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Abstract:

Nicotinic acetylcholine receptor (AChR) function and distribution are quite sensitive to cholesterol (Chol) levels in the plasma membrane (reviewed by Barrantes in J Neurochem 103 (suppl 1):72-80, 2007). Here we combined confocal fluorescence recovery after photobleaching (FRAP) and confocal fluorescence correlation spectroscopy (FCS) to examine the mobility of the AChR and its dependence on Chol content at the cell surface of a mammalian cell line. Plasma membrane AChR exhibited limited mobility and only ~55% of the fluorescence was recovered within 10 min after photobleaching. Depletion of membrane Chol by methyl-β-cyclodextrin strongly affected the mobility of the AChR at the plasma membrane; the fraction of mobile AChR fell from 55 to 20% in Chol-depleted cells, whereas Chol enrichment by methyl-β-cyclodextrin-Chol treatment did not reduce receptor mobility at the cell surface. Actin depolymerization caused by latrunculin A partially restored receptor mobility in Chol-depleted cells. In agreement with the FRAP data, scanning FCS experiments showed that the diffusion coefficient of the AChR was about 30% lower upon Chol depletion. Taken together, these results suggest that membrane Chol modulates AChR mobility at the plasma membrane through a Chol-dependent mechanism sensitive to cortical actin. © 2009 European Biophysical Societies' Association.

Registro:

Documento: Artículo
Título:Cholesterol modulation of nicotinic acetylcholine receptor surface mobility
Autor:Baier, C.J.; Gallegos, C.E.; Levi, V.; Barrantes, F.J.
Filiación:UNESCO, Department of Biophysics and Molecular Neurobiology, Instituto de Investigaciones Bioquímicas de Bahía Blanca, C.C. 857, B8000FWB Bahía Blanca, Argentina
Laboratorio de Electrónica Cuántica, Departamento de Física, Universidad de Buenos Aires, Buenos Aires 1428, Argentina
Palabras clave:Acetylcholine receptor; Cholesterol; Lateral mobility; Lipid microdomains; Membrane; Nicotinic; Actins; Animals; beta-Cyclodextrins; Bicyclo Compounds, Heterocyclic; Cell Membrane; CHO Cells; Cholesterol; Cricetinae; Cricetulus; Diffusion; Fluorescence Recovery After Photobleaching; Microscopy, Confocal; Motion; Protein Multimerization; Receptors, Nicotinic; Spectrometry, Fluorescence; Thiazolidines; Mammalia
Año:2010
Volumen:39
Número:2
Página de inicio:213
Página de fin:227
DOI: http://dx.doi.org/10.1007/s00249-009-0521-2
Título revista:European Biophysics Journal
Título revista abreviado:Eur. Biophys. J.
ISSN:01757571
CODEN:EBJOE
CAS:Actins; Bicyclo Compounds, Heterocyclic; Cholesterol, 57-88-5; Receptors, Nicotinic; Thiazolidines; beta-Cyclodextrins; latrunculin A, 76343-93-6; methyl-beta-cyclodextrin
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01757571_v39_n2_p213_Baier

Referencias:

  • Adkins, E.M., Samuvel, D.J., Fog, J.U., Eriksen, J., Jayanthi, L.D., Vaegter, C.B., Ramamoorthy, S., Gether, U., Membrane mobility and microdomain association of the dopamine transporter studied with fluorescence correlation spectroscopy and fluorescence recovery after photobleaching (2007) Biochemistry, 46 (37), pp. 10484-10497. , DOI 10.1021/bi700429z
  • Axelrod, D., Crosslinkage and visualization of acetylcholine receptors on myotubes with biotinylated α-bungarotoxin and fluorescent avidin (1980) Proceedings of the National Academy of Sciences of the United States of America, 77, pp. 4823-4827. , DOI 10.1073/pnas.77.8.4823
  • Axelrod, D., Ravdin, P., Koppel, D.E., Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers (1976) Proceedings of the National Academy of Sciences of the United States of America, 73 (12), pp. 4594-4598. , DOI 10.1073/pnas.73.12.4594
  • Barrantes, F.J., Endogenous chemical receptors: Some physical aspects (1979) Annu Rev Biophys Bioeng, 8, pp. 287-321. , 10.1146/annurev.bb.08.060179.001443 1:CAS:528:DyaE1MXksFWitLs%3D 224807
  • Barrantes, F.J., Oligomeric forms of the membrane-bound acetylcholine receptor disclosed upon extraction of the Mr 43,000 nonreceptor peptide (1982) J Cell Biol, 92, pp. 60-68. , 10.1083/jcb.92.1.60 1:CAS:528:DyaL38XpvVarug%3D%3D 6173390
  • Barrantes, F.J., The lipid environment of the nicotinic acetylcholine receptor in native and reconstituted membranes (1989) Crit Rev Biochem Mol Biol, 24, pp. 437-478. , 10.3109/10409238909086961 1:CAS:528:DyaK3cXis1Gj 2676352
  • Barrantes, F.J., Structural-functional correlates of the nicotinic acetylcholine receptor and its lipid microenvironment (1993) FASEB J, 7, pp. 1460-1467. , 1:CAS:528:DyaK2cXks1Slsg%3D%3D 8262330
  • Barrantes, F.J., Modulation of nicotinic acetylcholine receptor function through the outer and middle rings of transmembrane domains (2003) Curr Opin Drug Discov Dev, 6, pp. 620-632. , 1:CAS:528:DC%2BD3sXotFOnsL0%3D
  • Barrantes, F.J., Structural basis for lipid modulation of nicotinic acetylcholine receptor function (2004) Brain Research Reviews, 47 (1-3), pp. 71-95. , DOI 10.1016/j.brainresrev.2004.06.008, PII S0165017304000815, Chemical and Electrical Synapses
  • Barrantes, F.J., Cholesterol effects on nicotinic acetylcholine receptor (2007) J Neurochem, 103 (SUPPL 1), pp. 72-80. , 10.1111/j.1471-4159.2007.04719.x 1:CAS:528:DC%2BD2sXhtl2jur3E 17986142
  • Bates, I.R., Wiseman, P.W., Hanrahan, J.W., Investigating membrane protein dynamics in living cells (2006) Biochemistry and Cell Biology, 84 (6), pp. 825-831. , DOI 10.1139/O06-189
  • Bloch, R.J., Velez, M., Krikorian, J.G., Axelrod, D., Microfilaments and actin-associated proteins at sites of membrane-substrate attachment within acetylcholine receptor clusters (1989) Experimental Cell Research, 182 (2), pp. 583-596. , DOI 10.1016/0014-4827(89)90261-9
  • Borroni, V., Baier, C.J., Lang, T., Bonini, I., White, M.M., Garbus, I., Barrantes, F.J., Cholesterol depletion activates rapid internalization of submicron-sized acetylcholine receptor domains at the cell membrane (2007) Molecular Membrane Biology, 24 (1), pp. 1-15. , DOI 10.1080/09687860600903387, PII 770514670
  • Bruses, J.L., 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 (2001) J Neurosci, 21, pp. 504-512. , 1:CAS:528:DC%2BD3MXnslCmsw%3D%3D 11160430
  • Campagna, J.A., Fallon, J., Lipid rafts are involved in C95 (4,8) agrin fragment-induced acetylcholine receptor clustering (2006) Neuroscience, 138 (1), pp. 123-132. , DOI 10.1016/j.neuroscience.2005.11.019, PII S0306452205012923
  • Chen, Y., Lagerholm, B.C., Yang, B., Jacobson, K., Methods to measure the lateral diffusion of membrane lipids and proteins (2006) Methods, 39 (2), pp. 147-153. , DOI 10.1016/j.ymeth.2006.05.008, PII S1046202306000788
  • Christian, A.E., Haynes, M.P., Phillips, M.C., Rothblat, G.H., Use of cyclodextrins for manipulating cellular cholesterol content (1997) J Lipid Res, 38, pp. 2264-2272. , 1:CAS:528:DyaK2sXnsFWrtr4%3D 9392424
  • Corbin, J., Wang, H.H., Blanton, M.P., Identifying the cholesterol binding domain in the nicotinic acetylcholine receptor with [125I]azido-cholesterol (1998) Biochimica et Biophysica Acta - Biomembranes, 1414 (1-2), pp. 65-74. , DOI 10.1016/S0005-2736(98)00153-9, PII S0005273698001539
  • Coue, M., Brenner, S.L., Spector, I., Korn, E.D., Inhibition of actin polymerization by latrunculin A (1987) FEBS Letters, 213 (2), pp. 316-318. , DOI 10.1016/0014-5793(87)81513-2
  • Crane, J.M., Verkman, A.S., Long-range nonanomalous diffusion of quantum dot-labeled aquaporin-1 water channels in the cell plasma membrane (2008) Biophys J, 94, pp. 702-713. , 10.1529/biophysj.107.115121 1:CAS:528:DC%2BD1cXnsVOksQ%3D%3D 17890385
  • Criado, M., Eibl, H., Barrantes, F.J., Effects of lipids on acetylcholine receptor. Essential need of cholesterol for maintenance of agonist-induced state transitions in lipid vesicles (1982) Biochemistry, 21 (15), pp. 3622-3629. , DOI 10.1021/bi00258a015
  • Criado, M., Vaz, W.L., Barrantes, F.J., Jovin, T.M., Translational diffusion of acetylcholine receptor (monomeric and dimeric forms) of Torpedo marmorata reconstituted into phospholipid bilayers studied by fluorescence recovery after photobleaching (1982) Biochemistry, 21, pp. 5750-5755. , 10.1021/bi00266a004 1:CAS:528:DyaL38XlslOgs7c%3D 6897514
  • Dai, Z., Luo, X., Xie, H., Peng, H.B., The actin-driven movement and formation of acetylcholine receptor clusters (2000) Journal of Cell Biology, 150 (6), pp. 1321-1334. , DOI 10.1083/jcb.150.6.1321
  • Edidin, M., Fluorescence photobleaching and recovery, FPR, in the analysis of membrane structure and dynamics (1994) Mobility and Proximity in Biological Membranes, pp. 109-135. , Damjanovich S, Edidin M, Szollosi J, Tron L (eds) CRC Press, Boca Raton
  • Edidin, M., Lipids on the frontier: A century of cell-membrane bilayers (2003) Nature Reviews Molecular Cell Biology, 4 (5), pp. 414-418. , DOI 10.1038/nrm1102
  • Ellenberg, J., Siggia, E.D., Moreira, J.E., Smith, C.L., Presley, J.F., Worman, H.J., Lippincott-Schwartz, J., Nuclear membrane dynamics and reassembly in living cells: Targeting of an inner nuclear membrane protein in interphase and mitosis (1997) Journal of Cell Biology, 138 (6), pp. 1193-1206. , DOI 10.1083/jcb.138.6.1193
  • Guo, L., Har, J.Y., Sankaran, J., Hong, Y., Kannan, B., Wohland, T., Molecular diffusion measurement in lipid bilayers over wide concentration ranges: A comparative study (2008) Chemphyschem, 9, pp. 721-728. , 10.1002/cphc.200700611 1:CAS:528:DC%2BD1cXltFKms7g%3D 18338419
  • Hao, M., Mukherjee, S., Maxfield, F.R., Cholesterol depletion induces large scale domain segregation in living cell membranes (2001) Proceedings of the National Academy of Sciences of the United States of America, 98 (23), pp. 13072-13077. , DOI 10.1073/pnas.231377398
  • Hoch, W., Formation of the neuromuscular junction. Agrin and its unusual receptors (1999) European Journal of Biochemistry, 265 (1), pp. 1-10. , DOI 10.1046/j.1432-1327.1999.00765.x
  • Ishitsuka, R., Sato, S.B., Kobayashi, T., Imaging lipid rafts (2005) Journal of Biochemistry, 137 (3), pp. 249-254. , DOI 10.1093/jb/mvi041
  • Jacobson, K., Mouritsen, O.G., Anderson, R.G.W., Lipid rafts: At a crossroad between cell biology and physics (2007) Nature Cell Biology, 9 (1), pp. 7-14. , DOI 10.1038/ncb0107-7, PII NCB0107-7
  • Johnson, M.E., Berk, D.A., Blankschtein, D., Golan, D.E., Jain, R.K., Langer, R.S., Lateral diffusion of small compounds in human stratum corneum and model lipid bilayer systems (1996) Biophys J, 71, pp. 2656-2668. , 10.1016/S0006-3495(96)79457-2 1:CAS:528:DyaK28XmslGgt7Y%3D 8913603
  • Kellner, R.R., Baier, C.J., Willig, K.I., Hell, S.W., Barrantes, F.J., Nanoscale organization of nicotinic acetylcholine receptors revealed by stimulated emission depletion microscopy (2007) Neuroscience, 144 (1), pp. 135-143. , DOI 10.1016/j.neuroscience.2006.08.071, PII S0306452206011675
  • Kenworthy, A.K., Nichols, B.J., Remmert, C.L., Hendrix, G.M., Kumar, M., Zimmerberg, J., Lippincott-Schwartz, J., Dynamics of putative raft-associated proteins at the cell surface (2004) Journal of Cell Biology, 165 (5), pp. 735-746. , DOI 10.1083/jcb.200312170
  • Kojro, E., Gimpl, G., Lammich, S., Marz, W., Fahrenholz, F., Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM 10 (2001) Proceedings of the National Academy of Sciences of the United States of America, 98 (10), pp. 5815-5820. , DOI 10.1073/pnas.081612998
  • Kumari, S., Borroni, V., Chaudhry, A., Chanda, B., Massol, R., Mayor, S., Barrantes, F.J., Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynamin-independent endocytic pathway (2008) Journal of Cell Biology, 181 (7), pp. 1179-1193. , http://www.jcb.org/cgi/reprint/181/7/1179, DOI 10.1083/jcb.200709086
  • Kummer, T.T., Misgeld, T., Sanes, J.R., Assembly of the postsynaptic membrane at the neuromuscular junction: Paradigm lost (2006) Current Opinion in Neurobiology, 16 (1), pp. 74-82. , DOI 10.1016/j.conb.2005.12.003, PII S0959438805001856, Development
  • Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R.S., Fujiwara, T., Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules (2005) Annual Review of Biophysics and Biomolecular Structure, 34, pp. 351-378. , DOI 10.1146/annurev.biophys.34.040204.144637
  • Kwik, J., Boyle, S., Fooksman, D., Margolis, L., Sheetz, M.P., Edidin, M., Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin (2003) Proceedings of the National Academy of Sciences of the United States of America, 100 (SUPPL. 2), pp. 13964-13969. , DOI 10.1073/pnas.2336102100
  • Ladha, S., MacKie, A.R., Clark, D.C., Cheek cell membrane fluidity measured by fluorescence recovery after photobleaching and steady-state fluorescence anisotropy (1994) J Membr Biol, 142, pp. 223-228. , 1:CAS:528:DyaK2MXit1Gru7s%3D 7884814
  • Leibel, W.S., Firestone, L.L., Legler, D.C., Two pools of cholesterol in acetylcholine receptor-rich membranes from Torpedo (1987) Biochimica et Biophysica Acta - Biomembranes, 897 (2), pp. 249-260. , DOI 10.1016/0005-2736(87)90421-4
  • Lenne, P.-F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.-J., Rigneault, H., Marguet, D., Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork (2006) EMBO Journal, 25 (14), pp. 3245-3256. , DOI 10.1038/sj.emboj.7601214, PII 7601214
  • Lillemeier, B.F., Pfeiffer, J.R., Surviladze, Z., Wilson, B.S., Davis, M.M., Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton (2006) Proceedings of the National Academy of Sciences of the United States of America, 103 (50), pp. 18992-18997. , http://www.pnas.org/cgi/reprint/103/50/18992, DOI 10.1073/pnas.0609009103
  • Marchand, S., Devillers-Thiery, A., Pons, S., Changeux, J.P., Cartaud, J., Rapsyn escorts the nicotinic acetylcholine receptor along the exocytic pathway via association with lipid rafts (2002) J Neurosci, 22, pp. 8891-8901. , 1:CAS:528:DC%2BD38XosV2ju7o%3D 12388596
  • Marsh, D., Barrantes, F.J., Immobilized lipid in acetylcholine receptor-rich membranes from Torpedo marmorata (1978) Proc Natl Acad Sci USA, 75, pp. 4329-4333. , 10.1073/pnas.75.9.4329 1:CAS:528:DyaE1MXitVCl 212745
  • Maxfield, F.R., Plasma membrane microdomains (2002) Current Opinion in Cell Biology, 14 (4), pp. 483-487. , DOI 10.1016/S0955-0674(02)00351-4
  • Muller, J.D., Chen, Y., Gratton, E., Fluorescence correlation spectroscopy (2003) Methods in Enzymology, 361, pp. 69-92. , DOI 10.1016/S0076-6879(03)61006-2
  • Narayanaswami, V., McNamee, M.G., Protein-lipid interactions and Torpedo californica nicotinic acetylcholine receptor function. 2. Membrane fluidity and ligand-mediated alteration in the accessibility of γ subunit cysteine residues to cholesterol (1993) Biochemistry, 32 (46), pp. 12420-12427. , DOI 10.1021/bi00097a021
  • Nehls, S., Snapp, E.L., Cole, N.B., Zaal, K.J.M., Kenworthy, A.K., Roberts, T.H., Ellenberg, J., Lippincott-Schwartz, J., Dynamics and retention of misfolded proteins in native ER membranes (2000) Nature Cell Biology, 2 (5), pp. 288-295. , DOI 10.1038/35010558
  • Niggli, V., Structural properties of lipid-binding sites in cytoskeletal proteins (2001) Trends in Biochemical Sciences, 26 (10), pp. 604-611. , DOI 10.1016/S0968-0004(01)01927-2, PII S0968000401019272
  • Nishimura, S.Y., Vrljic, M., Klein, L.O., McConnell, H.M., Moerner, W.E., Cholesterol depletion induces solid-like regions in the plasma membrane (2006) Biophys J, 90, pp. 927-938. , 10.1529/biophysj.105.070524 1:CAS:528:DC%2BD28XhtFGhs7k%3D 16272447
  • Niv, H., Gutman, O., Kloog, Y., Henis, Y.I., Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells (2002) Journal of Cell Biology, 157 (5), pp. 865-872. , DOI 10.1083/jcb.200202009
  • O'Connell, K.M.S., Tamkun, M.M., Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains (2005) Journal of Cell Science, 118 (10), pp. 2155-2166. , DOI 10.1242/jcs.02348
  • Oliferenko, S., Paiha, K., Harder, T., Gerke, V., Schwarzler, C., Schwarz, H., Beug, H., Huber, L.A., Analysis of CD44-containing lipid rafts: Recruitment of annexin II and stabilization by the actin cytoskeleton (1999) Journal of Cell Biology, 146 (4), pp. 843-854. , DOI 10.1083/jcb.146.4.843
  • Orr, G., Hu, D., Ozcelik, S., Opresko, L.K., Wiley, H.S., Colson, S.D., Cholesterol dictates the freedom of EGF receptors and HER2 in the plane of the membrane (2005) Biophysical Journal, 89 (2), pp. 1362-1373. , DOI 10.1529/biophysj.104.056192
  • Pediconi, M.F., Gallegos, C.E., De Los Santos, E.B., Barrantes, F.J., Metabolic cholesterol depletion hinders cell-surface trafficking of the nicotinic acetylcholine receptor (2004) Neuroscience, 128 (2), pp. 239-249. , DOI 10.1016/j.neuroscience.2004.06.007, PII S0306452204004750
  • Pucadyil, T.J., Chattopadhyay, A., Effect of cholesterol on lateral diffusion of fluorescent lipid probes in native hippocampal membranes (2006) Chemistry and Physics of Lipids, 143 (1-2), pp. 11-21. , DOI 10.1016/j.chemphyslip.2006.04.003, PII S0009308406000867
  • Pucadyil, T.J., Mukherjee, S., Chattopadhyay, A., Organization and dynamics of NBD-labeled lipids in membranes analyzed by fluorescence recovery after photobleaching (2007) Journal of Physical Chemistry B, 111 (8), pp. 1975-1983. , DOI 10.1021/jp066092h
  • Pumplin, D.W., Acetylcholine receptor clusters of rat myotubes have at least three domains with distinctive cytoskeletal and membranous components (1989) J Cell Biol, 109, pp. 739-753. , 10.1083/jcb.109.2.739 1:STN:280:DyaL1MzktVKmtw%3D%3D 2760110
  • Rao, M., Mayor, S., Use of Forster's resonance energy transfer microscopy to study lipid rafts (2005) Biochimica et Biophysica Acta - Molecular Cell Research, 1746 (3), pp. 221-233. , DOI 10.1016/j.bbamcr.2005.08.002, PII S0167488905001667, Lipid Refts: From Model Membranes to Cells
  • Roccamo, A.M., Pediconi, M.F., Aztiria, E., Zanello, L., Wolstenholme, A., Barrantes, F.J., Cells defective in sphingolipids biosynthesis express low amounts of muscle nicotinic acetylcholine receptor (1999) European Journal of Neuroscience, 11 (5), pp. 1615-1623. , DOI 10.1046/j.1460-9568.1999.00574.x
  • Ruan, Q., Cheng, M.A., Levi, M., Gratton, E., Mantulin, W.W., Spatial-temporal studies of membrane dynamics: Scanning fluorescence correlation spectroscopy (SFCS) (2004) Biophysical Journal, 87 (2), pp. 1260-1267. , DOI 10.1529/biophysj.103.036483
  • Sato, S.B., Ishii, K., Makino, A., Iwabuchi, K., Yamaji-Hasegawa, A., Senoh, Y., Nagaoka, I., Kobayashi, T., Distribution and transport of cholesterol-rich membrane domains monitored by a membrane-impermeant fluorescent polyethylene glycol-derivatizied cholesterol (2004) Journal of Biological Chemistry, 279 (22), pp. 23790-23796. , DOI 10.1074/jbc.M313568200
  • Schootemeijer, A., Van Beekhuizen, A.E., Gorter, G., Tertoolen, L.G., De Laat, S.W., Akkerman, J.W., Rapid alterations in lateral mobility of lipids in the plasma membrane of activated human megakaryocytes (1994) Eur J Biochem, 221, pp. 353-362. , 10.1111/j.1432-1033.1994.tb18747.x 1:CAS:528:DyaK2cXis1Klt70%3D 8168523
  • Shvartsman, D.E., Kotler, M., Tall, R.D., Roth, M.G., Henis, Y.I., Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts (2003) Journal of Cell Biology, 163 (4), pp. 879-888. , DOI 10.1083/jcb.200308142
  • Sieber, J.J., Willig, K.I., Kutzner, C., Gerding-Reimers, C., Harke, B., Donnert, G., Rammner, B., Lang, T., Anatomy and dynamics of a supramolecular membrane protein cluster (2007) Science, 317 (5841), pp. 1072-1076. , DOI 10.1126/science.1141727
  • Simons, K., Ikonen, E., Functional rafts in cell membranes (1997) Nature, 387 (6633), pp. 569-572. , DOI 10.1038/42408
  • Simons, K., Van Meer, G., Lipid sorting in epithelial cells (1988) Biochemistry, 27 (17), pp. 6197-6202. , DOI 10.1021/bi00417a001
  • Spector, I., Shochet, N.R., Blasberger, D., Kashman, Y., Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D (1989) Cell Motil Cytoskeleton, 13, pp. 127-144. , 10.1002/cm.970130302 1:CAS:528:DyaL1MXlslWktrk%3D 2776221
  • Stetzkowski-Marden, F., Gaus, K., Recouvreur, M., Cartaud, A., Cartaud, J., Agrin elicits membrane lipid condensation at sites of acetylcholine receptor clusters in C2C12 myotubes (2006) Journal of Lipid Research, 47 (10), pp. 2121-2133. , http://www.jlr.org/cgi/reprint/47/10/2121, DOI 10.1194/jlr.M600182-JLR200
  • Stya, M., Axelrod, D., Mobility and detergent extractability of acetylcholine receptors on cultured rat myotubes: A correlation (1983) J Cell Biol, 97, pp. 48-51. , 10.1083/jcb.97.1.48 1:CAS:528:DyaL3sXks1Gjsr8%3D 6863395
  • Stya, M., Axelrod, D., Mobility of extrajunctional acetylcholine receptors on denervated adult muscle fibers (1984) J Neurosci, 4, pp. 70-74. , 1:CAS:528:DyaL2cXpslejtQ%3D%3D 6693947
  • Sun, M., Northup, N., Marga, F., Huber, T., Byfield, F.J., Levitan, I., Forgacs, G., The effect of cellular cholesterol on membrane-cytoskeleton adhesion (2007) Journal of Cell Science, 120 (13), pp. 2223-2231. , DOI 10.1242/jcs.001370
  • Suzuki, K., Ritchie, K., Kajikawa, E., Fujiwara, T., Kusumi, A., Rapid hop diffusion of a G-protein-coupled receptor in the plasma membrane as revealed by single-molecule techniques (2005) Biophysical Journal, 88 (5), pp. 3659-3680. , DOI 10.1529/biophysj.104.048538
  • Triller, A., Choquet, D., Synaptic structure and diffusion dynamics of synaptic receptors (2003) Biology of the Cell, 95 (7), pp. 465-476. , DOI 10.1016/j.biolcel.2003.07.001
  • Vaz, W.L., Criado, M., Madeira, V.M., Schoellmann, G., Jovin, T.M., Size dependence of the translational diffusion of large integral membrane proteins in liquid-crystalline phase lipid bilayers. A study using fluorescence recovery after photobleaching (1982) Biochemistry, 21, pp. 5608-5612. , 10.1021/bi00265a034 1:CAS:528:DyaL38XlslOgs7k%3D 6216914
  • Vrljic, M., Nishimura, S.Y., Moerner, W.E., McConnell, H.M., Cholesterol depletion suppresses the translational diffusion of class II major histocompatibility complex proteins in the plasma membrane (2005) Biophysical Journal, 88 (1), pp. 334-347. , DOI 10.1529/biophysj.104.045989
  • Willmann, R., Pun, S., Stallmach, L., Sadasivam, G., Santos, A.F., Caroni, P., Fuhrer, C., Cholesterol and lipid microdomains stabilize the postsynapse at the neuromuscular junction (2006) EMBO Journal, 25 (17), pp. 4050-4060. , DOI 10.1038/sj.emboj.7601288, PII 7601288
  • Zaal, K.J., Smith, C.L., Polishchuk, R.S., Altan, N., Cole, N.B., Ellenberg, J., Hirschberg, K., Lippincott-Schwartz, J., Golgi membranes are absorbed into and reemerge from the ER during mitosis (1999) Cell, 99, pp. 589-601. , 10.1016/S0092-8674(00)81548-2 1:CAS:528:DC%2BD3cXitVKh 10612395
  • Zhu, D., Xiong, W.C., Mei, L., Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering (2006) Journal of Neuroscience, 26 (18), pp. 4841-4851. , http://www.jneurosci.org/cgi/reprint/26/18/4841, DOI 10.1523/JNEUROSCI.2807-05.2006

Citas:

---------- APA ----------
Baier, C.J., Gallegos, C.E., Levi, V. & Barrantes, F.J. (2010) . Cholesterol modulation of nicotinic acetylcholine receptor surface mobility. European Biophysics Journal, 39(2), 213-227.
http://dx.doi.org/10.1007/s00249-009-0521-2
---------- CHICAGO ----------
Baier, C.J., Gallegos, C.E., Levi, V., Barrantes, F.J. "Cholesterol modulation of nicotinic acetylcholine receptor surface mobility" . European Biophysics Journal 39, no. 2 (2010) : 213-227.
http://dx.doi.org/10.1007/s00249-009-0521-2
---------- MLA ----------
Baier, C.J., Gallegos, C.E., Levi, V., Barrantes, F.J. "Cholesterol modulation of nicotinic acetylcholine receptor surface mobility" . European Biophysics Journal, vol. 39, no. 2, 2010, pp. 213-227.
http://dx.doi.org/10.1007/s00249-009-0521-2
---------- VANCOUVER ----------
Baier, C.J., Gallegos, C.E., Levi, V., Barrantes, F.J. Cholesterol modulation of nicotinic acetylcholine receptor surface mobility. Eur. Biophys. J. 2010;39(2):213-227.
http://dx.doi.org/10.1007/s00249-009-0521-2