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Molecular biology and biophysical properties of ion channel gating pores

  • Adrien Moreau (a1), Pascal Gosselin-Badaroudine (a1) and Mohamed Chahine (a1) (a2)

Abstract

The voltage sensitive domain (VSD) is a pivotal structure of voltage-gated ion channels (VGICs) and plays an essential role in the generation of electrochemical signals by neurons, striated muscle cells, and endocrine cells. The VSD is not unique to VGICs. Recent studies have shown that a VSD regulates a phosphatase. Similarly, Hv1, a voltage-sensitive protein that lacks an apparent pore domain, is a self-contained voltage sensor that operates as an H+ channel.

VSDs are formed by four transmembrane helices (S1–S4). The S4 helix is positively charged due to the presence of arginine and lysine residues. It is surrounded by two water crevices that extend into the membrane from both the extracellular and intracellular milieus. A hydrophobic septum disrupts communication between these water crevices thus preventing the permeation of ions. The septum is maintained by interactions between the charged residues of the S4 segment and the gating charge transfer center. Mutating the charged residue of the S4 segment allows the water crevices to communicate and generate gating pore or omega pore. Gating pore currents have been reported to underlie several neuronal and striated muscle channelopathies. Depending on which charged residue on the S4 segment is mutated, gating pores are permeant either at depolarized or hyperpolarized voltages. Gating pores are cation selective and seem to converge toward Eisenmann's first or second selectivity sequences. Most gating pores are blocked by guanidine derivatives as well as trivalent and quadrivalent cations. Gating pores can be used to study the movement of the voltage sensor and could serve as targets for novel small therapeutic molecules.

Copyright

Corresponding author

*Author for correspondence: Mohamed Chahine, Centre de recherche, Institut universitaire en santé mentale de Québec 2601 chemin de la Canardière, Quebec City, QC, CanadaG1J 2G3. Tel: 1-418-663-5747, ext. 4723; Fax: 1-418-663-8756; Email: mohamed.chahine@phc.ulaval.ca

References

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Aggarwal, S. K. & Mackinnon, R. (1996). Contribution of the S4 segment to gating charge in the Shaker K+ channel. Neuron 16, 11691177.
Ahern, C. A. & Horn, R. (2005). Focused electric field across the voltage sensor of potassium channels. Neuron 48, 2529.
Amaral, C., Carnevale, V., Klein, M. L. & Treptow, W. (2012). Exploring conformational states of the bacterial voltage-gated sodium channel NavAb via molecular dynamics simulations. Proceedings of the National Academy of Sciences of the United States of America 109, 2133621341.
Armstrong, C. M. & Bezanilla, F. (1973). Currents related to movement of the gating particles of the sodium channels. Nature 242, 459461.
Armstrong, C. M. & Bezanilla, F. (1977). Inactivation of the sodium channel. II. Gating current experiments. The Journal of General Physiology 70, 567590.
Banerjee, A. & Mackinnon, R. (2008). Inferred motions of the S3a helix during voltage-dependent K+ channel gating. Journal of Molecular Biology 381, 569580.
Batulan, Z., Haddad, G. A. & Blunck, R. (2010). An intersubunit interaction between S4–S5 linker and S6 is responsible for the slow off-gating component in Shaker K+ channels. The Journal of Biological Chemistry 285, 1400514019.
Berger, T. K. & Isacoff, E. Y. (2011). The pore of the voltage-gated proton channel. Neuron 72, 9911000.
Calcraft, P. J., Ruas, M., Pan, Z., Cheng, X., Arredouani, A., Hao, X., Tang, J., Rietdorf, K., Teboul, L., Chuang, K. T., Lin, P., Xiao, R., Wang, C., Zhu, Y., Lin, Y., Wyatt, C. N., Parrington, J., Ma, J., Evans, A. M., Galione, A. & Zhu, M. X. (2009). NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596600.
Campos, F. V., 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. Proceedings of the National Academy of Sciences of the United States of America 104, 79047909.
Capes, D. L., Arcisio-Miranda, M., Jarecki, B. W., French, R. J. & Chanda, B. (2012). Gating transitions in the selectivity filter region of a sodium channel are coupled to the domain IV voltage sensor. Proceedings of the National Academy of Sciences of the United States of America 109, 26482653.
Catterall, W. A. (1986). Molecular properties of voltage-sensitive sodium channels. Annual Review of Biochemistry 55, 953985.
Catterall, W. A. (2011). Voltage-gated calcium channels. Cold Spring Harbor Perspectives in Biology 3, a003947.
Cestele, S. & Catterall, W. A. (2000). Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82, 883892.
Cha, A., Ruben, P. C., George, A. L. Jr., Fujimoto, E. & Bezanilla, F. (1999). Voltage sensors in domains III and IV, but not I and II, are immobilized by Na+ channel fast inactivation. Neuron 22, 7387.
Chahine, M., Bennett, P. B., George, A. L. Jr. & Horn, R. (1994). Functional expression and properties of the human skeletal muscle sodium channel. Pflügers Archiv: European Journal of Physiology 427, 136142.
Chanda, B. & Bezanilla, F. (2002). Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. The Journal of General Physiology 120, 629645.
Decoursey, T. E. (2013). Voltage-gated proton channels: molecular biology, physiology, and pathophysiology of the HV family. Physiological Reviews 93, 599652.
Delemotte, L., Klein, M. L. & Tarek, M. (2012). Molecular dynamics simulations of voltage-gated cation channels: insights on voltage-sensor domain function and modulation. Frontiers in Pharmacology 3, 97.
Delemotte, L., Tarek, M., Klein, M. L., Amaral, C. & Treptow, W. (2011). Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations. Proceedings of the National Academy of Sciences of the United States of America, 108, 61096114.
Delemotte, L., Treptow, W., Klein, M. L. & 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. Biophysical Journal, 99, L7274.
Eisenman, G. (1962). Cation selective glass electrodes and their mode of operation. Biophysical Journal 2(Pt 2), 259323.
England, J. L. & Haran, G. (2011). Role of solvation effects in protein denaturation: from thermodynamics to single molecules and back. Annual Review of Physical Chemistry 62, 257277.
Fan, C., Lehmann-Horn, F., Weber, M. A., Bednarz, M., Groome, J. R., Jonsson, M. K. & Jurkat-Rott, K. (2013). Transient compartment-like syndrome and normokalaemic periodic paralysis due to a Ca(v)1.1 mutation. Brain 136(Pt 12), 37753786.
Francis, D. G., Rybalchenko, V., Struyk, A. & Cannon, S. C. (2011). Leaky sodium channels from voltage sensor mutations in periodic paralysis, but not paramyotonia. Neurology 76, 16351641.
Gamal El-Din, T. M., Heldstab, H., Lehmann, C. & Greeff, N. G. (2010). Double gaps along Shaker S4 demonstrate omega currents at three different closed states. Channels (Austin) 4, 93100.
Gao, Z., Zhang, T., Wu, M., Xiong, Q., Sun, H., Zhang, Y., Zu, L., Wang, W. & Li, M. (2010). Isoform-specific prolongation of Kv7 (KCNQ) potassium channel opening mediated by new molecular determinants for drug–channel interactions. Journal of Biological Chemistry 285, 2832228332.
Gonzalez, C., Baez-Nieto, D., Valencia, I., Oyarzun, I., Rojas, P., Naranjo, D. & Latorre, R. (2012). K(+) channels: function–structural overview. Comprehensive Physiology 2, 20872149.
Goodchild, S. J. & Fedida, D. (2012). Contributions of intracellular ions to kv channel voltage sensor dynamics. Frontiers in Pharmacology 3, 114.
Gosselin-Badaroudine, P., Delemotte, L., Moreau, A., Klein, M. L. & Chahine, M. (2012a). Gating pore currents and the resting state of Nav1.4 voltage sensor domains. Proceedings of the National Academy of Sciences of the United States of America 109, 1925019255.
Gosselin-Badaroudine, P., Keller, D. I., Huang, H., Pouliot, V., Chatelier, A., Osswald, S., Brink, M. & Chahine, M. (2012b). A proton leak current through the cardiac sodium channel is linked to mixed arrhythmia and the dilated cardiomyopathy phenotype. PLoS ONE 7, e38331.
Gosselin-Badaroudine, P., Moreau, A. & Chahine, M. (2013). Na 1.5 mutations linked to dilated cardiomyopathy phenotypes: Is the gating pore current the missing link? Channels (Austin) 8, 15.
Groome, J. R., Lehmann-Horn, F., Fan, C., Wolf, M., Winston, V., Merlini, L. & Jurkat-Rott, K. (2014). Nav1.4 mutations cause hypokalaemic periodic paralysis by disrupting IIIS4 movement during recovery. Brain 137, 9981008.
Guy, H. R. & Seetharamulu, P. (1986). Molecular model of the action potential sodium channel. Proceedings of the National Academy of Sciences of the United States of America 83, 508512.
Henrion, U., Renhorn, J., Borjesson, S. I., Nelson, E. M., Schwaiger, C. S., Bjelkmar, P., Wallner, B., Lindahl, E. & Elinder, F. (2012). Tracking a complete voltage-sensor cycle with metal–ion bridges. Proceedings of the National Academy of Sciences of the United States of America 109, 85528557.
Hodgkin, A. L. & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology 117, 500544.
Hong, L., Kim, I. H. & Tombola, F. (2014). Molecular determinants of Hv1 proton channel inhibition by guanidine derivatives. Proceedings of the National Academy of Sciences of the United States of America 111, 99719976.
Hong, L., Pathak, M. M., Kim, I. H., Ta, D. & Tombola, F. (2013). Voltage-sensing domain of voltage-gated proton channel Hv1 shares mechanism of block with pore domains. Neuron 77, 274287.
Ishibashi, K., Suzuki, M. & Imai, M. (2000). Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochemical and Biophysical Research Communications 270, 370376.
Jensen, M. O., Jogini, V., Borhani, D. W., Leffler, A. E., Dror, R. O. & Shaw, D. E. (2012). Mechanism of voltage gating in potassium channels. Science 336, 229233.
Jiang, Y., Lee, A., Chen, J., Ruta, V., Cadene, M., Chait, B. T. & Mackinnon, R. (2003). X-ray structure of a voltage-dependent K+ channel. Nature 423, 3341.
Khalili-Araghi, F., Tajkhorshid, E., Roux, B. & Schulten, K. (2012). Molecular dynamics investigation of the omega-current in the Kv1.2 voltage sensor domains. Biophysical Journal 102, 258267.
Klassen, T. L., Spencer, A. N. & Gallin, W. J. (2008). A naturally occurring omega current in a Kv3 family potassium channel from a platyhelminth. BMC Neuroscience 9, 52.
Koopmann, T. T., Bezzina, C. R. & Wilde, A. A. (2006). Voltage-gated sodium channels: action players with many faces. Annals of Medicine 38, 472482.
Kuzmenkin, A., Bezanilla, F. & Correa, A. M. (2004). Gating of the bacterial sodium channel, NaChBac: voltage-dependent charge movement and gating currents. The Journal of General Physiology 124, 349356.
Lacroix, J. J., Campos, F. V., Frezza, L. & Bezanilla, F. (2013). Molecular bases for the asynchronous activation of sodium and potassium channels required for nerve impulse generation. Neuron 79, 651657.
Leipold, E., Debie, H., Zorn, S., Borges, A., Olivera, B. M., Terlau, H. & Heinemann, S. H. (2007). muO conotoxins inhibit NaV channels by interfering with their voltage sensors in domain-2. Channels (Austin), 1, 253262.
Li, P., Chen, Z., Xu, H., Sun, H., Li, H., Liu, H., Yang, H., Gao, Z., Jiang, H. & Li, M. (2013). The gating charge pathway of an epilepsy-associated potassium channel accommodates chemical ligands. Cell Research 23, 11061118.
Li, Q., Wanderling, S., Paduch, M., Medovoy, D., Singharoy, A., Mcgreevy, R., Villalba-Galea, C. A., Hulse, R. E., Roux, B., Schulten, K., Kossiakoff, A. & Perozo, E. (2014). Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nature Structural and Molecular Biology 21, 244252.
Lin, M. C., Hsieh, J. Y., Mock, A. F. & Papazian, D. M. (2011). R1 in the Shaker S4 occupies the gating charge transfer center in the resting state. The Journal of General Physiology 138, 155163.
Long, S. B., Campbell, E. B. & Mackinnon, R. (2005). Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309, 903908.
Long, S. B., Tao, X., Campbell, E. B. & Mackinnon, R. (2007). Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450, 376382.
Mannikko, R., Elinder, F. & Larsson, H. P. (2002). Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages. Nature 419, 837841.
Mannikko, R., Pandey, S., Larsson, H. P. & Elinder, F. (2005). Hysteresis in the voltage dependence of HCN channels: conversion between two modes affects pacemaker properties. The Journal of General Physiology 125, 305326.
Marcus, Y. (2012). The guanidinium ion. The Journal of Chemical Thermodynamics 48, 7074.
Matthews, E., Labrum, R., Sweeney, M. G., Sud, R., Haworth, A., Chinnery, P. F., Meola, G., Schorge, S., Kullmann, D. M., Davis, M. B. & Hanna, M. G. (2009). Voltage sensor charge loss accounts for most cases of hypokalemic periodic paralysis. Neurology 72, 15441547.
Mccusker, E. C., Bagneris, C., Naylor, C. E., Cole, A. R., D'Avanzo, N., Nichols, C. G. & Wallace, B. A. (2012). Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing. Nature Communications 3, 1102.
Misra, S. N., Kahlig, K. M. & George, A. L. Jr. (2008). Impaired Nav1.2 function and reduced cell surface expression in benign familial neonatal-infantile seizures. Epilepsia 49, 15351545.
Moreau, A., Gosselin-Badaroudine, P. & Chahine, M. (2014). Biophysics, pathophysiology, and pharmacology of ion channel gating pores. Frontiers in Pharmacology 5, 53.
Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K. & Okamura, Y. (2005). Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 12391243.
Musset, B., Smith, S. M., Rajan, S., Morgan, D., Cherny, V. V. & Decoursey, T. E. (2011). Aspartate 112 is the selectivity filter of the human voltage-gated proton channel. Nature 480, 273277.
Nilius, B. & Owsianik, G. (2011). The transient receptor potential family of ion channels. Genome Biology 12, 218.
Noda, M., Shimizu, S., Tanabe, T., Takai, T., Kayano, T., Ikeda, T., Takahashi, H., Nakayama, H., Kanaoka, Y., Minamino, N., Kangawa, K., Matsuo, H., Raftery, M. A., Hirose, T., Inayama, S., Hayashida, H., Miyat, T. & Numa, S. (1984). Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312, 121127.
Olcese, R., Latorre, R., Toro, L., Bezanilla, F. & Stefani, E. (1997). Correlation between charge movement and ionic current during slow inactivation in Shaker K+ channels. The Journal of General Physiology 110, 579589.
Payandeh, J., Gamal El-Din, T. M., Scheuer, T., Zheng, N. & Catterall, W. A. (2012). Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486, 135139.
Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. (2011). The crystal structure of a voltage-gated sodium channel. Nature 475, 353358.
Peretz, A., Pell, L., Gofman, Y., Haitin, Y., Shamgar, L., Patrich, E., Kornilov, P., Gourgy-Hacohen, O., Ben-Tal, N. & Attali, B. (2010). Targeting the voltage sensor of Kv7.2 voltage-gated K+ channels with a new gating-modifier. Proceedings of the National Academy of Sciences of the United States of America 107, 1563715642.
Piper, D. R., Varghese, A., Sanguinetti, M. C. & Tristani-Firouzi, M. (2003). Gating currents associated with intramembrane charge displacement in HERG potassium channels. Proceedings of the National Academy of Sciences of the United States of America 100, 1053410539.
Pless, S. A., Galpin, J. D., Niciforovic, A. P. & Ahern, C. A. (2011). Contributions of counter-charge in a potassium channel voltage-sensor domain. Nature Chemical Biology 7, 617623.
Pomes, R. & Roux, B. (2002). Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophysical Journal 82, 23042316.
Posson, D. J., Ge, P., Miller, C., Bezanilla, F. & Selvin, P. R. (2005). Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer. Nature 436, 848851.
Quill, T. A., Sugden, S. A., Rossi, K. L., Doolittle, L. K., Hammer, R. E. & Garbers, D. L. (2003). Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proceedings of the National Academy of Sciences of the United States of America 100, 1486914874.
Ramsey, I. S., Mokrab, Y., Carvacho, I., Sands, Z. A., Sansom, M. S. & Clapham, D. E. (2010). An aqueous H+ permeation pathway in the voltage-gated proton channel Hv1. Nature Structural and Molecular Biology 17, 869875.
Ren, D., Navarro, B., Perez, G., Jackson, A. C., Hsu, S., Shi, Q., Tilly, J. L. & Clapham, D. E. (2001). A sperm ion channel required for sperm motility and male fertility. Nature 413, 603609.
Sasaki, M., Takagi, M. & Okamura, Y. (2006). A voltage sensor-domain protein is a voltage-gated proton channel. Science 312, 589592.
Seoh, S. A., Sigg, D., Papazian, D. M. & Bezanilla, F. (1996). Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 16, 11591167.
Shirokov, R., Levis, R., Shirokova, N. & Rios, E. (1992). Two classes of gating current from L-type Ca channels in guinea pig ventricular myocytes. The Journal of General Physiology 99, 863895.
Sigworth, F. J. (1994). Voltage gating of ion channels. Quarterly Reviews of Biophysics 27, 140.
Sokolov, S., Scheuer, T. & Catterall, W. A. (2005). Ion permeation through a voltage-sensitive gating pore in brain sodium channels having voltage sensor mutations. Neuron 47, 183189.
Sokolov, S., Scheuer, T. & Catterall, W. A. (2007). Gating pore current in an inherited ion channelopathy. Nature 446, 7678.
Sokolov, S., Scheuer, T. & Catterall, W. A. (2008). Depolarization-activated gating pore current conducted by mutant sodium channels in potassium-sensitive normokalemic periodic paralysis. Proceedings of the National Academy of Sciences of the United States of America 105, 1998019985.
Sokolov, S., Scheuer, T. & Catterall, W. A. (2010). Ion permeation and block of the gating pore in the voltage sensor of NaV1.4 channels with hypokalemic periodic paralysis mutations. The Journal of General Physiology 136, 225236.
Starace, D. M. & Bezanilla, F. (2004). A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427, 548553.
Starace, D. M., Stefani, E. & Bezanilla, F. (1997). Voltage-dependent proton transport by the voltage sensor of the Shaker K+ channel. Neuron 19, 13191327.
Stevens, M., Peigneur, S. & Tytgat, J. (2011). Neurotoxins and their binding areas on voltage-gated sodium channels. Frontiers in Pharmacology 2, 71.
Struyk, A. F. & Cannon, S. C. (2007). A Na+ channel mutation linked to hypokalemic periodic paralysis exposes a proton-selective gating pore. The Journal of General Physiology 130, 1120.
Struyk, A. F., Markin, V. S., Francis, D. & Cannon, S. C. (2008). Gating pore currents in DIIS4 mutations of NaV1.4 associated with periodic paralysis: saturation of ion flux and implications for disease pathogenesis. The Journal of General Physiology 132, 447464.
Stuhmer, W., Conti, F., Suzuki, H., Wang, X. D., Noda, M., Yahagi, N., Kubo, H. & Numa, S. (1989). Structural parts involved in activation and inactivation of the sodium channel. Nature 339, 597603.
Takeshita, K., Sakata, S., Yamashita, E., Fujiwara, Y., Kawanabe, A., Kurokawa, T., Okochi, Y., Matsuda, M., Narita, H., Okamura, Y. & Nakagawa, A. (2014). X-ray crystal structure of voltage-gated proton channel. Nature Structural and Molecular Biology 21, 352357.
Tao, X., Lee, A., Limapichat, W., Dougherty, D. A. & Mackinnon, R. (2010). A gating charge transfer center in voltage sensors. Science 328, 6773.
Tombola, F., Pathak, M. M., Gorostiza, P. & Isacoff, E. Y. (2007). The twisted ion-permeation pathway of a resting voltage-sensing domain. Nature 445, 546549.
Tombola, F., Pathak, M. M. & Isacoff, E. Y. (2005). Voltage-sensing arginines in a potassium channel permeate and occlude cation-selective pores. Neuron 45, 379388.
Vargas, E., Yarov-Yarovoy, V., Khalili-Araghi, F., Catterall, W. A., Klein, M. L., 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. The Journal of General Physiology 140, 587594.
Villalba-Galea, C. A., Sandtner, W., Starace, D. M. & Bezanilla, F. (2008). S4-based voltage sensors have three major conformations. Proceedings of the National Academy of Sciences of the United States of America 105, 1760017607.
Volkers, L., Kahlig, K. M., Verbeek, N. E., Das, J. H., Van Kempen, M. J., Stroink, H., Augustijn, P., Van Nieuwenhuizen, O., Lindhout, D., George, A. L. Jr., Koeleman, B. P. & Rook, M. B. (2011). Nav 1.1 dysfunction in genetic epilepsy with febrile seizures-plus or Dravet syndrome. European Journal of Neuroscience 34, 12681275.
Wang, X., Zhang, X., Dong, X. P., Samie, M., Li, X., Cheng, X., Goschka, A., Shen, D., Zhou, Y., Harlow, J., Zhu, M. X., Clapham, D. E., Ren, D. & Xu, H. (2012). TPC proteins are phosphoinositide- activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372383.
Wuttke, T. V., Jurkat-Rott, K., Paulus, W., Garncarek, M., Lehmann-Horn, F. & Lerche, H. (2007). Peripheral nerve hyperexcitability due to dominant-negative KCNQ2 mutations. Neurology 69, 20452053.
Xiao, Y., Blumenthal, K. M. & Cummins, T. R. (2014). Gating pore currents demonstrate selective and specific modulation of individual sodium channel voltage sensors by biological toxins. Molecular Pharmacology 86, 159167.
Yang, N., George, A. L. Jr. & Horn, R. (1996). Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16, 113122.
Yang, N. & Horn, R. (1995). Evidence for voltage-dependent S4 movement in sodium channels. Neuron 15, 213218.
Yu, F. H. & Catterall, W. A. (2004). The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Science's STKE: Signal Transduction Knowledge Environment 2004, re15.
Yu, F. H., Yarov-Yarovoy, V., Gutman, G. A. & Catterall, W. A. (2005). Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacological Reviews 57, 387395.
Yuan, A., Santi, C. M., Wei, A., Wang, Z. W., Pollak, K., Nonet, M., Kaczmarek, L., Crowder, C. M. & Salkoff, L. (2003). The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37, 765773.
Zhang, X., Ren, W., Decaen, P., Yan, C., Tao, X., Tang, L., Wang, J., Hasegawa, K., Kumasaka, T., He, J., Wang, J., Clapham, D. E. & Yan, N. (2012). Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486, 130134.
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