On the structural basis for ionic selectivity among Na+, K+, and Ca2+ in the voltage-gated sodium channel

Biophysical Journal

Volumn 71, Issue 6, 1996, Pages 3110-3125

  Favre, Isabelle ^a,b   Moczydlowski, Edward ^b   Schild, Laurent ^a  

^a University of Lausanne Departement de Pharmacologie et de Toxicologie   (Switzerland)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; LYSINE; POTASSIUM CHANNEL; POTASSIUM ION; SODIUM CHANNEL; SODIUM ION;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CONTROLLED STUDY; ION CONDUCTANCE; ION PERMEABILITY; NONHUMAN; OOCYTE; PROTEIN DOMAIN; VOLTAGE CLAMP; XENOPUS LAEVIS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0029754658     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79505-X     Document Type: Article

References (77)

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. Andersen, O. S. 1989. Kinetics of ion movement mediated by carriers and channels. Methods Enzymol. 171:62-112.
3. Armstrong, C. M. 1975. Potassium pores of nerve and muscle membranes. In Membranes: A Series of Advances, Vol. 3. G. Eisenman, editor. Marcel Dekker, New York. 325-358.
4. Backx, P. H., D. T. Yue, J. H. Lawrence, E. Marban, and G. F. Tomaselli. 1992. Molecular localization of an ion-binding site within the pore of mammalian sodium channels. Science. 257:248-251.
5. Begenisich, T. 1987. Molecular properties of ion permeation through sodium channels. Ann. Rev. Biophys. Biophys. Chem. 16:247-263.
6. Butler, J. N. 1964. Ionic Equilibrium. A Mathematical Approach. Addison-Wesley, Reading, MA.
7. Campbell, D. T. 1976. Ionic selectivity of the sodium channel of frog skeletal muscle. J. Gen. Physiol. 67:295-307.
8. Catterall, W. A. 1992. Cellular and molecular biology of voltage-gated sodium channels. Physiol Rev. 72:S15-S48.
9. Catterall, W. A. 1995. Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64:493-531.
10. Chandler, W. K., and H. Meves. 1965. Voltage clamp experiments on internally perfused giant axons. J. Physiol. (Lond.). 180:788-820.
11. Cukierman, S., and B. K. Krueger. 1990. Modulation of sodium channel gating by external divalent cations: differential effects on opening and closing rates. Pfluegers Arch. 416:360-367.
12. Dang, Q. D., A. Vindigni, and E. DiCera. 1995. An allosteric switch controls the procoagulant and anticoagulant activities of thrombin. Proc. Natl. Acad. Sci. U.S.A. 92:5977-5981.
13. 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.
14. Ebert, G. A., and L. Goldman. 1976. The permeability of the sodium channel in Myxicola to the alkali cations. J. Gen. Physiol. 68:327-340.
15. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilbrium processes in ion permeation through channels. J Membr. Biol. 76:197-225.
16. 2+ interactions. Neuron. 15:1121-1132.
17. Emsley, J., H. E. White, B. P. O'Hara, G. Oliva, N. Srinivasan, I. J. Tickle, T. L. Blundell, M. B. Pepys, and S. P. Wood. 1994. Structure of pentameric human serum amyloid P component. Nature. 367: 338-345.
18. Falke, J. J., S. K. Drake, A. L. Hazard, and O. B. Peerson. 1994. Molecular tuning of ion binding to calcium signaling proteins. Q. Rev. Biophys. 27:219-290.
19. 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.
20. 2+ selectivity in the voltage-gated Na channel. Biophys. J. 40:A78.
21. Fersht, A. R. 1985. Enzyme Structure and Mechanism. 2nd ed. W. H. Freeman and Co., New York.
22. Fersht, A. R. 1987. The hydrogen bond in molecular recognition. Trends Biochem. Sci. 12:301-304.
23. Frankenhaeuser, B., and A. L. Hodgkin. 1957. The action of calcium on the electrical properties of squid axons. J. Physiol. (Lond.). 137: 218-244.
24. French, R. J., J. F. Worley, W. F. Wonderlin, A. S. Kularatna, and B. K. Krueger. 1994. Ion permeation, divalent cation block, and chemical modification of single sodium channels. Description by single- and double-occupancy rate-theory models. J. Gen. Physiol. 103:447-470.
25. Glusker, J. P. 1991. Structural aspects of metal liganding to functional groups in proteins. Adv. Protein Chem. 42:1-76.
26. Goldin, A. L. 1995. Voltage-gated sodium channels. In Handbook of Receptors and Channels: Ligand and Voltage-Gated Channels. R. A. North, editor. CRC Press, Boca Raton, FL. 73-111.
27. + channels. In Ion Channels and Genetic Diseases. Society of General Physiologists Series, Vol. 50. D. C. Dawson and R. A. Frizzell, editors. Rockefeller University Press, New York. 3-16.
28. Heinemann, S. H., and F. J. Sigworth. 1993. Fluctuations of ionic currents and ion channel proteins. In Thermodynamics of Membrane Receptors and Channels. M. B. Jackson, editor. CRC Press, Boca Raton, FL. 407-422.
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. 56:441-443.
30. Hess, P., and R. W. Tsien. 1984. Mechanism of ion permeation through calcium channels. Nature. 309:453-456.
31. Hille, B. 1971. The permeability of the sodium channel to organic cations in myelinated nerve. J. Gen. Physiol. 58:599-619.
32. Hille, B. 1972. The permeability of the sodium channel to metal cations in myelinated nerve. J. Gen. Physiol. 59:637-658.
33. Hille, B. 1975a. Ionic selectivity of Na and K channels of nerve membranes. In Membranes: A Series of Advances, Vol. 3. G. Eisenman, editor. Marcel Dekker, New York. 255-323.
34. Hille, B. 1975b. Ionic selectivity, saturation, and block in sodium channels: a four-barrier model. J. Gen. Physiol. 66:535-560.
35. Hille, B. 1992. Ionic Channels of Excitable Membranes. 2nd ed. Sinauer Associates. Sunderland, MA.
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-Biol. Sci. 270:301-318.
37. Hohenester, E., J. W. Keller, and J. N. Jansonius. 1994. An alkali metal ion size-dependent switch in the active site structure of dialkylglycine decarboxylase. Biochemistry. 33:13561-13570.
38. Huber, A. H., Y. E. Wang, A. J. Bieber, and P. J. Bjorkman. 1994. Crystal structure of tandem type III fibronectin domains from Drosophila neuroglian at 2.0 A. Neuron. 12:717-731.
39. Kim, M-S., T. Morii, L-X. Sun, K. Imoto, and Y. Mon. 1993. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett. 318:145-148.
40. Läuger, P., W. Stephan, and E. Frehland. 1980. Fluctuations of barrier structure in ionic channels. Biochim. Biophys. Acta. 602:167-180.
41. Levitt, D. G. 1986. Interpretation of biological ion channel flux data - reaction rate versus continuum theory. Ann. Rev. Biophys. Biophys. Chem. 1986. 15:29-57.
42. 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. (Lond.). 286:417-445.
43. + channel. Biophys. J. 66:1-13.
44. McCleskey, E. W., and W. Almers. 1985. The Ca channel in skeletal muscle is a large pore. Proc. Natl. Acad. Sci. U.S.A. 82:7149-7153.
45. McKenna, R., D. Xia, P. Willingmann, L. L. Ilag, S. Krishaswamy, M. G. Rossmann, N. H. Olson, T. S. Baker, and N. L. Incardona. 1992. Atomic structure of single-stranded DNA bacteriophage FX174 and its functional implications. Nature. 355:137-143.
46. McPhalen, C. A., N. C. J. Strynadka, and M. N. G. James. 1991. Calcium-binding sites in proteins: a structural perspective. Adv. Protein Chem. 42:77-144.
47. Meves, H., and W. Vogel. 1973. Calcium inward curents in internally perfused giant axons. J. Physiol. (Lond.). 235:225-265.
48. 2+ channel pore. FEBS Lett. 335: 265-269.
49. Miller, C. 1993. Potassium selectivity in proteins: oxygen cage or π in the face? Science. 261:1692-1693.
50. Moss, G. W. J., and E. Moczydlowski. 1995. Concepts of single-channels analysis: inferring function from fluctuations. In Ion Channels: A Practical Approach. R. H. Ashley, editor. Oxford University Press, Oxford, UK. 69-112.
51. + channel from toad skeletal muscle. Biophys. J. 64:1038-1050.
52. Nilius, B. 1988. Calcium block of guinea-pig heart sodium channels with and without modification by the piperazinylindole DPI 201-106. J. Physiol. (Lond.). 399:537-558.
53. Pappone, P. A. 1980. Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibers. J. Physiol. (Lond). 306:377-410.
54. 2+ channel. Biophys. J. 69:1801-1813.
55. 2+ channel. Nature. 329:243-246.
56. + channels from rat skeletal muscle with a multi-ion pore. Biophys. J. 61:495-508.
57. + channels prolonged by batrachotoxin. J. Gen. Physiol. 97:89-115.
58. Satin, J., J. W. Kyle, M. Chen, P. Bell, L. L. Cribbs, H. A. Fozzard, and R. B. Rogart. 1992. A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science. 256:1202-1205.
59. + channels prolonged by batrachotoxin. Current-voltage behavior and single-channel kinetics. J. Gen. Physiol. 97:117-142.
60. 2+/saxitoxin binding site. Biophys. J. 59: 523-537.
61. 2+-occupied conductance states of cardiac sodium channels modified by batrachotoxin: exploring ion-ion interactions in a multi-ion channel. Biophys. J. 66:653-666.
62. Sheets, M. F., and D. A. Hanck. 1992. Mechanisms of extracellular divalent and trivalent cation block of the sodium current in canine cardiac purkinje cells. J. Physiol. (Lond.). 454:299-320.
63. K variability. J. Gen. Physiol. 97:1013-1041.
64. Spalding, B. C., P. Taber, J. G. Swift, and P. Horowicz. 1990. Zinc inhibition of chloride efflux from skeletal muscle of Rana pipiens and its modification by external pH and chloride activity. J. Membr. Biol. 116:195-214.
65. Strong, M., K. G. Chandy, and G. A. Gutman. 1993. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol Biol. Evol. 10:221-242.
66. Tanabe, T., H. Takeshima, A. Mikami, V. Flockerzi, H. Takahashi, K. Kangawa, M. Kojima, H. Matsuo, T. Hirose, and S. Numa. 1987. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 328:313-318.
67. 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.
68. 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 chanel II. FEBS Lett. 293:93-96.
69. Toney, M. D., E. Hohenester, S. W. Cowan, and J. N. Jansonius. 1993. Dialkylglycine decarboxylase structure: bifunctional active site and alkali metal sites. Science. 261:756-759.
70. 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.
71. Tsien, R. W., P. Hess, E. W. McCleskey, and R. L. Rosenberg. 1987. Calcium channels: mechanisms of selectivity, permeation and block. Ann. Rev. Biophys. Biophys. Chem. 16:265-290.
72. +-activated enzyme. Biochemistry. 31:11721-11730.
73. Woodhull, A. M. 1973. Ionic blockage of sodium chanels in nerve. J. Gen. Physiol. 61:687-708.
74. 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.
75. 2+ channels. Nature. 366:158-161.
76. Yellen, G. 1987. Permeation in potassium channels: implications for channel structure. Ann. Rev. Biophys. Biophys. Chem. 16:227-246.
77. 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.