Gating-induced conformational rearrangement of the γ-aminobutyric acid type A receptor β-α subunit interface in the membrane-spanning domain

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27762-27770

  Bali, Moez ^a   Akabas, Myles H ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOBUTYRIC ACIDS; CHANNEL GATING; CONFORMATIONAL CHANGE; DISULFIDE BOND FORMATION; EXTRACELLULAR; INNER RINGS; ION CHANNEL; MEMBRANE SPANNING DOMAINS; PROPOFOL; RELATIVE POSITIONS; RESTING STATE; RIGID BODY; STRUCTURAL REARRANGEMENT; SUBUNIT INTERFACES; SYNAPTIC TRANSMISSION; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE SEGMENTS; TRANSMEMBRANES;

ACTIVATION ANALYSIS; COVALENT BONDS; LIPID BILAYERS; REACTION RATES;

AMINO ACIDS;

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1M1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2M2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2M3; ANESTHETIC AGENT; CHLOROMERCURIBENZENESULFONIC ACID; CYSTEINE; PROPOFOL; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CHANNEL GATING; CHEMICAL REACTION KINETICS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; FEMALE; GENE MUTATION; LIPID BILAYER; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; RECEPTOR BINDING; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION; XENOPUS LAEVIS;

AMINO ACID SUBSTITUTION; ANESTHETICS, INTRAVENOUS; ANIMALS; ION CHANNEL GATING; LIPID BILAYERS; MUTATION, MISSENSE; PROPOFOL; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, GABA-A; XENOPUS LAEVIS;

EID: 84865046484     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.363341     Document Type: Article

References (47)

1. Hemmings, H. C., Jr., Akabas, M. H., Goldstein, P. A., Trudell, J. R., Orser, B. A., and Harrison, N. L. (2005) Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol. Sci. 26, 503-510
2. Franks, N. P. (2006) Molecular targets underlying general anaesthesia. Br. J. Pharmacol. 147, S72-81
3. A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141-148
4. Miller, P. S., and Smart, T. G. (2010) Binding, activation and modulation of Cys-loop receptors. Trends Pharmacol. Sci. 31, 161-174
5. A receptors as molecular targets of general anesthetics: identification of binding sites provides clues to allosteric modulation. Can. J. Anaesth. 58, 206-215
6. A receptor research. Synapse 21, 189-274
7. Moss, S. J., and Smart, T. G. (2001) Constructing inhibitory synapses. Nat. Rev. Neurosci. 2, 240-250
8. Akabas, M. H., Kaufmann, C., Archdeacon, P., and Karlin, A. (1994) Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the α-subunit. Neuron 13, 919-927
9. A receptor α1 subunit. J. Gen. Physiol. 107, 195-205
10. Cymes, G. D., Ni, Y., and Grosman, C. (2005) Probing ion-channel pores one proton at a time. Nature 438, 975-980
11. Parikh, R., 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
12. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J. Mol. Biol. 346, 967-989
13. 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
14. Hibbs, R. E., and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60
15. A receptor channel. J. Gen. Physiol. 129, 145-159
16. Brejc, K., van Dijk, W. J., Klaassen, R. V., Schuurmans, M., van Der Oost, J., Smit, A. B., and Sixma, T. K. (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411, 269-276
17. A receptor. Nature 421, 272-275
18. Reeves, D. C., Jansen, M., Bali, M., Lemster, T., and Akabas, M. H. (2005) A role for the β1-β2 loop in the gating of 5-HT3 receptors. J. Neurosci. 25, 9358-9366
19. A receptor. Mol. Pharmacol. 65, 68-76
20. A receptor anesthetic binding site at subunit interfaces by photolabeling with an etomidate analog. J. Neurosci. 26, 11599-11605
21. A receptor α1M1-β2M3 transmembrane subunit interface: experimental basis for homology modeling of an intravenous anesthetic binding site. J. Neurosci. 29, 3083-3092
22. A) receptors. J. Biol. Chem. 285, 8615-8620
23. Karlin, A., and Akabas, M. H. (1998) Substituted-cysteine accessibility method. Methods Enzymol. 293, 123-145
24. A and acetylcholine receptor M3 segments. J. Neurosci. 26, 4492-4499
25. Careaga, C. L., and Falke, J. J. (1992) Thermal motions of surface α-helices in the D-galactose chemosensory receptor: detection by disulfide trapping. J. Mol. Biol. 226, 1219-1235
26. Krovetz, H. S., VanDongen, H. M., and VanDongen, A. M. (1997) Atomic distance estimates from disulfides and high-affinity metal-binding sites in a K+ channel pore. Biophys. J. 72, 117-126
27. Butler, S. L., and Falke, J. J. (1998) Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry 37, 10746-10756
28. A receptor M2 segment. Biophys. J. 92, 3130-3139
29. Horenstein, J., Riegelhaupt, P., and Akabas, M. H. (2005) Differential protein mobility of the γ-aminobutyric acid, type A, receptor α and β subunit channel-lining segments. J. Biol. Chem. 280, 1573-1581
30. A receptor M2-M3 loop secondary structure and changes in accessibility during channel gating. J. Biol. Chem. 277, 43002-43010
31. A and glycine receptors. Nature 389, 385-389
32. A receptor M2 channel-lining segments. J. Biol. Chem. 280, 35506-35512
33. A receptor β1 subunit M2 channel-lining segment. J. Biol. Chem. 279, 11198-11205
34. Williams, D. B., and Akabas, M. H. (1999) γ-Aminobutyric acid increases the water accessibility of M3 membrane-spanning segment residues in γ-aminobutyric acid type A receptors. Biophys. J. 77, 2563-2574
35. Akabas, M. H., and Karlin, A. (1995) Identification of acetylcholine receptor channel-lining residues in the M1 segment of the α-subunit. Biochemistry 34, 12496-12500
36. 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
37. Hilf, R. J., and Dutzler, R. (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452, 375-379
38. 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
39. 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
40. 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
41. 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
42. 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
43. A receptor pore-lining M2 segment. Nat. Neurosci. 4, 477-485
44. Dahan, D. S., Dibas, M. I., Petersson, E. J., Auyeung, V. C., Chanda, B., Bezanilla, F., Dougherty, D. A., and Lester, H. A. (2004) A fluorophore attached to nicotinic acetylcholine receptor β M2 detects productive binding of agonist to the αδ site. Proc. Natl. Acad. Sci. U.S.A. 101, 10195-10200
45. Baenziger, J. E., Ryan, S. E., Goodreid, M. M., Vuong, N. Q., Sturgeon, R. M., and daCosta, C. J. (2008) Lipid composition alters drug action at the nicotinic acetylcholine receptor. Mol. Pharmacol. 73, 880-890
46. Fraser, J. S., van den Bedem, H., Samelson, A. J., Lang, P. T., Holton, J. M., Echols, N., and Alber, T. (2011) Accessing protein conformational ensembles using room-temperature x-ray crystallography. Proc. Natl. Acad. Sci. U.S.A. 108, 16247-16252
47. A receptor channel-lining residues probed in cysteine mutants. Biophys. J. 69, 1858-1867