NMR structures and activity of a novel α-like toxin from the scorpion Leiurus quinquestriatus hebraeus

Journal of Molecular Biology

Volumn 285, Issue 4, 1999, Pages 1749-1763

  Krimm, Isabelle ^a   Gilles, Nicolas ^b   Sautière, Pierre ^c   Stankiewicz, Maria ^d,e   Pelhate, Marcel ^d   Gordon, Dalia ^b   Lancelin, Jean Marc ^a  

^a UNIVERSITÉ LYON 1   (France)

^b CEA SACLAY   (France)

^c INSTITUT PASTEUR DE LILLE   (France)

^d UNIVERSITÉ D'ANGERS   (France)

^e NICOLAUS COPERNICUS UNIVERSITY   (Poland)

Author keywords

Leiurus quinquestriatus hebraeus scorpion; NMR; Scorpion toxin; Sodium channel; Structure

Indexed keywords

SCORPION VENOM; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN; COCKROACH; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; ISOTOPE LABELING; NERVE FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RAT; SODIUM CURRENT; TOXIN STRUCTURE;

ANDROCTONUS; ANDROCTONUS AUSTRALIS HECTOR; ANIMALIA; BLATTARIA; HEXAPODA; INSECTA; LEIURUS; LEIURUS QUINQUESTRIATUS HEBRAEUS; MAMMALIA; SCORPIONES;

EID: 0033613920     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2418     Document Type: Article

References (53)

1. Bernstein F. C., Koetzle T. F., Williams G. J. B., Meyer E. F., Brice M. D., Rodgers J. R., Kennard T., Shimanouchi O., Tamusi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542.
2. Booshard R. H. Mapping of contact areas in protein-nucleic acid and protein-protein complexes by differential chemical modification. Methods Biochem. Anal. 25:1979;273-301.
3. Braunschweiler L., Ernst R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:1983;521-528.
4. 1H-NMR: a structural motif common to toxic arthropod proteins. Biochemistry. 32:1993;715-724.
5. Brünger A. T. X-PLOR Version 3.851. 1996;Yale University Press, New Haven.
6. Burley S. K., Petsko G. A. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science. 240:1985;23-28.
7. Cestèle S., Gordon D., Kopeyan C., Rochat H. Toxin III from Leiurus quinquestriatus quinquestriatus: a specific probe for receptor site 3 on insect sodium channels. Insect Biochem. Mol. Biol. 27:1997;523-528.
8. Cestèle S., Stankiewicz M., Mansuelle P., Dargent B., De Waard M., Gilles N., Pelhate M., Rochat H., Martin-Eauclaire M.-F., Gordon D. Scorpion α-like toxins, toxic to both mammals and insects, differentially interact with receptor site 3 on voltage-gated sodium channels in mammals and insects. Eur. J. Neurosci. 1998.
9. Cornet B., Bonmatin J.-M., Hetru C., Hoffman J. A., Ptak M., Vovelle F. Refined three-dimensional solution structure of insect defensin A. Structure. 3:1995;435-448.
10. Darbon H., Jover E., Couraud F., Rochat H. α-Scorpion neurotoxin derivatives suitable as potential markers of sodium channels. Preparation and characterization. Int. J. Pept. Protein Res. 22:1983;179-186.
11. 1H nuclear magnetic resonance study of AaH IT, an anti-insect toxin from the scorpionAndroctonus australis Hector. Sequential resonance assignments and folding of the polypeptide chain. Biochemistry. 30:1991;1836-1845.
12. 1H NMR spectra via two-dimensional homonuclear Hartman-Hahn spectroscopy. J. Am. Chem. Soc. 107:1985;2820-2821.
13. Efimov A. V. Standard structures in proteins. Prog. Biophys. Mol. Biol. 60:1993;201-239.
14. Eitan M., Fowler E., Herrmann R., Duval A., Pelhate M., Zlotkin E. A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: Purification, primary structure, and mode of action. Biochemistry. 29:1990;5941-5947.
15. Fontecilla-Camps J.-C., Habersetzer-Rochat C., Rochat H. Orthorhombic crystals and three-dimensional structure of the potent toxin II from the scorpion Androctonus australis Hector. Proc. Natl Acad. Sci. USA. 85:1988;7443-7447.
16. Gordon D. Sodium channels as targets for neurotoxins. Mode of action and interaction of neurotoxins with receptor sites on sodium channels. Gutman Y., Lazarowici P. Toxins and Signal Transduction. 1997;119-149 Harwood Academic Publishers.
17. Gordon D., Zlotkin E. Binding of an α scorpion toxin to insect sodium channels is not dependent on membrane potential. FEBS Letters. 315:1993;125-128.
18. Gordon D., Martin-Eauclaire M.-F., Cestèle S., Kopeyan C., Carlier E., Ben Khafifa R., Pelhate M., Rochat H. Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J. Biol. Chem. 271:1996;8034-8045.
19. Gordon D., Savarin P., Gurevitz M., Zinn-Justin S. Functional anatomy of scorpion toxins affecting sodium channels. J. Toxicol. Toxin Rev. 17:1998;131-159.
20. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110:1988;7870-7872.
21. Housset D., Habersetzer-Rochat C., Astier J.-P., Fontecilla-Camps J.-C. Crystal structure of toxin II from the scorpion Androctonus australis Hector refined at 1.3 Å resolution. J. Mol. Biol. 238:1994;88-103.
22. Hyberts S. G., Marki W., Wagner G. Stereospecific assignments of side-chain protons and characterization of torsion angles in Eglin c. Eur. J. Biochem. 164:1987;625-635.
23. Jablonsky M. J., Watt D. D., Krishna N. R. Solution structure of an old world-like neurotoxin from the venom of the new world scorpion Centruroides sculpturatus Ewing. J. Mol. Biol. 248:1995;449-458.
24. Jeener J., Meier B. H., Bachmann P., Ernst R. R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:1979;4546-4553.
25. Kopeyan C., Mansuelle P., Martin-Eauclaire M.-F., Rochat H., Miranda F. Characterization of toxin III of the scorpion Leiurusquinquestriatus quinquestriatus: a new type of α-toxin highly toxic both to mammals and insects. Nat. Toxins. 1:1993;308-312.
26. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics. 14:1996;51-55.
27. Kuszewski J., Nilges M., Brünger A. T. Sampling and efficiency of metric matrix distance geometry: a novel partial metrization algorithm. J. Biomol. NMR. 2:1992;33-56.
28. Landon C., Sodano P., Cornet B., Bonmatin J.-M., Kopeyan C., Rochat H., Vovelle F., Ptak M. Refined solution structure of the anti-mammal and anti-insect LqqIII scorpion toxin: comparison with other scorpion toxins. Proteins: Struct. Funct. Genet. 28:1997;360-374.
29. Laskowski R. A., Rullmann J. A. C., MacArthur M. W., Kaptein R., Thornton J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:1996;477-486.
30. Lebreton F., Delepierre M., Ramírez A. N., Balderas C., Possani L. D. Primary and NMR three-dimensional structure determination of a novel crustacean from the venom of the scorpionCentruroides limpidus limpidus Karsch. Biochemistry. 33:1994;11135-11149.
31. Lee W., Jablonsky M. J., Watt D. D., Krishna N. R. Proton nuclear magnetic resonance and distance geometry/simulated annealing studies on the variant-1 neurotoxin from the new world scorpion Centruroides sculpturatus Ewing. Biochemistry. 33:1994a;2468-2475.
32. Lee W., Moore C. H., Watt D. D., Krishna N. R. Solution structure of the variant-3 neurotoxin from Centruroides sculpturatus Ewing. Eur. J. Biochem. 218:1994b;89-95.
33. Li H.-M., Wang D.-C., Zeng Z.-H., Jin L., Hu R.-Q. Crystal structure of an acidic neurotoxin from scorpion Buthus martensii Karsh at 1.85 Å resolution. J. Mol. Biol. 261:1996;415-431.
34. Lima M. E., Martin-Eauclaire M.-F., Hue B., Loret E., Dinitz C. R., Rochat H. On the binding of two scorpion toxins to the central nervous system of the cockroach Periplaneta americana. Insect Biochem. 19:1989;413-422.
35. Macura S., Hyang Y., Suter D., Ernst R. R. Two-dimensional chemical exchange and cross relaxation spectroscopy of coupled nuclear spins. J. Magn. Reson. 43:1981;259-281.
36. Marion D., Ikura M., Tschudin R., Bax A. Rapid recording of 2D NMR spectra without phase cycling. Application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85:1989;393-399.
37. Mikou A., LaPlante S. R., Guittet E., Lallemand J.-Y., Martin-Eauclaire M.-F., Rochat H. Toxin III of the scorpion Androctonus australis Hector: proton nuclear magnetic resonance assignment and secondary structure. J. Biomol. NMR. 2:1992;57-70.
38. Nilges M., Clore G. M., Gronenborn A. M. Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Letters. 229:1988;317-324.
39. 1H-NMR spectroscopy. Biophys. Chem. 31:1988;121-131.
40. Pelhate M., Sattelle D. B. Pharmacological properties of insect axons: a review. J. Insect Physiol. 28:1982;889-903.
41. Piotto M., Saudek V., Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:1992;661-666.
42. Pons J. L., Malliavin T. E., Delsuc M.-A. GIFA V.4: a complete package for NMR data set processing. J. Biomol. NMR. 8:1996;445-452.
43. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:1983;479-485.
44. Sautière P., Cestèle S., Kopeyan C., Martinage A., Drobecq H., Doljansky Y., Gordon D. New toxins acting on sodium channels from the scorpion Leiurusquinquestriatus hebraeus suggest a clue to mammalianvs insect selectivity. Toxicon. 36:1998;1141-1154.
45. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. sect. A. 102:1993;241-245.
46. Tugarinov V., Kustanovitch I., Zilberberg N., Gurevitz M., Anglister J. Solution structure of a highly insecticidal recombinant scorpion α-toxin and a mutant with increased activity. Biochemistry. 36:1997;2414-2424.
47. Wagner G., Braun W., Havel T. F., Schaumann T., Go N., Wüthrich K. 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 DISMANN. J. Mol. Biol. 196:1987;611-639.
48. Wishart D. S., Sykes B. D., Richards F. M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry. 31:1992;1647-1651.
49. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;Wiley Interscience, New York.
50. Zhao B., Carson M., Ealick S. E., Bugg C. E. Structure of scorpion toxin variant-3 at 1.2 Å resolution. J. Mol. Biol. 227:1992;239-252.
51. Zilberberg N., Gordon D., Pelhate M., Adams M. E., Norris T. M., Zlotkin E., Gurevitz M. Functional expression and genetic alteration of an α scorpion neurotoxin. Biochemistry. 35:1996;10215-10222.
52. Zilberberg N., Froy O., Loret E., Cestèle S., Arad D., Gordon D., Gurevitz M. Identification of structural elements of a scorpion α-neurotoxin important for receptor site recognition. J. Biol. Chem. 272:1997;14810-14816.
53. Zlotkin E., Gordon D. Detection, purification and receptor binding assays of insect neurotoxins derived from scorpion venoms. Miller T. A., Breer H. Neurochemical Techniques in Insect Research. 1985;243-295 Springer-Verlag, Berlin.