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Tetrodotoxin-resistant sodium channels

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Summary

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.

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References

  • Aguayo, L. G., Weight, F. F., and White, G. (1991). TTX-sensitive action potentials and excitability of adult rat sensory neurons cultured in serum- and exogenous nerve growth factor-free medium.Neurosci. Lett. 121:88–92.

    PubMed  Google Scholar 

  • 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 

  • Armstrong, C. M., and Bezanilla, F. (1974). Charge movement associated with the opening and closing of the activation gates of Na channels.J. Gen. Physiol. 63:533–552.

    PubMed  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 

  • Barchi, R. L. (1988). Probing the molecular structure of the voltage-dependent sodium channel.Annu. Rev. Neurosci. 11:455–495.

    PubMed  Google Scholar 

  • Barres, B. A., Chun, L. L. Y., and Corey, D. P. (1989). Glial and neuronal forms of the voltage-dependent sodium channel: Characteristics and cell-type distribution.Neuron 2:1375–1388.

    PubMed  Google Scholar 

  • Barres, B. A., Chun, L. L. Y., and Corey, D. P. (1990). Ion channels in vertebrate glia.Annu. Rev. Neurosci. 13:441–474.

    PubMed  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 

  • Bkaily, G., Jacques, D., Sculptoreanu, A., Yamamoto, T., Carrier, D., Vigneault, D., and Sperelakis, N. (1991). Apamin, a highly potent blocker of the TTX- and Mn2+-insensitive fast transient Na+ current in young embryonic heart.J. Mol. Cell. Cardiol. 23:25–39.

    PubMed  Google Scholar 

  • Bossu, J. L., and Feltz, A. (1984). Patch-clamp study of the tetrodotoxin-resistant sodium current in group C sensory neurons.Neurosci. Lett. 51:241–246.

    PubMed  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 

  • Caffrey, J. M., Eng, D. L., Black, J. A., Waxman, S. G., and Kocsis, J. D. (1992). Three types of sodium channels in adult rat dorsal root ganglion neurons.Brain Res. 592:283–297.

    PubMed  Google Scholar 

  • Campbell, D. T. (1992). Large and small vertebrate sensory neurons express different Na and K channel subtypes.Proc. Natl. Acad. Sci. USA 89:9569–9573.

    PubMed  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 

  • Catterall, W. A. (1980). Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes.Annu. Rev. Pharmacol. Toxicol. 20:15–43.

    PubMed  Google Scholar 

  • Catterall, W. A. (1988). Structure and function of voltage-sensitive ion channels.Science 242:50–61.

    PubMed  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 

  • Fedulova, S. A., Kostyuk, P. G., and Veslovsky, N. S. (1991). Ionic mechanisms of electrical excitability in rat sensory neurons during postnatal ontogenesis.Neuroscience 41:303–309.

    PubMed  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 

  • Fukuda, J., and Kameyama, M. (1980). Tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in tissue-cultured spinal ganglion neurons from adult mammals.Brain Res. 182:191–197.

    PubMed  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 

  • Gonoi, T., Sherman, S. J., and Catterall, W. A. (1985). Voltage clamp analysis of tetrodotoxin-sensitive and -insensitive sodium channels in rat muscle cells developing in vitro.J. Neurosci. 5:2559–2564.

    PubMed  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 

  • Harris, J. B., and Thesleff, S. (1971). Studies on tetrodotoxin resistant action potentials in denervated skeletal muscle.Acta Physiol. Scand. 83:382–388.

    PubMed  Google Scholar 

  • Heinemann, S. H., Terlau, H., Stühmer, W., Imoto, K., and Numa, S. (1992). Calcium channel characteristics conferred on the sodium channel by single mutations.Nature 356:441–443.

    PubMed  Google Scholar 

  • Heyer, E. J., and MacDonald, R. L. (1982). Calcium- and sodium-dependent action potentials of mouse spinal cord and dorsal root ganglion neurons in cell culture.J. Neurophysiol. 47:641–655.

    PubMed  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 

  • Ikeda, S. R., Schofield, G. G., and Weight, F. F. (1986). Na+ and Ca2+ currents of acutely isolated adult rat nodose ganglion cells.J. Neurophysiol. 55:527–539.

    PubMed  Google Scholar 

  • Jones, S. W. (1987). Sodium currents in dissociated bull-frog sympathetic neurones.J. Physiol. (Lond.) 389:605–627.

    Google Scholar 

  • Kallen, R. G., Sheng, Z. H., Yang, J., Chen, L. Q., Rogart, R. B., and Barchi, R. L. (1990). Primary structure and expression of a sodium channel characteristic of denervated and immature rat skeletal muscle.Neuron 4:233–242.

    PubMed  Google Scholar 

  • Kano, M. (1975). Development of excitability in embryonic chick skeletal muscle cells.J. Cell. Physiol. 86:503–510.

    PubMed  Google Scholar 

  • Kao, C. Y. (1966). Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena.Pharmacol. Rev. 18:997–1049.

    PubMed  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.

  • 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 

  • Kleinhaus, A. L., and Prichard, J. W. (1976). Sodium dependent tetrodotoxin-resistant action potentials in a leech neuron.Brain Res. 102:368–373.

    PubMed  Google Scholar 

  • Kostyuk, P. G., Veselovsky, N. S., and Tsyndrenko, A. Y. (1981). Ionic currents in the somatic membrane of rat dorsal root ganglion neurons. I. Sodium currents.Neuroscience 6:2423–2430.

    PubMed  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 

  • Lawson, S. N., Harper, A. A., Harper, E. I., Garson, J. A., and Anderton, B. H. (1984). A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones.J. Comp. Neurol. 228:263–272.

    PubMed  Google Scholar 

  • Mandel, G. (1992). Tissue-specific expression of the voltage-sensitive sodium channel.J. Membr. Biol. 125:193–205.

    PubMed  Google Scholar 

  • McDonald, T. F., Sachs, H. G., and DeHaan, R. L. (1973). Tetrodotoxin desensitization in aggregates of embryonic chick heart cells.J. Gen. Physiol. 62:286–302.

    PubMed  Google Scholar 

  • McLean, M. J., Bennett, P. B., and Thomas, R. M. (1988). Subtypes of dorsal root ganglion neurons based on different inward currents as measured by whole-cell voltage clamp.Mol. Cell. Biochem. 80:95–107.

    PubMed  Google Scholar 

  • Matsuda, Y., Yoshida, S., and Yonezawa, T. (1976). A Ca-dependent regenerative response in rodent dorsal root ganglion cellsin vitro.Brain Res. 115:334–338.

    PubMed  Google Scholar 

  • Matsuda, Y., Yoshida, S., and Yonezawa, T. (1978). Tetrodotoxin sensitivity and Ca component of action potentials of mouse dorsal root ganglion cells culturedin vitro.Brain Res. 154:69–82.

    PubMed  Google Scholar 

  • Mercuri, N. B., Stratta, F., Calabresi, P., and Bernardi, G. (1993). Neurotensin induces an inward current in rat mesencephalic dopaminergic neurons.Neurosci. Lett. 153:192–196.

    PubMed  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 

  • Miyazawa, K., Jeon, J. K., Noguchi, T., Ito, K., and Hashimoto, K. (1987). Distribution of tetrodotoxin in the tissues of the flatwormPlanocera multitentaculata (Platyhelminthes).Toxicon 25:975–980.

    PubMed  Google Scholar 

  • Morita, K., and Katayama, Y. (1989). Bullfrog dorsal root ganglion cells having tetrodotoxin-resistant spikes are endowed with nicotinic receptors.J. Neurophysiol. 62:657–664.

    PubMed  Google Scholar 

  • Mosher, H. S. (1986). The chemistry of tetrodotoxin.Ann. N.Y. Acad. Sci. 479:32–43.

    PubMed  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.

  • Mosher, H. S., Fuhrman, F. A., Buchwald, H. D., and Fischer, H. G. (1964). Tarichatoxin-tetrodotoxin: A potent neurotoxin.Science 144:1100–1114.

    PubMed  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 

  • Narahashi, T. (1974). Chemicals as tools in the study of excitable membrane.Physiol. Rev. 54:813–889.

    PubMed  Google Scholar 

  • Narahashi, T., Moore, J. W., and Scott, W. R. (1964). Tetrodotoxin blockage of sodium conductance increase in lobster giant axons.J. Gen. Physiol. 47:965–974.

    PubMed  Google Scholar 

  • Neumcke, B. (1990). Diversity of sodium channels in adult and cultured cells, in oocytes and in lipid bilayers.Rev. Physiol. Biochem. Pharmacol. 115:1–49.

    PubMed  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.

    PubMed  Google Scholar 

  • Noda, M., Ikeda, T., Kayano, T., Suzuki, H., Takeshima, H., Kurasaki, M., Takahashi, H., and Numa, S. (1986). Existence of distinct sodium channel messenger RNAs in rat brain.Nature 320:188–192.

    PubMed  Google Scholar 

  • Noda, M., Suzuki, H., Numa, S., and Stühmer, W. (1989). A single point mutation confers tetrodotoxin and saxitoxin insensitivity on the sodium channel II.FEBS Lett. 259:213–216.

    PubMed  Google Scholar 

  • Noguchi, T., Jeon, J. K., Arakawa, O., Sugita, H., Deguchi, Y., Shida, Y., and Hashimoto, K. (1986). Occurrence of tetrodotoxin and anhydrotetrodotoxin inVibrio sp. isolated from the intestines of a xanthid crab,Atergatis floridus.J. Biochem. 99:311–314.

    PubMed  Google 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. (1992b). Slow inactivation of tetrodotoxin-insensitive Na+ channels in neurons of rat dorsal root ganglia.J. Membr. Biol. 129:71–80.

    PubMed  Google Scholar 

  • Ogata, N., and Tatebayashi, H. (1992c) Na+ current kinetics are not the determinants of the action potential duration in neurons of the rat ventral tegmental area.Brain Res. Bull. 29:691–695.

    PubMed  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 

  • Omri, G., and Meiri, H. (1990). Characterization of sodium currents in mammalian sensory neurons cultured in serum-free defined medium with and without nerve growth factor.J. Membr. Biol. 115:13–29.

    PubMed  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 

  • Prince, R. C. (1988). Tetrodotoxin.Trends Biochem. Sci. 13:76–77.

    PubMed  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 

  • Ransom, B. R., and Holz, R. W. (1977). Ionic determinants of excitability in cultured mouse dorsal root ganglion and spinal cord cells.Brain Res. 136:445–453.

    PubMed  Google Scholar 

  • Redfern, P., and Thesleff, S. (1971). Action potential generation in denervated rat skeltal muscle. II. Action of tetrodotoxin.Acta Physiol. Scand. 82:70–79.

    PubMed  Google Scholar 

  • Ritchie, J. M., and Rogart, R. B. (1977). The binding of saxitoxin and tetrodotoxin to excitable tissue.Rev. Physiol. Biochem. Pharmacol. 79:1–50.

    PubMed  Google Scholar 

  • Roy, M. L., and Narahashi, T. (1992). Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons.J. Neurosci. 12:2104–2111.

    PubMed  Google Scholar 

  • Russel, F. E. (1965). Marine toxins and venomous and poisonous marine animals.Adv. Marine Biol. 3:255–383.

    Google Scholar 

  • Satin, J., Kyle, J. W., Chen, M., Bell, P., Cribbs, L. L., Fozzard, H. A., and Rogart, R. B. (1992). A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties.Science 256:1202–1205.

    PubMed  Google Scholar 

  • Schlichter, L. C. (1983). A role for action potentials in maturingRana pipiens oocytes.Dev. Biol. 98:60–69.

    PubMed  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 

  • Schwartz, A., Palti, Y., and Meiri, H. (1990). Structural and developmental differences between three types of Na channels in dorsal root ganglion cells of newborn rats.J. Membr. Biol. 116:117–128.

    PubMed  Google Scholar 

  • Shigenobu, K., and Sperelakis, N. (1971). Development of sensitivity to tetrodotoxin of chick embryonic hearts with age.J. Mol. Cell. Cardiol. 3:271–286.

    PubMed  Google Scholar 

  • Shrager, P., Chiu, S. Y., and Ritchie, J. M. (1985). Voltage-dependent sodium and potassium channels in mammalian cultured Schwann cells.Proc. Natl. Acad. Sci. USA 82:948–952.

    PubMed  Google Scholar 

  • Sigworth, F. J., and Spalding, B. C. (1980). Chemical modification reduces the conductance of sodium channels in nerve.Nature 283:293–295.

    PubMed  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 

  • Sperelakis, N., and Shigenobu, K. (1972). Changes in membrane properties of chick embryonic hearts during development.J. Gen. Physiol. 60: 430–453.

    PubMed  Google Scholar 

  • Spitzer, N. C. (1979). Ion channels in development.Annu. Rev. Neurosci. 2:363–397.

    PubMed  Google Scholar 

  • Stansfeld, C. E., and Wallis, D. I. (1985). Properties of visceral primary afferent neurons in the nodose ganglion of the rabbit.J. Neurophysiol. 54:245–260.

    PubMed  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 

  • Takahashi, K., Kameda, H., Kataoka, M., Ueno, S., and Akaike, N. (1992). Effects of Ca2+ antagonists and antiepileptics on tetrodotoxin-sensitive Ca2+-conducting channels in isolated rat hippocampal CA1 neurons.Neurosci. Lett. 148:60–62.

    PubMed  Google Scholar 

  • Terlau, H., Heinemann, S. H., Stühmer, W., Pusch, M., Conti, F., Imoto, K., and Numa, S. (1991). Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II.FEBS Lett. 293:93–96.

    PubMed  Google Scholar 

  • Thio, C. L., and Sontheimer, H. (1993). Differential modulation of TTX-sensitive and TTX-resistant Na+ channels in spinal cord astrocytes following activation of protein kinase C.J. Neurosci. 13:4889–4897.

    PubMed  Google Scholar 

  • Trimmer, J. S., and Agnew, W. S. (1989). Molecular diversity of voltage-sensitive Na channels.Annu. Rev. Physiol. 51:401–418.

    PubMed  Google Scholar 

  • Trimmer, J. S., Cooperman, S. S., Agnew, W. S., and Mandel, G. (1990). Regulation of muscle sodium channel transcripts during development and in response to denervation.Dev. Biol. 142:360–367.

    PubMed  Google Scholar 

  • Twarog, B. M., Hidaka, T., and Yamaguchi, H. (1972). Resistance to tetrodotoxin and saxitoxin in nerves of bivalve molluscs.Toxicon 10:273–278.

    PubMed  Google Scholar 

  • Ulbricht, W. (1981). Kinetics of drug action and equilibrium results at the node of Ranvier.Physiol. Rev. 61:785–828.

    PubMed  Google Scholar 

  • Unsworth, B. R., and Hafemann, D. R. (1975). Tetrodotoxin binding as a marker for functional differentiation of various brain regions during chick and mouse development.J. Neurochem. 24:261–270.

    PubMed  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 

  • Weiss, R. E., and Horn, R. (1986). Functional differences between two classes of sodium channels in developing rat skeletal muscle.Science 233:361–364.

    PubMed  Google Scholar 

  • Weiss, R. E., and Sidell, N. (1991). Sodium currents during differentiation in a human neuroblastoma cell line.J. Gen. Physiol. 97:521–539.

    PubMed  Google Scholar 

  • White, J. A., Alonso, A., and Kay, A. R. (1993). A heart-like Na+ current in the medial entorhinal cortex.Neuron 11:1037–1047.

    PubMed  Google Scholar 

  • White, M. M., Chen, L. Q., Kleinfield, R., Kallen, R. G., and Barchi, R. L. (1991). SkM2, a Na+ channel cDNA clone from denervated skeletal muscle, encodes a tetrodotoxin-insensitive Na+ channel.Mol. Pharmacol. 39:604–608.

    PubMed  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 

  • Yang, J. S., Sladky, J. T., Kallen, R. G., and Barchi, R. L. (1991). TTX-sensitive and TTX-insensitive sodium channel mRNA transcripts are independently regulated in adult skeletal muscle after denervation.Neuron 7:421–427.

    PubMed  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. (1985). Action potentials dependent on monovalent cations in developing mouse embryos.Dev. Biol. 110:200–206.

    PubMed  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., and Matsuda, Y. (1979). Studies on sensory neurons of the mouse with intracellular-recording and horseradish peroxidase-injection techniques.J. Neurophysiol. 42:1134–1145.

    PubMed  Google Scholar 

  • Yoshida, S., and Matsuda, Y. (1980). Responses dependent on alkaline earth cations (Ca, Sr, Ba) in dorsal root ganglion cells of the adult mouse.Brain Res. 188:593–597.

    PubMed  Google Scholar 

  • Yoshida, S., Matsuda, Y., and Samejima, A. (1978). Tetrodotoxin-resistant sodium and calcium components of action potentials in dorsal root ganglion cells of the adult mouse.J. Neurophysiol. 41:1096–1106.

    PubMed  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 

  • Yoshida, S., Matsuda, Y., and Yonezawa, T. (1980b). Spontaneous discharges caused by increasing external Na ion or divalent cation concentration in the mouse dorsal root ganglion cells in culture.Brain Res. 196:560–564.

    PubMed  Google Scholar 

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Yoshida, S. Tetrodotoxin-resistant sodium channels. Cell Mol Neurobiol 14, 227–244 (1994). https://doi.org/10.1007/BF02088322

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  • DOI: https://doi.org/10.1007/BF02088322

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