Transfer of ion binding site from ether-à-go-go to Shaker: Mg 2+ binds to resting state to modulate channel opening

Journal of General Physiology

Volumn 135, Issue 5, 2010, Pages 415-431

  Lin, Meng Chin A ^a   Abramson, Jeff ^a   Papazian, Diane M ^a,b,c  

^a Department of Physiology ^*  (United States)

^b Molecular Biology Institute   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNESIUM; POTASSIUM CHANNEL HERG; SHAKER POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; FEMALE; METABOLISM; MOLECULAR GENETICS; OOCYTE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; ETHER-A-GO-GO POTASSIUM CHANNELS; FEMALE; ION CHANNEL GATING; MAGNESIUM; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OOCYTES; PROTEIN BINDING; PROTEIN CONFORMATION; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; XENOPUS LAEVIS;

EID: 77951724342     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910320     Document Type: Article

References (52)

1. + channel. Neuron. 16:1169-1177. doi : 10.1016/S0896-6273 (00) 80143-80149
2. Alabi, A.A., M.I. Bahamonde, H.J. Jung, J.I. Kim, and K.J. Swartz. 2007. Portability of paddle motif function and pharmacology in voltage sensors. Nature.. 450:370-375. doi:10.1038/nature06266
3. + channel gating. Neuron. 20:1283-1294. doi:10.1016/S0896-6273(00)80507-3
4. + channel voltage sensor. Proc. Natl. Acad, Sci. USA. 102:18718-18723. doi:10.1073/ pnas.0505766102
5. Bezanilla, F., and C.M. Armstrong. 1977. Inactivation of the sodium channel. I. Sodium current experiments. J. Gen. Physiol. 70:549-566. doi: 10.1085/jgp.70.5.549 (Pubitemid 8239321)
6. - channels: II. The components of gating currents and a model of channel activation. Biophys. J. 66:1011-1021. doi:10.1016/S00063495(94)80882-3
7. Broomand, A., and F. Elinder. 2008. Large-scale movement within the voltage-sensor paddle of a potassium channel-support for a helical-screw motion. Neuron. 59:770-777. doi:10.1016/j.neuron .2008.07.008
8. Broomand, A., F. Österberg, T. Wardi, and F. Elinder. 2007. Electrostatic domino effect in the Shaker K channel turret. Biophys. J. 93:2307-2314, doi:10.1529/biophysj.107.104349 (Pubitemid 47511130)
9. Campos, F.V., B. Chanda, B. Roux, and F. Bezanilla. 2007. Two atomic constraints unambiguously position the S4 segment relative to S1 and S2 segments in the closed state of Shaker K channel. Proc. Natl. Acad. Sci USA. 104:7904-7909. doi:10.1073/pnas.0702638104
10. Chanda, B., O.K. Asamoah, R. Blunck, B. Roux, and F. Bezanilla. 2005. Gating charge displacement, in voltage-gated ion channels involves limited transmembrane movement. Nature, 436:852-856. doi:10.1038/nature03888 (Pubitemid 41160644)
11. Chandy, K.G., and G.A. Gutman. 1995. Voltage-gated potassium channel genes. In Ligand- and Voltage-Gated Ion Channels. R.A. North, editor. CRC Press, Boca Raton, FL. 1-71.
12. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystalogr. D Biol. Crystallogr. 50:760-763. doi:10.1107/S0907444994003112
13. DeLano, W.L. 2002. PyMOL Molecular Viewer. http:// www.pymol.org (accessed March 30, 2010).
14. Dhallan, R.S., K.W. Yau, K.A. Schrader, and R.R. Reed. 1990. Primary structure and functional expression of a cyclic nucleotideactivated channel from olfactory neurons. Nature. 347:184-187. doi:10.1038/347184a0
15. Dokmanič, I., M. Sikić, and S. Tomić. 2008. Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination. Acta Crystallogr. D Biol. Crystallogr. 64:257-263. doi: 10.1107/S090744490706595X (Pubitemid 351348051)
16. Elinder, F., and P. Århem. 2003. Metal ion effects on ion channel gating. Q. Rev. Biophys. 36:373-427. doi:10.1017/S0033583504003932 (Pubitemid 38902194)
17. Engelman, D.M., T.A. Steitz, and A. Goldman. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15:321-353. doi: 10.1146/annurev.bb.15.060186.001541
18. Eswar, N., B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M. Shen, U. Pieper, and A. Sali. 2006. Comparative protein structure modeling with MODELLER. In Current Protocols in Bioinformatics. John Wiley and Sons, Inc., New York. Supplement 15:5.6.1-5.6.30.
19. Hessa, T., H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, H. Andersson, I. Nilsson, S.H. White, and G. von Heijne. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature. 433:377-381. doi:10.1038/nature03216 (Pubitemid 40203311)
20. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538. doi: 10.1126/science.2122519 (Pubitemid 120031778)
21. + channel. Nature. 423:42-48. doi:10.1038/nature01581
22. Kaupp, U.B., T. Niidome, T. Tanabe, S. Terada, W. Bönigk, W. Stühmer, N.J. Cook, K. Kangawa, H. Matsuo, T. Hirose, et al. 1989. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature. 342:762-766. doi:10.1038/342762a0
23. Kyte, J., and R.F. Doolittlde 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132. doi : 10.1016/0022-2836(82)90515-0
24. Lainé, M., M.C. Lin, J.P.A. Bannister, W.R. Silverman, A.F. Mock, B. Roux, and D.M. Papazian. 2003. Atomic proximity between S4 segment and pore domain in Shaker potassium channels. Neuron. 39:467-481. doi: 10.1016/80896-6273(03) 00468-9 (Pubitemid 36937048)
25. Landt, O., H.P. Grunert, and U. Hahn. 1990. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene. 96:125-128. doi:10.1016/0378-1119(90)90351-Q
26. Lin, M.C., and D.M. Papazian. 2007. Differences between ion binding to eag and HERG voltage sensors contribute to differential regulation of activation and deactivation gating. Channels (Austin). 1:429-437.
27. + channel. Science. 309:897-903. doi: 10.1126/science.1116269
28. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005b. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science. 309:903-908. doi:10.1126/science.1116270
29. + channel in a lipid membrane-like environment. Nature. 450:376-382. doi:10.1038/ nature06265
30. Nelson, R.D., G. Kuan, M.H. Saier Jr., and M. Montal. 1999. Modular assembly of voltage-gated channel proteins: a sequence analysis and phylogenetic study. J. Mol Microbiol. Biotechnol. 1:281-287.
31. Papazian, D.M., L.C. Timpe, Y.N. Jan, and L.Y. Jan. 1991. Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature. 349:305-310. doi:10.1038/349305a0 (Pubitemid 21912066)
32. + channel. Neuron, 14:1293-1301. doi:10.1016/0896-6273(95)90276-7
33. + channel. Neuron. 56:124-140. doi:10.1016/j.neuron.2007.09. 023
34. Perozo, E., R. MacKinnon, F. Bezanilla, and E. Stefani. 1993. Gating currents from a nonconducting mutant reveal open-closed conformations in Shaker K+ channels. Neuron. 11:353-358. doi:10.1016/0896-6273(93)90190-3 (Pubitemid 23250352)
35. Perozo, E., L. Santacruz-Toloza, E. Stefani, F. Bezanilla, and D.M. Papazian. 1994, S4 mutations alter gating currents of Shaker K channels. Biophys. J 66:345-354. doi:10.1016/S0006-3495 (94)80783-80790
36. Ruta, V., J. Chen, and R. MacKinnon. 2005. Calibrated measurement of gating-charge arginine displacement in the KvAP voltage-dependent K+ channel. Cell. 123:463-475. doi:10.1016/ j.cell.2005.08.041 (Pubitemid 41546676)
37. + channel. Neuron. 16:1159-1167. doi:10.1016/S0896-6273 (00)80142-80147
38. 2+ modulates voltage-dependent activation in ether-à-go-go potassium channels by binding between transmembrane segments S2 and S3. J. Gen. Physiol 116:663-678. doi:10.1085/jgp.116.5.663
39. +channels. Proc. Natl. Acad. Sci USA. 100:2935-2940. doi:10.1073/pnas.0636603100
40. Silverman, W.R., J.P.A. Bannister, and D.M. Papazian. 2004. Binding site in eag voltage sensor accommodates a variety of ions and is accessible in closed channel. Biophys. J. 87:3110-3121. doi: 10.1529/ biophysj.104.044602
41. + channels: I. Ionic and gating currents. Biophys. J. 66:996-1010. doi:10.1016/S0006-3495(94)80881-l
42. 2+ modulates slow gating transitions and the opening of Drosophila ether-à-go-go potassium channels. J. Gen. Physiol. 115:319-338. doi:10.1085/jgp.115.3.319
43. Tempel, B.L., D.M. Papazian, T.L. Schwarz, Y.N. Jan, and L.Y. Jan. 1987. Sequence of a probable potassium channel component encoded at the Shaker locus of Drosophila. Science. 237:770-775. doi: 10.1126/science.2441471
44. 2+ regulates activation of rate ag potassium channel. Pflugers Arch. 432:301-312. doi:10.1007/ S004240050137
45. Timpe, L.C., T.L. Schwarz, B.L. Tempel, D.M. Papazian, Y.N. Jan, and L.Y. Jan. 1988. Expression of functional potassium channels from Shaker cDNA in Xenopus oocytes. Nature, 331:143-145. doi:10.1038/331143a0 (Pubitemid 18042146)
46. + channel subunits. Biophys. J. 72:1489-1500. doi: 10.1016/S0006-3495 (97) 78797-78806
47. + channel. J. Gen. Physiol. 115:123-138. doi:10.1085/jgp.115.2.123
48. Tombola, F., M.M. Pathak, and E.Y. Isacoff. 2005. Voltage- sensingarginines in a potassium channel permeate and occlude cation-selective pores. Neuron. 45:379-388. doi:10.1016/j.neuron.2004.12.047 (Pubitemid 40188206)
49. Warmke, J.W., and B. Ganetzky. 1994. A family of potassium channel genes related to eag in Drosophila and mammals. Proc. Natl Acad. Sci USA. 91:3438-3442. doi:10.1073/pnas.91.8.3438
50. Warmke, J., R. Drysdale, and B. Ganetzky. 1991. A distinct; potassium channel polypeptide encoded by the Drosophila eag locus. Science. 252:1560-1562. doi:10.1126/science.l840699 (Pubitemid 21917078)
51. Wimley, W.C., and S.H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol 3:842-848. doi:10.1038/nsb1096-842
52. Yarov-Yarovoy, V., D. Baker, and W.A. Catterall. 2006. Voltage sensor conformations in the open and closed states in ROSETTA structural models of K(+) channels. Proc. Natl. Acad. Sci. USA. 103:7292-7297. doi : 10.1073/pnas. 0602350103 (Pubitemid 43727826)