Role of the C-terminal domain in the structure and function of tetrameric sodium channels

Nature Communications

Volumn 4, Issue , 2013, Pages

  Bagnéris, Claire ^a   Decaen, Paul G ^b,c   Hall, Benjamin A ^d   Naylor, Claire E ^a   Clapham, David E ^b,c   Kay, Christopher W M ^e   Wallace, B A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MICROSOFT RESEARCH   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; TETRAMER; VOLTAGE GATED SODIUM CHANNEL;

BACTERIUM; CRYSTAL STRUCTURE; CYTOPLASM; ELECTRON SPIN RESONANCE; PROTEIN; SODIUM;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; MOLECULAR DYNAMICS; POROSITY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ALPHAPROTEOBACTERIA; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; ION CHANNEL GATING; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STATIC ELECTRICITY; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84884634287     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3465     Document Type: Article

References (34)

1. Hille, B. Ionic Channels of Excitable Membranes (Sinauer Associates Inc., Sunderland, MA, 2001)
2. Noda, M. et al. Expression of functional sodium channels from cloned cDNA. Nature 322, 826-828 (1986) (Pubitemid 16055252)
3. Charalambous, K. & Wallace, B. A. NaChBac: the long lost sodium channel ancestor. Biochemistry 50, 6742-6752 (2011)
4. Nurani, G. et al. Tetrameric bacterial sodium channels: characterization of structure, stability, and drug binding. Biochemistry 47, 8114-8121 (2008)
5. Powl, A. M., O'Reilly, A. O., Miles, A. J. & Wallace, B. A. Synchrotron radiation circular dichroism spectroscopy-defined structure of the C-terminal domain of NaChBac and its role in channel assembly. Proc. Natl Acad. Sci. USA 107, 14064-14069 (2010)
6. Mio, K., Mio, M., Arisaka, F., Sato, M. & Sato, C. 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 (2010)
7. Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011)
8. Payandeh, J., Gamal El-Din, T. M., Scheuer, T., Zheng, N. & Catterall, W. A. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486, 135-139 (2012)
9. McCusker, E. C. et al. The open conformation of a voltage-gated sodium channel reveals the transmembrane pathway and mechanism of channel opening and closing. Nat. Commun. 3, 1102 (2012)
10. Zhang, X. et al. Crystal structure of an orthologue of the NaChBac voltagegated sodium channel. Nature 486, 130-134 (2012)
11. Lobley, A., Pierron, V., Reynolds, L., Allen, L. & Michalovich, D. Identification of human and mouse CatSper3 and CatSper4 genes: characterisation of a common interaction domain and evidence for expression in testis. Reprod. Biol. Endocrinol. 1, 53 (2003)
12. Garcia-Sanz, N. et al. Identification of a tetramerization domain in the C terminus of the vanilloid receptor. J. Neurosci. 24, 5307 (2004)
13. Howard, R. J., Clark, K. A., Holton, J. M. & Minor, D. L. Structural insight into KCNQ (Kv7) channel assembly and channelopathy. Neuron 53, 663 (2007)
14. Irie, K., Shimomura, T. & Fujiyoshi, Y. The C-terminal helical bundle of the tetrameric prokaryotic sodium channel accelerates the inactivation rate. Nat. Commun. 3, 793 (2012)
15. Steinhoff, H. J. et al. Time-resolved detection of structural changes during the photocycle of spin-labeled bacteriorhodopsin. Science 266, 105-107 (1994)
16. Schiemann, O. & Prisner, T. F. Long-range distance determinations in biomacromolecules by EPR spectroscopy. Q. Rev. Biophys. 40, 1-53 (2007) (Pubitemid 47343581)
17. Polyhach, Y., Bordignon, E. & Jeschke, G. Rotamer libraries of spin labeled cysteines for protein studies. PCCP 13, 2356-2366 (2011)
18. Bricogne, G. et al. BUSTER version 1.10.0. (Global Phasing Ltd, Cambridge, UK, 2011)
19. Ulmschneider, M. B. et al. Molecular dynamics of ion transport through the open conformation of a bacterial voltage-gated sodium channel. Proc. Nat Acad. Sci. USA 110, 6364-6369 (2013)
20. Klaiber, K. et al. Functional expression of Shaker K? channels in a baculovirus-infected insect cell line. Neuron 5, 221-226 (1990) (Pubitemid 20262700)
21. Ren, D. et al. A prokaryotic voltage-gated sodium channel. Science 294, 2372-2375 (2001) (Pubitemid 33140564)
22. McCusker, E. C., D'Avanzo, N., Nichols, C. G. & Wallace, B. A. Simplified bacterial "pore" channel provides insight into the assembly, stability, and structure of sodium channels. J. Biol. Chem. 286, 16386-16391 (2011)
23. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673-4680 (1994) (Pubitemid 24354800)
24. Lupas, A., Van Dyke, M. & Stock, J. Predicting coiled coils from protein sequences. Science 252, 1162-1164 (1991) (Pubitemid 21917026)
25. Pannier, M., Veit, S., Godt, A., Jeschke, G. & Spiess, H. W. Dead-time free measurement of dipole-dipole interactions between electron spins. J. Magn. Reson. 142, 331-340 (2000)
26. Jeschke, G. et al. A comprehensive software package for analyzing pulsed ELDOR data. Appl. Magn. Reson. 30, 473-498 (2006)
27. Sali, A. & Blundell, T. L. Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993) (Pubitemid 24007801)
28. Yadav, M. K. et al. Coiled coils at the edge of configurational heterogeneity. Structural analyses of parallel and antiparallel homotetrameric coiled coils reveal configurational sensitivity to a single solvent exposed amino acid substitution. Biochemistry 45, 4463-4473 (2006)
29. Monticelli, L. et al. The MARTINI coarse-grained force field: Extension to proteins. J. Chem. Theory Comp. 4, 819-834 (2008)
30. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P. & deVries, A. H. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824 (2007) (Pubitemid 47169693)
31. Leslie, A. G. W. & Powell, H. R. Processing data with Mosfilm. Evolving Meth. Macromol. Cryst. 245, 41-51 (2007)
32. Evans, P. R. Scaling and assessment of data quality. Acta Cryst. D62, 72-82 (2006)
33. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007) (Pubitemid 47080256)
34. Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix refine. Acta Cryst. D Biol. Cryst. 68, 352-367 (2012).