Theoretical and simulation studies on voltage-gated sodium channels

Yang Li, Haipeng Gong

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Protein Cell ›› 2015, Vol. 6 ›› Issue (6) : 413-422. DOI: 10.1007/s13238-015-0152-6
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Theoretical and simulation studies on voltage-gated sodium channels

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Abstract

Voltage-gated sodium (Nav) channels are indispensable membrane elements for the generation and propagation of electric signals in excitable cells. The successes in the crystallographic studies on prokaryotic Nav channels in recent years greatly promote the mechanistic investigation of these proteins and their eukaryotic counterparts. In this paper, we mainly review the progress in computational studies, especially the simulation studies, on these proteins in the past years.

Keywords

voltage-gated sodium channels / molecular dynamics simulation / ion permeation / ion selectivity / voltage gating

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Yang Li, Haipeng Gong. Theoretical and simulation studies on voltage-gated sodium channels. Protein Cell, 2015, 6(6): 413‒422 https://doi.org/10.1007/s13238-015-0152-6

References

[1]
Allen TW, Andersen OS, Roux B (2004) On the importance of atomic fluctuations, protein flexibility, and solvent in ion permeation. J Gen Physiol124: 679-690
CrossRef Google scholar
[2]
Allen TW, Andersen OS, Roux B (2006) Molecular dynamics—potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels. Biophys Chem124: 251-267
CrossRef Google scholar
[3]
Amaral C, Carnevale V, Klein ML, Treptow W (2012) Exploring conformational states of the bacterial voltage-gated sodium channel NavAb via molecular dynamics simulations. Proc Natl Acad Sci USA109: 21336-21341
CrossRef Google scholar
[4]
Bagal S, Brown AD, Cox PJ, Omoto K, Owen RM, Pryde DC, Sidders B, Skerratt SE, Stevens EB, Storer RI (2013) Ion channels as therapeutic targets: a drug discovery perspective. J Med Chem56: 593-624
CrossRef Google scholar
[5]
Bagnéris C, DeCaen PG, Naylor CE, Pryde DC, Nobeli I, Clapham DE, Wallace BA (2014) Prokaryotic NavMs channel as a structural and functional model for eukaryotic sodium channel antagonism. Proc Natl Acad Sci USA111(23): 8428-8433
CrossRef Google scholar
[6]
Barber AF, Carnevale V, Raju SG, Amaral C, Treptow W, Klein ML (2012) Hinge-bending motions in the pore domain of a bacterial voltage-gated sodium channel. Biochim Biophys Acta1818: 2120-2125
CrossRef Google scholar
[7]
Bartels C, Karplus M (1998) Probability distributions for complex systems: adaptive umbrella sampling of the potential energy. J Phys Chem B102: 865-880
CrossRef Google scholar
[8]
Berneche S, Roux B (2001) Energetics of ion conduction through the K+ channel. Nature414: 73-77
CrossRef Google scholar
[9]
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
CrossRef Google scholar
[10]
Boiteuxa C, Vorobyov I, French RJ, French C, Yarov-Yarovoy V, Allen TW (2014a) Local anesthetic and antiepileptic drug access and binding to a bacterial voltage-gated sodium channel. Proc Natl Acad Sci USA111: 13057-13062
CrossRef Google scholar
[11]
Boiteuxa C, Vorobyov I, Allen TW (2014b) Ion conduction and conformational flexibility of a bacterial voltage-gated sodium channel. Proc Natl Acad Sci USA111: 3454-3459
CrossRef Google scholar
[12]
Bostick DL, Brooks CL III (2007) Selectivity in K+ channels is due to topological control of the permeant ion’s coordinated state. Proc Natl Acad Sci USA104: 9260-9265
CrossRef Google scholar
[13]
Brooks BR, Brooks CL III, Mackerell AD Jr, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S (2009) CHARMM: the biomolecular simulation program. J Comput Chem30: 1545-1614
CrossRef Google scholar
[14]
Carnevale V, Treptow W, Klein ML (2011) Sodium ion binding sites and hydration in the lumen of a bacterial ion channel from molecular dynamics simulations. J Phys Chem Lett2: 2504-2508
CrossRef Google scholar
[15]
Case D, Darden T, Cheatham T III, Simmerling C, Wang J, Duke R, Luo R, Walker R, Zhang W, Merz K (2012) AMBER 12, vol 1. University of California, San Francisco, p 3
[16]
Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron26: 13-25
CrossRef Google scholar
[17]
Catterall WA (2010) Ion channel voltage sensors: structure, function, and pathophysiology. Neuron67: 915-928
CrossRef Google scholar
[18]
Catterall WA, Goldin AL, Waxman SG (2005) International Union of Pharmacology. XLVII. Nomenclature and structure–function relationships of voltage-gated sodium channels. Pharmacol Rev57: 397-409
CrossRef Google scholar
[19]
Chakrabarti N, Ing C, Payandeh J, Zheng N, Catterall WA, Pomès R (2013) Catalysis of Na+ permeation in the bacterial sodium channel NaVAb. Proc Natl Acad Sci USA110: 11331-11336
CrossRef Google scholar
[20]
Chen R, Chung SH (2012a) Binding modes of muconotoxin to the bacterial sodium channel (NaVAb). Biophys J102: 483-488
CrossRef Google scholar
[21]
Chen R, Chung SH (2012b) Conserved functional surface of antimammalian scorpion beta-toxins. J Phys Chem B116: 4796-4800
CrossRef Google scholar
[22]
Chen R, Chung SH (2014) Mechanism of tetrodotoxin block and resistance in sodium channels. Biochem Biophys Res Commun446: 370-374
CrossRef Google scholar
[23]
Clare JJ, Tate SN, Nobbs M, Romanos MA (2000) Voltage-gated sodium channels as therapeutic targets. Drug Discov Today5: 506-520
CrossRef Google scholar
[24]
Corry B, Thomas M (2012) Mechanism of ion permeation and selectivity in a voltage gated sodium channel. J Am Chem Soc134: 1840-1846
CrossRef Google scholar
[25]
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 USA105: 15142-15147
CrossRef Google scholar
[26]
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 USA106: 22498-22503
CrossRef Google scholar
[27]
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 J99: L72-L74
CrossRef Google scholar
[28]
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 USA108: 6109-6114
CrossRef Google scholar
[29]
Delemotte L, Kasimova MA, Klein ML, Tarek M, Carnevale V (2015) Free-energy landscape of ion-channel voltage-sensor-domain activation. Proc Natl Acad Sci USA112: 124-129
CrossRef Google scholar
[30]
Dib-Hajj SD, Cummins TR, Black JA, Waxman SG (2010) Sodium channels in normal and pathological pain. Annu Rev Neurosci33: 325-347
CrossRef Google scholar
[31]
Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science280: 69-77
CrossRef Google scholar
[32]
Dudev T, Lim C (2010) Factors governing the Na(+) vs K(+) selectivity in sodium ion channels. J Am Chem Soc132: 2321-2332
CrossRef Google scholar
[33]
Dudev T, Lim C (2012) Why voltage-gated Ca2+ and bacterial Na+ channels with the same EEEE motif in their selectivity filters confer opposite metal selectivity. Phys Chem Chem Phys14: 12451-12456
CrossRef Google scholar
[34]
Dudev T, Lim C (2014) Evolution of eukaryotic ion channels: principles underlying the conversion of Ca2+-selective to Na+-selective channels. J Am Chem Soc136: 3553-3559
CrossRef Google scholar
[35]
Eisenman G, Horn R (1983) Ionic selectivity revisited—the role of kinetic and equilibrium processes in ion permeation through channels. J Membr Biol76: 197-225
CrossRef Google scholar
[36]
Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez- Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L (2000) Nomenclature of voltage-gated calcium channels. Neuron25: 533-535
CrossRef Google scholar
[37]
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 J71: 3110-3125
CrossRef Google scholar
[38]
Fowler PW, Tai K, Sansom MS (2008) The selectivity of K+ ion channels: testing the hypotheses. Biophys J95: 5062-5072
CrossRef Google scholar
[39]
Furini S, Domene C (2012) On conduction in a bacterial sodium channel. PLoS Comput Biol8: e1002476
CrossRef Google scholar
[40]
Furini S, Domene C (2013) K(+) and Na(+) conduction in selective and nonselective ion channels via molecular dynamics simulations. Biophys J105: 1737-1745
CrossRef Google scholar
[41]
Furini S, Barbini P, Domene C (2014) Effects of the protonation state of the EEEE motif of a bacterial NaD-channel on conduction and pore structure. Biophys J106: 2175-2183
CrossRef Google scholar
[42]
Gordon D, Karbat I, Ilan N, Cohen L, Kahn R, Gilles N, Dong K, Stuhmer W, Tytgat J, Gurevitz M (2007) The differential preference of scorpion alpha-toxins for insect or mammalian sodium channels: implications for improved insect control. Toxicon49: 452-472
CrossRef Google scholar
[43]
Gordon D, Chen R, Chung SH (2013) Computational methods of studying the binding of toxins from venomous animals to biological ion channels: theory and applications. Physiol Rev93: 767-802
CrossRef Google scholar
[44]
Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D, Pardo LA, Robertson GA, Rudy B, Sanguinetti MC, Stuhmer W (2005) International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev57: 473-508
CrossRef Google scholar
[45]
Hamelberg D, Mongan J, McCammon JA (2004) Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules. J Chem Phys120: 11919-11929
CrossRef Google scholar
[46]
Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput4: 435-447
CrossRef Google scholar
[47]
Hille B (2001) Ion channels of excitable membranes, vol 507. Sinauer, Sunderland
[48]
Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol117: 500-544
CrossRef Google scholar
[49]
Hodgkin AL, Keynes RD (1955) The potassium permeability of a giant nerve fibre. J Physiol128: 61-88
CrossRef Google scholar
[50]
Isacoff EY, Jan LY, Minor DL (2013) Conduits of life’s spark: a perspective on ion channel research since the birth of neuron. Neuron80: 658-674
CrossRef Google scholar
[51]
Jensen MO, Borhani DW, Lindorff-Larsen K, Maragakis P, Jogini V, Eastwood MP, Dror RO, Shaw DE (2010) Principles of conduction and hydrophobic gating in K+ channels. Proc Natl Acad Sci USA107: 5833-5838
CrossRef Google scholar
[52]
Jensen MO, Jogini V, Borhani DW, Leffler AE, Dror RO, Shaw DE (2012) Mechanism of voltage gating in potassium channels. Science336: 229-233
CrossRef Google scholar
[53]
Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) Crystal structure and mechanism of a calcium-gated potassium channel. Nature417: 515-522
CrossRef Google scholar
[54]
Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R (2003) X-ray structure of a voltage-dependent K+ channel. Nature423: 33-41
CrossRef Google scholar
[55]
Jiang W, Hardy DJ, Phillips JC, MacKerell AD, Schulten K, Roux B (2011) High-performance scalable molecular dynamics simulations of a polarizable force field based on classical Drude oscillators in NAMD. J Phys Chem Lett2: 87-92
CrossRef Google scholar
[56]
Kalia J, Milescu M, Salvatierra J, Wagner J, Klint JK, King GF, Olivera BM, Bosmans F (2015) From foe to friend: using animal toxins to investigate ion channel function. J Mol Biol427: 158-175
CrossRef Google scholar
[57]
Karplus M, Kuriyan J (2005) Molecular dynamics and protein function. Proc Natl Acad Sci USA102: 6679-6685
CrossRef Google scholar
[58]
Karplus M, McCammon JA (2002) Molecular dynamics simulations of biomolecules. Nat Struct Mol Biol9: 646-652
CrossRef Google scholar
[59]
Karplus M, Petsko GA (1990) Molecular dynamics simulations in biology. Nature347: 631-639
CrossRef Google scholar
[60]
Ke S, Zangerl EM, Stary-Weinzinger A (2013) Distinct interactions of Na+ and Ca2+ ions with the selectivity filter of the bacterial sodium channel Na(V)Ab. Biochem Biophys Res Commun430: 1272-1276
CrossRef Google scholar
[61]
Knapp O, McArthur JR, Adams DJ (2012) Conotoxins targeting neuronal voltage-gated sodium channel subtypes: potential analgesics? Toxins (Basel)4: 1236-1260
CrossRef Google scholar
[62]
Kuzmenkin A, Bezanilla F, Correa AM (2004) Gating of the bacterial sodium channel, NaChBac: voltage-dependent charge movement and gating currents. J Gen Physiol124: 349-356
CrossRef Google scholar
[63]
Laio A, Gervasio FL (2008) Metadynamics: a method to simulate rare events and reconstruct the free energy in biophysics, chemistry and material science. Rep Prog Phys71: 126601
CrossRef Google scholar
[64]
Lipkind GM, Fozzard HA (1994) A structural model of the tetrodotoxin and saxitoxin binding site of the Na+ channel. Biophys J66: 1-13
CrossRef Google scholar
[65]
Lipkind GM, Fozzard HA (2008) Voltage-gated Na channel selectivity: the role of the conserved domain III lysine residue. J Gen Physiol131: 523-529
CrossRef Google scholar
[66]
Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science309: 897-903
CrossRef Google scholar
[67]
Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature450: 376-382
CrossRef Google scholar
[68]
Mantegazza M, Curia G, Biagini G, Ragsdale DS, Avoli M (2010) Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol9: 413-424
CrossRef Google scholar
[69]
Maragliano L, Fischer A, Vanden-Eijnden E, Ciccotti G (2006) String method in collective variables: minimum free energy paths and isocommittor surfaces. J Chem Phys125: 24106
CrossRef Google scholar
[70]
McCormack K, Santos S, Chapman ML, Krafte DS, Marron BE, West CW, Krambis MJ, Antonio BM, Zellmer SG, Printzenhoff D (2013) Voltage sensor interaction site for selective small molecule inhibitors of voltage-gated sodium channels. Proc Natl Acad Sci USA110: E2724-E2732
CrossRef Google scholar
[71]
McCusker EC, Bagneris C, Naylor CE, Cole AR, D’Avanzo N, Nichols CG, Wallace BA (2012) Structure of a bacterial voltagegated sodium channel pore reveals mechanisms of opening and closing. Nat Commun3: 1102
CrossRef Google scholar
[72]
Moreau A, Gosselin-Badaroudine P, Chahine M (2014) Biophysics, pathophysiology, and pharmacology of ion channel gating pores. Front Pharmacol5: 53
CrossRef Google scholar
[73]
Noskov SY, Roux B (2006) Ion selectivity in potassium channels. Biophys Chem124: 279-291
CrossRef Google scholar
[74]
Noskov SY, Berneche S, Roux B (2004) Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands. Nature431: 830-834
CrossRef Google scholar
[75]
Payandeh J, Minor DL Jr (2015) Bacterial voltage-gated sodium channels (BacNas) from the soil, sea, and salt lakes enlighten molecular mechanisms of electrical signaling and pharmacology in the brain and heart. J Mol Biol427: 3-30
CrossRef Google scholar
[76]
Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature475: 353-358
CrossRef Google scholar
[77]
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. Nature486: 135-139
CrossRef Google scholar
[78]
Penzotti JL, Fozzard HA, Lipkind GM, Dudley SC Jr (1998) Differences in saxitoxin and tetrodotoxin binding revealed by mutagenesis of the Na+ channel outer vestibule. Biophys J75: 2647-2657
CrossRef Google scholar
[79]
Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem26: 1781-1802
CrossRef Google scholar
[80]
Piccinini E, Ceccarelli M, Affinito F, Brunetti R, Jacoboni C (2008) Biased molecular simulations for free-energy mapping: a comparison on the KcsA channel as a test case. J Chem Theory Comput4: 173-183
CrossRef Google scholar
[81]
Qiu H, Shen R, Guo W (2012) Ion solvation and structural stability in a sodium channel investigated by molecular dynamics calculations. Biochim Biophys Acta1818: 2529-2535
CrossRef Google scholar
[82]
Ragsdale DS, Avoli M (1998) Sodium channels as molecular targets for antiepileptic drugs. Brain Res Rev26: 16-28
CrossRef Google scholar
[83]
Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science294: 2372-2375
CrossRef Google scholar
[84]
Roux B, MacKinnon R (1999) The cavity and pore helices in the KcsA K+ channel: electrostatic stabilization of monovalent cations. Science285: 100-102
CrossRef Google scholar
[85]
Saparov SM, Pohl P (2004) Beyond the diffusion limit: water flow through the empty bacterial potassium channel. Proc Natl Acad Sci USA101: 4805-4809
CrossRef Google scholar
[86]
Sather WA, McCleskey EW (2003) Permeation and selectivity in calcium channels. Annu Rev Physiol65: 133-159
CrossRef Google scholar
[87]
Sato C, Ueno Y, Asai K, Takahashi K, Sato M, Engel A, Fujiyoshi Y (2001) The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature409: 1047-1051
CrossRef Google scholar
[88]
Schlief T, Schonherr R, Imoto K, Heinemann SH (1996) Pore properties of rat brain II sodium channels mutated in the selectivity filter domain. Eur Biophys J25: 75-91
CrossRef Google scholar
[89]
Shaya D, Findeisen F, Abderemane-Ali F, Arrigoni C, Wong S, Nurva SR, Loussouarn G, Minor DL (2014) Structure of a prokaryotic sodium channel pore reveals essential gating elements and an outer ion binding site common to eukaryotic channels. J Mol Biol426: 467-483
CrossRef Google scholar
[90]
Shrivastava IH, Sansom MSP (2000) Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophys J78: 557-570
CrossRef Google scholar
[91]
Sontheimer H, Black JA, Waxman SG (1996) Voltage-gated Na+ channels in glia: properties and possible functions. Trends Neurosci19: 325-331
CrossRef Google scholar
[92]
Stevens M, Peigneur S, Tytgat J (2011) Neurotoxins and their binding areas on voltage-gated sodium channels. Front Pharmacol2: 71
CrossRef Google scholar
[93]
Stevens M, Peigneur S, Dyubankova N, Lescrinier E, Herdewijn P, Tytgat J (2012) Design of bioactive peptides from naturally occurring muconotoxin structures. J Biol Chem287: 31382-31392
CrossRef Google scholar
[94]
Stock L, Delemotte L, Carnevale V, Treptow W, Klein ML (2013) Conduction in a biological sodium selective channel. J Phys Chem B117: 3782-3789
CrossRef Google scholar
[95]
Sun YM, Favre I, Schild L, Moczydlowski E (1997) On the structural basis for size-selective permeation of organic cations through the voltage-gated sodium channel—effect of alanine mutations at the DEKA locus on selectivity, inhibition by Ca2+ and H+, and molecular sieving. J Gen Physiol110: 693-715
CrossRef Google scholar
[96]
Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science328: 67-73
CrossRef Google scholar
[97]
Thottumkara AP, Parsons WH, Du Bois J (2014) Saxitoxin. Angew Chem Int Ed Engl53: 5760-5784
CrossRef Google scholar
[98]
Tikhonov DB, Zhorov BS (2012) Architecture and pore block of eukaryotic voltage-gated sodium channels in view of NavAb bacterial sodium channel structure. Mol Pharmacol82: 97-104
CrossRef Google scholar
[99]
Treptow W, Tarek M (2006) Environment of the gating charges in the Kv1.2 Shaker potassium channel. Biophys J90: L64-L66
CrossRef Google scholar
[100]
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 USA110: 6364-6369
CrossRef Google scholar
[101]
Vargas E, Yarov-Yarovoy V, Khalili-Araghi F, Catterall WA, Klein ML, Tarek M, Lindahl E, Schulten K, Perozo E, Bezanilla F (2012) An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J Gen Physiol140: 587-594
CrossRef Google scholar
[102]
Xia M, Liu H, Li Y, Yan N, Gong H (2013) The mechanism of Na(+)/ K(+) selectivity in mammalian voltage-gated sodium channels based on molecular dynamics simulation. Biophys J104: 2401-2409
CrossRef Google scholar
[103]
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 USA109: E93-E102
CrossRef Google scholar
[104]
Yu FH, Catterall WA (2004) The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE2004: re15
CrossRef Google scholar
[105]
Zhang X, Yan N (2013) The conformational shifts of the voltage sensing domains between NavRh and NavAb. Cell Res: 444
CrossRef Google scholar
[106]
Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, He J (2012) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature486: 130-134
CrossRef Google scholar
[107]
Zhang X, Xia MD, Li Y, Liu HH, Jiang X, Ren WL, Wu JP, DeCaen P, Yu F, Huang S (2013) Analysis of the selectivity filter of the voltage-gated sodium channel NavRh. Cell Res23: 409-422
CrossRef Google scholar
[108]
Zheng L, Chen M, Yang W (2008) Random walk in orthogonal space to achieve efficient free-energy simulation of complex systems. Proc Natl Acad Sci USA105: 20227-20232
CrossRef Google scholar
[109]
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. Nature414: 43-48
CrossRef Google scholar

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