Channel opening by anesthetics and GABA induces similar changes in the GABAA receptor M2 segment

Biophysical Journal

Volumn 92, Issue 9, 2007, Pages 3130-3139

  Rosen, Ayelet ^a   Bali, Moez ^a   Horenstein, Jeffrey ^a,b   Akabas, Myles H ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ISOFLURANE; PENTOBARBITAL; PHENANTHROLINE; PROPOFOL;

ANIMAL CELL; ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; NONHUMAN; OXIDATION; RECEPTOR UPREGULATION;

EID: 34247619386     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.094490     Document Type: Article

References (59)

1. Rudolph, U., and B. Antkowiak. 2004. Molecular and neuronal substrates for general anaesthetics. Nat. Rev. Neurosci. 5:709-720.
2. Jurd, R., M. Arras, S. Lambert, B. Drexler, R. Siegwart, F. Crestani, M. Zaugg, K. E. Vogt, B. Ledermann, B. Antkowiak, and U. Rudolph. 2003. General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor β3 subunit. FASEB J. 17:250-252.
3. Franks, N. P., and W. R. Lieb. 1998. Which molecular targets are most relevant to general anaesthesia? Toxicol. Lett. 100-101:1-8.
4. Evers, A. S., and J. H. Steinbach. 1999. Double-edged swords: volatile anesthetics both enhance and inhibit ligand-gated ion channels. Anesthesiology. 90:1-3.
5. Hemmings, H. C., Jr., M. H. Akabas, P. A. Goldstein, J. R. Trudell, B. A. Orser, and N. L. Harrison. 2005. Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol. Sci. 26:503-510.
6. A receptor needs two homologous domains of the β-subunit for activation by GABA but not by pentobarbital. Nature. 366:565-569.
7. A receptor. J. Neurosci. 17:625-634.
8. Fukami, S., I. Uchida, M. Takenoshita, T. Mashimo, and I. Yoshiya. 1999. The effects of a point mutation of the β2 subunit of GABA(A) receptor on direct and modulatory actions of general anesthetics. Eur. J. Pharmacol. 368:269-276.
9. Bai, D., P. S. Pennefather, J. F. MacDonald, and B. A. Orser. 1999. The general anesthetic propofol slows deactivation and desensitization of GABA(A) receptors. J. Neurosci. 19:10635-10646.
10. Williams, D. B., and M. H. Akabas. 2001. Evidence for distinct conformations of the two a(1) subunits in diazepam-bound GABA(A) receptors. Neuropharmacology. 41:539-545.
11. Williams, D. B., and M. H. Akabas. 2002. Structural evidence that propofol stabilizes different GABA(A) receptor states at potentiating and activating concentrations. J. Neurosci. 22:7417-7424.
12. Jackson, M. B., H. Lecar, D. A. Mathers, and J. L. Barker. 1982. Single channel currents activated by gamma-aminobutyric acid, muscimol, and (-)-pentobarbital in cultured mouse spinal neurons. J. Neurosci. 2:889-894.
13. Hales, T. G., and J. J. Lambert. 1991. The actions of propofol on inhibitory amino acid receptors of bovine adrenomedullary chromaffin cells and rodent central neurones. Br. J. Pharmacol. 104:619-628.
14. A channel subtypes. Mol. Neurobiol. 18:35-86.
15. Sieghart, W., and G. Sperk. 2002. Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem. 2:795-816.
16. A receptor structure-function studies: a reexamination in light of new acetylcholine receptor structures. Int. Rev. Neurobiol. 62:1-43.
17. A receptor subtype. J. Neurosci. 17:2728-2737.
18. 2+ binding site in the channel of α1β1 γ-aminobutyric acid A receptors. Mol. Pharmacol. 53:870-877.
19. Baumann, S. W., R. Baur, and E. Sigel. 2001. Subunit arrangement of γ-aminobutyric acid type A receptors. J. Biol. Chem. 276:36275-36280.
20. A receptor subunit requires a monomeric subunit of α6 or γ2. J. Biol. Chem. 270:26063-26066.
21. A receptor-associated protein. J. Neurosci. 25:11219-11230.
22. Brejc, K., W. J. van Dijk, R. V. Klaassen, M. Schuurmans, J. van Der Oost, A. B. Smit, and T. K. Sixma. 2001. Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature. 411:269-276.
23. 191 segment is involved in GABA binding and channel gating. J. Biol. Chem. 278:13166-13172.
24. Sarto, I., L. Wabnegger, E. Dogl, and W. Sieghart. 2002. Homologous sites of GABA(A) receptor α(1), β(3) and γ(2) subunits are important for assembly. Neuropharmacology. 43:482-491.
25. A receptor α1 subunit. J. Gen. Physiol. 107:195-205.
26. Unwin, N. 2005. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346:967-989.
27. Miller, C. 1989. Genetic manipulation of ion channels: a new approach to structure and mechanism. Neuron. 2:1195-1205.
28. Wilson, G. G., and A. Karlin. 1998. The location of the gate in the acetylcholine receptor channel. Neuron. 20:1269-1281.
29. Panicker, S., H. Cruz, C. Arrabit, and P. A. Slesinger. 2002. Evidence for a centrally located gate in the pore of a serotonin-gated ion channel. J. Neurosci. 22:1629-1639.
30. Akabas, M. H., C. Kaufmann, P. Archdeacon, and A. Karlin. 1994. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the α-subunit. Neuron. 13:919-927.
31. Horenstein, J., D. A. Wagner, C. Czajkowski, and M. H. Akabas. 2001. Protein mobility and GABA-induced conformational changes in GABA(A) receptor pore-lining M2 segment. Nat. Neurosci. 4:477-485.
32. Careaga, C. L., and J. J. Falke. 1992. Thermal motions of surface α-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J. Mol. Biol. 226:1219-1235.
33. Kobashi, K. 1968. Catalytic oxidation of sulfhydryl groups by o-phenanthroline copper complex. Biochim. Biophys. Acta. 158:239-245.
34. Wu, J., and H. R. Kaback. 1996. A general method for determining helix packing in membrane proteins in situ: helices I and II are close to helix VII in the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA. 93:14498-14502.
35. Guo, W., L. Shi, and J. A. Javitch. 2002. The fourth transmembrane segment forms the interface of the dopamine D2 receptor homodimer. J. Biol. Chem. 278:4385-4388.
36. Chen, C. A., and H. Okayama. 1988. Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques. 6:632-638.
37. Jespersen, T., M. Grunnet, K. Angelo, D. A. Klaerke, and S. P. Olesen. 2002. Dual-function vector for protein expression in both mammalian cells and Xenopus laevis oocytes. Biotechniques. 32:536-538.
38. A receptor. J. Neurosci. 21:R136:1-4.
39. Akabas, M. H., D. A. Stauffer, M. Xu, and A. Karlin. 1992. Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science. 258:307-310.
40. Peacock, S. L., M. P. Bates, D. W. Russell, M. S. Brown, and J. L. Goldstein. 1988. Human low density lipoprotein receptor expressed in Xenopus oocytes. Conserved signals for O-linked glycosylation and receptor-mediated endocytosis. J. Biol. Chem. 263:7838-7845.
41. A receptor channel-lining residues probed in cysteine mutants. Biophys. J. 69:1858-1867.
42. A receptor. J. Physiol. 577:569-577.
43. Imoto, K., C. Busch, B. Sakmann, M. Mishina, T. Konno, J. Nakai, H. Bujo, Y. Mori, K. Fukuda, and S. Numa. 1988. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature. 335:645-648.
44. Villarroel, A., S. Herlitze, M. Koenen, and B. Sakmann. 1991. Location of a threonine residue in the α-subunit M2 transmembrane segment that determines the ion flow through the acetylcholine receptor channel. Proc. R. Soc. Lond. B Biol. Sci. 243:69-74.
45. Villarroel, A., S. Herlitze, V. Witzemann, M. Koenen, and B. Sakmann. 1992. Asymmetry of the rat acetylcholine receptor subunits in the narrow region of the pore. Proc. R. Soc. Lond. B Biol. Sci. 249:317-324.
46. Hales, T. G., J. I. Dunlop, T. Z. Deeb, J. E. Carland, S. P. Kelley, J. J. Lambert, and J. A. Peters. 2006. Common determinants of single channel conductance within the large cytoplasmic loop of 5-hydroxytryptamine type 3 and α4β2 nicotinic acetylcholine receptors. J. Biol. Chem. 281:8062-8071.
47. A receptor {β}1 subunit M2 channel-lining segment. J. Biol. Chem. 279:11198-11205.
48. 3A receptor. J. Biol. Chem. 279:28149-28158.
49. Edwards, M. D., and G. Lees. 1997. Modulation of a recombinant invertebrate γ-aminobutyric acid receptor-chloride channel complex by isoflurane: effects of a point mutation in the M2 domain. Br. J. Pharmacol. 122:726-732.
50. A receptor. Mol. Pharmacol. 65:68-76.
51. A receptor β-subunit controls a binding cavity for propofol and other alkylphenol general anesthetics. Neuropharmacology. 41:952-964.
52. Grosman, C., M. Zhou, and A. Auerbach. 2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature. 403:773-776.
53. Cymes, G. D., C. Grosman, and A. Auerbach. 2002. Structure of the transition state of gating in the acetylcholine receptor channel pore: a phi-value analysis. Biochemistry. 41:5548-5555.
54. Mihic, S. J., Q. Ye, M. J. Wick, V. V. Koltchine, M. D. Krasowski, S. E. Finn, M. P. Mascia, C. F. Valenzuela, K. K. Hanson, E. P. Greenblatt, R. A. Harris, and N. L. Harrison. 1997. Sites of alcohol and volatile anaesthetic action on GABA(A) and glycine receptors. Nature. 389:385-389.
55. Amin, J. 1999. A single hydrophobic residue confers barbiturate sensitivity to γ-aminobutyric acid type C receptor. Mol. Pharmacol. 55:411-423.
56. A receptors. J. Biol. Chem. 277:44845-44853.
57. 3H]flunitrazepam binding in human embryonic kidney cell line 293. Eur. J. Pharmacol. 289:87-95.
58. Ueno, S., C. Zorumski, J. Bracamontes, and J. H. Steinbach. 1996. Endogenous subunits can cause ambiguities in the pharmacology of exogenous γ-aminobutyric acidA receptors expressed in human embryonic kidney 293 cells. Mol. Pharmacol. 50:931-938.
59. Qin, F., A. Auerbach, and F. Sachs. 1996. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70:264-280.