Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge

Nature Structural Biology

Volumn 7, Issue 6, 2000, Pages 505-513

  Wang, Xiu Hong ^a,b   Connor, Mark ^c   Smith, Ross ^d   Maciejewski, Mark W ^a   Howden, Merlin E H ^c   Nicholson, Graham M ^e   Christie, Macdonald J ^c   King, Glenn F ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c University of Sydney   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTOXIN; SPIDER VENOM;

ARTICLE; DISULFIDE BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN ISOLATION; SPIDER; TOXIN ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISULFIDES; EVOLUTION, MOLECULAR; INSECTICIDES; INSECTS; LETHAL DOSE 50; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEURONS; NEUROTOXINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CHOLINERGIC; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; SPIDER VENOMS;

ARANEAE; DIPLURIDAE; INSECTA; JANUS;

EID: 0034043512     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/75921     Document Type: Article

References (50)

1. Feyereisen, R. Molecular biology of insecticide resistance. Toxicol. Lett. 82/83 83-90 (1995).
2. Roush, R.T. & Shelton, A.M. Assessing the odds: the emergence of resistance tc Bt transgenic plants. Nature Biotech. 15, 816-817 (1997).
3. Chamberlain, D. & Stewart, C.N.J. Transgene escape and transplastomics. Nature Biotech. 17, 330-331 (1999).
4. Cory, J.S. et al. Field trial of a genetically improved baculovirus insecticide. Nature 370, 138-140 (1994).
5. Bonning, B.C. & Hammock, B.D. Development of recombinant baculoviruses for insert control. Annu. Rev. Entomol. 41, 191-210 (1996).
6. Black, B.C., Brennan, L.A., Dierks, P.M. & Gard, I.E. Commercialization of baculoviral insecticides. In The baculoviruses (Miller, L.K., ed.) 341-387 (Plenum Press, New York; 1997).
7. Treacy, M.F. Recombinant baculoviruses. In Biopesticides: uses and delivery (Hall, F.R. & Menn, J.J., eds) 321-340 (Humana Press, Totowa, New Jersey; 1999).
8. Miller, M.K., Whyte, I.M., White, J. & Keir, P.M. Clinical features and management of Hadronyche envenomation in man. Toxicon 38, 409-427 (2000).
9. Heitz, A., Le-Nguyen, D. & Chiche, L. Min-21 and Min-23, the smallest peptides that fold like a cystine-stabilized β-sheet motif: design, solution structure, and thermal stability. Biochemistry 38, 10615-10625 (1999).
10. Szeto, T.H. et al. Isolation of a funnel-web spider polypeptide with homology to mamba intestinal toxin 1 and the embryonic head inducer Dickkopf-1. Toxicon 38, 429-442 (1999).
11. Wang, X.-H. et al. Structure-function studies of ω-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur. J. Biochem. 264, 488-494 (1999).
12. Stewart, L.M.D. et al. Construction of an improved baculovirus insecticide containing an insect-specific toxin gene. Nature 352, 85-88 (1991).
13. Wüthrich, K. NMR of proteins and nucleic acids (John Wiley & Sons, Inc., New York; 1986).
14. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: a program to check the stereochemical quality of protein structure coordinates. J. Appl. Crystallogr. 26, 283-291 (1993).
15. Pallaghy, P.K., Nielsen, K.J., Craik, D.J. & Norton, R.S. A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci. 3, 1833-1839 (1994).
16. Norton, R.S. & Pallaghy, P.K. The cystine knot structure of ion channel toxins and related polypeptides. Toxicon 36, 1573-1583 (1998).
17. Fletcher, J.I. et al. The structure of a novel insecticidal neurotoxin, ω-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nature Struct. Biol. 4, 559-566 (1997).
18. Gray, W.R. Disulphide structures of highly bridged peptides: a new strategy for analysis. Protein Sci. 2, 1732-1748 (1993).
19. Blake, C.C.F., Ghosh, M., Harlos, K., Avezoux, A. & Anthony, C. The active site of methanol dehydrogenase contains a disulphide bridge between adjacent cysteine residues. Nature Struct. Biol. 1, 103-105 (1994).
20. Kao, P.N. & Karlin, A. Acetylcholine receptor binding site contains a disulphide cross-link between adjacent half-cystinyl residues. J. Biol. Chem. 261, 8085-8088 (1986).
21. Ramachandran, G.N. & Sasisekharan, V. Conformation of polypeptides and proteins. Adv. Protein. Chem. 23, 283-437 (1968).
22. Chandrasekaran, R. & Balasubramanian, R. Stereochemical studies of cyclic peptides. VI. Energy calculations of the cyclic dipeptide cysteinyl-cysteine. Biochim. Biophys. Acta 188, 1-9 (1969).
23. Capasso, S., Mattia, C., Mazzarella, L. & Puliti, R. Structure of a cis-peptide unit: molecular conformation of the cyclic disulphide L-cysteinyl-L-cysteine. Acta Crystallogr. B 33, 2080-2083 (1977).
24. Xia, Z.-X. et al. Detailed active-site configuration of a new crystal form of methanol dehydrogenase from Methylophilus W3A1 at 1.9 Å resolution. Biochemistry 38, 1214-1220 (1999).
25. Ghosh, M., Anthony, C., Harlos, K., Goodwin, M.G. & Blake, C. The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 Å. Structure 3, 177-187 (1995).
26. Gehrmann, J., Alewood, P.F. & Craik, D.J. Structure determination of the three disulfide bond isomers of α-conotoxin G1: a model for the role of disulf ide bonds in structural stability. J. Mol. Biol. 278, 401-405 (1998).
27. Fletcher, J.I., Chapman, B.E., Mackay, J.P., Howden, M.E.H. & King, G.F. The structure of versutoxin (δ-atracotoxin-Hv1) provides insights into the binding of site-3 neurotoxins to the voltage-gated sodium channel. Structure 5, 1525-1535 (1997).
28. Czajkowski, C. & Karlin, A. Structure of the nicotinic receptor acetylcholine-binding site: identification of acidic residues in the d subunit within 0.9 nm of the a subunit-binding site disulfide. J. Biol. Chem. 270, 3160-3164 (1995).
29. Holm, L. & Sander, C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138 (1993).
30. Pallaghy, P.K., Alewood, D., Alewood, PF. & Norton, R.S. Solution structure of robustoxin, the lethal neurotoxin from the funnel-web spider Atrax robustus. FEBS Lett. 419, 191-196 (1997).
31. Omecinsky, D.O., Holub, K.E., Adams, M.E. & Reily, M.D. Three-dimensional structure analysis of μ-agatoxins: further evidence for common motifs among neurotoxins with diverse ion channel specificities. Biochemistry 35, 2836-2844 (1996).
32. Hill, J.M., Alewood, P.F. & Craik, D.J. Solution structure of the sodium channel antagonist conotoxin GS: a new molecular caliper for probing sodium channel geometry. Structure 5, 571-583 (1997).
33. Kraulis, P.J. et al. Determination of the three-dimensional structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing. Biochemistry 28, 7241-7257 (1989).
34. Le-Nguyen, D., Heitz, A., Chiche, L., El Hajji, M. & Castro, B. Characteization and 2D NMR study of the stable [9-21, 15-27] 2 disulfide intermediate in the folding of the 3 disulfide trypsin inhibitor EETI II. Protein Sci. 2, 165-174 (1993).
35. Boisbouvier, J. et al. A structural homologue of colipase in black mamba venom revealed by NMR floating disulphide bridge analysis. J. Mol. Biol. 283, 205-219 (1998).
36. Lin, S.L. & Nussinov, R. A disulphide-reinforced structural scaffold shared by small proteins with diverse functions. Nature Struct. Biol. 2, 835-837 (1995).
37. Glinka, A. et al. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362 (1998).
38. Nicholson, G.M., Willow, M., Howden, M.E.H. & Narahashi, T. Modification of sodium channel gating and kinetics by versutoxin from the Australian funnel-web spider Hadronyche versuta. Pflügers Arch. (Eur. J. Pharmacol.) 428, 400-409 (1994).
39. Fletcher, J.I. et al. High-resolution solution structure of gurmarin, a sweet-taste suppressing plant polypeptide. Eur. J. Biochem. 264, 488-494 (1999).
40. Bartels, C., Xia, T-H., Billeter, M., Güntert, P. & Wüthrich, K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 5, 1-10 (1995).
41. Güntert, P., Mumenthaler, C. & Wüthrich, K. Torsion angle dyanamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298 (1997).
42. Szyperski, T., Güntert, P., Otting, G. & Wüthrich, K. Determination of scalar coupling constants by inverse Fourier transform of in-phase multiplets. J. Magn. Reson. 99, 552-560 (1992).
43. Clubb, R.T., Ferguson, S.B., Walsh, C.T. & Wagner, G. Three-dimensional solution structure of Escherichia coli periplasmic cyclophilin. Biochemistry 33, 2761-2722 (1994).
44. Ludvigsen, S. & Poulsen, F.M. Positive theta-angles in proteins by nuclear magnetic resonance spectroscopy. J. Biomol. NMR 2, 227-233 (1992).
45. Wagner, G. et al. 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 (1987).
46. Kline, A.D., Braun, W. & Wüthrich, K. 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 (1988).
47. Brünger, A.T. X-PLOR version 3.1: a system for X-ray crystallography and NMR. (Yale University Press, New Haven, Connecticut; 1992).
48. Koradi, R., Billeter, M. & Wüthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55 (1996).
49. Barton, G.J. ALSCRIPT. A tool to format multiple sequence alignments. Protein Eng. 6, 37-40 (1993).
50. van Tilbeurgh, H. et al. Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature 362, 814-820 (1993).