Synaptic proteins associate with a sub-set of lipid rafts when isolated from nerve endings at physiological temperature

Biochemical and Biophysical Research Communications

Volumn 348, Issue 4, 2006, Pages 1334-1342

  Gil, Carles ^a   Cubí, Roger ^a   Blasi, Juan ^b   Aguilera, José ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

cholesterol; Exocytosis; Lipid rafts; Membrane microdomains; SNARE proteins; Synaptic vesicles

Indexed keywords

LUBROL; METHYL BETA CYCLODEXTRIN; POLYOXYETHYLENE OLEYL ETHER; SYNTAXIN 1;

ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CONTROLLED STUDY; DEPOLARIZATION; EXOCYTOSIS; LIPID RAFT; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; RAT; SOLUBILIZATION; SUCROSE GRADIENT;

EID: 33748618706     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.07.201     Document Type: Article

References (39)

1. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
2. Brown D.A., and Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 69 (1992) 533-544
3. Pike L.J., Han X., and Gross R.W. Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids. J. Biol. Chem. 280 (2005) 26796-26804
4. Drobnik W., Borsukova H., Böttcher A., Pfeiffer A., Liebisch G., Schütz G.J., Schindler H., and Schmitz G. Apo AI/ABCA1-dependent and HDL3-mediated lipid efflux from compositionally distinct cholesterol-based microdomains. Traffic 3 (2002) 268-278
5. Madore N., Smith K.L., Graham C.H., Jen A., Bradi K., Hall L., and Morris S. Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18 (1999) 6917-6926
6. Röper K., Corbeil D., and Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell. Biol. 2 (2000) 582-592
7. Drevot P., Langlet C., Guo X., Bernard A., Colard O., Chauvin J.-P., Lasserre R., and He H.T. TCR signal initiation machinery is preassembled and activated in a subset of membrane rafts. EMBO J. 21 (2003) 1899-1908
8. Vinson M., Rausch O., Maycox P.R., Prinjha R.K., Chapman D., Morrow R., Harper A.J., Dingwall C., Walsh F.S., Burbidge S.A., and Riddell D.R. Lipid rafts mediate the interaction between myelin-associated glycoprotein (MAG) on myelin and MAG-receptors on neurons. Mol. Cell. Neuriosci. 22 (2003) 344-352
9. Brown D.A., and London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14 (1998) 111-136
10. Lang R., Jahn T., and Südhof T.C. Membrane fusion. Cell 112 (2003) 519-533
11. Dennison S.M., Bowen M.E., Brunger A.T., and Lentz B.R. Neuronal SNAREs do not trigger fusion between synthetic membranes but do promote PEG-mediated membrane fusion. Biophys. J. 90 (2005) 1661-1675
12. Mochida S. Protein-protein interactions in neurotransmitter release. Neurosci. Res. 36 (2000) 175-182
13. Chamberlain L.H., Burgoyne R.D., and Gould G.W. 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
14. Lang T., Bruns D., Wenzel D., Riedel D., Holroyd P., Thiele C., and Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20 (2001) 2202-2213
15. Gil C., Soler-Jover A., Blasi J., and Aguilera J. Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes. Biochem. Biophys. Res. Commun. 329 (2005) 117-124
16. Mauch D.H., Nägler K., Schumacher S., Göritz C., Müller E.C., Otto A., and Pfrieger F.W. CNS synaptogenesis promoted by glia-derived cholesterol. Science 294 (2001) 1354-1357
17. Pfrieger F.W. Role of cholesterol in synapse formation and function. Biochim. Biophys. Acta 1610 (2003) 271-280
18. Schmitz F., Augustin I., and Brose N. The synaptic vesicle priming protein munc13-1 is absent from tonically active ribbon synapses of the rat retina. Brain Res. 895 (2001) 258-263
19. 2+-triggered membrane fusion. J. Cell Sci. 118 (2005) 4833-4848
20. 2+-releasing channel. J. Cell Biol. 162 (2003) 211-222
21. Kozlovsky Y., Chernomordik L.V., and Kozlov M.M. Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragm. Biophys. J. 83 (2002) 2634-2651
22. Chamberlain L.H., and Gould G.W. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J. Biol. Chem. 277 (2002) 49750-49754
23. Hansen G.H., Immerdal L., Thorsen E., Niels-Christiansen L., Nystrøm B.T., Demant E.J.F., and Danielsen E.M. Lipid rafts exist as stable cholesterol-independent microdomains in the brush border membrane of enterocytes. J. Biol. Chem. 276 (2001) 32338-32344
24. Schroeder R.J., Ahmed S.N., Zhu Y., London E., and Brown D.A. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273 (1998) 1150-1157
25. 2+-triggered membrane fusion. J. Cell Sci. (2006) 10.1242/jcs.03007
26. Itoh K., Sakakibara M., Yamasaki S., Takeuchi A., Arase H., Miyazaki M., Nakajima N., Okada M., and Saito T. Cutting edge: negative regulation of immune synapse formation by anchoring lipid raft to cytoskeleton through Cbp-EBP50-ERM assembly. J. Immunol. 168 (2002) 541-544
27. Gomez-Mouton C., Abad J.L., Mira E., Lacalle R.A., Gallardo E., Jimenez- Baranda S., Illa I., Bernad A., Manes S., and Martinez A.C. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl. Acad. Sci. USA 98 (2001) 9642-9647
28. 2+-triggered exocytosis. Biochem. J. 366 (2002) 1-13
29. Marquèze B., Boudier J.A., Mizuta M., Inagaki N., Seino S., and Seagar M. Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat. J. Neurosci. 15 (1995) 4906-4917
30. Osborne S.L., Herreros J., Bastiaens P.I.H., and Schiavo G. Calcium dependent oligomerization of synaptotagmins I and II. J. Biol. Chem. 274 (1999) 59-66
31. Nagy G., Kim J.H., Pang Z.P., Matti U., Rettig J., Südhof T.C., and Sørensen J.B. Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26 (2006) 632-643
32. Rickman C., Archer D.A., Meunier F.A., Craxton M., Fukuda M., Burgoyne R.D., and Davletov B. Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate. J. Biol. Chem. 279 (2004) 12574-12579
33. 2+-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat. Struct. Mol. Biol. 13 (2006) 209-217
34. Sassa T., Harada S., Ogawa H., Rand J.B., Maruyama I.N., and Hosono R. Regulation of the UNC-18-caenorhabditis elegans syntaxin complex by UNC-13. J. Neurosci. 19 (1999) 4772-4777
35. Pevsner J., Hsu S., and Scheller R.H. n-sec1: a neural-specific syntaxin-binding protein. Proc. Natl. Acad. Sci. USA 91 (1994) 1445-1449
36. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Südhof T.C., and Rizo J. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18 (1999) 4372-4382
37. Ciufo L.F., Barclay J.W., Burgoyne R.D., and Morgan A. Munc18-1 regulates early and late stages of exocytosis via syntaxin-independent protein interactions. Mol. Biol. Cell 16 (2005) 470-482
38. Barclay J.W., Craig T.J., Fisher R.J., Ciufo L.F., Evans G.J.O., Morgan A., and Burgoyne R.D. Phosphorylation of munc18 by protein kinase C regulates the kinetics of exocytosis. J. Biol. Chem. 278 (2003) 10538-10545
39. Craig T.J., Evans G.J.O., and Morgan A. Physiological regulation of munc18/nSec1 phosphorylation on serine-313. J. Neurochem. 86 (2003) 1450-1457