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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Jan;81(1):262–266. doi: 10.1073/pnas.81.1.262

Electrical activity and cytosolic calcium regulate levels of tetrodotoxin-sensitive sodium channels in cultured rat muscle cells.

S J Sherman, W A Catterall
PMCID: PMC344652  PMID: 6320167

Abstract

Pharmacological blockade of the spontaneous electrical activity present in primary cultures of rat myotubes by growth in bupivacaine, tetrodotoxin, or KCl was found to increase the number of voltage-sensitive Na+ channels 38-83% as measured by the specific binding of [3H]saxitoxin. The inhibition of spontaneous electrical activity and increase in channel density by bupivacaine displayed an identical dose response, with a half-maximal effect at 3.0 microM. Growth of myotubes in the presence of 1 microM A23187, a Ca2+-specific ionophore, resulted in a 30-60% decrease in the number of tetrodotoxin-sensitive channels with no change in affinity for [3H]saxitoxin. A23187 was able to overcome the increase in channel density produced by bupivacaine. These results suggest the presence of a Ca2+-mediated negative feedback system in which electrical excitability may be regulated by altering the number of tetrodotoxin-sensitive Na+ channels.

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Selected References

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  1. Berg D. K., Hall Z. W. Increased extrajunctional acetylcholine sensitivity produced by chronic acetylcholine sensitivity produced by chronic post-synaptic neuromuscular blockade. J Physiol. 1975 Jan;244(3):659–676. doi: 10.1113/jphysiol.1975.sp010818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Caputo C. Excitation and contraction processes in muscle. Annu Rev Biophys Bioeng. 1978;7:63–83. doi: 10.1146/annurev.bb.07.060178.000431. [DOI] [PubMed] [Google Scholar]
  3. Catterall W. A. Activation and inhibition of the action potential Na+ ionophore of cultured rat muscle cells by neurotoxins. Biochem Biophys Res Commun. 1976 Jan 12;68(1):136–142. doi: 10.1016/0006-291x(76)90020-6. [DOI] [PubMed] [Google Scholar]
  4. Catterall W. A., Morrow C. S., Hartshorne R. P. Neurotoxin binding to receptor sites associated with voltage-sensitive sodium channels in intact, lysed, and detergent-solubilized brain membranes. J Biol Chem. 1979 Nov 25;254(22):11379–11387. [PubMed] [Google Scholar]
  5. 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]
  6. Desmedt J. E., Hainaut K. Dantrolene and A13187 ionophore: specific action on calcium channels revealed by the aequorin method. Biochem Pharmacol. 1979 Apr 1;28(7):957–964. doi: 10.1016/0006-2952(79)90286-7. [DOI] [PubMed] [Google Scholar]
  7. Fambrough D. M. Control of acetylcholine receptors in skeletal muscle. Physiol Rev. 1979 Jan;59(1):165–227. doi: 10.1152/physrev.1979.59.1.165. [DOI] [PubMed] [Google Scholar]
  8. Fischbach G. D. Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev Biol. 1972 Jun;28(2):407–429. doi: 10.1016/0012-1606(72)90023-1. [DOI] [PubMed] [Google Scholar]
  9. Gruener R., Baumbach N. Muscle insensitivity to tetrodotoxin: induction by alpha-bungarotoxin and removal by submechanical threshold stimulation. J Neurobiol. 1976 Nov;7(6):513–519. doi: 10.1002/neu.480070605. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Kameyama T., Etlinger J. D. Calcium-dependent regulation of protein synthesis and degradation in muscle. Nature. 1979 May 24;279(5711):344–346. doi: 10.1038/279344a0. [DOI] [PubMed] [Google Scholar]
  12. Kidokoro Y., Heinemann S., Schubert D., Brandt B. L., Klier F. G. Synapse formation and neurotrophic effects on muscle cell lines. Cold Spring Harb Symp Quant Biol. 1976;40:373–388. doi: 10.1101/sqb.1976.040.01.036. [DOI] [PubMed] [Google Scholar]
  13. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  14. Lawrence J. C., Jr, Salsgiver W. J. Levels of enzymes of energy metabolism are controlled by activity of cultured rat myotubes. Am J Physiol. 1983 May;244(5):C348–C355. doi: 10.1152/ajpcell.1983.244.5.C348. [DOI] [PubMed] [Google Scholar]
  15. Lomo T., Rosenthal J. Control of ACh sensitivity by muscle activity in the rat. J Physiol. 1972 Mar;221(2):493–513. doi: 10.1113/jphysiol.1972.sp009764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McManaman J. L., Blosser J. C., Appel S. H. Inhibitors of membrane depolarization regulate acetylcholine receptor synthesis by a calcium-dependent, cyclic nucleotide-independent mechanism. Biochim Biophys Acta. 1982 Feb 10;720(1):28–35. doi: 10.1016/0167-4889(82)90035-0. [DOI] [PubMed] [Google Scholar]
  17. Narahashi T. Chemicals as tools in the study of excitable membranes. Physiol Rev. 1974 Oct;54(4):813–889. doi: 10.1152/physrev.1974.54.4.813. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Pressman B. C. Biological applications of ionophores. Annu Rev Biochem. 1976;45:501–530. doi: 10.1146/annurev.bi.45.070176.002441. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Rieger F., Koenig J., Vigny M. Spontaneous contractile activity and the presence of the 16 S form of acetylcholinesterase in rat muscle cells in culture: reversible suppressive action of tetrodotoxin. Dev Biol. 1980 May;76(2):358–365. doi: 10.1016/0012-1606(80)90385-1. [DOI] [PubMed] [Google Scholar]
  22. Ritchie J. M., Rogart R. B., Strichartz G. R. A new method for labelling saxitoxin and its binding to non-myelinated fibres of the rabbit vagus, lobster walking leg, and garfish olfactory nerves. J Physiol. 1976 Oct;261(2):477–494. doi: 10.1113/jphysiol.1976.sp011569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ritchie J. M., Rogart R. B. The binding of saxitoxin and tetrodotoxin to excitable tissue. Rev Physiol Biochem Pharmacol. 1977;79:1–50. doi: 10.1007/BFb0037088. [DOI] [PubMed] [Google Scholar]
  24. Sastre A., Podleski T. R. Pharmacologic characterization of the Na+ ionophores in L6 myotubes. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1355–1359. doi: 10.1073/pnas.73.4.1355. [DOI] [PMC free article] [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., 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]
  27. Stallcup W. B., Cohn M. Electrical properties of a clonal cell line as determined by measurement of ion fluxes. Exp Cell Res. 1976 Mar 15;98(2):277–284. doi: 10.1016/0014-4827(76)90439-0. [DOI] [PubMed] [Google Scholar]
  28. Statham H. E., Duncan C. J., Smith J. L. The effect of the ionophore A23187 on the ultrastructure and electrophysiological properties of frog skeletal muscle. Cell Tissue Res. 1976 Oct 6;173(2):193–209. doi: 10.1007/BF00221375. [DOI] [PubMed] [Google Scholar]
  29. Yaffe D. Cellular aspects of muscle differentiation in vitro. Curr Top Dev Biol. 1969;4:37–77. doi: 10.1016/s0070-2153(08)60480-9. [DOI] [PubMed] [Google Scholar]

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