Deciphering voltage-gated Na+ and Ca2+ channels by studying prokaryotic ancestors

Trends in Biochemical Sciences

Volumn 40, Issue 9, 2015, Pages 526-534

  Catterall, William A ^a   Zheng, Ning ^a,b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

NaVAb; NaChBac; Selectivity filter; Slow inactivation; Voltage sensor; Voltage gated calcium channel; Voltage gated sodium channel

Indexed keywords

VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; CALCIUM CHANNEL;

ACTION POTENTIAL; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; GENETIC CONSERVATION; HORMONE RELEASE; HYDROPHOBICITY; ION CONDUCTANCE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTIC CELL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; CHEMISTRY; HUMAN; METABOLISM;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

ANIMALS; CALCIUM CHANNELS; HUMANS; PROTEIN CONFORMATION; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84940467041     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.07.002     Document Type: Review

References (56)

1. Hille B. Ionic Channels of Excitable Membranes 2001, Sinauer Associates. 3rd edn.
2. Tsien R.W. Calcium channels in excitable cell membranes. Annu. Rev. Physiol. 1983, 45:341-358.
3. Catterall W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 2011, 3:a003947.
4. Catterall W.A. The molecular basis of neuronal excitability. Science 1984, 223:653-661.
5. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
6. Stühmer W. Structure-function studies of voltage-gated ion channels. Annu. Rev. Biophys. Biophys. Chem. 1991, 20:65-78.
7. Yu F.H., Catterall W.A. The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci. STKE 2004, 2004:re15.
8. Ren D., et al. A prokaryotic voltage-gated sodium channel. Science 2001, 294:2372-2375.
9. Payandeh J., et al. The crystal structure of a voltage-gated sodium channel. Nature 2011, 475:353-358.
10. Payandeh J., et al. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 2012, 486:135-139.
11. Zhang X., et al. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 2012, 486:130-134.
12. Tsai C.J., et al. Two alternative conformations of a voltage-gated sodium channel. J. Mol. Biol. 2013, 425:4074-4088.
13. McCusker E.C., et al. Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing. Nat. Commun. 2012, 3:1102.
14. V) protein dissection creates a set of functional pore-only proteins. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12313-12318.
15. Shaya D., et al. Structure of a prokaryotic sodium channel pore reveals essential gating elements and an outer ion binding site common to eukaryotic channels. J. Mol. Biol. 2014, 426:467-483.
16. Bagneris C., et al. Structural model of the open-closed-inactivated cycle of prokaryotic voltage-gated sodium channels. J. Gen. Physiol. 2015, 145:5-16.
17. Bagneris C., et al. Role of the C-terminal domain in the structure and function of tetrameric sodium channels. Nat. Commun. 2013, 4:2465.
18. Irie K., et al. The C-terminal helical bundle of the tetrameric prokaryotic sodium channel accelerates the inactivation rate. Nat. Commun. 2012, 3:793.
19. Armstrong C.M., Bezanilla F. Currents related to movement of the gating particles of the sodium channels. Nature 1973, 242:459-461.
20. Bezanilla F. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 2000, 80:555-592.
21. + channels. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:7292-7297.
22. Yarov-Yarovoy V., et al. Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E93-E102.
23. Catterall W.A. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 2010, 67:915-928.
24. Vargas E., et al. An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J. Gen. Physiol. 2012, 140:587-594.
25. V1.2: structural basis of electromechanical coupling. Science 2005, 309:903-908.
26. + channel. Science 2005, 309:897-903.
27. + channel in a lipid membrane-like environment. Nature 2007, 450:376-382.
28. Li Q., et al. Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nat. Struct. Mol. Biol. 2014, 21:244-252.
29. Hodgkin A.L., Huxley A.F. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J. Physiol. 1952, 116:497-506.
30. Vilin Y.Y., Ruben P.C. Slow inactivation in voltage-gated sodium channels: molecular substrates and contributions to channelopathies. Cell Biochem. Biophys. 2001, 35:171-190.
31. Rudy B. Slow inactivation of the sodium conductance in squid giant axons. Pronase resistance. J. Physiol. 1978, 283:1-21.
32. + channels; a molecular switch for electrical signaling. Neuron 2004, 41:859-865.
33. Pavlov E., et al. The pore, not cytoplasmic domains, underlies inactivation in a prokaryotic sodium channel. Biophys. J. 2005, 89:232-242.
34. Zhao Y., et al. Reversed voltage-dependent gating of a bacterial sodium channel with proline substitutions in the S6 transmembrane segment. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17873-17878.
35. Hille B. The permeability of the sodium channel to organic cations in myelinated nerve. J. Gen. Physiol. 1971, 59:599-619.
36. Hille B. The permeability of the sodium channel to metal cations in myelinated nerve. J. Gen. Physiol. 1972, 59:637-658.
37. Hille B. Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J. Gen. Physiol. 1975, 66:535-560.
38. Ulmschneider M.B., et al. Molecular dynamics of ion transport through the open conformation of a bacterial voltage-gated sodium channel. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:6364-6369.
39. Zhou Y., et al. Chemistry of ion coordination and hydration revealed by a potassium channel-Fab complex at 2.0Å resolution. Nature 2001, 414:43-48.
40. VAb. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:11331-11336.
41. VRh. Cell Res. 2013, 23:409-422.
42. Heinemann S.H., et al. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 1992, 356:441-443.
43. 2+ interactions. Neuron 1995, 15:1121-1132.
44. 2+ channels. Nature 1993, 366:158-161.
45. Yue L., et al. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 2002, 120:845-853.
46. 2+ selectivity of a voltage-gated calcium channel. Nature 2014, 505:56-61.
47. Mccleskey E.W., Almers W. The Ca channel in skeletal-muscle is a large pore. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:7149-7153.
48. Almers W., McCleskey E.W. The nonselective conductance due to calcium channels in frog muscle: calcium-selectivity in a single file pore. J. Physiol. 1984, 353:585-608.
49. ++. J. Physiol. 1984, 353:565-583.
50. Hess P., Tsien R.W. Mechanism of ion permeation through calcium channels. Nature 1984, 309:453-456.
51. Dang T.X., McCleskey E.W. Ion channel selectivity through stepwise changes in binding affinity. J. Gen. Physiol. 1998, 111:185-193.
52. Sather W.A., McCleskey E.W. Permeation and selectivity in calcium channels. Annu. Rev. Physiol. 2003, 65:133-159.
53. Ashcroft F.M. Ion Channels and Disease 2000, Academic Press.
54. Cox B., Gosling M. Ion Channel Drug Discovery 2014, Royal Society of Chemistry.
55. VMs channel as a structural and functional model for eukaryotic sodium channel antagonism. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:8428-8433.
56. Catterall W.A., Swanson T.M. Structural basis for pharmacology of voltage-gated sodium and calcium channels. Mol. Pharmacol. 2015, 88:141-150.