Advertisement

Effects of Goniopora toxin on the membrane currents of bullfrog atrial muscle

  • Mami Noda
  • Ikunobu Muramatsu
  • Motohatsu Fujiwara
Article

Summary

The effects of Goniopora toxin (GPT), isolated from the Goniopora species, on the action potential and membrane currents of bullfrog atrial muscle were studied using the double sucrose-gap method. GPT at concentrations above 10 nmol/l prolonged the duration of the action potential and sometimes induced arrhythmias. The prolongation was also induced in the presence of Ca channel blockers (Mn or verapamil). These effects were not reversed by continuous superfusion of GPT-free solution, but were rapidly antagonized by tetrodotoxin (1 μmol/l). The resting potential was not affected by GPT. Voltage clamp experiments revealed that sustained inward current flows following the fast sodium current upon depolarization, in the presence of GPT. The current was elicited by the toxin in Mn-treated fibers and abolished in the presence of TTX. The delayed outward current (Ix) was slightly reduced; the background K current (IK1), inward background current (Ib) and slow inward current (Islow) were not altered by GPT. These results suggest that GPT acts on sodium channels to give rise to a prolonged sodium current which is in turn responsible for the prolongation of the action potential.

Key words

Frog atria Sucrose-gap voltage clamp Goniopora toxin Sodium channel 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alsen C, Béress L, Fischer K, Proppe D, Reinberg T, Sattler RW (1976) The action of a toxin from the sea anemone Anemonia sulcata upon mammalian heart muscles. Naunyn-Schmiedeberg's Arch Pharmacol 295:55–62Google Scholar
  2. Beeler GW Jr, Reuter H (1970) Voltage clamp experiments on ventricular myocardial fibres. J Physiol 207:165–190Google Scholar
  3. Benninger C, Einwächter HM, Haas HG, Kern R (1976) Calcium-sodium antagonism on the frog's heart: a voltage-clamp study. J Physiol 259:617–645Google Scholar
  4. Brown BF, Clark A, Noble SJ (1976a) Analysis of pace-maker and repolarization currents in frog atrial muscle. J Physiol 258:547–577Google Scholar
  5. Brown HF, Noble D, Noble SJ (1976b) The influence of nonuniformity on the analysis of potassium currents in heart muscle. J Physiol 258:615–629Google Scholar
  6. Chapman RA, Ellis D (1977) The effects of manganese ions on the contraction of the frog's heart. J Physiol 272:331–354Google Scholar
  7. Cohen IS, Falk RT, Mulrine NK (1983) Actions of barium and rubidium on membrane currents in canine purkinje fibres. J Physiol 338:580–612Google Scholar
  8. DiFrancesco D (1981) A new interpretation of the pace-maker current in calf purkinje fibres. J Physiol 314:359–376Google Scholar
  9. Einwächter HM, Haas HG, Kern R (1972) Membrane current and contraction in frog atrial fibres. J Physiol 227:141–171Google Scholar
  10. Fujiwara M, Muramatsu I, Hidaka H, Ikushima S, Ashida K (1979) Effects of goniopora toxin, a polypeptide isolated from coral, on electromechanical properties of rabbit myocardium. J Pharmacol Exp Ther 210(2):153–157Google Scholar
  11. Fujiwara M, Hong S-C, Muramatsu I (1982) Effects of goniopora toxin on non-adrenergic, non-cholinergic response and purine nucleotide release in guinea-pig taenia coli. J Physiol 326:515–526Google Scholar
  12. Gillespie JI, Meves H (1980) The effect of scorpion venoms on the sodium currents of the squid giant axon. J Physiol 308:479–499Google Scholar
  13. Goto M, Tsuda Y, Yatani A, Saito M (1978) Effects of low temperature on the membrane currents and tension components of bulllfrog atrial muscle. Jpn J Physiol 28:211–224Google Scholar
  14. Haas HG, Kern R, Einwächter HM, Tarr M (1971) Kinetics of Na inactivation in frog atria. Pflügers Arch 323:141–157Google Scholar
  15. Hashimoto K, Ochi R, Hashimoto K, Miura Y (1980) The ionic mechanism of prolongation of action potential duration of cardiac ventricular muscle by anthopleurin-A and its relationship to the inotropic effect. J Pharmacol Exp Ther 215: 479–485Google Scholar
  16. Hashimoto Y, Ashida K (1973) Screening of toxic corals and isolation of a toxic polypeptide from Goniopora spp. In: Proceedings of the Second International Symposium on Cnidaria. Publ Seto Mar Biol Lab 20:703–711Google Scholar
  17. Hemptinne A De (1976) Voltage clamp analysis in isolated cardiac fibres as performed with two different perfusion chambers for double sucrose gap. Pflügers Arch 363:87–95Google Scholar
  18. Hermsmeyer K, Sperelakis N (1970) Decrease in K conductance and depolarization of frog cardiac muscle produced by Ba2+. Am J Physiol 219 (4):1108–1114Google Scholar
  19. Honerjäger P (1982) Cardioactive substances that prolong the open state of sodium channels. Rev Physiol Biochem Pharmacol 92:1–74Google Scholar
  20. Horackova M, Vassort G (1979) Na−Ca exchange in regulation of cardiac contractility: evidence for electrogenic voltage-dependent mechanism. J Gen Physiol 73:403–424Google Scholar
  21. Hume JR, Giles W (1981) Active and passive electrical properties of single bullfrog atrial cells. J Gen Physiol 78:19–42Google Scholar
  22. Ikushima S, Muramatsu I, Fujiwara M, Ashida K (1981) Relationship between the effects of goniopora toxin on action potential and on contractile force in guinea-pig papillary muscle. Jpn J Pharmacol 31:1051–1060Google Scholar
  23. Johnson EA, Lieberman M (1971) Heart: excitation and contraction. Annu Rev Physiol 33:479–532Google Scholar
  24. Julian FJ, Moore JW, Goldman DE (1982) Membrane potentials of the lobster giant axon obtained by use of the sucrose-gap technique. J Gen Physiol 45:1195–1216Google Scholar
  25. Kohlhardt M, Bauer B, Krause H, Fleckenstein A (1973) Selective inhibition of the transmembrane Ca conductivity of mammalian myocardial fibres by Ni, Co and Mn ions. Pflügers Arch 336:115–123Google Scholar
  26. Kohlhardt M, Haap K (1980) On the mechanism underlying the cobalt-induced inhibition of slow inward current in mammalian ventricular myocardium. J Mol Cell Cardiol 12:1075–1090Google Scholar
  27. Kootsey JM, Johnson EA (1972) Voltage clamp of cardiac muscle. A theoretical analysis of early currents in the single sucrose gap. Biophys J 12:1496–1508Google Scholar
  28. McGuigan JAS (1974) Some limitations of the double sucrose gap, and its use in a study of the slow outward current in mammalian ventricular muscle. J Physiol 240:775–806Google Scholar
  29. Muramatsu I, Fujiwara M, Ikushima S, Ashida K (1980) Effects of goniopora toxin on guinea-pig blood vessels. Naunyn-Schmiedeberg's Arch Pharmacol 312:193–197Google Scholar
  30. Muramatsu I, Fujiwara M, Narahashi T (1981) Effects of goniopora toxin, a polypeptide isolated from coral on crayfish giant axon. Eighth International Congress of Pharmacology, Tokyo, p 318 (Abstract)Google Scholar
  31. Page SG, Niedergerke R (1972) Structure of physiological interest in frog heart ventricle. J Cell Sci 11:179–203Google Scholar
  32. Ramon R, Anderson N, Jayner RW, Moore JW (1975) Axon voltage-clamp simulations. IV. A multicellular preparation. Biophys J 15:55–69Google Scholar
  33. Rathmayer W, Béress L (1976) The effect of toxins from Anemonia sulcata (Coelenterata) on neuromuscular transmission and nerve action potentials in the crayfish (Astacus leptodactylus). J Comp Physiol 109:373–382Google Scholar
  34. Ravens U (1976) Electromechanical studies of an Anemonia sulcata toxin in mammalian cardiac muscle. Naunyn-Schmiedebergs's Arch Pharmacol 296:73–78Google Scholar
  35. Romey G, Chicheportiche R, Lazdunski M, Rochat H, Miranda F, Lissitzky S (1965) Scorpion neurotoxin — a presynaptic toxin which affects both Na+ and K+ channels in axons. Biochem Biophys Res Commun 64:115–121Google Scholar
  36. Romey G, Abita JP, Schweitz H, Wunderer G, Lazdunski M (1976) Sea anemone toxin: a tool to study molecular mechanisms of nerve conduction and excitation-secretion coupling. Proc Natl Acad Sci USA 73:4055–4059Google Scholar
  37. Rougier O, Vassort G, Stämpfli R (1968) Voltage clamp experiments on frog atrial heart muscle fibres with the sucrose gap technique. Pflügers Arch 301:91–108Google Scholar
  38. Rougier O, Vassort G, Garnier D, Gargouil YM, Corabocuf E (1969) Existencce and role of a slow inward current during the frog atrial action potential. Pflügers Arch 308:91–110Google Scholar
  39. Tarr M, Trank JW (1974) An assessment of the double sucrosegap voltage clamp technique as applied to frog atrial muscle. Biophys J 14:627–643Google Scholar
  40. Tsuda Y (1979) The nature of the initial positive inotropic effect of K depletion in bullfrog atrial muscle. Jpn J Physiol 29:103–117Google Scholar
  41. Vassort G, Rougier O (1972) Membrane potential and slow inward current dependence of frog cardiac mechanical activity. Pflügers Arch 331:191–203Google Scholar
  42. Warashina A, Fujita S (1983) Effect of sea anemone toxins on the sodium inactivation process in crayfish axons. J Gen Physiol 81:305–323Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • Mami Noda
    • 1
  • Ikunobu Muramatsu
    • 2
  • Motohatsu Fujiwara
    • 1
  1. 1.Department of Pharmacology, Eaculty of MedicineKyoto UniversityKyotoJapan
  2. 2.Department of PharmacologyFukui Medical SchoolFukuiJapan

Personalised recommendations