Advertisement

Pharmacology of Small-Conductance, Calcium-Activated K+Channels

  • Eric Blanc
  • Hervé Darbon

Abstract

K+ channels are transmembrane proteins dedicated to allowing K+ fluxes through physiological membranes. Topologically, they can be described as transmembrane segments surrounding a pore-forming region directly involved in K+ selectivity and transfer. As originally depicted by Hodgkin and Huxley (1952a)-Hodgkin and Huxley (1952d), K+ channels are involved in the propagation of the action potential. Their opening is regulated by the level of membrane depolarization, and their role is to return the membrane to its resting potential. However, far beyond this unique role, K+ channels form the most diverse ion channel family described so far. They are present in nearly all cell types, and their biophysical as well as their pharmacological profiles are among the most complex ever seen.

Keywords

Disulfide Bridge Basic Residue Selectivity Filter Pore Region Scorpion Venom 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abia, A., Lobaton, C. D., Moreno, A., and Garcia-Sancho, J., 1986, Leiurus quinquestriatus venom inhibits different kinds of Ca2+-dependent K+ channels, Biochim. Biophys. Acta 856:403–407.PubMedCrossRefGoogle Scholar
  2. Adelman, J. P., Shen, Z. K., Kavanaugh, M. P., Warren, R. A., Wu, Y. N., Lagrutta, A., Bond, C. T., and North, R. A., 1992, Calcium-activated K+ channels expressed from cloned complementary DNAs, Neuron 9:209–216.PubMedCrossRefGoogle Scholar
  3. Aiyar, J., Withka, J. M., Rizzi, J. P., Singleton, D. H., Andrews, G. C., Lin, W., Boyd, J., Hanson, D. G., Simon, M., Dethlefs, B., Lee, C. L., Hall, J. E., Gutman, G. A., and Chandy, K. G., 1995, Topology of the pore-region of a K+ channel revealed by the NMR-derived structures of scorpion toxins, Neuron 15:1169–1181.PubMedCrossRefGoogle Scholar
  4. Aiyar, J., Rizzi, J. P., Gutman, G. A., and Chandy, K. G., 1996, The signature sequence of voltage-gated K + channels projects into the external vestibule, J. Biol. Chem. 271:31013–31016PubMedCrossRefGoogle Scholar
  5. Atkinson, N. S., Robertson, G. A., and Ganetzky, B., 1991, A component of calcium-activated K+ channels encoded by the Drosophila slo locus, Science 253:551–555.PubMedCrossRefGoogle Scholar
  6. Auguste, P., Hugues, M., and Lazdunski, M., 1989, Polypeptide constitution of receptors for apamin, a neurotoxin which blocks a class of Ca2+-activated K+ channels, FEBS Lett. 248:150–154.CrossRefGoogle Scholar
  7. Auguste, P., Hugues, M., Gravé, B., Gesquire, J. C., Maes, P., Tartar, A., Romey, G., Schweitz, H., and Lazdunski, M., 1990. Leiurotoxin I (scyllatoxin), a peptide ligand for Ca2+-activated K+ channels, J. Biol. Chem. 265:4753–4759.PubMedGoogle Scholar
  8. Auguste, P., Hugues, M., Mourre, C., Moinier, D., Tartar, A., and Lazdunski, M., 1992, Scyllatoxin, a blocker of Ca2+-activated K+ channels: Structure-function relationships and brain localization of the binding sites, Biochemistry 31:648–654.PubMedCrossRefGoogle Scholar
  9. Bargmann, C I., 1998, Neurobiology of the Caenorhabditis elegans genome, Science 282:2028–2033.PubMedCrossRefGoogle Scholar
  10. Blanc, E., Fremont, V., Sizun, P., Meunie, S, Van Rietschoten, J., Thevand A., Bernassau, J. M., and Darbon, H., 1996, Solution structure of P01, a natural scorpion peptide structurally analogous to scorpion toxins specific for apamin-sensitive K+ channel, Proteins 24:359–369.PubMedCrossRefGoogle Scholar
  11. Blanc, E., Sabatier, J. M., Kharrat, R., Meunier, S., el Ayeb, M., Van Rietschoten, J., and Darbon H., 1997, Solution structure of maurotoxin, a scorpion toxin from Scorpio maurus, with high affinity for voltage-gated K+ channels, Proteins 29:321–233.PubMedCrossRefGoogle Scholar
  12. Buisine, E., Wieruszeski, J. M., Lippens, G., Wouters, D., Tartar, A., and Sautiere, P., 1997, Characterization of a new family of toxin-like peptides from the venom of the scorpion Leiurus quinquestriatus hebraeus. 1H-NMR structure of leiuropeptide II, J. Pept. Res. 49:545–555.PubMedCrossRefGoogle Scholar
  13. Butler, A. Tsunoda, S., McCobb, D. P., Wei., A,. and Salkoff, L., 1993, mSlo, a complex mouse gene encoding “maxi” calcium-activated K+ channels, Science 261:221–224.PubMedCrossRefGoogle Scholar
  14. Bystrov, V. F., Okhanov, V. V., Miroshnikov, A. I., and Ovchinnikov. Y. A., 1980, Solution spatial structure of apamin as derived from NMR study, FEBS Lett 119:113–117.PubMedCrossRefGoogle Scholar
  15. Castle, N. A., Haylett, D. G., Morgan, J. M., and Jenkinson, D. H., 1993, Dequalinium: A potent inhibitor of apamin-sensitive K+ channels in hepatocytes and of nicotinic responses in skeletal muscle, Eur. J. Pharmacol. 236:201–207.PubMedCrossRefGoogle Scholar
  16. Chicchi, G. G., Gimenez-Gallego, G., Ber, E., Garcia, M. L., Winquist, R., and Cascieri, M., 1988, Purification and characterization of a unique potent inhibitor of apamin binding from Leiurus quinquestriatus hebraeus venom, J. Biol. Chem. 263:10192–10197.PubMedGoogle Scholar
  17. Cornet, B., Bonmatin, J. M., Hetru, C., Hoffmann, J. A, Ptak, M., and Vovelle, F., 1995, Refined three dimensional structure of insect defensin A, Structure 3:435–448.PubMedCrossRefGoogle Scholar
  18. Cotton, J., Crest, M., Bouet, F., Alessandri, N., Gola, M., Forest, E., Karlsson, E., Castaeda, O., Harvey, A. L., Vita, C., and Menez, A., 1997, A K+ channel toxin from the sea anemone Bunodosoma granulifera, an inhibitor for Kv1 channels, Eur. J. Biochem. 244:192–202.PubMedCrossRefGoogle Scholar
  19. Darbon, H., Blanc, E., and Sabatier, J. M., 1999, Three dimensional structure of scorpion toxins: Towards a new model of interaction with K+ channels, in: Perspectives in Drug Discovery and Design Vol. 15/16 (H. Darbon and J. M. Sabatier, eds.), Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 41–60.Google Scholar
  20. Devaux, C., Knibiehler, M., Defendini, M. L., Mabrouk, K., Rochat, H., Van Rietschoten, J., Baty, D., and Granier, C., 1995, Recombinant and chemical derivatives of apamin: Implication of post-transcriptional C-terminal amidation of apamin in biological activity, Eur. J. Biochem. 231:544–550.PubMedCrossRefGoogle Scholar
  21. Doyle, D. A., Cabral, J. M., Pluetzner, R. A., Kuo A., Gulbis, J. M., Cohen, S. L., Chait, B. T., and MacKinnon, R., 1998, The structure of the K+ channel: Molecular basis of K+ conduction and selectivity, Science 280:69–77.PubMedCrossRefGoogle Scholar
  22. Durell, S. R., and Guy, H. R., 1996, Structural model of the outer vestibule and selectivity filter of the Shaker voltage-gated K+ channel, Neuropharmacolog 35:761–773.CrossRefGoogle Scholar
  23. Durell, S. R., Hao, Y., and Guy, H. R., 1998, Structural models of the transmembrane region of voltage-gated and other K+ channels in open, closed, and inactivated conformations, J. Struct. Biol. 121:263–284.PubMedCrossRefGoogle Scholar
  24. Fremont, V., Blanc, E., Crest, M., Martin-Eauclaire, M.-F., Gola, M., Darbon, H., and Van Rietschoten, J., 1997, Dipole moments of scorpion toxins direct the interaction towards small- or large-conductance Ca2+-activated K+ channels, Lett. Pept. Sci. 4:305–312.Google Scholar
  25. Galanakis, D., Davis C. A., Del Rey Herrero, B., Ganellin, C. R., Dunn, P. M., and Jenkinson D. H., 1995, Synthesis and structure-activity relationships of dequalinium analogues as K+ channel blockers: Investigations on the role of the charged heterocycle, J. Med. Chem. 38:595–606.PubMedCrossRefGoogle Scholar
  26. Galanakis, D., Ganellin, R. C., Dunn, P. M., and Jenkinson, D. H., 1996, On the concept of a bivalent pharmacophore for SKCa channel blockers: Synthesis, pharmacological testing, and radioligand binding studies on mono-, bis-, and trisquinolinium compounds, Arch. Pharm. 329:524–528.CrossRefGoogle Scholar
  27. Goldstein, S. A. N., 1996, A structural vignette common to voltage sensors and conduction pores: Canaliculi, Neuron 16:717–722.PubMedCrossRefGoogle Scholar
  28. Granier, C., Pedroso Muller, E., and Van Rietschoten, J., 1978, Use of synthetic analogs for a study on the structure-activity relationship of apamin, Eur. J. Biochem. 82:293–299.PubMedCrossRefGoogle Scholar
  29. Guy, H. R., and Conti, F., 1990, Pursuing the structure and function of voltage-gated channels, Trends Neurosci. 13:201–206.PubMedCrossRefGoogle Scholar
  30. Habermann, E., and Fischer, K., 1979, Apamin, a centrally acting neurotoxic peptide: Binding and actions, Adv. Cytopharmacol. 3:387–394.PubMedGoogle Scholar
  31. Hanner, M., Schmalhofer, W. A., Munujos, P., Knaus, H. G., Kaczorowski, G. J., and Garcia, M. L., 1997, The β subunit of the high-conductance calcium-activated K+ channel contributes to the high-affinity receptor for charybdotoxin, Proc. Natl. Acad. Sci, U.S.A. 94:2853–2858.PubMedCrossRefGoogle Scholar
  32. Hanner, M., Vianna-Jorge, R., Kamassah, A., Schmalhofer, W. A., Knaus, H. G., Kaczorowski, G. J., and Garcia, M. L., 1998, The beta subunit of the high conductance calcium-activated K+ channel: Identification of residues involved in charybdotoxin binding, J. Biol. Chem. 273:16289–16296.PubMedCrossRefGoogle Scholar
  33. Harvey, A. L., 1997, Recent studies on dendrotoxins and K+ ion channels, Gen Pharmacol. 28:7–12.PubMedCrossRefGoogle Scholar
  34. Harvey, A. L., Bradley, K. N., Cochran, S. A., Rowan, E. G., Pratt, J. A., Quillfeldt, J. A., and Jerusalinsky D. A., 1998, What can toxins tell us for drug discovery?, Toxicon 36:1635–1640.PubMedCrossRefGoogle Scholar
  35. Heginbotham, L. and MacKinnon, R., 1992, The aromatic binding site for tetraethylammonium ion on K+ channels, Neuron 8:483–491.PubMedCrossRefGoogle Scholar
  36. Heginbotham, L., Lu, Z., Abramson, T., and MacKinnon, R., 1994, Mutations in the K+ channel signature sequence, Biophys. J. 66:1061–1067.PubMedCrossRefGoogle Scholar
  37. Hodgkin, A. L., and Huxley, A. F., 1952a, Currents carried by sodium and K+ ions through the membrane of the giant axon of Loligo, J. Physiol. (London) 116:449–472.Google Scholar
  38. Hodgkin, A. L., and Huxley, A.F., 1952b, The components of membrane conductance in the giant axon of Loligo, J. Physiol. (London) 116:473–496.Google Scholar
  39. Hodgkin, A. L., and Huxley, A. F., 1952c, The dual effect of membrane potential on sodium conductance in the giant axon of the squid, J. Physiol. (London) 116:497–506.Google Scholar
  40. Hermann, A. and Erxleben, C. 1987, Charbdotoxin selectively blocks small Ca-activated K channels in Aplysia neurons. J. Gen. Physiol. 90(l):27–47.PubMedCrossRefGoogle Scholar
  41. Hodgkin, A. L., and Huxley, A. F., 1952d, A quantitative description of membrane current and its application to conduction and excitation in nerve, J. Physiol. (London) 117:500–544.Google Scholar
  42. Inisan, A. G., Meunier, S., Fedelli, O., Altbach, M., Fremont, V., Sabatier, J. M., Thevan, A., Bernassau, J.M., Cambillau, C., and Darbon, H., 1995, Structure-activity relationship study of a scorpion toxin with high affinity for apamin-sensitive K+ channels by means of the solution structure of analogues, Int. J. Pept. Protein Res. 45:441–450.PubMedCrossRefGoogle Scholar
  43. Ishii T. M., Maylie J., and Adelman J. P., 1997, Determinants of apamin and d-tubocurarine block in SK K + channels, J. Biol. Chem. 272:23195–23200.PubMedCrossRefGoogle Scholar
  44. Jan, L.Y., and Jan, Y. N., 1992, Structural elements involved in specific K+ channel functions, Annu. Rev. Physiol. 54:537–555.PubMedCrossRefGoogle Scholar
  45. Jaravine, V. A., Nolde, D. E., Reibarkh, M. J., Korolkova, Y. V., Kozlov, S. A., Pluzhnikov, K. A., Grishin, E. V., and Arseniev, A. S., 1997, Three-dimensional structure of OSK1 from Orthochirus scrobiculosus scorpion venom, Biochemistry 36:1223–1232.PubMedCrossRefGoogle Scholar
  46. Kerr, I. D., and Sansom, M. S., 1997, The pore-lining region of Shaker voltage-gated K + channels: Comparison of beta-barrel and alpha-helix bundle models, Biophys. J. 73:581–602.PubMedCrossRefGoogle Scholar
  47. Kharrat, R., Mansuelle, P., Sampieri, F., Crest, M., Martin-Eauclaire, M. F., Rochat, H., and El Ayeb, M., 1997, Maurotoxin, a new four disulfide bridges toxin from Scorpio maurus venom: Purification, structure and pharmacology on K+ channels, FEBS Lett. 406:284–290.PubMedCrossRefGoogle Scholar
  48. Köhler, M., Hirschberg, B., Bond, C. T., Kinzie, J. M., Marrion, N. V., Maylie, J., and Adelman, J. P., 1996, Small-conductance, calcium-activated K+ channels from mammalian brain, Science 273:1709–1714.PubMedCrossRefGoogle Scholar
  49. Labbé-Jullié, C., Granier, C., Albericio, F., Defendini, M. L., Ceard, B., Rochat, H, and Van Rietschoten, J., 1991, Binding and toxicity of apamin: Characterization of the active site, Eur. J. Biochem. 196:639–645.PubMedCrossRefGoogle Scholar
  50. Legros, C., Oughuideni, R., Darbon, H., Rochat, H., Bougis, P. E., and Martin-Eauclaire, M. F., 1996, Characterization of a new peptide from Tityus serrulatus scorpion venom which is a ligand of the apamin-binding site, FEBS Lett. 390:81–84.PubMedCrossRefGoogle Scholar
  51. Levèque, C., Marqueze, B., Couraud, F., and Seagar, M., 1990, Polypeptide components of the apamin receptor associated with a calcium activated K+ channel, FEBS Lett. 275:185–189.PubMedCrossRefGoogle Scholar
  52. Lipkind, G. M., and Fozzard, H. A., 1997, A model of scorpion toxin binding to voltage-gated K+ channels, J. Membr. Biol. 158:187–196.PubMedCrossRefGoogle Scholar
  53. MacKinnon, R., Cohen, S. E., Kuo, A., Lee, A., and Chait, B. T., 1998, Structural conservation in prokaryotic and eukaryotic K+ channels,Science 280:106–109.PubMedCrossRefGoogle Scholar
  54. Martins, J. C, Zhang, W., Tartar, A., Lazdunski, M., and Borremans, F., 1990, Solution conformation of leiurotoxin I (scyllatoxin) by 1H nuclear magnetic resonance, FEBS Lett. 260:249–253.PubMedCrossRefGoogle Scholar
  55. Martins, J. C, Van de Ven, F. J. M., and Borremans, F. A. M., 1995, Determination of the three-dimensional solution structure of scyllatoxin by 1H nuclear magnetic resonance, J. Mol. Biol. 253:590–603.PubMedCrossRefGoogle Scholar
  56. Meunier, S., Bernassau, J. M., Martin-Eauclaire, M. F., Van Rietschoten, J., Cambillau, C., and Darbon, H., 1993, Solution structure of P05-NH2, a scorpion toxin analog with high affinity for the apamin-sensitive K+ channel, Biochemistry 32:11969–11976.PubMedCrossRefGoogle Scholar
  57. Miller, C., Moczydlowski, E., Latorre, R., and Philips, M., 1985, Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle, Nature 313:316–318.PubMedCrossRefGoogle Scholar
  58. Park, C. S., and Miller, C., 1992a, Mapping function to structure in a channel-blocking peptide: Electrostatic mutants of charybdotoxin, Biochemistry 31:7749–7755.PubMedCrossRefGoogle Scholar
  59. Park, C. S., and Miller, C., 1992b, Interaction of charybdotoxin with permeant ions inside the pore of a K+ channel, Neuron 9:307–313.PubMedCrossRefGoogle Scholar
  60. Pease, J. H., and Wemmer, D. E., 1988, Solution structure of apamin determined by nuclear magnetic resonance and distance geometry, Biochemistry 27:8491–8498.PubMedCrossRefGoogle Scholar
  61. Pennington, M. W., Byrnes, M. E., Zaydenberg, I., Khaytin, I., De Chastonay, J., Krafte, D. S., Hill, R., Mahnir, V. M., Volberg, W. A., Gorczyca, W., and Kem, W. R., 1995, Chemical synthesis and characterization of ShK toxin: A potent K+ channel inhibitor from a sea anemone, Int. J. Pept. Protein Res. 46:354–358.PubMedCrossRefGoogle Scholar
  62. Ranganathan, R., Lewis, J. H., and MacKinnon, R., 1996, Spatial localization of the K+ channel selectivity filter by mutant cycle-based structure analysis, Neuron 16:131–139.PubMedCrossRefGoogle Scholar
  63. Rochat, H., Kharrat, R., Sabatier, J. M., Mansuelle, P., Cres, M., Martin-Eauclaire, M. F., Sampieri, F., Oughideni, R., Mabrou, K., Jacquet, G., Van Rietschoten, J., and El Ayeb, M., 1998, Maurotoxin, a four disulfide bridges scorpion toxin acting on K+ channels, Toxicon 36:1609–1611.PubMedCrossRefGoogle Scholar
  64. Romi-Lebrun, R., Martin-Eauclaire, M. F., Escoubas, P., Wu, F. Q., Lebrun, B., Hisada, M., Nakajima, T. 1997, Characterization of four toxins from Buthus martens, scorpion venom, which act on apamin sensitive Ca2+ activated K+ channels. Eur. J. Biochem. 245(2):457–464.PubMedCrossRefGoogle Scholar
  65. Rosa, J. C, Galanaki, D., Ganellin, C. R., Dunn, P. M., and Jenkinson, D. H., 1998, Bis-quinolinium cyclophanes: 6,10-diaza-3(l,3),8(l,4)-dibenzena-l,5(l,4)-diquinolinacyclodecaphane(UCL 1684), the first nanomolar, non-peptidic blocker of the apamin-sensitive Ca2+-activated K+ channel, J. Med. Chem. 41:2–5.PubMedCrossRefGoogle Scholar
  66. Sabatier, J. M., Zerrouck, H., Darbon, H., Mabrouk, K., Benslimane, A., Rochat, H., Martin-Eauclaire, M. F., and Van Rietschoten, J., 1993, P05, a new leiurotoxin I-like scorpion toxin: Synthesis and structure-activity relationships of the α-amidated analog, a ligand of Ca2+-activated K+ channels with increased affinity, Biochemistry 32:2763–2770.PubMedCrossRefGoogle Scholar
  67. Sabatier, J. M., Frmont, V., Mabrouk, K., Crest, M., Darbon, H., Rochat, H., Van Rietschoten, J., and Martin-Eauclaire, M. F., 1994, Leiurotoxin I, a scorpion toxin specific for Ca2+-activated K+ channels, Int. J. Pept. Protein Res. 43:486–495.PubMedCrossRefGoogle Scholar
  68. Sandberg, B. E., 1979, Solid phase synthesis of 13-lysine-apamin, 14-apamin, and the corresponding guanidinated derivatives, Int. J. Pept. Protein Res. 13:327–333.PubMedCrossRefGoogle Scholar
  69. Sanguinetti, M. C., Johnson, J. H., Hammerland, L G., Kelbaugh, P. R., Volkmann, R. A., Saccomano, N.A., and Mueller A. L., 1997, Heteropodatoxins: Peptides isolated from spider venom that block Kv4.2 K + channels, Mol Pharmacol 51:491–498.PubMedGoogle Scholar
  70. Schmid-Antomarchi, H., Hugues, M., Norman, R., Ellory, C., Borsotto, M., and Lazdunski, M., 1984, Molecular properties of the apamin-binding component of the Ca2+ -dependent K+ channel, radiation- inactivation, affinity labeling and solubilization. Eur. J.Biochem. 142:1–6.PubMedCrossRefGoogle Scholar
  71. Schweitz, H., Bruhn, T., Guillemare, E., Moinier, D., Lancelin, J. M., Beress, L., and Lazdunski, M., 1995, Kalicludines and kaliseptine, J. Biol. Chem. 270:25121–25126.PubMedCrossRefGoogle Scholar
  72. Seagar, M., Labbé-Jullié, C., Granier, C., Goll, A., Glossmann, A., Van Rietschoten, J. and Couraud, F., 1986, Molecular structure of rat brain apamin receptor: differential photoaffinity labeling of putative K + channel subunits and target size analysis, Biochemistry 25:4051–4057.PubMedCrossRefGoogle Scholar
  73. Shon, K. J., Stocker, M., Terlau H., Stuhmer W., Jacobsen R., Walker, C., Grilley M., Watkins M., Hillyard, D. R., Gray, W. R., and Olivera, B. M., 1998, K-Conotoxin PVIIA is a peptide inhibiting the Shaker K + channel, J. Biol. Chem. 273:33–38.PubMedCrossRefGoogle Scholar
  74. Swartz, K. J., and MacKinnon, R., 1995, An inhibitor of the Kv2.1 K+ channel isolated from the venom of a Chilean tarantula, Neuron 15:941–949.PubMedCrossRefGoogle Scholar
  75. Vergara, C., Latorre, R., Marrion, N. V., and Adelman, J. P., 1998, Calcium-activated K+ channels, Curr. Opin. Neurobiol. 8:321–329.PubMedCrossRefGoogle Scholar
  76. Vincent, J. P., Schweitz, H., and Lazdunski, M., 1975, Structure-function relationships and site of action of apamin, a neurotoxic polypeptide of bee venom with an action on the central nervous system, Biochemistry 14:2521–2525.PubMedCrossRefGoogle Scholar
  77. Wadsworth, J. D. F., Doorty, K. B., and Strong, P. N., 1994, Comparable 30-kDa apamin binding polypeptides may fulfill equivalent roles within putative subtypes of small conductance Ca2+ -activated K+ channels, J. Biol. Chem. 269:18053–18061.PubMedGoogle Scholar
  78. Wadsworth, J. D. F., Doorty, K. B., Ganellin, C. R., and Strong, P.N., 1996, Photolabile derivatives of 125I-apamin: Defining the structural criteria required for labeling high and low molecular mass polypeptides associated with small conductance Ca2+-activated K+ channels, Biochemistry 35:7917– 7927.PubMedCrossRefGoogle Scholar
  79. Wadsworth, J. D., Torelli, S., Doorty, K. B., and Strong P. N., 1997, Structural diversity among subtypes of small-conductance Ca2+-activated K+ channels, Arch. Biochem. Biophys. 346:151–160.PubMedCrossRefGoogle Scholar
  80. Wallner, M., Meera, P., and Toro, L., 1996, Determinant for β-subunit regulation in high-conductance voltage-activated and Ca2+-sensitive K+ channels: An additional transmembrane region at the N- terminus, Proc. Natl Acad. Sci., USA 93:14922–14927.PubMedCrossRefGoogle Scholar
  81. Wei, A., Jegla,, T., and Salkoff, L., 1996, Eight K+ families revealed by the C. elegans project, Neuropharmacol. 35:805–829.CrossRefGoogle Scholar
  82. Yang, P. K., Lee, C. Y., and Hwang, M. J., 1997, Shaker pore structure as predicted by annealed atomic simulation using symmetry and novel geometric restraints, Biophys. J. 72:2479–2489.PubMedCrossRefGoogle Scholar
  83. Yool, A., and Schwartz, T. L., 1991, Alteration of ionic selectivity of a K+ channel by mutation of the H5 region. Nature 349:700–704.PubMedCrossRefGoogle Scholar
  84. Zerrouk, H., Mansuelle, P., Benslimane, A., Rochat, H., and Martin-Eauclaire, M. F., 1993, Characterization of a new leiurotoxin I-like scorpion toxin P05 from Androctonus mauretanicus mauretanicus, FEBS Lett. 320:389–392.Google Scholar
  85. Zerrouk, H., Laraba-Djebari, F., Fremont, V., Meki, A., Darbon, H., Mansuelle, P., Oughuideni, R., Van Rietschoten, J., Rochat, H, and Martin-Eauclaire, M. F., 1996, Characterization of POl, a new peptide ligand of the apamin-sensitive Ca2+-activated K+ channel, Int. J. Pept. Protein Res. 48:514–521.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Eric Blanc
    • 1
  • Hervé Darbon
    • 1
  1. 1.Architecture et Fonction des Macromolécules BiologiquesMarseille Cedex 20France

Personalised recommendations