Charged residues in the α1 and β2 pre-M1 regions involved in GABAA receptor activation

Journal of Neuroscience

Volumn 26, Issue 7, 2006, Pages 2031-2040

  Mercado, Jose ^a   Czajkowski, Cynthia ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Allosteric protein; Electrostatic interactions; GABA; GabaA receptor; Ligand gated ion channel; Pre M1 region; Substituted cysteine accessibility method

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; CYSTEINE; MUSCIMOL; REAGENT; RECEPTOR SUBUNIT; THIOL DERIVATIVE; TRITIUM; UNCLASSIFIED DRUG; COMPLEMENTARY DNA; PROTEIN SUBUNIT;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CHANNEL GATING; CHEMICAL MODIFICATION; CONTROLLED STUDY; ELECTRICITY; MUTATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RECEPTOR BINDING; WILD TYPE; XENOPUS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG EFFECT; FEMALE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RAT; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; DNA, COMPLEMENTARY; FEMALE; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; OOCYTES; PROTEIN SUBUNITS; RATS; RECEPTORS, GABA-A; XENOPUS LAEVIS;

EID: 33644520967     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4555-05.2006     Document Type: Article

References (46)

1. Absalom NL, Lewis TM, Kaplan W, Pierce KD, Schofield PR (2003) Role of charged residues in coupling ligand binding and channel activation in the extracellular domain of the glycine receptor. J Biol Chem 278:50151-50157.
2. Amin J, Weiss DS (1993) GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital. Nature 366:565-569.
3. A receptor: three residues are required for allosteric coupling. J Neurosci 19:10213-10220.
4. Boileau AJ, Kucken AM, Evers AR, Czajkowski C (1998) Molecular dissection of benzodiazepine binding and allosteric coupling using chimeric gamma-aminobutyric acidA receptor subunits. Mol Pharmacol 53:295-303.
5. A receptor: evidence for a β-strand. J Neurosci 19:4847-4854.
6. 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.
7. 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.
8. Castaldo P, Stefanoni P, Miceli F, Coppola G, Miraglia Del Giudice E, Bellini G, Pascotto A, Trudell JR, Harrison NL, Annunziato L, Taglialatela M (2004) A novel hyperekplexia-causing mutation in the pre-transmembrane segment 1 of the human glycine receptor alpha 1 subunit reduces membrane expression and impairs gating by agonists. J Biol Chem 279:25598-25606.
9. Celie PH, 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.
10. Chakrapani S, Bailey TD, Auerbach A (2004) Gating dynamics of the acetylcholine receptor extracellular domain. J Gen Physiol 123:341-356.
11. Cheung M, Akabas MH (1997) Locating the anion-selectivity filter of the cystic fibrosis transmembrane conductance regulator (CFTR) chloride channel. J Gen Physiol 109:289-299.
12. Cromer BA, Morton CJ, Parker MW (2002) Anxiety over GABA(A) receptor structure relieved by AChBP. Trends Biochem Sci 27:280-287.
13. Dennis M, Giraudat J, Kotzyba-Hibert F, Goeldner M, Hirth C, Chang JY, Lazure C, Chretien M, Changeux JP (1988) Amino acids of the Torpedo marmorata acetylcholine receptor alpha subunit labeled by a photoaffinity ligand for the acetylcholine binding site. Biochemistry 27:2346-2357.
14. Galzi JL, Revah F, Bouet F, Menez A, Goeldner M, Hirth C, Changeux JP (1991a) Allosteric transitions of the acetylcholine receptor probed at the amino acid level with a photolabile cholinergic ligand. Proc Natl Acad Sci USA 88:5051-5055.
15. Galzi JL, Bertrand D, Devillers-Thiery A, Revah F, Bertrand S, Changeux JP (1991b) Functional significance of aromatic amino acids from three peptide loops of the alpha 7 neuronal nicotinic receptor site investigated by site-directed mutagenesis. FEBS Lett 294:198-202.
16. Grosman C, Zhou M, Auerbach A (2000a) Mapping the conformational wave of acetylcholine receptor channel gating. Nature 403:773-776.
17. Grosman C, Salamone FN, Sine SM, Auerbach A (2000b) The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J Gen Physiol 116:327-340.
18. Gruia AD, Fischer S, Smith JC (2003) Molecular dynamics simulation reveals a surface salt bridge forming a kinetic trap in unfolding of truncated Staphylococcal nuclease. Proteins 50:507-515.
19. Henchman RH, Wang HL, Sine SM, Taylor P, McCammon JA (2005) Ligand-induced conformational change in the alpha7 nicotinic receptor ligand binding domain. Biophys J 88:2564-2576.
20. Holden JH, Czajkowski C (2002) Different residues in the GABA(A) receptor alpha 1T60-alpha 1K70 region mediate GABA and SR-95531 actions. J Biol Chem 277:18785-18792.
21. Hu XQ, Zhang L, Stewart RR, Weight FF (2003) Arginine 222 in the pretransmembrane domain 1 of 5-HT3A receptors links agonist binding to channel gating. J Biol Chem 278:46583-46589.
22. Kao PN, Dwork AJ, Kaldany RR, Silver ML, Wideman J, Stein S, Karlin A (1984) Identification of the alpha subunit half-cystine specifically labeled by an affinity reagent for the acetylcholine receptor binding site. J Biol Chem 259:11662-11665.
23. Karlin A, Akabas MH (1998) Substituted-cysteine accessibility method. Methods Enzymol 293:123-145.
24. Kash TL, Jenkins A, Kelley JC, Trudell JR, Harrison NL (2003) Coupling of agonist binding to channel gating in the GABA(A) receptor. Nature 421:272-275.
25. Kash TL, Dizon MJ, Trudell JR, Harrison NL (2004) Charged residues in the beta2 subunit involved in GABAA receptor activation. J Biol Chem 279:4887-4893.
26. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486.
27. + channel determined by construction of multimeric cDNAs. Neuron 9:861-871.
28. Mishina M, Tobimatsu T, Imoto K, Tanaka K, Fujita Y, Fukuda K, Kurasaki M, Takahashi H, Morimoto Y, Hirose T, Inayama S, Takahashi T, Kuno M, Numa S (1985) Location of functional regions of acetylcholine receptor alpha-subunit by site-directed mutagenesis. Nature 313:364-369.
29. Miyazawa A, Fujiyoshi Y, Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 424:949-955.
30. Mukhtasimova N, Free C, Sine SM (2005) Initial coupling of binding to gating mediated by conserved residues in the muscle nicotinic receptor. J Gen Physiol 126:23-39.
31. Pascual JM, Karlin A (1998) State-dependent accessibility and electrostatic potential in the channel of the acetylcholine receptor. Inferences from rates of reaction of thiosulfonates with substituted cysteines in the M2 segment of the alpha subunit. J Gen Physiol 111:717-739.
32. Powell JMD (1977) Restart procedures for the conjugate gradient method. Math Program 12:241-251.
33. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1988) Numerical recipes in C: the art of scientific computing. In: Minimization and maximization of functions, Ed 1, Chap 10, pp 301-327. Cambridge, UK: Cambridge UP.
34. Rajendra S, Vandenberg RJ, Pierce KD, Cunningham AM, French PW, Barry PH, Schofield PR (1995) The unique extracellular disulfide loop of the glycine receptor is a principal ligand binding element. EMBO J 14:2987-2998.
35. Robertson GA, Warmke JM, Ganetzky B (1996) Potassium currents expressed from Drosophila and mouse eag cDNAs in Xenopus oocytes. Neuropharmacology 35:841-850.
36. Ruiz-Gomez A, Morato E, Garcia-Calvo M, Valdivieso F, Mayor Jr F (1990) Localization of the strychnine binding site on the 48-kilodalton subunit of the glycine receptor. Biochemistry 29:7033-7040.
37. Schreiber G, Fersht AR (1995) Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J Mol Biol 248:478-486.
38. Sheldahl C, Harvey SC (1999) Molecular dynamics on a model for nascent high-density lipoprotein: role of salt bridges. Biophys J 76:1190-1198.
39. Stauffer DA, Karlin A (1994) Electrostatic potential of the acetylcholine binding sites in the nicotinic receptor probed by reactions of binding-site cysteines with charged methanethiosulfonates. Biochemistry 33:6840-6849.
40. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol 346:967-989.
41. Unwin N, Miyazawa A, Li J, Fujiyoshi Y (2002) Activation of the nicotinic acetylcholine receptor involves a switch in conformation of the alpha subunits. J Mol Biol 319:1165-1176.
42. Vandenberg RJ, French CR, Barry PH, Shine J, Schofield PR (1992a) Antagonism of ligand-gated ion channel receptors: two domains of the glycine receptor alpha subunit form the strychnine-binding site. Proc Natl Acad Sci USA 89:1765-1769.
43. Vandenberg RJ, Handford CA, Schofield PR (1992b) Distinct agonist- and antagonist-binding sites on the glycine receptor. Neuron 9:491-496.
44. Vicente-Agullo F, Rovira JC, Sala S, Sala F, Rodriguez-Ferrer C, Campos-Caro A, Criado M, Ballesta JJ (2001) Multiple roles of the conserved key residue arginine 209 in neuronal nicotinic receptors. Biochemistry 40:8300-8306.
45. Wagner DA, Czajkowski C (2001) Structure and dynamics of the GABA binding pocket: a narrowing cleft that constricts during activation. J Neurosci 21:67-74.
46. Yang N, George Jr AL, Horn R (1997) Probing the outer vestibule of a sodium channel voltage sensor. Biophys J 73:2260-2268.