Structural and dynamic studies of the γ-M4 trans-membrane domain of the nicotinic acetylcholine receptor

References

• 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 and functional crosstalk between acetylcholine-receptor and its membrane environment. Mol Neurobiol 1993; 6: 463–482
   Google Scholar
• Barrantes FJ. Transmembrane modulation of nicotinic acetylcholine receptor function. Curr Opin Drug Discov Dev 2003; 6: 620–632
   PubMedGoogle Scholar
• Barrantes FJ. Structural basis for lipid modulation of nicotinic acetylcholine receptor function. Brain Res Reviews 2004; 47: 71–95
   PubMedGoogle Scholar
• Barrantes FJ, Antollini S, Blanton MP, Prieto M. Topography of nicotinic acetylcholine receptor membrane embedded domains. J Biol Chem 2000; 275: 37333–37339
   Google Scholar
• Belohorcova K, Qian J, Davis JH. Molecular dynamics and H-2-NMR study of the influence of an amphiphilic peptide on membrane order and dynamics. Biophys J 2000; 79: 3201–3216
   PubMed Web of Science ®Google 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, Cohen JB. Mapping the lipid-exposed regions in the torpedo-californica nicotinic acetylcholine-receptor. Biochemistry 1992; 31: 3738–3750
   PubMedGoogle Scholar
• Bolze J, Fujisawa T, Nagao T, Norisada K, Saito H, Naito A. Small angle X-ray scattering and 31P NMR studies on the phase behaviour of phospholipid bilayered mixed micelles. Chem Phys Lett 2000; 329: 215–220
   Google Scholar
• Campagna JA, Miller KW, Forman SA. Mechanisms of action of inhaled anesthetics. N Engl J Med 2003; 348: 2110–2124
   PubMed Web of Science ®Google Scholar
• Cavagnero S, Jane Dyson H, Wright PE. Improved low pH bicelle system for orienting macromolecules over a wide temperature range. J Biomol NMR 1999; 13: 387–391
   Google Scholar
• Changeux JP, Edelstein SJ. Allosteric receptors after 30 years. Neuron 1998; 21: 959–980
   PubMedGoogle Scholar
• Corbin J, Methot N, Wang HH, Baenziger JE, Blanton MP. Secondary structure analysis of individual transmembrane segments of the nicotinic acetylcholine receptor by circular dichroism and Fourier transform infrared spectroscopy. J Biol Chem 1998; 273: 771–777
   PubMed Web of Science ®Google Scholar
• Cornell BA, Separovic F, Baldassi AJ, Smith R. Conformation and orientation of gramacidin-A in oriented phospholipid bilayers measured by solid state NMR. Biophys J 1988; 53: 67–76
   PubMedGoogle Scholar
• Davis JH, Jeffrey KR, Bloom MM, Valic MI, Higgs TP. Quadrupolar echo deuterium magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem Phys Lett 1976; 42: 390–394
   Web of Science ®Google Scholar
• de Almeida RFM, Loura LMS, Prieto M, Watts A, Fedorov A, Barrantes FJ. Cholesterol modulates the organization of the gamma M4 transmembrane domain of the muscle nicotinic acetylcholine receptor. Biophys J 2004; 86: 2261–2272
   PubMedGoogle Scholar
• de Planque MRR, Rijkers DTS, Liskamp RMJ, Separovic F. The alpha-M1 transmembrane segment of the nicotinic acetylcholine receptor interacts strongly with model membranes. Mag Reson Chem 2004; 42: 148–154
   PubMedGoogle Scholar
• Fraser DM, Louro SRW, Horvath LI, Miller KW, Watts A. A study of the effect of general-anesthetics on lipid protein interactions in acetylcholine-receptor enriched membranes from torpedo-nobiliana using nitroxide spin-labels. Biochemistry 1990; 29: 2664–2669
   PubMedGoogle Scholar
• Hartzell CJ, Pratum TK, Drobny GP. Mutual orientation of three magnetic tensors in polycrystalline dipeptide by dipole-modulated 15N chemical shift spectroscopy. J Chem Phys 1987; 87: 4324–4331
   Google Scholar
• Hartzell CJ, Whitfield M, Oas TG, Drobny GP. Determination of 15N and 13C chemical shift tensors of L-[13C]-alanyl-L-[15N]-alanine from dipolar coupled powder patterns. J Am Chem Soc 1987; 109: 5966–5969
   Google Scholar
• Hediger S, Meier BH, Kurur ND, Bodenhausen G, Ernst RR. Nmr cross-polarization by Adiabatic Passage through the Hartmann–Hahn condition (APHH). Chem Phys Lett 1994; 223: 283–288
   Web of Science ®Google Scholar
• Jones J. Amino acid and peptide synthesis. Oxford University Press, Oxford 1997
   Google Scholar
• Kameda T, Ando I. The relationship between the helical conformation and 13C NMR chemical shift of amino acid residue carbonyl carbons of polypeptides in the solid state. J Mol Struct 1997; 412: 197–203
   Google Scholar
• Lee DK, Wittebort RJ, Ramamoorthy A. Characterization of N-15 chemical shift and H-1-N-15 dipolar coupling interactions in a peptide bond of a uniaxially oriented and polycrystalline samples by one-dimensional dipolar chemical shift solid state NMR spectroscopy. J Am Chem Soc 1998; 120: 8868–8874
   Web of Science ®Google Scholar
• Lewis BA, Harbison GS, Herzfeld J, Griffin RG. NMR structural analysis of a membrane protein – bacteriorhodopsin peptide backbone orientation and motion. Biochemistry 1985; 24: 4671–4679
   Google Scholar
• Live DH, Davis DG, Agosta WC, Cowburn D. Long-range hydrogen bond mediated effects in peptides-N-15 NMR study of gramacidin-S in water and organic solvents. J Am Chem Soc 1984; 106: 1939–1941
   Google Scholar
• Lugovskoy AA, Maslennikov IV, Utkin YN, Tsetlin VI, Cohen JB, Arseniev A. Spatial structure of the M3 transmembrane segment of the nicotinic acetylcholine receptor alpha-subunit. Eur J Biochem 1998; 255: 455–461
   PubMedGoogle Scholar
• Mantipragada SBL, Horvath LI, Arias HR, Schwarzmann G, Sandhoff K, Barrantes FJ, Marsh D. Lipid protein interactions and teh effect of local anaesthetics in acetylcholine receptor rich membranes from Torpedo marmorata electric organ. Biochemistry 2003; 42: 9167–9175
   PubMed Web of Science ®Google Scholar
• Marassi FM, Opella SJ, Juvvadi P, Merrifield RB. Orientation of cecropin A helices in phospholipid bilayers determined by solid-state NMR spectroscopy. Biophys J 1999; 77: 3152–3155
   PubMed Web of Science ®Google 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
• Mehring M. Principles of high-resolution NMR in solids. Springer-Verlag, Berlin 1983
   Google Scholar
• Miller KW. The nature of sites of general anaesthetic action. Br J Anaesthes 2002; 89: 17–21
   PubMed Web of Science ®Google 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
• Nagle JF, Tristran-Nagle S. Structure of lipid bilayers. Biochim Biophys Acta 2000; 1469: 159–195
   PubMed Web of Science ®Google Scholar
• Nicholson LK, Teng Q, Cross TA. Solid state nuclear magnetic resonance derived model for dynamics in the polypeptide backbone of the gramacidin-A channel. J Mol Biol 1991; 218: 621–637
   PubMed Web of Science ®Google Scholar
• Opella SJ, Marassi FM, Gesell JJ, Valente AP, Kim Y, Oblatt-Montal M, Montal M. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nature Struct Biol 1999; 6: 374–379
   PubMedGoogle Scholar
• Ottiger M, Bax A. Bicelle-based liquid crystals for NMR measurement of dipolar couplings at acidic and basic pH values. J Biomol NMR 1999; 13: 187–191
   PubMedGoogle Scholar
• Provencher SW, Glockner J. Estimation of globular protein secondary structure from circular dichroism. Biochemistry 1981; 20: 33–37
   PubMed Web of Science ®Google Scholar
• Saito H. Conformation-dependent C-13 chemical-shifts-a new means of conformational characterization as obtained by high-resolution solid-state C-13 Nmr. Mag Res Chem 1986; 24: 835–852
   Web of Science ®Google Scholar
• Sanders CR, Schwonek JP. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid state NMR. Biochemistry 1992; 31: 8898–8905
   PubMed Web of Science ®Google Scholar
• Separovic F, Pax R, Cornell BA. NMR Order parameter analysis of a peptide plane aligned in a lyotropic liquid crystal. Mol Phys 1993; 78: 357–369
   Web of Science ®Google Scholar
• Separovic F, Pax R, Cornell BA. NMR order parameter analysis of a peptide plane aligned in the lyotropic liquid crystal. Mol Phys 1993; 78: 357–369
   Web of Science ®Google Scholar
• Sharpe S, Barber KR, Grant CWM, Goodyear D, Morrow MR. Organization of model helical peptides in lipid bilayers: Insight into the behaviour of single span protein transmembrane domains. Biophys J 2002; 83: 345–358
   PubMed Web of Science ®Google Scholar
• Sixl F, Watts A. Headgroup interactions in mixed phospholipid bilayers. Proc Natl Acad Sci USA 1983; 80: 1613–1615
   PubMedGoogle Scholar
• Smith R, Separovic F, Milne TJ, Whittaker A, Bennett FM, Cornell BA, Makriyannis A. Structure and orientation of pore-forming peptide, mellitin, in lipid bilayers. J Mol Biol 1994; 241: 456–466
   PubMed Web of Science ®Google Scholar
• Smith R, Thomas DE, Separovic F, Atkins AR, Cornell BA. Determination of the structure of a membrane incorporated ion channel. Biophys J 1989; 56: 307–314
   PubMedGoogle Scholar
• Stark RE, Jelinski LW, Ruben DJ, Torchia DA, Griffin RG. 13C chemical shift and 13C-15N dipolar tensors for the peptide bond [1-13C]glycyl[15N]glycine.HCl.H20. J Mag Res 1983; 55: 266–273
   Google Scholar
• Sunshine C, McNamee MG. Lipid modulation of nioctinic acetylcholine receptor function: the role of membrane lipid composition and fluidity. Biochim Biophys Acta 1994; 1191: 59–64
   PubMed Web of Science ®Google Scholar
• Unwin N. The Croonian Lecture 2000. Nicotinic acetylcholine receptor and the structural basis of fast synaptic transmission. Phil Trans Roy Soc London Ser B. Biol Sci 2000; 355: 1813–1829
   Google Scholar
• Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4 angstrom resolution. J Mol Biol 2005; 346: 967–989
   PubMed Web of Science ®Google Scholar
• Vanstokim IHM, Spoelder HJW, Bloemendal M, VanGrondelle R, Groen FCA. Estimation of protein secondary structure and error analysis from circula-dichroism spectra. Anal Biochem 1990; 191: 110–118
   Google Scholar
• Watts A. Magnetic resonance studies of lipid–protein interfaces and lipophilic molecule partitioning. Ann NY Acad Sci 1991; 625: 653–669
   Google Scholar
• Wishart DS, Sykes BD. The C-13 chemical-shift index–a simple method for the identification of protein secondary structure using C-13 chemical-shift data. Journal of Biomolecular NMR 1994; 4: 171–180
   PubMed Web of Science ®Google Scholar
• Wu CH, Ramamoorthy A, Gierasch LM, Opella SJ. Simultaneous characterization of the amide H-1 chemical shift,H-1-N-15 dipolar, and N-15 chemical-shift interaction tensors in a peptide-bond by 3-dimensional solid-state NMR- spectroscopy. J Am Chem Soc 1995; 117: 6148–6149
   Google Scholar
• Yamaguchi S, Hong T, Waring A, Lehrer RI, Hong M. Solid state NMR investigations of peptide–lipid interaction and orientation of ss-sheet antimicrobial peptide, protegrin. Biochemistry 2002; 41: 9852–9862
   PubMed Web of Science ®Google Scholar
• Yamaguchi S, Huster D, Tack B, Kearney WR, Lehrer RI, Waring AJ, Hong M. Orientation and dynamics of an antimicrobial peptide by solid-state NMR. Biophys J 2001; 80: 2421
   Google Scholar
• Zandomeneghi G, Tomaselli M, Williamson PTF, Meier BH. NMR of bicelles: Orientation and mosaic spread of the liquid crystal director under sample rotation. J Biomol NMR 2003; 25: 113–123
   Google Scholar
• Zhang H, Karlin A. Contribution of the beta subunit M2 segment to the ion conducting pathway of the acetylcholine receptor. Biochemistry 1998; 37: 7952–2964
   Google Scholar
• Zhang H, Karlin A. Identification of acetylcholine receptor channel-lining residues in the M1 segment of the beta-subunit. Biochemistry 1997; 36: 15856–15864
   PubMed Web of Science ®Google Scholar