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

Journal of General Physiology

Volumn 110, Issue 6, 1997, Pages 693-715

  Sun, Ye Ming ^a   Favre, Isabelle ^a   Schild, Laurent ^b   Moczydlowski, Edward ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

conotoxin; Ca2+ channel; Ionic selectivity; Na+ channel; Selectivity filter

Indexed keywords

ALANINE; ASPARTIC ACID; CALCIUM CHANNEL; CALCIUM ION; DIVALENT CATION; GLUTAMIC ACID; LYSINE; MUTANT PROTEIN; OMEGA CONOTOXIN; PROTON; SODIUM CHANNEL; SODIUM ION; TETRYLAMMONIUM;

AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; ION CURRENT; PROTEIN DOMAIN;

ALANINE; ALKALIES; CALCIUM; CATIONS, DIVALENT; CELLS, CULTURED; CONOTOXINS; ELECTRIC STIMULATION; HUMANS; ION CHANNEL GATING; KIDNEY; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; PATCH-CLAMP TECHNIQUES; PEPTIDES, CYCLIC; PROTONS; SAXITOXIN; SENSITIVITY AND SPECIFICITY; SODIUM CHANNELS; TETRODOTOXIN;

EID: 0030777655     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.110.6.693     Document Type: Article

References (60)

1. Almers, W., and E.W. McCleskey. 1984. Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J. Physiol. (Lond.). 353:585-608.
2. Almers, W., E.W. McCleskey, and P.T. Palade. 1984. A non-selective cation conductance in frog muscle membrane blocked by micromolar external calcium ions J. Physiol. (Lond.). 353:565-583.
3. Armstrong, C.M., and G. Cota. 1991. Calcium ion as a cofactor in Na channel gating. Proc. Natl. Acad. Sci. USA. 88:6528-6531.
4. Armstrong, C.M., and W.F. Gilly. 1992. Access resistance and space clamp problems associated with whole-cell patch clamping. Methods Enzymol. 207:100-122.
5. Becker, S., E. Prusak-Sochaczewski, G. Zamponi, A.G. Beck-Sickinger, R.D. Gordon, and R.J. French. 1992. Action of derivatives of μ-conotoxin GIIIA on sodium channels. Single amino acid substitutions in the toxin separately affect association and dissociation rates. Biochemistry. 31:8229-8238.
6. Behrens, M.I., A. Oberhauser, F. Bezanilla, and R. Latorre. 1989. Batrachotoxin-inodified sodium channels from squid optic nerve in planar bilayers: ion conduction and gating properties. J. Gen. Physiol. 93:23-41.
7. Bezanilla, F., and C.M. Armstrong. 1972. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J. Gen. Physiol. 60:588-608.
8. Campbell, D.T. 1976. Ionic selectivity of the sodium channel of frog skeletal muscle. J. Gen. Physiol. 67:295-307.
9. Campbell, D.T., and B. Hille. 1976. Kinetic and pharmacological properties of the sodium channel of frog skeletal muscle. J. Gen. Physiol. 67:309-323.
10. Chanine, M., L.-Q. Chen, N. Fotouhi, R. Walsky, D. Fry, V. Santarelli, R. Horn, and R.G. Kallen. 1995. Characterizing the μ-conotoxin binding site on voltage-sensitive sodium channels with toxin analogs and channel mutations. Receptors Channels. 3:161-174.
11. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
12. + channel pore. J. Membr. Biol. 155:11-25.
13. 2+ channels. J. Gen. Physiol. 108: 363-374.
14. + channel revealed by cysteine mutagenesis. Neuron. 16:1037-1047.
15. + permeability ratios of nicotinic acetylcholine receptors are reduced by mutations near the intracellular end of the M2 region. J. Gen. Physiol. 99:545-572.
16. Coronado, R., and J.S. Smith. 1987. Monovalent ion current through single calcium channels of skeletal muscle transverse tubules. Biophys. J. 51:497-502.
17. Cukierman, S., W.C. Zinkand, R.J. French, and B.K. Krueger. 1988. Effects of membrane surface charge and calcium on the gating of rat brain sodium channels in planar bilayers. J. Gen. Physiol. 92: 431-447.
18. Daumas, P., and O.S. Andersen. 1993. Proton block of rat brain sodium channels: evidence for two proton binding sites and multiple occupancy. J. Gen. Physiol. 101:27-43.
19. + channel mutant: possible localization of a binding site in the outer vestibule. Biophys. J. 69:1657-1665.
20. Dwyer, T.M., D.J. Adams, and B. Hille. 1980. The permeability of the endplate channel to organic cations in frog muscle. J. Gen. Physiol. 75:469-492.
21. Dwyer, T.M., and J.M. Farley. 1984. Permeability properties of chick myotube acetycholine-activated channels. Biophys. J. 45:529-539.
22. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J. Membr. Biol. 76:197-225.
23. Eisenman, G., and J.A. Dani. 1987. An introduction to molecular architecture and permeability of ion channels. Annu. Rev. Biophys. Biophys. Chem. 16:205-226.
24. 2+ interactions. Neuron. 15:1121-1132.
25. Favre, I., E. Moczydlowski, and L. Schild. 1995. Specificity for block by saxitoxin and divalent cations at a residue which determines sensitivity of sodium channel subtypes to guanidinium toxins. J. Gen. Physiol. 106:203-229.
26. 2+ in the voltagegated sodium channel. Biophys. J. 71:3110-3125.
27. Frankenhaeuser, B., and A.L. Hodgkin. 1957. The action of calcium on the electrical properties of squid axons. J. Physiol. (Lond.). 137:218-244.
28. Goulding, E.H., G.R. Tibbs, D. Liu, and S.A. Siegelbaum. 1993. Role of H5 domain in determining pore diameter and ion permeation through cyclic nucleotide-gated channels. Nature. 364: 61-64.
29. Heinemann, S.H., H. Terlau, W. Stühmer, K. Imoto, and S. Numa. 1992. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature. 356:441-443.
30. Heinemann, S.H., T. Schlief, Y. Mori, and K. Imoto. 1994. Molecular pore structure of voltage-gated sodium and potassium channels. Braz. J. Med. Biol. Res. 27:2781-2802.
31. Hess, P., and R.W. Tsien. 1984. Mechanism of ion permeation through calcium channels. Nature (Lond.). 309:453-456.
32. Hille, B. 1971. The permeability of the sodium channel to organic cations in myelinated nerve. J. Gen. Physiol. 58:599-619.
33. Hille, B. 1972. The permeability of the sodium channel to metal cations in myelinated nerve. J. Gen. Physiol. 59:637-658.
34. Hille, B. 1973. Potassium channels in myelinated nerve. Selective permeability to small cations. J. Gen. Physiol. 61:669-686.
35. Hille, B. 1992. Ionic Channels of Excitable Membranes. 2nd ed. Sinauer Associates, Inc., Sunderland, MA. 607 pp.
36. Hille, B., A.M. Woodhull, and B.I. Shapiro. 1975. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos. Trans. R Soc. Lond. B Biol. Sci. 270:301-318.
37. Kim, M.-S., T. Mori, L.-X. Sun, K. Imoto, and Y. Mori. 1993. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett. 318:145-148.
38. 2+ channel in rat phaeochromocytoma cells: two sets of ion binding sites in the pore. J. Physiol. (Camb.). 466:629-655.
39. Lancelin, J.-M., D. Kohda, S. Tate, Y. Yanagawa, T. Abe, M. Satake, and F. Inagaki. 1991. Tertiary structure of conotoxin GIIIA in aqueous solution. Biochemistry. 30:6908-6916.
40. Lewis, C.A. 1979. Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J. Physiol. (Camb.). 286:417-445.
41. McCleskey, E.W., and W. Almers. 1985. The Ca channel in skeletal muscle is a large pore. Proc. Natl. Acad. Sci. USA. 82:7149-7153.
42. Mozhayeva, G.N., A.P. Naumov, and Y.A. Negulyaev. 1981. Evidence for existence of two acid groups controlling the conductance of sodium channel. Biochim. Biophys. Acta. 643:251-255.
43. Nilius, B. 1988. Calcium block of guinea-pig heart sodium channels with and without modification by the piperazynylindole DPI 201-106. J. Physiol. (Camb.). 399:537-558.
44. Pappone, P.A. 1980. Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibers. J. Physiol. (Camb.). 306:377-410.
45. 2+ channel. Biophys. J. 69:1801-1813.
46. + channels. J. Gen. Physiol. 97:89-115.
47. Sather, W.A., J. Yang, and R.W. Tsien. 1994. Structural basis of ion channel permeation and selectivity. Curr. Opin. Neurobiol. 4:313-323.
48. Sato, K., Y. Ishida, K. Wakamatsu, R. Kato, H. Honda, Y. Ohizumi, H. Nakamura, M. Ohya, J.-M. Lancelin, D. Kohda, and F. Inagaki. 1991. Active site of μ-conotoxin GIIIA, a peptide blocker of muscle sodium channels. J. Biol. Chem. 266:16989-16991.
49. + channels prolonged by batrachotoxin: current-voltage behavior and single-chanel kinetics. J. Gen. Physiol. 97:117-142.
50. Schlief, T., R. Schönherr, K. Imoto, and S.H. Heinemann. 1996. Pore properties of rat brain II sodium channels mutated in the selectivity filter domain. Eur. Biophys. J. 25:75-91.
51. Sternberg, M.J.E., F.R.F. Hayes, A.J. Russell, P.G. Thomas, and A.R. Fersht. 1987. Prediction of electrostatic effects of engineering of protein charges. Nature. 330:86-88.
52. Tang, S., G. Mikala, A. Bahinski, A. Yatani, G. Varadi, and A. Schwartz. 1993. Molecular localization of ion selectivity sites within the pore of a human L-type cardiac calcium channel. J. Biol. Chem. 268:13026-13029.
53. Terlau, H., S.H. Heinemann, W. Stühmer, M. Pusch, F. Conti, K. Imoto, and S. Numa. 1991. Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II. FEBS Lett. 293:93-96.
54. Trimmer, J.S., S.S. Cooperman, S.A. Tomiko, J. Zhou, S.M. Crean, M.B. Boyle, R.G. Kallen, Z. Sheng, R.L. Barchi, F.J. Sigworth, R.H. Goodman, W.S. Agnew, and G. Mandel. 1989. Primary structure and functional expression of a mammalian skeletal muscle sodium channel. Neuron. 3:33-49.
55. Tsushima, R.G., R.A. Li, and P.H. Backx. 1997. Altered ionic selectivity of the sodium channel revealed by cysteine mutations within the pore. J. Gen. Physiol. 109:463-475.
56. Wang, F., and K. Imoto. 1992. Pore size and negative charge as structural determinants of permeability in the Torpedo nicotinic acetylcholine receptor channel. Proc. R. Soc. Lond. B Biol. Sci. 250: 11-17.
57. Woodhull, A.M. 1973. Ionic blockage of sodium channel in nerve. J. Gen. Physiol. 61:687-708.
58. Yamamoto, D., J.Z. Yeh, and T. Narahashi. 1984. Voltage-dependent calcium block of normal and tetramethrin-modified single sodium channels. Biophys. J. 45:337-344.
59. 2+ channels. Nature. 366:158-161.
60. Zhang, J.-F., and S.A. Siegelbaum. 1991. Effects of external protons on single cardiac sodium channels from guinea pig ventricular myocytes. J. Gen. Physiol. 98:1065-1083.