Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1989 Jul;414:159–177. doi: 10.1113/jphysiol.1989.sp017682

Geographutoxin-sensitive and insensitive sodium currents in mouse skeletal muscle developing in situ.

T Gonoi 1, Y Hagihara 1, J Kobayashi 1, H Nakamura 1, Y Ohizumi 1
PMCID: PMC1189136  PMID: 2607429

Abstract

1. The whole-cell voltage-clamp technique was used to examine developmental changes of Na+ current properties in single fibres of mouse flexor digitorum brevis muscles developing in situ from birth to 20 days post-natal. 2. Geographutoxin II (GTX II), a novel polypeptide toxin from the marine snail Conus geographus, distinguished two different types of voltage-sensitive Na+ currents: GTX II-sensitive and GTX II-insensitive currents, which corresponded respectively to currents with high or low TTX sensitivity. 3. Voltage-dependent activation and inactivation of the GTX II-insensitive currents occurred at membrane potentials 10-20 mV more negative than those for the GTX II-sensitive currents. 4. The GTX II-insensitive current in fibres from mice older than 8 days inactivated more slowly than the GTX II-sensitive current. However, in fibres from younger mice, the two currents decayed with similar speed. 5. The mean specific Na+ conductance (gNa) for the total (GTX II-sensitive plus GTX II-insensitive) Na+ channels was 0.22 mS/muF at a Na+ concentration of 5 mM at birth. The total gNa increased 6-fold to 1.32 mS/muF during the first 20 days after birth. 6. The mean specific gNa for the GTX II-insensitive channels was 0.15 mS/muF at birth, remained at approximately the same level for the first 8 days, and then decreased progressively to become undetectable by day 16. 7. In muscle fibres denervated 12 days after birth, the GTX II-insensitive gNa increased over the next 8 days, whereas the total gNa increased less than normal. 8. By contrast, in fibres denervated on day 4, the total gNa increased more than normal in the following 8 days, and the GTX II-insensitive specific gNa increased above the level seen at birth. 9. Half-maximal activation and inactivation potentials of the total and the GTX II-insensitive currents shifted in the negative direction by 9-17 mV in the first 8 days after birth. 10. We conclude that the regulatory effects of innervation on the total gNa are either suppressive or enhancing depending on the stage of development. On the other hand, denervation elicits an increase in GTX II-insensitive Na+ currents at all ages studied.

Full text

PDF
159

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adrian R. H., Marshall M. W. Sodium currents in mammalian muscle. J Physiol. 1977 Jun;268(1):223–250. doi: 10.1113/jphysiol.1977.sp011855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albuquerque E. X., Schuh F. T., Kauffman F. C. Early membrane depolarization of the fast mammalian muscle after denervation. Pflugers Arch. 1971;328(1):36–50. doi: 10.1007/BF00587359. [DOI] [PubMed] [Google Scholar]
  3. Beam K. G., Knudson C. M. Effect of postnatal development on calcium currents and slow charge movement in mammalian skeletal muscle. J Gen Physiol. 1988 Jun;91(6):799–815. doi: 10.1085/jgp.91.6.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bekoff A., Betz W. J. Physiological properties of dissociated muscle fibres obtained from innervated and denervated adult rat muscle. J Physiol. 1977 Sep;271(1):25–40. doi: 10.1113/jphysiol.1977.sp011988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caillé J., Ildefonse M., Rougier O. Existence of a sodium current in the tubular membrane of frog twitch muscle fibre; its possible role in the activation of contraction. Pflugers Arch. 1978 May 18;374(2):167–177. doi: 10.1007/BF00581298. [DOI] [PubMed] [Google Scholar]
  6. Catterall W. A. Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Annu Rev Pharmacol Toxicol. 1980;20:15–43. doi: 10.1146/annurev.pa.20.040180.000311. [DOI] [PubMed] [Google Scholar]
  7. Cruz L. J., Gray W. R., Olivera B. M., Zeikus R. D., Kerr L., Yoshikami D., Moczydlowski E. Conus geographus toxins that discriminate between neuronal and muscle sodium channels. J Biol Chem. 1985 Aug 5;260(16):9280–9288. [PubMed] [Google Scholar]
  8. Gilly W. F., Armstrong C. M. Threshold channels--a novel type of sodium channel in squid giant axon. 1984 May 31-Jun 6Nature. 309(5967):448–450. doi: 10.1038/309448a0. [DOI] [PubMed] [Google Scholar]
  9. Gonoi T., Hasegawa S. Post-natal disappearance of transient calcium channels in mouse skeletal muscle: effects of denervation and culture. J Physiol. 1988 Jul;401:617–637. doi: 10.1113/jphysiol.1988.sp017183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gonoi T., Hille B. Gating of Na channels. Inactivation modifiers discriminate among models. J Gen Physiol. 1987 Feb;89(2):253–274. doi: 10.1085/jgp.89.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gonoi T., Ohizumi Y., Nakamura H., Kobayashi J., Catterall W. A. The Conus toxin geographutoxin IL distinguishes two functional sodium channel subtypes in rat muscle cells developing in vitro. J Neurosci. 1987 Jun;7(6):1728–1731. doi: 10.1523/JNEUROSCI.07-06-01728.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gonoi T., Sherman S. J., Catterall W. A. Voltage clamp analysis of tetrodotoxin-sensitive and -insensitive sodium channels in rat muscle cells developing in vitro. J Neurosci. 1985 Sep;5(9):2559–2564. doi: 10.1523/JNEUROSCI.05-09-02559.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  14. Harris J. B., Marshall M. W. Tetrodotoxin-resistant action potentials in newborn rat muscle. Nat New Biol. 1973 Jun 6;243(127):191–192. doi: 10.1038/newbio243191a0. [DOI] [PubMed] [Google Scholar]
  15. Harris J. B., Thesleff S. Studies on tetrodotoxin resistant action potentials in denervated skeletal muscle. Acta Physiol Scand. 1971 Nov;83(3):382–388. doi: 10.1111/j.1748-1716.1971.tb05091.x. [DOI] [PubMed] [Google Scholar]
  16. Jaimovich E., Chicheportiche R., Lombet A., Lazdunski M., Ildefonse M., Rougier O. Differences in the properties of Na+ channels in muscle surface and T-tubular membranes revealed by tetrodotoxin derivatives. Pflugers Arch. 1983 Apr;397(1):1–5. doi: 10.1007/BF00585159. [DOI] [PubMed] [Google Scholar]
  17. Kobayashi M., Wu C. H., Yoshii M., Narahashi T., Nakamura H., Kobayashi J., Ohizumi Y. Preferential block of skeletal muscle sodium channels by geographutoxin II, a new peptide toxin from Conus geographus. Pflugers Arch. 1986 Aug;407(2):241–243. doi: 10.1007/BF00580684. [DOI] [PubMed] [Google Scholar]
  18. Moczydlowski E., Olivera B. M., Gray W. R., Strichartz G. R. Discrimination of muscle and neuronal Na-channel subtypes by binding competition between [3H]saxitoxin and mu-conotoxins. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5321–5325. doi: 10.1073/pnas.83.14.5321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nakamura H., Kobayashi J., Ohizumi Y., Hirata Y. Isolation and amino acid compositions of geographutoxin I and II from the marine snail Conus geographus. Experientia. 1983 Jun 15;39(6):590–591. doi: 10.1007/BF01971110. [DOI] [PubMed] [Google Scholar]
  20. Ohizumi Y., Nakamura H., Kobayashi J., Catterall W. A. Specific inhibition of [3H] saxitoxin binding to skeletal muscle sodium channels by geographutoxin II, a polypeptide channel blocker. J Biol Chem. 1986 May 15;261(14):6149–6152. [PubMed] [Google Scholar]
  22. Pappone P. A. Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibres. J Physiol. 1980 Sep;306:377–410. doi: 10.1113/jphysiol.1980.sp013403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Redfern P., Thesleff S. Action potential generation in denervated rat skeletal muscle. II. The action of tetrodotoxin. Acta Physiol Scand. 1971 May;82(1):70–78. doi: 10.1111/j.1748-1716.1971.tb04943.x. [DOI] [PubMed] [Google Scholar]
  24. Sato S., Nakamura H., Ohizumi Y., Kobayashi J., Hirata Y. The amino acid sequences of homologous hydroxyproline-containing myotoxins from the marine snail Conus geographus venom. FEBS Lett. 1983 May 8;155(2):277–280. doi: 10.1016/0014-5793(82)80620-0. [DOI] [PubMed] [Google Scholar]
  25. Sherman S. J., Catterall W. A. Biphasic regulation of development of the high-affinity saxitoxin receptor by innervation in rat skeletal muscle. J Gen Physiol. 1982 Nov;80(5):753–768. doi: 10.1085/jgp.80.5.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sherman S. J., Catterall W. A. Electrical activity and cytosolic calcium regulate levels of tetrodotoxin-sensitive sodium channels in cultured rat muscle cells. Proc Natl Acad Sci U S A. 1984 Jan;81(1):262–266. doi: 10.1073/pnas.81.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sherman S. J., Lawrence J. C., Messner D. J., Jacoby K., Catterall W. A. Tetrodotoxin-sensitive sodium channels in rat muscle cells developing in vitro. J Biol Chem. 1983 Feb 25;258(4):2488–2495. [PubMed] [Google Scholar]
  28. WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weiss R. E., Horn R. Functional differences between two classes of sodium channels in developing rat skeletal muscle. Science. 1986 Jul 18;233(4761):361–364. doi: 10.1126/science.2425432. [DOI] [PubMed] [Google Scholar]
  30. Weiss R. E., Horn R. Single-channel studies of TTX-sensitive and TTX-resistant sodium channels in developing rat muscle reveal different open channel properties. Ann N Y Acad Sci. 1986;479:152–161. doi: 10.1111/j.1749-6632.1986.tb15567.x. [DOI] [PubMed] [Google Scholar]
  31. Yamamoto D., Yeh J. Z., Narahashi T. Voltage-dependent calcium block of normal and tetramethrin-modified single sodium channels. Biophys J. 1984 Jan;45(1):337–344. doi: 10.1016/S0006-3495(84)84159-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yanagawa Y., Abe T., Satake M. Mu-conotoxins share a common binding site with tetrodotoxin/saxitoxin on eel electroplax Na channels. J Neurosci. 1987 May;7(5):1498–1502. doi: 10.1523/JNEUROSCI.07-05-01498.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES