Structural basis for gating charge movement in the voltage sensor of a sodium channel

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 2, 2012, Pages

  Yarov Yarovoy, Vladimir ^a,b   DeCaen, Paul G ^a,c   Westenbroek, Ruth E ^a   Pan, Chien Yuan ^a,d   Scheuer, Todd ^a   Baker, David ^a   Catterall, William A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; VOLTAGE GATED SODIUM CHANNEL;

ARTICLE; CRYSTAL STRUCTURE; ELECTRIC FIELD; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE CHARGE;

AMINO ACID SEQUENCE; ARGININE; BACTERIAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY; ELECTROMAGNETIC FIELDS; ELECTROPHYSIOLOGY; HYDROGEN BONDING; ION CHANNEL GATING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SODIUM CHANNELS;

BACTERIA (MICROORGANISMS);

EID: 84855998904     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1118434109     Document Type: Article

References (61)

1. Hille B (2001) Ion Channels of Excitable Membranes (Sinauer, Sunderland, MA), 3rd Ed.
2. Catterall WA (2000) From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 26:13-25.
3. Yu FH, Catterall WA (2004) The VGL-chanome: A protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004:re15.
4. Ren D, et al. (2001) A prokaryotic voltage-gated sodium channel. Science 294:2372-2375. (Pubitemid 33140564)
5. Koishi R, et al. (2004) A superfamily of voltage-gated sodium channels in bacteria. J Biol Chem 279:9532-9538. (Pubitemid 38296021)
6. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544.
7. Armstrong CM (1981) Sodium channels and gating currents. Physiol Rev 61:644-683.
8. Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555-592.
9. Catterall WA (1986) Voltage-dependent gating of sodium channels: Correlating structure and function. Trends Neurosci 9:7-10.
10. Catterall WA (1986) Molecular properties of voltage-sensitive sodium channels. Annu Rev Biochem 55:953-985.
11. Guy HR, Seetharamulu P (1986) Molecular model of the action potential sodium channel. Proc Natl Acad Sci USA 83:508-512. (Pubitemid 16080043)
12. Sigworth FJ (1994) Voltage gating of ion channels. Q Rev Biophys 27:1-40.
13. Kontis KJ, Rounaghi A, Goldin AL (1997) Sodium channel activation gating is affected by substitutions of voltage sensor positive charges in all four domains. J Gen Physiol 110:391-401. (Pubitemid 27431177)
14. Papazian DM, Timpe LC, Jan YN, Jan LY (1991) Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature 349:305-310. (Pubitemid 21912066)
15. StühmerW, et al. (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597-603. (Pubitemid 19174342)
16. Long SB, Campbell EB, Mackinnon R (2005) Voltage sensor of Kv1.2: Structural basis of electromechanical coupling. Science 309:903-908. (Pubitemid 41099920)
17. Jiang Y, et al. (2003) X-ray structure of a voltage-dependent K+ channel. Nature 423: 33-41.
18. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897-903. (Pubitemid 41099919)
19. + channel in a lipid membrane-like environment. Nature 450:376-382.
20. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353-358.
21. Catterall WA (2010) Ion channel voltage sensors: Structure, function, and pathophysiology. Neuron 67:915-928.
22. Söding J (2005) Protein homology detection by HMM-HMMcomparison. Bioinformatics 21:951-960.
23. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244-W248. (Pubitemid 44529917)
24. Hildebrand A, Remmert M, Biegert A, Söding J (2009) Fast and accurate automatic structure prediction with HHpred. Proteins 77(Suppl 9):128-132.
25. Barth P, Schonbrun J, Baker D (2007) Toward high-resolution prediction and design of transmembrane helical protein structures. Proc Natl Acad Sci USA 104:15682-15687. (Pubitemid 350035360)
26. Yarov-Yarovoy V, Baker D, Catterall WA (2006) Voltage sensor conformations in the open and closed states in ROSETTA structural models of K+ channels. Proc Natl Acad Sci USA 103:7292-7297. (Pubitemid 43727826)
27. Yarov-Yarovoy V, Schonbrun J, Baker D (2006) Multipass membrane protein structure prediction using Rosetta. Proteins 62:1010-1025. (Pubitemid 43364164)
28. André I, Bradley P, Wang C, Baker D (2007) Prediction of the structure of symmetrical protein assemblies. Proc Natl Acad Sci USA 104:17656-17661. (Pubitemid 350210890)
29. Clayton GM, Altieri S, Heginbotham L, Unger VM, Morais-Cabral JH (2008) Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel. Proc Natl Acad Sci USA 105:1511-1515. (Pubitemid 351346545)
30. Campos FV, Chanda B, Roux B, Bezanilla F (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. (Pubitemid 47185849)
31. DeCaen PG, Yarov-Yarovoy V, Zhao Y, Scheuer T, Catterall WA (2008) Disulfide locking a sodium channel voltage sensor reveals ion pair formation during activation. Proc Natl Acad Sci USA 105:15142-15147.
32. DeCaen PG, Yarov-Yarovoy V, Sharp EM, Scheuer T, Catterall WA (2009) Sequential formation of ion pairs during activation of a sodium channel voltage sensor. Proc Natl Acad Sci USA 106:22498-22503.
33. + channel voltage sensor. Proc Natl Acad Sci USA 108:18825-18830.
34. Barth P, Wallner B, Baker D (2009) Prediction of membrane protein structures with complex topologies using limited constraints. Proc Natl Acad Sci USA 106:1409-1414.
35. Chen X, Wang Q, Ni F, Ma J (2010) Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc Natl Acad Sci USA 107:11352-11357.
36. Broomand A, Elinder F (2008) Large-scale movement within the voltage-sensor paddle of a potassium channel-support for a helical-screw motion. Neuron 59:770-777.
37. +channel. Cell 111:231-239.
38. Careaga CL, Falke JJ (1992) Thermal motions of surface alpha-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping. J Mol Biol 226:1219-1235.
39. + channel in a membrane environment. Biophys J 93:3070-3082.
40. Sokolov S, Scheuer T, Catterall WA (2005) Ion permeation through a voltage- sensitive gating pore in brain sodium channels having voltage sensor mutations. Neuron 47:183-189. (Pubitemid 41019250)
41. Sokolov S, Scheuer T, Catterall WA (2010) Ion permeation and block of the gating pore in the voltage sensor of NaV1.4 channels with hypokalemic periodic paralysis mutations. J Gen Physiol 136:225-236.
42. Tombola F, Pathak MM, Gorostiza P, Isacoff EY (2007) The twisted ion-permeation pathway of a resting voltage-sensing domain. Nature 445:546-549. (Pubitemid 46197635)
43. Tombola F, Pathak MM, Isacoff EY (2005) Voltage-sensing arginines in a potassium channel permeate and occlude cation-selective pores. Neuron 45:379-388. (Pubitemid 40188206)
44. Yang N, George AL, Jr., Horn R (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16:113-122. (Pubitemid 26044734)
45. Yang N, George AL, Jr., Horn R (1997) Probing the outer vestibule of a sodium channel voltage sensor. Biophys J 73:2260-2268. (Pubitemid 27471438)
46. Ahern CA, Horn R (2005) Focused electric field across the voltage sensor of potassium channels. Neuron 48:25-29. (Pubitemid 41384163)
47. Islas LD, Sigworth FJ (2001) Electrostatics and the gating pore of Shaker potassium channels. J Gen Physiol 117:69-89. (Pubitemid 32061907)
48. + channel S4. Neuron 16:387-397.
49. Asamoah OK, Wuskell JP, Loew LM, Bezanilla F (2003) A fluorometric approach to local electric field measurements in a voltage-gated ion channel. Neuron 37:85-97. (Pubitemid 36106436)
50. Aggarwal SK, MacKinnon R (1996) Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron 16:1169-1177. (Pubitemid 26227238)
51. Kuzmenkin A, Bezanilla F, Correa AM (2004) Gating of the bacterial sodium channel, NaChBac: Voltage-dependent charge movement and gating currents. J Gen Physiol 124:349-356. (Pubitemid 39346639)
52. + channel. Neuron 16:1159-1167.
53. + channel. Neuron 56:124-140.
54. Posson DJ, Selvin PR (2008) Extent of voltage sensor movement during gating of shaker K+ channels. Neuron 59:98-109. (Pubitemid 351905849)
55. GrabeM, Lai HC, Jain M, Jan YN, Jan LY (2007) Structure prediction for the down state of a potassium channel voltage sensor. Nature 445:550-553. (Pubitemid 46197636)
56. Mannuzzu LM, Moronne MM, Isacoff EY (1996) Direct physical measure of conformational rearrangement underlying potassium channel gating. Science 271:213-216. (Pubitemid 26033303)
57. Glauner KS, Mannuzzu LM, Gandhi CS, Isacoff EY (1999) Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel. Nature 402:813-817.
58. Cha A, Snyder GE, Selvin PR, Bezanilla F (1999) Atomic scale movement of the voltagesensing region in a potassium channel measured via spectroscopy. Nature 402:809-813.
59. Cha A, Bezanilla F (1998) Structural implications of fluorescence quenching in the Shaker K+ channel. J Gen Physiol 112:391-408. (Pubitemid 28467597)
60. Cestèle S, et al. (2006) Structure and function of the voltage sensor of sodium channels probed by a beta-scorpion toxin. J Biol Chem 281:21332-21344. (Pubitemid 44115472)
61. Shafrir Y, Durell SR, Guy HR (2008) Models of voltage-dependent conformational changes in NaChBac channels. Biophys J 95:3663-3676.