Skip to main content
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1987 Jul;91(3):671–681. doi: 10.1111/j.1476-5381.1987.tb11261.x

Role of ion conductance changes and of the sodium-pump in adrenaline-induced hyperpolarization of rat diaphragm muscle fibres.

K Kuba, M Nohmi
PMCID: PMC1853544  PMID: 2440508

Abstract

The ionic mechanism of membrane hyperpolarization induced by adrenaline in rat diaphragm muscle fibres was studied. Removal of the extracellular K+ ([K+]o) from Krebs-Ringer solution initially increased the resting membrane potential and then caused an increase in the intracellular Na+ activity ([Na+]i) and a decrease in the intracellular K+ activity ([K+]i). All the changes were maintained for more than 3 h. Application of ouabain (0.1 mM) or lowering the temperature rapidly reduced the resting potential by about 10 mV in the K+-free solution. It then produced further progressive decreases in resting potential and in [K+]i and a progressive increase in [Na+]i. These observations indicate that an electrogenic Na-pump operates in the K+-free solution. Removal of most of the Cl- in the K+-free solution did not affect the resting potential or the magnitude of the initial decrease produced by ouabain, despite an increased input resistance; this result implies a passive distribution of Cl-. Adrenaline (30-60 microM) either added to the bathing solution or applied to the membrane by ionophoresis produced a hyperpolarization (3-10 mV: adrenaline hyperpolarization), the amplitude of which was decreased with a rise in [K+]o and increased with a reduction in [K+]o, but unaffected by the removal of Cl-. Adrenaline produced an increase in input resistance, the relative magnitude (17-18%) of which was constant whether external K+ or Cl- was removed. In contrast, a conditioning membrane hyperpolarization hardly affected the resistance. Ouabain (0.1 mM) or low temperature (8-10 degrees C) abolished both the hyperpolarization and the increased input resistance induced by adrenaline. The [K+]i, [Na+]i and the peak of the action potential remained unchanged after a 20 min exposure to adrenaline (30 microM). The hyperpolarization induced by the replacement of all Na+ with Tris (Tris-hyperpolarization) in the K+-free solution was depressed by 39% during the early period (4-31 min) of exposure to adrenaline (30 microM), while it was enhanced by 26% during the later period (80-130 min). The initial depression suggested a decrease in the ratio of the membrane permeability for Na+ (PNa) to that for K+ (PK). These results suggest that the adrenaline hyperpolarization is generated largely by a decrease in PNa/PK, which is associated with the activity of the Na-pump.

Full text

PDF
671

Selected References

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

  1. Akaike N. Contribution of an electrogenic sodium pump to membrane potential in mammalian skeletal muscle fibres. J Physiol. 1975 Mar;245(3):499–520. doi: 10.1113/jphysiol.1975.sp010858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akiyama T., Grundfest H. The hyperpolarization of frog skeletal muscle fibres induced by removing potassium from the bathing medium. J Physiol. 1971 Aug;217(1):33–60. doi: 10.1113/jphysiol.1971.sp009558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowman W. C., Raper C. Adrenotropic receptors in skeletal muscle. Ann N Y Acad Sci. 1967 Feb 10;139(3):741–753. doi: 10.1111/j.1749-6632.1967.tb41241.x. [DOI] [PubMed] [Google Scholar]
  4. Bray J. J., Hawken M. J., Hubbard J. I., Pockett S., Wilson L. The membrane potential of rat diaphragm muscle fibres and the effect of denervation. J Physiol. 1976 Mar;255(3):651–667. doi: 10.1113/jphysiol.1976.sp011301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bressler B. H., Phillis J. W., Kozachuk W. Noradrenaline stimulation of a membrane pump in frog skeletal muscle. Eur J Pharmacol. 1975 Aug;33(1):201–204. doi: 10.1016/0014-2999(75)90158-2. [DOI] [PubMed] [Google Scholar]
  6. Clausen T., Flatman J. A. The effect of catecholamines on Na-K transport and membrane potential in rat soleus muscle. J Physiol. 1977 Sep;270(2):383–414. doi: 10.1113/jphysiol.1977.sp011958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Den Hertog A., Mooij J. J. Potassium induced potential changes in rat diaphragm muscle. Pflugers Arch. 1976 Mar 11;362(1):69–79. doi: 10.1007/BF00588683. [DOI] [PubMed] [Google Scholar]
  8. Dulhunty A. F. The dependence of membrane potential on extracellular chloride concentration in mammalian skeletal muscle fibres. J Physiol. 1978 Mar;276:67–82. doi: 10.1113/jphysiol.1978.sp012220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fujimoto M., Kubota T. Physicochemical properties of a liquid ion exchanger microelectrode and its application to biological fluids. Jpn J Physiol. 1976;26(6):631–650. doi: 10.2170/jjphysiol.26.631. [DOI] [PubMed] [Google Scholar]
  10. Gadsby D. C., Kimura J., Noma A. Voltage dependence of Na/K pump current in isolated heart cells. Nature. 1985 May 2;315(6014):63–65. doi: 10.1038/315063a0. [DOI] [PubMed] [Google Scholar]
  11. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. KERKUT G. A., THOMAS R. C. AN ELECTROGENIC SODIUM PUMP IN SNAIL NERVE CELLS. Comp Biochem Physiol. 1965 Jan;14:167–183. doi: 10.1016/0010-406x(65)90017-4. [DOI] [PubMed] [Google Scholar]
  14. Kaibara K., Koketsu K., Akasu T., Miyagawa M. A kinetic analysis of the facilitatory action of adrenaline. Pflugers Arch. 1982 Jan;392(3):304–306. doi: 10.1007/BF00584316. [DOI] [PubMed] [Google Scholar]
  15. Koketsu K., Ohta Y. Acceleration of the electrogenic Na+ pump by adrenaline in frog skeletal muscle fibres. Life Sci. 1976 Oct 1;19(7):1009–1013. doi: 10.1016/0024-3205(76)90292-7. [DOI] [PubMed] [Google Scholar]
  16. Koketsu K. The electrogenic sodium pump. Adv Biophys. 1971;2:77–112. [PubMed] [Google Scholar]
  17. Kuba K. Effects of catecholamines on the neuromuscular junction in the rat diaphragm. J Physiol. 1970 Dec;211(3):551–570. doi: 10.1113/jphysiol.1970.sp009293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kuba K., Kuba M., Koketsu K. Adrenaline hyperpolarization in rat diaphragm muscle fibers. Nihon Seirigaku Zasshi. 1978 Oct;40(10):377–380. [PubMed] [Google Scholar]
  19. Marshall K. C., Engberg I. Reversal potential for noradrenaline-induced hyperpolarization of spinal motoneurons. Science. 1979 Jul 27;205(4404):422–424. doi: 10.1126/science.451613. [DOI] [PubMed] [Google Scholar]
  20. Palade P. T., Barchi R. L. Characteristics of the chloride conductance in muscle fibers of the rat diaphragm. J Gen Physiol. 1977 Mar;69(3):325–342. doi: 10.1085/jgp.69.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Phillis J. W., Wu P. H. Catecholamines and the sodium pump in excitable cells. Prog Neurobiol. 1981;17(3):141–184. doi: 10.1016/0301-0082(81)90012-5. [DOI] [PubMed] [Google Scholar]
  22. Rang H. P., Ritchie J. M. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol. 1968 May;196(1):183–221. doi: 10.1113/jphysiol.1968.sp008502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sjodin R. A. Contributions of electrogenic pumps to resting membrane potentials: the theory of electrogenic potentials. Soc Gen Physiol Ser. 1984;38:105–127. [PubMed] [Google Scholar]
  24. Somlyo A. P., Somlyo A. V. Pharmacology of excitation-contraction coupling in vascular smooth muscle and in avian slow muscle. Fed Proc. 1969 Sep-Oct;28(5):1634–1642. [PubMed] [Google Scholar]
  25. Tashiro N. Effects of isoprenaline on contractions of directly stimulated fast and slow skeletal muscles of the guinea-pig. Br J Pharmacol. 1973 May;48(1):121–131. doi: 10.1111/j.1476-5381.1973.tb08229.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  27. Tomita T., Yamamoto T. Effects of removing the external potassium on the smooth muscle of guinea-pig taenia coli. J Physiol. 1971 Feb;212(3):851–868. doi: 10.1113/jphysiol.1971.sp009360. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES