Structural basis for allosteric coupling at the membrane-protein interface in Gloeobacter violaceus ligand-gated ion channel (GLIC)

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 3013-3025

  Velisetty, Phanindra ^a   Chalamalasetti, Sreevatsa V ^a   Chakrapani, Sudha ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYS-LOOP RECEPTORS; GATING; ION CHANNELS; MEMBRANE RECONSTITUTION; SPECTROSCOPY;

ALCOHOLS; ALLOSTERIC REGULATION; CYANOBACTERIA; ION CHANNEL GATING; LIGAND-GATED ION CHANNELS; LIGANDS; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84893466183     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.523050     Document Type: Article

References (69)

1. Unwin, N., and Fujiyoshi, Y. (2012) Gating movement of acetylcholine receptor caught by plunge-freezing. J. Mol. Biol. 422, 617-634
2. Taly, A., Delarue, M., Grutter, T., Nilges, M., Le Novère, N., Corringer, P. J., and Changeux, J. P. (2005) Normal mode analysis suggests a quaternary twist model for the nicotinic receptor gating mechanism. Biophys. J. 88, 3954-3965
3. Hilf, R. J., and Dutzler, R. (2009) Structure of a potentially open state of a proton-activated pentameric ligand-gated ion channel. Nature 457, 115-118
4. Bocquet, N., Nury, H., Baaden, M., Le Poupon, C., Changeux, J. P., Delarue, M., and Corringer, P. J. (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457, 111-114
5. Hilf, R. J., and Dutzler, R. (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452, 375-379
6. Gonzalez-Gutierrez, G., Lukk, T., Agarwal, V., Papke, D., Nair, S. K., and Grosman, C. (2012) Mutations that stabilize the open state of the Erwinia chrisanthemi ligand-gated ion channel fail to change the conformation of the pore domain in crystals. Proc. Natl. Acad. Sci. U. S. A. 109, 6331-6336
7. Sauguet, L., Poitevin, F., Murail, S., Van Renterghem, C., Moraga-Cid, G., Malherbe, L., Thompson, A. W., Koehl, P., Corringer, P. J., Baaden, M., and Delarue, M. (2013) Structural basis for ion permeation mechanism in pentameric ligand-gated ion channels. EMBO J. 32, 728-741
8. Gonzalez-Gutierrez, G., and Grosman, C. (2010) Bridging the gap between structural models of nicotinic receptor superfamily ion channels and their corresponding functional states. J. Mol. Biol. 403, 693-705
9. Velisetty, P., and Chakrapani, S. (2012) Desensitization mechanism in prokaryotic ligand-gated ion channel. J. Biol. Chem. 287, 18467-18477
10. Parikh, R. B., Bali, M., and Akabas, M. H. (2011) Structure of the M2 transmembrane segment of GLIC, a prokaryotic Cys loop receptor homologue from Gloeobacter violaceus, probed by substituted cysteine accessibility. J. Biol. Chem. 286, 14098-14109
11. Nury, H., Van Renterghem, C., Weng, Y., Tran, A., Baaden, M., Dufresne, V., Changeux, J. P., Sonner, J. M., Delarue, M., and Corringer, P. J. (2011) X-ray structures of general anaesthetics bound to a pentameric ligandgated ion channel. Nature 469, 428-431
12. Howard, R. J., Murail, S., Ondricek, K. E., Corringer, P. J., Lindahl, E., Trudell, J. R., and Harris, R. A. (2011) Structural basis for alcohol modulation of a pentameric ligand-gated ion channel. Proc. Natl. Acad. Sci. U. S. A. 108, 12149-12154
13. Duret, G., Van Renterghem, C., Weng, Y., Prevost, M., Moraga-Cid, G., Huon, C., Sonner, J. M., and Corringer, P. J. (2011) Functional prokaryoticeukaryotic chimera from the pentameric ligand-gated ion channel family. Proc. Natl. Acad. Sci. U. S. A. 108, 12143-12148
14. Goyal, R., Salahudeen, A. A., and Jansen, M. (2011) Engineering a prokaryotic Cys-loop receptor with a third functional domain. J. Biol. Chem. 286, 34635-34642
15. Sine, S. M., and Engel, A. G. (2006) Recent advances in Cys-loop receptor structure and function. Nature 440, 448-455
16. Bartos, M., Corradi, J., and Bouzat, C. (2009) Structural basis of activation of Cys-loop receptors. The extracellular-transmembrane interface as a coupling region. Mol. Neurobiol. 40, 236-252
17. Dacosta, C. J., and Baenziger, J. E. (2013) Gating of pentameric ligandgated ion channels. Structural insights and ambiguities. Structure 21, 1271-1283
18. Bouzat, C., Bartos, M., Corradi, J., and Sine, S. M. (2008) The interface between extracellular and transmembrane domains of homomeric Cysloop receptors governs open-channel lifetime and rate of desensitization. J. Neurosci. 28, 7808-7819
19. Kash, T. L., Jenkins, A., Kelley, J. C., Trudell, J. R., and Harrison, N. L. (2003) Coupling of agonist binding to channel gating in the GABA (A) receptor. Nature 421, 272-275
20. Absalom, N. L., Lewis, T. M., Kaplan, W., Pierce, K. D., and Schofield, P. R. (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
21. Xiu, X., Hanek, A. P., Wang, J., Lester, H. A., and Dougherty, D. A. (2005) A unified view of the role of electrostatic interactions in modulating the gating of Cys loop receptors. J. Biol. Chem. 280, 41655-41666
22. Da Costa, C. J., and Baenziger, J. E. (2009) A lipid-dependent uncoupled conformation of the acetylcholine receptor. J. Biol. Chem. 284, 17819-17825
23. Heidmann, T., Sobel, A., Popot, J. L., and Changeux, J. P. (1980) Reconstitution of a functional acetylcholine receptor. Conservation of the conformational and allosteric transitions and recovery of the permeability response; role of lipids. Eur. J. Biochem. 110, 35-55
24. Barrantes, F. J. (2002) Lipid matters. Nicotinic acetylcholine receptor-lipid interactions (Review). Mol. Membr. Biol. 19, 277-284
25. Baier, C. J., Fantini, J., and Barrantes, F. J. (2011) Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor. Sci. Rep. 1, 69
26. Borghese, C. M., Henderson, L. A., Bleck, V., Trudell, J. R., and Harris, R. A. (2003) Sites of excitatory and inhibitory actions of alcohols on neuronal a2β4 nicotinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 307, 42-52
27. Williams, D. B., and Akabas, M. H. (1999) 7-Aminobutyric acid increases the water accessibility of M3 membrane-spanning segment residues in y-aminobutyric acid type A receptors. Biophys. J. 77, 2563-2574
28. Velisetty, P., Chalamalasetti, S. V., and Chakrapani, S. (2012) Conformational transitions underlying pore opening and desensitization in membrane-embedded Gloeobacter violaceus ligand-gated ion channel (GLIC). J. Biol. Chem. 287, 36864-36872
29. Hansen, S. B., Sulzenbacher, G., Huxford, T., Marchot, P., Taylor, P., and Bourne, Y. (2005) Structures of aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBOJ. 24, 3635-3646
30. Amadi, S. T., Koteiche, H. A., Mishra, S., and McHaourab, H. S. (2010) Structure, dynamics, and substrate-induced conformational changes of the multidrug transporter EmrE in liposomes. J. Biol. Chem. 285, 26710-26718
31. Gross, A., and Hubbell, W. L. (2002) Identification of protein side chains near the membrane-aqueous interface: a site-directed spin labeling study of KcsA. Biochemistry 41, 1123-1128
32. Farahbakhsh, Z. T., Altenbach, C, and Hubbell, W. L. (1992) Spin labeled cysteines as sensors for protein-lipid interaction and conformation in rhodopsin. Photochem. Photobiol. 56, 1019-1033
33. Altenbach, C, Froncisz, W., Hemker, R., McHaourab, H., and Hubbell, W. L. (2005) Accessibility of nitroxide side chains. Absolute Heisenberg exchange rates from power saturation EPR. Biophys. J. 89, 2103-2112
34. McHaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35, 7692-7704
35. Lee, W. Y., and Sine, S. M. (2005) Principal pathway coupling agonist binding to channel gating in nicotinic receptors. Nature 438, 243-247
36. Mercado, J., and Czajkowski, C. (2006) Charged residues in the a1 and β2 pre-M1 regions involved in GABAA receptor activation. J. Neurosci. 26, 2031-2040
37. Hu, X. Q., Zhang, L., Stewart, R. R., and Weight, F. F. (2003) Arginine 222 in the pre-transmembrane domain 1 of 5-HT3A receptors links agonist binding to channel gating. J. Biol. Chem. 278, 46583-46589
38. Zhang, H, and Karlin, A. (1997) Identification of acetylcholine receptor channel-lining residues in the M1 segment of the β-subunit. Biochemistry 36, 15856-15864
39. Grosman, C, Salamone, F. N, Sine, S. M., and Auerbach, A. (2000) The extracellular linker of muscle acetylcholine receptor channels is a gating control element. J. Gen. Physiol. 116, 327-340
40. Campos-Caro, A., Sala, S., Ballesta, J. J., Vicente-Agulló, F., Criado, M., and Sala, F. (1996) A single residue in the M2-M3 loop is a major determinant of coupling between binding and gating in neuronal nicotinic receptors. Proc. Natl. Acad. Sci. U. S. A. 93, 6118-6123
41. Lummis, S. C, Beene, D. L., Lee, L. W., Lester, H. A., Broadhurst, R. W., and Dougherty, D. A. (2005) Cis-trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel. Nature 438, 248-252
42. Lynch, J. W., Rajendra, S., Pierce, K. D., Handford, C. A., Barry, P. H., and Schofield, P. R. (1997) Identification of intracellular and extracellular domains mediating signal transduction in the inhibitory glycine receptor chloride channel. EMBOJ. 16, 110-120
43. Bera, A. K., Chatav, M., and Akabas, M. H. (2002) GABA (A) receptor M2-M3 loop secondary structure and changes in accessibility during channel gating. J. Biol. Chem. 277, 43002-43010
44. Mitra, A., Bailey, T. D., and Auerbach, A. L. (2004) Structural dynamics of the M4 transmembrane segment during acetylcholine receptor gating. Structure 12, 1909-1918
45. Bouzat, C, Roccamo, A. M., Garbus, I., and Barrantes, F. J. (1998) Mutations at lipid-exposed residues of the acetylcholine receptor affect its gating kinetics. Mol. Pharmacol. 54, 146-153
46. Chakrapani, S., Bailey, T. D., and Auerbach, A. (2004) Gating dynamics of the acetylcholine receptor extracellular domain. J. Gen. Physiol. 123, 341-356
47. Reeves, D. C, Jansen, M., Bali, M., Lemster, T., and Akabas, M. H. (2005) A role for the β1-β 2 loop in the gating of 5-HT3 receptors. J. Neurosci. 25, 9358-9366
48. Green, W. N., and Wanamaker, C. P. (1997) The role of the cystine loop in acetylcholine receptor assembly. J. Biol. Chem. 272, 20945-20953
49. Grutter, T., Prado De Carvalho, L., Virginie, D., Taly, A., Fischer, M., and Changeux, J. P. (2005) A chimera encoding the fusion of an acetylcholinebinding protein to an ion channel is stabilized in a state close to the desensitized form of ligand-gated ion channels. C R Biol. 328, 223-234
50. Miyazawa, A., Fujiyoshi, Y., and Unwin, N. (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423, 949-955
51. Hibbs, R. E., Johnson, D. A., Shi, J., and Taylor, P. (2006) Structural dynamics of the acetylcholine binding protein. Hydrodynamic and fluorescence anisotropy decay analyses. J. Mol. Neurosci. 30, 73-74
52. Galzi, J. L., Bertrand, S., Corringer, P. J., Changeux, J. P., and Bertrand, D. (1996) Identification of calcium binding sites that regulate potentiation of a neuronal nicotinic acetylcholine receptor. EMBO J. 15, 5824-5832
53. Thompson, A. J., Padgett, C. L., and Lummis, S. C. (2006) Mutagenesis and molecular modeling reveal the importance of the 5-HT3 receptor F-loop. J. Biol. Chem. 281, 16576-16582
54. Hibbs, R. E., and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60
55. Celie, P. H, Van Rossum-Fikkert, S. E., Van Dijk, W. J., Brejc, K., Smit, A. B., and Sixma, T. K. (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41, 907-914
56. Mukhtasimova, N, Lee, W. Y., Wang, H. L., and Sine, S. M. (2009) Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 459, 451-454
57. Galzi, J. L., Revah, F., Black, D., Goeldner, M., Hirth, C, and Changeux, J. P. (1990) Identification of a novel amino acid a-tyrosine 93 within the cholinergic ligands-binding sites of the acetylcholine receptor by photoaffinity labeling. Additional evidence for a three-loop model of the cholinergic ligands-binding sites. J. Biol. Chem. 265, 10430-10437
58. Chakrapani, S., Bailey, T. D., and Auerbach, A. (2003) The role of loop 5 in acetylcholine receptor channel gating. J. Gen. Physiol. 122, 521-539
59. Boileau, A. J., Newell, J. G., and Czajkowski, C. (2002) GABA (A) receptor β 2 Tyr-97 and Leu-99 line the GABA-binding site. Insights into mechanisms of agonist and antagonist actions. J. Biol. Chem. 277, 2931-2937
60. Bocquet, N, Prado De Carvalho, L., Cartaud, J., Neyton, J., Le Poupon, C, Taly, A., Grutter, T., Changeux, J. P., and Corringer, P. J. (2007) A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 445, 116-119
61. Corringer, P. J., Baaden, M., Bocquet, N, Delarue, M., Dufresne, V., Nury, H, Prevost, M., and Van Renterghem, C. (2010) Atomic structure and dynamics of pentameric ligand-gated ion channels. New insight from bacterial homologues. J. Physiol. 588, 565-572
62. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346, 967-989
63. Pan, J., Chen, Q., Willenbring, D., Yoshida, K., Tillman, T., Kashlan, O. B., Cohen, A., Kong, X. P., Xu, Y., and Tang, P. (2012) Structure of the pentameric ligand-gated ion channel ELIC cocrystallized with its competitive antagonist acetylcholine. Nat Commun. 3, 714
64. Labriola, J. M., Pandhare, A., Jansen, M., Blanton, M. P., Corringer, P. J., and Baenziger, J. E. (2013) Structural sensitivity of a prokaryotic pentameric ligand-gated ion channel to its membrane environment. J. Biol. Chem. 288, 11294-11303
65. Fong, T. M., and McNamee, M. G. (1986) Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25, 830-840
66. Wang, Q., Pless, S. A., and Lynch, J. W. (2010) Ligand- and subunit-specific conformational changes in the ligand-binding domain and the TM2-TM3 linker of a1 02 72 GABAA receptors. J. Biol. Chem. 285, 40373-40386
67. Prevost, M. S., Sauguet, L., Nury, H., Van Renterghem, C, Huon, C, Poitevin, F., Baaden, M., Delarue, M., and Corringer, P. J. (2012) A locally closed conformation of a bacterial pentameric proton-gated ion channel. Nat. Struct. Mol. Biol. 19, 642-649
68. Gonzalez-Gutierrez, G., Cuello, L. G., Nair, S. K., and Grosman, C. (2013) Gating of the proton-gated ion channel from Gloeobacter violaceus at pH 4 as revealed by x-ray crystallography. Proc. Natl. Acad. Sci. U. S. A. 110, 18716-18721
69. Mowrey, D. D., Cui, T., Jia, Y., Ma, D., Makhov, A. M., Zhang, P., Tang, P., and Xu, Y. (2013) Open-channel structures of the human glycine receptor a1 full-length transmembrane domain. Structure 21, 1897-1904