Structure and dynamics of the γM4 transmembrane domain of the acetylcholine receptor in lipid bilayers: insights into receptor assembly and function

References

• Corringer PJ, Le Novère N, Changeux JP. Nicotinic receptors at the amino acid level. Ann Rev Pharmacol Toxicol 2000; 40: 431–458
   PubMed Web of Science ®Google Scholar
• Barrantes FJ. Transmembrane modulation of nicotinic acetylcholine receptor function. Curr Opin Drug Disc Develop 2003; 6: 620–632
   PubMedGoogle Scholar
• Barrantes FJ. Structural basis for lipid modulation of nicotinic acetylcholine receptor function. Brain Res Rev 2004; 47: 71–95
   PubMedGoogle Scholar
• Marsh D, Barrantes FJ. Immobilized lipid in acetylcholine receptor-rich membranes from Torpedo marmorata. Proc Natl Acad Sci USA 1978; 75: 4329–4333
   PubMedGoogle Scholar
• Blanton MP, Cohen JB. Mapping the lipid-exposed regions in the Torpedo californica nicotinic acetylcholine receptor. Biochemistry 1992; 31: 3738–3750
   PubMedGoogle Scholar
• Blanton MP, Cohen JB. Identifying the lipid-protein interface of the Torpedo nicotinic acetylcholine receptor: secondary structure implications. Biochemistry 1994; 33: 2859–2872
   PubMedGoogle 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
• Miyazawa A, Fujiyoshi Y, Unwin N. Structure and gating mechanism of the acetylcholine receptor pore. Nature 2003; 423: 949–955
   PubMed Web of Science ®Google Scholar
• Watts A. Solid-state NMR in drug design and discovery for membrane-embedded targets. Nat Rev Drug Discov 2006; 54: 555–568
   Google Scholar
• Xu Y, Barrantes FJ, Luo X, Chen K, Shen J, Jiang H. Conformational dynamics of the nicotinic acetylcholine receptor channel: A 35-ns molecular dynamics simulation study. J Am Chem Soc 2005; 127: 1291–1299
   Google Scholar
• Tamamizu S, Guzman GR, Santiago J, Rojas LV, McNamee MG, Lasalde-Dominicci JA. Functional effects of periodic tryptophan substitutions in the γM4 transmembrane domain of the Torpedo californica nicotinic acetylcholine receptor. Biochemistry 2000; 39: 4666–4673
   PubMedGoogle Scholar
• Lee YH, Li L, Lasalde J, Rojas L, McNamee MG, Ortiz-Miranda SI, Pappone P. Mutations in the M4 domain of Torpedo californica acetylcholine receptor dramatically alter ion channel function. Biophys J 1994; 66: 646–653
   PubMedGoogle Scholar
• Bouzat C, Roccamo AM, Garbus I, Barrantes FJ. Mutations at lipid-exposed residues of the acetylcholine receptor affect its gating kinetics. Mol Pharmacol 1998; 54: 146–153
   PubMed Web of Science ®Google Scholar
• daCosta CJ, Ogrel AA, McCardy EA, Blanton MP, Baenziger JE. Lipid-protein interactions at the nicotinic acetylcholine receptor. A functional coupling between nicotinic receptors and phosphatidic acid-containing lipid bilayers. J Biol Chem 2002; 277: 201–208
   PubMed Web of Science ®Google Scholar
• de Almeida RFM, Fedorov A, Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys J 2003; 85: 2406–2416
   PubMed Web of Science ®Google Scholar
• Gill SC, von Hippel PH. Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 1989; 182: 319–326
   PubMed Web of Science ®Google Scholar
• de Almeida RFM, Loura LMS, Prieto M, Watts A, Fedorov A, Barrantes FJ. Cholesterol modulates the organization of the γM4 transmembrane domain of the muscle nicotinic acetylcholine receptor. Biophys J 2004; 86: 2261–2272
   PubMedGoogle Scholar
• Chen RF. Fluorescence quantum yields of tryptophan and tyrosine. Anal Lett 1967; 1: 35–42
   Google Scholar
• Loura LMS, Fedorov A, Prieto M. Resonance energy transfer in a model system of membranes: Application to gel and liquid crystalline phases. Biophys J 1996; 71: 1823–1836
   PubMed Web of Science ®Google Scholar
• Lakowicz JR. Principles of fluorescence spectroscopy2nd ed. Kluwer/Plenum, New York 1999
   Google Scholar
• Knutson JR, Beechem JM, Brand L. Simultaneous analysis of multiple fluorescence decay curves – a global approach. Chem Phys Lett 1983; 102: 501–507
   Web of Science ®Google Scholar
• Valeur B, Weber G. Resolution of the fluorescence excitation spectrum of indole into the 1La and 1Lb excitation bands. Photochem Photobiol 1977; 25: 441–444
   PubMed Web of Science ®Google Scholar
• Dutt GB. Rotational diffusion of nondipolar probes in Triton X-100 micelles: Role of specific interactions and micelle size on probe dynamics. J Phys Chem B 2002; 106: 7398–7404
   Google Scholar
• McClare CWF. An accurate and convenient organic phosphorus assay. Anal Biochem 1971; 39: 527–530
   PubMedGoogle Scholar
• Deeg R, Ziegenhorn J. Kinetic enzymathic method for automated determination of total cholesterol in serum. Clin Chem 1983; 29: 1798–1802
   PubMed Web of Science ®Google Scholar
• Antollini SS, Xu Y, Jiang H, Barrantes FJ. Fluorescence and molecular dynamics studies of the acetylcholine receptor γM4 transmembrane peptide in reconstituted systems. Mol Membr Biol 2005; 22: 471–483
   PubMed Web of Science ®Google Scholar
• Chattopadhyay A, Raghuraman H. Application of fluorescence spectroscopy to membrane protein structure and dynamics. Curr Sci 2004; 87: 175–180
   Google Scholar
• Itoh KI, Azumi T. Shift of emission band upon excitation at long wavelength absorption-edge 2. importance of solute-solvent interaction and solvent reorientation relaxation process. J Chem Phys 1975; 62: 3431–3438
   Web of Science ®Google Scholar
• de Almeida RFM, Loura LMS, Prieto M. Application of fluorescence to understand the interaction of peptides with binary lipid membranes. Rev Fluorescence 2005; 2: 271–323
   Google Scholar
• Ridder ANJA, Morein S, Stam JG, Kuhn A, de Kruijff B, Killian JA. Analysis of the role of interfacial tryptophan residues in controlling the topology of membrane proteins. Biochemistry 2000; 39: 6521–6528
   PubMed Web of Science ®Google Scholar
• Chen Y, Barkley MD. Toward understanding tryptophan fluorescence in proteins. Biochemistry 1998; 37: 9976–9982
   PubMed Web of Science ®Google Scholar
• Sillen A, Engelborghs Y. The correct use of ‘average’ fluorescence parameters. Photochem Photobiol 1998; 67: 475–486
   Web of Science ®Google Scholar
• Dahms TES, Szabo AG. Probing local secondary structure by fluorescence: Time-resolved and circular dichroism studies of highly purified neurotoxins. Biophys J 1995; 69: 569–576
   PubMedGoogle Scholar
• Kingsman SM, Kingsman AJ. The regulation of human immunodeficiency virus type-1 gene expression. Eur J Biochem 1996; 240: 491–507
   PubMedGoogle Scholar
• Larsen OFA, van Stokkum IHM, Pandit A, van Grondelle R, van Amerongen H. Ultrafast polarized fluorescence measurements on tryptophan and a tryptophan-containing peptide. J Phys Chem B 2003; 107: 3080–3085
   Google Scholar
• Ladokhin AS. On the interpretation of decay-associated fluorescence spectra in proteins. Biopolymers Cell 2001; 17: 221
   Google Scholar
• Rinia HA, Boots JWP, Kik RA, Sneel MME, Demel RA, Killian JA, van der Erden JPJM, de Kruijff B. Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: Specific effects of flanking residues. Biochemistry 2002; 41: 2814–2824
   PubMed Web of Science ®Google Scholar
• de Foresta B, Tortech L, Vincent M, Gallay J. Location and dynamics of tryptophan in transmembrane alpha-helix peptides: A fluorescence and circular dichroism study. Eur Biophys J 2002; 31: 185–198
   PubMedGoogle Scholar
• Vogel H, Nilsson L, Rigler R, Vogues KL, Jung G. Structural fluctuations of a helical polypeptide traversing a lipid bilayer. Proc Natl Acad Sci USA 1988; 85: 5067–5071
   PubMedGoogle Scholar
• Sparr E, Ganchev DN, Snel MME, Ridder ANJA, Kroon-Batenburg LMJ, Chupin V, Rijkers DTS, Killian JA, de Kruijff B. Molecular organization in striated domains induced by transmembrane γ-helical peptides in dipalmitoyl phosphatidylcholine bilayers. Biochemistry 2005; 44: 2–10
   PubMedGoogle Scholar
• Lipari G, Szabo A. Effect of vibrational motion on fluorescence depolarization and nuclear magnetic resonance relaxation in macromolecules and membranes. Biophys J 1980; 30: 489–506
   PubMed Web of Science ®Google Scholar
• Kinosita K, Jr, Kawato S, Ikegami A. A theory of fluorescence polarization decay in membranes. Biophys J 1977; 20: 289–305
   PubMed Web of Science ®Google Scholar
• Poveda JA, Prieto M, Encinar JA, Gonzalez-Ros JM, Mateo CR. Intrinsic tyrosine fluorescence as a tool to study the interaction of the Shaker B ‘Ball’ peptide with anionic membranes. Biochemistry 2003; 42: 7124–7132
   PubMedGoogle Scholar
• Bowie JU. Helix packing in membrane proteins. J Mol Biol 1997; 272: 780–789
   PubMedGoogle Scholar
• de Planque MR, Kruijtzer JA, Liskamp RM, Marsh D, Greathouse DV, Koeppe 2nd RE, de Kruijff B, Killian JA. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane alpha-helical peptides. J Biol Chem 1999; 274: 20839–20846
   PubMed Web of Science ®Google Scholar
• Williamson PTF, Zandomeneghi G, Barrantes FJ, Watts A, Meier BH. Structural and dynamic studies of the γ-M4 trans-membrane domain of the nicotinic acetylcholine receptor. Mol Membr Biol 2005; 22: 485–496
   PubMed Web of Science ®Google Scholar
• Lakowicz JR. On spectral relaxation in proteins. Photochem Photobiol 2000; 72: 421
   PubMedGoogle Scholar
• Pandit A, Larsen OFA, van Stokkum IHM, van Grondelle R, Kraayenhof R, van Amerongen H. Ultrafast polarized fluorescence measurements on monomeric and self-associated melittin. J Phys Chem B 2003; 107: 3086–3090
   Google Scholar
• Toptygin D, Savtchenko RS, Meadow ND, Brand L. Homogeneous spectrally- and time-resolved fluorescence emission from single-tryptophan mutants of IIAGlc Protein. J Phys Chem B 2001; 105: 2043–2055
   Google Scholar
• Lundbaek JA, Anderson OS, Werge T, Nielsen C. Cholesterol-induced protein sorting: An analysis of energetic feasibility. Biophys J 2003; 84: 2080–2089
   PubMed Web of Science ®Google Scholar
• Vidal A, McIntosh TJ. Transbilayer peptide sorting between raft and nonraft bilayers: Comparisons of detergent extraction and confocal microscopy. Biophys J 2005; 89: 1102–1108
   PubMed Web of Science ®Google Scholar
• Poveda JA, Encinar JA, Fernandez AM, Mateo CR, Ferragut JA, Gonzalez-Ros JM. Segregation of phosphatidic acid-rich domains in reconstituted acetylcholine receptor membranes. Biochemistry 2002; 41: 12253–12262
   PubMedGoogle Scholar
• Noda M, Takahashi H, Tanabe T, Toyosato M, Kikyotani S, Furutani Y, Hirose T, Takashima H, Inayama S, Miyata T, Numa S. Structural homology of Torpedo californica acetylcholine receptor subunits. Nature 1983; 302: 528–532
   PubMed Web of Science ®Google Scholar
• Wenz J, Barrantes FJ. Nicotinic acetylcholine receptor induces lateral segregation of phosphatidic acid and phosphatidylcholine in reconstituted membranes. Biochemistry 2005; 44: 398–410
   PubMedGoogle Scholar