α1F64 residue at GABAA receptor binding site is involved in gating by influencing the receptor flipping transitions

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3193-3209

  Szczot, Marcin ^a   Kisiel, Magdalena ^a   Czyzewska, Marta M ^a   Mozrzymas, Jerzy W ^a  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

Author keywords

Agonist binding; Desensitization; Receptor gating; aminobutyric acid

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHLORIDE ION; PHENYLALANINE; 4 AMINOBUTYRIC ACID; GABAERGIC RECEPTOR AFFECTING AGENT; LYSINE;

ARTICLE; BINDING KINETICS; BINDING SITE; CELL CULTURE; CHANNEL GATING; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; EVOKED RESPONSE; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; LIGAND BINDING; PATCH CLAMP TECHNIQUE; POINT MUTATION; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; SIMULATION; AGONIST BINDING; ANIMAL; CELL LINE; CHEMISTRY; COMPUTER SIMULATION; DESENSITIZATION; DOSE RESPONSE; DRUG EFFECT; GABAA RECEPTOR; GENETIC TRANSFECTION; GENETICS; KINETICS; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; RAT; RECEPTOR GATING; SITE DIRECTED MUTAGENESIS; Γ-AMINOBUTYRIC ACID;

AGONIST BINDING; DESENSITIZATION; GABAA RECEPTOR; RECEPTOR GATING; Γ-AMINOBUTYRIC ACID;

ANIMALS; BINDING SITES; CELL LINE, TRANSFORMED; COMPUTER SIMULATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; HUMANS; ION CHANNEL GATING; KINETICS; LYSINE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PATCH-CLAMP TECHNIQUES; PHENYLALANINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, GABA-A; TRANSFECTION;

EID: 84894466719     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2533-13.2014     Document Type: Article

References (75)

1. Absalom N, Eghorn LF, Villumsen IS, Karim N, Bay T, Olsen JV, Knudsen GM, Bräuner-Osborne H, Frølund B, Clausen RP, Chebib M, Wellendorph P (2012) α4βδ GABA(A) receptors are high-affinity targets for γ-hydroxybutyric acid (GHB). Proc Natl Acad Sci U S A 109:13404-13409. CrossRef Medline
2. Akk G (2002) Contributions of the non-alpha subunit residues (loop D) to agonist binding and channel gating in the muscle nicotinic acetylcholine receptor. J Physiol 544(Pt 3):695-705. Medline
3. Akk G, Li P, Bracamontes J, Wang M, Steinbach JH (2011) Pharmacology of structural changes at the GABA(A) receptor transmitter binding site. Br J Pharmacol 162:840-850. CrossRef Medline
4. 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. CrossRef Medline
5. Auerbach A (2005) Gating of acetylcholine receptor channels: Brownian motion across a broad transition state. Proc Natl Acad Sci U S A 102: 1408-1412. CrossRef Medline
6. Bafna PA, Jha A, Auerbach A (2009) Aromatic residues εTrp-55 and ΔTrp-57 and the activation of acetylcholine receptor channels. J Biol Chem 284:8582-8588. Medline
7. Bianchi MT, Macdonald RL (2001) Mutation of the 9́ leucine in the GABA(A) receptor gamma2L subunit produces an apparent decrease in desensitization by stabilizing open states without altering desensitized states. Neuropharmacology 41:737-744. CrossRef Medline
8. Bianchi MT, Macdonald RL (2003) Neurosteroids shift partial agonist activation of GABAA receptor channels from low-to high-efficacy gating patterns. J Neurosci 23:10934-10943. Medline
9. Bianchi MT, Botzolakis EJ, Haas KF, Fisher JL, Macdonald RL (2007) Microscopic kinetic determinants of macroscopic currents: insights from coupling and uncoupling of GABAA receptor desensitization and deactivation. J Physiol 584:769-787. CrossRef Medline
10. Boileau AJ, Newell JG, Czajkowski C (2002) GABA(A) receptor beta 2 Tyr97 and Leu99 line the GABA-binding site. Insights into mechanisms of agonist and antagonist actions. J Biol Chem 277:2931-2937. CrossRef Medline
11. Bouzat C (2012) New insights into the structural bases of activation of Cysloop receptors. J Physiol Paris 106:23-33. CrossRef Medline
12. Burzomato V, Beato M, Groot-Kormelink PJ, Colquhoun D, Sivilotti LG (2004) Single-channel behavior of heteromericα1β glycine receptors: an attempt to detect a conformational change before the channel opens. J Neurosci 24:10924-10940. CrossRef Medline
13. Carpenter TS, Lau EY, Lightstone FC (2012) A role for loop F in modulating GABA binding affinity in the GABA(A) receptor. J Mol Biol 422:310-323. CrossRef Medline
14. Cederholm JM, Schofield PR, Lewis TM (2009) Gating mechanisms in Cysloop receptors. Eur Biophys J 39:37-49. CrossRef Medline
15. Chang CS, Olcese R, Olsen RW (2003) A single M1 residue in the beta2 subunit alters channel gating of GABAA receptor in anesthetic modulation and direct activation. J Biol Chem 278:42821-42828. CrossRef Medline
16. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752. Medline
17. Colquhoun D (1998) Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br J Pharmacol 125:924-947. Medline
18. Colquhoun D, Hawkes AG (1982) On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Philos Trans R Soc Lond B Biol Sci 300:1-59. CrossRef Medline
19. Colquhoun D, Hawkes AG (1995) Desensitization of N-methyl-Daspartate receptors: a problem of interpretation. Proc Natl Acad SciU S A 92:10327-10329. CrossRef Medline
20. Colquhoun D, Lape R (2012) Perspectives on: conformational coupling in ion channels: allosteric coupling in ligand-gated ion channels. J Gen Physiol 140:599-612. CrossRef Medline
21. Cromer BA, Morton CJ, Parker MW (2002) Anxiety over GABA(A) receptor structure relieved by AChBP. Trends Biochem Sci 27:280-287. CrossRef Medline
22. Dalziel JE, Cox GB, Gage PW, Birnir B (2000) Mutating the highly conserved second membrane-spanning region 9́ leucine residue in the alpha(1) or beta(1) subunit produces subunit-specific changes in the function of human alpha(1)beta(1) gamma-aminobutyric acid(A) receptors. Mol Pharmacol 57:875-882. Medline
23. De Koninck Y, Mody I (1994) Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels. J Neurophysiol 71:1318-1335. Medline
24. Drafts BC, Fisher JL (2006) Identification of structures within GABAA receptor alpha subunits that regulate the agonist action of pentobarbital. J Pharmacol Exp Ther 318:1094-1101. CrossRef Medline
25. Feng HJ, Bianchi MT, Macdonald RL (2004) Pentobarbital differentially modulatesα1β3δ andα1β3γ2L GABAA receptor currents. Mol Pharmacol 66:988-1003. CrossRef Medline
26. Fisher JL (2004) A mutation in the GABAA receptor alpha 1 subunit linked to human epilepsy affects channel gating properties. Neuropharmacology 46:629-637. CrossRef Medline
27. Gay EA, Giniatullin R, Skorinkin A, Yakel JL (2008) Aromatic residues at position 55 of rat alpha7 nicotinic acetylcholine receptors are critical for maintaining rapid desensitization. J Physiol 586:1105-1115. Medline
28. Ghavanini AA, Isbasescu IM, Mathers DA, Puil E (2006) Optimizing fluctuation analysis of GABAAergic IPSCs for accurate unitary currents. J Neurosci Methods 158:150-156. CrossRef Medline
29. Gielen MC, Lumb MJ, Smart TG (2012) Benzodiazepines modulate GABAA receptors by regulating the preactivation step after GABA binding. J Neurosci 32:5707-5715. CrossRef Medline
30. Gingrich KJ, Burkat PM, Roberts WA (2009) Pentobarbital produces activation and block ofα1β2γ2S GABAA receptors in rapidly perfused whole cells and membrane patches: divergent results can be explained by pharmacokinetics. J Gen Physiol 133:171-188. CrossRef Medline
31. Goldschen-Ohm MP, Wagner DA, Jones MV (2011) Three arginines in the GABAA receptor binding pocket have distinct roles in formation and stability of agonist-versus antagonist-bound complexes. Mol Pharmacol 80:647-656. CrossRef Medline
32. Gonzales EB, Bell-Horner CL, Dibas MI, Huang RQ, Dillon GH (2008) Stoichiometric analysis of the TM2 6́ phenylalanine mutation on desensitization in alpha1beta2 and alpha1beta2gamma2 GABA A receptors. Neurosci Lett 431:184-189. CrossRef Medline
33. 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. CrossRef Medline
34. Im HK, Im WB, Von Voigtlander PF, Carter DB, Murray BH, Jacobsen EJ (1996) Characterization of U-101017 as a GABA(A) receptor ligand of dual functionality. Brain Res 714:165-168. CrossRef Medline
35. Jadey S, Auerbach A (2012) An integrated catch-and-hold mechanism activates nicotinic acetylcholine receptors. J Gen Physiol 140:17-28. CrossRef Medline
36. Jonas P (1995) Fast application of agonists to isolated membrane patches. In: Single-channel recording (Sakmann B, Neher E, eds), pp 231-243. New York: Plenum.
37. Jones MV, Westbrook GL (1995) Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15:181-191. CrossRef Medline
38. Jones MV, Sahara Y, Dzubay JA, Westbrook GL (1998) Defining affinity with the GABAA receptor. J Neurosci 18:8590-8604. Medline
39. Jones MV, Jonas P, Sahara Y, Westbrook GL (2001) Microscopic kinetics and energetics distinguish gabaa receptor agonists from antagonists. Biophys J 81:2660-2670. CrossRef Medline
40. Karlsson U, Druzin M, Johansson S (2011) Cl(+) concentration changes and desensitization of GABA(A) and glycine receptors. J Gen Physiol 138:609-626. CrossRef Medline
41. 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. CrossRef Medline
42. Keramidas A, Harrison NL (2010) The activation mechanism of alpha1beta2gamma2S and alpha3beta3gamma2S GABAA receptors. J Gen Physiol 135:59-75. CrossRef Medline
43. Keramidas A, Lynch JW (2013) An outline of desensitization in pentameric ligand-gated ion channel receptors. Cell Mol Life Sci 70:1241-1253. CrossRef Medline
44. Laha KT, Tran PN (2013) Multiple tyrosine residues at the GABA binding pocket influence surface expression and mediate kinetics of the GABAA receptor. J Neurochem 124:200-209. CrossRef Medline
45. Laha KT, Wagner DA (2011) A state-dependent salt-bridge interaction ex-ists across the beta/alpha intersubunit interface of the GABAA receptor. Mol Pharmacol 79:662-671. CrossRef Medline
46. Lape R, Colquhoun D, Sivilotti LG (2008) On the nature of partial agonism in the nicotinic receptor superfamily. Nature 454:722-727. Medline
47. Lape R, Plested AJ, Moroni M, Colquhoun D, Sivilotti LG (2012) The α1K276E startle disease mutation reveals multiple intermediate states in the gating of glycine receptors. J Neurosci 32:1336-1352. CrossRef Medline
48. Lema GM, Auerbach A (2006) Modes and models of GABA(A) receptor gating. J Physiol 572(Pt 1):183-200. Medline
49. Maconochie DJ, Zempel JM, Steinbach JH (1994) How quickly can GABAA receptors open? Neuron 12:61-71. CrossRef Medline
50. Mercado J, Czajkowski C (2008) Gamma-aminobutyric acid (GABA) and pentobarbital induce different conformational rearrangements in the GABA A receptor alpha1 and beta2 pre-M1 regions. J Biol Chem 283: 15250-15257. CrossRef Medline
51. Miller PS, Smart TG (2010) Binding, activation and modulation of Cysloop receptors. Trends Pharmacol Sci 31:161-174. CrossRef Medline
52. Moroni M, Biro I, Giugliano M, Vijayan R, Biggin PC, Beato M, Sivilotti LG (2011) Chloride ions in the pore of glycine and GABA channels shape the time course and voltage dependence of agonist currents. J Neurosci 31: 14095-14106. CrossRef Medline
53. Mortensen M, Kristiansen U, Ebert B, Frølund B, Krogsgaard-Larsen P, Smart TG (2004) Activation of single heteromeric GABA(A) receptor ion channels by full and partial agonists. J Physiol 557:389-413. CrossRef Medline
54. Mortensen M, Ebert B, Wafford K, Smart TG (2010) Distinct activities of GABA agonists at synaptic-and extrasynaptic-type GABAA receptors. J Physiol 588(Pt 8):1251-1268. CrossRef Medline
55. Mozrzymas JW, Barberis A, Michalak K, Cherubini E (1999) Chlorpromazine inhibits miniature GABAergic currents by reducing the binding and by increasing the unbinding rate of GABAA receptors. J Neurosci 19: 2474-2488. Medline
56. Mozrzymas JW, Barberis A, Mercik K, Zarnowska ED (2003a) Binding sites, singly bound states, and conformation coupling shape GABA-evoked currents. J Neurophysiol 89:871-883. Medline
57. Mozrzymas JW, Zarnowska ED, Pytel M, Mercik K (2003b) Modulation of GABAA receptors by hydrogen ions reveals synaptic GABA transient and a crucial role of the desensitization process. J Neurosci 23:7981-7992. Medline
58. Mukhtasimova N, Lee WY, Wang HL, Sine SM (2009) Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 459:451-454. CrossRef Medline
59. Muroi Y, Czajkowski C, Jackson MB (2006) Local and global ligandinduced changes in the structure of the GABA(A) receptor. Biochemistry 45:7013-7022. CrossRef Medline
60. Newell JG, McDevitt RA, Czajkowski C (2004) Mutation of glutamate 155 of the GABAA receptor β2 subunit produces a spontaneously open channel: a trigger for channel activation. J Neurosci 24:11226-11235. CrossRef Medline
61. 2 Tyr97. J Neurosci 27:886-892. CrossRef Medline
62. Petrini EM, Nieus T, Ravasenga T, Succol F, Guazzi S, Benfenati F, Barberis A (2011) Influence of GABAAR monoliganded states on GABAergic responses. J Neurosci 31:1752-1761. CrossRef Medline
63. Scheller M, Forman SA (2002) Coupled and uncoupled gating and desensitization effects by pore domain mutations inGABAA receptors. J Neurosci 22:8411-8421. Medline
64. Sigel E, Baur R, Kellenberger S, Malherbe P (1992) Point mutations affecting antagonist affinity and agonist dependent gating of GABAA receptor channels. EMBO J 11:2017-2023. Medline
65. Sigworth FJ (1980) The variance of sodium current fluctuations at the node of Ranvier. J Physiol 307:97-129. Medline
66. Smith GB, Olsen RW (1995) Functional domains of GABAA receptors. Trends Pharmacol Sci 16:162-168. CrossRef Medline
67. Spier AD, Lummis SC (2000) The role of tryptophan residues in the 5-hydroxytryptamine(3) receptor ligand binding domain. J Biol Chem 275:5620-5625. CrossRef Medline
68. Torres VI, Weiss DS (2002) Identification of a tyrosine in the agonist binding site of the homomeric rho1 gamma-aminobutyric acid (GABA) receptor that, when mutated, produces spontaneous opening. J Biol Chem 277:43741-43748. CrossRef Medline
69. Tran PN, Laha KT, WagnerDA (2011) Atight coupling between beta(2)Y97 and beta(2)F200 of the GABA(A) receptor mediates GABA binding. J Neurochem 119:283-293. CrossRef Medline
70. Twyman RE, Rogers CJ, Macdonald RL (1989) Differential regulation of gamma-aminobutyric acid receptor channels by diazepam and phenobarbital. Ann Neurol 25:213-220. CrossRef Medline
71. Ueno S, Bracamontes J, Zorumski C, Weiss DS, Steinbach JH (1997) Bicuculline and gabazine are allosteric inhibitors of channel opening of the GABAA receptor. J Neurosci 17:625-634. Medline
72. Venkatachalan SP, Czajkowski C (2008) A conserved salt bridge critical for GABA(A) receptor function and loop C dynamics. Proc Natl Acad Sci U S A 105:13604-13609. CrossRef Medline
73. Wagner DA, Czajkowski C, JonesMV (2004) An arginine involved inGABA binding and unbinding but not gating of the GABAA receptor. J Neurosci 24:2733-2741. CrossRef Medline
74. Xie Y, Cohen JB (2001) Contributions of Torpedo nicotinic acetylcholine receptor gamma Trp-55 and delta Trp-57 to agonist and competitive antagonist function. J Biol Chem 276:2417-2426. CrossRef Medline
75. Xiu X, Hanek AP, Wang J, Lester HA, Dougherty DA (2005) A unified view of the role of electrostatic interactions in modulating the gating of Cys loop receptors. J Biol Chem 280:41655-41666. CrossRef Medline