Charge and geometry of residues in the loop 2 β hairpin differentially affect agonist and ethanol sensitivity in glycine receptors

Journal of Pharmacology and Experimental Therapeutics

Volumn 341, Issue 2, 2012, Pages 543-551

  Perkins, Daya I ^a,c   Trudell, James R ^b   Asatryan, Liana ^a   Davies, Daryl L ^a   Alkana, Ronald L ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c ALLERGAN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALCOHOL; ASPARTIC ACID; CELL PROTEIN; GLUTAMIC ACID; GLYCINE RECEPTOR; GLYCINE RECEPTOR AGONIST; ION CHANNEL;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BETA HAIRPIN; BINDING AFFINITY; BINDING SITE; BIOTINYLATION; CELL POLARITY; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ETHANOL SENSITIVITY; FEEDBACK SYSTEM; FEMALE; GEOMETRY; IMMUNOBLOTTING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; OOCYTE; PHYSICAL CHEMISTRY; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; RECEPTOR BINDING; RESIDUE ANALYSIS; SENSITIVITY ANALYSIS; SENSITIVITY AND SENSIBILITY; STATIC ELECTRICITY; WILD TYPE; XENOPUS LAEVIS;

ALANINE; ANIMALS; ASPARTIC ACID; ETHANOL; FEMALE; GLUTAMIC ACID; GLYCINE; HUMANS; ION CHANNEL GATING; ION CHANNELS; MUTATION; OOCYTES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, GLYCINE; STATIC ELECTRICITY; XENOPUS LAEVIS;

EID: 84859951743     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.190942     Document Type: Article

References (40)

1. Baenziger JE and Corringer PJ (2011) 3D structure and allosteric modulation of the transmembrane domain of pentameric ligand-gated ion channels. Neuropharmacology 60:116-125.
2. Bertaccini EJ, Wallner B, Trudell JR, and Lindahl E (2010) Modeling anesthetic binding sites within the glycine α one receptor based on prokaryotic ion channel templates: the problem with TM4. J Chem Inf Model 50:2248-2255.
3. Bocquet N, Nury H, Baaden M, Le Poupon C, Changeux JP, Delarue M, and Corringer PJ (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457:111-114.
4. Castaldo P, Stefanoni P, Miceli F, Coppola G, Del Giudice EM, Bellini G, Pascotto A, Trudell JR, Harrison NL, Annunziato L, et al. (2004) A novel hyperekplexia-causing mutation in the pre-transmembrane segment 1 of the human glycine receptor α1 subunit reduces membrane expression and impairs gating by agonists. J Biol Chem 279:25598-25604. (Pubitemid 38756821)
5. Cederholm JM, Absalom NL, Sugiharto S, Griffith R, Schofield PR, and Lewis TM (2010) Conformational changes in extracellular loop 2 associated with signal transduction in the glycine receptor. J Neurochem 115:1245-1255.
6. Chen ZW, Chang CS, Leil TA, Olcese R, and Olsen RW (2005) GABAA receptor-associated protein regulates GABAA receptor cell-surface number in Xenopus laevis oocytes. Mol Pharmacol 68:152-159. (Pubitemid 41002954)
7. Cheng MH, Cascio M, and Coalson RD (2007) Homology modeling and molecular dynamics simulations of the α1 glycine receptor reveals different states of the channel. Proteins 68:581-593. (Pubitemid 46981950)
8. Crawford DK, Perkins DI, Trudell JR, Bertaccini EJ, Davies DL, and Alkana RL (2008) Roles for loop 2 residues of α1 glycine receptors in agonist activation. J Biol Chem 283:27698-27706.
9. Crawford DK, Trudell JR, Bertaccini EJ, Li K, Davies DL, and Alkana RL (2007) Evidence that ethanol acts on a target in loop 2 of the extracellular domain of α1 glycine receptors. J Neurochem 102:2097-2109. (Pubitemid 47329273)
10. Davies DL, Crawford DK, Trudell JR, Mihic SJ, and Alkana RL (2004) Multiple sites of ethanol action in α1 and α2 glycine receptors suggested by sensitivity to pressure antagonism. J Neurochem 89:1175-1185. (Pubitemid 38715835)
11. Davies DL, Trudell JR, Mihic SJ, Crawford DK, and Alkana RL (2003) Ethanol potentiation of glycine receptors expressed in Xenopus oocytes antagonized by increased atmospheric pressure. Alcohol Clin Exp Res 27:743-755. (Pubitemid 36583356)
12. Grosman C, Zhou M, and Auerbach A (2000) Mapping the conformational wave of acetylcholine receptor channel gating. Nature 403:773-776. (Pubitemid 30111838)
13. Hibbs RE and Gouaux E (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474:54-60.
14. Karlin A and Akabas MH (1998) Substituted-cysteine accessibility method. Methods Enzymol 293:123-145. (Pubitemid 29342485)
15. Kash TL, Jenkins A, Kelley JC, Trudell JR, and Harrison NL (2003) Coupling of agonist binding to channel gating in the GABAA receptor. Nature 421:272-275. (Pubitemid 36139131)
16. Kash TL, Kim T, Trudell JR, and Harrison NL (2004) Evaluation of a proposed mechanism of ligand-gated ion channel activation in the GABAA and glycine receptors. Neurosci Lett 371:230-234. (Pubitemid 39440777)
17. Lynch JW (2004) Molecular structure and function of the glycine receptor chloride channel. Physiol Rev 84:1051-1095.
18. Mascia MP, Machu TK, and Harris RA (1996a) Enhancement of homomeric glycine receptor function by long-chain alcohols and anaesthetics. Br J Pharmacol 119:1331-1336. (Pubitemid 26402009)
19. Mascia MP, Mihic SJ, Valenzuela CF, Schofield PR, and Harris RA (1996b) A single amino acid determines differences in ethanol actions on strychnine-sensitive glycine receptors. Mol Pharmacol 50:402-406. (Pubitemid 26265146)
20. Meera P, Olsen RW, Otis TS, and Wallner M (2010) Alcohol- and alcohol antagonist-sensitive human GABAA receptors: tracking δ subunit incorporation into functional receptors. Mol Pharmacol 78:918-924.
21. Mihic SJ, Ye Q, Wick MJ, Koltchine VV, Krasowski MD, Finn SE, Mascia MP, Valenzuela CF, Hanson KK, Greenblatt EP, et al. (1997) Sites of alcohol and volatile anaesthetic action on GABAA and glycine receptors. Nature 389:385-389. (Pubitemid 27415220)
22. Mody I, Glykys J, and Wei W (2007) A new meaning for "Gin & Tonic": tonic inhibition as the target for ethanol action in the brain. Alcohol 41:145-153. (Pubitemid 46962951)
23. Molander A, Lidö HH, Löf E, Ericson M, and Söderpalm B (2007) The glycine reuptake inhibitor Org 25935 decreases ethanol intake and preference in male wistar rats. Alcohol Alcohol 42:11-18. (Pubitemid 46062634)
24. Molander A and Söderpalm B (2005) Accumbal strychnine-sensitive glycine receptors: an access point for ethanol to the brain reward system. Alcohol Clin Exp Res 29:27-37. (Pubitemid 40129208)
25. Murail S, Wallner B, Trudell JR, Bertaccini E, and Lindahl E (2011) Microsecond simulations indicate that ethanol binds between subunits and could stabilize an open-state model of a glycine receptor. Biophys J 100:1642-1650.
26. Nury H, Poitevin F, Van Renterghem C, Changeux JP, Corringer PJ, Delarue M, and Baaden M (2010) One-microsecond molecular dynamics simulation of channel gating in a nicotinic receptor homologue. Proc Natl Acad Sci U S A 107:6275-6280.
27. Nury H, Van Renterghem C, Weng Y, Tran A, Baaden M, Dufresne V, Changeux JP, Sonner JM, Delarue M, and Corringer PJ (2011) X-ray structures of general anaesthetics bound to a pentameric ligand-gated ion channel. Nature 469:428-431.
28. Olsen RW, Hanchar HJ, Meera P, and Wallner M (2007) GABAA receptor subtypes: the "one glass of wine" receptors. Alcohol 41:201-209. (Pubitemid 46964889)
29. Perkins DI, Trudell JR, Crawford DK, Alkana RL, and Davies DL (2008) Targets for ethanol action and antagonism in loop 2 of the extracellular domain of glycine receptors. J Neurochem 106:1337-1349.
30. Perkins DI, Trudell JR, Crawford DK, Alkana RL, and Davies DL (2010) Molecular targets and mechanisms for ethanol action in glycine receptors. Pharmacol Ther 127:53-65.
31. Perkins DI, Trudell JR, Crawford DK, Asatryan L, Alkana RL, and Davies DL (2009) Loop 2 structure in glycine and GABAA receptors plays a key role in determining ethanol sensitivity. J Biol Chem 284:27304-27314.
32. Pless SA and Lynch JW (2009) Magnitude of a conformational change in the glycine receptor β1-β2 loop is correlated with agonist efficacy. J Biol Chem 284:27370-27376.
33. Ponder JW and Richards FM (1987) Tertiary templates for proteins. Use of packing criteria in the enumeration of allowed sequences for different structural classes. J Mol Biol 193:775-791. (Pubitemid 17020078)
34. Purohit P and Auerbach A (2011) Glycine hinges with opposing actions at the acetylcholine receptor-channel transmitter binding site. Mol Pharmacol 79:351-359.
35. Rajendra S, Lynch JW, and Schofield PR (1997) The glycine receptor. Pharmacol Ther 73:121-146. (Pubitemid 27191614)
36. Santhakumar V, Wallner M, and Otis TS (2007) Ethanol acts directly on extrasynaptic subtypes of GABAA receptors to increase tonic inhibition. Alcohol 41:211-221. (Pubitemid 46970812)
37. Wallner M, Hanchar HJ, and Olsen RW (2003) Ethanol enhances α4β3δ and α6β3δ γ-aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci U S A 100:15218-15223. (Pubitemid 37518043)
38. Webb TI and Lynch JW (2007) Molecular pharmacology of the glycine receptor chloride channel. Curr Pharm Des 13:2350-2367. (Pubitemid 47317028)
39. Xiu X, Hanek AP, Wang J, Lester HA, and 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. (Pubitemid 41832228)
40. Zhu F and Hummer G (2010) Pore opening and closing of a pentameric ligand-gated ion channel. Proc Natl Acad Sci U S A 107:19814-19819.