Cholesterol depletion activates rapid internalization of submicron-sized acetylcholine receptor domains at the cell membrane

References

• Antollini SS, Soto MA, Bonini de Romanelli I, Gutierrez-Merino C, Sotomayor P, Barrantes FJ. Physical state of bulk and protein-associated lipid in nicotinic acetylcholine receptor-rich membrane studied by laurdan generalized polarization and fluorescence energy transfer. Biophys J 1996; 70: 1275–1284
   Google Scholar
• Baenziger JE, Morris ML, Darsaut TE, Ryan SE. Effect of membrane lipid composition on the conformational equilibria of the nicotinic acetylcholine receptor. J Biol Chem 2000; 275: 777–784
   PubMedGoogle Scholar
• Barrantes FJ. Structural basis for lipid modulation of nicotinic acetylcholine receptor function. Brain Res Brain Res Rev 2004; 47: 71–95
   PubMedGoogle Scholar
• Barrantes FJ, Antollini SS, Blanton MP, Prieto M. Topography of nicotinic acetylcholine receptor membrane-embedded domains. J Biol Chem 2000; 275: 37333–37339
   Google Scholar
• Blanton MP, Xie Y, Dangott LJ, Cohen JB. The steroid promegestone is a noncompetitive antagonist of the Torpedo nicotinic acetylcholine receptor that interacts with the lipid-protein interface. Mol Pharmacol 1999; 55: 269–278
   PubMedGoogle Scholar
• Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911–917
   PubMedGoogle Scholar
• Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000; 275: 17221–17224
   PubMed Web of Science ®Google Scholar
• Bruses J, Chauvet N, Rutishauser U. Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J Neurosci 2001; 21: 504–512
   Google Scholar
• Corbin J, Wang HH, Blanton MP. Identifying the cholesterol binding domain in the nicotinic acetylcholine receptor with [125I]azido-cholesterol. Biochim Biophys Acta 1998; 1414: 65–74
   Web of Science ®Google Scholar
• Edidin M. Lipid microdomains in cell surface membranes. Curr Opin Struct Biol 1997; 7: 528–532
   PubMed Web of Science ®Google Scholar
• Fukasawa M, Nishijima M, Itabe H, Takano T, Hanada K. Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-beta-cyclodextrin. J Biol Chem 2000; 275: 34028–34034
   Google Scholar
• Gimpl G, Klein U, Reiländer H, Fahrenholz F. Expression of the human oxytocin receptor in baculovirus-infected insect cells: high-affinity binding is induced by a cholesterol-cyclodextrin complex. Biochemistry 1996; 34: 13794–13801
   Google Scholar
• Hancock, JF. 2006. Lipid rafts: contentious only from simplistic standpoints. Nature Rev Molec Cell Biol, 7:456–462.
   PubMed Web of Science ®Google Scholar
• Jacobson K, Dietrich C. Looking at lipid rafts?. Trends Cell Biol 1999; 9(3)87–91
   PubMed Web of Science ®Google Scholar
• Jones OT, McNamee MG. Annular and nonannular binding sites for cholesterol associated with the nicotinic aceytlcholine receptor. Biochemistry 1988; 27: 2364–2374
   PubMed Web of Science ®Google Scholar
• Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 2005; 168: 465–476
   PubMed Web of Science ®Google Scholar
• Kwik J, Boyle S, Fooksman D, Margolis L, Sheetz MP, Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 2003; 100: 13964–13969
   PubMed Web of Science ®Google Scholar
• Le PU, Guay G, Altschuler Y, Nabi IR. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J Biol Chem 2002; 277: 3371–3379
   PubMedGoogle Scholar
• Marchand S, Devillers-Thiery A, Pons S, Changeux JP, Cartaud J. Rapsyn escorts the nicotinic acetylcholine receptor along the exocytic pathway via association with lipid rafts. J Neurosci 2002; 22: 8891–8901
   Google Scholar
• Marcheselli V, Daniotti JL, Vidal AC, Maccioni H, Marsh D, Barrantes FJ. Gangliosides in acetylcholine receptor-rich membranes from Torpedo marmorata and Discopyge tschudii. Neurochem Res 1993; 18: 599–603
   Google Scholar
• Maxfield FR. Plasma membrane microdomains. Curr Opin Cell Biol 2002; 14: 483–487
   PubMedGoogle Scholar
• Parasassi T, De Stasio G, d'Ubaldo A, Gratton E. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys J 1990; 57: 1179–1186
   PubMed Web of Science ®Google Scholar
• Phillips DW, Vladeta D, Han H, Noakes PG. Rapsyn and agrin slow the metabolic degradation of the acetylcholine receptor. Mol Cel Neurosci 1997; 10: 16–26
   Google Scholar
• Pichler H, Riezman H. Where sterols are required for endocytosis. Biochim Biophys Acta 2004; 1666: 51–61
   Google Scholar
• Roccamo AM, Pediconi MF, Aztiria E, Zanello L, Wolstenholme A, Barrantes FJ. Cells defective in sphingolipids biosynthesis express low amounts of muscle nicotinic acetylcholine receptor. Eur J Neurosci 1999; 11: 1615–1623
   Google Scholar
• Sanes JR, Lichtman JW. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2001; 2: 791–805
   PubMed Web of Science ®Google Scholar
• Santiago J, Guzman GR, Rojas LV, Marti R, Asmar-Rovira GA, Santana LF, McNamee MG, Lasalde-Dominicci JA. Probing the effects of membrane cholesterol in the Torpedo californica acetylcholine receptor and the novel lipid-exposed mutation (C418W in Xenopus oocytes). J Biol Chem 2001; 276: 46523–46532
   PubMedGoogle Scholar
• Sieber JJ, Willig KI, Heintzmann R, Hell SW, Lang T. The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane. Biophys J 2006; 90: 2843–2851
   PubMedGoogle Scholar
• Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA 1999; 96: 6775–6780
   PubMed Web of Science ®Google Scholar
• Sunshine C, McNamee MG. Lipid modulation of nicotinic acetylcholine receptor function: The role of membrane lipid composition and fluidity. Biochim Biophys Acta 1994; 1191: 59–64
   PubMed Web of Science ®Google Scholar
• Turner MS, Sens P, Socci ND. Nonequilibrium raft-like domains under continuous recycling. Phys Rev Lett 2005; 95: 168301
   Google Scholar
• Vrljic M, Nishimura SY, Moerner WE, McConnell HM. Cholesterol depletion suppresses the translational diffusion of class II major histocompatibility complex proteins in the plasma membrane. Biophys J 2005; 88: 334–347
   Google Scholar
• Warnock DE, Roberts C, Lutz MS, Blackburn WA, Young WW, Jr, Baenziger JU. Determination of plasma membrane lipid mass and composition in cultured Chinese hamster ovary cells using high gradient magnetic affinity chromatography. J Biol Chem 1993; 268: 10145–10153
   PubMed Web of Science ®Google Scholar
• Zanello LP, Aztiria E, Antollini S, Barrantes FJ. Nicotinic acetylcholine receptor channels are influenced by the physical state of their membrane environment. Biophys J 1996; 70: 2155–2164
   Google Scholar
• Zhu D, Xiong WC, Mei L. Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J Neurosci 2006; 26: 4841–4851
   PubMed Web of Science ®Google Scholar