The α7 nicotinic acetylcholine receptor: Molecular modelling, electrostatics, and energetics

Molecular Membrane Biology

Volumn 22, Issue 3, 2005, Pages 151-162

  Amiri, Shiva ^a   Tai, Kaihsu ^a   Beckstein, Oliver ^a   Biggin, Philip C ^a   Sansom, Mark S P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Electrostatics; Gaussian network model; Molecular modelling; Nicotinic receptor

Indexed keywords

ACETYLCHOLINE; BINDING PROTEIN; CALCIUM ION; CHLORIDE ION; ION CHANNEL; MEMBRANE PROTEIN; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT; SODIUM CHLORIDE; SODIUM ION; ALPHA-BUNGAROTOXIN RECEPTOR; BUNGAROTOXIN; BUNGAROTOXIN RECEPTOR;

ARTICLE; ELECTRON MICROSCOPY; ENERGY TRANSFER; LYMNAEA; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NORMAL DISTRIBUTION; POISSON DISTRIBUTION; PRIORITY JOURNAL; STATISTICAL MODEL; STEREOCHEMISTRY; STRUCTURE ACTIVITY RELATION; TORPEDO; AMINO ACID SEQUENCE; CHANNEL GATING; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ELECTRICITY; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; BUNGAROTOXINS; COMPUTER SIMULATION; ELECTROSTATICS; ION CHANNEL GATING; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, NICOTINIC; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 17844406709     PISSN: 09687688     EISSN: None     Source Type: Journal    
DOI: 10.1080/09687860500063340     Document Type: Article

References (72)

1. Allen TW, Andersen OS, Roux B. 2004. Energetics of ion conduction through the gramicidin channel. Proc Nat Acad Sci USA 101:117-122.
2. Anishkin A, Sukharev S. 2004. Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys J 86:2883-2895.
3. Ashcroft FM. 2000. Ion channels and disease. San Diego: Academic Press.
4. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, Bahar I. 2001. Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80:505-515.
5. Bahar I, Atilgan AR, Erman B. 1997. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold Des 2:173-181.
6. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Nat Acad Sci USA 98:10037-10041.
7. Beckstein O, Biggin PC, Bond PJ, Bright JN, Domene C, Grottesi A, Holyoake J, Sansom MSP. 2003. Ion channel gating: insights via molecular simulations. FEBS Lett 555:85-90.
8. Beckstein O, Biggin PC, Sansom MSP. 2001. A hydrophobic gating mechanism for nanopores. J Phys Chem B 105:12902-12905.
9. Beckstein O, Sansom MSP. 2004. The influence of geometry, surface character and flexibility on the permeation of ions and water through biological pores. Phys Biol 1:42-52.
10. Beckstein O, Tai K, Sansom MSP. 2004. Not ions alone: Barriers to ion permeation in nanopores and channels. J Amer Chem Soc 126:14694-14695.
11. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. 1984. Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684-3690.
12. Bertrand D, Devillers-Thiéry A, Revah F, Galzi J, Hussy N, Mulle C, Bertrand S, Ballivet M, Changeux J. 1992. Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain. Proc Natl Acad Sci USA 89:1261-1265.
13. Bouzat C, Gumilar F, Spitzmaul G, Wang HL, Rayes D, Hansen SB, Taylor P, Sine SM. 2004. Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel. Nature 430:896-900.
14. Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van der Oost J, Smit AB, Sixma TK. 2001. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411:269-276.
15. Celie PHN, van Rossum-Fikkert SE, van Dijk WJ, Brejc K, Smit AB, Sixma TK. 2004. Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41:907-914.
16. Changeux JP, Galzi JI, Devillers-Thiéry A, Bertrand D. 1992. The functional architecture of the acetylcholine nicotinic receptor explored by affinity labelling and site-directed mutagenesis. Quart Rev Biophys 25:395-432.
17. Corringer PJ, Le Novere N, Changeux JP. 2000. Nicotinic receptors at the amino acid level. Ann Rev Pharmacol Toxicol 40:431-458.
18. Corry B. 2004. Theoretical conformation of the closed and open states of the acetylcholine receptor channel. Biochim Biophys Acta 1663:2-5.
19. Couturier S, Bertrand D, Matter J-M, Hernandez M-C, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M. 1990. A neuronal nicotinic acetylcholine receptor subunit (alpha 7) is developmentally regulated and forms a homooligomeric channel blocked by alpha BTX. Neuron 5:847-856.
20. Cymes GD, Grosman C, Auerbach A. 2002. Structure of the transition state of gating in the acetylcholine receptor channel pore: A F-value analysis. Biochem 41:5548-5555.
21. Darden T, York D, Pedersen L. 1993. Particle mesh Ewald-an N.log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092.
22. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. 2004. PDB2PQR: An automated pipeline for the setup, execution, and analysis of Poisson-Boltzmann electrostatics calculations. Nucl Acids Res 32:W665-667.
23. Erkip A, Erman B. 2003. Dynamics of large-scale fluctuations in native proteins. Analysis based on harmonic inter-residue potentials and random external noise. Polymer 45:641-648.
24. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. 1995. A smooth particle mesh Ewald method. J Chem Phys 103:8577-8593.
25. Fiser A, Kinh Gian Do R, Sali A. 2000. Modeling of loops in protein structures. Prot Sci 9:1753-1773.
26. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35:1-8.
27. Galzi JL, Devillers-Thiery A, Hussy N, Bertrand S, Changeux JP, Bertrand D. 1992. Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature 359:500-505.
28. Goh CS, Milburn D, Gerstein M. 2004. Conformational changes associated with protein-protein interactions. Curr Opin Struct Biol 14:104-109.
29. Grosman C, Zhou M, Auerbach A. 2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature 403:773-776.
30. Henchman RH, Wang HL, Sine SM, Taylor P, McCammon JA. 2003. Asymmetric structural motions of the homomeric a7 nicotinic receptor ligand binding domain revealed by molecular dynamics simulation. Biophys J 85:3007-3018.
31. Hermans J, Berendsen HJC, van Gunsteren WF, Postma JPM. 1984. A consistent empirical potential for water-protein interactions. Biopolymers 23:1513-1518.
32. Hille B. 2001. Ionic channels of excitable membranes, 3rd ed. Sunderland, Mass: Sinauer Associates Inc.
33. Hung A, Tai K, Sansom MSP. 2004. Molecular dynamics simulation of the M2 helices within the nicotinic acetylcholine receptor transmembrane domain: Insights into structure and collective motions. Biophys J (in press)
34. Itier V, Bertrand D. 2001. Neuronal nicotinic receptors: From protein structure to function. FEBS Lett 504:118-125.
35. Karlin A. 2002. Emerging structure of the nicotinic acetylcholine receptors. Nature Rev Neurosci 3:102-114.
36. Karlin A, Akabas MH. 1995. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15:1231-1244.
37. Kash TL, Jenkins A, Kelley JC, Trudell JR, Harrison NL. 2003. Coupling of agonist binding to channel gating in the GABAA receptor. Nature 421:272-275.
38. 3 receptors. Nature 424:321-324.
39. Kim S, Chamberlain AK, Bowie JU. 2004. A model of the closed form of the nicotinic acetylcholine receptor M2 channel pore. Biophys J 87:792-799.
40. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method. J Comp Chem 13:1011-1021.
41. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. 1993. Procheck - a program to check the stereochemical quality of protein structures. J Appl Cryst 26:283-291.
42. Law RJ, Forrest LR, Ranatunga KM, La Rocca P, Tieleman DP, Sansom MSP. 2000. Structure and dynamics of the pore-lining helix of the nicotinic receptor: MD simulations in water, lipid bilayers and transbilayer bundles. Proteins: Struct Func Genet 39:47-55.
43. Law RJ, Tieleman DP, Sansom MSP. 2003. Pores formed by the nicotinic receptor M2d peptide: A molecular dynamics simulation study. Biophys J 84:14-27.
44. 2+-binding sites. Proc Nat Acad Sci USA 99:3210-3215.
45. Lester H. 1992. The permeation pathway of neurotransmitter-gated ion channels. Ann Rev Biophys Biomol Struct 21:267-292.
46. Lester HA, Dibas MI, Dahan DS, Leite JF, Dougherty DA. 2004. Cys-loop receptors: New twists and turns. Trends Neurosci 27:329-336.
47. Lindahl E, Hess B, van der Spoel D. 2001. GROMACS 3.0: A package for molecular simulation and trajectory analysis. J Molec Model 7:306-317.
48. Marinou M, Tzartos SJ. 2003. Identification of regions involved in the binding of a-bungarotoxin to the human a7 neuronal nicotinic acetylcholine receptor using synthetic peptides. Biochem J 372:543-545.
49. Mayer ML, Armstrong N. 2004. Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
50. Ming D, Kong Y, Lambert MA, Huang Z, Ma J. 2002. How to describe protein motion without amino acid sequence and atomic coordinates. Proc Nat Acad Sci USA 99:8620-8625.
51. Miyazawa A, Fujiyoshi Y, Unwin N. 2003. Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949-955.
52. Montai M. 1995. Design of molecular function: channels of communication. Ann Rev Biophys Biomol Struct 24:31-57.
53. Oiki S, Danho W, Madison V, Montai M. 1988. M2d, a candidate for the structure lining the ionic channel of the nicotinic cholinergic receptor. Proc Natl Acad Sci USA 85:8703-8707.
54. Opella SJ, Marassi FM, Gesell JJ, Valente AP, Kim Y, Oblatt-Montal M, Montai M. 1999. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nature Struct Biol 6:374-379.
55. Panicker S, Cruz H, Arrabit C, Slesinger PA. 2002. Evidence for a centrally located gate in the pore of a serotonin-gated ion channel. J Neurosci 22:1629-1639.
56. Rashin A, Honig B. 1985. Reevaluation of the Born model of ion hydration. J Phys Chem 89:5588.
57. 3 receptor: a model ligand-gated ion channel. Molec Membrane Biol 19:11-26.
58. Saiz L, Bandyopadhyay S, Klein ML. 2004. Effect of the pore region of a transmembrane ion channel on the physical properties of a simple membrane. J Phys Chem B 108:2608-2613.
59. Saiz L, Klein ML. 2002. Computer simulation studies of model biological membranes. Acc Chem Res 35:482-489.
60. Sali A, Blundell TL. 1993. Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779-815.
61. Samson AO, Chill JH, Rodriguez E, Scherf T, Anglister J. 2001. NMR mapping and secondary structure determination of the major acetylcholine receptor a-subunit determinant interacting with a-bungarotoxin. Biochem 40:5464-5473.
62. Schofield CM, Jenkins A, Harrison NL. 2003. A highly conserved aspartic acid residue in the signature disulfide loop of the a1 subunit is a determinant of gating in the glycine receptor. J Biol Chem 278:34079-34083.
63. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MSP. 1996. Hole: A program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 14:354-360.
64. Unwin N. 1989. The structure of ion channels in membranes of excitable cells. Neuron 3:665-676.
65. Unwin N. 1993. Nicotinic acetylcholine receptor at 9Å resolution. J Mol Biol 229:1101-1124.
66. Unwin N. 1995. Acetylcholine receptor channel imaged in the open state. Nature 373:37-43.
67. Unwin N. 2000. The Croonian Lecture 2000. Nicotinic acetylcholine receptor and the structural basis of fast synaptic transmission. Phil Trans Roy Soc Lond B 355:1813-1829.
68. Unwin N, Miyazawa A, Fujiyoshi Y. 2002. Activation of the nicotinic acetylcholine receptor involves a switch in conformation of the a subunits. J Mol Biol 319:1165-1176.
69. Valleau JP, Torrie GM. 1977. A guide to Monte Carlo for statistical mechanics: 2. Byways. In: Berne BJ, editor. Statistical mechanics Part A: Equilibrium techniques. New York: Plenum Press, p 164-194.
70. Vriend G. 1990. WhatIf-a molecular modeling and drug design program. J Mol Graph 8:52-56.
71. Wilson GG, Karlin A. 1998. The location of the gate in the acetylcholine receptor channel. Neuron 20:1269-1281.
72. Wilson GG, Pascual JM, Brooijmans N, Murray D, Karlin A. 2000. The intrinsic electrostatic potential and the intermediate ring of charge in the acetylcholine receptor channel. J Gen Physiol 115:93-106.