Conformational Gating Dynamics in the GluCl Anion-Selective Chloride Channel

ACS Chemical Neuroscience

Volumn 6, Issue 8, 2015, Pages 1459-1467

  Yoluk, Özge ^a,b   Lindahl, Erik ^a,b,c   Andersson, Magnus ^a,b  

^a SCIENCE FOR LIFE LABORATORY   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

cys loop receptor; ligand gated ion channel; Membrane protein; molecular dynamics simulations

Indexed keywords

ANION; CHLORIDE CHANNEL; GLUTAMATE GATED CHLORIDE CHANNEL; GLUTAMIC ACID; IVERMECTIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; GLUTAMATE-GATED CHLORIDE CHANNELS;

AGONIST; ARTICLE; CALCULATION; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; FORCE; HYDRATION; HYDROGEN BOND; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; X RAY; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

EUKARYOTA;

CHLORIDE CHANNELS; GLUTAMIC ACID; HYDROGEN BONDING; IVERMECTIN; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION;

EID: 84939864190     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.5b00111     Document Type: Article

References (62)

1. Sine, S. M. and Engel, A. G. (2006) Recent advances in Cys-loop receptor structure and function Nature 440, 448-455
2. Howard, R. J., Trudell, J. R., and Harris, R. A. (2014) Seeking structural specificity: direct modulation of pentameric ligand-gated ion channels by alcohols and general anesthetics Pharmacol. Rev. 66, 396-412
3. Olsen, R. W., Li, G. D., Wallner, M., Trudell, J. R., Bertaccini, E. J., Lindahl, E., Miller, K. W., Alkana, R. L., and Davies, D. L. (2014) Structural models of ligand-gated ion channels: Sites of action for anesthetics and ethanol Alcohol.: Clin. Exp. Res. 38, 595-603
4. Hilf, R. J. and Dutzler, R. (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel Nature 452, 375-379
5. 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
6. 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
7. Sauguet, L., Shahsavar, A., Poitevin, F., Huon, C., Menny, A., Nemecz, A., Haouz, A., Changeux, J. P., Corringer, P. J., and Delarue, M. (2014) Crystal structures of a pentameric ligand-gated ion channel provide a mechanism for activation Proc. Natl. Acad. Sci. U. S. A. 111, 966-971
8. Hibbs, R. E. and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor Nature 474, 54-60
9. Hassaine, G., Deluz, C., Grasso, L., Wyss, R., Tol, M. B., Hovius, R., Graff, A., Stahlberg, H., Tomizaki, T., Desmyter, A., Moreau, C., Li, X. D., Poitevin, F., Vogel, H., and Nury, H. (2014) X-ray structure of the mouse serotonin 5-HT3 receptor Nature 512, 276-281
10. Miller, P. S. and Aricescu, A. R. (2014) Crystal structure of a human GABAA receptor Nature 512, 270-275
11. Althoff, T., Hibbs, R. E., Banerjee, S., and Gouaux, E. (2014) X-ray structures of GluCl in apo states reveal a gating mechanism of Cys-loop receptors Nature 512, 333-337
12. Miller, P. S. and Smart, T. G. (2010) Binding, activation and modulation of Cys-loop receptors Trends Pharmacol. Sci. 31, 161-174
13. Dacosta, C. J. and Baenziger, J. E. (2013) Gating of pentameric ligand-gated ion channels: structural insights and ambiguities Structure 21, 1271-1283
14. 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
15. Cully, D. F., Vassilatis, D. K., Liu, K. K., Paress, P. S., Van der Ploeg, L. H., Schaeffer, J. M., and Arena, J. P. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans Nature 371, 707-711
16. Etter, A., Cully, D. F., Schaeffer, J. M., Liu, K. K., and Arena, J. P. (1996) An amino acid substitution in the pore region of a glutamate-gated chloride channel enables the coupling of ligand binding to channel gating J. Biol. Chem. 271, 16035-16039
17. Aziz, M. A., Diallo, S., Diop, I. M., Lariviere, M., and Porta, M. (1982) Efficacy and tolerance of ivermectin in human onchocerciasis Lancet 2, 171-173
18. Campbell, W. C., Fisher, M. H., Stapley, E. O., Albers-Schonberg, G., and Jacob, T. A. (1983) Ivermectin: a potent new antiparasitic agent Science 221, 823-828
19. Yoluk, O., Bromstrup, T., Bertaccini, E. J., Trudell, J. R., and Lindahl, E. (2013) Stabilization of the GluCl ligand-gated ion channel in the presence and absence of ivermectin Biophys. J. 105, 640-647
20. 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
21. 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
22. Cheng, X., Ivanov, I., Wang, H., Sine, S. M., and McCammon, J. A. (2009) Molecular-dynamics simulations of ELIC-a prokaryotic homologue of the nicotinic acetylcholine receptor Biophys. J. 96, 4502-4513
23. Mowrey, D., Cheng, M. H., Liu, L. T., Willenbring, D., Lu, X., Wymore, T., Xu, Y., and Tang, P. (2013) Asymmetric ligand binding facilitates conformational transitions in pentameric ligand-gated ion channels J. Am. Chem. Soc. 135, 2172-2180
24. Murail, S., Wallner, B., Trudell, J. R., 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
25. Cheng, X., Ivanov, I., Wang, H., Sine, S. M., and McCammon, J. A. (2007) Nanosecond-timescale conformational dynamics of the human alpha7 nicotinic acetylcholine receptor Biophys. J. 93, 2622-2634
26. Haddadian, E. J., Cheng, M. H., Coalson, R. D., Xu, Y., and Tang, P. (2008) In silico models for the human alpha4beta2 nicotinic acetylcholine receptor J. Phys. Chem. B 112, 13981-13990
27. Nury, H., Poitevin, F., Van Renterghem, C., Changeux, J. P., Corringer, P. J., 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
28. Cheng, X., Wang, H., Grant, B., Sine, S. M., and McCammon, J. A. (2006) Targeted molecular dynamics study of C-loop closure and channel gating in nicotinic receptors PLoS Comput. Biol. 2, e134
29. Calimet, N., Simoes, M., Changeux, J. P., Karplus, M., Taly, A., and Cecchini, M. (2013) A gating mechanism of pentameric ligand-gated ion channels Proc. Natl. Acad. Sci. U. S. A. 110, E3987-3996
30. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics J. Mol. Graphics 14 (33-38) 27-38
31. Lummis, S. C., D, L. B., Harrison, N. J., Lester, H. A., and Dougherty, D. A. (2005) A cation-pi binding interaction with a tyrosine in the binding site of the GABAC receptor Chem. Biol. 12, 993-997
32. Xiu, X., Puskar, N. L., Shanata, J. A., Lester, H. A., and Dougherty, D. A. (2009) Nicotine binding to brain receptors requires a strong cation-pi interaction Nature 458, 534-537
33. Taly, A., Delarue, M., Grutter, T., Nilges, M., Le Novere, 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
34. Andersson, M., Bondar, A. N., Freites, J. A., Tobias, D. J., Kaback, H. R., and White, S. H. (2012) Proton-coupled dynamics in lactose permease Structure 20, 1893-1904
35. Beckstein, O. and Sansom, M. S. (2006) A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor Phys. Biol. 3, 147-159
36. Ivanov, I., Cheng, X., Sine, S. M., and McCammon, J. A. (2007) Barriers to ion translocation in cationic and anionic receptors from the Cys-loop family J. Am. Chem. Soc. 129, 8217-8224
37. Miyazawa, A., Fujiyoshi, Y., and Unwin, N. (2003) Structure and gating mechanism of the acetylcholine receptor pore Nature 423, 949-955
38. Khatri, A., Sedelnikova, A., and Weiss, D. S. (2009) Structural Rearrangements in Loop F of the GABA Receptor Signal Ligand Binding, Not Channel Activation Biophys. J. 96, 45-55
39. Cheng, M. H. and Coalson, R. D. (2012) Energetics and ion permeation characteristics in a glutamate-gated chloride (GluCl) receptor channel J. Phys. Chem. B 116, 13637-13643
40. Pless, S. A. and Lynch, J. W. (2009) Ligand-specific conformational changes in the alpha1 glycine receptor ligand-binding domain J. Biol. Chem. 284, 15847-15856
41. Newell, J. G. and Czajkowski, C. (2003) The GABA(A) receptor alpha(1) subunit Pro(174)-Asp(191) segment is involved in GABA binding and channel gating J. Biol. Chem. 278, 13166-13172
42. Thompson, A. J., Padgett, C. L., and Lummis, S. C. R. (2006) Mutagenesis and molecular modeling reveal the importance of the 5-HT3 receptor F-loop J. Biol. Chem. 281, 16576-16582
43. Daeffler, K. N., Lester, H. A., and Dougherty, D. A. (2014) Functional evaluation of key interactions evident in the structure of the eukaryotic Cys-loop receptor GluCl ACS Chem. Biol. 9, 2283-2290
44. Lee, W. Y. and Sine, S. M. (2004) Invariant aspartic Acid in muscle nicotinic receptor contributes selectively to the kinetics of agonist binding J. Gen. Physiol. 124, 555-567
45. Cashin, A. L., Torrice, M. M., McMenimen, K. A., Lester, H. A., and Dougherty, D. A. (2007) Chemical-scale studies on the role of a conserved aspartate in preorganizing the agonist binding site of the nicotinic acetylcholine receptor Biochemistry 46, 630-639
46. Schaefer, N., Kluck, C. J., Price, K. L., Meiselbach, H., Vornberger, N., Schwarzinger, S., Hartmann, S., Langlhofer, G., Schulz, S., Schlegel, N., Brockmann, K., Lynch, B., Becker, C. M., Lummis, S. C., and Villmann, C. (2015) Disturbed neuronal ER-Golgi sorting of unassembled glycine receptors suggests altered subcellular processing is a cause of human hyperekplexia J. Neurosci. 35, 422-437
47. Dent, J. A. (2006) Evidence for a diverse Cys-loop ligand-gated ion channel superfamily in early bilateria J. Mol. Evol. 62, 523-535
48. Gay, E. A., Giniatullin, R., Skorinkin, A., and Yakel, J. L. (2008) Aromatic residues at position 55 of rat alpha7 nicotinic acetylcholine receptors are critical for maintaining rapid desensitization J. Physiol. 586, 1105-1115
49. Sigel, E., Baur, R., Kellenberger, S., and Malherbe, P. (1992) Point mutations affecting antagonist affinity and agonist dependent gating of GABAA receptor channels EMBO J. 11, 2017-2023
50. Berger, O., Edholm, O., and Jahnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72, 2002-2013
51. Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., and Shaw, D. E. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 78, 1950-1958
52. Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., and Lindahl, E. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29, 845-854
53. Essmann, U., Perera, L., Berkowitz, M., Darden, T., Lee, H., and Pedersen, L. (1995) A smooth particle mesh Ewald method J. Chem. Phys. 103, 8577-8593
54. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling J. Chem. Phys. 126, 014101
55. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath J. Chem. Phys. 81, 3684-3690
56. Kumar, S., Rosenberg, J., Bouzida, D., Swendsen, R., and Kollman, P. (1992) THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13, 1011-1021
57. Smart, O. S., Neduvelil, J. G., Wang, X., Wallace, B. A., and Sansom, M. S. (1996) HOLE: A program for the analysis of the pore dimensions of ion channel structural models J. Mol. Graphics 14 (354-360) 376
58. Frishman, D. and Argos, P. (1995) Knowledge-based protein secondary structure assignment Proteins 23, 566-579
59. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator Genome Res. 14, 1188-1190
60. Schneider, T. D. and Stephens, R. M. (1990) Sequence logos: a new way to display consensus sequences Nucleic Acids Res. 18, 6097-6100
61. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-A visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612
62. Persistence of Vision Pty. Ltd. (2004) Persistence of Vision Raytracer, Version 3.6, Persistence of Vision Pty. Ltd., Williamstown, Victoria, Australia.