Skip to main content
SpringerLink
Log in

Structural and Functional Analysis of Sodium Channels Viewed from an Evolutionary Perspective

  • Chapter
  • First Online:
Voltage-gated Sodium Channels: Structure, Function and Channelopathies

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 246))

Abstract

Voltage-gated sodium channels initiate and propagate action potentials in excitable cells. They respond to membrane depolarization through opening, followed by fast inactivation that terminates the sodium current. This ON-OFF behavior of voltage-gated sodium channels underlays the coding of information and its transmission from one location in the nervous system to another. In this review, we explore and compare structural and functional data from prokaryotic and eukaryotic channels to infer the effects of evolution on sodium channel structure and function.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Adelman WJ Jr, Palti Y (1969) The effects of external potassium and long duration voltage conditioning on the amplitude of sodium currents in the giant axon of the squid, Loligo pealei. J Gen Physiol 54:589–606

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ahern CA, Horn R (2005) Focused electric field across the voltage sensor of potassium channels. Neuron 48:25–29

    Article  PubMed  CAS  Google Scholar 

  • Ahern CA, Payandeh J, Bosmans F, Chanda B (2016) The hitchhiker’s guide to the voltage-gated sodium channel galaxy. J Gen Physiol 147:1–24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arrigoni C, Rohaim A, Shaya D, Findeisen F, Stein RA, Nurva SR, Mishra S, McHaourab HS, Minor DL Jr (2016) Unfolding of a temperature-sensitive domain controls voltage-gated channel activation. Cell 164:922–936

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bagneris C, Decaen PG, Hall BA, Naylor CE, Clapham DE, Kay CW, Wallace BA (2013) Role of the C-terminal domain in the structure and function of tetrameric sodium channels. Nat Commun 4:2465

    Article  PubMed  CAS  Google Scholar 

  • Balser JR, Nuss HB, Chiamvimonvat N, Pérez-García MT, Marban E, Tomaselli GF (1996) External pore residue mediates slow inactivation in mu-1 rat skeletal muscle sodium channels. J Physiol 494:431–442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benitah JP, Tomaselli GF, Marban E (1996) Adjacent pore-lining residues within sodium channels identified by paired cysteine mutagenesis. Proc Natl Acad Sci U S A 93:7392–7396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benitah JP, Ranjan R, Yamagishi T, Janecki M, Tomaselli GF, Marban E (1997) Molecular motions within the pore of voltage-dependent sodium channels. Biophys J 73:603–613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555–592

    Article  PubMed  CAS  Google Scholar 

  • Blanchet J, Chahine M (2007) Accessibility of four arginine residues on the S4 segment of the Bacillus halodurans sodium channel. J Membr Biol 215:169–180

    Article  PubMed  CAS  Google Scholar 

  • Capes DL, Goldschen-Ohm MP, Arcisio-Miranda M, Bezanilla F, Chanda B (2013) Domain IV voltage-sensor movement is both sufficient and rate limiting for fast inactivation in sodium channels. J Gen Physiol 142:101–112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Catterall WA (1986a) Molecular properties of voltage-sensitive sodium channels. Annu Rev Biochem 55:953–985

    Article  PubMed  CAS  Google Scholar 

  • Catterall WA (1986b) Voltage-dependent gating of sodium channels: correlating structure and function. Trends Neurosci 9:7–10

    Article  CAS  Google Scholar 

  • Catterall WA (2010) Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67:915–928

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Catterall WA (2012) Voltage-gated sodium channels at 60: structure, function and pathophysiology. J Physiol 590:2577–2589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Catterall WA, Zheng N (2015) Deciphering voltage-gated Na+ and Ca2+ channels by studying prokaryotic ancestors. Trends Biochem Sci 40:526–534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Catterall WA, Goldin AL, Waxman SG (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397–409

    Article  PubMed  CAS  Google Scholar 

  • Chakrabarti N, Ing C, Payandeh J, Zheng N, Catterall WA, Pomes R (2013) Catalysis of Na+ permeation in the bacterial sodium channel NaVAb. Proc Natl Acad Sci U S A 110:11331–11336

    Article  PubMed  PubMed Central  Google Scholar 

  • Chanda B, Bezanilla F (2002) Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J Gen Physiol 120:629–645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cormier JW, Rivolta I, Tateyama M, Yang AS, Kass RS (2002) Secondary structure of the human cardiac Na+ channel C terminus: evidence for a role of helical structures in modulation of channel inactivation. J Biol Chem 277:9233–9241

    Google Scholar 

  • Cuello LG, Romero JG, Cortes DM, Perozo E (1998) pH-dependent gating in the Streptomyces lividans K+ channel. Biochemistry 37:3229–3236

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 105:15142–15147

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deschenes I, Trottier E, Chahine M (2001) Implication of the C-terminal region of the α-subunit of voltage-gated sodium channels in fast inactivation. J Membr Biol 183:103–114

    Article  PubMed  Google Scholar 

  • Favre I, Moczydlowski E, Schild L (1996) On the structural basis for ionic selectivity among Na+, K+, and Ca2+ in the voltage-gated sodium channel. Biophys J 71(6):3110–3125

    Google Scholar 

  • Gabelli SB, Yoder JB, Tomaselli GF, Amzel LM (2016) Calmodulin and Ca(2+) control of voltage gated Na(+) channels. Channels (Austin) 10:45–54

    Google Scholar 

  • Gamal El-Din TM, Grogler D, Lehmann C, Heldstab H, Greeff NG (2008) More gating charges are needed to open a Shaker K+ channel than are needed to open an rBIIA Na+ channel. Biophys J 95:1165–1175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gamal El-Din TM, Heldstab H, Lehmann C, Greeff NG (2010) Double gaps along Shaker S4 demonstrate omega currents at three different closed states. Channels (Austin) 4(2):93–100

    Article  Google Scholar 

  • Gamal El-Din TM, Martinez GQ, Payandeh J, Scheuer T, Catterall WA (2013) A gating charge interaction required for late slow inactivation in the bacterial sodium channel NaVAb. J Gen Physiol 142:181–190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gamal El-Din TM, Scheuer T, Catterall WA (2014) Tracking S4 movement by gating pore currents in the bacterial sodium channel NaChBac. J Gen Physiol 144:147–157

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gamal El-Din TM, Lenaeus MJ, Ramanadane K, Zheng N, Catterall WA (2017) Control of slow, use dependent inactivation of NaVAb by its C-terminal tail. Biophys J 112(3, Suppl 1):105a. https://doi.org/10.1016/j.bpj.2016.11.597

    Article  Google Scholar 

  • Gosselin-Badaroudine P, Delemotte L, Moreau A, Klein ML, Chahine M (2012) Gating pore currents and the resting state of Nav1.4 voltage sensor domains. Proc Natl Acad Sci U S A 109:19250–19255

    Article  PubMed  PubMed Central  Google Scholar 

  • Guy HR, Seetharamulu P (1986) Molecular model of the action potential sodium channel. Proc Natl Acad Sci U S A 83(2):508–512

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heinemann SH, Terlau H, Stuhmer W, Imoto K, Numa S (1992) Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 356:441–443

    Article  PubMed  CAS  Google Scholar 

  • Hille B (1971) The hydration of sodium ions crossing the nerve membrane. Proc Natl Acad Sci U S A 68:280–282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hille B (2001) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Hirschberg B, Rovner A, Lieberman M, Patlak J (1995) Transfer of twelve charges is needed to open skeletal muscle Na+ channels. J Gen Physiol 106:1053–1068

    Article  PubMed  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952a) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 116:449–472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952b) The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol 116:497–506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952c) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952d) The components of membrane conductance in the giant axon of Loligo. J Physiol 116:473–496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Irie K, Shimomura T, Fujiyoshi Y (2012) The C-terminal helical bundle of the tetrameric prokaryotic sodium channel accelerates the inactivation rate. Nat Commun 3:793

    Article  PubMed  CAS  Google Scholar 

  • Isom LL, Ragsdale DS, De Jongh KS, Westenbroek RE, Reber BF, Scheuer T, Catterall WA (1995) Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83:433–442

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002a) Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:515–522

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002b) The open pore conformation of potassium channels. Nature 417:523–526

    Article  PubMed  CAS  Google Scholar 

  • Kellenberger S, West JW, Scheuer T, Catterall WA (1997) Molecular analysis of the putative inactivation particle in the inactivation gate of brain type IIA Na+ channels. J Gen Physiol 109:589–605

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuhn FJ, Greeff NG (1999) Movement of voltage sensor S4 in domain 4 is tightly coupled to sodium channel fast inactivation and gating charge immobilization. J Gen Physiol 114:167–183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsson HP, Baker OS, Dhillon DS, Isacoff EY (1996) Transmembrane movement of the Shaker potassium channel S4. Neuron 16:387–397

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Goodchild SJ, Ahern CA (2012) Local anesthetic inhibition of a bacterial sodium channel. J Gen Physiol 139:507–516

    Article  PubMed  PubMed Central  Google Scholar 

  • Lenaeus MJ, El-Din TMG, Ing C, Ramanadane K, Pomes R, Zheng N, Catterall WA (2017) Structures of closed and open states of a voltage-gated sodium channel. Proc Natl Acad Sci U S A 114:E3051–E3060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Q, Wanderling S, Paduch M, Medovoy D, Singharoy A, McGreevy R, Villalba-Galea CA, Hulse RE, Roux B, Schulten K et al (2014) Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nat Struct Mol Biol 21:244–252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Logothetis DE, Movahedi S, Satler C, Lindpaintner K, Nadal-Ginard B (1992) Incremental reductions of positive charge within the S4 region of a voltage-gated K+ channel result in corresponding decreases in gating charge. Neuron 8:531–540

    Article  PubMed  CAS  Google Scholar 

  • Mantegazza M, Yu FH, Catterall WA, Scheuer T (2001) Role of the C-terminal domain in inactivation of brain and cardiac sodium channels. Proc Natl Acad Sci U S A 98:15348–15353

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCusker EC, Bagneris C, Naylor CE, Cole AR, D’Avanzo N, Nichols CG, Wallace BA (2012) Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing. Nat Commun 3:1102

    Article  PubMed  CAS  Google Scholar 

  • Mio K, Mio M, Arisaka F, Sato M, Sato C (2010) The C-terminal coiled-coil of the bacterial voltage-gated sodium channel NaChBac is not essential for tetramer formation, but stabilizes subunit-to-subunit interactions. Prog Biophys Mol Biol 103:111–121

    Article  PubMed  CAS  Google Scholar 

  • Morais-Cabral JH, Zhou Y, MacKinnon R (2001) Energetic optimization of ion conduction rate by the K+ selectivity filter. Nature 414:37–42

    Article  PubMed  CAS  Google Scholar 

  • Naylor CE, Bagneris C, DeCaen PG, Sula A, Scaglione A, Clapham DE, Wallace BA (2016) Molecular basis of ion permeability in a voltage-gated sodium channel. EMBO J 35:820–830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nguyen HM, Goldin AL (2010) Sodium channel carboxy terminal residue regulates fast inactivation. J Biol Chem 285(12):9077–9089

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ong BH, Tomaselli GF, Balser JR (2000) A structural rearrangement in the sodium channel pore linked to slow inactivation and use dependence. J Gen Physiol 116:653–662

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palti Y, Adelman WJ Jr (1969) Measurement of axonal membrane conductances and capacity by means of a varying potential control voltage clamp. J Membr Biol 1:431–458

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Patton DE, West JW, Catterall WA, Goldin AL (1992) Amino acid residues required for fast Na+-channel inactivation: charge neutralizations and deletions in the III-IV linker. Proc Natl Acad Sci U S A 89:10905–10909

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pavlov E, Bladen C, Winkfein R, Diao C, Dhaliwal P, French RJ (2005) The pore, not cytoplasmic domains, underlies inactivation in a prokaryotic sodium channel. Biophys J 89:232–242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353–358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486:135–139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perozo E, Cortes DM, Cuello LG (1999) Structural rearrangements underlying K+-channel activation gating. Science 285:73–78

    Article  PubMed  CAS  Google Scholar 

  • Powl AM, O'Reilly AO, Miles AJ, Wallace BA (2010) Synchrotron radiation circular dichroism spectroscopy-defined structure of the C-terminal domain of NaChBac and its role in channel assembly. Proc Natl Acad Sci U S A 107:14064–14069

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu Y, Isom LL, Westenbroek RE, Rogers JC, Tanada TN, McCormick KA, Scheuer T, Catterall WA (1995) Modulation of cardiac Na+ channel expression in Xenopus oocytes by beta 1 subunits. J Biol Chem 270:25696–25701

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294:2372–2375

    Article  PubMed  CAS  Google Scholar 

  • Rogers JC, Qu Y, Tanada TN, Scheuer T, Catterall WA (1996) Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit. J Biol Chem 271:15950–15962

    Article  PubMed  CAS  Google Scholar 

  • Rohl CA, Boeckman FA, Baker C, Scheuer T, Catterall WA, Klevit RE (1999) Solution structure of the sodium channel inactivation gate. Biochemistry 38:855–861

    Article  PubMed  CAS  Google Scholar 

  • Rudy B (1975) Proceedings: slow recovery of the inactivation of sodium conductance in Myxicola giant axons. J Physiol 249:22–24

    Google Scholar 

  • Rudy B (1981) Inactivation in Myxicola giant axons responsible for slow and accumulative adaptation phenomena. J Physiol 312:531–549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sather WA, McCleskey EW (2003) Permeation and selectivity in calcium channels. Annu Rev Physiol 65:133–159

    Article  PubMed  CAS  Google Scholar 

  • Shaya D, Findeisen F, Abderemane-Ali F, Arrigoni C, Wong S, Nurva SR, Loussouarn G, Minor DL Jr (2014) Structure of a prokaryotic sodium channel pore reveals essential gating elements and an outer ion binding site common to eukaryotic channels. J Mol Biol 426:467–483

    Article  PubMed  CAS  Google Scholar 

  • Sheets MF, Kyle JW, Kallen RG, Hanck DA (1999) The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys J 77:747–757

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen HZ, Zhou Q, Pan XJ, Li ZQ, Wu JP, Yan N (2017) Structure of a eukaryotic voltage-gated sodium channel at near-atomic resolution. Science 355(6328). pii: eaal4326

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sokolov S, Scheuer T, Catterall WA (2008) Depolarization-activated gating pore current conducted by mutant sodium channels in potassium-sensitive normokalemic periodic paralysis. Proc Natl Acad Sci U S A 105:19980–19985

    Article  PubMed  PubMed Central  Google Scholar 

  • Starace DM, Bezanilla F (2001) Histidine scanning mutagenesis of basic residues of the S4 segment of the Shaker K+ channel. J Gen Physiol 117:469–490

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Starace DM, Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427:548–553

    Article  PubMed  CAS  Google Scholar 

  • Stephens RF, Guan W, Zhorov BS, Spafford JD (2015) Selectivity filters and cysteine-rich extracellular loops in voltage-gated sodium, calcium, and NALCN channels. Front Physiol 6:153

    Article  PubMed  PubMed Central  Google Scholar 

  • Stuhmer W, Conti F, Suzuki H, Wang X, Noda M, Yahadi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597–603

    Article  PubMed  CAS  Google Scholar 

  • Sula A, Booker J, Ng LC, Naylor CE, DeCaen PG, Wallace BA (2017) The complete structure of an activated open sodium channel. Nat Commun 8:14205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang L, Gamal El-Din TM, Payandeh J, Martinez GQ, Heard TM, Scheuer T, Zheng N, Catterall WA (2014) Structural basis for Ca2+ selectivity of a voltage-gated calcium channel. Nature 505:56–61

    Article  PubMed  CAS  Google Scholar 

  • Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328:67–73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ulbricht W (2005) Sodium channel inactivation: molecular determinants and modulation. Physiol Rev 85:1271–1301

    Article  PubMed  CAS  Google Scholar 

  • Ulmschneider MB, Bagneris C, McCusker EC, Decaen PG, Delling M, Clapham DE, Ulmschneider JP, Wallace BA (2013) Molecular dynamics of ion transport through the open conformation of a bacterial voltage-gated sodium channel. Proc Natl Acad Sci U S A 110:6364–6369

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas E, Yarov-Yarovoy V, Khalili-Araghi F, Catterall WA, Klein ML, Tarek M, Lindahl E, Schulten K, Perozo E, Bezanilla F et al (2012) An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J Gen Physiol 140:587–594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vassilev PM, Scheuer T, Catterall WA (1988) Identification of an intracellular peptide segment involved in sodium channel inactivation. Science 241:1658–1661

    Article  PubMed  CAS  Google Scholar 

  • Vassilev P, Scheuer T, Catterall WA (1989) Inhibition of inactivation of single sodium channels by a site-directed antibody. Proc Natl Acad Sci U S A 86:8147–8151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vilin YY, Ruben PC (2001) Slow inactivation in voltage-gated sodium channels: molecular substrates and contributions to channelopathies. Cell Biochem Biophys 35:171–190

    Article  PubMed  CAS  Google Scholar 

  • West JW, Patton DE, Scheuer T, Wang Y, Goldin AL, Catterall WA (1992) A cluster of hydrophobic amino acid residues required for fast Na+-channel inactivation. Proc Natl Acad Sci U S A 89:10910–10914

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu J, Yan Z, Li Z, Qian X, Lu S, Dong M, Zhou Q, Yan N (2016) Structure of the voltage-gated calcium channel CaV1.1 at 3.6 a resolution. Nature 537:191–196

    Article  PubMed  CAS  Google Scholar 

  • Xiong W, Li RA, Tian YL, Tomaselli GF (2003) Molecular motions of the outer ring of charge of the sodium channel: do they couple to slow inactivation? J Gen Physiol 122:323–332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan Z, Zhou Q, Wang L, Wu J, Zhao Y, Huang G, Peng W, Shen H, Lei J, Yan N (2017) Structure of the Nav1.4-beta1 complex from electric eel. Cell 170(3):470–482.e11

    Article  PubMed  CAS  Google Scholar 

  • Yang N, Horn R (1995) Evidence for voltage-dependent S4 movement in sodium channels. Neuron 15:213–218

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Ellinor PT, Sather WA, Zhang JF, Tsien RW (1993) Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature 366:158–161

    Article  PubMed  CAS  Google Scholar 

  • Yang N, George AL Jr, Horn R (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16:113–122

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Yue L, Navarro B, Ren D, Ramos A, Clapham DE (2002) The cation selectivity filter of the bacterial sodium channel, NaChBac. J Gen Physiol 120:845–853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, He J et al (2012) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:130–134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Scheuer T, Catterall WA (2004a) Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc Natl Acad Sci U S A 101:17873–17878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Yarov-Yarovoy V, Scheuer T, Catterall WA (2004b) A gating hinge in Na+ channels; a molecular switch for electrical signaling. Neuron 41:859–865

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel- Fab complex at 2.0 a resolution. Nature 414:43–48

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, University of Washington, Seattle, WA, 98195-7280, USA

    Tamer M. Gamal El-Din, Michael J. Lenaeus & William A. Catterall

Authors
  1. Tamer M. Gamal El-Din
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael J. Lenaeus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William A. Catterall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tamer M. Gamal El-Din .

Editor information

Editors and Affiliations

  1. CERVO Brain Research Center, Institut Universitaire en Santé Mentale, Quebec, Canada

    Mohamed Chahine

1 Electronic Supplementary Material

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Gamal El-Din, T.M., Lenaeus, M.J., Catterall, W.A. (2017). Structural and Functional Analysis of Sodium Channels Viewed from an Evolutionary Perspective. In: Chahine, M. (eds) Voltage-gated Sodium Channels: Structure, Function and Channelopathies. Handbook of Experimental Pharmacology, vol 246. Springer, Cham. https://doi.org/10.1007/164_2017_61

Download citation

Publish with us

Policies and ethics

Search

Navigation