A novel conotoxin inhibitor of Kv1.6 channel and nAChR subtypes defines a new superfamily of conotoxins

Biochemistry

Volumn 45, Issue 27, 2006, Pages 8331-8340

  Imperial, Julita S ^a,b   Bansal, Paramjit S ^b   Alewood, Paul F ^b   Daly, Norelle L ^b   Craik, David J ^b   Sporning, Annett ^c   Terlau, Heinrich ^c,d   López Vera, Estuardo ^a   Bandyopadhyay, Pradip K ^a   Olivera, Baldomero M ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BARRELING; CHEMICAL BONDS; GENES; NEUROMUSCULAR REHABILITATION; SYNTHESIS (CHEMICAL);

CONOTOXIN INHIBITOR; N-TERMINAL TAIL; THREE-DIMENSIONAL STRUCTURE; VERMIVOROUS CONE;

POTASSIUM;

AMINO ACID; COMPLEMENTARY DNA; CONOTOXIN; ION CHANNEL; LIGAND GATED ION CHANNEL; NICOTINIC RECEPTOR; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; PROTEIN P114A; RECEPTOR SUBTYPE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; DNA DETERMINATION; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN STRUCTURE; SEIZURE; SNAIL;

AMINO ACID SEQUENCE; ANIMALS; CONOTOXINS; CONUS SNAIL; DNA, COMPLEMENTARY; KV1.6 POTASSIUM CHANNEL; MICE; MOLECULAR SEQUENCE DATA; MUSCLES; NEURONS; NICOTINIC ANTAGONISTS; PHYLOGENY; PROTEIN CONFORMATION; RECEPTORS, NICOTINIC;

CONUS PLANORBIS; GASTROPODA;

EID: 33745846440     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060263r     Document Type: Article

References (60)

1. Terlau, H., Shon, K., Grilley, M., Stocker, M., Stühmer, W., and Olivera, B. M. (1996) Strategy for rapid immobilization of prey by a fish-hunting cone snail, Nature 381, 148-151.
2. Olivera, B. M., Gray, W. R., Zeikus, R., McIntosh, J. M., Varga, J., Rivier, J., de Santos, V., and Cruz, L. J. (1985) Peptide neurotoxins from fish-hunting cone snails, Science 230, 1338-1343.
3. Olivera, B. M. (2002) Conus venom peptides: Reflections from the biology of clades and species, Annu. Rev. Ecol. Syst. 33, 25-42.
4. Olivera, B. M. (1997) Conus venom peptides, receptor and ion channel targets and drug design: 50 million years of neuropharmacology (E. E. Just Lecture, 1996), Mol. Biol. Cell 8, 2101-2109.
5. Duda, T. F., Jr., Kohn, A. J., and Palumbi, S. R. (2001) Origins of diverse feeding ecologies within Conus, a genus of venomous marine gastropods, Biol. J. Linn. Soc. 73, 391-409.
6. Röckel, D., Korn, W., and Kohn, A. J. (1995) Manual of the Living Conidae, Vol. I: Indo-Pacific Region, Verlag Christa Hemmen, Wiesbaden, Germany.
7. Massilia, G. R., Schininà, M. E., Ascenzi, P., and Polticelli, F. (2001) Contryphan-Vn: A novel peptide from the venom of the Mediterranean snail Conus ventricosus, Biochem. Biophys. Res. Commun. 288, 908-913.
8. Sudarslal, S., Singaravadivelan, G., Ramasamy, P., Ananda, K., Sarma, S. P., Sikdar, S. K., Krishnan, K. S., and Balaram, P. (2004) A novel 13 residue acyclic peptide from the marine snail, Conus monile, targets potassium channels, Biochem. Biophys. Res. Commun. 317, 682-688.
9. Kauferstein, S., Huys, I., Kuch, U., Melaun, C., Tytgat, J., and Mebs, D. (2004) Novel conopeptides of the I-superfamily occur in several clades of cone snails, Toxicon 44, 539-548.
10. Ellison, M., McIntosh, J. M., and Olivera, B. M. (2003) α-Conotoxins ImI and ImII: Similar α7 nicotinic receptor antagonists act at different sites, J. Biol. Chem. 278, 757-764.
11. Fan, C.-X., Chen, X.-K., Zhang, C., Wang, L.-X., Duan, K. L., He, L. L., Cao, Y., Liu, S.-Y., Zhong, M-N., Ulens, C., Tytgat, J., Chen, J.-S., Chi, C.-W., and Zhou, Z. (2003) A novel conotoxin from Conus betulinus, κ-BtX, unique in cysteine pattern and in function is a specific BK channel modulator, J. Biol. Chem. 278, 12624-12633.
12. McIntosh, J. M., Yoshikami, D., Mahe, E., Nielsen, D. B., Rivier, J. E., Gray, W. R., and Olivera, B. M. (1994) A nicotinic acetylcholine receptor ligand of unique specificity, α-conotoxin ImI, J. Biol. Chem. 269, 16733-16739.
13. Abogadie, F. C., Ramilo, C. A., Corpuz, G. P., and Cruz, L. J. (1990) Biologically active peptides from Conus quercinus, a worm-hunting species, Trans. Natl. Acad. Sci. Technol., Repub. Philipp. 12, 219-232.
14. Braga, M. C. V., Katsuhiro, K., Portaro, F. C. V., De Freitas, J. C., Yamane, T., Olivera, B. M., and Pimenta, D. C. (2005) Mass spectrophotometric and high performance liquid chromatography profiling of the venom of the Brazilian vermivorous mollusk Conus regius: Feeding behavior and identification of one novel conotoxin, Toxicon 45, 113-122.
15. Loughnan, M. L., Nicke, A., Jones, A., Adams, D. J., Alewood, P. F., and Lewis, R. J. (2004) Chemical and functional identification and characterization of novel sulfated α-conotoxins from the cone snail Conus anemone, J. Med. Chem. 47, 1234-1241.
16. Moller, C., Rahmankhah, S., Lauer-Fields, J., Bubis, J., Fields, G. B., and Mari, F. (2005) A novel conotoxin framework with a helix-loop-helix (Cs α/α) fold, Biochemistry 44, 15986-15996.
17. Aguilar, M. B., Lopez-Vera, E., Imperial, J. S., Falcon, A., Olivera, B. M., and Heimer de la Cortera, E. P. (2005) Putative γ-conotoxins in vermivorous cone snails: The case of Conus delessertii, Peptides 26, 23-27.
18. Terlau, H., and Olivera, B. M. (2004) Conus venoms: A rich source of novel ion channel-targeted peptides, Physiol. Rev. 84, 41-68.
19. Espiritu, D. J. D., Watkins, M., Dia-Monje, V., Cartier, G. E., Cruz, L. J., and Olivera, B. M. (2001) Venomous cone snails: Molecular phylogeny and the generation of toxin diversity, Toxicon 39, 1899-1916.
20. Alewood, P. F., Alewood, D., Miranda, L. P., Love, S., Meutermans, W. D. F., and Wilson, D. (1997) Rapid in situ neutralization protocols for Boc and Fmoc solid-phase chemistries, Methods Enzymol. 289, 14-29.
21. Manuscript in preparation.
22. Gray, W. R. (1993) Disulfide structures of highly bridged peptides: A new strategy for analysis, Protein Sci. 2, 1732-1748.
23. Daly, N. L., Ekberg, J. A., Thomas, L., Adams, D. J., Lewis, R. J., and Craik, D. J. (2004) Structures of μO-conotoxins from Conus marmoreus. Inhibitors of tetrodotoxin (TTX)-sensitive and TTX-resistant sodium channels in mammalian sensory neurons, J. Biol. Chem. 279, 25774-25782.
24. Rosengren, K. J., Daly, N. L., Plan, M. R., Waine, C., and Craik, D. J. (2003) Twists, knots, and rings in proteins. Structural definition of the cyclotide framework, J. Biol. Chem. 278, 8606-8616.
25. Guntert, P., Mumenthaler, C., and Wutrich, K. (1997) Torsion angle dyanmics for NMR structure calculation with the new program DYANA, J. Mol. Biol. 273, 283-298.
26. Brunger, A. T., Adams, P. D., and Rice, L. M. (1997) New applications of simulated annealing in X-ray crystallography and solution, Structure 5, 325-336.
27. Hutchinson, E. G., and Thornton, J. M. (1996) PROMOTIF: A program to identify and analyze structural motifs in proteins, Protein Sci. 5, 212-220.
28. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
29. Frohman, M. A. (1990) RACE: Rapid amplification of cDNA ends, in PCR Protocols (Innis, M. A., Ed.) pp 28-45, Academic Press, San Diego.
30. Cartier, G. E., Yoshikami, D., Gray, W. R., Luo, S., Olivera, B. M., and McIntosh, J. M. (1996) A new α-conotoxin which targets α3β2 nicotinic acetylcholine receptors, J. Biol. Chem. 271, 7522-7528.
31. + channel, J. Biol. Chem. 275, 24639-24644.
32. Horton, R. M., Manfredi, A. A., and Conti-Tronconi, B. M. (1993) The 'embryonic' γ subunit of the nicotinic acetylcholine receptor is expressed in adult extraocular muscle, Neurology 43, 983-986.
33. Cruz, L. J., Johnson, D. S., and Olivera, B. M. (1987) Characterization of the ω-conotoxin target. Evidence for tissue-specific heterogeneity in calcium channel types, J. Biol. Chem. 26, 820-824.
34. Wutrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley-Interscience, New York.
35. Eipper, B. A., Perkins, S. N., Hustin, E. J., Johnson, R. C., Keutmann, H. T., and Mains, R. E. (1991) Peptidyl-α-hydroxylglycine α-amidating lyase, J. Biol. Chem. 266, 7827-7833.
36. Olivera, B. M., Rivier, J., Clark, C., Ramilo, C. A., Corpuz, G. P., Abogadie, F. C., Mena, E. E., Woodward, S. R., Hillyard, D. R., and Cruz, L. J. (1990) Diversity of Conus neuropeptides, Science 249, 257-263.
37. Groebe, D. R., Gray, W. R., and Abramson, S. N. (1997) Determinants involved in the affinity of α-conotoxins GI and SI for the muscle subtype of nicotinic acetylcholine receptors, Biochemistry 36, 6469-6474.
38. + channel, J. Biol. Chem. 273, 33-38.
39. + channels, J. Biol. Chem. 278, 2177-2183.
40. Bayrhuber, M., Vijayan, V., Ferber, M., Graf, R., Korukottu, J., Imperial, J., Garrett, J. E., Olivera, B. M., Terlau, H., Zweckstetter, M., and Becker, S. (2005) Conkunitzin-S1 is the first member of a new Kunitz-type neurotoxin family: Structural and functional characterization, J. Biol. Chem. 180, 21246-21255.
41. Imperial, J. S., Silverton, N., Olivera, B. M., Bandyopadhyay, P. K., Sporning, A., Ferber, M., and Terlau, H. (2006) Using venom chemistry to reveal the origins of fish-hunting in cone snails, Proc. Am. Philos. Soc. (in press).
42. Cotton, J., Crest, M., Bouet, F., Alessandri, N., Gola, M., Forest, E., Karlsson, E., Castaneda, O., Harvey, A. L., Vita, C., and Menez, A. (1997) A potassium-channel toxin from the sea anemone Bundosoma granulifera, an inhibitor for Kv1 channels. Revision of the amino acid sequence, disulfide-bridge arrangement, chemical synthesis and biological activity, Eur. J. Biochem. 244, 192-202.
43. + channels, Eur. J. Biochem. 267, 5149-5155.
44. Chagot, B., Pimentel, C., Dai, L., Pil, J., Tytgat, J., Nakajima, T., Corzo, G., Darbon, H., and Ferrat, G. (2005) An unusual fold for potassium channel blockers: NMR structure of three toxins from the scorpion Opisthacanthus madagascariensis, Biochem. J. 388, 263-271.
45. Srinivasan, K. N., Sivaraja, V., Huys, I., Sasaki, T., Cheng, B., Kumar, T. K. S., Sato, K., Tytgat, J., Yu, C., San, B. C. C., Ranganathan, S., Bowie, H. J., Kini, R. M., and Gopalakrishnakone, P. (2002) κ-Hefutoxin1, a novel toxin from the scorpion Heterometrus fulvipes with unique structure and function, J. Biol. Chem. 277, 30040-30047.
46. Dauplais, M., Lecoq, A., Song, J., Cotton, J., Jamin, N., Gilquin, B., Roumestand, C., Vita, C., de Medieros, C. L. C., Rowan, E. G., Harvey, A. L., and Menez, A. (1997) On the convergent evolution of animal toxins, J. Biol. Chem. 272, 4302-4309.
47. Gilquin, B., Racape, J., Wrisch, A., Visan, V., Lecoq, A., Grissmer, S., Menez, A., and Gasparini, S. (2002) Structure of the BgK-Kv1.1 complex based on distance restraints identified by double mutant cycles, J. Biol. Chem. 277, 37406-37413.
48. + channels, J. Biol. Chem. 280, 21246-21255.
49. Mouhat, S., Mosbah, A., Visan, V., Wulff, H., Delepierre, M., Darbon, H., Grissmer, S., De Waard, M., and Sabatier, J. (2004) The functional dyad of scorpion toxin Pi1 is not itself a prerequisite for toxin binding to the voltage-gated Kv1.2 potassium channels, Biochem. J. 377, 25-36.
50. Johnson, D. S., Martinez, J., Elgoyhen, A. B., Heinemann, S. F., and McIntosh, J. M. (1995) α-Conotoxin ImI exhibits subtype-specific nicotinic acetylcholine receptor blockade: Preferential inhibition of homomeric α7 and α9 receptors, Mol. Pharmacol. 48, 194-199.
51. Luo, S., Kulak, J. M., Cartier, G. E., Jacobsen, R. B., Yoshikami, D., Olivera, B. M., and McIntosh, J. M. (1998) α-Conotoxin AuIB selectively blocks α3β4 nicotinic acetylcholine receptors and nicotine-evoked norepinephrine release, J. Neurosci. 18, 8571-8579.
52. McIntosh, J. M., Plazas, P. V., Watkins, M., Gomez-Casati, M. E., Olivera, B. M., and Elgoyhen, A. B. (2005) A novel κ-conotoxin, PeIA, cloned from Conus pergrandis, discriminates between rat κ9κ10 and K7 nicotinic cholinergic receptors, J. Biol. Chem. 280, 30107-30112.
53. Azam, L., Dowell, C., Watkins, M., Stitzel, J. A., Olivera, B. M., and McIntosh, J. M. (2005) κ-Conotoxin BuIA, a novel peptide from Conus bullatus, J. Biol. Chem. 280, 80-87.
54. + channels of T cells, Toxicon 46, 418-429.
55. + channel-blocking peptides, Neuron 15, 5-10.
56. Selisko, B., Garcia, C., Becerril, B., Gomez-Lagunas, F., Garay, C., and Possani, L. D. (1998) Cobatoxins 1 and 2 from Centruroides noxius Hoffmann constitute a subfamily of potassium-channel-blocking scorpion toxins, Eur. J. Biochem. 254, 468-479.
57. Dudina, E. E., Korolkova, Y. V., Bocharova, N. E., Koshelev, S. G., Egorov, T. A., Huys, I., Tytgat, J., and Grishin, E. V. (2001) OsK2, a new selective inhibitor of Kv1.2 potassium channels purified from the venom of the scorpion Orthochirus scrobiculosus, Biochem. Biophys. Res. Commun. 286, 841-847.
58. Peter, M. J., Varga, Z., Hajdu, P., Gaspar, R. J., Damjanovich, S., Horjales, E., Possani, L. D., and Panyi, G. (2001) Effect of toxins Pi2 and Pi3 on human T lymphocyte Kv1.3 channels: The role of glu7 and lys24, J. Membr. Biol. 179, 13-25.
59. Abdel-Mottaleb, Y., Coronas, F. V., de Roodt, A. R., Possani, L. D., and Tytgat, J. (2006) A novel toxin from the venom of the scorpion Tityus trivittatus is the first member of a new α-KTX subfamily, FEBS Lett. 580, 592-596.
60. + and HERG currents, Biochem. J. 378, 745-752.