Coupled motions between pore and voltage-sensor domains: A model for Shaker B, a voltage-gated potassium channel

Biophysical Journal

Volumn 87, Issue 4, 2004, Pages 2365-2379

  Treptow, Werner ^a,b   Maigret, Bernard ^a   Chipot, Christophe ^a   Tarek, Mounir ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITY OF BRASILIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

DOCKING PROTEIN; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY; PROTEIN SUBUNIT; VOLTAGE GATED POTASSIUM CHANNEL; POTASSIUM; POTASSIUM CHANNEL; SHAKER POTASSIUM CHANNEL;

ARTICLE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; HYDRATION; ION CONDUCTANCE; ION CURRENT; LIPID BILAYER; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; MOLECULAR MODEL; POROSITY; PROTEIN ANALYSIS; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CHEMICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; COMPUTER SIMULATION; EVALUATION; MOTION; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; VALIDATION STUDY;

COMPUTER SIMULATION; ION CHANNEL GATING; MEMBRANE POTENTIALS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOTION; POROSITY; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 15244339069     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.039628     Document Type: Article

References (93)

1. 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.
2. Amadei, A., A. B. M. Linssen, and H. J. C. Berendsen. 1993. Essential dynamics of proteins. Proteins Struct. Funct. Genet. 17:412-425.
3. Åqvist, J., and V. Luzhkov. 2000. Ion permeation mechanism of the potassium channel. Nature. 404:881-884.
4. Beckstein, O., P. C. Biggin, P. Bond, J. N. Bright, C. Domene, A. Grottesi, J. Holyoake, and M. S. P. Sansom. 2003. Ion channel gating: insights via molecular dynamics. FEBS Lett. 555:85-90.
5. Bell, D., H. Yao, R. Saenger, J. Riley, and S. Sielgelbaum. 2004. Changes in local S4 environment provide a voltage-sensing mechanism for mammalian hyperpolarization-activated HCN channels. J. Gen. Physiol. 123:5-19.
6. + channel in a bilayer membrane. Biophys. J. 78:2900-2917.
7. Bernèche, S., and B. Roux. 2003. A microscopic view of ion conduction through the potassium channel. Proc. Natl. Acad. Sci. USA. 100:8644-8648.
8. Bezanilla, F. 2000. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 80:555-592.
9. Bezanilla, F. 2002. Voltage-sensor movements. J. Gen. Physiol. 120:465-473.
10. Blaustein, R. O., and C. Miller. 2004. Shake, rattle or roll. Nature. 427:499-500.
11. Bright, J. N., I. H. Shrivastava, F. S. Cordes, and M. S. P. Sansom. 2002. Conformational dynamics of helix S6 from Shaker potassium channel: simulation studies. Biopolymers. 64:303-313.
12. Broomand, A., R. Männikkö, P. Larsson, and F. Elinder. 2003. Molecular movement of the voltage sensor in a K channel. J. Gen. Physiol. 122:741-748.
13. + channel model: sensitivity to changes in ions, waters, and membrane environment. J. Phys. Chem. 106:4543-4551.
14. Cha, A., P. C. Ruben, A. L. George, E. Fujimoto, and F. Bezanilla. 1999. Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature. 402:813-817.
15. Choe, S. 2002. Potassium channel structures. Nat. Rev. Neurosci. 3:115-121.
16. Chung, S. H., and S. Kuyucak. 2002. Recent advances in ion channel research. Biochim. Biophys. Acta. 1565:267-286.
17. Cohen, B. E., M. Grabe, and L. Y. Jan. 2003. Answers and questions from the KvAP structures. Neuron. 39:395-400.
18. Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16:10881-10890.
19. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald - an Nlog(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
20. de Groot, B. L., A. Amadei, R. M. Scheek, N. A. J. van Nuland, and H. J. C. Berendsen. 1996. An extended sampling of the configurational space of HPr from E. coli. Proteins Struct. Funct. Genet. 26:314-322.
21. + channel and its structural implications. Nature. 403:321-325.
22. Domene, C., S. Haider, and M. S. P. Sansom. 2003. Ion channel structures: a review of recent progress. Curr. Opin. Drug Discov. Dev. 6:611-619.
23. Domene, C., and M. S. Sansom. 2003. Potassium channel, ions, and water: simulation studies based on the high resolution x-ray structure of KcsA. Biophys. J. 85:2787-2800.
24. + conduction and selectivity. Science. 280:69-77.
25. Eisenberg, D., E. Schwarz, M. Komaromy, and R. Wall. 1984. Analysis of membrane and protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179:125-142.
26. Flower, D. R. 1997. SERF: a program for accessible surface area calculations. J. Mol. Graph. Model. 15:238-244.
27. Frishman, D., and P. Argos. 1995. Knowledge-based protein secondary structure assignment. Proteins. 23:566-579.
28. Gandhi, C., E. Clark, E. Loots, A. Pralle, and E. Isacoff. 2003. The orientation and molecular movement of a potassium channel voltage-sensing domain. Neuron. 40:515-525.
29. Green, M. E. 2002. Water as a structural element in a channel: gating in the KcsA channel, and implications for voltage-gated ion channels. J. Biomol. Struct. Dyn. 19:725-730.
30. Hess, B. 2002. Convergence of sampling in protein simulations. Phys. Rev. E. 65:1-10.
31. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer, Sunderland, MA.
32. Hodgkin, A. L., and A. F. Huxley. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.). 117:500-544.
33. + channel. J. Gen. Physiol. 115:51-58.
34. Horiuchi, T., and N. Go. 1991. Projection of Monte Carlo and molecular dynamics trajectories onto normal mode axes: human lysozyme. Proteins. 10:106-116.
35. Horn, R. 2000. Conversation between voltage sensors and gates of ion channels. Biochemistry. 39:15653-15658.
36. Ichiye, T., and M. Karplus. 1991. Collective motions in proteins: a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulation. Proteins. 11:205-217.
37. + channel. Nature. 353:86-90.
38. Islas, L. D., and F. J. Sigworth. 2001. Electrostatics and the gating pore of Shaker potassium channels. J. Gen. Physiol. 117:69-89.
39. Izaguirre, J. A., S. Reich, and R. D. Skeel. 1999. Longer timesteps for molecular dynamics. J. Chem. Phys. 110:9853-9864.
40. Jan, L. Y., and Y. N. Jan. 1994. Potassium channels and their evolving gates. Nature. 371:119-122.
41. Jan, L. Y., and Y. N. Jan. 1997. Cloned potassium channels from eukaryotes and prokaryotes. Annu. Rev. Neurosci. 20:91-123.
42. Jiang, Y., A. Lee, J. Chen, M. Cadene, B. T. Chalt, and R. Mackinnon. 2002. The open pore conformation of potassium channels. Nature. 417:523-526.
43. + channel. Nature. 423:33-41.
44. + channel. Nature. 423:42-48.
45. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
46. Kalé, L., R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz, J. Phillips, A. Shinozaki, K. Varadarajan, and K. Schulten. 1999. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151:283-312.
47. + channels lacking the "tetramerization" domain: implications for pore structure. Nat. Struct. Biol. 6:1122-1125.
48. Koprowski, P., and A. Kubalski. 2001. Bacterial ion channels and their eukariotic homologues. Bioessays. 23:1148-1158.
49. Kreusch, A., P. J. Pfaffinger, C. F. Stevens, and S. Choe. 1998. Crystal structure of the tetramerization domain of the Shaker potassium channel. Nature. 392:945-948.
50. Krogh, A., B. Larsson, G. von Heijne, and E. L. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
51. Lainé, M., M. A. 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.
52. + channel S4. Neuron. 16:387-397.
53. Lee, H. C., J. M. Wang, and K. J. Swartz. 2003. Interaction between extracellular hanatoxin and the resting conformation of the voltage-sensor paddle in Kv channels. Neuron. 40:527-536.
54. + channel. J. Gen. Physiol. 115:33-49.
55. Lu, Z., A. M. Klem, and Y. Ramu. 2001. Ion conduction pore is conserved among potassium channels. Nature. 413:809-813.
56. Luzhkov, V., J. Nilsson, P. Arhem, and J. Åqvist. 2003. Computational modelling of the open-state Kv 1.5 ion channel block by bupivacaine. Biochim. Biophys. Acta. 1652:35-51.
57. MacKerell, A. D., Jr., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, W. E. Reiher III, B. Roux, M. Schlenkrich, J. C. Smith, R. Stole, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
58. + channels in pulmonary hypertension. Vasc. Pharmacol. 38:25-33.
59. Mannuzzu, L. M., and E. Y. Isacoff. 2000. Independence and cooperativity in rearrangements of a potassium channel voltage sensor revealed by single subunit fluorescence. J. Gen. Physiol. 115:257-268.
60. McCollum, I. L., Y. Y. Vilin, E. Spackman, E. Fujimoto, and P. C. Ruben. 2003. Negatively charged residues adjacent to IFM motif in the DIII-DIV linker of hNa(V)1.4 differentially affect slow inactivation. FEBS Lett. 552:163-169.
61. Merlino, A., L. Vitagliano, M. A. Ceruso, A. Di Nola, and L. Mazzarela. 2002. Global and local motions in ribonuclease A: a molecular dynamics study. Biopolymers. 65:274-283.
62. Milkman, R. 1994. An Escherichia coli homologue of eukaryotic potassium channel proteins. Proc. Natl. Acad. Sci. USA. 91:3510-3514.
63. + channel. J. Gen. Physiol. 113:415-423.
64. Neale, E. J., D. J. S. Elliott, M. Hunter, and A. Sivaprasadarao. 2003. Evidence for intersubunit interactions between S4 and S5 transmembrane segments of the Shaker potassium channel. J. Biol. Chem. 278:29079-29085.
65. Ohlenschlager, O., H. Hojo, R. Ramachandran, M. Gorlach, and P. I. Haris. 2002. Three-dimensional structure of the S4-S5 segment of the Shaker potassium channel. Biophys. J. 82:2995-3002.
66. + channel activation gating. Science. 285:73-78.
67. + channel selectively modulates channel gating. Proc. Natl Acad. Sci. USA. 92:9422-9426.
68. Popot, J.-L., and D. M. Engelman. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry. 2721:4031-4037.
69. + channel pore. Eur. Biophys. J. 30:295-303.
70. Roux, B. 1997. Influence of the membrane potential on the free energy of an intrinsic protein. Biophys. J. 73:2980-2989.
71. Roux, B. 2002. Theoretical and computational models of ion channels. Curr. Opin. Struct. Biol. 12:182-189.
72. + channel. Nature. 422:180-185.
73. Sato, C., Y. Ueno, K. Asal, K. Takahashi, M. Sato, A. Engel, and Y. Fujiyoshi. 2001. The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature. 409:1047-1051.
74. Schoppa, N. E., and F. J. Sigworth. 1998. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channel. J. Gen. Physiol. 111:313-342.
75. + channel. Neuron. 16:1159-1167.
76. + channel and the energy landscape of activation. Proc. Natl. Acad. Sci. USA. 100:7611-7615.
77. Smart, O. S., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 72:1109-1126.
78. Sokolova, O., L. Kolmakova-Partensky, and N. Grigorieff. 2001. Three-dimensional structure of a voltage-gated potassium channel at 2.5 nm resolution. Structure (Camb.). 9:215-220.
79. Starace, D. M., and F. Bezanilla. 2001. Histidine scanning mutagenesis of basic residues of the S4 segment of the Shaker potassium channel. J. Gen. Physiol. 117:469-490.
80. 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.
81. + channel. Neuron. 19:1319-1327.
82. Stern, H. A., and S. E. Feller. 2003. Calculation of the dielectric permittivity profile for a nonuniform system: application to a lipid bilayer simulation. J. Chem. Phys. 118:3401-3412.
83. Tieleman, D. P., J. H. C. Berendsen, and M. S. P. Sansom. 2001. Voltage-dependent insertion of alamethicin at phospholipid/water and octane water interfaces. Biophys. J. 80:331-346.
84. Tieleman, D. P., L. R. Forrest, M. S. P. Sansom, and H. J. C. Berendsen. 1998. Lipid properties and the orientation of aromatic residues in OmpF, Influenza M2 and alamethicin systems: molecular dynamics simulations. Biochemistry. 37:17544-17561.
85. Tieleman, D. P., B. Hess, and M. S. P. Sansom. 2002. Analysis and evaluation of channel models: simulations of alamethicin. Biophys. J. 83:2393-2407.
86. + channel subunits. Biophys. J. 72:1489-1500.
87. Tristani-Firouzi, M., J. Chen, and M. Sanguinetti. 2002. Interactions between S4-S5 linker and S6 transmembrane domain modulate gating of HERG potassium channels. J. Biol. Chem. 277:18994-19000.
88. Tusnády, G. E., and I. Simon. 1998. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283:489-506.
89. Vakser, A., and C. Aflalo. 1994. Hydrophobic docking: a proposed enhancement to molecular recognition techniques. Proteins. 20:320-329.
90. Webster, S. M., D. del Camino, J. P. Dekker, and G. Yellen. 2004. Intracellular gate opening in Shaker K1 channels defined by high-affinity metal bridges. Nature. 428:864-868.
91. Yang, N., A. L. J. George, and R. Horn. 1996. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 16:113-122.
92. Yellen, G. 2002. The voltage-gated potassium channels and their relatives. Nature. 419:35-42.
93. 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. 411:657-661.