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Natural α-conotoxins and their synthetic analogues in study of nicotinic acetylcholine receptors

Russian Journal of Bioorganic Chemistry volume 32, pages 103–115 (2006)Cite this article

Abstract

α-Conotoxins, peptide neurotoxins from poisonous marine snails of the genus Conus that highly specifically block nicotinic acetylcholine receptors (AChRs) of various types, are reviewed. Preliminarily, the structural organization of AChRs of the muscular and neuronal types, their involvement in physiological processes, and their role in various diseases are briefly discussed. In this connection, the necessity of quantitative determination of AChR subtypes using neurotoxins and other approaches is substantiated. The chemical structure, spatial organization, and specificity of α-conotoxins are mainly discussed, taking into consideration the recent results on the ability of α-conotoxins to interact with muscular or neuronal hetero-and homooligomeric AChRs exhibiting a high species specificity. Particular emphasis is placed upon a thorough characterization of the surfaces of interaction of α-conotoxins with AChRs using synthetic analogues of α-conotoxins, mutations in AChRs, and pairwise mutations in both α-conotoxins and AChRs. The discovery in 2001 of the acetylcholine-binding protein from the pond snail Lymnaea stagnalis and the determination of its crystalline structure led to rapid progress in understanding the structural organization of ligand-binding domains of AChRs with which α-conotoxins also interact. We discuss the interaction of various α-conotoxins with acetylcholine-binding proteins, the recently reported X-ray structure of the complex of the acetylcholine-binding protein from Aplysia californica with the α-conotoxin analogue PnIA, and the application of this structure to the modeling of complexes of α-conotoxins with various AChRs.

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Abbreviations

AChR:

nicotinic acetylcholine receptor

ACHBP:

acetylcholine-binding protein; amino acid residues are given in the one-letter code.

References

  1. Karlin, A., Nat. Rev. Neurosci., 2002, vol. 3, pp. 102–114.

    Article  PubMed  CAS  Google Scholar 

  2. Lindstrom, J, in Handbook of Experimental Pharmacology, vol. 44, Clementi, F., Fornassi, D., and Gotti, C., Eds., Berlin: Springer, 2000, pp. 101–162.

    Google Scholar 

  3. Le Novere, N., Corringer, P.J., and Changeux, J.P., J. Neurobiol., 2002, vol. 53, pp. 447–456.

    PubMed  Google Scholar 

  4. Conti-Fine, B.M., Navaneetham, D., Lei, S., and Maus, A.D., Eur. J. Pharmacol., 2000, vol. 393, pp. 279–294.

    Article  PubMed  CAS  Google Scholar 

  5. Sciamanna, M.A., Griesmann, G.E., Williams, C.L., and Lennon, V.A., J. Neurochem., 1997, vol. 69, pp. 2302–2311.

    PubMed  CAS  Google Scholar 

  6. Kumar, P. and Meizel, S., J. Biol. Chem., 2005, vol. 280, pp. 25 928–25 935.

    CAS  Google Scholar 

  7. Vincent, A., Beeson, D., and Lang, B., Eur. J. Biochem., 2000, vol. 267, pp. 6717–6728.

    Article  PubMed  CAS  Google Scholar 

  8. Steinlein, O.K., Prog. Brain Res., 2004, vol. 145, pp. 275–285.

    PubMed  CAS  Google Scholar 

  9. O’Neill, M.J., Murray, T.K., Lakics, V., Visanji, N.P., and Duty, S., Curr. Drug Targets CNS Neurol. Disord., 2002, vol. 1, pp. 399–411.

    PubMed  CAS  Google Scholar 

  10. Tsetlin, V., Eur. J. Biochem., 1999, vol. 264, pp. 281–286.

    Article  PubMed  CAS  Google Scholar 

  11. Tsetlin, V.I. and Hucho, F., FEBS Lett., 2004, vol. 557, pp. 9–13.

    Article  PubMed  CAS  Google Scholar 

  12. Terlau, H. and Olivera, B.M., Physiol. Rev., 2004, vol. 84, pp. 41–68.

    Article  PubMed  CAS  Google Scholar 

  13. Armishaw, C.J. and Alewood, P.F., Curr. Protein Pept. Sci., 2005, vol. 6, pp. 221–240.

    Article  PubMed  CAS  Google Scholar 

  14. McIntosh, J.M., Santos, A.D., and Olivera, B.M., Annu. Rev. Biochem., 1999, vol. 68, pp. 59–88.

    Article  PubMed  CAS  Google Scholar 

  15. Arias, H.R. and Blanton, M.P., Int. J. Biochem. Cell Biol., 2000, vol. 32, pp. 1017–1028.

    Article  PubMed  CAS  Google Scholar 

  16. Dutton, J.L. and Craik, D.J., Curr. Med. Chem., 2000, vol. 8, pp. 327–344.

    Google Scholar 

  17. Janes, R.W., Curr. Opin. Pharmacol., 2005, vol. 5, pp. 280–292.

    PubMed  CAS  Google Scholar 

  18. Celie, P.H., Kasheverov, I.E., Mordvintsev, D.Y., Hogg, R.C., van Nierop, P., van Elk, R., van Rossum-Fikkert, S.E., Zhmak, M.N., Bertrand, D., Tsetlin, V., Sixma, T.K., and Smit, A.B., Nat. Struct. Mol. Biol., 2005, vol. 12, pp. 582–588.

    Article  PubMed  CAS  Google Scholar 

  19. Gray, W.R., Luque, A., Olivera, B.M., Barrett, J., and Cruz, L.J., J. Biol. Chem., 1981, vol. 256, pp. 4734–4740.

    PubMed  CAS  Google Scholar 

  20. Kobayashi, Y., Ohkubo, T., Kyogoku, Y., Nishiuchi, Y., Sakakibara, S., Braun, W., and Go, N., Biochemistry, 1989, vol. 28, pp. 4853–4860.

    Article  PubMed  CAS  Google Scholar 

  21. Pardi, A., Galdes, A., Florance, J., and Maniconte, D., Biochemistry, 1989, vol. 28, pp. 5494–5501.

    Article  PubMed  CAS  Google Scholar 

  22. Maslennikov, I.V., Sobol, A.G., Gladky, K.V., Lugovskoy, A.A., Ostrovsky, A.G., Tsetlin, V.I., Ivanov, V.T., and Arseniev, A.S., Eur. J. Biochem., 1998, vol. 254, pp. 238–247.

    Article  PubMed  CAS  Google Scholar 

  23. Guddat, L.W., Martin, J.A., Shan, L., Edmundson, A.B., and Gray, W.R., Biochemistry, 1996, vol. 35, pp. 11 329–11 335.

    Article  CAS  Google Scholar 

  24. McManus, O.B. and Musick, J.R., J. Neurosci., 1985, vol. 5, pp. 110–116.

    PubMed  CAS  Google Scholar 

  25. Marshall, I.G. and Harvey, A.L., Toxicon, 1990, vol. 28, pp. 231–234.

    Article  PubMed  CAS  Google Scholar 

  26. Blount, K., Johnson, A., Prior, C., and Marshall, I.G., Toxicon, 1992, vol. 30, pp. 835–842.

    Article  PubMed  CAS  Google Scholar 

  27. Utkin, Y.N., Kobayashi, Y., Hucho, F., and Tsetlin, V.I., Toxicon, 1994, vol. 32, pp. 1153–1157.

    Article  PubMed  CAS  Google Scholar 

  28. Hann, R.M., Pagan, O.R., and Eterovic, V.A., Biochemistry, 1994, vol. 33, pp. 14 058–14 063.

    Article  CAS  Google Scholar 

  29. Groebe, D.R., Dumm, J.M., Levitan, E.S., and Abramson, S.N., Mol. Pharmacol., 1995, vol. 48, pp. 105–111.

    PubMed  CAS  Google Scholar 

  30. Groebe, D.R., Gray, W.R., and Abramson, S.N., Biochemistry, 1997, vol. 36, pp. 6469–6474.

    Article  PubMed  CAS  Google Scholar 

  31. Luetje, C.W., Wada, K., Rogers, S., Abramson, S.N., Tsuji, K., Heinemann, S., and Patrick, J., J. Neurochem., 1990, vol. 55, pp. 632–640.

    PubMed  CAS  Google Scholar 

  32. McIntosh, J.M., Cruz, L.J., Hunkapiller, M.W., Gray, W.R., and Olivera, B.M., Arch. Biochem. Biophys., 1982, vol. 218, pp. 329–334.

    Article  PubMed  CAS  Google Scholar 

  33. Gray, W.R., Rivier, J.E., Galyean, R., Cruz, L.J., and Olivera, B.M., J. Biol. Chem., 1983, vol. 258, pp. 12 247–12 251.

    CAS  Google Scholar 

  34. Gouda, H., Yamazaki, K., Hasegawa, J., Kobayashi, Y., Nishiuchi, Y., Sakakibara, S., and Hirono, S., Biochim. Biophys. Acta, 1997, vol. 1343, pp. 327–334.

    PubMed  CAS  Google Scholar 

  35. Gouda, H., Yamazaki, K., Hasegawa, J., and Hirono, S., Chem. Pharm. Bull., (Tokyo), 2001, vol. 49, pp. 249–252.

    Article  PubMed  CAS  Google Scholar 

  36. Sine, S.M., Kreienkamp, H.J., Bren, N., Maeda, R., and Taylor, P., Neuron, 1995, vol. 15, pp. 205–211.

    Article  PubMed  CAS  Google Scholar 

  37. Sugiyama, N., Marchot, P., Kawanishi, C., Osaka, H., Molles, B., Sine, S.M., and Taylor, P., Mol. Pharmacol., 1998, vol. 53, pp. 787–794.

    PubMed  CAS  Google Scholar 

  38. Chiara, D.C., Xie, Y., and Cohen, J.B., Biochemistry, 1999, vol. 38, pp. 6689–6698.

    Article  PubMed  CAS  Google Scholar 

  39. Cortez, L.M., del Canto, S.G., Testai, F.D., and Biscoglio De Jimenez Bonino, M.J., Biochem. Biophys. Res. Commun., 2002, vol. 295, pp. 791–795.

    Article  PubMed  CAS  Google Scholar 

  40. Zafaralla, G.C., Ramilo, C., Gray, W.R., Karlstrom, R., Olivera, B.M., and Cruz, L.J., Biochemistry, 1988, vol. 27, pp. 7102–7105.

    Article  PubMed  CAS  Google Scholar 

  41. Benie, A.J., Whitford, D., Hargittai, B., Barany, G., and Janes, R.W., FEBS Lett., 2000, vol. 476, pp. 287–295.

    Article  PubMed  CAS  Google Scholar 

  42. Myers, R.A., Zafaralla, G.C., Gray, W.R., Abbott, J., Cruz, L.J., and Olivera, B.M., Biochemistry, 1991, vol. 30, pp. 9370–9377.

    PubMed  CAS  Google Scholar 

  43. Ramilo, C.A., Zafaralla, G.C., Nadasdi, L., Hammerland, L.G., Yoshikami, D., Gray, W.R., Kristipati, R., Ramachandran, J., Miljanich, G., and Olivera, B.M., Biochemistry, 1992, vol. 31, pp. 9919–9926.

    Article  PubMed  CAS  Google Scholar 

  44. Martinez, J.S., Olivera, B.M., Gray, W.R., Craig, A.G., Groebe, D.R., Abramson, S.N., and McIntosh, J.M., Biochemistry, 1995, vol. 34, pp. 14 519–14 526.

    CAS  Google Scholar 

  45. Park, K.H., Suk, J.E., Jacobsen, R., Gray, W.R., McIntosh, J.M., and Han, K.H., J. Biol. Chem., 2001, vol. 276, pp. 49 028–49 033.

    CAS  Google Scholar 

  46. McIntosh, J.M., Yoshikami, D., Mahe, E., Nielsen, D.B., Rivier, J.E., Gray, W.R., and Olivera, B.M., J. Biol. Chem., 1994, vol. 269, pp. 16 733–16 739.

    CAS  Google Scholar 

  47. Maslennikov, I.V., Shenkarev, Z.O., Zhmak, M.N., Ivanov, V.T., Methfessel, C., Tsetlin, V.I., and Arseniev, A.S., FEBS Lett., 1999, vol. 444, pp. 275–280.

    Article  PubMed  CAS  Google Scholar 

  48. Rogers, J.P., Luginbuhl, P., Shen, G.S., McCabe, R.T., Stevens, R.C., and Wemmer, D.E., Biochemistry, 1999, vol. 38, pp. 3874–3882.

    Article  PubMed  CAS  Google Scholar 

  49. Gouda, H. and Hirono, S., Biochim. Biophys. Acta, 1999, vol. 1431, pp. 384–394.

    PubMed  CAS  Google Scholar 

  50. Gehrmann, J., Daly, N.L., Alewood, P.F., and Craik, D.J., J. Med. Chem., 1999, vol. 42, pp. 2364–2372.

    Article  PubMed  CAS  Google Scholar 

  51. Johnson, D.S., Martinez, J., Elgoyhen, A.B., Heinemann, S.F., and McIntosh, J.M., Mol. Pharmacol., 1995, vol. 48, pp. 194–199.

    PubMed  CAS  Google Scholar 

  52. Pereira, E.F., Alkondon, M., McIntosh, J.M., and Albuquerque, E.X., J. Pharmacol. Exp. Ther., 1996, vol. 278, pp. 1472–1483.

    PubMed  CAS  Google Scholar 

  53. Quiram, P.A. and Sine, S.M., J. Biol. Chem., 1998, vol. 273, pp. 11 001–11 006.

    CAS  Google Scholar 

  54. Kehoe, J. and McIntosh, J.M., J. Neurosci., 1998, vol. 18, pp. 8198–8213.

    PubMed  CAS  Google Scholar 

  55. Ellison, M., Gao, F., Wang, H.L., Sine, S.M., McIntosh, J.M., and Olivera, B.M., Biochemistry, 2004, vol. 43, pp. 16 019–16 026.

    Article  CAS  Google Scholar 

  56. Broxton, N.M., Down, J.G., Gehrmann, J., Alewood, P.F., Satchell, D.G., and Livett, B.G., J. Neurochem., 1999, vol. 72, pp. 1656–1662.

    Article  PubMed  CAS  Google Scholar 

  57. Fainzilber, M., Hasson, A., Oren, R., Burlingame, A.L., Gordon, D., Spira, M.E., and Zlotkin, E., Biochemistry, 1994, vol. 33, pp. 9523–9529.

    Article  PubMed  CAS  Google Scholar 

  58. Wolfender, J.L., Chu, F., Ball, H., Wolfender, F., Fainzilber, M., Baldwin, M.A., and Burlingame, A.L., J. Mass Spectrom., 1999, vol. 34, pp. 447–454.

    Article  PubMed  CAS  Google Scholar 

  59. Hogg, R.C., Miranda, L.P., Craik, D.J., Lewis, R.J., Alewood, P.F., and Adams, D.J., J. Biol. Chem., 1999, vol. 274, pp. 36 559–36 564.

    Article  CAS  Google Scholar 

  60. Hu, S.H., Gehrmann, J., Guddat, L.W., Alewood, P.F., Craik, D.J., and Martin, J.L., Structure, 1996, vol. 4, pp. 417–423.

    Article  PubMed  CAS  Google Scholar 

  61. Luo, S., Nguyen, T.A., Cartier, G.E., Olivera, B.M., Yoshikami, D., and McIntosh, J.M., Biochemistry, 1999, vol. 38, pp. 14 542–14 548.

    CAS  Google Scholar 

  62. Broxton, N., Miranda, L., Gehrmann, J., Down, J., Alewood, P., and Livett, B., Eur. J. Pharmacol., 2000, vol. 390, pp. 229–236.

    Article  PubMed  CAS  Google Scholar 

  63. Everhart, D., Reiller, E., Mirzoian, A., McIntosh, J.M., Malhotra, A., and Luetje, C.W., J. Pharmacol. Exp. Ther., 2003, vol. 306, pp. 664–670.

    Article  PubMed  CAS  Google Scholar 

  64. Hogg, R.C., Hopping, G., Alewood, P.F., Adams, D.J., and Bertrand, D., J. Biol. Chem., 2003, vol. 278, pp. 26 908–26 914.

    Article  CAS  Google Scholar 

  65. Dutertre, S., Nicke, A., and Lewis, R.J., J. Biol. Chem., 2005, vol. 280, pp. 30 460–30 468.

    Article  CAS  Google Scholar 

  66. Hu, S.H., Gehrmann, J., Alewood, P.F., Craik, D.J., and Martin, J.L., Biochemistry, 1997, vol. 36, pp. 11 323–11 330.

    CAS  Google Scholar 

  67. Cartier, G.E., Yoshikami, D., Gray, W.R., Luo, S., Olivera, B.M., and McIntosh, J.M., J. Biol. Chem., 1996, vol. 271, pp. 7522–7528.

    PubMed  CAS  Google Scholar 

  68. Shon, K.J., Koerber, S.C., Rivier, J.E., Olivera, B.M., and McIntosh, J.M., Biochemistry, 1997, vol. 36, pp. 15 693–15 700.

    CAS  Google Scholar 

  69. Hill, J.M., Oomen, C.J., Miranda, L.P., Bingham, J.P., Alewood, P.F., and Craik, D.J., Biochemistry, 1998, vol. 37, pp. 15 621–15 630.

    Article  CAS  Google Scholar 

  70. Harvey, S.C., McIntosh, J.M., Cartier, G.E., Maddox, F.N., and Luetje, C.W., Mol. Pharmacol., 1997, vol. 51, pp. 336–342.

    PubMed  CAS  Google Scholar 

  71. Kaiser, S.A., Soliakov, L., Harvey, S.C., Luetje, C.W., and Wonnacott, S., J. Neurochem., 1998, vol. 70, pp. 1069–1076.

    PubMed  CAS  Google Scholar 

  72. Fu, Y., Matta, S.G., McIntosh, J.M., and Sharp, B.M., Neurosci. Lett., 1999, vol. 266, pp. 113–116.

    Article  PubMed  CAS  Google Scholar 

  73. Vailati, S., Hanke, W., Bejan, A., Barabino, B., Longhi, R., Balestra, B., Moretti, M., Clementi, F., and Gotti, C., Mol. Pharmacol., 1999, vol. 56, pp. 11–19.

    PubMed  CAS  Google Scholar 

  74. Vailati, S., Moretti, M., Balestra, B., McIntosh, M., Clementi, F., and Gotti, C., Eur. J. Pharmacol., 2000, vol. 393, pp. 23–30.

    Article  PubMed  CAS  Google Scholar 

  75. Kuryatov, A., Olale, F., Cooper, J., Choi, C., and Lindstrom, J., Neuropharmacology, 2000, vol. 39, pp. 2570–2590.

    Article  PubMed  CAS  Google Scholar 

  76. Champtiaux, N., Han, Z.Y., Bessis, A., Rossi, F.M., Zoli, M., Marubio, L., McIntosh, J.M., and Changeux, J.P., J. Neurosci., 2002, vol. 22, pp. 1208–1217.

    PubMed  CAS  Google Scholar 

  77. Whiteaker, P., Peterson, C.G., Xu, W., McIntosh, J.M., Paylor, R., Beaudet, A.L., Collins, A.C., and Marks, M.J., J. Neurosci., 2002, vol. 22, pp. 2522–2529.

    PubMed  CAS  Google Scholar 

  78. Salminen, O., Whiteaker, P., Grady, S.R., Collins, A.C., McIntosh, J.M., and Marks, M.J., Neuropharmacology, 2005, vol. 48, pp. 696–705.

    Article  PubMed  CAS  Google Scholar 

  79. McIntosh, J.M., Gardner, S., Luo, S., Garrett, J.E., and Yoshikami, D., Eur. J. Pharmacol., 2000, vol. 393, pp. 205–208.

    Article  PubMed  CAS  Google Scholar 

  80. Loughnan, M., Bond, T., Atkins, A., Cuevas, J., Adams, D.J., Broxton, N.M., Livett, B.G., Down, J.G., Jones, A., Alewood, P.F., and Lewis, R.J., J. Biol. Chem., 1998, vol. 273, pp. 15667–15674.

    Article  PubMed  CAS  Google Scholar 

  81. Hu, S.H., Loughnan, M., Miller, R., Weeks, C.M., Blessing, R.H., Alewood, P.F., Lewis, R.J., and Martin, J.L., Biochemistry, 1998, vol. 37, pp. 11425–11433.

    PubMed  CAS  Google Scholar 

  82. Nicke, A., Samochocki, M., Loughnan, M.L., Bansal, P.S., Maelicke, A., and Lewis, R.J., FEBS Lett., 2003, vol. 554, pp. 219–223.

    Article  PubMed  CAS  Google Scholar 

  83. Luo, S., Kulak, J.M., Cartier, G.E., Jacobsen, R.B., Yoshikami, D., Olivera, B.M., and McIntosh, J.M., J. Neurosci., 1998, vol. 18, pp. 8571–8579.

    PubMed  CAS  Google Scholar 

  84. Cho, J.H., Mok, K.H., Olivera, B.M., McIntosh, J.M., Park, K.H., and Han, K.H., J. Biol. Chem., 2000, vol. 275, pp. 8680–8685.

    PubMed  CAS  Google Scholar 

  85. Dutton, J.L., Bansal, P.S., Hogg, R.C., Adams, D.J., Alewood, P.F., and Craik, D.J., J. Biol. Chem., 2002, vol. 277, pp. 48 849–48 857.

    Article  CAS  Google Scholar 

  86. McIntosh, J.M., Dowell, C., Watkins, M., Garrett, J.E., Yoshikami, D., and Olivera, B.M., J. Biol. Chem., 2002, vol. 277, pp. 33 610–33 615.

    Article  CAS  Google Scholar 

  87. Chi, S.W., Kim, D.H., Olivera, B.M., McIntosh, J.M., and Han, K.H., Biochem. J., 2004, vol. 380, pp. 347–352.

    Article  PubMed  CAS  Google Scholar 

  88. Ellison, M., McIntosh, J.M., and Olivera, B.M., J. Biol. Chem., 2003, vol. 278, pp. 757–764.

    PubMed  CAS  Google Scholar 

  89. Nicke, A., Loughnan, M.L., Millard, E.L., Alewood, P.F., Adams, D.J., Daly, N.L., Craik, D.J., and Lewis, R.J., J. Biol. Chem., 2003, vol. 278, pp. 3137–3144.

    Article  PubMed  CAS  Google Scholar 

  90. Sandall, D.W., Satkunanathan, N., Keays, D.A., Polidano, M.A., Liping, X., Pham, V., Down, J.G., Khalil, Z., Livett, B.G., and Gayler, K.R., Biochemistry, 2003, vol. 42, pp. 6904–6911.

    Article  PubMed  CAS  Google Scholar 

  91. Dowell, C., Olivera, B.M., Garrett, J.E., Staheli, S.T., Watkins, M., Kuryatov, A., Yoshikami, D., Lindstrom, J.M., and McIntosh, J.M., J. Neurosci., 2003, vol. 23, pp. 8445–8452.

    PubMed  CAS  Google Scholar 

  92. Loughnan, M.L., Nicke, A., Jones, A., Adams, D.J., Alewood, P.F., and Lewis, R.J., J. Med. Chem., 2004, vol. 47, pp. 1234–1241.

    Article  PubMed  CAS  Google Scholar 

  93. Azam, L., Dowell, C., Watkins, M., Stitzel, J.A., Olivera, B.M., and McIntosh, J.M., J. Biol. Chem., 2005, vol. 280, pp. 80–87.

    PubMed  CAS  Google Scholar 

  94. McIntosh, J.M., Plazas, P.V., Watkins, M., Gomez-Casati, M.E., Olivera, B.M., and Elgoyhen, A.B., J. Biol. Chem., 2005, vol. 280, pp. 30107–30112.

    Article  PubMed  CAS  Google Scholar 

  95. Hopkins, C., Grilley, M., Miller, C., Shon, K.J., Cruz, L.J., Gray, W.R., Dykert, J., Rivier, J., Yoshikami, D., and Olivera, B.M., J. Biol. Chem., 1995, vol. 270, pp. 22361–22367.

    PubMed  CAS  Google Scholar 

  96. Shon, K.J., Grilley, M., Jacobsen, R., Cartier, G.E., Hopkins, C., Gray, W.R., Watkins, M., Hillyard, D.R., Rivier, J., Torres, J., Yoshikami, D., and Olivera, B.M., Biochemistry, 1997, vol. 36, pp. 9581–9587.

    PubMed  CAS  Google Scholar 

  97. Jacobsen, R., Yoshikami, D., Ellison, M., Martinez, J., Gray, W.R., Cartier, G.E., Shon, K.J., Groebe, D.R., Abramson, S.N., Olivera, B.M., and McIntosh, J.M., J. Biol. Chem., 1997, vol. 272, pp. 22 531–22 537.

    Article  CAS  Google Scholar 

  98. Teichert, R.W., Rivier, J., Dykert, J., Cervini, L., Gulyas, J., Bulaj, G., Ellison, M., and Olivera, B.M., Toxicon, 2004, vol. 44, pp. 207–214.

    Article  PubMed  CAS  Google Scholar 

  99. Teichert, R.W., Jimenez, E.C., and Olivera, B.M., Biochemistry, 2005, vol. 44, pp. 7897–7902.

    Article  PubMed  CAS  Google Scholar 

  100. Craig, A.G., Zafaralla, G., Cruz, L.J., Santos, A.D., Hillyard, D.R., Dykert, J., Rivier, J.E., Gray, W.R., and Imperial, J., DelaCruz, R.G., Sporning, A., Terlau, H., West, P.J., Yoshikami, D., Olivera, B.M, Biochemistry, 1998, vol. 37, pp. 16019–16025.

    PubMed  CAS  Google Scholar 

  101. Rigby, A.C., Lucas-Meunier, E., Kalume, D.E., Czerwiec, E., Hambe, B., Dahlqvist, I., Fossier, P., Baux, G., Roepstorff, P., Baleja, J.D., Furie, B.C., Furie, B., and Stenflo, J., Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 5758–5763.

    Article  PubMed  CAS  Google Scholar 

  102. Jimenez, E.C., Watkins, M., Juszczak, L.J., Cruz, L.J., and Olivera, B.M., Toxicon, 2001, vol. 39, pp. 803–808.

    Article  PubMed  CAS  Google Scholar 

  103. Millard, E.L., Daly, N.L., and Craik, D.J., Eur. J. Biochem., 2004, vol. 271, pp. 2320–2326.

    Article  PubMed  CAS  Google Scholar 

  104. McIntosh, J.M., Azam, L., Staheli, S., Dowell, C., Lindstrom, J.M., Kuryatov, A., Garrett, J.E., Marks, M.J., and Whiteaker, P., Mol. Pharmacol., 2004, vol. 65, pp. 944–952.

    Article  PubMed  CAS  Google Scholar 

  105. Gray, W.R., Luque, F.A., Galyean, R., Atherton, E., Sheppard, R.C., Stone, B.L., Reyes, A., Alford, J., McIntosh, M., and Olivera, B.M., Biochemistry, 1984, vol. 23, pp. 2796–2802.

    Article  PubMed  CAS  Google Scholar 

  106. Almquist, R.G., Kadambi, S.R., Yasuda, D.M., Weitl, F.L., Polgar, W.E., and Toll, L.R., Int. J. Pept. Protein Res., 1989, vol. 34, pp. 455–462.

    PubMed  CAS  Google Scholar 

  107. Hashimoto, K., Uchida, S., Yoshida, H., Nishiuchi, Y., Sakakibara, S., and Yukari, K., Eur. J. Pharmacol., 1985, vol. 118, pp. 351–354.

    PubMed  CAS  Google Scholar 

  108. Hann, R.M., Pagan, O.R., Gregory, L.M., Jacome, T., and Eterovic, V.A., Biochemistry, 1997, vol. 36, pp. 9051–9056.

    Article  PubMed  CAS  Google Scholar 

  109. Quiram, P.A., and Sine, S.M., J. Biol. Chem., 1998, vol. 273, pp. 11 007–11 011.

    CAS  Google Scholar 

  110. Servent, D., Thanh, H.L., Antil, S., Bertrand, D., Corringer, P.J., Changeux, J.P., and Menez, A., J. Physiol. (Paris), 1998, vol. 92, pp. 107–111.

    CAS  Google Scholar 

  111. Utkin, Y.N., Zhmak, M.N., Methfessel, C., and Tsetlin, V.I., Toxicon, 1999, vol. 37, pp. 1683–1695.

    Article  PubMed  CAS  Google Scholar 

  112. Jacobsen, R.B., DelaCruz R.G., Grose J.H., McIntosh J.M., Yoshikami D., Olivera B.M., Biochemistry, 1999, vol. 38, pp. 13 310–13 315.

    Article  CAS  Google Scholar 

  113. Papineni, R.V., Sanchez, J.U., Baksi, K., Willcockson, I.U., and Pedersen, S.E., J. Biol. Chem., 2001, vol. 276, pp. 23 589–23 598.

    Article  CAS  Google Scholar 

  114. Everhart, D., Cartier, G.E., Malhotra, A., Gomes, A.V., McIntosh, J.M., and Luetje, C.W., Biochemistry, 2004, vol. 43, pp. 2732–2737.

    Article  PubMed  CAS  Google Scholar 

  115. Kasheverov, I.E., Zhmak, M.N., Maslennikov, I.V., Utkin, Y.N., and Tsetlin, V.I., Neurochem. Res., 2003, vol. 28, pp. 599–606.

    PubMed  CAS  Google Scholar 

  116. Kasheverov, I.E., Zhmak, M.N., Mordvintsev, D.Yu., Utkin, Y.N., Smit, A.B., and Tsetlin, V.I., FEBS J., 2005, vol. 272,Suppl. 1, p. 401.

    Google Scholar 

  117. Gehrmann, J., Alewood, P.F., and Craik, D.J., J. Mol. Biol., 1998, vol. 278, pp. 401–415.

    Article  PubMed  CAS  Google Scholar 

  118. Hargittai, B. and Barany, G., J. Pept. Res., 1999, vol. 54, pp. 468–479.

    Article  PubMed  CAS  Google Scholar 

  119. Kaerner, A. and Rabenstein, D.L., Biochemistry, 1999, vol. 38, pp. 5459–5470.

    Article  PubMed  CAS  Google Scholar 

  120. Lamthanh, H., Jegou-Matheron, C., Servent, D., Menez, A., and Lancelin, J.M., FEBS Lett., 1999, vol. 454, pp. 293–298.

    Article  PubMed  CAS  Google Scholar 

  121. Mok, K.H. and Han, K.H., Biochemistry, 1999, vol. 38, pp. 11 895–11 904.

    Article  CAS  Google Scholar 

  122. Hargittai, B., Sole, N.A., Groebe, D.R., Abramson, S.N., and Barany, G., J. Med. Chem., 2000, vol. 43, pp. 4787–4792.

    Article  PubMed  CAS  Google Scholar 

  123. Zhang, R. and Snyder, G., Biochemistry, 1991, vol. 30, pp. 11 343–11 348.

    CAS  Google Scholar 

  124. Rogers, J.P., Luginbuhl, P., Pemberton, K., Harty, P., Wemmer, D.E., and Stevens, R.C., J. Mol. Biol., 2000, vol. 304, pp. 911–926.

    Article  PubMed  CAS  Google Scholar 

  125. Kasheverov, I., Zhamk, M., Chivilyov, E., Saez-Brionez, P., Utkin, Y., Hucho, F., and Tsetlin, V., J. Recept. Signal Transduct. Res., 1999, vol. 19, pp. 559–571.

    PubMed  CAS  Google Scholar 

  126. Kasheverov, I., Rozhkova, A., Zhmak, M., Utkin, Y., Ivanov, V., and Tsetlin, V.I., Eur. J. Biochem., 2001, vol. 268, pp. 3664–3673.

    Article  PubMed  CAS  Google Scholar 

  127. Luo, S. and McIntosh, J.M., Biochemistry, 2004, vol. 43, pp. 6656–6662.

    PubMed  CAS  Google Scholar 

  128. Whiteaker, P., McIntosh, J.M., Luo, S., Collins, A.C., and Marks, M.J., Mol. Pharmacol., 2000, vol. 57, pp. 913–925.

    PubMed  CAS  Google Scholar 

  129. Zolotarev, Yu.A., Bocharov, E.V., Dadayan, A.K., Kasheverov, I.E., Zhmak, M.N., Maslennikov, I.V., Borisov, Yu.A., Arseniev, A.S., Myasoedov, N.F., and Tsetlin, V.I., Rus. J. Bioorg. Khim., 2000, vol. 26, pp. 527–531.

    CAS  Google Scholar 

  130. Ashcom, J.D. and Stiles, B.G., Biochem. J., 1997, vol. 328, pp. 245–250.

    PubMed  CAS  Google Scholar 

  131. Quiram, P.A., McIntosh, J.M., and Sine, S.M., J. Biol. Chem., 2000, vol. 275, pp. 4889–4896.

    Article  PubMed  CAS  Google Scholar 

  132. Quiram, P.A., Jones, J.J., and Sine, S.M., J. Biol. Chem., 1999, vol. 274, pp. 19 517–19 524.

    Article  CAS  Google Scholar 

  133. Bren, N. and Sine, S.M., J. Biol. Chem., 2000, vol. 275, pp. 12 692–12 700.

    Article  CAS  Google Scholar 

  134. Velez-Carrasco, W., Valdes, S., Agresar, L., Lettich, A., Guerra, A.Y., and Hann, R.M., Biochemistry, 2004, vol. 43, pp. 12 700–12 708.

    Article  CAS  Google Scholar 

  135. Blanchfield, J.T., Dutton, J.L., Hogg, R.C., Gallagher, O.P., Craik, D.J., Jones, A., Adams, D.J., Lewis, R.J., Alewood, P.F., and Toth, I., J. Med. Chem., 2003, vol. 46, pp. 1266–1272.

    Article  PubMed  CAS  Google Scholar 

  136. Mezo, G., Drakopoulou, E., Paal, V., Rajnavolgyi, E., Vita, C., and Hudecz, F., J. Pept. Res., 2000, vol. 55, pp. 7–17.

    Article  PubMed  CAS  Google Scholar 

  137. Drakopoulou, E., Uray, K., Mezo, G., Price, M.R., Vita, C., and Hudecz, F., J. Pept. Sci., 2000, vol. 6, pp. 175–185.

    PubMed  CAS  Google Scholar 

  138. Sandall, D.W., Satkunanathan, N., Keays, D.A., Polidano, M.A., Liping, X., Pham, V., Down, J.G., Khalil, Z., Livett, B.G., and Gayler, K.R., Biochemistry, 2003, vol. 42, pp. 904–911.

    Article  CAS  Google Scholar 

  139. Sine, S.M., J. Neurobiol., 2002, vol. 53, pp. 431–446.

    Article  PubMed  CAS  Google Scholar 

  140. Brejc, K., van Dijk, W.J., Klaassen, R.V., Schuurmans, M., van Der Oost, J., Smit, A.B., and Sixma, T.K., Nature, 2001, vol. 411, pp. 269–276.

    Article  PubMed  CAS  Google Scholar 

  141. Smit, A.B., Syed, N.I., Schaap, D., van Minnen, J., Klumperman, J., Kits, K.S., Lodder, H., van der Schors, R.C., van Elk, R., Sorgedrager, B., Brejc, K., Sixma, T.K., and Geraerts, W.P., Nature, 2001, vol. 411, pp. 261–268.

    Article  PubMed  CAS  Google Scholar 

  142. Fruchart-Gaillard, C., Gilquin, B., and Antil-Delbeke, S., Le Novere, N., Tamiya, T., Corringer, P.J., Changeux, J.P., Menez, A., Servent, D., Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 3216–3221.

    Article  PubMed  CAS  Google Scholar 

  143. Moise, L., Piserchio, A., Basus, V.J., and Hawrot, E., J. Biol. Chem., 2002, vol. 277, pp. 12 406–12 417.

    Article  CAS  Google Scholar 

  144. Samson, A., Scherf, T., Eisenstein, M., Chill, J., and Anglister, J., Neuron, 2002, vol. 35, pp. 319–332.

    Article  PubMed  CAS  Google Scholar 

  145. Harel, M., Kasher, R., Nicolas, A., Guss, J.M., Balass, M., Fridkin, M., Smit, A.B., Brejc, K., Sixma, T.K., Katchalski-Katzir, E., Sussman, J.L., and Fuchs, S., Neuron, 2001, vol. 32, pp. 265–275.

    Article  PubMed  CAS  Google Scholar 

  146. Zeng, H. and Hawrot, E., J. Biol. Chem., 2002, vol. 277, pp. 37 439–37 445.

    CAS  Google Scholar 

  147. Utkin, Y.N., Kukhtina, V.V., Kryukova, E.V., Chiodini, F., Bertrand, D., Methfessel, C., and Tsetlin, V.I., J. Biol. Chem., 2001, vol. 276, pp. 15 810–15 815.

    Article  CAS  Google Scholar 

  148. Celie, P.H., van Rossum-Fikkert, S.E., van Dijk, W.J., Brejc, K., Smit, A.B., and Sixma, T.K., Neuron, 2004, vol. 41, pp. 907–914.

    Article  PubMed  CAS  Google Scholar 

  149. Dutertre, S. and Lewis, R.J., Eur. J. Biochem., 2004, vol. 271, pp. 2327–2334.

    Article  PubMed  CAS  Google Scholar 

  150. Hansen, S.B., Talley, T.T., Radic, Z., and Taylor, P., J. Biol. Chem., 2004, vol. 279, pp. 24 197–24 202.

    CAS  Google Scholar 

  151. Gao, F., Bren, N., Burghardt, T.P., Hansen, S., Henchman, R.H., Taylor, P., McCammon, J.A., and Sine, S.M., J. Biol. Chem., 2005, vol. 280, pp. 8443–8451.

    PubMed  CAS  Google Scholar 

  152. Unwin, N., J. Mol. Biol., 2005, vol. 346, pp. 967–989.

    Article  PubMed  CAS  Google Scholar 

  153. Bourne, Y., Talley, T.T., Hansen, S.B., Taylor, P., and Marchot, P., EMBO J., 2005, vol. 24, pp. 1512–1522.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, ul. Miklukho-Maklaya 16/10, Moscow, 117997, Russia

    I. E. Kasheverov, Yu. N. Utkin & V. I. Tsetlin

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  1. I. E. Kasheverov
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  2. Yu. N. Utkin
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  3. V. I. Tsetlin
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Correspondence to I. E. Kasheverov.

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Original Russian Text © I.E. Kasheverov, Yu.N. Utkin, V.I. Tsetlin, 2006, published in Bioorganicheskaya Khimiya, 2006, Vol. 32, No. 2, pp. 115–129.

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Kasheverov, I.E., Utkin, Y.N. & Tsetlin, V.I. Natural α-conotoxins and their synthetic analogues in study of nicotinic acetylcholine receptors. Russ J Bioorg Chem 32, 103–115 (2006). https://doi.org/10.1134/S1068162006020014

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Key words

  • acetylcholine-binding proteins
  • α-conotoxins
  • synthetic analogues
  • structure
  • biological activity
  • nicotinic acetylcholine receptors