Kinetic, mechanistic, and structural aspects of unliganded gating of acetylcholine receptor channels: A single-channel study of second transmembrane segment 12' mutants

Journal of General Physiology

Volumn 115, Issue 5, 2000, Pages 621-635

  Grosman, Claudio ^a   Auerbach, Anthony ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Allosteric proteins; Nicotinic receptors; Site directed mutagenesis

Indexed keywords

COMPLEMENTARY DNA; ION CHANNEL; NICOTINIC RECEPTOR;

ANIMAL CELL; ARTICLE; CHOLINERGIC SYSTEM; KIDNEY CELL; KINETICS; MEMBRANE CHANNEL; MOUSE; NONHUMAN; PATCH CLAMP; SITE DIRECTED MUTAGENESIS;

ALLOSTERIC SITE; ANIMALS; CELL LINE; ELECTRIC STIMULATION; FIBROBLASTS; HUMANS; ION CHANNEL GATING; KIDNEY; KINETICS; MEMBRANE POTENTIALS; MICE; MUSCLE FIBERS; MUSCLE, SKELETAL; MUTAGENESIS, SITE-DIRECTED; PATCH-CLAMP TECHNIQUES; RECEPTORS, NICOTINIC; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0034100847     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.115.5.621     Document Type: Article

References (62)

1. Akabas, M.H., C. Kaufmann, P. Archdeacon, and A. Karlin. 1994. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the α subunit. Neuron. 13:919-927.
2. Akk, G., S. Sine, and A. Auerbach. 1996. Binding sites contribute unequally to the gating of mouse nicotinic αD200N acetylcholine receptors. J. Physiol. 496:185-196.
3. Auerbach, A., and C.J. Lingle. 1986. Heterogeneous kinetic properties of acetylcholine receptor channels in Xenopus myocytes. J. Physiol. 378:119-140.
4. Auerbach, A., W. Sigurdson, J. Chen, and G. Akk. 1996. Voltage dependence of mouse acetylcholine receptor gating: different charge movements in di-, mono- and unliganded receptors. J. Physiol. 494:155-170.
5. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1992. Short Protocols in Molecular Biology. John Wiley & Sons, New York, NY. 9.1.1-9.1.6.
6. Brehm, P., R. Kullberg, and F. Moody-Corbett. 1984. Properties of non-junctional acetylcholine receptor channels in innervated muscle of Xenopus laevis. J. Physiol. 350:631-648.
7. Chay, T.R. 1988. Kinetic modeling for the channel gating process from single channel patch clamp data. J. Theor. Biol. 132:449-468.
8. Chen, J., and A. Auerbach. 1998. A distinct contribution of the δ subunit to acetylcholine receptor channel activation revealed by mutations of the M2 segment. Biophys. J. 75:218-225.
9. Chen, Z.M., and M.M. White. 1999. The outer leucine ring is another determinant for AChR gating. Biophys. J. 76:A373. (Abstr.)
10. Chen, J., Y. Zhang, G. Akk, S. Sine, and A. Auerbach. 1995. Activation kinetics of recombinant mouse nicotinic acetylcholine receptors: mutations of α-subunit tyrosine 190 affect both binding and gating. Biophys. J. 69:849-859.
11. Croxen, R., C. Newland, D. Beeson, H. Oosterhuis, G. Chauplannaz, A. Vincent, and J. Newsom-Davis. 1997. Mutations in different functional domains of the human muscle acetylcholine receptor alpha subunit in patients with the slow-channel congenital myasthenic syndrome. Hum. Mol. Genet. 6:767-774.
12. Davies, P.A., M. Pistis, M.C. Hanna, J.A. Peters, J.J. Lambert, T.G. Hales, and E.F. Kirkness. 1999. The 5-HT3B subunit is a major determinant of serotonin-receptor function. Nature. 397:359-363.
13. Edelstein, S.J., and J.-P. Changeux. 1998. Allosteric transitions of the acetylcholine receptor. Adv. Prot. Chem. 51:121-184.
14. Edelstein, S.J., O. Schaad, E. Henry, D. Bertrand, and J.-P. Changeux. 1996. A kinetic mechanism for nicotinic acetylcholine receptors based on multiple allosteric transitions. Biol. Cybern. 75:361-379.
15. Eertmoed, A.L., and W.N. Green. 1999. Nicotinic receptor assembly requires multiple regions throughout the γ subunit. J. Neurosci. 19:6298-6308.
16. Engel, A.G., K. Ohno, M. Milone, H.-L. Wang, S. Nakano, C. Bouzat, J.N. Pruitt II, D.O. Hutchinson, J.M. Brengman, N. Bren, et al. 1996. New mutations in acetylcholine receptor subunit genes reveal heterogeneity in the slow-channel congenital myasthenic syndrome. Hum. Mol. Genet. 5:1217-1227.
17. Ferrer-Montiel, A.V., M.S. Montal, M. Díaz-Muñoz, and M. Montal. 1991. Agonist-independent activation of acetylcholine receptor channels by protein kinase A phosphorylation. Proc. Natl. Acad. Sci. USA. 88:10213-10217.
18. Gardner, P. 1990. Nucleotide sequence of the ε-subunit of the mouse muscle nicotinic receptor. Nucleic Acids Res. 18:6714.
19. Gibb, A.J., H. Kojima, J.A. Carr, and D. Colquhoun. 1990. Expression of cloned receptor subunits produces multiple receptors. Proc. R. Soc. Lond. B Biol. Sci. 242:108-112.
20. Grosman, C., and A. Auerbach. 2000. Asymmetric and independent contribution of M2 12′ residues to diliganded gating of acetylcholine receptor channels: a single-channel study with choline as the agonist. J. Gen. Physiol. 115:637-651.
21. Grosman, C., M. Zhou, and A. Auerbach. 2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature. 403:773-776.
22. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch clamp technique for high resolution current recordings from cells and cell-free membrane patches. Pflügers Arch. 391:85-100.
23. Higuchi, R. 1990. Recombinant PCR. In PCR Protocols: A Guide to Methods and Applications. M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White, editors. Academic Press, Inc., San Diego, CA. 177-183.
24. Horn, R., and K. Lange. 1983. Estimating kinetic constants from single channel data. Biophys. J. 43:207-223.
25. Jackson, M.B. 1984. Spontaneous openings of the acetylcholine receptor channel. Proc. Natl. Acad. Sci. USA. 81:3901-3904.
26. Jackson, M.B. 1986. Kinetics of unliganded acetylcholine receptor channel gating. Biophys. J. 49:663-672.
27. Jackson, M.B. 1989. Perfection of a synaptic receptor: kinetics and energetics of the acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 86:2199-2203.
28. Jackson, M.B. 1994. Single channel currents in the nicotinic acetylcholine receptor: a direct demonstration of allosteric transitions. Trends Biochem. Sci. 19:396-398.
29. Jackson, M.B., K. Imoto, M. Mishina, T. Konno, S. Numa, and B. Sakmann. 1990. Spontaneous and agonist-induced openings of an acetylcholine receptor channel composed of α-, β- and δ-subunits. Pflügers Arch. 417:129-135.
30. Karlin, A., and M.H. Akabas. 1995. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron. 15:1231-1244.
31. Kearney, P.C., H. Zhang, W. Zhong, D.A. Dougherty, and H.A. Lester. 1996. Determinants of nicotinic receptor gating in natural and unnatural side chain structures at the M2 9′ position. Neuron. 17:1221-1229.
32. Korn, S.J., and R. Horn. 1991. Discrimination of kinetic models of ion channel gating. In Methods in Neurosciences. Vol. 4. Electrophysiology and Microinjection. P.M. Conn, editor. Academic Press, Inc., San Diego, CA. 428-456.
33. Kyte, J. 1995. Mechanism in Protein Chemistry. Garland Publishing, Inc., New York, NY. 461-519.
34. Lee, B.S., R.B. Gunn, and R.R. Kopito. 1991. Functional differences among nonerythroid anion exchangers expressed in a transfected human cell line. J. Biol. Chem. 266:11448-11454.
35. Leffler, J.E., and E. Grunwald. 1963. Rates and equilibria of organic reactions. John Wiley & Sons, New York, NY. 458 pp.
36. Machold, J., Y. Utkin, D. Kirsch, R. Kaufmann, V. Tsetlin, and F. Hucho. 1995a. Photolabeling reveals the proximity of the α-neurotoxin binding site to the M2 helix of the ion channel in the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 92:7282-7286.
37. Machold, J., C. Weise, Y. Utkin, V. Tsetlin, and F. Hucho. 1995b. The handedness of the subunit arrangement of the nicotinic acetylcholine receptor from Torpedo californica. Eur. J. Biochem. 234: 427-430.
38. Magleby, K.L., and C.F. Stevens. 1972. The effect of voltage on the time course of end-plate currents. J. Physiol. 223:151-171.
39. Milone, M., H.-L. Wang, K. Ohno, T. Fukudome, J.N. Pruitt, N. Bren, S.M. Sine, and A.G. Engel. 1997. Slow-channel myasthenic syndrome caused by enhanced activation, desensitization, and agonist binding affinity attributable to mutation in the M2 domain of the acetylcholine receptor α subunit. J. Neurosci. 17: 5651-5665.
40. Miyazawa, A., Y. Fujiyoshi, M. Stowell, and N. Unwin. 1999. Nicotinic acetylcholine receptor at 4.6 Å resolution: transverse tunnels in the channel wall. J. Mol. Biol. 288:765-786.
41. Monod, J., J. Wyman, and J.-P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88-118.
42. Naranjo, D., and P. Brehm. 1993. Modal shifts in acetylcholine receptor channel gating confer subunit-dependent desensitization. Science. 260:1811-1814.
43. A receptor channels formed by ∈ subunit-containing isoforms. Mol. Pharmacol. 1:168-178.
44. Neher, E., and J.H. Steinbach. 1978. Local anesthetics transiently block currents through single acetylcholine-receptor channels. J. Physiol. 277:153-176.
45. Ohno, K., D.O. Hutchinson, M. Milone, J.M. Brengman, C. Bouzat, S.M. Sine, and A.G. Engel. 1995. Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 domain of the ∈ subunit. Proc. Natl. Acad. Sci. USA. 92:758-762.
46. Qin, F., A. Auerbach, and F. Sachs. 1996. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70:264-280.
47. Qin, F., A. Auerbach, and F. Sachs. 1997. Maximum likelihood estimation of aggregated Markov processes. Proc. R. Soc. Lond. B Biol. Sci. 264:375-383.
48. Rabiner, L.R., J.G. Wilpon, and B.H. Juang. 1986. A segmental-k-means training procedure for connected word recognition. AT&T Tech J. 65:21-31.
49. + channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for flickers. J. Gen. Physiol. 111:751-780.
50. Roux, B., and R. Sauvé. 1985. A general solution to the time interval omission problem applied to single channel analysis. Biophys. J. 48:149-158.
51. Salamone, F.N., M. Zhou, and A. Auerbach. 1999. A re-examination of adult mouse nicotinic acetylcholine receptor channel activation kinetics. J. Physiol. 516:315-330.
52. Schoepfer, R., W.G. Conroy, P. Whiting, M. Gore, and J. Lindstrom. 1990. Brain α-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron. 5:35-48.
53. Sine, S.M. 1993. Molecular dissection of subunit interfaces in the acetylcholine receptor: identification of residues that determine curare selectivity. Proc. Natl. Acad. Sci. USA. 90:9436-9440.
54. Skinner, M.M., and T.C. Terwilliger. 1996. Potential use of additivity of mutational effects in simplifying protein engineering. Proc. Natl. Acad. Sci. USA. 93:10753-10757.
55. Swope, S.L., S.J. Moss, L.A. Raymond, and R.L. Huganir. 1999. Regulation of ligand-gated ion channels by protein phosphorylation. Adv. Second Messenger Phosphoprotein Res. 33:49-78.
56. Valenzuela, C.F., P. Weign, J. Yguerabide, and D.A. Johnson. 1994. Transverse distance between the membrane and the agonist binding sites on the Torpedo acetylcholine receptor: a fluorescence study. Biophys. J. 66:674-682.
57. Verrall, S., and Z.H. Hall. 1992. The N-terminal domains of acetylcholine receptor subunits contain recognition signals for the initial steps of receptor assembly. Cell. 68:23-31.
58. Villarroel, A., S. Herlitze, V. Witzemann, M. Koenen, and B. Sakmann. 1992. Asymmetry of the rat acetylcholine receptor subunits in the narrow region of the pore. Proc. R. Soc. Lond. B Biol. Sci. 249:317-324.
59. Wells, J.A. 1990. Additivity of mutational effects in proteins. Biochemistry. 37:8509-8517.
60. Zhang, H., and A. Karlin. 1998. Contribution of the β subunit M2 segment to the ion-conducting pathway of the acetylcholine receptor. Biochemistry. 37:7952-7964.
61. Zhou, M., A.G. Engel, and A. Auerbach. 1999a. Serum choline activates mutant acetylcholine receptors that cause slow channel congenital myasthenic syndromes. Proc. Natl. Acad. Sci. USA. 96: 10466-10471.
62. Zhou, M., C. Grosman, and A. Auerbach. 1999b. Single channel properties of the ∈-less acetylcholine receptor channel. Biophys. J. 76:A371. (Abstr.)