Molecular template for a voltage sensor in a novel K+ channel. I. Identification and functional characterization of KvLm, a voltage-gated K+ channel from Listeria monocytogenes

Journal of General Physiology

Volumn 128, Issue 3, 2006, Pages 283-292

  Santos, Jose S ^a   Lundby, Alicia ^a,b   Zazueta, Cecilia ^a,c   Montal, Mauricio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOSOME; POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; DEPOLARIZATION; EUKARYOTIC CELL; LISTERIA MONOCYTOGENES; SENSOR; SPHEROPLAST;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; DROSOPHILA; GENOME, BACTERIAL; ION CHANNEL GATING; LISTERIA MONOCYTOGENES; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; SEQUENCE ALIGNMENT; SPHEROPLASTS;

EID: 33748103925     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609572     Document Type: Article

References (78)

1. Ache, P., D. Becker, N. Ivashikina, P. Dietrich, M.R. Roelfsema, and R. Hedrich. 2000. GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K(+)-selective, K(+)-sensing ion channel. FEBS Lett. 486:93-98.
2. Aggarwal, S.K., and R. MacKinnon. 1996. Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron. 16:1169-1177.
3. Ahern, C.A., and R. Horn. 2004. Specificity of charge-carrying residues in the voltage sensor of potassium channels. J. Gen. Physiol. 123:205-216.
4. Bell, D.C., H. Yao, R.C. Saenger, J.H. Riley, and S.A. Siegelbaum. 2004. Changes in local S4 environment provide a voltage-sensing mechanism for mammalian hyperpolarization-activated HCN channels. J. Gen. Physiol. 123:5-19.
5. Bezanilla, F. 2000. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 80:555-592.
6. Caprini, M., M. Fava, P. Valente, G. Fernandez-Ballester, C. Rapisarda, S. Ferroni, and A. Ferrer-Montiel. 2005. Molecular compatibility of the channel gate and the N terminus of S5 segment for voltage-gated channel activity. J. Biol. Chem. 280:18253-18264.
7. Caprini, M., S. Ferroni, R. Planells-Cases, J. Rueda, C. Rapisarda, A. Ferrer-Montiel, and M. Montal. 2001. Structural compatibility between the putative voltage sensor of voltage-gated K+ channels and the prokaryotic KcsA channel. J. Biol. Chem. 276:21070-21076.
8. Cohen, B.E., M. Grabe, and L.Y. Jan. 2003. Answers and questions from the KvAP structures. Neuron. 39:395-400.
9. Cuello, L.G., D.M. Cortes, and E. Perozo. 2004. Molecular architecture of the KvAP voltage-dependent K+ channel in a lipid bilayer. Science. 306:491-495.
10. Ding, S., and R. Horn. 2002. Tail end of the s6 segment: role in permeation in shaker potassium channels. J. Gen. Physiol. 120:87-97.
11. Ding, S., L. Ingleby, C.A. Ahern, and R. Horn. 2005. Investigating the putative glycine hinge in Shaker potassium channel. J. Gen. Physiol. 126:213-226.
12. Doyle, D.A., J. Morais Cabral, R.A. Pfuetzner, A. Kuo, J.M. Gulbis, S.L. Cohen, B.T. Chait, and R. MacKinnon. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 280:69-77.
13. Eddy, S.R. 1998. Profile hidden Markov models. Bioinformatics. 14:755-763.
14. Elliott, D.J., E.J. Neale, Q. Aziz, J.P. Dunham, T.S. Munsey, M. Hunter, and A. Sivaprasadarao. 2004. Molecular mechanism of voltage sensor movements in a potassium channel. EMBO J. 23:4717-4726.
15. Ferroni, S., R. Planells-Cases, C.M. Ahmed, and M. Montal. 1992. Expression of a genomic clone encoding a brain potassium channel in mammalian cells using lipofection. Eur. Biophys. J. 21:185-191.
16. Gambale, F., and M. Montal. 1990. Voltage-gated sodium channels expressed in the human cerebellar medulloblastoma cell line TE671. Brain Res. Mol. Brain Res. 7:123-129.
17. Gonnet, G.H., M.A. Cohen, and S.A. Benner. 1992. Exhaustive matching of the entire protein sequence database. Science. 256:1443-1445.
18. Gonzalez, C., F.J. Morera, E. Rosenmann, O. Alvarez, and R. Latorre. 2005. S3b amino acid residues do not shuttle across the bilayer in voltage-dependent Shaker K+ channels. Proc. Natl. Acad. Sci. USA. 102:5020-5025.
19. Harvey, A.L. 2001. Twenty years of dendrotoxins. Toxicon. 39:15-26.
20. Heginbotham, L., L. Kolmakova-Partensky, and C. Miller. 1998. Functional reconstitution of a prokaryotic K+ channel. J. Gen. Physiol. 111:741-749.
21. Heginbotham, L., and R. MacKinnon. 1993. Conduction properties of the cloned Shaker K+ channel. Biophys. J. 65:2089-2096.
22. Hille, B. 2001. Ion Channels of Excitable Cells. Third edition. Sinauer, Sunderland, MA. 814 pp.
23. Hurst, R.S., L. Toro, and E. Stefani. 1996. Molecular determinants of external barium block in Shaker potassium channels. FEBS Lett. 388:59-65.
24. Imredy, J.P., and R. MacKinnon. 2000. Energetic and structural interactions between delta-dendrotoxin and a voltage-gated potassium channel. J. Mol. Biol. 296:1283-1294.
25. Jiang, Q.X., D.N. Wang, and R. MacKinnon. 2004. Electron microscopic analysis of KvAP voltage-dependent K+ channels in an open conformation. Nature. 430:806-810.
26. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002a. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522.
27. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002b. The open pore conformation of potassium channels. Nature. 417:523-526.
28. Jiang, Y., A. Lee, J. Chen, V. Ruta, M. Cadene, B.T. Chait, and R. MacKinnon. 2003a. X-ray structure of a voltage-dependent K+ channel. Nature. 423:33-41.
29. Jiang, Y., V. Ruta, J. Chen, A. Lee, and R. MacKinnon. 2003b. The principle of gating charge movement in a voltage-dependent K+ channel. Nature. 423:42-48.
30. Keller, B.U., R.P. Hartshorne, J.A. Talvenheimo, W.A. Catterall, and M. Montal. 1986. Sodium channels in planar lipid bilayers. Channel gating kinetics of purified sodium channels modified by batrachotoxin. J. Gen. Physiol. 88:1-23.
31. Kuo, A., J.M. Gulbis, J.F. Antcliff, T. Rahman, E.D. Lowe, J. Zimmer, J. Cuthbertson, F.M. Ashcroft, T. Ezaki, and D.A. Doyle. 2003. Crystal structure of the potassium channel KirBac1.1 in the closed state. Science. 300:1922-1926.
32. Labarca, P., J.A. Rice, D.R. Fredkin, and M. Montal. 1985. Kinetic analysis of channel gating. Application to the cholinergic receptor channel and the chloride channel from Torpedo californica. Biophys. J. 47:469-478.
33. Larsson, H.P., O.S. Baker, D.S. Dhillon, and E.Y. Isacoff. 1996. Transmembrane movement of the shaker K+ channel S4. Neuron. 16:387-397.
34. + channel KAT1. J. Gen. Physiol. 122:459-469.
35. Long, S.B., E.B. Campbell, and R. MacKinnon. 2005a. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 309:897-903.
36. Long, S.B., E.B. Campbell, and R. MacKinnon. 2005b. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science. 309:903-908.
37. Lu, Z., A.M. Klem, and Y. Ramu. 2001. Ion conduction pore is conserved among potassium channels. Nature. 413:809-813.
38. Lundby, A., J.S. Santos, C. Zazueta, and M. Montal. 2006. Molecular template for a voltage sensor in a novel K+ channel. II. Conservation of a eukaryotic sensor fold in a prokaryotic K+ channel. J. Gen. Physiol. 128:293-300.
39. Magidovich, E., and O. Yifrach. 2004. Conserved gating hinge in ligand- and voltage-dependent K+ channels. Biochemistry. 43:13242-13247.
40. Mannikko, R., F. Elinder, and H.P. Larsson. 2002. Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages. Nature. 419:837-841.
41. Martinac, B., J. Adler, and C. Kung. 1990. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 348:261-263.
42. Miller, A.G., and R.W. Aldrich. 1996. Conversion of a delayed rectifier K+ channel to a voltage-gated inward rectifier K+ channel by three amino acid substitutions. Neuron. 16:853-858.
43. Montal, M. 1990. Molecular anatomy and molecular design of channel proteins. FASEB J. 4:2623-2635.
44. Murata, Y., H. Iwasaki, M. Sasaki, K. Inaba, and Y. Okamura. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature. 435:1239-1243.
45. Myers, M.P., R. Khanna, E.J. Lee, and D.M. Papazian. 2004. Voltage sensor mutations differentially target misfolded K+ channel subunits to proteasomal and non-proteasomal disposal pathways. FEBS Lett. 568:110-116.
46. 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.
47. Niu, X., X. Qian, and K.L. Magleby. 2004. Linker-gating ring complex as passive spring and Ca(2+)-dependent machine for a voltage-and Ca(2+)-activated potassium channel. Neuron. 42:745-756.
48. Papazian, D.M., X.M. Shao, S.A. Seoh, A.F. Mock, Y. Huang, and D.H. Wainstock. 1995. Electrostatic interactions of S4 voltage sensor in Shaker K+ channel. Neuron. 14:1293-1301.
49. 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.
50. Patten, C.D., M. Caprini, R. Planells-Cases, and M. Montal. 1999. Structural and functional modularity of voltage-gated potassium channels. FEBS Lett. 463:375-381.
51. Perozo, E., D.M. Papazian, E. Stefani, and F. Bezanilla. 1992. Gating currents in Shaker K+ channels. Implications for activation and inactivation models. Biophys. J. 62:160-168, discussion 169-171.
52. 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.
53. Planells-Cases, R., A.V. Ferrer-Montiel, C.D. Patten, and M. Montal. 1995. Mutation of conserved negatively charged residues in the S2 and S3 transmembrane segments of a mammalian K+ channel selectively modulates channel gating. Proc. Natl. Acad. Sci. USA. 92:9422-9426.
54. Posson, D.J., P. Ge, C. Miller, F. Bezanilla, and P.R. Selvin. 2005. Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer. Nature. 436:848-851.
55. Ramsey, I.S., M.M. Moran, J.A. Chong, and D.E. Clapham. 2006. A voltage-gated proton-selective channel lacking the pore domain. Nature. 440:1213-1216.
56. Ren, D., B. Navarro, H. Xu, L. Yue, Q. Shi, and D.E. Clapham. 2001. A prokaryotic voltage-gated sodium channel. Science. 294:2372-2375.
57. Rhoads, D.B., F.B. Waters, and W. Epstein. 1976. Cation transport in Escherichia coli. VIII. Potassium transport mutants. J. Gen. Physiol. 67:325-341.
58. 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.
59. Ruta, V., Y. Jiang, A. Lee, J. Chen, and R. MacKinnon. 2003. Functional analysis of an archaebacterial voltage-dependent K+ channel. Nature. 422:180-185.
60. Sasaki, M., M. Takagi, and Y. Okamura. 2006. A voltage sensor-domain protein is a voltage-gated proton channel. Science. 312:589-592.
61. Sato, Y., Y. Hosoo, M. Sakaguchi, and N. Uozumi. 2003a. Requirement of negative residues, Asp 95 and Asp 105, in S2 on membrane integration of a voltage-dependent K+ channel, KAT1. Biosci. Biotechnol. Biochem. 67:923-926.
62. Sato, Y., M. Sakaguchi, S. Goshima, T. Nakamura, and N. Uozumi. 2003b. Molecular dissection of the contribution of negatively and positively charged residues in S2, S3, and S4 to the final membrane topology of the voltage sensor in the K+ channel, KAT1. J. Biol. Chem. 278:13227-13234.
63. Schachtman, D.P., J.I. Schroeder, W.J. Lucas, J.A. Anderson, and R.F. Gaber. 1992. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science. 258:1654-1658.
64. Seoh, S.A., D. Sigg, D.M. Papazian, and F. Bezanilla. 1996. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron. 16:1159-1167.
65. Sesti, F., S. Rajan, R. Gonzalez-Colaso, N. Nikolaeva, and S.A. Goldstein. 2003. Hyperpolarization moves S4 sensors inward to open MVP, a methanococcal voltage-gated potassium channel. Nat. Neurosci. 6:353-361.
66. Shao, X.M., and D.M. Papazian. 1993. S4 mutations alter the single-channel gating kinetics of Shaker K+ channels. Neuron. 11:343-352.
67. Shealy, R.T., A.D. Murphy, R. Ramarathnam, E. Jakobsson, and S. Subramaniam. 2003. Sequence-function analysis of the K+-selective family of ion channels using a comprehensive alignment and the KcsA channel structure. Biophys. J. 84:2929-2942.
68. Shi, N., S. Ye, A. Alam, L. Chen, and Y. Jiang. 2006. Atomic structure of a Na+- and K+-conducting channel. Nature. 440:570-574.
69. Starace, D.M., and F. Bezanilla. 2004. A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature. 427:548-553.
70. Stefani, E., L. Toro, E. Perozo, and F. Bezanilla. 1994. Gating currents of cloned Shaker potassium channels. In Handbook of Membrane Channels: Molecular and Cellular Physiology. C. Peracchia, editor. Academic Press, San Diego, CA. 29-40.
71. Stuhmer, W., F. Conti, H. Suzuki, X.D. Wang, M. Noda, N. Yahagi, H. Kubo, and S. Numa. 1989. Structural parts involved in activation and inactivation of the sodium channel. Nature. 339:597-603.
72. 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 Shaker locus of Drosophila. Science. 237:770-775.
73. Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
74. Tiwari-Woodruff, S.K., M.A. Lin, C.T. Schulteis, and D.M. Papazian. 2000. Voltage-dependent structural interactions in the Shaker K+ channel. J. Gen. Physiol. 115:123-138.
75. + channel subunits. Biophys. J. 72:1489-1500.
76. Yifrach, O., and R. MacKinnon. 2002. Energetics of pore opening in a voltage-gated K(+) channel. Cell. 111:231-239.
77. Yu, F.H., V. Yarov-Yarovoy, G.A. Gutman, and W.A. Catterall. 2005. Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol. Rev. 57:387-395.
78. Zhao, Y., T. Scheuer, and W.A. Catterall. 2004. Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc. Natl. Acad. Sci. USA. 101:17873-17878.