Crystal structure of a voltage-gated sodium channel in two potentially inactivated states

Nature

Volumn 486, Issue 7401, 2012, Pages 135-139

  Payandeh, Jian ^a,c   Gamal El Din, Tamer M ^a   Scheuer, Todd ^a   Zheng, Ning ^a,b   Catterall, William A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DIMER; VOLTAGE GATED SODIUM CHANNEL;

BACTERIUM; CELL ORGANELLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DRUG; MAMMAL; MEMBRANE; MOLECULAR ANALYSIS; MUTATION; NUMERICAL MODEL; SODIUM;

ALPHA HELIX; ARCOBACTER; ARCOBACTER BUTZLERI; ARTICLE; BILAYER MEMBRANE; CELL ACTIVATION; CHANNEL GATING; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; WILD TYPE; X RAY CRYSTALLOGRAPHY;

ARCOBACTER; CONSERVED SEQUENCE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ION CHANNEL GATING; MODELS, MOLECULAR; PROTEIN CONFORMATION; SODIUM CHANNELS; STRUCTURE-ACTIVITY RELATIONSHIP;

ARCOBACTER BUTZLERI; MAMMALIA;

EID: 84861945912     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11077     Document Type: Article

References (46)

1. Hodgkin, A. L. & Huxley, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500-544 (1952).
2. Rudy, B. Slow inactivation of the sodium conductance in squid giant axons. Pronase resistance. J. Physiol. (Lond.) 283, 1-21 (1978).
3. Vilin, Y. Y. & Ruben, P. C. Slow inactivation in voltage-gated sodium channels: molecular substratesandcontributions to channelopathies. Cell Biochem. Biophys. 35, 171-190 (2001).
4. Payandeh, J., Scheuer, T., Zheng, N. & Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 475, 353-358 (2011).
5. Long, S. B., Tao, X., Campbell, E. B. & MacKinnon, R. Atomic structure of a voltagedependent K1 channel in a lipid membrane-like environment. Nature 450, 376-382 (2007).
6. Ren, D. et al. A prokaryotic voltage-gated sodium channel. Science 294, 2372-2375 (2001).
7. Catterall, W. A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26, 13-25 (2000).
8. Armstrong, C. M., Bezanilla, F. & Rojas, E. Destruction of sodium conductance inactivation in squid axons perfused with pronase. J. Gen. Physiol. 62, 375-391 (1973).
9. West, J. W. et al.A cluster of hydrophobicamino acid residues required for fast Na1 channel inactivation. Proc. Natl Acad. Sci. USA 89, 10910-10914 (1992).
10. Eaholtz, G., Scheuer, T. & Catterall, W. A. Restoration of inactivation and block of open sodium channels by an inactivation gate peptide. Neuron 12, 1041-1048 (1994).
11. Nesterenko, V. V., Zygmunt, A. C., Rajamani, S., Belardinelli, L. & Antzelevitch, C. Mechanisms of atrial-selective block of Na1 channels by ranolazine: II. Insights froma mathematicalmodel.Am. J. Physiol. Heart Circ. Physiol. 301, H1615-H1624 (2011).
12. Wang, Y. et al. Merging structural motifs of functionalized amino acids and a-aminoamides results in novel anticonvulsant compounds with significant effects on slow and fast inactivation of voltage-gated sodium channels and in the treatment of neuropathic pain. ACS Chem. Neurosci. 2, 317-322 (2011).
13. Pavlov, E. et al. The pore, not cytoplasmic domains, underlies inactivation in a prokaryotic sodium channel. Biophys. J. 89, 232-242 (2005).
14. Yue, L.,Navarro, B., Ren, D., Ramos, A.&Clapham, D. E. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 120, 845-853 (2002).
15. Zhao, Y., Yarov-Yarovoy, V., Scheuer, T. & Catterall, W. A. A gating hinge in Na1 channels: a molecular switch for electrical signaling. Neuron 41, 859-865 (2004).
16. Zhao, Y., Scheuer, T. & Catterall, W. A. Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc. Natl Acad. Sci. USA 101, 17873-17878 (2004).
17. Irie, K. et al. Comparative study of the gating motif and C-type inactivation in prokaryotic voltage-gatedsodiumchannels. J. Biol.Chem.285,3685- 3694(2010).
18. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K1 conduction and selectivity. Science 280, 69-77 (1998).
19. Cuello, L. G., Jogini, V., Cortes, D. M. & Perozo, E. Structural mechanism of C-type inactivation in K1 channels. Nature 466, 203-208 (2010).
20. Chen, Y., Yu, F. H., Surmeier, D. J., Scheuer, T. & Catterall, W. A. Neuromodulation of Na1 channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 49, 409-420 (2006).
21. Wang, S. Y. & Wang, G. K. A mutation in segment I-S6 alters slow inactivation of sodium channels. Biophys. J. 72, 1633-1640 (1997).
22. Vilin, Y. Y., Fujimoto, E. & Ruben, P. C. A single residue differentiates between human cardiac and skeletal muscle Na1 channel slow inactivation. Biophys. J. 80, 2221-2230 (2001).
23. Zarrabi, T. et al. A molecular switch between the outer and the inner vestibules of the voltage-gated Na1 channel. J. Biol. Chem. 285, 39458-39470 (2010).
24. Ragsdale, D. S.,McPhee, J. C., Scheuer, T.&Catterall, W. A.Molecular determinants of state-dependent block of sodium channels by local anesthetics. Science 265, 1724-1728 (1994).
25. Yarov-Yarovoy, V. et al. Molecular determinants of voltage-dependent gating and binding of pore-blocking drugs in transmembrane segment IIIS6 of the Na1 channel a subunit. J. Biol. Chem. 276, 20-27 (2001).
26. Yarov-Yarovoy, V. et al. Role of amino acid residues in transmembrane segments IS6 and IIS6 of the sodium channel a subunit in voltage-dependent gating and drug block. J. Biol. Chem. 277, 35393-35401 (2002).
27. Nau, C. & Wang, G. K. Interactions of local anesthetics with voltage-gated Na1 channels. J. Membr. Biol. 201, 1-8 (2004).
28. Hille, B. Local anesthetics: hydrophilic and hydrophobic pathways for the drugreceptor reaction. J. Gen. Physiol. 69, 497-515 (1977).
29. Villalba-Galea, C. A., Sandtner, W., Starace, D. M. & Bezanilla, F. S4-based voltage sensors have three major conformations. Proc. Natl Acad. Sci. USA 105, 17600-17607 (2008).
30. Wang, J. et al. Mapping the receptor site for a-scorpion toxins on a Na1 channel voltage sensor. Proc. Natl Acad. Sci. USA 108, 15426-15431 (2011).
31. Koth, C. M. & Payandeh, J. Strategies for the cloning and expression ofmembrane proteins. Adv. Protein Chem. Struct. Biol. 76, 43-86 (2009).
32. Faham, S. et al. Crystallization of bacteriorhodopsin from bicelle formulations at room temperature. Protein Sci. 14, 836-840 (2005).
33. Kauffmann, B., Weiss, M. S., Lamzin, V. S. & Schmidt, A. How to avoid premature decay of your macromolecular crystal: a quick soak for long life. Structure 14, 1099-1105 (2006).
34. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
35. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
36. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
37. Jones, T. A., Zou, J. Y., Cowan,S. W.&Kjeldgaard, M.Improved methods for building proteinmodels in electron densitymaps and the location of errors in thesemodels. Acta Crystallogr. A 47, 110-119 (1991).
38. Painter, J. & Merritt, E. A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D 62, 439-450 (2006).
39. Winn, M. D., Murshudov, G. N. & Papiz, M. Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321 (2003).
40. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255 (1997).
41. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
42. Laskowski, R. A., Moss, D. S. & Thornton, J. M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067 (1993).
43. Petrek, M., Kosinova, P., Koca, J. & Otyepka, M. MOLE: a Voronoi diagram-based explorer of molecular channels, pores, and tunnels. Structure 15, 1357-1363 (2007).
44. Ho, B. K. & Gruswitz, F. HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49 (2008).
45. Kleywegt, G. J. Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D 52, 842-857 (1996).
46. PyMOL Molecular Graphics System. Version 1.2r3pre (Schrödinger LLC).