Partitioning of synaptotagmin i C2 domains between liquid-ordered and liquid-disordered inner leaflet lipid phases

Biochemistry

Volumn 50, Issue 13, 2011, Pages 2478-2485

  Wan, Chen ^a,b   Kiessling, Volker ^a,b   Cafiso, David S ^a   Tamm, Lukas K ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PHOSPHOLIPIDS; BILAYER SYSTEMS; CALCIUM SENSORS; CHOLESTEROL CONTENT; CHOLESTEROL-RICH DOMAINS; DISORDERED DOMAINS; DISORDERED PHASE; INNER LEAFLETS; LIPID DISTRIBUTIONS; LIPID PHASE; LIQUID-ORDERED PHASE; MEMBRANE BINDING; MEMBRANE DOMAIN; MEMBRANE FUSION; NEUROTRANSMITTER RELEASE; PRESYNAPTIC; SYNAPTIC VESICLE; SYNAPTOTAGMINS;

CALCIUM; CELL MEMBRANES; CHOLESTEROL; LIPID BILAYERS; MEMBRANES; PHOSPHOLIPIDS;

LIQUIDS;

CALCIUM ION; CHOLESTEROL; LIPID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLSERINE; SYNAPTOTAGMIN; SYNAPTOTAGMIN C2A; SYNAPTOTAGMIN C2AB; SYNAPTOTAGMIN I; SYNAPTOTAGMIN I C2; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; ASYMMETRIC SYNTHESIS; BINDING AFFINITY; CONTROLLED STUDY; LIPID ANALYSIS; LIPID BILAYER; LIPID MEMBRANE; LIQUID; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; STEREOCHEMISTRY;

ANIMALS; CALCIUM; CHOLESTEROL; FLUORESCENT DYES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MICROSCOPY, FLUORESCENCE; MUTANT PROTEINS; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLSERINES; PROTEIN INTERACTION DOMAINS AND MOTIFS; QUINOLINIUM COMPOUNDS; RATS; RECOMBINANT PROTEINS; SOLUBILITY; SYNAPTOTAGMIN I; UNILAMELLAR LIPOSOMES;

EID: 79953223640     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101864k     Document Type: Article

References (53)

1. Jahn, R., Lang, T., and Sudhof, T. C. (2003) Membrane fusion Cell 112, 519-533 (Pubitemid 36263084)
2. Rizo, J. and Rosenmund, C. (2008) Synaptic vesicle fusion Nat. Struct. Mol. Biol. 15, 665-674 (Pubitemid 351932007)
3. Sudhof, T. C. and Rothman, J. E. (2009) Membrane fusion: Grappling with SNARE and SM proteins Science 323, 474-477
4. Brunger, A. T. (2005) Structure and function of SNARE and SNARE-interacting proteins Q. Rev. Biophys. 38, 1-47 (Pubitemid 43338671)
5. Fasshauer, D. (2003) Structural insights into the SNARE mechanism Biochim. Biophys. Acta 1641, 87-97 (Pubitemid 36952589)
6. Jahn, R. and Scheller, R. H. (2006) SNAREs: Engines for membrane fusion Nat. Rev. Mol. Cell Biol. 7, 631-643
7. McNew, J. A. (2008) Regulation of SNARE-mediated membrane fusion during exocytosis Chem. Rev. 108, 1669-1686 (Pubitemid 351796404)
8. Sollner, T. H. (2003) Regulated exocytosis and SNARE function (Review) Mol. Membr. Biol. 20, 209-220 (Pubitemid 37046246)
9. Brose, N., Petrenko, A. G., Sudhof, T. C., and Jahn, R. (1992) Synaptotagmin: A calcium sensor on the synaptic vesicle surface Science 256, 1021-1025
10. Chapman, E. R. (2008) How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615-641
11. Fernandez-Chacon, R., Konigstorfer, A., Gerber, S. H., Garcia, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., and Sudhof, T. C. (2001) Synaptotagmin I functions as a calcium regulator of release probability Nature 410, 41-49 (Pubitemid 32225830)
12. 2+-triggered exocytosis Annu. Rev. Biophys. Biomol. Struct. 35, 135-160 (Pubitemid 43877373)
13. Perin, M. S., Fried, V. A., Mignery, G. A., Jahn, R., and Sudhof, T. C. (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C Nature 345, 260-263
14. Perin, M. S., Brose, N., Jahn, R., and Sudhof, T. C. (1991) Domain structure of synaptotagmin (p65) J. Biol. Chem. 266, 623-629 (Pubitemid 21906167)
15. Fernandez, I., Arac, D., Ubach, J., Gerber, S. H., Shin, O., Gao, Y., Anderson, R. G., Sudhof, T. C., and Rizo, J. (2001) Three-dimensional structure of the synaptotagmin 1 C2B-domain: Synaptotagmin 1 as a phospholipid binding machine Neuron 32, 1057-1069 (Pubitemid 34075396)
16. 2+ ions bind to the tip of a C2-domain? EMBO J. 17, 3921-3930 (Pubitemid 28333978)
17. Martens, S. and McMahon, H. T. (2008) Mechanisms of membrane fusion: Disparate players and common principles Nat. Rev. Mol. Cell Biol. 9, 543-556 (Pubitemid 351881838)
18. 2+-binding loop of synaptotagmin with lipid bilayers J. Biol. Chem. 273, 13995-14001 (Pubitemid 28268455)
19. Herrick, D. Z., Sterbling, S., Rasch, K. A., Hinderliter, A., and Cafiso, D. S. (2006) Position of synaptotagmin I at the membrane interface: Cooperative interactions of tandem C2 domains Biochemistry 45, 9668-9674 (Pubitemid 44257414)
20. Rufener, E., Frazier, A. A., Wieser, C. M., Hinderliter, A., and Cafiso, D. S. (2005) Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling Biochemistry 44, 18-28 (Pubitemid 40095703)
21. Kuo, W., Herrick, D. Z., Ellena, J. F., and Cafiso, D. S. (2009) The calcium-dependent and calcium-independent membrane binding of synaptotagmin 1: Two modes of C2B binding J. Mol. Biol. 387, 284-294
22. Bai, J., Tucker, W. C., and Chapman, E. R. (2004) PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane Nat. Struct. Mol. Biol. 11, 36-44 (Pubitemid 38173439)
23. 2+-triggered membrane penetration activity within the C2B domain of synaptotagmin I Proc. Natl. Acad. Sci. U.S.A. 99, 1665-1670 (Pubitemid 34136550)
24. Cafiso, D. S. (2005) Structure and Interactions of C2 Domains at Membrane Surfaces, Wiley-VCH, Weinheim, Germany.
25. Martens, S., Kozlov, M. M., and McMahon, H. T. (2007) How synaptotagmin promotes membrane fusion Science 316, 1205-1208 (Pubitemid 46877485)
26. 2+-dependent stimulation of vesicle fusion by membrane-anchored synaptotagmin 1 Science 328, 760-763
27. 2+- dependent trans interaction with phospholipids Nat. Struct. Mol. Biol. 14, 904-911 (Pubitemid 47525181)
28. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., and Jahn, R. (2001) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis EMBO J. 20, 2202-2213 (Pubitemid 32410590)
29. Ohara-Imaizumi, M., Nishiwaki, C., Kikuta, T., Kumakura, K., Nakamichi, Y., and Nagamatsu, S. (2004) Site of docking and fusion of insulin secretory granules in live MIN6 β cells analyzed by TAT-conjugated anti-syntaxin 1 antibody and total internal reflection fluorescence microscopy J. Biol. Chem. 279, 8403-8408 (Pubitemid 38294733)
30. Wan, C., Kiessling, V., and Tamm, L. K. (2008) Coupling of cholesterol-rich lipid phases in asymmetric bilayers Biochemistry 47, 2190-2198 (Pubitemid 351287145)
31. Wang, T. Y. and Silvius, J. R. (2001) Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane Biophys. J. 81, 2762-2773 (Pubitemid 33020063)
32. Kiessling, V., Crane, J. M., and Tamm, L. K. (2006) Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking Biophys. J. 91, 3313-3326 (Pubitemid 44788265)
33. Frazier, A. A., Roller, C. R., Havelka, J. J., Hinderliter, A., and Cafiso, D. S. (2003) Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling Biochemistry 42, 96-105 (Pubitemid 36083855)
34. Crane, J. M., Kiessling, V., and Tamm, L. K. (2005) Measuring lipid asymmetry in planar supported bilayers by fluorescence interference contrast microscopy Langmuir 21, 1377-1388 (Pubitemid 40275074)
35. Kalb, E., Frey, S., and Tamm, L. K. (1992) Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers Biochim. Biophys. Acta 1103, 307-316
36. Wagner, M. L. and Tamm, L. K. (2000) Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: Silane-polyethyleneglycol-lipid as a cushion and covalent linker Biophys. J. 79, 1400-1414
37. Oreopoulos, J. and Yip, C. M. (2009) Combinatorial microscopy for the study of protein-membrane interactions in supported lipid bilayers: Order parameter measurements by combined polarized TIRFM/AFM J. Struct. Biol. 168, 21-36
38. Kiessling, V., Domanska, M. K., and Tamm, L. K. (2010) Single SNARE-mediated vesicle fusion observed in vitro by polarized TIRFM Biophys. J. 99, 4047-4055
39. Crane, J. M. and Tamm, L. K. (2004) Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes Biophys. J. 86, 2965-2979 (Pubitemid 38552700)
40. Gorter, E. and Grendel, F. (1925) On Bimolecular Layers of Lipoids on the Chromocytes of the Blood J. Exp. Med. 41, 439-443
41. Singer, S. J. and Nicolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes Science 175, 720-731
42. London, E. (2005) How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells Biochim. Biophys. Acta 1746, 203-220 (Pubitemid 41815017)
43. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes Nature 387, 569-572 (Pubitemid 27248754)
44. Lingwood, D. and Simons, K. (2010) Lipid rafts as a membrane-organizing principle Science 327, 46-50
45. Foster, L. J., De Hoog, C. L., and Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc. Natl. Acad. Sci. U.S.A. 100, 5813-5818 (Pubitemid 36576890)
46. Chamberlain, L. H., Burgoyne, R. D., and Gould, G. W. (2001) SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis Proc. Natl. Acad. Sci. U.S.A. 98, 5619-5624 (Pubitemid 32435691)
47. Salaun, C., Gould, G. W., and Chamberlain, L. H. (2005) Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells J. Biol. Chem. 280, 19449-19453 (Pubitemid 41379464)
48. Murray, D. H. and Tamm, L. K. (2009) Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol Biochemistry 48, 4617-4625
49. Bacia, K., Schuette, C. G., Kahya, N., Jahn, R., and Schwille, P. (2004) SNAREs prefer liquid-disordered over "raft" (liquid-ordered) domains when reconstituted into giant unilamellar vesicles J. Biol. Chem. 279, 37951-37955 (Pubitemid 39195510)
50. Kiessling, V., Wan, C., and Tamm, L. K. (2009) Domain coupling in asymmetric lipid bilayers Biochim. Biophys. Acta 1788, 64-71
51. Kiessling, V. and Tamm, L. K. (2003) Measuring distances in supported bilayers by fluorescence interference-contrast microscopy: Polymer supports and SNARE proteins Biophys. J. 84, 408-418 (Pubitemid 36026409)
52. Collins, M. D. and Keller, S. L. (2008) Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers Proc. Natl. Acad. Sci. U.S.A. 105, 124-128
53. Cheng, H. T., Megha, and London, E. (2009) Preparation and properties of asymmetric vesicles that mimic cell membranes: Effect upon lipid raft formation and transmembrane helix orientation J. Biol. Chem. 284, 6079-6092