β Subunit M2-M3 loop conformational changes are uncoupled from α1 β glycine receptor channel gating: Implications for human hereditary hyperekplexia

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Shan, Qiang ^a   Han, Lu ^a   Lynch, Joseph W ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 BETA GLYCINE RECEPTOR; COMPLEMENTARY DNA; GLYCINE; GLYCINE RECEPTOR; UNCLASSIFIED DRUG; GLRB PROTEIN, HUMAN; GLYCINE RECEPTOR ALPHA1;

ALPHA CHAIN; ALPHA1 CHAIN; ANIMAL CELL; ARTICLE; BETA CHAIN; CELL STRAIN HEK293; CHANNEL GATING; CHANNELOPATHY; CHIMERA; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXTRACELLULAR DOMAIN; FEMALE; FLUOROMETRY; HUMAN; HYPEREKPLEXIA; M2 M3 LOOP; MUTAGENESIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; TRANSMEMBRANE DOMAIN; VOLTAGE CLAMP; XENOPUS LAEVIS; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; FLUORESCENCE; METABOLISM; MOLECULAR GENETICS; MUSCLE RIGIDITY; OOCYTE; PATHOPHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; FLUORESCENCE; FLUOROMETRY; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; MUSCLE RIGIDITY; OOCYTES; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RECEPTORS, GLYCINE; STRUCTURE-ACTIVITY RELATIONSHIP; XENOPUS;

EID: 81555205699     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028105     Document Type: Article

References (47)

1. Harvey RJ, Topf M, Harvey K, Rees MI, (2008) The genetics of hyperekplexia: more than startle! Trends Genet 24: 439-447.
2. Lynch JW, (2009) Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56: 303-309.
3. Chung SK, Vanbellinghen JF, Mullins JG, Robinson A, Hantke J, et al. (2010) Pathophysiological mechanisms of dominant and recessive GLRA1 mutations in hyperekplexia. J Neurosci 30: 9612-9620.
4. Lynch JW, (2004) Molecular Structure and Function of the Glycine Receptor Chloride Channel. Physiol Rev 84: 1051-1095.
5. Miller PS, Smart TG, (2010) Binding, activation and modulation of Cys-loop receptors. Trends Pharmacol Sci 3: 161-174.
6. Thompson AJ, Lester HA, Lummis SC, (2010) The structural basis of function in Cys-loop receptors. Q Rev Biophys pp. 1-51.
7. Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, et al. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411: 269-276.
8. Purohit P, Mitra A, Auerbach A, (2007) A stepwise mechanism for acetylcholine receptor channel gating. Nature 446: 930-933.
9. Grosman C, Zhou M, Auerbach A, (2000) Mapping the conformational wave of acetylcholine receptor channel gating. Nature 403: 773-776.
10. Bocquet N, Nury H, Baaden M, Le Poupon C, Changeux JP, et al. (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457: 111-114.
11. Bouzat C, Gumilar F, Spitzmaul G, Wang HL, Rayes D, et al. (2004) Coupling of agonist binding to channel gating in an ACh-binding protein linked to an ion channel. Nature 430: 896-900.
12. Hilf RJ, Dutzler R, (2009) Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 457: 115-118.
13. Hilf RJC, Dutzler R, (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452: 375-379.
14. Lee WY, Free CR, Sine SM, (2009) Binding to gating transduction in nicotinic receptors: Cys-loop energetically couples to Pre-M1 and M2-M3 regions. J Neurosci 29: 3189-3199.
15. Lummis SC, Beene DL, Lee LW, Lester HA, Broadhurst RW, et al. (2005) Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 438: 248-252.
16. Unwin N, (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol 346: 967-989.
17. Grudzinska J, Schemm R, Haeger S, Nicke A, Schmalzing G, et al. (2005) The beta subunit determines the ligand binding properties of synaptic glycine receptors. Neuron 45: 727-739.
18. Breitinger HG, Becker CM, (2002) The inhibitory glycine receptor- Simple views of a complicated channel. ChemBioChem 3: 1042-1052.
19. Engel AG, Ohno K, Sine SM, (2003) Sleuthing molecular targets for neurological diseases at the neuromuscular junction. Nat Rev Neurosci 4: 339-352.
20. Lynch JW, Rajendra S, Pierce KD, Handford CA, Barry PH, et al. (1997) Identification of intracellular and extracellular domains mediating signal transduction in the inhibitory glycine receptor chloride channel. Embo J 16: 110-120.
21. Macdonald RL, Gallagher MJ, Feng HJ, Kang J, (2004) GABA(A) receptor epilepsy mutations. Biochem Pharmacol 68: 1497-1506.
22. Shan Q, Nevin ST, Haddrill JL, Lynch JW, (2003) Asymmetric contribution of alpha and beta subunits to the activation of alphabeta heteromeric glycine receptors. J Neurochem 86: 498-507.
23. Wang Q, Pless SA, Lynch JW, (2010) Ligand- and subunit-specific conformational changes in the ligand-binding domain and the TM2-TM3 linker of α1β2γ2 GABA-A receptors *. J Biol Chem 285: 40373-40386.
24. 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.
25. Lewis TM, Sivilotti LG, Colquhoun D, Gardiner RM, Schoepfer R, et al. (1998) Properties of human glycine receptors containing the hyperekplexia mutation alpha1(K276E), expressed in Xenopus oocytes. J Physiol 507 (Pt 1): 25-40.
26. Grosman C, Salamone FN, Sine SM, Auerbach A, (2000) The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J Gen Physiol 116: 327-340.
27. Yifrach O, MacKinnon R, (2002) Energetics of pore opening in a voltage-gated K(+) channel. Cell 111: 231-239.
28. 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.
29. Pribilla I, Takagi T, Langosch D, Bormann J, Betz H, (1992) The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. Embo J 11: 4305-4311.
30. Shan Q, Haddrill JL, Lynch JW, (2001) A single beta subunit M2 domain residue controls the picrotoxin sensitivity of alphabeta heteromeric glycine receptor chloride channels. J Neurochem 76: 1109-1120.
31. Gandhi CS, Isacoff EY, (2005) Shedding light on membrane proteins. Trends Neurosci 28: 472-479.
32. Pless SA, Lynch JW, (2008) Illuminating the structure and function of Cys-loop receptors. Clin Exp Pharmacol Physiol 35: 1137-1142.
33. Pless SA, Dibas MI, Lester HA, Lynch JW, (2007) Conformational variability of the glycine receptor M2 domain in response to activation by different agonists. J Biol Chem 282: 36057-36067.
34. Dahan DS, Dibas MI, Petersson EJ, Auyeung VC, Chanda B, et al. (2004) A fluorophore attached to nicotinic acetylcholine receptor βM2 detects productive binding of agonist to the αδ site. Proc Nat Acad Sci USA 101: 10195-10200.
35. Beato M, Groot-Kormelink PJ, Colquhoun D, Sivilotti LG, (2004) The activation mechanism of alpha1 homomeric glycine receptors. J Neurosci 24: 895-906.
36. Gentet LJ, Clements JD, (2002) Binding site stoichiometry and the effects of phosphorylation on human alpha1 homomeric glycine receptors. J Physiol 544: 97-106.
37. Grewer C, (1999) Investigation of the alpha(1)-glycine receptor channel-opening kinetics in the submillisecond time domain. Biophys J 77: 727-738.
38. Lewis TM, Schofield PR, McClellan AM, (2003) Kinetic determinants of agonist action at the recombinant human glycine receptor. J Physiol 549: 361-374.
39. Burzomato V, Beato M, Groot-Kormelink PJ, Colquhoun D, Sivilotti LG, (2004) Single-channel behavior of heteromeric alpha1beta glycine receptors: an attempt to detect a conformational change before the channel opens. J Neurosci 24: 10924-10940.
40. Rayes D, De Rosa MJ, Sine SM, Bouzat C, (2009) Number and locations of agonist binding sites required to activate homomeric Cys-loop receptors. J Neurosci 29: 6022-6032.
41. Le Novere N, Corringer PJ, Changeux JP, (2002) The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J Neurobiol 53: 447-456.
42. Ortells MO, Lunt GG, (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends NeuroSci 18: 121-127.
43. Tsunoyama K, Gojobori T, (1998) Evolution of nicotinic acetylcholine receptor subunits. Mol Biol Evol 15: 518-527.
44. Liman ER, Tytgat J, Hess P, (1992) Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9: 861-871.
45. Shan Q, Lynch JW, (2010) Chimera construction using multiple-template-based sequential PCRs. J Neurosci Methods 193: 86-89.
46. Lynch JW, Han N-LR, Haddrill J, Pierce KD, Schofield PR, (2001) The Surface Accessibility of the Glycine Receptor M2-M3 Loop Is Increased in the Channel Open State. J Neurosci 21: 2589-2599.
47. Vogel N, Kluck CJ, Melzer N, Schwarzinger S, Breitinger U, et al. (2009) Mapping of disulfide bonds within the amino-terminal extracellular domain of the inhibitory glycine receptor. J Biol Chem 284: 36128-36136.