Differential effects of five 'classical' scorpion β-toxins on rNav1.2a and DmNav1 provide clues on species-selectivity

Toxicology and Applied Pharmacology

Volumn 218, Issue 1, 2007, Pages 45-51

  Bosmans, Frank ^a   Martin Eauclaire, Marie France ^b   Tytgat, Jan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b CNRS   (France)

Author keywords

Androctonus australis Hector; Centruroides suffusus suffusus; Scorpion toxins; Species selectivity; Voltage activated Na+ channels

Indexed keywords

SCORPION VENOM; TOXIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL DMNAV1; VOLTAGE GATED SODIUM CHANNEL RNAV1.2A;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BRAIN SYNAPTOSOME; CLASSIFICATION; COCKROACH; CONTROLLED STUDY; ELECTRODE; HETEROLOGOUS EXPRESSION; INVERTEBRATE; MAGGOT; MEASUREMENT; MOLECULAR CLONING; NONHUMAN; PROTEIN BINDING; RAT; SODIUM CURRENT; SPECIES DIFFERENCE; VERTEBRATE; VOLTAGE CLAMP; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; BRAIN; FEMALE; INSECT PROTEINS; MEMBRANE POTENTIALS; MICROINJECTIONS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROTOXINS; OOCYTES; PATCH-CLAMP TECHNIQUES; RATS; SCORPION VENOMS; SODIUM CHANNELS; SPECIES SPECIFICITY; SYNAPTOSOMES; TERMINOLOGY; XENOPUS LAEVIS;

ANDROCTONUS AUSTRALIS HECTOR; BLATTARIA; CENTRUROIDES SUFFUSUS SUFFUSUS; INVERTEBRATA; MUS; RATTUS; SCORPIONES; VERTEBRATA; XENOPUS LAEVIS;

EID: 33845971895     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2006.10.009     Document Type: Article

References (43)

1. Auld V.J., Goldin A.L., Krafte D.S., Marshall J., Dunn J.M., Catterall W.A., Lester H.A., Davidson N., and Dunn R.J. A rat brain Na+ channel alpha subunit with novel gating properties. Neuron 1 (1988) 449-461
2. Bechis G., Sampieri F., Yuan P.M., Brando T., Martin M.F., Diniz C.R., and Rochat H. Amino acid sequence of toxin VII, a beta-toxin from the venom of the scorpion Tityus serrulatus. Biochem. Biophys. Res. Commun. 122 (1984) 1146-1153
3. Borges A., Alfonzo M.J., Garcia C.C., Winand N.J., Leipold E., and Heinemann S.H. Isolation, molecular cloning and functional characterization of a novel beta-toxin from the Venezuelan scorpion, Tityus zulianus. Toxicon 43 (2004) 671-684
4. Cahalan M.D. Modification of sodium channel gating in frog myelinated nerve fibres by Centruroides sculpturatus scorpion venom. J. Physiol. 244 (1975) 511-534
5. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26 (2000) 13-25
6. Catterall W.A., Goldin A.L., and Waxman S.G. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 57 (2005) 397-409
7. Ceard B., De Lima M.E., Bougis P.E., and Martin-Eauclaire M.F. Purification of the main beta-toxin from Tityus serrulatus scorpion venom using high-performance liquid chromatography. Toxicon 30 (1992) 105-110
8. Cestele S., and Catterall W.A. Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82 (2000) 883-892
9. Cestele S., Qu Y., Rogers J.C., Rochat H., Scheuer T., and Catterall W.A. Voltage sensor-trapping: enhanced activation of sodium channels by beta-scorpion toxin bound to the S3-S4 loop in domain II. Neuron 21 (1998) 919-931
10. Cestele S., Scheuer T., Mantegazza M., Rochat H., and Catterall W.A. Neutralization of gating charges in domain II of the sodium channel alpha subunit enhances voltage-sensor trapping by a beta-scorpion toxin. J. Gen. Physiol. 118 (2001) 291-302
11. Cohen L., Karbat I., Gilles N., Froy O., Corzo G., Angelovici R., Gordon D., and Gurevitz M. Dissection of the functional surface of an anti-insect excitatory toxin illuminates a putative "hot spot" common to all scorpion beta-toxins affecting Na+ channels. J. Biol. Chem. 279 (2004) 8206-8211
12. Cohen L., Karbat I., Gilles N., Ilan N., Benveniste M., Gordon D., and Gurevitz M. Common features in the functional surface of scorpion beta-toxins and elements that confer specificity for insect and mammalian voltage-gated sodium channels. J. Biol. Chem. 280 (2005) 5045-5053
13. Couraud F., Jover E., Dubois J.M., and Rochat H. Two types of scorpion receptor sites, one related to the activation, the other to the inactivation of the action potential sodium channel. Toxicon 20 (1982) 9-16
14. De Lima M.E., Martin M.F., Diniz C.R., and Rochat H. Tityus serrulatus toxin VII bears pharmacological properties of both beta-toxin and insect toxin from scorpion venoms. Biochem. Biophys. Res. Commun. 139 (1986) 296-302
15. De Lima M.E., Martin-Eauclaire M.F., Hue B., Loret E., Diniz C.R., and 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
16. del Rio-Portilla F., Hernandez-Marin E., Pimienta G., Coronas F.V., Zamudio F.Z., Rodriguez de la Vega R.C., Wanke E., and Possani L.D. NMR solution structure of Cn12, a novel peptide from the Mexican scorpion Centruroides noxius with a typical beta-toxin sequence but with alpha-like physiological activity. Eur. J. Biochem. 271 (2004) 2504-2516
17. Feng G., Deak P., Chopra M., and Hall L.M. Cloning and functional analysis of TipE, a novel membrane protein that enhances Drosophila para sodium channel function. Cell 82 (1995) 1001-1011
18. French R.J., and Terlau H. Sodium channel toxins-receptor targeting and therapeutic potential. Curr. Med. Chem. 11 (2004) 3053-3064
19. Froy O., and Gurevitz M. New insight on scorpion divergence inferred from comparative analysis of toxin structure, pharmacology and distribution. Toxicon 42 (2003) 549-555
20. Froy O., Zilberberg N., Gordon D., Turkov M., Gilles N., Stankiewicz M., Pelhate M., Loret E., Oren D.A., Shaanan B., and Gurevitz M. The putative bioactive surface of insect-selective scorpion excitatory neurotoxins. J. Biol. Chem. 274 (1999) 5769-5776
21. Gordon D., Martin-Eauclaire M.F., Cestele S., Kopeyan C., Carlier E., Khalifa R.B., Pelhate M., and 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., and Zinn-Justin S. Functional anatomy of scorpion toxins affecting sodium channels. J. Toxicol., Toxin. Rev. 17 (1998) 131-159
23. Gordon D., Ilan N., Zilberberg N., Gilles N., Urbach D., Cohen L., Karbat I., Froy O., Gaathon A., Kallen R.G., Benveniste M., and Gurevitz M. An 'Old World' scorpion beta-toxin that recognizes both insect and mammalian sodium channels. Eur. J. Biochem. 270 (2003) 2663-2670
24. Gurevitz M., Gordon D., Ben-Natan S., Turkov M., and Froy O. Diversification of neurotoxins by C-tail 'wiggling': a scorpion recipe for survival. FASEB J. 15 (2001) 1201-1205
25. Hassani O., Mansuelle P., Cestele S., Bourdeaux M., Rochat H., and Sampieri F. Role of lysine and tryptophan residues in the biological activity of toxin VII (Ts gamma) from the scorpion Tityus serrulatus. Eur. J. Biochem. 260 (1999) 76-86
26. Isom L.L., De Jongh K.S., Patton D.E., Reber B.F., Offord J., Charbonneau H., Walsh K., Goldin A.L., and Catterall W.A. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 256 (1992) 839-842
27. Karbat I., Cohen L., Gilles N., Gordon D., and Gurevitz M. Conversion of a scorpion toxin agonist into an antagonist highlights an acidic residue involved in voltage sensor trapping during activation of neuronal Na+ channels. FASEB J. 18 (2004) 683-689
28. Legros C., Ceard B., Vacher H., Marchot P., Bougis P.E., and Martin-Eauclaire M.F. Expression of the standard scorpion alpha-toxin AaH II and AaH II mutants leading to the identification of some key bioactive elements. Biochim. Biophys. Acta 1723 (2005) 91-99
29. Mantegazza M., and Cestele S. Beta-scorpion toxin effects suggest electrostatic interactions in domain II of voltage-dependent sodium channels. J. Physiol. 568 (2005) 13-30
30. Martin M.F., Garcia y Perez L.G., el Ayeb M., Kopeyan C., Bechis G., Jover E., and Rochat H. Purification and chemical and biological characterizations of seven toxins from the Mexican scorpion, Centruroides suffusus suffusus. J. Biol. Chem. 262 (1987) 4452-4459
31. Martin-Eauclaire M.F., Ceard B., Bosmans F., Rosso J.P., Tytgat J., and Bougis P.E. New "Birtoxin analogs" from Androctonus australis venom. Biochem. Biophys. Res. Commun. 333 (2005) 524-530
32. Mejri T., Borchani L., Srairi-Abid N., Benkhalifa R., Cestele S., Regaya I., Karoui H., Pelhate M., Rochat H., and El Ayeb M. BotIT6: a potent depressant insect toxin from Buthus occitanus tunetanus venom. Toxicon 41 (2003) 163-171
33. Moskowitz H., Herrmann R., Jones A.D., and Hammock B.D. A depressant insect-selective toxin analog from the venom of the scorpion Leiurus quinquestriatus hebraeus-purification and structure/function characterization. Eur. J. Biochem. 254 (1998) 44-49
34. Noda M., Ikeda T., Kayano T., Suzuki H., Takeshima H., Kurasaki M., Takahashi H., and Numa S. Existence of distinct sodium channel messenger RNAs in rat brain. Nature 320 (1986) 188-192
35. Pelhate M., and Zlotkin E. Actions of insect toxin and other toxins derived from the venom of the scorpion Androctonus australis on isolated giant axons of the cockroach (Periplaneta americana). J. Exp. Biol. 97 (1982) 67-77
36. Possani L.D., Becerril B., Delepierre M., and Tytgat J. Scorpion toxins specific for Na+-channels. Eur. J. Biochem. 264 (1999) 287-300
37. Schiavon E., Sacco T., Cassulini R.R., Currola G., Tempia F., Possani L.D., and Wanke E. Resurgent current and voltage sensor trapping enhanced activation by a beta-scorpion toxin solely in Nav1.6 channel. Significance in mice Purkinje neurons. J. Biol. Chem. 281 29 (2006) 20326-20337
38. Warmke J.W., Reenan R.A., Wang P., Qian S., Arena J.P., Wang J., Wunderler D., Liu K., Kaczorowski G.J., Van der Ploeg L.H., Ganetzky B., and Cohen C.J. Functional expression of Drosophila para sodium channels. Modulation by the membrane protein TipE and toxin pharmacology. J. Gen. Physiol. 110 (1997) 119-133
39. Ye X., Bosmans F., Li C., Zhang Y., Wang D.C., and Tytgat J. Structural basis for the voltage-gated Na+ channel selectivity of the scorpion alpha-like toxin BmK M1. J. Mol. Biol. 353 (2005) 788-803
40. Yu F.H., Westenbroek R.E., Silos-Santiago I., McCormick K.A., Lawson D., Ge P., Ferriera H., Lilly J., DiStefano P.S., Catterall W.A., Scheuer T., and Curtis R. Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2. J. Neurosci. 23 (2003) 7577-7585
41. Zlotkin E., Kadouri D., Gordon D., Pelhate M., Martin M.F., and Rochat H. An excitatory and a depressant insect toxin from scorpion venom both affect sodium conductance and possess a common binding site. Arch. Biochem. Biophys. 240 (1985) 877-887
42. Zlotkin E., Eitan M., Bindokas V.P., Adams M.E., Moyer M., Burkhart W., and Fowler E. Functional duality and structural uniqueness of depressant insect-selective neurotoxins. Biochemistry 30 (1991) 4814-4821
43. Zuo X.P., He H.Q., He M., Liu Z.R., Xu Q., Ye J.G., and Ji Y.H. Comparative pharmacology and cloning of two novel arachnid sodium channels: exploring the adaptive insensitivity of scorpion to its toxins. FEBS Lett. 580 (2006) 4508-4514