Tetrodotoxin-resistant sodium channels
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1. Tetrodotoxin (TTX) has been widely used as a chemical tool for blocking Na+ channels. However, reports are accumulating that some Na+ channels are resistant to TTX in various tissues and in different animal species. Studying the sensitivity of Na+ channels to TTX may provide us with an insight into the evolution of Na+ channels.
2. Na+ channels present in TTX-carrying animals such as pufferfish and some types of shellfish, frogs, salamanders, octopuses, etc., are resistant to TTX.
3. Denervation converts TTX-sensitive Na+ channels to TTX-resistant ones in skeletal muscle cells, i.e., reverting-back phenomenon. Also, undifferentiated skeletal muscle cells contain TTX-resistant Na+ channels. Cardiac muscle cells and some types of smooth muscle cells are considerably insensitive to TTX.
4. TTX-resistant Na+ channels have been found in cell bodies of many peripheral nervous system (PNS) neurons in both immature and mature animals. However, TTX-resistant Na+ channels have been reported in only a few types of central nervous system (CNS). Axons of PNS and CNS neurons are sensitive to TTX. However, some glial cells have TTX-resistant Na+ channels.
5. Properties of TTX-sensitive and TTX-resistant Na+ channels are different. Like Ca2+ channels, TTX-resistant Na+ channels can be blocked by inorganic (Co2+, Mn2+, Ni2+, Cd2+, Zn2+, La3+) and organic (D-600) Ca2+ channel blockers. Usually, TTX-resistant Na+ channels show smaller single-channel conductance, slower kinetics, and a more positive current-voltage relation than TTX-sensitive ones.
6. Molecular aspects of the TTX-resistant Na+ channel have been described. The structure of the channel has been revealed, and changing its amino acid(s) alters the sensitivity of the Na+ channel to TTX.
7. TTX-sensitive Na+ channels seem to be used preferentially in differentiated cells and in higher animals instead of TTX-resistant Na+ channels for rapid and effective processing of information.
8. Possible evolution courses for Na+ and Ca2+ channels are discussed with regard to ontogenesis and phylogenesis.
Key wordstetrodotoxin Na+ channels neurons muscles development
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- Akaike, N., and Takahashi, K. (1992). Tetrodotoxin-sensitive calcium-conducting channels in the rat hippocampal CA1 region.J Physiol. (Lond.) 450:529–546.Google Scholar
- Baccaglini, P., and Cooper, E. (1982). Electrophysiological studies of new-born rat nodose neurones in cell culture.J. Physiol. (Lond.) 324:429–439.Google Scholar
- Benoit, E., Corbier, A., and Dubois, J. M. (1985). Evidence for two transient sodium currents in the frog node of Ranvier.J. Physiol. (Lond.) 361:339–360.Google Scholar
- Bevan, S., Chiu, S. Y., Gray, P. T. A., and Ritchie, J. M. (1985). The presence of voltage-gated sodium, potassium and chloride channels in rat cultured astrocytes.Proc. R. Soc. London Ser. B 225:299–313.Google Scholar
- Brown, A. M., Lee, K. S., and Powell, T. (1981). Sodium current in single rat heart muscle cells.J. Physiol. (Lond.) 318:479–500.Google Scholar
- Campbell, D. T. (1993). Single-channel current/voltage relationships of two kinds of Na+ channel in vertebrate sensory neurons.Pflügers Arch. 423:492–496.Google Scholar
- Chiu, S. Y. (1987). Sodium currents in axon-associated Schwann cells from adult rabbits.J. Physiol. (Lond.) 386:181–203.Google Scholar
- Clark, R. B., Tse, A., and Giles, W. R. (1990). Electrophysiology of parasympathetic neurones isolated from the interatrial septum of bull-frog heart.J. Physiol. (Lond.) 427:89–125.Google Scholar
- Cook, J. (1777).A Voyage Towards the South Pole and Around the World, Vol. 2, Straham and Cadell, London, pp. 112–113.Google Scholar
- Dichter, M. A., and Fischbach, G. D. (1977). The action potential of chick dorsal root ganglion neurones maintained in cell culture.J. Physiol. (Lond.) 267:281–298.Google Scholar
- Elliott, A. A., and Elliott, J. R. (1993). Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia.J. Physiol. (Lond.) 463:39–56.Google Scholar
- Flamm, R. E., Birnberg, N. C., and Kaczmarek, L. K. (1990). Transfection of activated ras into an excitable cell line (AtT-20) alters tetrodotoxin sensitivity of voltage-dependent sodium current.Pflügers Arch. 416:120–125.Google Scholar
- Gallego, R. (1983). The ionic basis of action potentials in petrosal ganglion cells of the cat.J. Physiol. (Lond.) 342:591–602.Google Scholar
- Hagiwara, S., and Takahashi, K. (1967). Resting and spike potentials of skeletal muscle fibres of salt-water elasmobranch and teleost fish.J. Physiol. (Lond.) 190:499–518.Google Scholar
- Halstead, B. W. (1967).Poisonous and Venomous Marine Animals of the World, U.S. Government Printing Office, Washington, DC, VolI, pp. 83–87, Vol. II, pp. 679–844.Google Scholar
- Harper, A. A., and Lawson, S. N. (1985a). Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones.J. Physiol. (Lond.) 359:31–46.Google Scholar
- Harper, A. A., and Lawson, S. N. (1985b). Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities.J. Physiol. (Lond.) 359:47–63.Google Scholar
- Hille, B. (1992).Ionic Channels of Excitable Membranes, Sinauer Associates, Sunderland, MA.Google Scholar
- Ikeda, S. R., and Schofield, G. G. (1987). Tetrodotoxin-resistant sodium current of rat nodose neurones: monovalent cation selectivity and divalent cation block.J. Physiol. (Lond.) 389:255–270.Google Scholar
- Jones, S. W. (1987). Sodium currents in dissociated bull-frog sympathetic neurones.J. Physiol. (Lond.) 389:605–627.Google Scholar
- Kao, C. Y., and Fuhrman, F. A. (1963). Pharmacological studies on tarichatoxin, a potent neurotoxin.J. Pharmacol. Exp. Ther. 140:31–40.Google Scholar
- Kao, C. Y., and Levinson, S. R. (Eds.) (1986).Tetrodotoxin, Saxitoxin, and the Molecular Biology of the Sodium Channel, Ann. N.Y. Acad. Sci. Vol. 479.Google Scholar
- Kidokoro, Y. (1973). Development of action potentials in a clonal rat skeletal muscle cell line.Nature 241:158–159.Google Scholar
- Kidokoro, Y. (1975). Sodium and calcium components of the action potential in a developing skeletal muscle cell line.J. Physiol. (Lond.) 244:145–159.Google Scholar
- Kidokoro, Y., Grinnell, A. D., and Eaton, D. C. (1974). Tetrodotoxin sensitivity of muscle action potentials in pufferfishes and related fishes.J. Comp. Physiol. 89:59–72.Google Scholar
- Kostyuk, P. G., Pronchuk, N., Savchenko, A., and Verkhratsky, A. (1993). Calcium currents in aged rat dorsal root ganglion neurones.J. Physiol. (Lond.) 461:467–483.Google Scholar
- Mitani, S. (1985). The reduction of calcium current associated with early differentiation of the murine embryo.J. Physiol. (Lond.) 363:71–86.Google Scholar
- Miyazaki, S., Takahashi, K., and Tsuda, J. (1974). Electrical excitability in the egg cell membrane of the tunicate.J. Physiol. (Lond.) 238:37–54.Google Scholar
- Miyazaki, S., Ohmori, H., and Sasaki, S. (1975). Action potential and non-linear current-voltage relation in starfish oocytes.J. Physiol. (Lond.) 246:37–54.Google Scholar
- Mosher, H. S., and Fuhrman, F. A. (1984). Occurrence and origin of tetrodotoxin. InSeafood Toxins, (E. P. Ragelis, Ed.), American Chemical Society Symposium 262, pp. 333–344.Google Scholar
- Muraki, K., Imaizumi, Y., and Watanabe, M. (1991). Sodium currents in smooth muscle cells freshly isolated from stomach fundus of the rat and ureter of the guinea-pig.J. Physiol. (Lond.) 442:351–375.Google Scholar
- Noda, M., Shimizu, S., Tanabe, T., Takai, T., Kayano, T., Ikeda, T., Takahashi, H., Nakayama, H., Kanaoka, Y., Minamino, N., Kanagawa, K., Matsuo, H., Raftery, M. A., Hirose, T., Inayama, S., Hayashida, H., Miyata, T., and Numa, S. (1984). Primary structure ofElectrophorus electricus sodium channel deduced from cDNA sequence.Nature 312:121–127.PubMedGoogle Scholar
- Numa, S. (1989). A molecular view of neurotransmitter receptors and ionic channels.Harvey Lect. 83:121–165.Google Scholar
- Ogata, N., and Tatebayashi, H. (1992a). Ontogenic development of the TTX-sensitive and TTX-insensitive Na+ channels in neurons of the rat dorsal root ganglia.Dev. Brain Res. 65:93–100.Google Scholar
- Ogata, N., and Tatebayashi, H. (1993). Kinetic analysis of two types of Na+ channels in rat dorsal root ganglia.J. Physiol. (Lond.) 466:9–37.Google Scholar
- Okamoto, H., Takahashi, K., and Yoshii, M. (1976). Membrane currents of the tunicate egg under the voltage-clamp condition.J. Physiol. (Lond.) 254:607–638.Google Scholar
- Okamoto, H., Takahashi, K., and Yamashita, N. (1977). Ionic currents through the membrane of the mammalian oocytes and their comparison with those in the tunicate and sea urchin.J. Physiol. (Lond.) 267:465–495.Google Scholar
- Okamura, Y., and Shidara, M. (1990). Changes in sodium channels during neural differentiation in the isolated blastomere of the ascidian embryo.J. Physiol. (Lond.) 431:39–74.Google Scholar
- Pappone, P. A. (1980). Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibres.J. Physiol. (Lond.) 306:377–410.Google Scholar
- Petersen, M., Pierau, Fr. K., and Weyrich, M. (1987). The influence of capsaicin on membrane currents in dorsal root ganglion neurones of guinea-pig and chicken.Pflügers Arch. 409:403–410.Google Scholar
- Raggenbass, M., and Dreifuss, J. J. (1992). Mechanism of action of oxytocin in rat vagal neurones: induction of a sustained sodium-dependent current.J. Physiol. (Lond.) 457:131–142.Google Scholar
- Russel, F. E. (1965). Marine toxins and venomous and poisonous marine animals.Adv. Marine Biol. 3:255–383.Google Scholar
- Schlichter, L. C., Bader, C. R., and Bernheim, L. (1991). Development of anomalous rectification (l h) and of a tetrodotoxin-resistant sodium current in embryonic quail neurones.J. Physiol. (Lond.) 442:127–145.Google Scholar
- Schofield, G. G., and Ikeda, S. R. (1988). Sodium and calcium currents of acutely isolated adult rat superior cervical ganglion neurons.Pflügers Arch. 411:481–490.Google Scholar
- Spalding, B. C. (1980). Properties of toxin-resistant sodium channels produced by chemical modification in frog skeletal muscle.J. Physiol. (Lond.) 305:485–500.Google Scholar
- Sutton, F., Davidson, N., and Lester, H. (1988). Tetrodotoxin-sensitive voltage-dependent Na currents recorded fromXenopus oocytes injected with mammalian cardiac muscle RNA.Mol. Brain Res. 3:195–200.Google Scholar
- Wald, F. (1972). Ionic differences between somatic and axonal action potentials in snail giant neurones.J. Physiol. (Lond.) 220:267–281.Google Scholar
- Yamaguchi, K. (1992). Electrophysiological properties of the growth cone membrane of the cultured rat dorsal root ganglion neuron.Jpn. J. Physiol. 42(Suppl).:S119 (abstr.).Google Scholar
- Yasumoto, T., Yasumura, D., Yotsu, M., Michishita, T., Endo, A., and Kotani, Y. (1986). Bacterial production of tetrodotoxin and anhydrotetrodotoxin.Agr. Biol. Chem. 50:793–795.Google Scholar
- Yoshida, S. (1982). Na and Ca spikes produced by ions passing through Ca channels in mouse ovarian oocytes.Pflügers Arch. 395:84–86.Google Scholar
- Yoshida, S. (1983a). Permeation of divalent and monovalent cations through the ovarian oocyte membrane of the mouse.J. Physiol. (Lond.) 339:631–642.Google Scholar
- Yoshida, S. (1983b). Excitability of ovarian oocytes and cleaving embryos of the mouse. InPhysiology of Excitable Cells (A. D. Grinnell and W. J. Moody Eds.), Alan R. Liss, New York, pp. 267–277.Google Scholar
- Yoshida, S. (1986a). Effects of the calcium channel blocker diltiazem on the excitability of mouse oocytes.Gamete Res. 13:309–316.Google Scholar
- Yoshida, S. (1986b). Electrical properties of oocytes and developing embryos of the mouse. InMembrane Excitation and Macromolecules (A. Watanabe, S., Terakawa, and K. Uchizono, Eds.), Biomedical Research Foundation, Tokyo, pp. 99–102.Google Scholar
- Yoshida, S., Mukainaka, T., and Yonezawa, T. (1979). Effects of alkaline earth cations (Ca, Sr, Ba) on cultured spinal neurons of the mouse. A light and electron microscopic study.Brian Res. 173:168–173.Google Scholar
- Yoshida, S., Matsuda, Y., and Sasaki, K. (1980a). Calcium and tetrodotoxin-resistant sodium currents in mammalian neurons. InTopics in General Physiology and Biophysics The Committee for Publication in Honor of Professor A. Inouye (Ed.), Kitami Shobo, Tokyo, pp. 92–102.Google Scholar