An electrostatic potassium channel opener targeting the final voltage sensor transition

Journal of General Physiology

Volumn 137, Issue 6, 2011, Pages 563-577

  Börjesson, Sara I ^a   Elinder, Fredrik ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

UNSATURATED FATTY ACID; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE POTENTIAL; CHEMICAL STRUCTURE; DRUG EFFECT; ION TRANSPORT; METABOLISM; MUTATION; OOCYTE; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; FATTY ACIDS, UNSATURATED; ION TRANSPORT; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MUTATION; OOCYTES; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY; XENOPUS LAEVIS;

EID: 79958041271     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201110599     Document Type: Article

References (57)

1. Baker, O.S., H.P. Larsson, L.M. Mannuzzu, and E.Y. Isacoff. 1998. Three transmembrane conformations and sequence-dependent displacement of the S4 domain in shaker K+ channel gating. Neuron. 20:1283-1294.
2. Bjelkmar, P., P.S. Niemelä, I. Vattulainen, and E. Lindahl. 2009. Conformational changes and slow dynamics through microsecond polarized atomistic molecular simulation of an integral Kv1.2 ion channel. PLOS Comput. Biol. 5:e1000289.
3. Blom, S.M., N. Schmitt, and H.S. Jensen. 2009. The acrylamide (S)-2 as a positive and negative modulator of Kv7 channels expressed in Xenopus laevis oocytes. PLoS ONE. :e8251.
4. Boland, L.M., and M.M. Drzewiecki. 2008. Polyunsaturated fatty acid modulation of voltage-gated ion channels. Cell Biochem. Biophys. 52:59-84.
5. Börjesson, S.I., and F. Elinder. 2008. Structure, function, and modification of the voltage sensor in voltage-gated ion channels. Cell Biochem. Biophys. 52:149-174.
6. Börjesson, S.I., S. Hammarström, and F. Elinder. 2008. Lipoelectric modification of ion channel voltage gating by polyunsaturated fatty acids. Biophys. J. 95:2242-2253.
7. Börjesson, S.I., T. Parkkari, S. Hammarström, and F. Elinder. 2010. Electrostatic tuning of cellular excitability. Biophys. J. 98:396-403.
8. Broomand, A., and F. Elinder. 2008. Large-scale movement within the voltage-sensor paddle of a potassium channel-support for a helicalscrew motion. Neuron. 59:770-777.
9. Broomand, A., R. Männikkö, H.P. Larsson, and F. Elinder. 2003. Molecular movement of the voltage sensor in a K channel. J. Gen. Physiol. 122:741-748.
10. Catterall, W.A. 1986. Voltage-dependent gating of sodium channels: correlating structure and function. Trends Neurosci. 9:7-10.
11. Catterall, W.A., S. Cestèle, V. Yarov-Yarovoy, F.H. Yu, K. Konoki, and T. Scheuer. 2007. Voltage-gated ion channels and gating modifier toxins. Toxicon. 49:124-141.
12. DeCaen, P.G., V. Yarov-Yarovoy, E.M. Sharp, T. Scheuer, and W.A. Catterall. 2009. Sequential formation of ion pairs during activation of a sodium channel voltage sensor. Proc. Natl. Acad. Sci. USA. 106:22498-22503.
13. Decher, N., A.K. Streit, M. Rapedius, M.F. Netter, S. Marzian, P. Ehling, G. Schlichthörl, T. Craan, V. Renigunta, A. Köhler, et al. 2010. RNA editing modulates the binding of drugs and highly unsaturated fatty acids to the open pore of Kv potassium channels. EMBO J. 29:2101-2113.
14. Elinder, F., and P. Århem. 2003. Metal ion effects on ion channel gating. Q. Rev. Biophys. 36:373-427.
15. Elinder, F., P. Århem, and H.P. Larsson. 2001a. Localization of the extracellular end of the voltage sensor S4 in a potassium channel. Biophys. J. 80:1802-1809.
16. Elinder, F., R. Männikkö, and H.P. Larsson. 2001b. S4 charges move close to residues in the pore domain during activation in a K channel. J. Gen. Physiol. 118:1-10.
17. Guy, H.R., and P. Seetharamulu. 1986. Molecular model of the action potential sodium channel. Proc. Natl. Acad. Sci. USA. 83:508-512.
18. Holmgren, M., Y. Liu, Y. Xu, and G. Yellen. 1996. On the use of thiolmodifying agents to determine channel topology. Neuropharmacology. 35:797-804.
19. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538.
20. Keynes, R.D., and F. Elinder. 1998a. Modelling the activation, opening, inactivation and reopening of the voltage-gated sodium channel. Proc. Biol. Sci. 265:263-270.
21. Keynes, R.D., and F. Elinder. 1998b. On the slowly rising phase of the sodium gating current in the squid giant axon. Proc. Biol. Sci. 265:255-262.
22. Keynes, R.D., and F. Elinder. 1999. The screw-helical voltage gating of ion channels. Proc. Biol. Sci. 266:843-852.
23. Kopljar, I., A.J. Labro, E. Cuypers, H.W. Johnson, J.D. Rainier, J. Tytgat, and D.J. Snyders. 2009. A polyether biotoxin binding site on the lipid-exposed face of the pore domain of Kv channels revealed by the marine toxin gambierol. Proc. Natl. Acad. Sci. USA. 106:9896-9901.
24. Lainé, M., M.C. Lin, J.P. 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.
25. Lange, W., J. Geissendörfer, A. Schenzer, J. Grötzinger, G. Seebohm, T. Friedrich, and M. Schwake. 2009. Refinement of the binding site and mode of action of the anticonvulsant Retigabine on KCNQ K+ channels. Mol. Pharmacol. 75:272-280.
26. Leaf, A., Y.F. Xiao, J.X. Kang, and G.E. Billman. 2003. Prevention of sudden cardiac death by n-3 polyunsaturated fatty acids. Pharmacol. Ther. 98:355-377.
27. Lecar, H., H.P. Larsson, and M. Grabe. 2003. Electrostatic model of S4 motion in voltage-gated ion channels. Biophys. J. 85:2854-2864.
28. Ledwell, J.L., and R.W. Aldrich. 1999. Mutations in the S4 region isolate the final voltage-dependent cooperative step in potassium channel activation. J. Gen. Physiol. 113:389-14.
29. Lefevre, F., and N. Aronson. 2000. Ketogenic diet for the treatment of refractory epilepsy in children: a systematic review of efficacy. Pediatrics. 105:E46.
30. Long, S.B., X. Tao, E.B. Campbell, and R. MacKinnon. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membranelike environment. Nature. 450:376-382.
31. MacKinnon, R., L. Heginbotham, and T. Abramson. 1990. Mapping the receptor site for charybdotoxin, a pore-blocking potassium channel inhibitor. Neuron. 5:767-771.
32. McLaughlin, S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:113-136.
33. Milescu, M., F. Bosmans, S. Lee, A.A. Alabi, J.I. Kim, and K.J. Swartz. 2009. Interactions between lipids and voltage sensor paddles detected with tarantula toxins. Nat. Struct. Mol. Biol. 16:1080-1085.
34. Pathak, M., L. Kurtz, F. Tombola, and E. Isacoff. 2005. The cooperative voltage sensor motion that gates a potassium channel. J. Gen. Physiol. 125:57-69.
35. Peretz, A., L. Pell, Y. Gofman, Y. Haitin, L. Shamgar, E. Patrich, P. Kornilov, O. Gourgy-Hacohen, N. Ben-Tal, and B. Attali. 2010. Targeting the voltage sensor of Kv7.2 voltage-gated K+ channels with a new gating-modifier. Proc. Natl. Acad. Sci. USA. 107:15637-15642.
36. 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. 1:353-358.
37. Phillips, L.R., and K.J. Swartz. 2010. Position and motions of the S4 helix during opening of the Shaker potassium channel. J. Gen. Physiol. 136:629-644.
38. Rooney, E.K., J.M. East, O.T. Jones, J. McWhirter, A.C. Simmonds, and A.G. Lee. 1983. Interaction of fatty acids with lipid bilayers. Biochim. Biophys. Acta. 728:159-170.
39. Schmidt, D., Q.X. Jiang, and R. MacKinnon. 2006. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature. 444:775-779.
40. Schoppa, N.E., and F.J. Sigworth. 1998. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J. Gen. Physiol. 11:313-342.
41. Schoppa, N.E., K. McCormack, M.A. Tanouye, and F.J. Sigworth. 1992. The size of gating charge in wild-type and mutant Shaker potassium channels. Science. 255:1712-1715.
42. Schow, E.V., J.A. Freites, K. Gogna, S.H. White, and D.J. Tobias. 2010. Down-state model of the voltage-sensing domain of a potassium channel. Biophys. J. 98:2857-2866.
43. Sfondouris, J., L. Rajagopalan, F.A. Pereira, and W.E. Brownell. 2008. Membrane composition modulates prestin-associated charge movement. J. Biol. Chem. 283:22473-2481.
44. Shafrir, Y., S.R. Durell, and H.R. Guy. 2008. Models of voltage-dependent conformational changes in NaChBac channels. Biophys. J. 95:3663-3676.
45. Sigg, D., E. Stefani, and F. Bezanilla. 1994. Gating current noise produced by elementary transitions in Shaker potassium channels. Science. 264:578-582.
46. Smith-Maxwell, C.J., J.L. Ledwell, and R.W. Aldrich. 1998. Uncharged S4 residues and cooperativity in voltage-dependent potassium channel activation. J. Gen. Physiol. 11:421-439.
47. Swartz, K.J. 2007. Tarantula toxins interacting with voltage sensors in potassium channels. Toxicon. 49:213-230.
48. Swartz, K.J., and R. MacKinnon. 1997. Mapping the receptor site for hanatoxin, a gating modifier of voltage-dependent K+ channels. Neuron. 18:675-682.
49. Tao, X., A. Lee, W. Limapichat, D.A. Dougherty, and R. MacKinnon. 2010. A gating charge transfer center in voltage sensors. Science. 328:67-73.
50. + channel. J. Gen. Physiol. 115:123-138.
51. Tombola, F., M.M. Pathak, and E.Y. Isacoff. 2006. How does voltage open an ion channel? Annu. Rev. Cell Dev. Biol. 22:23-52.
52. Villarroel, A., and T.L. Schwarz. 1996. Inhibition of the Kv4 (Shal) family of transient K+ currents by arachidonic acid. J. Neurosci. 16:1016-1025.
53. Xiong, Q., H. Sun, and M. Li. 2007. Zinc pyrithione-mediated activation of voltage-gated KCNQ potassium channels rescues epileptogenic mutants. Nat. Chem. Biol. 3:287-296.
54. Xu, X.P., D. Erichsen, S.I. Börjesson, M. Dahlin, P. Åmark, and F. Elinder. 2008. Polyunsaturated fatty acids and cerebrospinal fluid from children on the ketogenic diet open a voltage-gated K channel: a putative mechanism of antiseizure action. Epilepsy Res. 80:57-66.
55. Xu, Y., Y. Ramu, and Z. Lu. 2008. Removal of phospho-head groups of membrane lipids immobilizes voltage sensors of K+ channels. Nature. 451:826-829.
56. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1994. Shaker potassium channel gating. III: evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362.
57. Zhou, M., J.H. Morais-Cabral, S. Mann, and R. MacKinnon. 2001. Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors. Nature. 411:657-61.