Molecular basis of ion permeability in a voltage-gated sodium channel

EMBO Journal

Volumn 35, Issue 8, 2016, Pages 820-830

  Naylor, Claire E ^a   Bagnéris, Claire ^a   Decaen, Paul G ^b,c   Sula, Altin ^a   Scaglione, Antonella ^b,c,d   Clapham, David E ^b,c   Wallace, B ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CNR   (Italy)

Author keywords

crystal structure; electrophysiology; ion permeability; sodium channel

Indexed keywords

CALCIUM ION; GLUTAMIC ACID; LITHIUM ION; MAGNESIUM ION; POTASSIUM ION; SODIUM ION; VOLTAGE GATED SODIUM CHANNEL; BACTERIAL PROTEIN; CATION; SODIUM; SODIUM CHANNEL;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIELECTRIC CONSTANT; EXTRACELLULAR MATRIX; HEK293 CELL LINE; HYDROPHOBICITY; ION CONDUCTANCE; ION PERMEABILITY; IONIC STRENGTH; MAGNETOCOCCUS MARINUS; MEMBRANE ELECTROPHYSIOLOGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN EXPRESSION; REVERSAL POTENTIAL; STATIC ELECTRICITY; ALPHAPROTEOBACTERIA; CHANNEL GATING; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PATCH CLAMP TECHNIQUE; PERMEABILITY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; BINDING SITES; CATIONS; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MODELS, MOLECULAR; MUTATION; PATCH-CLAMP TECHNIQUES; PERMEABILITY; PROTEIN CONFORMATION; SODIUM; SODIUM CHANNELS; STATIC ELECTRICITY;

EID: 84975726435     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201593285     Document Type: Article

References (48)

1. 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 USA 109: 21336-21341
2. Amey JS, O'Reilly AO, Burton MJ, Puinean AM, Mellor IR, Duce IR, Field LM, Wallace BA, Williamson MS, Davies TG, (2015) An evolutionarily-unique heterodimeric voltage-gated cation channel found in aphids. FEBS Lett 5895: 598-607
3. Bagnéris C, Naylor CE, McCusker EC, Wallace BA, (2015) Structural model of the open-closed-inactivated cycle of prokaryotic voltage-gated sodium channels. J Gen Physiol 145: 5-16
4. Bagneris C, DeCaen PG, Hall BA, Naylor CE, Clapham DE, Kay CWM, Wallace BA, (2013) Role of the C-terminal domain in the structure and function of tetrameric sodium channels. Nat Commun 4: 2465
5. Bagneris 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 USA 111: 8428-8433
6. Boiteux C, Vorobyov I, Allen TW, (2014) Ion conduction and conformational flexibility of a bacterial voltage-gated sodium channel. Proc Natl Acad Sci USA 111: 3454-3459
7. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, Paciorek W, Roversi P, Sharff A, Smart OS, Vonrhein C, (2011) BUSTER version 2.10.0. Cambridge, UK: Global Phasing Ltd.
8. Callenberg KM, Choudhary OP, de Forest GL, Gohara DW, Baker NA, Grabe M, (2010) APBSmem: a graphical interface for electrostatic calculations at membrane. PLoS ONE 5: e12722
9. + permeation in the bacterial sodium channel Na(V)Ab. Proc Natl Acad Sci USA 110: 11331-11336
10. 2+-dependent gating in CorA. Nat Commun 5: 3590
11. DeCaen PG, Takahashi Y, Krulwich TA, Ito M, Clapham DE, (2014) Ionic selectivity and thermal adaptations within the voltage-gated sodium channel family of alkaliphilic Bacillus. eLife 3: e04387
12. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA, (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: W665-W667
13. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker N, (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35: W522-W525
14. Doyle DA, Cabral JM, Pfuetzner RA, Kuo AL, Gulbis JM, Cohen SL, Chait BT, MacKinnon R, (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280: 69-77
15. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen M-Y, Pieper U, Sali A, (2006) Comparative protein structure modelling with MODELLER. Curr Protoc Bioinformatics 5: Unit 5.6
16. Evans PR, (2006) Scaling and assessment of data quality. Acta Cryst D62: 72-82
17. Finol-Urdaneta RK, Wang Y, Al-Sabi A, Zhao C, Noskov SY, French RJ, (2014) Sodium channel selectivity and conduction: prokaryotes have devised their own molecular strategy. J Gen Physiol 143: 157-171
18. Furini S, Barbini P, Domene C, (2014) Effects of the protonation state of the EEEE motif of a bacterial Na(+)-channel on conduction and pore structure. Biophys J 106: 2175-2183
19. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38
20. Irie K, Kitagawa K, Nagura H, Imai T, Shimomura T, Fujiyoshi Y, (2010) Comparative study of the gating motif and C-type inactivation In prokaryotic voltage-gated sodium channels. J Biol Chem 285: 3685-3694
21. Jiang YX, Lee A, Chen JY, Cadene M, Chait BT, MacKinnon R, (2002) The open pore conformation of potassium channels. Nature 417: 523-526
22. Jiang YX, Lee A, Chen JY, Ruta V, Cadene M, Chait BT, MacKinnon R, (2003) X-ray structure of a voltage-dependent K+ channel. Nature 423: 33-41
23. Kabsch W, (1976) A solution for best rotation to relate two sets of vectors. Acta Cryst A32: 922-923
24. Kabsch W, (2010) XDS. Acta Cryst D66: 125-132
25. Krissinel E, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Cryst D60: 2256-2268
26. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ, (2007) Phaser crystallographic software. J Appl Cryst 40: 658-674
27. McCusker EC, D'Avanzo N, Nichols CG, Wallace BA, (2011) Simplified bacterial "pore" channel provides insight into the assembly, stability, and structure of sodium channels. J Biol Chem 286: 16386-16391
28. McCusker EC, Bagnéris 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
29. Neher E, (1992) Ion channels for communication between and within cells. Science 256: 498-502
30. Noda M, Ikeda T, Suzuki H, Takeshima H, Takahashi T, Kuno M, Numa S, (1986) Expression of functional sodium channels from cloned cDNA. Nature 322: 826-828
31. Payandeh J Gamal, El-Din T, Scheuer T, Zheng N, Catterall WA, (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486: 135-139
32. Payandeh J, Scheuer T, Zheng N, Catterall WA, (2011) The crystal structure of a voltage-gated sodium channel. Nature 475: 353-358
33. Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE, (2001) A prokaryotic voltage-gated sodium channel. Science 294: 2372-2375
34. Shaya D, Kreir M, Robbins RA, Wong S, Hammon J, Brüggemann A, Minor DL Jr, (2011) Voltage-gated sodium channel (NaV) protein dissection creates a set of functional pore-only proteins. Proc Natl Acad Sci USA 108: 12313-12318
35. 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
36. Sitkoff D, Sharp KA, Honig B, (1994) Accurate calculation of hydration free-energies using macroscopic solvent models. J Phys Chem 98: 1978-1988
37. Stock L, Delemotte L, Carnevale V, Treptow W, Klein ML, (2013) Conduction in a biological sodium selective channel. J Phys Chem B 117: 3782-3789
38. Strugatsky D, McNulty R, Munson K, Chen CK, Soltis SM, Sachs G, Luecke H, (2013) Structure of the proton-gated urea channel from the gastric pathogen Helicobacter pylori. Nature 493: 255-258
39. 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. J Gen Physiol 110: 693-715
40. +2 selectivity of a voltage-gated calcium channel. Nature 505: 56-61
41. Tsai CJ, Tani K, Irie K, Hiroaki Y, Shimomura T, McMillan DG, Cook GM, Schertler GF, Fujiyoshi Y, Li XD, (2013) Two alternative conformations of a voltage-gated sodium channel. J Mol Biol 425: 4074-4088
42. Ulmschneider MB, Bagnéris 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 Nat Acad Sci USA 110: 6364-6369
43. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS, (2011) Overview of the CCP4 suite and current developments. Acta Cryst D67: 235-242
44. + selectivity in mammalian voltage-gated sodium channels based on molecular dynamics simulation. Biophys J 104: 2401-2409
45. 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
46. Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, He J, Wang J, Clapham DE, Yan N, (2012) Crystal structure of an orthologue of the NaChBac voltage gated sodium channel. Nature 486: 130-134
47. Zhang X, Xia M, Li Y, Liu H, Jiang X, Ren W, Wu J, DeCaen P, Yu F, Huang S, He J, Clapham DE, Yan N, Gong H, (2013) Analysis of the selectivity filter of the voltage-gated sodium channel Na(v)Rh. Cell Res 23: 409-422
48. Zhou Y, Morais-Cabral J, 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