Kinked-helices model of the nicotinic acetylcholine receptor ion channel and its complexes with blockers: Simulation by the Monte Carlo minimization method

Biophysical Journal

Volumn 74, Issue 1, 1998, Pages 242-255

  Tikhonov, Denis B ^a   Zhorov, Boris S ^a,b  

^a SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPROMAZINE; ION CHANNEL; NICOTINIC RECEPTOR; PENTAMETHONIUM;

AFFINITY LABELING; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CALCULATION; ELECTRON MICROSCOPY; FOURIER TRANSFORMATION; HYDROGEN BOND; MUTAGENESIS; SYSTEM ANALYSIS;

EID: 0031972865     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77783-5     Document Type: Article

References (73)

1. Adams, P. R. 1977. Voltage jump analysis of procaine action at frog end-plate. J. Physiol. (Lond.). 268:291-318.
2. Aguayo, L. G., and E. X. Albuquerque. 1986. Effects of phencyclidine and its analogs on the end-plate current of the neuromuscular junction. J. Pharmacol. Exp. Ther. 239:15-24.
3. Akabas, M. H., and A. Karlin. 1995. Identification of acetylcholine receptor channel-lining residues in the Ml segment of the alpha-subunit. Biochemistry: 34:12496-12500.
4. Akabas, M. H., C. Kauffmann, P. Archdeacon, and A. Karlin. 1994. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the alpha-subunit. Neuron. 13:919-927.
5. Amador, M., and J. A. Dani. 1991. MK-801 inhibition of nicotinic acetylcholine receptor channel. Synapse. 7:207-215.
6. Antonov, S. M., J. W. Johnson, N. Ya. Lukomskaya, N. N. Potapyeva, V. E. Gmiro, and L. G. Magazanik. 1995. Novel adamantane derivatives act as blockers of open ligand-gated channels and as anticonvulsants. Mol. Pharmacol. 47:558-567.
7. Baenziger, J. E., and N. Methot. 1995. Fourier transform infrared and hydrogen/deuterium exchange reveal an exchange-resistant core of α-helical peptide hydrogens in the nicotinic acetylcholine receptor. J. Biol. Chem. 270:29129-29137.
8. Bechinger, B. K. Y., L. E. Chirlian, J. Gesell, J. M. Neumann, M. Montai, J. Tomich, M. Zasloff, and S. J. Opela. 1991. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J. Biomol. NMR. 1:167-173.
9. Benoit, P., and J. P. Changeux. 1993. Voltage dependencies of the effects of chlorpromazine on the nicotinic receptor channel from mouse muscle sell line So18. Neurosci. Lett. 160:81-84.
10. Bertrand, D., J. L. Galzi, A. Devillers-Thiery, S. Bertrand, and J. P. Changeux. 1993. Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal alpha7 nicotinic receptor. Proc. Natl. Acad. Sci. USA. 90:6971-6975.
11. Bolin, J. T., D. J. Filman, D. A. Matthews, R. C. Hamlin, and J. Kraut. 1982. Crystal structure of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 A resolution. J. Biol. Chem. 257:13650-13662.
12. Brooks, C. L., B. M. Pettitt, and M. Karplus. 1985. Structural and energetic effects of truncating long ranged interactions in ionic polar fluids. J. Chem. Phys. 83:5897-5908.
13. Brovtsyna, N. B., D. B. Tikhonov, O. B. Gorbunova, V. E. Gmiro, S. E. Serduk, N. Ya. Lukomskaya, L. G. Magazanik, and B. S. Zhorov. 1996. Architecture of the neuronal nicotinic acetylcholine receptor ion channel at the binding site of bis-ammonium blockers. J. Membr. Biol. 152:77-87.
14. Changeux, J. P., J. L. Galzi, A. Devillers-Thiery, and D. Bertrand. 1992. The functional architecture of the acetylcholine nicotinic receptor explored by affinity labelling and site-directed mutagenesis. Q. Rev. Biophys. 25:395-432.
15. Charnet, P., C. Labarca, R. J. Leonard, N. J. Vogelaar, L. Czyzyk, A. Gouin, N. Davidson, and H. A. Lester. 1990. An open channel blocker interacts with adjacent turns of alpha-helices in the nicotmic acetylcholine receptor. Neuron. 4:87-95.
16. Cohen, B. N., C. Labarca, N. Davidson, and H. A. Lester. 1992. Mutations in M2 alter the selectivity of the mouse nicotinic acetylcholine receptor for organic and alkali metal cations. J. Gen. Physiol. 100:373-400.
17. Cuevas, J., and D. J. Adams. 1994. Local anaesthetics blockade of neuronal nicotinic ACh receptor-channels in rat parasympathetic ganglion cells. Br. J. Pharmacol. 111:663-672.
18. Devillers-Thiery, A., J. L. Galzi, J. L. Eisele, S. Bertrand, D. Bertrand, and J. P. Changeux. 1993. Functional architecture of the nicotinic acetylcholine receptor: a prototype of ligand-gated ion channels. J. Membr. Biol. 136:97-112.
19. DiPaola, M., P. N. Kao, and A. Karlin. 1990. Mapping the alpha-subunit site photolabelled by the noncompetitive inhibitor quinacrine azide in the active state of the nicotinic acetylcholine receptor. J. Biol. Chem. 265:11017-11029.
20. Dwyer, T. M., D. J. Adams, and B. Hille. 1980. The permeability of the endplate channel to organic cations in frog muscle. J. Gen. Physiol. 75:469-492.
21. Eisenman, G., A. Villarroel, M. Montai, and O. Alvarez. 1990. Energy profiles for ion permeation in pentameric protein channels: from viruses to receptor channels. In Progress in Cell Research, Vol. 1. J. M. Ritchie, P. J. Magistrelli, and L. Bolis, editors. Elsevier Science Publishers, Amsterdam. 195-211.
22. Feltz, A., and A. Trautmann. 1982. Desensitization at the frog neuromuscular junction: a biphasic process. J. Physiol. (Lond.). 322:257-272.
23. Filatov, G. N., and M. M. White. 1995. The role of conserved leucines in the M2 domain of the acetylcholine-receptor in channel gating. Mol. Pharmacol. 48:379-384.
24. Furois-Corbin, S., and A. Pullman. 1989. A possible model for the inner wall of the acetylcholine receptor channel. Biochim. Biophys. Acta. 984:339-350.
25. Galzi, J. L., and J. P. Changeux. 1994. Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr. Opin. Struct. Biol. 4:554-565.
26. Galzi, J. L., and J. P. Changeux. 1995. Neuronal nicotinic receptors: molecular organisation and regulations. Neuropharmacology. 34:563-582.
27. Hille, B. 1992. Ionic Channels of Excitable Membranes, 2nd Ed. Sinauer Associates, Sunderland, MA.
28. Hucho, F., U. Gorne-Tschelnokow, and A. Strecker. 1994. Beta-structure in the membrane-spanning part of the nicotinic acetylcholine receptor (or how helical are transmembrane helices?). Trends Neurosci. 19:383-387.
29. Hucho, F., and R. Hilgenfeld. 1989. The selectivity filter of a ligand-gated ion channel. FEBS Lett. 257:17-23.
30. Hucho, F., W. Oberthur, and F. Lottspeich. 1986, The ion channel of the nicotinic acetylcholine receptor is formed by the homologous helices MII of the receptor subunits. FEBS Lett. 205:137-142.
31. Imoto, K., C. Busch, B. Sakmann, M. Mishina, T. Konno, J. Nakai, H. Buyo, Y. Mori, K. Kukuda, and S. Numa. 1988. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature. 335:645-648.
32. Imoto, K., T. Konno, J. Nakai, F. Wang, M. Mishina, and S. Numa. 1991. A ring of uncharged polar amino acids as a component of channel constriction in the nicotinic acetylcholine receptor. FEBS Lett. 289:193-200.
33. Konno, T., C. Busch, E. Von Kitzing, K. Imoto, F. Wang, J. Nakai, M. Mishina, S. Numa, and B. Sakmann. 1991. Rings of anionic amino acids as structural determinants of ion selectivity in the acetylcholine receptor channel. Proc. R. Soc. Lond. B. 244:69-79.
34. Labarca, C., M. W. Nowak, H. Zhang, L. Tang, P. Deshpande, and H. A. Lester. 1995. Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature. 376:514-516.
35. Large, W. A., and J. A. Sim. 1986. A comparison between mechanisms of action of different nicotinic blocking agents on rat submandibular ganglia. Br. J. Pharmacol. 89:583-592.
36. Le Novere, N., and J. P. Changeux. 1995. Molecular evolution of the nicotmic acetylcholine receptor: an example of multigene family in excitable cells. J. Mol. Evol. 40:155-172.
37. Leonard, R. J., C. G. Labarca, P. Charnet, N. Davidson, and H. A. Lester. 1988. Evidence that the M2 membrane-spanning region lines the ion channel pore of the nicotinic receptor. Science. 242:1578-1581.
38. Lester, H. A. 1992. The permeation pathway of neurotransmitter-gated ion channels. Annu. Rev. Biophys. Biomol. Struct. 21:267-292.
39. Levitt, M. 1978. Conformational preferences of amino acids in global proteins. Biochemistry. 17:4277-4284.
40. Li, Z., and H. A., Scheraga. 1988. Structure and free energy of complex thermodynamic systems. J. Mol. Struct. 179:333-352.
41. Malashkevich, V. N., R. A. Kammerer, V. P. Efimov, T. Schulthess, and J. Engel. 1996. The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel? Science. 274:761-765.
42. Momany, F. A., R. F. McGuire, A. W. Burgess, and H. A. Scheraga. 1975. Energy parameters in polypeptides. VII. Geometric parameters, partial atomic charges, nonbonded interactions, hydrogen bond interactions, and intrinsic torsional potentials of the naturally occurring amino acids. J. Phys. Chem. 79:2361-2381.
43. Moore, W. J. 1972. Physical Chemistry. Longman, London.
44. Neher, E., and J. H. Steinbach. 1978. Local anaesthetic transiently block currents through single acetylcholine-receptor channels. J. Physiol. (Lond.). 277:153-176.
45. Nemethy, G., M. S. Pottle, and H. A. Scheraga. 1983. Energy parameters in polypeptides. 9. Updating of geometrical parameters, nonbonded interactions, and hydrogen bond interactions for the naturally occurring amino acids. J. Phys. Chem. 87:1883-1887.
46. Nutter, T. J., and D. J. Adams. 1995. Monovalent and divalent cation permeability and block of neuronal nicotinic receptor channels in rat parasympathetic ganglia. J. Gen. Physiol. 105:701-723.
47. Oblatt-Montal, M., L. Buhler, T. Iwamoto, J. M. Tomich, and M. Montal. 1993a. Synthetic peptides and four-helix bundle proteins as model systems for the pore-forming structure of channel proteins: transmembrane segment M2 of the nicotinic cholinergic receptor channel is a key pore-lining structure. J. Biol. Chem. 268:14601-14607.
48. Oblatt-Montal, M., T. Iwamoto, J. M. Tomich, and M. Montal. 1993b. Design, synthesis and functional characterization of a pentameric channel protein that mimics the presumed pore structure of the nicotinic cholinergic receptor. FEBS Lett. 320:261-266.
49. Oiki, S., W. Danho, V. Madison, and M. Montal. 1988. M2 delta, a candidate for the structure lining the ionic channel of the nicotinic cholinergic receptor. Proc. Natl. Acad. Sci. USA. 85:8703-8707.
50. Oiki, S., V. Madison, and M. Montal. 1990. Bundles of amphipathic transmembrane alpha-helices as a structural motif for ion-conducting channel proteins: studies on sodium channels and acetylcholine receptors. Proteins Struct. Funct. Genet. 8:226-236.
51. Ortels, M. O., and G. G. Lunt. 1996. A mixed helix-beta-sheet model of the transmembrane region of the nicotinic acetylcholine receptor. Protein Eng. 9:51-59.
52. Opella, S. J., J. Gasell, A. P. Valente, F. M. Marassi, M. Oblatt-Montal, W. Sun, A. Ferrer-Montiel, and M. Montal. 1997. Structural studies of the pore-lining segments of neurotransmitter-gated channel. CHEMTRACTS Biochem. Mol. Biol. 10:153-174.
53. Papke, R. L., and R. E. Oswald. 1989. Mechanisms of noncompetitive inhibition of acetylcholine-induced single-channel currents. J. Gen. Physiol. 93:785-811.
54. Revah, F., D. Bertrand, J. L. Galzi, A. Devillers-Thiery, C. Mulle, N. Hussy, S. Bertrand, M. Ballivet, and J. P. Changeux. 1991. Mutations in the channel domain alter desensitization of a neuronal nicotinic receptor. Nature. 353:846-849.
55. 3H]chlorpromazine labels three amino acids of the acetylcholine receptor gamma subunit: implication for the alpha-helical organization of regions MII and for the structure of the ion channel. Proc. Natl. Acad. Sci. USA. 87:4675-4679.
56. Sands, S. B., and M. E. Barish. 1991. Calcium permeability of neuronal nicotinic channels in PC12 cells. Brain Res. 560:38-42.
57. Sankararamakrishnan, R., C. Adcock, and M. S. P. Sansom. 1996. The pore domain of the nicotinic acetylcholine receptor: molecular modelling, pore dimensions, and electrostatics. Biophys. J. 71:1659-1671.
58. Sankararamakrishnan, R., and M. S. P. Sansom. 1994. Kinked structure of isolated nicotinic receptor M2 helices: a molecular dynamics study. Biopolymers. 34:1647-1657.
59. Tikhonov, D. B., N. N. Potapyeva, V. E. Gmiro, B. S. Zhorov, and L. G. Magazanik. 1996. A proposed binding mechanism of pentamethylenebisammonium derivatives to the muscle nicotinic acetylcholine receptor channel. Biol. Membr. 13:185-195.
60. Unwin, N. 1993. Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229:1101-1124.
61. Unwin, N. 1995. Acetylcholine receptor channel imaged in the open state. Nature. 373:37-43.
62. Unwin, N. 1996. Projection structure of the nicotinic acetylcholine receptor: distinct conformations of the alpha subunits. J. Mol. Biol. 257:586-596.
63. Vasquez, M., G. Nemethy, and H. A. Scheraga. 1983. Computed conformational states of the 20 naturally occurring amino acids and of the prototype residue α-aminobutyric acid. Macromolecules. 16:1043-1049.
64. Verino, S., M. Amador, C. W. Luetje, J. Patrick, and J. A. Dani. 1992. Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptor. Neuron. 8:127-134.
65. Villarroel, A., S. Herlitze, M. Koenen, and B. Sakmann. 1991. Location of a threonine residue in the alpha-subunit M2 transmembrane segment that determines the ion flow through the acetylcholine receptor channel. Proc. R. Soc. Lond. B. 243:69-74.
66. Villarroel, A., and B. Sakmann. 1992. Threonine in the selectivity filter of the acetylcholine receptor channel. Biophys. J. 62:196-205.
67. von Kitzing, E. 1995. Structure modelling of the acetylcholine receptor channel, and related ligand gated channels. In Modelling of Biomolecular Structures and Mechanisms A. Pullman, J. Jortner, and B. Pullman, editors. Kluwer Academic Publishers, Dordrecht, the Netherlands. 39-57.
68. 125I]iodophenyl)-diazirine is a novel noncompetitive antagonist of the nicotinic acetylcholine receptor. J. Biol. Chem. 266:21595-21607.
69. Zhorov, B. S. 1981. Vector method for calculating derivatives of energy of atom-atom interactions of complex molecules according to generalized coordinates. J. Struct. Chem. 22:4-8.
70. Zhorov, B. S. 1983. Vector method for calculating derivatives of the energy deformation of valence angles and torsion energy of complex molecules according to generalized coordinates. J. Struct. Chem. 23:649-655.
71. 2+, and calcium entry blockers. J. Membr. Biol. 135:119-127.
72. 2+ ions and dihydropyridine ligand. Biophys. J. 70:22-37.
73. Zhorov, B. S., N. B. Brovtsyna, V. E. Gmiro, N. Ya. Lukomskaya, S. E. Serduk, N. N. Potapyeva, L. G. Magazanik, D. E. Kurenniy, and V. I. Skok. 1991. Dimensions of the ion channel in neuronal nicotinic acetylcholine receptor as estimated from analysis of conformation-activity relationships of open-channel blocking drug. J. Membr. Biol. 121:119-132.