Reversal of ion-charge selectivity renders the pentameric ligand-gated ion channel GLIC insensitive to anaesthetics

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 61-68

  Tillman, Tommy ^a   Cheng, Mary H ^a   Chen, Qiang ^a   Tang, Pei ^a   Xu, Yan ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Anaesthetic action; GLIC; Ion selectivity; Pentameric ligand gated ion channel (pLGIC)

Indexed keywords

ETOMIDATE; LIGAND GATED ION CHANNEL; PICROTOXIN; PROPOFOL;

ANESTHESIA MECHANISM; ARTICLE; CHEMICAL STRUCTURE; DRUG BINDING; HYDRATION; MOLECULAR DYNAMICS; MUTATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANESTHETICS; ANIMALS; CHLORIDE CHANNELS; FEMALE; IONS; LIGAND-GATED ION CHANNELS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROPOFOL; PROTEIN BINDING; XENOPUS LAEVIS;

PROKARYOTA;

EID: 84870935940     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121072     Document Type: Article

References (46)

1. Franks, N. P. and Lieb, W. R. (1994) Molecular and cellular mechanisms of general anaesthesia. Nature 367, 607-614 (Pubitemid 24067700)
2. Dilger, J. P. (2002) The effects of general anaesthetics on ligand-gated ion channels. Br. J. Anaesth. 89, 41-51
3. 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 ligand-gated ion channel. Nature 469, 428-431
4. Weng, Y., Yang, L., Corringer, P. J. and Sonner, J. M. (2010) Anesthetic sensitivity of the Gloeobacter violaceus proton-gated ion channel. Anesth. Analg. 110, 59-63
5. Bertaccini, E. J., Wallner, B., Trudell, J. R. and Lindahl, E. (2010) Modeling anesthetic binding sites within the glycine alpha one receptor based on prokaryotic ion channel templates: the problem with TM4. J. Chem. Inf. Model. 50, 2248-2255
6. 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
7. Hibbs, R. E. and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60
8. Perkins, D. I., Trudell, J. R., Asatryan, L., Davies, D. L. and Alkana, R. L. (2012) Charge and geometry of residues in the loop 2 β hairpin differentially affect agonist and ethanol sensitivity in glycine receptors. J. Pharmacol. Exp. Ther. 341, 543-551
9. McCracken, L. M., McCracken, M. L., Gong, D. H., Trudell, J. R. and Harris, R. A. (2010) Linking of glycine receptor transmembrane segments three and four allows assignment of intrasubunit-facing residues. ACS Chem. Neurosci. 1, 482
10. Keramidas, A., Moorhouse, A. J., Schofield, P. R. and Barry, P. H. (2004) Ligand-gated ion channels: mechanisms underlying ion selectivity. Prog. Biophys. Mol. Biol. 86, 161-204 (Pubitemid 39027232)
11. Galzi, J. L., Devillers-Thiery, A., Hussy, N., Bertrand, S., Changeux, J. P. and Bertrand, D. (1992) Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature 359, 500-505
12. 3a receptor from cationic to anionic reveals a conserved feature of the ligand-gated ion channel superfamily. J. Biol. Chem. 276, 10977-10983
13. Lee, D. J., Keramidas, A., Moorhouse, A. J., Schofield, P. R. and Barry, P. H. (2003) The contribution of proline 250 (P-2′) to pore diameter and ion selectivity in the human glycine receptor channel. Neurosci. Lett. 351, 196-200 (Pubitemid 37410337)
14. Keramidas, A., Moorhouse, A. J., Pierce, K. D., Schofield, P. R. and Barry, P. H. (2002) Cation-selective mutations in the M2 domain of the inhibitory glycine receptor channel reveal determinants of ion-charge selectivity. J. Gen. Physiol. 119, 393-410 (Pubitemid 34522287)
15. Wotring, V. E., Miller, T. S. and Weiss, D. S. (2003) Mutations at the GABA receptor selectivity filter: a possible role for effective charges. J. Physiol. 548, 527-540 (Pubitemid 36527474)
16. Jensen, M. L., Timmermann, D. B., Johansen, T. H., Schousboe, A., Varming, T. and Ahring, P. K. (2002) The β subunit determines the ion selectivity of the GABAA receptor. J. Biol. Chem. 277, 41438-41447 (Pubitemid 35257445)
17. Sive, H. L., Grainger, R. M. and Harland, R. M. (2000) Early development of Xenopus laevis: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
18. Dascal, N. (2001) Voltage clamp recordings from Xenopus oocytes. Curr. Protoc. Neurosci. Chapter 6, Unit 6.12.
19. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (Pubitemid 26152973)
20. Willenbring, D., Liu, L., Mowrey, D., Xu, Y. and Tang, P. (2011) Isoflurane alters the structure and dynamics of GLIC. Biophys. J. 101, 1905-1912
21. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L. and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
22. MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S. et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102, 3586-3616 (Pubitemid 128576688)
23. Chipot, C. and Hénin, J. (2005) Exploring the free-energy landscape of a short peptide using an average force. J. Chem. Phys. 123, 244906
24. Darve, E., Rodriguez-Gomez, D. and Pohorille, A. (2008) Adaptive biasing force method for scalar and vector free energy calculations. J. Chem. Phys. 128, 144120
25. Cheng, M. H., Coalson, R. D. and Tang, P. (2010) Molecular dynamics and brownian dynamics investigation of ion permeation and anesthetic halothane effects on a proton-gated ion channel. J. Am. Chem. Soc. 132, 16442-16449
26. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K. and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662 (Pubitemid 128590223)
27. Corringer, P. J., Bertrand, S., Galzi, J. L., Devillers-Thiery, A., Changeux, J. P. and Bertrand, D. (1999) Mutational analysis of the charge selectivity filter of the α7 nicotinic acetylcholine receptor. Neuron 22, 831-843 (Pubitemid 29203505)
28. 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
29. Alqazzaz, M., Thompson, A. J., Price, K. L., Breitinger, H. G. and Lummis, S. C. (2011) Cys-loop receptor channel blockers also block GLIC. Biophys. J. 101, 2912-2918
30. 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
31. 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
32. Thompson, A. J. and Lummis, S. C. (2003) A single ring of charged amino acids at one end of the pore can control ion selectivity in the 5-HT3 receptor. Br. J. Pharmacol. 140, 359-365 (Pubitemid 37249196)
33. Keramidas, A., Moorhouse, A. J., French, C. R., Schofield, P. R. and Barry, P. H. (2000) M2 pore mutations convert the glycine receptor channel from being anion- to cation-selective. Biophys. J. 79, 247-259 (Pubitemid 30436741)
34. Fritsch, S., Ivanov, I., Wang, H. and Cheng, X. (2011) Ion selectivity mechanism in a bacterial pentameric ligand-gated ion channel. Biophys. J. 100, 390-398
35. 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
36. Erkkila, B. E., Weiss, D. S. and Wotring, V. E. (2004) Picrotoxin-mediated antagonism of α3β4 and α7 acetylcholine receptors. NeuroReport 15, 1969-1973
37. Pribilla, I., Takagi, T., Langosch, D., Bormann, J. and Betz, H. (1992) The atypical M2 segment of the β-subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J. 11, 4305-4311
38. Takeuchi, A. and Takeuchi, N. (1969) A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish. J. Physiol. 205, 377-391
39. Wang, T. L., Hackam, A. S., Guggino, W. B. and Cutting, G. R. (1995) A single amino acid in γ-aminobutyric acid rho 1 receptors affects competitive and noncompetitive components of picrotoxin inhibition. Proc. Natl. Acad. Sci. U.S.A. 92, 11751-11755 (Pubitemid 26014191)
40. Duret, G., Van Renterghem, C., Weng, Y., Prevost, M., Moraga-Cid, G., Huon, C., Sonner, J. M. and Corringer, P. J. (2011) Functional prokaryotic-eukaryotic chimera from the pentameric ligand-gated ion channel family. Proc. Natl. Acad. Sci. U.S.A. 108, 12143-12148
41. Das, P. and Dillon, G. H. (2005) Molecular determinants of picrotoxin inhibition of 5-hydroxytryptamine type 3 receptors. J. Pharmacol. Exp. Ther. 314, 320-328 (Pubitemid 41058269)
42. Violet, J. M., Downie, D. L., Nakisa, R. C., Lieb, W. R. and Franks, N. P. (1997) Differential sensitivities of mammalian neuronal and muscle nicotinic acetylcholine receptors to general anesthetics. Anesthesiology 86, 866-874 (Pubitemid 27174727)
43. Flood, P., Ramirez-Latorre, J. and Role, L. (1997) α4β2 neuronal nicotinic acetylcholine receptors in the central nervous system are inhibited by isoflurane and propofol, but α7-type nicotinic acetylcholine receptors are unaffected. Anesthesiology 86, 859-865 (Pubitemid 27174726)
44. Pistis, M., Belelli, D., Peters, J. A. and Lambert, J. J. (1997) The interaction of general anaesthetics with recombinant GABAA and glycine receptors expressed in Xenopus laevis oocytes: a comparative study. Br. J. Pharmacol. 122, 1707-1719 (Pubitemid 28000208)
45. Wang, H. L., Cheng, X., Taylor, P., McCammon, J. A. and Sine, S. M. (2008) Control of cation permeation through the nicotinic receptor channel. PLoS Comput. Biol. 4, e41
46. Chen, Q., Cheng, M. H., Xu, Y. and Tang, P. (2010) Anesthetic binding in a pentameric ligand-gated ion channel: GLIC. Biophys. J. 99, 1801-1809