Advertisement

Perspectives in Drug Discovery and Design

, Volume 15, Issue 0, pp 15–40 | Cite as

Structure and function of scorpion toxins affecting K+-channels

  • Lourival D. Possani
  • Barbara Selisko
  • Georgina B. Gurrola
Article

Abstract

This chapter reviews current literature dealing with peptides isolated from the venom of scorpions. Only peptides that recognize K+-channels are reported. They are called K+-channel-ligands or simply peptides, because the actual toxicity effects of all these peptides has not been demonstrated. The primary structures of 35 peptides are reviewed, and a general nomenclature has been proposed to define 9 distinct sub-families of related sequences. Partial sequences were not included in this classification. They are 29 to 39 amino acid residues long peptides with a common structural motif composed of an α-helix segment and three anti-parallel β-sheet strands stabilized by three or four disulfide bridges. Binding and/or electrophysiological experiments showed that the affinity of these peptides for the various sub-types of K+-channels varies from micromolar to picomolar concentrations. Some data on the three-dimensional structures and on specific functions of the various peptides on voltage-dependent K+-channels, high-conductance and small-conductance, Ca2+-dependent K+-channels are also briefly reviewed.

binding K+-channels nomenclature peptide scorpion toxins three-dimensional structure venom 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Possani, L.D., In Tu, A.T. (Ed.) Handbook of Natural Toxins, vol. 2, Marcel Dekker, New York, NY, 1984, pp. 513–550.Google Scholar
  2. 2.
    Catterall, W.A., J. Gen. Physiol., 74 (1979) 357.Google Scholar
  3. 3.
    Possani, L.D., Martin, B.M. and Svendsen, I., Carlsberg Res. Commun., 47 (1982) 285.Google Scholar
  4. 4.
    Valdivia, H.H., Kirby, M.S., Lederer, J.W. and Coronado, R., Proc. Natl. Acad. Sci. USA, 89 (1992) 12185.Google Scholar
  5. 5.
    Debin, J.A., Maggio, J.E. and Strichartz, G.R., Am. J. Physiol. (Cell Physiol. 33), 264 (1993) 361.Google Scholar
  6. 6.
    Sands, S.B., Lewis, R.S. and Cahalan, M.D., J. Gen. Physiol., 93 (1989) 1016.Google Scholar
  7. 7.
    Miranda, F., Kopeyan, C., Rochat, C. and Lissitzky, S., Eur. J. Biochem., 16 (1970) 514.Google Scholar
  8. 8.
    Catterall, W.A., Annu. Rev. Biochem., 64 (1995) 493.Google Scholar
  9. 9.
    Yatani, A., Kirsh, G.E., Possani, L.D. and Brown, A.M., Am. J. Physiol. (Heart Circ. Physiol. 23), 254 (1988) H443.Google Scholar
  10. 10.
    Kirsh, G.E., Skattebol, A., Possani, L.D. and Brown, A., J. Gen. Physiol., 93 (1989) 67.Google Scholar
  11. 11.
    Jover, E., Couraud, F. and Rochat, H., Biochem. Biophys. Res. Commun., 95 (1980) 1607.Google Scholar
  12. 12.
    Zlotkin, E., Kadouri, D., Gordon, D., Pelhate, M., Martin, M.F. and Rochat, H., Arch. Biochem. Biophys., 240 (1995) 877.Google Scholar
  13. 13.
    Zlotkin, E., Gurevitz, M., Fowler, E. and Admans, M.E., Arch. Insect Biochem. Physiol., 22 (1993) 55.Google Scholar
  14. 14.
    Lebreton, F., Delepierre, M., Ramirez, A.N., Balderas, C. and Possani, L.D., Biochemistry, 33 (1994) 11135.Google Scholar
  15. 15.
    Selisko, B., Garcia, C., Becerril, B., Delepierre, M. and Possani, L.D., Eur. J. Biochem., 242 (1996) 235.Google Scholar
  16. 16.
    Garcia, C., Becerril, B., Selisko, B., Delepierre, M. and Possani, L.D., Comp. Biochem. Physiol., 116B (1997) 315.Google Scholar
  17. 17.
    Zamudio, F.Z., Conde, R., Arévalo, C., Becerril, B., Martin, B.M., Valdivia, H.H. and Possani, L.D., J. Biol. Chem., 272 (1997) 11886.Google Scholar
  18. 18.
    Zamudio, F.Z., Gurrola, G.B., Arévalo, C., Sreekumar, R., Walker, J.W., Valdivia, H.H. and Possani, L.D., FEBS Lett., 405 (1997) 385.Google Scholar
  19. 19.
    Carbone, E., Wanke., E., Prestipino, G., Possani, L.D. and Maelicke, A., Nature (Lond.), 296 (1982) 90.Google Scholar
  20. 20.
    Miller, C., Moczydlowski, E., Latorre, R. and Phillips, M., Nature (London), 313 (1985) 316.Google Scholar
  21. 21.
    Galvez, A., Gimenez-Gallego, G., Reuben, J.P., Roy-Contancin, L., Feigenbaum, P., Kaczorowski, G.J. and Garcia, M.L., J. Biol. Chem., 265 (1990) 11083.Google Scholar
  22. 22.
    Garcia-Calvo, M., Leonard, R.J., Novick, J., Stevens, S.P., Schmalhofer, W., Kaczorowski, G.J. and Garcia, M.L., J. Biol. Chem., 268 (1993) 18866.Google Scholar
  23. 23.
    Crest, M., Jacquet, G., Zerrouk, H., Benslimane, A., Rochat, H., Mansuelle, P. and Martin-Eauclaire, M., J. Biol. Chem., 267 (1992) 1670.Google Scholar
  24. 24.
    Sabatier, J.-M., Zerrouk, H., Darbon, H., Mabrouk, K., Benslimane, A., Rochat, H., Martin-Eauclaire, M.-F. and Van Rietschoten, J., Biochemistry, 32 (1993) 2763.Google Scholar
  25. 25.
    Auguste, P., Hugues, M., Gravé, B., Gesquière, J.-C., Maes, P., Tartar, A., Romey, G., Schweitz, H. and Lazdunski, M., J. Biol. Chem., 265 (1990) 4753.Google Scholar
  26. 26.
    García, M.L., García-Calvo, M., Hidalgo, P., Lee, A. and MacKinnon, R., Biochemistry, 33 (1994) 6834.Google Scholar
  27. 27.
    Miller, C., Neuron, 15 (1995) 5.Google Scholar
  28. 28.
    Gimenez-Gallego, G., Navia, M.A., Reuben, J.P., Katz, G.M., Kaczorowski, G.J. and Garcia, M.L., Proc. Natl. Acad. Sci. USA, 85 (1988) 3329.Google Scholar
  29. 29.
    Olamendi-Portugal, T., Gómez-Lagunas, F., Gurrola, G.B. and Possani, L.D., Biochem. J., 315 (1996) 977.Google Scholar
  30. 30.
    Romi-Lebrun, R., Martin-Eauclaire, M.-F., Escoubas, P., Wu, F.Q., Lebrun, B., Hisada, M. and Nakajima, T., Eur. J. Biochem., 245 (1997) 457.Google Scholar
  31. 31.
    Nieto, A., Gurrola, G., Vaca, L. and Possani, L.D., Toxicon, 34 (1996) 913.Google Scholar
  32. 32.
    Gurrola, G.B., Molinar-Rode, R., Sitges, M., Bayon, A. and Possani, L.D., J. Neural. Transm., 77 (1989) 11.Google Scholar
  33. 33.
    Olamendi-Portugal, T., Gomez-Lagunas, F., Gurrola, G.B. and Possani, L.D., Toxicon, 36 (1998) 759.Google Scholar
  34. 34.
    Gómez-Lagunas, F., Olamendi-Portugal, T., Zamudio, F.Z. and Possani, L.D., J. Membr. Biol., 152 (1996) 49.Google Scholar
  35. 35.
    Selisko, B., García, C., Becerril, B., Gómez-Lagunas, F., Garay, C. and Possani, L.D., Eur. J. Biochem., 254 (1998) 468.Google Scholar
  36. 36.
    Lucchesi, K., Ravindran, A., Young, H. and Moczydlowski, E., J. Membr. Biol., 109 (1989) 269.Google Scholar
  37. 37.
    Novick, J., Leonard, R.J., King, V.F., Schmalhofer, W., Kaczorowski, G.J. and Garcia, M.L., Biophys. J., 59 (1991) 78a.Google Scholar
  38. 38.
    Romi-Lebrun, R., Lebrun, B., Martin-Eauclaire, M.-F., Ishiguro, M., Escoubas, P., Wu, F.Q., Hisada, M., Pongs, O. and Nakajima, T., Biochemistry, 36 (1997) 13473.Google Scholar
  39. 39.
    Martin, B.M., Ramirez, A.N., Gurrola, G.B., Nobile, M., Prestipino, G. and Possani, L.D., Biochem. J., 304 (1994) 51.Google Scholar
  40. 40.
    Laraba-Djebari, F., Legros, C., Crest, M., Céard, B., Romi, R., Mansuelle, P., Jacquet, G., van Rietschoten, J., Gola, M., Rochat, H., Bougis, P.E. and Martin-Eauclaire, M.-F., J. Biol. Chem., 269 (1994) 32835.Google Scholar
  41. 41.
    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., Biochemistry, 36 (1997) 1223.Google Scholar
  42. 42.
    Rogowski, R.S., Krueger, B.K., Collins, J.H. and Blaustein, M.P., Proc. Natl. Acad. Sci. USA, 91 (1994) 1475.Google Scholar
  43. 43.
    Legros, C., Oughuideni, R., Darbon, H., Rochat, H., Bougis, P.E. and Martin-Eauclaire, M.F., FEBS Lett., 390 (1996) 81.Google Scholar
  44. 44.
    Chicchi, G.G., Gimenez-Gallego, G., Ber, E., Garcia, M.L., Winquist, R. and Cascieri, M.A., J. Biol. Chem., 263 (1988) 10192.Google Scholar
  45. 45.
    Kharrat, R., Mabrouk, K., Crest, M., Darbon, H., Oughideni, R., Martin-Eauclaire, M.F., Jacquet, G., el Ayeb, M., Van Rietschoten, J., Rochat, H. and Sabatier, J.M., Eur. J. Biochem., 242 (1996) 491.Google Scholar
  46. 46.
    Lebrun, B., Romi-Lebrun, R., Martin-Eauclaire, M.-F., Yasuda, A., Ishiguro, M., Oyama, Y., Pongs, O. and Nakajima, T., Biochem. J., 328 (1997) 321.Google Scholar
  47. 47.
    Zerrouk, H., Laraba-Djebari, F., Fremont, V., Meki, A., Darbon, H., Mansuelle, P., Oughideni, R., van Rietschoten, J., Rochat, H. and Martin-Eauclaire, M.F., Int. J. Pept. Protein Res., 48 (1996) 514.Google Scholar
  48. 48.
    Zerrouk, H., Mansuelle, P., Benslimane, A., Rochat, H. and Martin-Eauclaire, M.F., FEBS Lett., 320 (1993) 189.Google Scholar
  49. 49.
    Martins, J.C., Zhang, W., Tartar, A., Lazdunski, M. and Borremans, F.A.M., FEBS Lett., 260 (1990) 249.Google Scholar
  50. 50.
    Johnson, B.A. and Sugg, E.E., Biochemistry, 31 (1992) 8151.Google Scholar
  51. 51.
    Bontems, F., Roumestand C., Gilquin, B., Ménez, A. and Toma, F., Science, 254 (1991) 1521.Google Scholar
  52. 52.
    Meunier, S., Bernassau, J.-M., Sabatier, J.-M., Martin-Eauclaire, M.F., Van Rietschoten J., Cambillau, C. and Darbon, H., Biochemistry, 32 (1993) 11969.Google Scholar
  53. 53.
    Dauplais, M., Gilquin, B., Possani, L.D., Gurrola-Briones, G., Roumestand, C. and Menez, A., Biochemistry, 34 (1995) 16563.Google Scholar
  54. 54.
    Krezel, A.M., Kasibhatla, C., Hidalgo, P., MacKinnon, R. and Wagner, G., Protein Sci., 4 (1995) 1478.Google Scholar
  55. 55.
    Aiyar, J., Withka, J.M., Rizzi, J.P., Singleton, D.H., Andrews, G.C., Lin, W., Boyd, J., Hanson, D.C., Simon, M., Dethlefs, B., Lee, C., Hall, J.E., Gutman, G.A. and Chandy, K.G., Neuron, 15 (1995) 1169.Google Scholar
  56. 56.
    Delepierre, M., Prochnicka-Chalufour, A. and Possani, L.D., Biochemistry, 36 (1997) 2649.Google Scholar
  57. 57.
    Tenenholz, T.C., Rogowski, R.S., Collins, J.H., Blaustein, M.P. and Weber, D.J., Biochemistry, 36 (1997) 2763.Google Scholar
  58. 58.
    Blanc, E., Fremont, V., Sizun, P., Meunier, S., Van Rietschoten, J., Thevand, A., Bernassau, J.-M. and Darbon, H., Proteins, 24 (1996) 359.Google Scholar
  59. 59.
    Blanc, E., Sabatier, J.M., Kharrat, R., Meunier, S., el Ayeb, M., Van Rietschoten, J. and Darbon, H., Proteins, 29 (1997) 321.Google Scholar
  60. 60.
    Blanc, E., Lecomte, C., Van Rietschoten, J., Sabatier, J.M. and Darbon, H., Proteins, 29 (1997) 359.Google Scholar
  61. 61.
    Bruix, M., Jimenez, M.A., Santoro, J., Gonzalez, C., Colilla, F.J., Mendez, E. and Rico, M., Biochemistry, 32 (1993) 715.Google Scholar
  62. 62.
    Sitges, M., Possani, L.D. and Bayon, A., J. Neurosci., 6 (1986) 1570.Google Scholar
  63. 63.
    Harvey, A.L., Marshall, D.L. and Possani. L.D., Toxicon., 11 (1992) 1497.Google Scholar
  64. 64.
    Robbitaille, Garcia, M.L., Kaczorowski, G.J. and Charlton, M.P., Neuron, 11 (1993) 645.Google Scholar
  65. 65.
    Vazquez, J., Feigenbaum, P., King, V.F., Kaczorowski, G. and Garcia, M.L., J. Biol. Chem., 265 (1990) 15564.Google Scholar
  66. 66.
    Knaus, H.G., Koch, R.O.A., Eberhardt, A., Kaczorowski, G., Garcia, M.L. and Slaughter, R.S., Biochemistry, 34 (1995) 13627.Google Scholar
  67. 67.
    Valdivia, H.H., Martin, B.M., Escobar, L. and Possani, L.D., Biochem. Intl., 27 (1992) 953.Google Scholar
  68. 68.
    Romi, R., Crest, M., Gola, M., Sampieri, F., Jacquet, G., Zerrouk, H. and Mansuelle, P., J. Biol. Chem., 268 (1993) 26302.Google Scholar
  69. 69.
    DeLean, A., Munson, P.J. and Rodbard, D., Am. J. Physiol., 235 (1978) E97.Google Scholar
  70. 70.
    Cheng, Y.-C. and Prusoff, W.H., Biochem. Pharmacol., 22 (1973) 3099.Google Scholar
  71. 71.
    Péter, M. Jr., Varga, Z., Panyi, G., Bene, L., Damjanovich, S., Pieri, C., Possani, L.D. and Gáspár, R. Jr., Biochem. Biophys. Res. Commun., 242 (1998) 621.Google Scholar
  72. 72.
    Veh, R.W., Lichtinghagen, R., Sewing, S., Wunder, F., Grumbach, I.G. and Pongs, O., Eur. J. Neurosci., 7 (1995) 2189.Google Scholar
  73. 73.
    Auguste, P., Hugues, M., Mourre, C., Moinier, D., Tartar, A. and Lazdunski, M., Biochemistry, 31 (1992) 648.Google Scholar
  74. 74.
    Sabatier, J.M., Fremond, V., Mabrouk, K., Crest, M., Darbon, H., Rochat, H., van Rietschoten, J. and Martin-Eauclaire, M.-F., Int. J. Pept. Protein Res., 43 (1994) 486.Google Scholar
  75. 75.
    Sabatier, J.M., Lecomte, C., Mabroux, K., Darbon, H., Oughideni, R., Canarelli, S., Rochat, H., Martin-Eauclaire, M.F. and van Rietschoten, J.V., Biochemistry, 35 (1996) 10651.Google Scholar
  76. 76.
    Köhler, M., Hirschberg, B., Bond, C.T., Kinzie, J.M., Marrion, N.V., Maylie, J. and Adelman, J.P., Science, 273 (1996) 1709.Google Scholar
  77. 77.
    Inisan, A.G., Meunier, S., Fedelli, O., Altbach, M., Fremont, V., Sabatier, J.M., Thévan, A., Bernassau, J.M., Cambillau, C. and Darbon, H., Int. J. Pept. Protein Res., 45 (1995) 441.Google Scholar
  78. 78.
    García-Calvo, M., Vazquez, J., Smith, M., Kaczorowski, G.J. and García, M.L., Biochemistry, 30 (1991) 11157.Google Scholar
  79. 79.
    García-Calvo, M., Knaus, H.G., McManus, O.B., Giangiacomo, K.M., Kaczorowski, G.J. and García, M.L., J. Biol. Chem., 269 (1994) 676.Google Scholar
  80. 80.
    Giangiacomo, K.M., Sugg, E.E., Garcia-Calvo, M., Leonard, R.J., McManus, O.B., Kaczorowski, G.J. and Garcia, M.L., Biochemistry, 32 (1993) 2363.Google Scholar
  81. 81.
    Koschak, A., Koch, R.O., Liu, J., Kaczorowski, G.J., Reinhart, P.H., Garcia, M.L. and Knaus, H., Biochemistry, 36 (1997) 1943.Google Scholar
  82. 82.
    Carbone, E., Prestipino, G., Spadavecchia, L., Franciolini, F. and Possani, L.D., Pfluegers Arch. (Eur. J. Physiol.), 408 (1987) 423.Google Scholar
  83. 83.
    Deutsch, C., Price, M., Lee, S., King, V.F. and Garcia, M.L., J. Biol. Chem., 266 (1993) 3668.Google Scholar
  84. 84.
    Leonard, R.J., Garcia, M.L., Slaughter, R.S. and Reuben, J.P., Proc. Natl. Acad. Sci. USA, 89 (1992) 10094.Google Scholar
  85. 85.
    Pisciotta, M., Coronas, F.I., Possani, L.D. and Prestipino, G., Eur. Biophys. J., 27 (1998) 69.Google Scholar
  86. 86.
    Gómez-Lagunas, F., Olamendi-Portugal, T. and Possani, L.D., FEBS Lett., 400 (1997) 197.Google Scholar
  87. 87.
    Pisciotta, M., Otalia, M., Possani, L.D. and Prestipino, G., Biochem. Biophys. Res. Commun., 242 (1998) 287.Google Scholar
  88. 88.
    Goldstein, S.A.N. and Miller, C., Biophys. J., 65 (1993) 1613.Google Scholar
  89. 89.
    MacKinnon, R. and Miller, C., Science, 245 (1989) 1382.Google Scholar
  90. 90.
    MacKinnon, R., Heginbotham, L. and Abramson, T., Neuron, 5 (1990) 767.Google Scholar
  91. 91.
    MacKinnon, R., Nature, 350 (1991) 232.Google Scholar
  92. 92.
    MacKinnon, R., Aldrich, R.W. and Lee, A.W., Science, 262 (1993) 757.Google Scholar
  93. 93.
    Stampe, P., Kolmakova-Partensky, L. and Miller, C., Biochemistry, 33 (1994) 443.Google Scholar
  94. 94.
    Stocker, M. and Miller, C., Proc. Natl. Acad. Sci. USA, 91 (1994) 9509.Google Scholar
  95. 95.
    Goldstein, S.A.N., Pheasant, D.J. and Miller, C., Neuron, 12 (1994) 1377.Google Scholar
  96. 96.
    Hidalgo, P. and MacKinnon, R., Science, 268 (1995) 307.Google Scholar
  97. 97.
    Aiyar, J., Rizzi, J.P., Gutman, G.A. and Chandy, K.G., J. Biol. Chem., 271 (1996) 31013.Google Scholar
  98. 98.
    Ranganathan, R., Lewis, J.H. and McKinnon, R., Neuron, 16 (1996) 131.Google Scholar
  99. 99.
    Gross, A. and MacKinnon, R., Neuron, 16 (1996) 399.Google Scholar
  100. 100.
    Park, C.S. and Miller, C., Neuron, 9 (1992) 307.Google Scholar
  101. 101.
    Park, C.S. and Miller, C., Biochemistry, 33 (1992) 443.Google Scholar
  102. 102.
    Naranjo, D. and Miller, C., Neuron, 16 (1996) 123.Google Scholar
  103. 103.
    Papazian, D.M., Schwarz, T.L., Tempel, B.L., Jan, Y.N. and Jan, L.Y., Science, 237 (1987) 749.Google Scholar
  104. 104.
    Pongs, O., Kecskemethy, N., Müller, R., Krah-Jentgens, I., Baumann, A., Kiltz, H.H., Canal, I., Llamazares, S. and Ferrus, A., EMBO J., 7 (1988) 1087.Google Scholar
  105. 105.
    Stühmer, W., Ruppersberg, J.P., Schröter, Sakmann B., Stocker M., Giese, K.P., Perschke, A., Baumann, A. and Pongs, O., EMBO J., 8 (1989) 3235.Google Scholar
  106. 106.
    Butler, A., Tsunoda, S., McCobb, D.P., Wei, A. and Salkoff, L., Science, 261 (1993) 221.Google Scholar
  107. 107.
    Naini, A.A. and Miller, C., Biochemistry, 35 (1996) 6181.Google Scholar
  108. 108.
    Martínez, F., Becerril, B., Gurrola, G.B., Martin, B.M. and Possani, L.D., Toxicon, 34 (1996) 1413.Google Scholar
  109. 109.
    Goldstein, S.A.N. and Miller, C., Biophys. J., 62 (1992) 5.Google Scholar
  110. 110.
    Werkman, T.R., Kawamura, S., Yokoyama, H., Higashida, H. and Rogawski, M.A., Neuroscience, 50 (1992) 935.Google Scholar
  111. 111.
    Rogowski, R.S., Collins, J.H., O'Neil, T.J., Gustafson, T.A., Werkman, T.A., Rogawski, M.A., Tenenholz, T.C., Weber, D.J. and Blaustein, M.P., Mol. Pharmacol., 50 (1996) 1167.Google Scholar
  112. 112.
    Giangiacomo, K.M., Garcia, M.L. and McManus, O.B., Biochemistry, 31 (1992) 6719.Google Scholar
  113. 113.
    Knaus, H.-G., Folander, K., Garcia-Calvo, M., Garcia, M.L., Kaczorowski, G.L., Smith, M. and Swanson, R., J. Biol. Chem., 269 (1994) 17274.Google Scholar
  114. 114.
    Wei, A., Solaro, C., Lingle, C. and Salkoff, L., Neuron, 13 (1994) 671.Google Scholar
  115. 115.
    Scott, V.E.S., Rettig, J., Parcej, D.N., Keen, J.N., Findlay, J.B.C., Pongs, O. and Dolly, J.O., Proc. Natl. Acad. Sci. USA, 91 (1994) 1637.Google Scholar
  116. 116.
    Isom, L.L., De Jongh, K.S. and Catterall, W.A., Neuron, 12 (1994) 1183.Google Scholar
  117. 117.
    Rettig, J., Heinemann, S.H., Wunder, F., Lorra, C., Parcej, D.N., Dolly, J.O. and Pongs, O., Nature, 369 (1994) 289.Google Scholar
  118. 118.
    Heinemann, S.H., Rettig, J., Wunder, F. and Pongs, O., FEBS Lett., 377 (1995) 383.Google Scholar
  119. 119.
    Munujos, P., Knaus, H.-G., Kaczorowski, G.J. and Garcia, M.L., Biochemistry, 34 (1995) 10771.Google Scholar
  120. 120.
    Hanner, M., Schmalhofer, W.A., Munujos, P., Knaus, H.-G., Kaczorowski, G.J. and Garcia, M.L., Proc. Natl. Acad. Sci. USA, 94 (1997) 2853.Google Scholar
  121. 121.
    Valdivia, H.H., Smith, J.S., Martin, B.M., Coronado, R. and Possani, L.D., FEBS Lett., 226 (1988) 280.Google Scholar
  122. 122.
    Vaca, L., Gurrola, G.B., Possani, L.D. and Kunze, D.L., J.Membrane Biol., 134 (1993) 123.Google Scholar
  123. 123.
    Grishin, E.V., Korolkova, Y.V., Kozlov, S.A., Lipkin, A.V., Nosyreva, E.D., Pluzhnikov, K.A., Sukhanov, S.V. and Volkova, T.M., Pure Appl. Chem., 68 (1996) 2105.Google Scholar
  124. 124.
    Vita, C., Roumestand, C., Toma, F. and Menez, A., Proc. Natl. Acad. Sci. USA, 92 (1995) 6404.Google Scholar
  125. 125.
    Drakopoulou, E., Zinn-Justin, S., Guenneugues, M., Gilquin, B., Ménez, A. and Vita, C., J. Biol. Chem., 271 (1996) 11979.Google Scholar
  126. 126.
    Zinn-Justin, S., Guenneugues, M., Drakopoulou, E., Gilquin, B., Vita, C. and Ménez, A., Biochemistry, 35 (1996) 8535.Google Scholar
  127. 127.
    Chandy, K.G., Proc. 12th World Congress on Animal, Plant and Microbial Toxins, Cuernavaca, Sept. 1997, Abstract S-24Th.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Lourival D. Possani
    • 1
  • Barbara Selisko
    • 1
  • Georgina B. Gurrola
    • 1
  1. 1.Department of Molecular Recognition and Structural BiologyBiotechnology Institute – National Autonomous University of MexicoCuernavaca MORMexico

Personalised recommendations