Crystal structures of two α-like scorpion toxins: Non-proline cis peptide bonds and implications for new binding site selectivity on the sodium channel

Journal of Molecular Biology

Volumn 292, Issue 1, 1999, Pages 125-135

  He, Xiao Lin ^a   Li, Hong Min ^a   Zeng, Zong Hao ^a   Liu, Xin Qi ^a   Wang, Miao ^a   Wang, Da Cheng ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Binding selectivity; Buthus martensii Karsch; cis peptide bond; Crystal structure; Scorpion like toxin

Indexed keywords

ALPHA TOXIN; AMINO ACID; ARGININE; PEPTIDE; SCORPION VENOM; SODIUM CHANNEL;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHEMICAL BOND; CIS ISOMER; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN TERTIARY STRUCTURE; SCORPION; TOXIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

EID: 0033543581     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3036     Document Type: Article

References (63)

1. Almassy R. J., Fonticilla-Camps J. C., Suddath F. L., Bugg C. E. Structure of variant-3 scorpion toxin from Centruroides sculpturatus Ewing, refined at 1. 8 Å resolution. J. Mol. Biol. 170:1983;497-527.
2. Babin D. R., Watt D. D., Goos S. M., Mlejnek R. V. Amino acid sequences of neurotoxic protein variants from the venom of Centruroides sculpturatus Ewing. Arch. Biochem. Biophys. 164:1974;694-706.
3. Babin D. R., Watt D. D., Goos S. M., Mlejnek R. V. Amino acid sequence of neurotoxin I from Centruroides sculpturatus Ewing. Arch. Biochem. Biophys. 166:1975;125-134.
4. Barton G. J. ALSCRIPT, a tool to format multiple sequence alignments. Protein Eng. 6:1993;37-40.
5. Bates P. A., Dokurno P., Freemont P. S., Sternberg M. J. E. Conformational analysis of the first observed non-proline cis peptide bond occurring within the complementary determining region (CDR) of an antibody. J. Mol. Biol. 284:1998;549-555.
6. 1H-NMR-derived secondary structure and overall fold of a natural anatoxin from the scorpion Androctunus australis Hector. Eur. J. Biochem. 247:1997;1118-1126.
7. Brünger A. T., Kuriyan J., Karplus M. Crystallographic R factor refinement by molecular dynamics. Science. 235:1987;458-460.
8. Catterall W. A. Binding of scorpion toxin to receptor sites associated with sodium channels in frog muscle. J. Gen. Physiol. 74:1979;357-391.
9. Catterall W. A. Neurotoxins that act on voltage-sensitive sodium channels in exitable membranes. Annu. Rev. Pharmacol. Toxicol. 20:1980;15-43.
10. Catterall W. A. Molecular properties of voltage-sensitive sodium channels. Annu. Rev. Biochem. 55:1986;953-985.
11. Catterall W. A. Molecular properties of the sodium channel: a receptor for multiple neurotoxins. Bull. Soc. Pathol. Exoc. 85:1992;481-485.
12. Acta Crystallog. sect. D. 50:1994;760-763.
13. Couraud F., Jover E., Dobois J. M., Rochat H. Two types of scorpion toxin receptor sites, one related to activation, the other to inactivation of the action potential sodium channel. Toxicon. 20:1982;9-16.
14. Darbon H., Jover E., Couraud F., Rochat H. α-Scorpion neurotoxin derivatives suitable as potential markers of sodium channel. Int. J. Pept. Protein Res. 22:1983;179-186.
15. 1H-nuclear magnetic resonance study of AaH IT, an anti-insect toxin from the scorpionAndroctonus australis Hector. Sequential resonance assignments and folding of the peptide chain. Biochemistry. 30:1991;1836-1845.
16. Delori P., Van Rietschoten J., Rochat H. Scorpion venoms and neurotoxins: an immunological study. Toxicon. 19:1981;393-407.
17. Dokurno P., Bates P. A., Band H. A., Stewart L. M. D., Lally J. M., Burchell J. M., Yaylour-Papadimitrious J., Snary D., Sterberg M. J. E., Freemont P. S. Crystal structure at 1. 95 Å resolution of the breast tumour-specific antibody SM3 complexed with its peptide epitope reveals novel hypervariable loop recognition. J. Mol. Biol. 284:1998;691-706.
18. Dufton M. J., Rochat H. Classification of scorpion toxins according to amino acid composition and sequence. J. Mol. Evol. 20:1984;120-127.
19. El Ayeb M., Bahraoui E. M., Granier C., Rochat H. Use of antibodies specific to defined regions of scorpion α-toxin to study its interaction with its receptor site on the sodium channel. Biochemistry. 25:1986;6671-6678.
20. Fontecilla-Camps J. C., Habersetzer-Rochat C., Rochat H. Orthorhombic crystals and three-dimensional structure of potent toxin II from the scorpion. Proc. Natl Acad. Sci. USA. 85:1988;7443-7447.
21. Gordon D., Martineauclaire M. F., Cestele S., Kopeyan C., Carlier E., Benkhalifa 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.
22. 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.
23. Granier C., Novotny J., Fonticilla-Camps J. C., Fourquet P., El Ayeb M., Bahraoui E. The antigentic structure of a scorpion toxin. Mol. Immunol. 26:1989;503-513.
24. Houset D., Habersetzer-Rochat C., Astier J., 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.
25. Hu R. Q., Wang M., Lin J. L., Lei K. J. Purification and partial characterization of several new neurotoxins from East-Asia scorpion. Zool. Res. Sinica. 10:1989;185-188.
26. Hutchinson E. G., Thorton J. M. A revised set of potentials for β-turn formation in proteins. Protein Sci. 3:1994;2207-2216.
27. 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.
28. Ji Y. H., Mansuelle P., Terakawa S., Kopeyan C., Yanaihara N., Xu K., Rochat H. Two neurotoxins (BmK I and BmK MII) from the venom of the scorpion Buthus martensii Karsch: purification, amino acid sequences and assessment of specific activity. Toxicon. 34:1996;987-1001.
29. Jones T. A., Zou J. Y., Cowan S. W., Kjeldgawd M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
30. Jover E., Couvand F., Rochat H. Two types of scropion neurotoxins characterized by their binding to two separate receptor sites on rat brain synaptosomes. Biocehm. Biophys. Res. Commun. 95:1980;1607-1614.
31. Kharrat R., Darbon H., Rochat H., Granier C. Structure activity relationships of scorpion α-toxins: multiple residues contribute to the interaction with receptor. Eur. J. Biochem. 181:1989;381-390.
32. Kleywegt G. J., Brünger A. T. Checking your imagination: applications of the free R value. Structure. 4:1996;897-904.
33. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots for protein structures. J. Appl. Crystallog. 24:1991;946-950.
34. Landon C., Sodano P., Cornet B., Bonmatin J.-M., Kopeyan C., Rochat H., Vovelle F. Q., 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.
35. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. PROCHECK: a program to check the sterochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
36. 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. 33:1994;2468-2475.
37. Li H. M. Studies on the structures of neurotoxins from Chinese scorpion Buthus martensii Karsch. PhD dissertation. 1995;Institute of Biophysics, Chinese Academy of Sciences.
38. Li H. M., Wang D. C., Zeng Z. H., Jin L., Hu R. Q. Crystal Structure of an acidic neurotoxin from scorpion Buthus martensii Karsch at 1.85 Å resolution. J. Mol. Biol. 261:1996;415-431.
39. Li H. M., Zhao T., Jin L. ,Wang M., Zhang Y., Wang D. C. A series of bioactivity-variant neurotoxins from scorpion Buthus martensii Karsch: purification, crystallization and crystallographic analysis. Acta. Crystallog. sect. D. 55:1999;341-344.
40. Luo M. J., Xiong Y. M., Wang M., Wang D. C., Chi C. W. Purification and sequence determination of a new neutral mammalian neurotoxin from the scorpion Buthus martensii Karsch. Toxicon. 35:1997;723-728.
41. Luzzati V. Traitment statistique des erreurs dans la determination des structures cristallines. Acta Crystallog. 5:1952;802-810.
42. Martin-Eauclaire M. F., Couraud F. Scorpion neurotoxins: effects and mechanisms. Chang L. W., Dyer R. S. Handbook of Neurotoxicology. 1995;683-716 Marcel Dekker, New York.
43. Merritt E. A., Murphy M. E. P. Raster3D version 2.0, a program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.
44. Mikou A., La Plante S. R., Guittet E., Lallemand J.-Y., Martin-Eauclaire M. F., Rochat H. Toxin III of the scorpion Androctunus australis Hector. Proton nuclear magnetic resonace assignment and secondary strucure. J. Biol. Mol. NMR. 2:1992;57-70.
45. Miranda F., Kupeyan C., Rochat H., Rochat C., Lissitzky S. Purification of animal neurotoxins: isolation and characterization of eleven neurotoxins from the venom of scorpionsAndroctnus australis Hector,Buthus occitanus tunetanus and Leiurus quinquestriatus. Eur. J. Biochem. 17:1970;477-484.
46. Navaza J. AMoRe - an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
47. Oren D. A., Froy O., Amit E., Kleinberger-Doren N., Gurevitz M., Shaanan B. An excitatory scorpion toxin with a distinct feature: an additional α helix at the C terminus and its implications for interaction with insect sodium channels. Structure. 6:1998;1095-1103.
48. Pallaghy P. K., Nielsen K. J., Craik D. J., Norton R. S. A common structural motif in incorporating a cystine knot and a triple-strand β-sheet in toxic and inhibitory polypeptides. Protein Sci. 3:1994;1833-1839.
49. Pashkov V. S., Maicorov V. N., Bystrov V. F., Hoang A. N., Volkora T. M., Grishin E. V. Solution spatial structure of long neurotoxin M9 from the scorpian Buthus eupeus by 1H-NMR spectroscopy. Biophys. Chem. 31:1988;121-131.
50. Possanni L. D. Structure of scorpion toxins. Insect, poisons, allergens and other inverbrate venoms. Tu T. Handbook of Natural Toxins. 1984;513-550 Marcel Dekker, New York.
51. Possani L. D., Martin B. M., Svendsen I., Rode G. S., Ericson B. W. Scorpion toxins from Centruroides noxius and Tityus serulatus. Primary structures and sequence comparison by metric analysis. Biochem. J. 229:1985;739-750.
52. Ramachandran G. N., Sasusekharan V. Conformation of polypeptides and proteins. Adv. Protein Chem. 23:1968;283-437.
53. Rees D. C., Lewis M., Honzatko R. B., Lipscomb W. N., Hardman K. D. Zinc enviroment and cis peptide bonds in carboxypeptidase A at 1.75 Å resolution. Proc. Natl Acad. Sci. USA. 78:1981;3408-3412.
54. Rochat H., Rochat C., Sampieri F., miranda F. The amino acid sequence of neurotoxin II of Androctonus australis Hector. Eur. J. Biochem. 28:1972;381-388.
55. Rochat H., Benard P., Couraud F. Scorpion toxins: chemistry and mode of action. Cecarelli B., Clementi F. Advances in Cytopharmacology. 1979;325-334 Raven Press, New York.
56. Sakabe N. A focusing Weissenberg camera with multi-layer-line screens for macromolecular crystallography. J. Appl. Crystallog. 16:1989;542-547.
57. Serre L., Vallee B., Bureaud N., Schoentgen F., Zelwer C. Crystal structure of the phosphatidylethanolamine-binding protein from bovine brain: a novel structural class of phospholipid-binding proteins. Structure. 6:1998;1255-1265.
58. Stewart D. E., Sarker A., Wampler J. E. Occurrence and role of cis peptide bnds in protein structures. J. Mol. Biol. 214:1990;253-260.
59. Watt D. D., Simard J. M. Neurotoxic proteins in scorpion venom. J. Toxicol. 3:1984;181-221.
60. 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.
61. Zilberberg N., Froy O., Loret E., Cestele 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.
62. Zlotkin E., Miranda F., Lissizky S. Proteins toxic to mammals and insects in scorpion venom. Toxicon. 10:1972;207-210.
63. Zlotkin E., Martinez G., Rochat H., Miranda F. A protein from scorpion venom toxic to crustaceans. Ohsaka A., Hayashi K., Sawai T. Animal, Plant and Microbial Toxins. 1976;73-80 Plenum Publishing Corporation, New York.