Allosteric activation mechanism of the α1β2γ2 γ-aminobutyric acid type A receptor revealed by mutation of the conserved M2 leucine

Biophysical Journal

Volumn 77, Issue 5, 1999, Pages 2542-2551

  Chang, Yongchang ^a   Weiss, David S ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BICUCULLINE; COMPLEMENTARY DNA; COMPLEMENTARY RNA; ION CHANNEL; LEUCINE; PICROTOXIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CENTRAL NERVOUS SYSTEM; DOSE RESPONSE; NEUROTRANSMISSION; NONHUMAN; OOCYTE; RAT; SITE DIRECTED MUTAGENESIS; VOLTAGE CLAMP; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0032728861     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77089-X     Document Type: Article

References (56)

1. Akabas, H., M. D. Stauffer, A. M. Xu, and A. Karlin. 1992. Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science. 258:307-310.
2. Akabas, M., C. Kaufmann, P. Archdeacon, and A. Karlin. 1994. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the a subunit. Neuron. 13:919-927.
3. Amin, J., I. Dickerson, and D. S. Weiss. 1994. The agonist binding site of the γ-aminobutyric acid type A channel is not formed by the extracellular cysteine loop. Mol. Pharmacol. 45:317-323.
4. A receptor needs two homologous domains of the β-subunit for activation by GABA but not by pentobarbital. Nature. 366:565-569.
5. 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. (Lond.). 494:155-170.
6. A receptor: the receptor/channel superfamily. Trends Neurosci. 10:502-509.
7. Changeux, J.-P., and S. J. Edelstein. 1998. Allosteric receptors after 30 years. Neuron. 21:959-980.
8. A receptor. J. Neurosci. 16:5415-5424.
9. Chang, Y., and D. S. Weiss. 1998. Substitutions of the highly conserved M2 leucine create spontaneously opening ρ1 γ-aminobutyric acid receptors. Mol. Pharmacol. 53:511-523.
10. Colquhoun, D. 1973. The relation between classical and cooperative models for drug action. In Drug Receptors. Macmillan, London. 149-182.
11. Cooper, E., S. Couturier, and M. Ballivet. 1991. Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature. 350:235-238.
12. Cully, D. F., D. K. Vassilatis, K. K. Liu, P. S. Paress, L. H. Van der Ploeg, J. M. Schaeffer, and J. P. Arena. 1994. Cloning of an avermectinsensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature. 371:707-711.
13. Cutting, G. R., L. Lu, B. F. O'Hara, L. M. Kasch, C. Montrose-Rafizadeh, D. M. Donovan, S. Shimada, S. E. Antonarakis, W. B. Guggino, G. R. Uhl, and H. H. Kazazian. 1991. Cloning of the γ-aminobutyric acid (GABA) ρ1 cDNA: a GABA receptor subunit highly expressed in the retina. Proc. Natl. Acad. Sci. USA. 88:2673-2677.
14. Del Castillo, J., and B. Katz. 1957. Interaction at end-plate receptors between different choline derivatives. Proc. R. Soc. Lond. B. 146: 369-381.
15. Edelstein, S. J., and J.-P. Changeux. 1996. Allosteric proteins after thirty years: the binding and state functions of the neuronal α7 nicotinic acetylcholine receptors. Experientia. 52:1083-1090.
16. Enz, R., and J. Bormann. 1995. A single point mutation decreases picrotoxinin sensitivity of the human GABA receptor ρ1 subunit. Neuroreport. 6:1569-1572.
17. Filatov, G., and M. White. 1995. The role of conserved leucines in the M2 domain of the acetylcholine receptor in channel gating. Mol. Pharmacol. 48:379-384.
18. French-Constant, R. H., T. A. Rocheleau, J. C. Steichen, and A. E. Chalmers. 1993. A point mutation in a Drosopnila GABA receptor confers insecticide resistance. Nature. 363:449-451.
19. Garret, M., L. Bascles, E. Boue-Grabot, P. Sartor, G. Charron, B. Bloch, and R. F. Margolskee. 1997. An mRNA encoding a putative GABA-gated chloride channel is expressed in the human cardiac conduction system. J. Neurochem. 68:1382-1389.
20. Gurley, D., J. Amin, P. C. Ross, D. S. Weiss, and G. White. 1995. Point mutations in the M2 rregion of the α, β or γ subunit of the GABAchannel that abolish block by picrotoxin. Receptors Channels. 3:13-20.
21. A receptor subunit in tissues of the reproductive system. J. Biol. Chem. 272: 15346-15350.
22. Jackson, M. B. 1984. Spontaneous openings of the acetylcholine receptor channel. Proc. Natl. Acad. Sci. USA. 81:3901-3904.
23. Jackson, M. B. 1986. Kinetics of unliganded acetylcholine receptor channel gating. Biophys. J. 49:663-672.
24. Johnston, G. A. R. 1986. Multiplicity of GABA receptors. In Benzodiazepine/GABA Receptors and Chloride Channels. Receptor Biochemistry and Methodology. O. R. W.O. R. W. and J. C. Venter, editors. Alan R. Liss, New York.
25. Karlin, A. 1967. On the application of "a plausible model" of allosteric proteins to the receptor for acetylcholine. J. Theor. Biol. 16:306-320.
26. A receptors. Neuron. 3:745-753.
27. Labarca, C., M. 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.
28. Langosch, D., L. Thomas, and H. Betz. 1988. Conserved quaternary structure of ligand-gated ion channels: the postsynaptic glycine receptor is a pentamer. Proc. Natl. Acad. Sci. USA. 85:7394-7398.
29. 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.
30. Monod, J., J. Wyman, and J. P. Changeux. 1965. On the nature of allosteric proteins: a plausible model. J. Mol. Biol. 12:88-118.
31. A receptor determined by electron microscopic image analysis. J. Neurochem. 62:815-818.
32. Noda, M., H. Takahashi, T. Tanabe, M. Toyosato, Y. Furutani, T. Hirose, M. Asai, S. Inayama, T. Miyata, and S. Numa. 1982. Primary structure of alpha subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature. 299:793-797.
33. A receptors. FASEB J. 4:1469-1480.
34. Pan, Z.-H., D. Zhang, X. Zhang, and S. A. Lipton. 1997. Agonist-induced closure of constitutively open γ-aminobutyric acid channels with mutated domains. Proc. Natl. Acad. Sci. USA. 94:6490-6495.
35. Polenzani, L., R. M. Woodward, and R. Miledi. 1991. Expression of mammalian γ-aminobutyric acid receptors with distinct pharmacology in Xenopus oocytes. Neurobiology. 88:4318-4322.
36. Pribilla, I., T. Takagi, D. Langosch, J. Bormann, and H. Betz. 1992. The atypical M2 segment of the β subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J. 11:4305-4311.
37. A receptor subunit for benzodiazepine pharmacology. Nature. 338: 582-586.
38. Revah, F., D. Bertrand, J.-L. Gaizi, 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.
39. Sanger, F. S., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
40. Schofield, P. R., M. G. Darlison, N. Fujita, D. R. Burt, F. A. Stephenson, H. Rodriguez, L. M. Rhee, J. Ramachandran, V. Reale, T. A. Glencorse, P. H. Seeburg, and E. A. Barnard. 1987. Sequence and functional expression of the GABA-A receptor shows a ligand-gated receptor superfamily. Nature. 328:221-227.
41. Sigel, E., R. Baur, S. Kellenberger, and P. Malherbe. 1992. Point mutations affecting antagonist affinity and agonist dependent gating of GABAa receptor channels. EMBO J. 11:2017-2023.
42. A receptors on channel function. Neuron. 5:703-711.
43. Sivilotti, L., and A. Nistri. 1989. Pharmacology of a novel effect of γ-aminobutyric acid on the frog optic tectum in vitro. Eur. J. Pharmacol. 164:205-212.
44. A α1β1 receptors. J. Membr. Biol. 154:11-21.
45. A receptor. J. Neurosci. 17:625-634.
46. Unwin, N. 1995. Acetylcholine receptor channel imaged in the open state. Nature. 373:37-43.
47. a receptors depend upon subunit composition. Neuron. 4:919-928.
48. Wang, T.-L., A. S. Hackam, W. B. Guggino, and G. R. Cutting. 1995. A single amino acid in γ-aminobutyric acid ρ1 receptors affects competitive and non-competitive components of picrotoxin inhibition. Proc. Natl. Acad. Sci. USA. 92:11751-11755.
49. White, B., and J. Cohen. 1992. Agonist-induced changes in the structure of the acetylcholine receptor M2 regions revealed by photoincorporation of an uncharged nicotinic noncompetitive antagonist. J. Biol. Chem. 267: 15770-15783.
50. A receptor subunit conferring atypical functional properties. J. Neurosci. 17:5027-5037.
51. Wilson, G. G., and A. Karlin. 1998. The location of the gate in the acetylcholine receptor channel. Neuron. 20:1269-1281.
52. A receptor α1 subunit. J. Gen. Physiol. 107:195-205.
53. A receptor channel-lining residues probed in cysteine mutants. Biophys. J. 69:1858-1867.
54. Yakel, J. L., A. Lagrutta, J. P. Adelman. and R. A. North. 1993. Single amino acid substitution affects desensitization of the 5-hydroxytryptamine type 3 receptor expressed in Xenopus oocytes. Proc. Natl. Acad. Sci. USA. 90:5030-5033.
55. Zhang, D., Z.-H. Pan, A. D. Brideau, and S. A. Lipton. 1995. Cloning of a γ-aminobutyric acid type C receptor subunit in rat retina with a methionine residue criticial for picrotoxinin channel block. Proc. Natl. Acad. Sci. USA. 92:11756-11760.
56. Zhang, H.-G., R. H. Ffrench-Constant, and M. B. Jackson. 1994. A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J. Physiol. (Lond.). 479:65-75.