Syntaxin is efficiently excluded from sphingomyelin-enriched domains in supported lipid bilayers containing cholesterol

Journal of Membrane Biology

Volumn 194, Issue 3, 2003, Pages 153-164

  Saslowsky, D E ^a   Lawrence, J C ^a   Henderson, R M ^a   Edwardson, J M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Atomic force microscopy; Lipid bilayer; Lipid microdomain; Membrane; SNARE; Syntaxin

Indexed keywords

CHOLESTEROL; DETERGENT; LIPOSOME; MICA; MUNC 18; RECOMBINANT PROTEIN; SNARE PROTEIN; SPHINGOMYELIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN; SYNTAXIN IA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; COMPLEX FORMATION; LIPID BILAYER; LIPID VESICLE; NONHUMAN; PROTEIN AGGREGATION; PROTEIN STRUCTURE; RAT; SOLUBILIZATION;

ANIMALS; ANTIGENS, SURFACE; CHOLESTEROL; CHOLIC ACIDS; DETERGENTS; LIPID BILAYERS; LIPOSOMES; MACROMOLECULAR SUBSTANCES; MEMBRANE FUSION; MEMBRANE MICRODOMAINS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; PARTICLE SIZE; PEPTIDE FRAGMENTS; PHOSPHATIDYLCHOLINES; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT FUSION PROTEINS; SPHINGOMYELINS; SYNTAXIN 1;

ANIMALIA; MICA;

EID: 0042932808     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00232-003-2035-7     Document Type: Article

References (38)

1. Ahn, A., Gibbons, D.L., Kielian, M. 2002. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 76:3267-3275
2. Barnstable, C.J., Hofstein, R., Akagawa, K. 1985. A marker of early amacrine cell development in rat retina. Dev. Brain Res. 20:286-290
3. Brown, D.A., London, E. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224
4. Brown, D.A., Rose, J.K. 1992. Sorting of GP1-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544
5. Chamberlain, L.H., Burgoyne, R.D., Gould, G.W. 2002. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. USA 98:5619-5624
6. Dietrich, C., Bagatolli, L.A., Volovyk, Z.N., Thompson, N.L., Levi, M., Jacobson, K., Gratton, E. 2000. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417-1428
7. Edstrom, R.D., Meinke, M.H., Yang, X.R., Yang, R., Elings, V., Evans, D.F. 1990. Direct visualization of phosphorylase-phosphorylase kinase complexes by scanning tunneling and atomic force microscopy. Biophys. J. 58:1437-1448
8. Garcia, E.P., McPherson, P.S., Chilcote, T.J., Takei, K., DeCamilli, P. 1995. rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin. J. Cell Biol. 129:105-120
9. Hodel, A., An, S.J., Hansen, N.J., Lawrence, J., Wäsle, B., Schrader, M., Edwardson, J.M. 2001. Cholesterol-dependent interaction of syncollin with the membrane of the pancreatic zymogen granule. Biochem. J. 356:843-850
10. Hua, Y., Scheller, R.H. 2001. Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. USA 98:8065-8070
11. Jahn, R., Südhof, T.C. 1999. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68:863-911
12. Kalus, I., Hodel, A., Koch, A., Kleene, R., Edwardson, J.M., Schrader, M. 2002. Interaction of syncollin with GP-2, the major membrane protein of pancreatic zymogen granules, and association with lipid microdomains. Biochem. J. 362:433-442
13. Kato, M., Wickner, W. 2001. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. EMBO J. 20:4035-4040
14. Laage, R., Rohde, J., Brosig, B., Langosch, D. 2000. A conserved membrane-spanning amino acid motif drives homomeric and supports heteromeric assembly of presynaptic SNARE proteins. J. Biol. Chem. 275:17481-17487
15. Lafont, F., Verkade, P., Galli, T., Wimmer, C., Louvard, D., Simons, K. 1999. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc. Natl. Acad. Sci. USA 96:3734-3738
16. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., Jahn, R. 2002. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20:2202-2213
17. Lewis, J.L., Dong, M., Earles, C.A., Chapman, E.R. 2001. The transmembrane domain of syntaxin 1A is critical for cytoplasmic domain protein-protein interactions. J. Biol. Chem. 276:15458-15465
18. Lin, R.C., Scheller, R.H. 2000. Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16:19-49
19. Markovic, I., Leikina, E., Zhukovsky, M., Zimmerberg, J., Chernomordik, L.V. 2001. Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J. Cell Biol. 155:833-843
20. Melkonian, K.A., Ostermeyer, A.G., Chen, J.Z., Roth, M.G., Brown, D.A. 1999. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. J. Biol. Chem. 274:3910-3917
21. Milhiet, P.E., Giocondi, M.-C., Le Grimellec, C. 2002. Cholesterol is not critical for the existence of microdomains in kidney brush-border membrane models. J. Biol. Chem. 277:875-878
22. Misura, K.M.S., Scheller, R.H., Weis, W.I. 2000. Three-dimensional structure of the neuonal-Sec1-syntaxin 1a complex. Nature 404:355-362
23. Naim, H.Y., Amarneh, B., Ktistakis, N.T., Roth, M.G. 1992. Effects of altering palmitylation sites on biosynthesis and function of the influenza virus hemagglutinin. J. Virol. 66:7585-7588
24. Neish, C.S., Martin, I.L., Henderson, R.M., Edwardson, J.M. 2002. Direct visualization of ligand-protein interactions using atomic force microscopy. Brit. J. Pharmacol. 135:1943-1950
25. Prydz, K., Simons, K. 2002. Cholesterol depletion reduces apical transport capacity in epithelial Madin-Darby canine kidney cells. Biochem. J. 357:11-15
26. Reviakine, I., Brisson, A. 2000. Formation of supported phospholipid bilayers from unilamellar vesicles investigated by atomic force microscopy. Langmuir 16:1806-1815
27. Röper, K., Corbeil, D., Huttner, W.B. 2000. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nature Cell Biol. 2:582-592
28. Samsonov, A.V., Mihalyov, I., Cohen, F. 2001. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys. J. 81:1486-1500
29. Saslowsky, D.E., Lawrence, J., Ren, X., Brown, D.A., Henderson, R.M., Edwardson, J.M. 2002. Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J. Biol. Chem. 277:26966-26970
30. Schneider, S.W., Lärmer, J., Henderson, R.M., Oberleithner, H. 1998. Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pfluegers Arch. 435:362-367
31. Simons, K., Toomre, D. 2000. Lipid rafts and signal transduction. Nature Rev. Mol. Cell Biol. 1:31-39
32. Skehel, J.J., Wiley, D.C. 1998. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95:871-874
33. Skibbens, J.E., Roth, M.G., Marlin, K.S. 1989. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts J. Cell Biol 108:821-832
34. Sprong, H., van der Sluijs, P., van Meer, G. 2001. How proteins move lipids and lipids move proteins. Nature Rev. Mol. Cell Biol. 2:504-513
35. Sutton, R.B., Fasshauer, D., Jahn, R., Brunger, A.T. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution. Nature 395:347-353
36. Waarts, B.-L., Bittman, R., Wilschut, J. 2002. Sphingolipid- and cholesterol-dependence of alphavirus membrane fusion. J. Biol. Chem. 277:38141-38147
37. Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T.H., Rothman, J.E. 1998. SNAREpins: minimal machinery for membrane fusion. Cell 92:759-772
38. Yang, B., Steegmaier, M., Gonazalez, L.C. Jr., Scheller, R.H. 2000. nSec1 binds to a closed conformation of syntaxin1A. J. Cell Biol. 148:247-252