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Voltage-dependent gating in K channels: experimental results and quantitative models

  • Luigi CatacuzzenoEmail author
  • Luigi Sforna
  • Fabio FrancioliniEmail author
Invited Review
  • 57 Downloads
Part of the following topical collections:
  1. Invited Review

Abstract

Voltage-dependent K channels open and close in response to voltage changes across the cell membrane. This voltage dependence was postulated to depend on the presence of charged particles moving through the membrane in response to voltage changes. Recording of gating currents originating from the movement of these particles fully confirmed this hypothesis, and gave substantial experimental clues useful for the detailed understanding of the process. In the absence of structural information, the voltage-dependent gating was initially investigated using discrete Markov models, an approach only capable of providing a kinetic and thermodynamic comprehension of the process. The elucidation of the crystal structure of the first voltage-dependent channel brought in a dramatic change of pace in the understanding of channel gating, and in modeling the underlying processes. It was now possible to construct quantitative models using molecular dynamics, where all the interactions of each individual atom with the surroundings were taken into account, and its motion predicted by Newton’s laws. Unfortunately, this modeling is computationally very demanding, and in spite of the advances in simulation procedures and computer technology, it is still limited in its predictive ability. To overcome these limitations, several groups have developed more macroscopic voltage gating models. Their approaches understandably require a number of approximations, which must however be physically well justified. One of these models, based on the description of the voltage sensor as a Brownian particle, that we have recently developed, is able to simultaneously describe the behavior of a single voltage sensor and to predict the macroscopic gating current originating from a population of sensors. The basics of this model are here described, and a typical application using the Kv1.2/2.1 chimera channel structure is also presented.

Keywords

Voltage-dependent gating Voltage-gated potassium channels Mathematical models Gating currents 

Notes

Acknowledgements

This work was supported by Progetto Ricerca di Base 2017, Department of Chemistry, Biology and Biotechnology, University of Perugia and by Progetto Ricerca Finalizzata 2018 #RF-2018-12366215.

Authors’ contribution

LC developed the Brownian model of channel gating; LC and FF designed and wrote the first draft of the Ms; LC, LS, and FF discussed and amended the first draft, and finalized the Ms.

References

  1. 1.
    Aggarwal SK, MacKinnon R (1996) Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron 16:1169–1177PubMedGoogle Scholar
  2. 2.
    Ahern CA, Horn R (2005) Focused electric field across the voltage sensor of potassium channels. Neuron 48:25–29PubMedGoogle Scholar
  3. 3.
    Alberts IL, Nadassy K, Wodak SJ (1998) Analysis of zinc binding sites in protein crystal structures. Protein Sci 7:1700–1716PubMedPubMedCentralGoogle Scholar
  4. 4.
    Armstrong CM (1981) Sodium channels and gating currents. Physiol Rev 61:644–683PubMedGoogle Scholar
  5. 5.
    Armstrong CM, Bezanilla F (1973) Currents related to movement of the gating particles of the sodium channels. Nature 242(5398):459–461PubMedGoogle Scholar
  6. 6.
    Asamoah OK, Wuskell JP, Loew LM, Bezanilla F (2003) A fluorometric approach to local electric field measurements in a voltage-gated ion channel. Neuron 37:85–97PubMedGoogle Scholar
  7. 7.
    Batulan Z, Haddad GA, Blunck R (2010) An intersubunit interaction between S4-S5 linker and S6 is responsible for the slow off-gating component in Shaker K+ channels. J Biol Chem 285:14005–14019.  https://doi.org/10.1074/jbc.M109.097717 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555–592PubMedGoogle Scholar
  9. 9.
    Bezanilla F, Perozo E, Papazian DM, Stefani E (1991) Molecular basis of gating charge immobilization in Shaker potassium channels. Science 254(5032):679–683PubMedGoogle Scholar
  10. 10.
    Bezanilla F, Perozo E, Stefani E (1994) Gating of Shaker K+ channels: II. The components of gating currents and a model of channel activation. Biophys J 66:1011–1021PubMedPubMedCentralGoogle Scholar
  11. 11.
    Blunck R, Batulan Z (2012) Mechanism of electromechanical coupling in voltage-gated potassium channels. Front Pharmacol 3:166.  https://doi.org/10.3389/fphar.2012.00166 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    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 U S A 104:7904–7909PubMedPubMedCentralGoogle Scholar
  13. 13.
    Catacuzzeno L, Franciolini F (2019) Simulation of gating currents of the Shaker K channel using a Brownian model of the voltage sensor. Biophys J 117(10):2005–2019PubMedGoogle Scholar
  14. 14.
    Catacuzzeno L, Fioretti B, Franciolini F (2008) Modeling study of the effects of membrane surface charge on calcium microdomains and neurotransmitter release. Biophys J 95(5):2160–2171PubMedPubMedCentralGoogle Scholar
  15. 15.
    Catterall WA (1986) Molecular properties of voltage-sensitive sodium channels. Annu Rev Biochem 55:953–985PubMedGoogle Scholar
  16. 16.
    Catterall WA (1988) Structure and function of voltage-sensitive ion channels. Science 242(4875):50–61PubMedGoogle Scholar
  17. 17.
    Cha A, Snyder GE, Selvin PR, Bezanilla F (1999) Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature 402(6763):809–813PubMedGoogle Scholar
  18. 18.
    Chanda B, Asamoah OK, Blunck R, Roux B, Bezanilla F (2005) Gating charge displacement in voltage-gated ion channels involves limited trans membrane movement. Nature 436(7052):852–856PubMedGoogle Scholar
  19. 19.
    Chupin L (2010) Fokker-Planck equation in bounded domain. Annales de l'Institut Fourier 60:217–255Google Scholar
  20. 20.
    Conti F, Stühmer W (1989) Quantal charge redistributions accompanying the structural transitions of sodium channels. Eur Biophys J 17(2):53–59PubMedGoogle Scholar
  21. 21.
    Cooper K, Jakobsson E, Wolynes P (1985) The theory of ion transport through membrane channels. Prog Biophys Mol Biol 46(1):51–96PubMedGoogle Scholar
  22. 22.
    DeCaen PG, Yarov-Yarovoy V, Zhao Y, Scheuer T, Catterall WA (2008) Disulfide docking a sodium channel voltage sensor reveals ion pair formation during activation. Proc Natl Acad Sci U S A 105:15142–15147.  https://doi.org/10.1073/pnas.0806486105 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    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 U S A 106:22498–22503.  https://doi.org/10.1073/pnas.0912307106 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    DeCaen PG, Yarov-Yarovoy V, Scheuer T, Catterall WA (2011) Gating charge interactions with the S1 segment during activation of a Na+ channel voltage sensor. Proc Natl Acad Sci U S A 108:18825–18830.  https://doi.org/10.1073/pnas.1116449108 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Delemotte L, Treptow W, Klein ML, Tarek M (2010) Effect of sensor domain mutations on the properties of voltage-gated ion channels: molecular dynamics studies of the potassium channel Kv1.2. Biophys J 99:L72–L74.  https://doi.org/10.1016/j.bpj.2010.08.069 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Delemotte L, Tarek M, Klein ML, Amaral C, Treptow W (2011) Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations. Proc Natl Acad Sci U S A 108:6109–6114.  https://doi.org/10.1073/pnas.1102724108 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Dryga A, Chakrabarty S, Vicatos S, Warshel A (2012a) Realistic simulation of the activation of voltage-gated ion channels. Proc Natl Acad Sci U S A 109:3335–3340.  https://doi.org/10.1073/pnas.1121094109 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Dryga A, Chakrabarty S, Vicatos S, Warshel A (2012b) Coarse grained model for exploring voltage dependent ion channels. Biochim Biophys Acta 1818:303–317.  https://doi.org/10.1016/j.bbamem.2011.07.043 CrossRefPubMedGoogle Scholar
  29. 29.
    Gandhi CS, Clark E, Loots E, Pralle A, Isacoff EY (2003) The orientation and molecular movement of a K(+) channel voltage-sensing domain. Neuron 40:515–525PubMedGoogle Scholar
  30. 30.
    Glauner KS, Mannuzzu LM, Gandhi CS, Isacoff EY (1999) Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel. Nature 402(6763):813–817PubMedGoogle Scholar
  31. 31.
    Greenblatt RE, Blatt Y, Montal M (1985) The structure of the voltage-sensitive sodium channel. Inferences derived from computer-aided analysis of the Electrophorus electricus channel primary structure. FEBS Lett 193:125–134PubMedGoogle Scholar
  32. 32.
    Guy HR, Seetharamulu P (1986) Molecular model of the action potential sodium channel. Proc Natl Acad Sci U S A 83(2):508–512PubMedPubMedCentralGoogle Scholar
  33. 33.
    Haddad GA, Blunck R (2011) Mode shift of the voltage sensors in Shaker K+ channels is caused by energetic coupling to the pore domain. J Gen Physiol 137(5):455–472.  https://doi.org/10.1085/jgp.201010573 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Henrion U, Renhorn J, Börjesson SI, Nelson EM, Schwaiger CS, Bjelkmar P, Wallner B, Lindahl E, Elinder F (2012) Tracking a complete voltage-sensor cycle with metal-ion bridges. Proc Natl Acad Sci U S A 109:8552–8557.  https://doi.org/10.1073/pnas.1116938109 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544PubMedPubMedCentralGoogle Scholar
  36. 36.
    Horng TL, Eisenberg RS, Liu C, Bezanilla F (2019) Continuum gating current models computed with consistent interactions. Biophys J 116:270–282.  https://doi.org/10.1016/j.bpj.2018.11.3140 CrossRefPubMedGoogle Scholar
  37. 37.
    Islas LD, Sigworth FJ (2001) Electrostatics and the gating pore of Shaker potassium channels. J Gen Physiol 117:69–89PubMedPubMedCentralGoogle Scholar
  38. 38.
    Jensen MØ, Jogini V, Borhani DW, Leffler AE, Dror RO, Shaw DE (2012) Mechanism of voltage gating in potassium channels. Science 336(6078):229–233.  https://doi.org/10.1126/science.1216533 CrossRefPubMedGoogle Scholar
  39. 39.
    Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R (2003) X-ray structure of a voltage-dependent K+ channel. Nature. 423(6935):33–41PubMedGoogle Scholar
  40. 40.
    Kalstrup T, Blunck R (2013) Dynamics of internal pore opening in K(V) channels probed by a fluorescent unnatural amino acid. Proc Natl Acad Sci U S A 110:8272–8277.  https://doi.org/10.1073/pnas.1220398110 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kalstrup T, Blunck R (2018) S4-S5 linker movement during activation and inactivation in voltage-gated K(+) channels. Proc Natl Acad Sci U S A 115:E6751–E6759.  https://doi.org/10.1073/pnas.1719105115 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Keynes RD, Rojas E (1974) Kinetics and steady-state properties of the charged system controlling sodium conductance in the squid giant axon. J Physiol 239:393–434PubMedPubMedCentralGoogle Scholar
  43. 43.
    Khalili-Araghi F, Jogini V, Yarov-Yarovoy V, Tajkhorshid E, Roux B, Schulten K (2010) Calculation of the gating charge for the Kv1.2 voltage-activated potassium channel. Biophys J 98:2189–2198.  https://doi.org/10.1016/j.bpj.2010.02.056 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Kim I, Warshel A (2014) Coarse-grained simulations of the gating current in the voltage-activated Kv1.2 channel. Proc Natl Acad Sci U S A 111:2128–2133.  https://doi.org/10.1073/pnas.1324014111 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Labro AJ, Raes AL, Grottesi A, Van Hoorick D, Sansom MS, Snyders DJ (2008) Kv channel gating requires a compatible S4-S5 linker and bottom part of S6, constrained by non-interacting residues. J Gen Physiol 132:667–680.  https://doi.org/10.1085/jgp.200810048 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Lacroix JJ, Campos FV, Frezza L, Bezanilla F (2013) Molecular bases for the asynchronous activation of sodium and potassium channels required for nerve impulse generation. Neuron 79(4):651–657.  https://doi.org/10.1016/j.neuron.2013.05.036 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Lacroix JJ, Hyde HC, Campos FV, Bezanilla F (2014) Moving gating charges through the gating pore in a Kv channel voltage sensor. Proc Natl Acad Sci U S A 111:E1950–E1959.  https://doi.org/10.1073/pnas.1406161111 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Larsson HP, Baker OS, Dhillon DS, Isacoff EY (1996) Transmembrane movement of the Shaker K+ channel S4. Neuron 16:387–397PubMedGoogle Scholar
  49. 49.
    Lemons DS, Gythiel A (1997) Paul Langevin’s 1908 paper “On the Theory of Brownian Motion” [“Sur la théorie du mouvement brownien,” C. R. Acad. Sci. (Paris) 146, 530–533 (1908)]. Am J Phys 65:1079–1081.  https://doi.org/10.1119/1.18725 CrossRefGoogle Scholar
  50. 50.
    Lin MC, Hsieh JY, Mock AF, Papazian DM (2011) R1 in the Shaker S4 occupies the gating charge transfer center in the resting state. J Gen Physiol 138:155–163.  https://doi.org/10.1085/jgp.201110642 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Li-Smerin Y, Hackos DH, Swartz KJ (2000) A localized interaction surface for voltage-sensing domains on the pore domain of a K+ channel. Neuron 25:411–423PubMedGoogle Scholar
  52. 52.
    Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309(5736):897–903PubMedGoogle Scholar
  53. 53.
    Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450(7168):376–382PubMedGoogle Scholar
  54. 54.
    Lu Z, Klem AM, Ramu Y (2001) Ion conduction pore is conserved among potassium channels. Nature 413(6858):809–813PubMedGoogle Scholar
  55. 55.
    Lu Z, Klem AM, Ramu Y (2002) Coupling between voltage sensors and activation gate in voltage-gated K+ channels. J Gen Physiol 120:663–676PubMedPubMedCentralGoogle Scholar
  56. 56.
    Ma LJ, Ohmert I, Vardanyan V (2011) Allosteric features of KCNQ1 gating revealed by alanine scanning mutagenesis. Biophys J 100(4):885–894.  https://doi.org/10.1016/j.bpj.2010.12.3726 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    McCammon JA, Gelin BR, Karplus M (1977) Dynamics of folded proteins. Nature. 267(5612):585–590PubMedGoogle Scholar
  58. 58.
    McCormack K, Joiner WJ, Heinemann SH (1994) A characterization of the activating structural rearrangements in voltage-dependent Shaker K+ channels. Neuron 12:301–315PubMedGoogle Scholar
  59. 59.
    Noceti F, Baldelli P, Wei X, Qin N, Toro L, Birnbaumer L, Stefani E (1996) Effective gating charges per channel in voltage-dependent K+ and Ca2+ channels. J Gen Physiol 108:143–155PubMedGoogle Scholar
  60. 60.
    Noda M, Shimizu S, Tanabe T, Takai T, Kayano T, Ikeda T, Takahashi H, Nakayama H, Kanaoka Y, Minamino N et al (1984) Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312(5990):121–127PubMedGoogle Scholar
  61. 61.
    Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY (1987) Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237(4816):749–753PubMedGoogle Scholar
  62. 62.
    Papazian DM, Shao XM, Seoh SA, Mock AF, Huang Y, Wainstock DH (1995) Electrostatic interactions of S4 voltage sensor in Shaker K+ channel. Neuron 14:1293–1301PubMedGoogle Scholar
  63. 63.
    Pathak MM, Yarov-Yarovoy V, Agarwal G, Roux B, Barth P, Kohout S, Tombola F, Isacoff EY (2007) Closing in on the resting state of the Shaker K(+) channel. Neuron 56:124–140PubMedGoogle Scholar
  64. 64.
    Peyser A, Nonner W (2012a) Voltage sensing in ion channels: mesoscale simulations of biological devices. Phys Rev E Stat Nonlin Soft Matter Phys 86:011910Google Scholar
  65. 65.
    Peyser A, Nonner W (2012b) The sliding-helix voltage sensor: mesoscale views of a robust structure-function relationship. Eur Biophys J 41:705–721.  https://doi.org/10.1007/s00249-012-0847-z CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Pongs O, Kecskemethy N, Müller R, Krah-Jentgens I, Baumann A, Kiltz HH, Canal I, Llamazares S, Ferrus A (1988) Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO J 7(4):1087–1096PubMedPubMedCentralGoogle Scholar
  67. 67.
    Posson DJ, Selvin PR (2008) Extent of voltage sensor movement during gating of Shaker K+ channels. Neuron 59:98–109.  https://doi.org/10.1016/j.neuron.2008.05.006 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Posson DJ, Ge P, Miller C, Bezanilla F, Selvin PR (2005) Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer. Nature 436(7052):848–851PubMedPubMedCentralGoogle Scholar
  69. 69.
    Pusch M, Noda M, Stühmer W, Numa S, Conti F (1991) Single point mutations of the sodium channel drastically reduce the pore permeability without preventing its gating. Eur Biophys J 20:127–133PubMedGoogle Scholar
  70. 70.
    Schneider MF, Chandler WK (1973) Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature 242(5395):244–246PubMedGoogle Scholar
  71. 71.
    Schoppa NE, Sigworth FJ (1998) Activation of Shaker potassium channels: I. Characterization of voltage-dependent transitions. J Gen Physiol 111:271–294PubMedPubMedCentralGoogle Scholar
  72. 72.
    Schoppa NE, McCormack K, Tanouye MA, Sigworth FJ (1992) The size of gating charge in wild-type and mutant Shaker potassium channels. Science 255(5052):1712–1715PubMedGoogle Scholar
  73. 73.
    Schwaiger CS, Bjelkmar P, Hess B, Lindahl E (2011) 310-helix conformation facilitates the transition of a voltage sensor S4 segment toward the down state. Biophys J 100:1446–1454.  https://doi.org/10.1016/j.bpj.2011.02.003 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Seoh SA, Sigg D, Papazian DM, Bezanilla F (1996) Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 16:1159–1167PubMedGoogle Scholar
  75. 75.
    Shrivastava IH, Durell SR, Guy HR (2004) A model of voltage gating developed using the KvAP channel crystal structure. Biophys J 87(4):2255–2270PubMedPubMedCentralGoogle Scholar
  76. 76.
    Sigg D, Stefani E, Bezanilla F (1994) Gating current noise produced by elementary transitions in Shaker potassium channels. Science 264(5158):578–582PubMedGoogle Scholar
  77. 77.
    Sigg D, Bezanilla F, Stefani E (2003) Fast gating in the Shaker K+ channel and the energy landscape of activation. Proc Natl Acad Sci U S A 100:7611–7615PubMedPubMedCentralGoogle Scholar
  78. 78.
    Smith-Maxwell CJ, Ledwell JL, Aldrich RW (1998) Uncharged S4 residues and cooperativity in voltage-dependent potassium channel activation. J Gen Physiol 111:421–439PubMedPubMedCentralGoogle Scholar
  79. 79.
    Soler-Llavina GJ, Chang TH, Swartz KJ (2006) Functional interactions at the interface between voltage-sensing and pore domains in the Shaker K(v) channel. Neuron 52:623–634PubMedGoogle Scholar
  80. 80.
    Starace DM, Bezanilla F (2001) Histidine scanning mutagenesis of basic residues of the S4 segment of the Shaker K+ channel. J Gen Physiol 117:469–490PubMedPubMedCentralGoogle Scholar
  81. 81.
    Starace DM, Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427(6974):548–553PubMedGoogle Scholar
  82. 82.
    Starace DM, Stefani E, Bezanilla F (1997) Voltage-dependent proton transport by the voltage sensor of the Shaker K+ channel. Neuron 19:1319–1327PubMedGoogle Scholar
  83. 83.
    Stühmer W, Conti F, Suzuki H, Wang XD, Noda M, Yahagi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339(6226):597–603PubMedGoogle Scholar
  84. 84.
    Stühmer W, Conti F, Stocker M, Pongs O, Heinemann SH (1991) Gating currents of inactivating and non-inactivating potassium channels expressed in Xenopus oocytes. Pflugers Arch 418:423–429PubMedGoogle Scholar
  85. 85.
    Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328(5974):67–73.  https://doi.org/10.1126/science.1185954 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Tiwari-Woodruff SK, Schulteis CT, Mock AF, Papazian DM (1997) Electrostatic interactions between transmembrane segments mediate folding of Shaker K+ channel subunits. Biophys J 72(4):1489–1500PubMedPubMedCentralGoogle Scholar
  87. 87.
    Tiwari-Woodruff SK, Lin MA, Schulteis CT, Papazian DM (2000) Voltage-dependent structural interactions in the Shaker K(+) channel. J Gen Physiol 115(2):123–138PubMedPubMedCentralGoogle Scholar
  88. 88.
    Tombola F, Pathak MM, Isacoff EY (2005) Voltage-sensing arginines in a potassium channel permeate and occlude cation-selective pores. Neuron 45(3):379–388PubMedGoogle Scholar
  89. 89.
    Tombola F, Pathak MM, Gorostiza P, Isacoff EY (2007) The twisted ion-permeation pathway of a resting voltage-sensing domain. Nature 445(7127):546–549PubMedGoogle Scholar
  90. 90.
    Tytgat J, Hess P (1992) Evidence for cooperative interactions in potassium channel gating. Nature 359(6394):420–423PubMedGoogle Scholar
  91. 91.
    Vardanyan V, Pongs O (2012) Coupling of voltage-sensors to the channel pore: a comparative view. Front Pharmacol 3:145.  https://doi.org/10.3389/fphar.2012.00145 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Vargas E, Bezanilla F, Roux B (2011) In search of a consensus model of the resting state of a voltage-sensing domain. Neuron 72(5):713–720.  https://doi.org/10.1016/j.neuron.2011.09.024 CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Vargas E, Yarov-Yarovoy V, Khalili-Araghi F, Catterall WA, Klein ML, Tarek M, Lindahl E, Schulten K, Perozo E, Bezanilla F, Roux B (2012) An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J Gen Physiol 140:587–594.  https://doi.org/10.1085/jgp.201210873 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Wisedchaisri G, Tonggu L, McCord E, Gamal El-Din TM, Wang L, Zheng N, Catterall WA (2019) Resting-state structure and gating mechanism of a voltage-gated sodium channel. Cell 178:993–1003PubMedGoogle Scholar
  95. 95.
    Yang N, George AL Jr, Horn R (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 16(1):113–122PubMedGoogle Scholar
  96. 96.
    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 U S A 103:7292–7297PubMedPubMedCentralGoogle Scholar
  97. 97.
    Yarov-Yarovoy V, DeCaen PG, Westenbroek RE, Pan CY, Scheuer T, Baker D, Catterall WA (2012) Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc Natl Acad Sci U S A 109:E93–E102.  https://doi.org/10.1073/pnas.1118434109 CrossRefPubMedGoogle Scholar
  98. 98.
    Zagotta WN, Hoshi T, Aldrich RW (1994) Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J Gen Physiol 103:321–362PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Chemistry, Biology and BiotechnologyUniversity of PerugiaPerugiaItaly

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