisse LN, et al. 2010. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 327: 1614-8.
40. Hui EF, Johnson CP, Yao J, Dunning FM, et al. 2009. Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2+)-regulated fusion. Cell 138: 709-21.
41. Diao J, Yoon TY, Su ZL, Shin YK, et al. 2009. C2AB: a molecular glue for lipid vesicles with a negatively charged surface. Langmuir 25: 7177-80.
42. Martens S, Kozlov MM, McMahon HT. 2007. How synaptotagmin promotes membrane fusion. Science 316: 1205-8.
43. Bremer A, Henn C, Engel A, Baumeister W, et al. 1992. Has negative staining still a place in biomacromolecular electron-microscopy. Ultramicroscopy 46: 85-111.
44. Hsieh CE, Leith A, Mannella CA, Frank J, et al. 2006. Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J Struct Biol 153: 1-13.
45. Zhou ZH. 2008. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr Opin Struc Biol 18: 218-28.
46. Xu Y, Seven AB, Su L, Jiang QX, et al. 2011. Membrane bridging and hemifusion by denaturated Munc18. Plos ONE 6: e22012.
47. Holt M, Riedel D, Stein A, Schuette C, et al. 2008. Synaptic vesicles are constitutively active fusion machines that function independently of Ca(2+). Curr Biol 18: 715-22.
48. 2+-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat Struct Mol Biol 13: 209-17.
49. Hernandez JM, Stein A, Behrmann E, Riedel D, et al. 2012. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336: 1581-4.
50. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
51. Vrljic M, Strop P, Ernst JA, Sutton RB, et al. 2010. Molecular mechanism of the synaptotagmin-SNARE interaction in Ca(2+)-triggered vesicle fusion. Nat Struct Mol Biol 17: 325-31.
52. Sutton RB, Fasshauer D, Jahn R, Brunger AT. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 angstrom resolution. Nature 395: 347-53.
53. Choi UB, Strop P, Vrljic M, Chu S, et al. 2010. Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex. Nat Struct Mol Biol 17: 318-24.
54. Rizzoli SO, Betz WJ. 2005. Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
55. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
56. Denker A, Bethani I, Krohnert K, Korber C, et al. 2011. A small pool of vesicles maintains synaptic activity in vivo. Proc Natl Acad Sci USA 108: 17177-82.
57. Ivanovic T, Choi J, Whelan S, van Oijen A, et al. 2013. Influenza-virus membrane fusion: cooperative fold-back of stochastically induced hemagglutinin intermediates. eLife 2: e00333.
58. Ivanovic T, Rozendaal R, Floyd DL, Popovic M, et al. 2012. Kinetics of proton transport into influenza virions by the viral M2 channel. Plos ONE 7: e31566.