The structure of versutoxin (δ-atracotoxin-Hv1) provides insights into the binding of site 3 neurotoxins to the voltage-gated sodium channel

Structure

Volumn 5, Issue 11, 1997, Pages 1525-1535

  Fletcher, Jamie I ^a   Chapman, Bogdan E ^a   Mackay, Joel P ^a   Howden, Merlin E H ^b   King, Glenn F ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b University of Sydney   (Australia)

Author keywords

Anthopleurin; Gurmarin; Sodium channel inactivation; Versutoxin; scorpion toxin

Indexed keywords

EID: 0030727613     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00301-8     Document Type: Article

References (62)

1. Olivera, B.M., Miljanich, G.P., Ramachandran, J. & Adams, M.E. (1994). Calcium channel diversity and neurotransmitter release: the •-conotoxins and •-agatoxins. Annu. Rev. Biochem. 63, 823-867.
2. McIntosh, J.M., et al., & Olivera, B.M. (1995). A new family of conotoxins that blocks voltage-gated sodium channels. J. Biol. Chem. 270, 16796-16802.
3. Valentino, K., et al., & Ramachandran, J. (1993). A selective N-type calcium channel antagonist protects against neuronal loss after global cerebral ischemia. Proc. Natl. Acad. Sci. USA 90, 7894-7897.
4. Fletcher, J.I., et al., & King, G.F. (1997). The structure of a novel insecticidal neurotoxin, •-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nat. Struct. Biol. 4, 559-566.
5. Gray, M.R. (1988). Aspects of the systematics of the Australian funnel web spiders (Araneae: Hexathelidae: Atracinae) based upon morphological and electrophoretic data. In Australian arachnology. (Austin, A.D. & Heather, N.W., eds), pp. 113-125, The Australian Entomological Society, Brisbane, Australia.
6. Sheumack, D.D., Baldo, B.A., Carroll, P.R., Hampson, F., Howden, M.E.H. & Skorulis, A. (1984). A comparative study of properties and toxic constituents of funnel web spiders (Atrax) venoms. Comp. Biochem. Physiol. 78C, 55-68.
7. Sutherland, S.K. (1980). Antivenom to the venom of the male Sydney funnel web spider, Atrax robustus. Med. J. Aust. 2, 437-441.
8. Mylecharane, E.J., Spence, I., Scheumack, D.D., Claassens, R. & Howden, M.E.H. (1989). Actions of robustoxin, a neurotoxic polypeptide from the venom of the male funnel-web spider (Atrax robustus) in anaesthetized monkeys. Toxicon 27, 481-492.
9. Phillips, C.A., et al., & Howden, M.E.H. (1987). The effects of the venom from the Blue Mountains funnel-web spider (Atrax versutus) in anaesthetized monkeys. Clin. Exp. Pharmacol. Physiol. Suppl. 10, 14-15.
10. Nicholson, G.M., Willow, M., Howden, M.E.H. & Narahashi, T. (1994). Modification of sodium channel gating and kinetics by versutoxin from the Australian funnel-web spider Hadronyche versuta. Pflügers Arch. 428, 400-409.
11. Sheumack, D.D., Claassens, R., Howden, M.E.H. & Whitley, N.M. (1985). Complete amino acid sequence of a new type of lethal neurotoxin from the venom of the funnel-web spider Atrax robustus. FEBS Lett. 181, 154-156.
12. Brown, M.R., Sheumack, D.D., Tyler, M.I. & Howden, M.E.H. (1988). Amino acid sequence of versutoxin, a lethal neurotoxin from the venom of the funnel-web spider Atrax versutus. Biochem. J. 250, 401-405.
13. Catterall, W.A. (1988). Structure and function of voltage-sensitive ion channels. Science 242, 50-61.
14. Nicholson, G.M., Little, M.J., Tyler, M. & Narahashi, T. (1996). Selective alteration of sodium channel gating by Australian funnel-web spider toxins. Toxicon 34, 1443-1453.
15. Omecinsky, D.O., Holub, K.E., Adams, M.E. & Reily, M.D. (1996). Three-dimensional structure analysis of •-agatoxins: further evidence for common motifs among neurotoxins with diverse ion channel specificities. Biochemistry 35, 2836-2844.
16. Arai, K., et al., & Akasaka, K. (1995). Three-dimensional structure of gurmarin, a sweet-taste suppressing polypeptide. J. Biomol. NMR 5, 297-305.
17. Imoto, T., Miyasaka, A., Ishima, R. & Akasaka, K. (1991). A novel peptide isolated from the leaves of Gymnema sylvestre. I. Characterization and its suppressive effect on the neural responses to sweet taste stimuli in the rat. Comp. Biochem. Physiol. 100A, 309-314.
18. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. John Wiley & Sons, Inc., New York.
19. Nilges, M., Clore, G.M. & Gronenborn, A.M. (1988). Determination of the three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Lett. 229, 317-324.
20. Güntert, P., Braun, W. & Wüthrich, K. (1991). Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217, 517-530.
21. Brünger, AT. (1992). X-PLOR Version 3.1. A System for Crystallography and NMR. Yale University Press, New Haven, CT, USA.
22. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structure coordinates. J. Appl. Cryst. 26, 283-291.
23. Hyberts, S.V., Goldberg, M.S., Havel, T.F. & Wagner, G. (1992). The solution structure of eglin c based on measurements of many NOEs and coupling constants and its comparison with X-ray structures. Protein Sci. 1, 736-751.
24. Richardson, J.S. (1981). The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167-339.
25. Pallaghy, P.K., Nielsen, K.J., Craik, D.J. & Norton, R.S. (1994). A common structural motif incorporating a cystine knot and a triple-stranded •-sheet in toxic and inhibitory polypeptides. Protein Sci. 3, 1833-1839.
26. Hutchinson, E.G. & Thornton, J.M. (1994). A revised set of potentials for •-turn formation in proteins. Protein Sci. 3, 2207-2216.
27. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
28. Reily, M.D., Thanabal, V. & Adams, M.E. (1995). The solution structure of •-Aga-IVB, a P-type calcium channel antagonist from venom of the funnel web spider, Agelenopsis aperta. J. Biomol. NMR 5, 122-132.
29. Yu, H., et al., & Schreiber, S.L. (1993). Sequential assignment and structure determination of spider toxin •-Aga-IVB. Biochemistry 32, 13123-13129.
30. Miyasaka, A. & Imoto, T. (1995). Electrophysiological characterization of the inhibitory effect of a novel peptide gurmarin on the sweet taste response in rats. Brain Res. 676, 63-68.
31. Lindemann, B. (1996). Taste reception. Physiol. Rev. 76, 719-766.
32. + channel • subunit. J. Biol. Chem. 271, 15950-15962.
33. Gordon, D., et al., & Rochat, H. (1996). Scorpion toxins affecting sodium channel current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J. Biol. Chem 271, 8034-8045.
34. Loret, E.P., Mansuelle, P., Rochat, H. & Granier, C. (1990). Neurotoxins active on insects: amino acid sequences, chemical modification and secondary structure estimation by circular dichroism of toxins from the scorpion Androctonus australia Hector. Biochemistry 29, 1492-1501.
35. Kharrat, R., Darbon, H., Rochat, H. & Granier, C. (1989). Structure/activity relationships of scorpion •-toxins. Multiple residues contribute to the interaction with receptors. Eur. J. Biochem. 181, 381-390.
36. Khera, P.K. & Blumenthal, K.M. (1994). Role of the cationic residues arginine 14 and lysine 48 in the function of the cardiotonic polypeptide anthopleurin B. J. Biol. Chem. 269, 921-925.
37. Norton, R.S. (1991). Structure and structure-function relationships of sea anemone proteins that interact with the sodium channel. Toxicon 29, 1051-1084.
38. Gallagher, M.J. & Blumenthal, K.M. (1992). Cloning and expression of wild-type and mutant forms of the cardiotonic polypeptide anthopleurin B. J. Biol. Chem. 267, 13958-13963.
39. Gallagher, M.J. & Blumenthal, K.M. (1994). Importance of the unique cationic residues arginine 1 2 and lysine 49 in the activity of the cardiotonic polypeptide anthopleurin B. J. Biol. Chem. 269, 254-259
40. Khera, P.K. & Blumenthal, K.M. (1996). Importance of highly conserved anionic residues and electrostatic interactions in the activity and structure of the cardiotonic polypeptide anthopleurin B. Biochemistry 35, 3503-3507.
41. Monks, S.A., Pallaghy, P.K., Scanlon, M.J. & Norton, R.S. (1995). Solution structure of the cardiostimulant polypeptide anthopleurin-B and comparison with anthopleurin-A. Structure 3, 791-803.
42. Housset, D., Habersetzer-Rochat, C., Astier, J.-P. & Fontecilla-Camps, J.C. (1994). Crystal structure of toxin II from Androctonus australis Hector refined at 1.3 Å resolution. J. Mol. Biol. 238, 88-103.
43. Dias-Kadambi, B.L., Combs, K.A., Drum, C.L., Hanck, DA & Blumenthal, K.M. (1996). The role of exposed tryptophan residues in the activity of the cardiotonic polypeptide anthopleurin B. J. Biol. Chem. 271, 23828-23835.
44. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117, 479-485.
45. Derome, A.E. & Williamson, M.P. (1990). Rapid-pulsing artifacts in double-quantum-filtered COSY. J. Magn. Reson. 88, 177-185.
46. Bax, A. & Davis, D.G. (1985). MLEV-17 based two-dimensional homonuclear magnetisation transfer spectroscopy. J. Magn. Reson. 65, 355-360.
47. Griesinger, C., Sørensen, O.W. & Ernst, R.R. (1987). Practical aspects of the E.COSY technique. Measurement of scalar spin-spin coupling constants in peptides. J. Magn. Reson. 75, 474-492.
48. Kumar, A., Ernst, R.R. & Wüthrich, K. (1980). A two-dimensional nuclear Overhauser enhancement (2D nOe) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Comm. 95, 1-6.
49. Piotto, M., Saudek, V. & Sklenár, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
50. 1H NMR spectra in proteins. J. Magn. Reson. 77, 166-169.
51. Wüthrich, K., Billeter, M. & Braun, W. (1983). Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance. J. Mol. Biol. 169, 949-961.
52. Clore, G.M., Wingfield, P.T. & Gronenborn, A.M. (1991). High-resolution three-dimensional structure of interleukin 1• in solution by three- and four-dimensional nuclear magnetic resonance spectroscopy. Biochemistry 30, 2315-2323.
53. HN• for identification of helical secondary structure. J. Mol. Biol. 180, 741-751.
54. Clubb, R.T., Ferguson, S.B., Walsh, C.T. & Wagner, G. (1994). Three-dimensional solution structure of Escherichia coli periplasmic cyclophilin. Biochemistry 33, 2761-2722.
55. Ludvigsen, S. & Poulsen, F.M. (1992). Positive theta-angles in proteins by nuclear magnetic resonance spectroscopy. J. Biomol. NMR 2, 227-233.
56. Wagner, G., Braun, W., Havel, T.F., Schaumann, T., Gõ, N. & Wüthrich, K. (1987). Protein structures in solution by nuclear magnetic resonance and distance geometry. The polypeptide fold of the basic pancreatic trypsin inhibitor determined using two different algorithms, DISGEO and DISMAN. J. Mol. Biol. 196, 611-639.
57. 1H-NMR methyl lines and conformation of valyl residues in the lac represser headpiece. Biopolymers 24, 601-611.
58. Kline, A.D., Braun, W. & Wüthrich, K. (1988). Determination of the complete three-dimensional structure of the alpha-amylase inhibitor tendamistat in aqueous solution by nuclear magnetic resonance and distance geometry. J. Mol. Biol. 204, 675-724.
59. Güntert, P. & Wüthrich, K. (1991). Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J. Biomol. NMR 1, 447-456.
60. Hutchinson, E.G. & Thornton, J.M. (1996). PROMOTIF - A program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212-220.
61. Barton, G.J. (1993). ALSCRIPT. A tool to format multiple sequence alignments. Protein Eng. 6, 37-40.
62. Koradi, R., Billeter, M. & Wüthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55.