Position and motions of the S4 helix during opening of the Shaker potassium channel

Journal of General Physiology

Volumn 136, Issue 6, 2010, Pages 629-644

  Phillips, L Revell ^a   Swartz, Kenton J ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SHAKER POTASSIUM CHANNEL;

ANIMAL; ARTICLE; CELL CULTURE; CHANNEL GATING; CHEMISTRY; CHO CELL; CRICETULUS; HAMSTER; HUMAN; PATCH CLAMP; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE;

ANIMALS; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; ION CHANNEL GATING; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, SECONDARY; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 78650049168     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010517     Document Type: Article

References (51)

1. Alberts, I.L., K. Nadassy, and S.J. Wodak. 1998. Analysis of zinc binding sites in protein crystal structures. Protein Sci. 7:1700-1716. doi:10.1002/pro.5560070805
2. Benndorf, K., R. Koopmann, E. Eismann, and U.B. Kaupp. 1999. Gating by cyclic GMP and voltage in the α subunit of the cyclic GMP-gated channel from rod photoreceptors. J. Gen. Physiol. 114:477-490. doi:10.1085/jgp.114.4.477 (Pubitemid 29473418)
3. Bezanilla, F. 2002. Voltage sensor movements. J. Gen. Physiol. 120:465-473. doi:10.1085/jgp.20028660 (Pubitemid 35155089)
4. Bezanilla, F., R.E. Taylor, and J.M. Fernández. 1982. Distribution and kinetics of membrane dielectric polarization. 1. Long-term inactivation of gating currents. J. Gen. Physiol. 79:21-40. (Pubitemid 12207667)
5. Bezanilla, F., E. Perozo, and E. Stefani. 1994. Gating of Shaker K+ channels: II. The components of gating currents and a model of channel activation. Biophys. J. 66:1011-1021. doi:10.1016/ S0006-3495(94)80882-3
6. 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.
7. Chakrapani, S., L.G. Cuello, D.M. Cortes, and E. Perozo. 2008. Structural dynamics of an isolated voltage-sensor domain in a lipid bilayer. Structure. 16:398-409. doi:10.1016/j.str.2007.12.015 (Pubitemid 351324110)
8. Colquhoun, D., and A.G. Hawkes. 1995. A Q-matrix cookbook: How to write only one program to calculate the single-channel and macroscopic predictions for any kinetic mechansim. In Single- Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. 589-636.
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. doi:10.1126/science.1101373 (Pubitemid 39372450)
10. del Camino, D., and G. Yellen. 2001. Tight steric closure at the intracellular activation gate of a voltage-gated K(+) channel. Neuron. 32:649-656.
11. del Camino, D., M. Kanevsky, and G. Yellen. 2005. Status of the intracellular gate in the activated-not-open state of Shaker K+ channels. J. Gen. Physiol. 126:419-428. doi:10.1085/jgp.200509385 (Pubitemid 41565858)
12. Hille, B. 2001. Ion channels of excitable membranes. Third edition. Sinauer, Sunderland, MA. 814 pp.
13. Holmgren, M., K.S. Shin, and G. Yellen. 1998. The activation gate of a voltage-gated K+ channel can be trapped in the open state by an intersubunit metal bridge. Neuron. 21:617-621.
14. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1994. Shaker potassium channel gating. I: Transitions near the open state. J. Gen. Physiol. 103:249-278. doi:10.1085/jgp.103.2.249 (Pubitemid 24068560)
15. Jiang, Y., A. Lee, J. Chen, V. Ruta, M. Cadene, B.T. Chait, and R. MacKinnon. 2003. X-ray structure of a voltage-dependent K+ channel. Nature. 423:33-41. doi:10.1038/nature01580 (Pubitemid 36569577)
16. 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. doi:10.1016/S0896- 6273(03)00468-9 (Pubitemid 36937048)
17. 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. 113:389-414.
18. Lee, S.Y., A. Lee, J. Chen, and R. Mackinnon. 2005. Structure of the KvAP voltage-dependent K+ channel and its dependence on the lipid membrane. Proc. Natl. Acad. Sci. USA. 102:15441-15446.
19. Lewis, A., V. Jogini, L. Blachowicz, M. Lainé, and B. Roux. 2008. Atomic constraints between the voltage sensor and the pore domain in a voltage-gated K+ channel of known structure. J. Gen. Physiol. 131:549-561.
20. Li, M., T. Kawate, S.D. Silberberg, and K.J. Swartz. 2010. Pore-opening mechanism in trimeric P2X receptor channels. Nat. Commun. 1:1-7.
21. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 309:897-903. doi:10.1126/science.1116269 (Pubitemid 41099919)
22. Long, S.B., X. Tao, E.B. Campbell, and R. MacKinnon. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature. 450:376-382. doi:10.1038/ nature06265 (Pubitemid 350126743)
23. Ma, Z., X.J. Lou, and F.T. Horrigan. 2006. Role of charged residues in the S1-S4 voltage sensor of BK channels. J. Gen. Physiol. 127:309-328.
24. Martínez-François, J.R., Y. Xu, and Z. Lu. 2009. Mutations reveal voltage gating of CNGA1 channels in saturating cGMP. J. Gen. Physiol. 134:151-164.
25. Milescu, M., J. Vobecky, S.H. Roh, S.H. Kim, H.J. Jung, J.I. Kim, and K.J. Swartz. 2007. Tarantula toxins interact with voltage sensors within lipid membranes. J. Gen. Physiol. 130:497-511. doi:10 .1085/jgp.200709869 (Pubitemid 350036736)
26. 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. doi:10.1038/nsmb.1679
27. Olcese, R., R. Latorre, L. Toro, F. Bezanilla, and E. Stefani. 1997. Correlation between charge movement and ionic current during slow inactivation in Shaker K+ channels. J. Gen. Physiol. 110:579-589. doi:10.1085/jgp.110.5.579 (Pubitemid 27494947)
28. 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.
29. Phillips, L.R., D. Enkvetchakul, and C.G. Nichols. 2003. Gating dependence of inner pore access in inward rectifier K(+) channels. Neuron. 37:953-962.
30. Ramu, Y., Y. Xu, and Z. Lu. 2006. Enzymatic activation of voltagegated potassium channels. Nature. 442:696-699. doi:10.1038/ nature04880
31. Sack, J.T., and R.W. Aldrich. 2006. Binding of a gating modifier toxin induces intersubunit cooperativity early in the Shaker K channel's activation pathway. J. Gen. Physiol. 128:119-132. doi:10.1085/ jgp.200609492 (Pubitemid 43967555)
32. Schmidt, D., and R. MacKinnon. 2008. Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc. Natl. Acad. Sci. USA. 105:19276-19281.
33. Schmidt, D., Q.X. Jiang, and R. MacKinnon. 2006. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature. 444:775-779. doi:10.1038/nature05416 (Pubitemid 44949608)
34. Schoppa, N.E., and F.J. Sigworth. 1998a. Activation of Shaker potassium channels. I. Characterization of voltage-dependent transitions. J. Gen. Physiol. 111:271-294.
35. Schoppa, N.E., and F.J. Sigworth. 1998b. Activation of Shaker potassium channels. II. Kinetics of the V2 mutant channel. J. Gen. Physiol. 111:295-311. doi:10.1085/jgp.111.2.295 (Pubitemid 28113079)
36. Schoppa, N.E., and F.J. Sigworth. 1998c. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J. Gen. Physiol. 111:313-342. doi:10.1085/ jgp.111.2.313
37. Smith-Maxwell, C.J., J.L. Ledwell, and R.W. Aldrich. 1998a. Role of the S4 in cooperativity of voltage-dependent potassium channel activation. J. Gen. Physiol. 111:399-420. doi:10.1085/jgp.111 .3.399 (Pubitemid 28136461)
38. Smith-Maxwell, C.J., J.L. Ledwell, and R.W. Aldrich. 1998b. Uncharged S4 residues and cooperativity in voltage-dependent potassium channel activation. J. Gen. Physiol. 111:421-439.
39. Stefani, E., L. Toro, E. Perozo, and F. Bezanilla. 1994. Gating of Shaker K+ channels: I. Ionic and gating currents. Biophys. J. 66: 996-1010. (Pubitemid 24106346)
40. Sukhareva, M., D.H. Hackos, and K.J. Swartz. 2003. Constitutive activation of the Shaker Kv channel. J. Gen. Physiol. 122:541-556. doi:10.1085/jgp.200308905 (Pubitemid 37420849)
41. Swartz, K.J. 2004. Towards a structural view of gating in potassium channels. Nat. Rev. Neurosci. 5:905-916. doi:10.1038/nrn1559 (Pubitemid 39593354)
42. Vamvouka, M., J. Cieslak, N. Van Eps, W. Hubbell, and A. Gross. 2008. The structure of the lipid-embedded potassium channel voltage sensor determined by double-electron-electron resonance spectroscopy. Protein Sci. 17:506-517. doi:10.1110/ ps.073310008 (Pubitemid 351281551)
43. Villalba-Galea, C.A., W. Sandtner, D.M. Starace, and F. Bezanilla. 2008. S4-based voltage sensors have three major conformations. Proc. Natl. Acad. Sci. USA. 105:17600-17607.
44. Voets, T., G. Droogmans, U. Wissenbach, A. Janssens, V. Flockerzi, and B. Nilius. 2004. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature. 430:748-754.
45. Voets, T., G. Owsianik, A. Janssens, K. Talavera, and B. Nilius. 2007. TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat. Chem. Biol. 3:174-182. doi:10.1038/nchembio862
46. Webster, S.M., D. Del Camino, J.P. Dekker, and G. Yellen. 2004. Intracellular gate opening in Shaker K+ channels defined by high-affinity metal bridges. Nature. 428:864-868. doi:10.1038/ nature02468
47. 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. doi:10.1038/nature06618 (Pubitemid 351253175)
48. Yellen, G. 2002. The voltage-gated potassium channels and their relatives. Nature. 419:35-42.
49. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1990. Restoration of inactivation in mutants of Shaker potassium channels by a peptide derived from ShB. Science. 250:568-571.
50. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1994a. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362. doi:10.1085/jgp.103.2.321 (Pubitemid 24068562)
51. Zagotta, W.N., T. Hoshi, J. Dittman, and R.W. Aldrich. 1994b. Shaker potassium channel gating. II: Transitions in the activation pathway. J. Gen. Physiol. 103:279-319. doi:10.1085/ jgp.103.2.279 (Pubitemid 24068561)