Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1977 Sep;270(2):383–414. doi: 10.1113/jphysiol.1977.sp011958

The effect of catecholamines on Na—K transport and membrane potential in rat soleus muscle

Torben Clausen, John A Flatman
PMCID: PMC1353519  PMID: 198530

Abstract

1. The action of catecholamines on the transport and the distribution of Na and K and the resting membrane potential (EM) has been investigated in soleus muscles isolated from fed rats.

2. In a substrate-free Krebs—Ringer bicarbonate buffer adrenaline (ADR) (6 × 10-6 M) increased 22Na efflux by 83%, 42K influx by 34%, and EM by 10%. Similar effects were exerted by noradrenaline (NA), phenylephrine, salbutamol and isoprenaline. The effects of ADR on Na—K transport and EM were suppressed by ouabain (10-3 M) and propranolol (10-5 M), but not by thymoxamine (10-5 M) or tetracaine (10-4 M).

3. Following 90 min of incubation in the presence of ADR (6 × 10-6 M), the intracellular K/Na-ratio was increased threefold. NA produced almost the same change, and both catecholamines seem to induce a new steady-state distribution of Na and K which can be maintained for several hours in vitro.

4. The effect of ADR on 22Na efflux and EM could be detected at concentrations down to 6 × 10-9 and 6 × 10-10 M, respectively, and half-maximum increase was obtained at around 2 × 10-8 M. NA was at least one order of magnitude less potent.

5. The effect of low concentrations of ADR on 22Na efflux was potentiated by theophylline (2 mM). When added together, dibutyryl-cyclic AMP and theophylline mimicked the action of ADR on 22Na efflux, 42K influx, Na/K content and EM. Ouabain (10-3 M) also suppressed the effect of dibutyryl-cyclic AMP and theophylline on Na—K transport.

6. Following the addition of ouabain (10-3 M), EM rapidly dropped from a mean of -71 to -63 mV, and then showed a slow linear fall for up to 4hr.

7. The hyperpolarization induced by ADR was associated with a decrease in membrane conductance, 22Na influx and 42K efflux. The time course and the response to ouabain suggests that all of these effects are secondary to stimulation of the active coupled transport of Na and K.

8. It is concluded that in rat soleus muscle, the active Na—K transport is electrogenic and susceptible to stimulation by catecholamines via beta-adrenoceptors. This effect is mediated by adenyl cyclase activation and may account for the increase in EM and the intracellular K/Na ratio.

Full text

PDF
383

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. BOWMAN W. C., RAPER C. THE EFFECTS OF SYMPATHOMIMETIC AMINES ON CHRONICALLY DENERVATED SKELETAL MUSCLES. Br J Pharmacol Chemother. 1965 Feb;24:98–109. doi: 10.1111/j.1476-5381.1965.tb02083.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birmingham A. T., Ernest K., Newcombe J. F. Antagonism of the response of human isolated arteries to noradrenaline. Br J Pharmacol. 1969 Jan;35(1):127–131. doi: 10.1111/j.1476-5381.1969.tb07973.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bittar E. E., Chambers G., Schultz R. Mode of stimulation by adenosine 3':5'-cyclic monophosphate of the sodium efflux in barnacle muscle fibres. J Physiol. 1976 Jun;257(3):561–579. doi: 10.1113/jphysiol.1976.sp011385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowman W. C., Nott M. W. Actions of sympathomimetic amines and their antagonists on skeletal muscle. Pharmacol Rev. 1969 Mar;21(1):27–72. [PubMed] [Google Scholar]
  6. 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]
  7. Caswell A. H., Lau Y. H., Brunschwig J. P. Ouabain-binding vesicles from skeletal muscle. Arch Biochem Biophys. 1976 Oct;176(2):417–430. doi: 10.1016/0003-9861(76)90184-3. [DOI] [PubMed] [Google Scholar]
  8. Clausen T., Kohn P. G. The effect of insulin on the transport of sodium and potassium in rat soleus muscle. J Physiol. 1977 Feb;265(1):19–42. doi: 10.1113/jphysiol.1977.sp011703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clausen T. The relationship between the transport of glucose and cations across cell membranes in isolated tissues. V. Stimulating effect of ouabain, K+-free medium and insulin on efflux of 3-O-methylglucose from epidimal adipose tissue. Biochim Biophys Acta. 1969;183(3):625–634. doi: 10.1016/0005-2736(69)90175-8. [DOI] [PubMed] [Google Scholar]
  10. DURY A. The effect of epinephrine and insulin on the plasma potassium level. Endocrinology. 1951 Nov;49(5):663–670. doi: 10.1210/endo-49-5-663. [DOI] [PubMed] [Google Scholar]
  11. Dahl-Hansen A. B., Clausen T. The effect of membrane stabilizers and ouabain on the transport of Na+ and K+ in rat soleus muscle. Biochim Biophys Acta. 1973 Aug 9;318(1):147–153. doi: 10.1016/0005-2736(73)90344-1. [DOI] [PubMed] [Google Scholar]
  12. Daniel E. E., Paton D. M., Taylor G. S., Hodgson B. J. Adrenergic receptors for catecholamine effects on tissue electrolytes. Fed Proc. 1970 Jul-Aug;29(4):1410–1425. [PubMed] [Google Scholar]
  13. Dockry M., Kernan R. P., Tangney A. Active transport of sodium and potassium in mammalian skeletal muscle and its modification by nerve and by cholinergic and adrenergic agents. J Physiol. 1966 Sep;186(1):187–200. doi: 10.1113/jphysiol.1966.sp008028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Evans R. H., Smith J. W. Mode of action of catecholamines on skeletal muscle. J Physiol. 1973 Jul;232(2):81P–82P. [PubMed] [Google Scholar]
  15. GOFFART M., PERRY W. L. M. The action of adrenaline on the rate of loss of potassium ions from unfatigued striated muscle. J Physiol. 1951 Jan;112(1-2):95–101. doi: 10.1113/jphysiol.1951.sp004511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Galbo H., Holst J. J., Christensen N. J. Glucagon and plasma catecholamine responses to graded and prolonged exercise in man. J Appl Physiol. 1975 Jan;38(1):70–76. doi: 10.1152/jappl.1975.38.1.70. [DOI] [PubMed] [Google Scholar]
  17. Gardner J. D., Klaeveman H. L., Bilezikian J. P., Aurbach G. D. Effect of beta-adrenergic catecholamines on sodium transport in turkey erythrocytes. J Biol Chem. 1973 Aug 25;248(16):5590–5597. [PubMed] [Google Scholar]
  18. HAAS H. G., TRAUTWEIN W. Increase of sodium efflux induced by epinephrine in the heart of the frog. Nature. 1963 Jan 5;197:80–81. doi: 10.1038/197080a0. [DOI] [PubMed] [Google Scholar]
  19. Hays E. T., Dwyer T. M., Horowicz P., Swift J. G. Epinephrine action on sodium fluxes in frog striated muscle. Am J Physiol. 1974 Dec;227(6):1340–1347. doi: 10.1152/ajplegacy.1974.227.6.1340. [DOI] [PubMed] [Google Scholar]
  20. Heinemann U., Lux H. D. Undershoots following stimulus-induced rises of extracellular potassium concentration in cerebral cortex of cat. Brain Res. 1975 Jul 25;93(1):63–76. doi: 10.1016/0006-8993(75)90286-3. [DOI] [PubMed] [Google Scholar]
  21. Hidaka T., Kuriyama H. Effects of catecholamines on the cholinergic neuromuscular transmission in fish red muscle. J Physiol. 1969 Mar;201(1):61–71. doi: 10.1113/jphysiol.1969.sp008742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hoffman B. F., Singer D. H. Appraisal of the effects of catecholamines on cardiac electrical activity. Ann N Y Acad Sci. 1967 Feb 10;139(3):914–939. doi: 10.1111/j.1749-6632.1967.tb41261.x. [DOI] [PubMed] [Google Scholar]
  23. Kernan R. P., MacDermott M. Proceedings: Changes in potassium activity within frog sartorius muscle fibres during sodium enrichment in potassium-free Ringer fluid. J Physiol. 1975 Jul;249(1):25P–26P. [PubMed] [Google Scholar]
  24. Kernan R. P., MacDermott M., Westphal W. Proceedings: Measurement of chloride activity within frog sartorius muscle fibres by means of chloride-sensitive micro-electrodes. J Physiol. 1974 Aug;241(1):60P–61P. [PubMed] [Google Scholar]
  25. Kohn P. G., Clausen T. The relationship between the transport of glucose and cations across cell membranes in isolated tissues. VI. The effect of insulin, ouabain, and metabolic inhibitors on the transport of 3-O-methylglucose and glucose in rat soleus muscles. Biochim Biophys Acta. 1971 Feb 2;225(2):277–290. doi: 10.1016/0005-2736(71)90221-5. [DOI] [PubMed] [Google Scholar]
  26. Kohn P. G., Clausen T. The relationship between the transport of glucose and cations across cell membranes in isolated tissues. VII. The effects of extracellular Na + and K + on the transport of 3-O-methylglucose and glucose in rat soleus muscle. Biochim Biophys Acta. 1972 Mar 17;255(3):798–814. doi: 10.1016/0005-2736(72)90392-6. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Lee C. O., Armstrong W. M. State and distribution of potassium and sodium ions in frog skeletal muscle. J Membr Biol. 1974;15(4):331–362. doi: 10.1007/BF01870094. [DOI] [PubMed] [Google Scholar]
  29. Leitch A. G., Clancy L. J., Costello J. F., Flenley D. C. Effect of intravenous infusion of salbutamol on ventilatory response to carbon dioxide and hypoxia and on heart rate and plasma potassium in normal men. Br Med J. 1976 Feb 14;1(6006):365–367. doi: 10.1136/bmj.1.6006.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mathias C. J., Christensen N. J., Corbett J. L., Frankel H. L., Spalding J. M. Plasma catecholamines during paroxysmal neurogenic hypertension in quadriplegic man. Circ Res. 1976 Aug;39(2):204–208. doi: 10.1161/01.res.39.2.204. [DOI] [PubMed] [Google Scholar]
  31. Raper C., Bowman W. C. Effects of catecholamines on the gastrocnemius muscle of the domestic fowl. Eur J Pharmacol. 1968 Oct;4(3):309–316. doi: 10.1016/0014-2999(68)90099-x. [DOI] [PubMed] [Google Scholar]
  32. Smith J. W., Thesleff S. Spontaneous activity in denervated mouse diaphragm muscle. J Physiol. 1976 May;257(1):171–186. doi: 10.1113/jphysiol.1976.sp011362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. WADDELL A. W. Adrenaline, noradrenaline and potassium fluxes in rabbit auricles. J Physiol. 1961 Feb;155:209–220. doi: 10.1113/jphysiol.1961.sp006623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wang P., Clausen T. Treatment of attacks in hyperkalaemic familial periodic paralysis by inhalation of salbutamol. Lancet. 1976 Jan 31;1(7953):221–223. doi: 10.1016/s0140-6736(76)91340-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES