Coupling of S4 helix translocation and S6 gating analyzed by molecular-dynamics simulations of mutated Kv channels

Biophysical Journal

Volumn 97, Issue 1, 2009, Pages 90-100

  Nishizawa, Manami ^a   Nishizawa, Kazuhisa ^a  

^a TEIKYO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL KV1.2; PROTEIN KV 2.1 CHANNEL; SHAB POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; ENERGY; MOLECULAR DYNAMICS; PROTEIN CONFORMATION;

COMPUTER SIMULATION; KV1.2 POTASSIUM CHANNEL; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; SHAB POTASSIUM CHANNELS; TIME FACTORS; WATER;

EID: 68949118408     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.074     Document Type: Article

References (67)

1. Hille, B. 2001. Ion Channels of Excitable Membranes, 3rd ed. Sinauer, Sunderland, MA., 131-160.
2. Jan, L. Y., and Y. N. Jan. 1997. Voltage-gated and inwardly rectifying potassium channels. J. Physiol. 505:267-282.
3. + channels. Proc. Natl. Acad. Sci. USA. 95:8585-8589.
4. + channel. Nature. 423:33-41.
5. + channel. Science. 309:897-903.
6. + channel. Neuron. 32:649-656.
7. + channels. J. Gen. Physiol. 126:419-428.
8. + channel. Neuron. 16:1169-1177.
9. + channel. Neuron. 56:124-140.
10. + channel in a lipid membrane-like environment. Nature. 450:376-382.
11. Gandhi, C. S., and E. Y. Isacoff. 2002. Molecular models of voltage sensing. J. Gen. Physiol. 120:455-463.
12. Lecar, H., H. P. Larsson, and M. Grabe. 2003. Electrostatic model of S4 motion in voltage-gated ion channels. Biophys. J. 85:2854-2864.
13. Chanda, B., O. K. Asamoah, R. Blunck, B. Roux, and F. Bezanilla. 2005. Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement. Nature. 436:852-856.
14. Campos, F. V., B. Chanda, B. Roux, and F. Bezanilla. 2007. Two atomic constraints unambiguously position the S4 segment relative to S1 and S2 segments in the closed state of Shaker K channel. Proc. Natl. Acad. Sci. USA. 104:7904-7909.
15. 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. 117:500-544.
16. Armstrong, C. M., and F. Bezanilla. 1973. Currents related to movement of the gating particles of the sodium channels. Nature. 242: 459-461.
17. 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.
18. + channels: II. The components of gating currents and a model of channel activation. Biophys. J. 66:1011-1021.
19. + channels. Neuron. 11:353-358.
20. Horn, R., S. Ding, and H. J. Gruber. 2000. Immobilizing the moving parts of voltage-gated ion channels. J. Gen. Physiol. 116:461-476.
21. 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.
22. Soler-Llavina, G. J., T.-H. Chang, and K. J. Swartz. 2006. Functional interactions at the interface between voltage-sensing and pore domains in the Shaker Kv channel. Neuron. 52:623-634.
23. Schoppa, N. E., and F. J. Sigworth. 1998. Activation of Shaker potassium channels I. Characterization of voltage-dependent transitions. J. Gen. Physiol. 111:271-294.
24. 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.
25. + channels. J. Gen. Physiol. 120:663-676.
26. Yifrach, O. 2004. Hill coefficient for estimating the magnitude of cooperativity in gating transitions of voltage-dependent ion channels. Biophys. J. 87:822-830.
27. Labro, A. J., A. L. Raes, and D. J. Snyders. 2005. Coupling of voltage sensing to channel opening reflects intrasubunit interactions in Kv channels. J. Gen. Physiol. 125:71-80.
28. + channels. J. Biol. Chem. 277:18994-19000.
29. Ding, S., and R. Horn. 2003. Effect of S6 tail mutations on charge movement in Shaker potassium channels. Biophys. J. 84:295-305.
30. Decher, N., J. Chen, and M. C. Sanguinetti. 2004. Voltage-dependent gating of hyperpolarization-activated, cyclic nucleotide-gated pacemaker channels. J. Biol. Chem. 279:13859-13865.
31. Ash, W. L., M. R. Zlomislic, E. O. Oloo, and D. P. Tieleman. 2004. Computer simulations of membrane proteins. Biochim. Biophys. Acta. 1666:158-189.
32. Gumbart, J. Y., A. Wang, E. Aksimentiev, and K. Schulten. 2005. Molecular dynamics simulations of proteins in lipid bilayers. Curr. Opin. Struct. Biol. 15:423-431.
33. Kandt, C., W. L. Ash, and D. P. Tieleman. 2007. Setting up and running molecular dynamics simulations of membrane proteins. Methods. 41:475-488.
34. Sotomayor, M., V. Vasquez, E. Perozo, and K. Schulten. 2007. Ion conduction through MscS as determined by electrophysiology and simulation. Biophys. J. 92:886-902.
35. Treptow, W., B. Maigret, C. Chipot, and M. Tarek. 2004. Coupled motions between pore and voltage-sensor domains: a model for Shaker B, a voltage-gated potassium channel. Biophys. J. 87:2365-2379.
36. Treptow, W., and M. Tarek. 2006. Environment of the gating charges in the Kv1.2 Shaker potassium channel. Biophys. J. 90:L64-L66.
37. + channel in a membrane environment. Biophys. J. 93:3070-3082.
38. Tieleman, D. P., and H. J. C. Berendsen. 1996. Molecular dynamics simulations of fully hydrated DPPC with different macroscopic boundary conditions and parameters. J. Chem. Phys. 105:4871-4880.
39. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and J. Hermans. 1981. Intermolecular Forces, Interaction Models for Water in Relation to Protein Hydration. D. Reidel Publishing Co., Dordrecht, The Netherlands., 331-342.
40. Nishizawa, M., and K. Nishizawa. 2007. Molecular dynamics simulations of a stretch-activated channel inhibitor GsMTx4 with lipid membranes: two binding modes and effects of lipid structure. Biophys. J. 92:4233-4243.
41. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
42. 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.
43. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
44. + channel. Cell. 123:463-475.
45. Shrivastava, I. H., and M. S. P. Sansom. 2000. Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophys. J. 78:557-570.
46. Tieleman, D. P. 2004. The molecular basis of electroporation. BMC Biochem. 5:10.
47. Smart, O. S., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460.
48. Kumar, S., D. Bouzida, R. H. Swensen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13:1011-1021.
49. Kanevsky, M., and R. W. Aldrich. 1999. Determinants of voltage-dependent gating and open-state stability in the S5 segment of Shaker potassium channels. J. Gen. Physiol. 114:215-242.
50. Kitaguchi, T., M. Sukhareva, and K. J. Swartz. 2004. Stabilizing the closed S6 gate in the Shaker Kv channel through modification of a hydrophobic seal. J. Gen. Physiol. 124:319-332.
51. + channel modulates its interaction with scaffold proteins. Proc. Natl. Acad. Sci. USA. 104:13022-13027.
52. Nishizawa, M., and K. Nishizawa. 2008. Molecular dynamics simulation of Kv channel voltage sensor helix in a lipid membrane with applied electric field. Biophys. J. 95:1729-1744.
53. + channel of known structure. J. Gen. Physiol. 131:549-561.
54. 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.
55. 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. 111:421-439.
56. + channel. J. Gen. Physiol. 119:521-531.
57. Marks, T. N., and S. W. Jones. 1992. Calcium currents in the A7r5 smooth muscle-derived cell line. An allosteric model for calcium channel activation and dihydropyridine agonist action. J. Gen. Physiol. 99:367-390.
58. + channel. J. Gen. Physiol. 110:257-281.
59. +). J. Gen. Physiol. 114:305-336.
60. Altomare, C., A. Bucchi, E. Camatini, M. Baruscotti, C. Viscomi, et al. 2001. Integrated allosteric model of voltage gating of HCN channels. J. Gen. Physiol. 117:519-532.
61. Sukhareva, M., D. H. Hackos, and K. J. Swartz. 2003. Constitutive activation of the Shaker Kv channel. J. Gen. Physiol. 122:541-556.
62. Chapman, M. L., and A. M. J. VanDongen. 2005. K channel subconductance levels results from heteromeric pore conformations. J. Gen. Physiol. 126:87-103.
63. Monod, J., J. Wyman, and J. P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88-118.
64. Changeux, J. P., and S. J. Edelstein. 1998. Allosteric receptors after 30 years. Neuron. 21:959-980.
65. Chapman, M. L., H. M. A. VanDongen, and A. M. L. VanDongen. 1997. Activation-dependent subconductance levels in the drk1 K channel suggest a subunit basis for ion permeation and gating. Biophys. J. 72:708-719.
66. Zheng, J., and F. J. Sigworth. 1997. Selectivity changes during activation of mutant Shaker potassium channels. J. Gen. Physiol. 110:101-117.
67. Hoshi, T., W. N. Zagotta, and R. W. Aldrich. 1994. Shaker potassium channel gating I: transition near the open state. J. Gen. Physiol. 103:249-278.