Dual action of a dinoflagellate-derived precursor of Pacific ciguatoxins (P-CTX-4B) on voltage-dependent K+ and Na+ channels of single myelinated axons

Toxicon

Volumn 56, Issue 5, 2010, Pages 768-775

  Schlumberger, Sébastien ^a   Mattei, César ^a   Molgó, Jordi ^a   Benoit, Evelyne ^a  

^a LABORATOIRE DE NEUROBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

Author keywords

Ciguatoxin; Gambierdiscus toxicus dinoflagellate; Gambiertoxin; K+ channels; Myelinated axons; Na+ channels

Indexed keywords

CIGUATOXIN; GAMBIERTOXIN; LIDOCAINE; POTASSIUM CHANNEL; SODIUM CHANNEL; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; DINOFLAGELLATE; DOSE RESPONSE; ELECTROPHYSIOLOGY; FROG; MEMBRANE POTENTIAL; MYELINATED NERVE; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RANVIER NODE; SODIUM CONDUCTANCE; SODIUM CURRENT; STEADY STATE; VOLTAGE CLAMP;

ANIMALS; AXONS; CIGUATOXINS; DINOFLAGELLIDA; MALE; MYELIN SHEATH; POTASSIUM CHANNELS; RANA ESCULENTA; SODIUM CHANNELS;

ANURA; DINOPHYCEAE; GAMBIERDISCUS; GAMBIERDISCUS TOXICUS;

EID: 77955844292     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.06.035     Document Type: Article

References (36)

1. Benoit E., Legrand A.M. Purified ciguatoxin-induced modifications in excitability of myelinated nerve fibre. Bull. Soc. Pathol. Exot 1992, 85:497-499.
2. Benoit E., Legrand A.M. Gambiertoxin-induced modifications of the membrane potential of myelinated nerve fibres. Mem. Queensl. Mus 1994, 34:461-464.
3. Benoit E., Corbier A., Dubois J.M. Evidence for two transient sodium currents in the frog node of Ranvier. J. Physiol. Lond 1985, 361:339-360.
4. Benoit E., Legrand A.M., Dubois J.M. Effects of ciguatoxin on current and voltage clamped frog myelinated nerve fibre. Toxicon 1986, 24:357-364.
5. Benoit E., Juzans P., Legrand A.M., Molgó J. Nodal swelling produced by ciguatoxin-induced selective activation of sodium channels in myelinated nerve fibers. Neuroscience 1996, 71:1121-1131.
6. + channel toxin. J. Biol. Chem. 1984, 259:8353-8357.
7. Birinyi-Strachan L.C., Gunning S.J., Lewis R.J., Nicholson G.M. Block of voltage-gated potassium channels by Pacific ciguatoxin-1 contributes to increased neuronal excitability in rat sensory neurons. Toxicol. Appl. Pharmacol 2005, 204:175-186.
8. Cuypers E., Yanagihara A., Rainier J.D., Tytgat J. TRPV1 as a key determinant in ciguatera and neurotoxic shellfish poisoning. Biochem. Biophys. Res. Commun 2007, 361:214-217.
9. Cuypers E., Abdel-Mottaleb Y., Kopljar I., Rainier J.D., Raes A.L., Snyders D.J., Tytgat J. Gambierol, a toxin produced by the dinoflagellate Gambierdiscus toxicus, is a potent blocker of voltage-gated potassium channels. Toxicon 2008, 51:974-983.
10. Dechraoui M.Y., Naar J., Pauillac S., Legrand A.M. Ciguatoxins and brevetoxins, neurotoxic polyether compounds active on sodium channels. Toxicon 1999, 37:125-143.
11. Ghiaroni V., Sasaki M., Fuwa H., Rossini G.P., Scalera G., Yasumoto T., Pietra P., Bigiani A. Inhibition of voltage-gated potassium currents by gambierol in mouse taste cells. Toxicol. Sci. 2005, 85:657-665.
12. + currents in mouse taste cells. Chem. Senses 2006, 31:673-680.
13. 2+ signals in cultured rat myotubes. Br. J. Pharmacol 2002, 137:1055-1062.
14. Hille B. Charges and potentials at the nerve surface. Divalent ions and pH. J. Gen. Physiol 1968, 51:221-236.
15. Hogg R.C., Lewis R.J., Adams D.J. Ciguatoxin-induced oscillations in membrane potential and action potential firing in rat parasympathetic neurons. Eur. J. Neurosci 1998, 16:242-248.
16. Isbister G.K., Kiernan M.C. Neurotoxic marine poisoning. Lancet Neurol 2005, 4:219-228.
17. Kopljar I., Labro A.J., Cuypers E., Johnson H.W.B., Rainier J.D., Tytgat J., Snyders D.J. A polyether biotoxin binding site on the lipid-exposed face of the pore domain of Kv channels revealed by the marine toxin gambierol. Proc. Natl. Acad. Sci. USA 2009, 106:9896-9901.
18. Legrand A.M., Litaudon M., Genthon J.N., Bagnis R., Yasumuto T. Isolation and some properties of ciguatoxin. J. Appl. Phycol 1989, 1:183-188.
19. Lehane L., Lewis R.J. Ciguatera: recent advances but the risk remains. Int. J. Food Microbiol 2000, 61:91-125.
20. Lewis R.J., Sellin M., Poli M.A., Norton R.S., Macleod J.K., Sheil M.M. Purification and characterization of ciguatoxins from moray eel (Lycodontis javanicus, muraenidae). Toxicon 1991, 29:1115-1127.
21. + channel. FEBS Lett. 1987, 219:355-359.
22. Mattei C., Benoit E., Juzans P., Legrand A.M., Molgó J. Gambiertoxin (CTX-4B), purified from wild Gambierdiscus toxicus dinoflagellates, induces Na+-dependent swelling of single frog myelinated axons and motor nerve terminals in situ. Neurosci. Lett. 1997, 234:75-78.
23. Mattei C., Molgó J., Marquais M., Vernoux J., Benoit E. Hyperosmolar d-mannitol reverses the increased membrane excitability and the nodal swelling caused by Caribbean ciguatoxin-1 in single frog myelinated axons. Brain Res. 1999, 847:50-58.
24. Mattei C., Wen P.J., Nguyen-Huu T.D., Alvarez M., Benoit E., Bourdelais A.J., Lewis R.J., Baden D.G., Molgó J., Meunier F.A. Brevenal inhibits Pacific ciguatoxin-1B-induced neurosecretion from bovine chromaffin cells. PloS ONE 2008, 3(10):e3448. 10.1371/journal.pone.0003448.
25. Molgó J., Benoit E., Comella J.X., Legrand A.M. Ciguatoxin: a tool for research on sodium-dependent mechanisms. Methods in Neurosciences: Neurotoxins 1992, Vol. 8:149-164. Academic Press, New York. P.M. Conn (Ed.).
26. Murata M., Legrand A.M., Ishibashi Y., Yasumoto T. Structures of ciguatoxin and its congener. J. Am. Chem. Soc. 1989, 111:8929-8931.
27. Murata M., Legrand A.M., Ishibashi Y., Fukui M., Yasumuto T. Structures and configurations of ciguatoxin from the moray eel Gymnothorax javanicus and its likely precursor from the dinoflagellate Gambierdiscus toxicus. J. Am. Chem. Soc. 1990, 112:4380-4386.
28. Neumcke B., Stämpfli R. Heterogeneity of external surface charges near sodium channels in the nodal membrane of frog nerve. Pflügers Arch. 1984, 401:125-131.
29. Nicholson G.M., Lewis R.J. Ciguatoxins: cyclic polyether modulators of voltage-gated ion channel function. Mar. Drugs 2006, 4:82-118.
30. Nonner W. A new voltage clamp method for Ranvier nodes. Pflügers Arch. 1969, 309:176-192.
31. Paternostre M., Pichon Y. Effects of N-alcohols on potassium conductance in squid giant axons. Eur. Biophys. J 1987, 14:279-288.
32. Sauviat M.P., Boydron-Le Garrec R., Masson J.B., Lewis R.L., Vernoux J.P., Molgó J., Laurent D., Benoit E. Mechanisms involved in the swelling of erythrocytes caused by Pacific and Caribbean ciguatoxins. Blood Cells Mol. Dis 2006, 36:1-9.
33. Stämpfli R., Hille B. Electrophysiology of the peripheral myelinated nerve. Handbook of Frog Neurobiology 1976, 3-32. Springer, Heidelberg. R. Llinas, W. Precht (Eds.).
34. Strachan L.C., Lewis R.J., Nicholson G.M. Differential actions of Pacific ciguatoxin-1 on sodium channel subtypes in mammalian sensory neurons. J. Pharmacol. Exp. Ther 1999, 288:379-388.
35. Swift A.E.B., Swift T.R. Ciguatera. J. Toxicol. Clin. Toxicol 1993, 31:1-29.
36. Yamaoka K., Inoue M., Miyahara H., Miyazaki K., Hirama M. A quantitative and comparative study of the effects of a synthetic ciguatoxin CTX3C on the kinetic properties of voltage-dependent sodium channels. Br. J. Pharmacol 2004, 142:879-889.