Computer simulations of voltage-gated potassium channel KvAP
Corresponding Author
D. Peter Tieleman
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, CanadaT2N 1N4Search for more papers by this authorKindal M. Robertson
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Search for more papers by this authorJustin L. Maccallum
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Search for more papers by this authorLuca Monticelli
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Centre for Biomolecular Interdisciplinary Studies and Industrial Applications, University of Milan, Milan, Italy
Search for more papers by this authorCorresponding Author
D. Peter Tieleman
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, CanadaT2N 1N4Search for more papers by this authorKindal M. Robertson
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Search for more papers by this authorJustin L. Maccallum
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Search for more papers by this authorLuca Monticelli
Dept. of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, Alberta, Canada T2N 1N4
Centre for Biomolecular Interdisciplinary Studies and Industrial Applications, University of Milan, Milan, Italy
Search for more papers by this authorAbstract
The recent crystal structures of the voltage-gated potassium channel KvAP and its isolated voltage-sensing “paddle” (composed of segments S1 to S4) (Jiang et al., Nature 2003, 423, 33–41) challenged existing models of voltage gating and encouraged a large number of experimental and theoretical studies to answer a number of questions about the structure of the physiologically relevant states of voltage-gated potassium channels and their gating mechanism. We describe equilibrium simulations of the KvAP crystal structure. The crystal structure of the full channel undergoes a large conformational change, localized to the S1–S4 domains, as the S1–S4 domains move into the membrane. We also present a model of the closed state, in agreement with the position of the paddle in the paddle model of voltage gating. Finally, we estimate the energetic cost of transferring a single arginine sidechain from water into an octane slab with the approximate hydrophobic thickness of a membrane. © 2004 Wiley Periodicals, Inc. Int J Quantum Chem, 2004
REFERENCES
- 1 Doyle, D. A.; Cabral, J. M.; Pfuetzner, R. A.; Kuo, A.; Gulbis, J. M.; Cohen, S. L.; Cahit, B. T.; MacKinnon, R. Science 1998, 280, 69–77.
- 2 Morais-Cabral, J. H.; Zhou, Y.; MacKinnon, R. Nature 2001, 414, 37–42.
- 3 Jiang, Y.; Lee, A.; Chen, J.; Cadene, M.; Chait, B. T.; MacKinnon, R. Nature 2002, 417, 523–526.
- 4 Kuo, A.; Gulbis, J. M.; Antcliff, J. F.; Rahman, T.; Lowe, E. D.; Zimmer, J.; Cuthbertson, J.; Ashcroft, F. M.; Ezaki, T.; Doyle, D. A. Science 2003, 300, 1922–1926.
- 5 Ruta, V.; Jiang, Y.; Lee, A.; Chen, J.; MacKinnon, R. Nature 2003, 422, 180–185.
- 6 Jiang, Y.; Lee, A.; Chen, J.; Ruta, V.; Cadene, M.; Chait, B. T.; MacKinnon, R. Nature 2003, 423, 33–41.
- 7 Tempel, B. L.; Papazian, D. M.; Schwarz, T. L.; Jan, Y. N.; Jan, L. Y. Science 1987, 237, 770–775.
- 8 Hillle, B. Ion Channels of Excitable Membranes; Sinauer Associates, Inc.: Sunderland; 2001.
- 9 Yellen, G. Nature 2002, 419, 35–42.
- 10 Sansom, M. S. P.; Shrivastava, I. H.; Bright, J. N.; Tate, J.; Capener, C. E.; Biggin, P. C. Biochim Biophys Acta Biomembranes 2002, 1565, 294–307.
- 11 Roux, B. Curr Opin Struct Biol 2002, 12, 182–189.
- 12 Bezanilla, F.; Perozo, E. Adv Protein Chem 2003, 63, 211–241.
- 13 Blaustein, R. O.; Miller, C. Nature 2004, 427, 499–500.
- 14 Starace, D. M.; Bezanilla, F. Nature 2004, 427, 548–553.
- 15 Laine, M.; Lin, M. C.; Bannister, J. P.; Silverman, W. R.; Mock, A. F.; Roux, B.; Papazian, D. M. Neuron 2003, 39, 467–481.
- 16 Jiang, Y.; Ruta, V.; Chen, J.; Lee, A.; MacKinnon, R. Nature 2003, 423, 42–48.
- 17 Miller, C. Nat Struct Biol 2003, 10, 422–424.
- 18 Cohen, B. E.; Grabe, M.; Jan, L. Y. Neuron 2003, 39, 395–400.
- 19 Broomand, A.; Mannikko, R.; Larsson, H. P.; Elinder, F. J Gen Physiol 2003, 122, 741–748.
- 20 Lee, H. C.; Wang, J. M.; Swartz, K. J. Neuron 2003, 40, 527–536.
- 21 Glauner, K. S.; Mannuzzau, L. M.; Gandhi, C. S.; Isacoff, E. Y. Nature 1999, 402, 813–817.
- 22 Cha, A.; Snyder, G. E.; Selvin, P. R.; Bezanilla, F. Nature 1999, 402, 809–813.
- 23 Faraldo-Gomez, J. D.; Smith, G. R.; Sansom, M. S. Eur Biophys J 2002, 31, 217–227.
- 24 Monticelli, L.; Robertson, K. M.; MacCallum, J. L.; Tieleman, D. P. FEBS Lett 2004, 564, 325–332.
- 25 Grubmuller, H.; Heymann, B.; Tavan, P. Science 1996, 271, 997–999.
- 26 Jarzynski, C. Phys Rev Lett 1997, 78, 2690–2693.
- 27 Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. Comp Phys Comm 1995, 95, 43–56.
- 28 Lindahl, E.; Hess, B.; van der Spoel, D. J Mol Model 2001, 7, 306–317.
- 29 Jorgensen, W. L.; Maxwell, D. S.; TiradoRives, J. J Am Chem Soc 1996, 118, 11225–11236.
- 30 MacCallum, J. L.; Tieleman, D. P. J Comput Chem 2003, 24, 1930–1935.
- 31 Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; Hermans, J. In Intermolecular Forces; B. Pullman, Ed.; D. Reidel: Dordrecht, 1981; p 331–342.
- 32 Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. J Chem Phys 1995, 103, 8577–8593.
- 33 Darden, T.; York, D.; Pedersen, L. J Chem Phys 1993, 98, 10089–10092.
- 34 Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. J Chem Phys 1984, 81, 3684–3690.
- 35 Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. J Comput Chem 1997, 18, 1463–1472.
- 36 Miyamoto, S.; Kollman, P. A. J Comput Chem 1992, 13, 952–962.
- 37
Feenstra, K. A.;
Hess, B.;
Berendsen, H. J. C.
J Comput Chem
1999, 20,
786–798.
10.1002/(SICI)1096-987X(199906)20:8<786::AID-JCC5>3.0.CO;2-B CAS PubMed Web of Science® Google Scholar
- 38 Humphrey, W.; Dalke, A.; Schulten, K. J Mol Graphics 1996, 14, 33; 1996, 14.
- 39 Tieleman, D. P.; Leontiadou, H.; Mark, A. E.; Marrink, S. J. J Am Chem Soc 2003, 125, 6382–6383.
- 40 Tieleman, D. P. The molecular basis of electroporation. BMC Biochemistry 2004, 5: 10.
- 41 Sakai, N.; Matile, S. J Am Chem Soc 2003, 125, 14348–14356.