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. 1993 Dec;472:521–536. doi: 10.1113/jphysiol.1993.sp019960

Na(+)-K+ pump stimulation elicits recovery of contractility in K(+)-paralysed rat muscle.

T Clausen 1, S L Andersen 1, J A Flatman 1
PMCID: PMC1160500  PMID: 8145158

Abstract

1. This study explores the role of active electrogenic Na(+)-K+ transport in restoring contractility in isolated rat soleus muscles exposed to high extracellular potassium concentration ([K+]o). This was done using agents (catecholamines and insulin) known to stimulate the Na(+)-K+ pump via different mechanisms. 2. When exposed to Krebs-Ringer bicarbonate buffer containing 10 mM K+, the isometric twitch and tetanic force of intact muscles decreased by 40-69%. The major part of this decline could be prevented by the addition of salbutamol (10(-5) M). In the presence of 10 mM K+, force could be restored almost completely within 5-10 min by the addition of salbutamol or adrenaline and partly by insulin. 3. In muscles exposed to 12.5 mM K+, force declined by 96%. Salbutamol (10(-5) M), adrenaline (10(-6) M) and insulin (100 mU ml-1) produced 57-71, 61-71 and 38-47% recovery of force within 10-20 min, respectively. The effects of these supramaximal concentrations of salbutamol and insulin on force recovery were additive. Salbutamol and adrenaline produced significant recovery of contractility at concentrations down to 10(-8) M (P < 0.005). 4. In soleus, the same agents stimulated 86Rb+ uptake and decreased intracellular Na+. These actions reflect stimulation of active Na(+)-K+ transport and both showed a highly significant correlation to the recovery of twitch as well as tetanic force (r = 0.80-0.88; P < 0.001). 5. The force recovery induced by salbutamol, adrenaline and insulin was suppressed by pre-exposure to ouabain (10(-5) M for 10 min or 10(-3) M for 1 min) as well as by tetrodotoxin (10(-6) M). 6. The observations support the conclusion that the inhibitory effect of high [K+]o on contractility in skeletal muscle can be counterbalanced by stimulation of active electrogenic Na(+)-K+ transport, the ensuing increase in the clearance of extracellular K+ and in the transmembrane electrochemical gradient for Na+.

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Selected References

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  1. Andersen S. L., Clausen T. Calcitonin gene-related peptide stimulates active Na(+)-K+ transport in rat soleus muscle. Am J Physiol. 1993 Feb;264(2 Pt 1):C419–C429. doi: 10.1152/ajpcell.1993.264.2.C419. [DOI] [PubMed] [Google Scholar]
  2. BOWMAN W. C., RAPER C. THE EFFECTS OF ADRENALINE AND OTHER DRUGS AFFECTING CARBOHYDRATE METABOLISM ON CONTRACTIONS OF THE RAT DIAPHRAGM. Br J Pharmacol Chemother. 1964 Aug;23:184–200. doi: 10.1111/j.1476-5381.1964.tb01578.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bendheim P. E., Reale E. O., Berg B. O. beta-Adrenergic treatment of hyperkalemic periodic paralysis. Neurology. 1985 May;35(5):746–749. doi: 10.1212/wnl.35.5.746. [DOI] [PubMed] [Google Scholar]
  4. Clausen T., Everts M. E. K(+)-induced inhibition of contractile force in rat skeletal muscle: role of active Na(+)-K+ transport. Am J Physiol. 1991 Nov;261(5 Pt 1):C799–C807. doi: 10.1152/ajpcell.1991.261.5.C799. [DOI] [PubMed] [Google Scholar]
  5. Clausen T., Everts M. E., Kjeldsen K. Quantification of the maximum capacity for active sodium-potassium transport in rat skeletal muscle. J Physiol. 1987 Jul;388:163–181. doi: 10.1113/jphysiol.1987.sp016608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clausen T., Flatman J. A. Beta 2-adrenoceptors mediate the stimulating effect of adrenaline on active electrogenic Na-K-transport in rat soleus muscle. Br J Pharmacol. 1980 Apr;68(4):749–755. doi: 10.1111/j.1476-5381.1980.tb10868.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  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. Dørup I., Skajaa K., Clausen T. A simple and rapid method for the determination of the concentrations of magnesium, sodium, potassium and sodium, potassium pumps in human skeletal muscle. Clin Sci (Lond) 1988 Mar;74(3):241–248. doi: 10.1042/cs0740241. [DOI] [PubMed] [Google Scholar]
  10. ENGSTFELD G., ANTONI H., FLECKENSTEIN A. [The restoration of stimulus transmission and contraction power of K ion paralysed frog and mammalian myocardium by adrenaline. Analysis of an effect of adrenaline not observed until now]. Pflugers Arch Gesamte Physiol Menschen Tiere. 1961;273:145–163. [PubMed] [Google Scholar]
  11. Everts M. E., Clausen T. Activation of the Na-K pump by intracellular Na in rat slow- and fast-twitch muscle. Acta Physiol Scand. 1992 Aug;145(4):353–362. doi: 10.1111/j.1748-1716.1992.tb09375.x. [DOI] [PubMed] [Google Scholar]
  12. Everts M. E., Retterstøl K., Clausen T. Effects of adrenaline on excitation-induced stimulation of the sodium-potassium pump in rat skeletal muscle. Acta Physiol Scand. 1988 Oct;134(2):189–198. doi: 10.1111/j.1748-1716.1988.tb08479.x. [DOI] [PubMed] [Google Scholar]
  13. GAMSTORP I., HAUGE M., HELWEGLARSEN H. F., MJONES H., SAGILD U. Adynamia episodica hereditaria: a disease clinically resembling familial periodic paralysis but characterized by increasing serum potassium during the paralytic attacks. Am J Med. 1957 Sep;23(3):385–390. doi: 10.1016/0002-9343(57)90318-2. [DOI] [PubMed] [Google Scholar]
  14. Hirche H., Schumacher E., Hagemann H. Extracellular K+ concentration and K+ balance of the gastrocnemius muscle of the dog during exercise. Pflugers Arch. 1980 Sep;387(3):231–237. doi: 10.1007/BF00580975. [DOI] [PubMed] [Google Scholar]
  15. Hník P., Holas M., Krekule I., Kŭriz N., Mejsnar J., Smiesko V., Ujec E., Vyskocil F. Work-induced potassium changes in skeletal muscle and effluent venous blood assessed by liquid ion-exchanger microelectrodes. Pflugers Arch. 1976 Mar 11;362(1):85–94. doi: 10.1007/BF00588685. [DOI] [PubMed] [Google Scholar]
  16. Holmberg E., Waldeck B. On the possible role of potassium ions in the action of terbutaline on skeletal muscle contractions. Acta Pharmacol Toxicol (Copenh) 1980 Feb;46(2):141–149. doi: 10.1111/j.1600-0773.1980.tb02434.x. [DOI] [PubMed] [Google Scholar]
  17. Holmberg E., Waldeck B. The effect of insulin on skeletal muscle contractions and its relation to the effect produced by BETA-adrenoceptor stimulation. Acta Physiol Scand. 1980 Jun;109(2):225–229. doi: 10.1111/j.1748-1716.1980.tb06590.x. [DOI] [PubMed] [Google Scholar]
  18. Hoya A., Venosa R. A. Ionic movements mediated by monensin in frog skeletal muscle. Biochim Biophys Acta. 1992 Feb 17;1104(1):123–131. doi: 10.1016/0005-2736(92)90140-h. [DOI] [PubMed] [Google Scholar]
  19. Juel C. Muscle action potential propagation velocity changes during activity. Muscle Nerve. 1988 Jul;11(7):714–719. doi: 10.1002/mus.880110707. [DOI] [PubMed] [Google Scholar]
  20. Juel C. The effect of beta 2-adrenoceptor activation on ion-shifts and fatigue in mouse soleus muscles stimulated in vitro. Acta Physiol Scand. 1988 Oct;134(2):209–216. doi: 10.1111/j.1748-1716.1988.tb08481.x. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. McArdle J. J., D'Alonzo A. J. Effects of terbutaline, a beta 2-adrenergic agonist, on the membrane potentials of innervated and denervated fast- and slow-twitch muscles. Exp Neurol. 1981 Jan;71(1):134–143. doi: 10.1016/0014-4886(81)90076-5. [DOI] [PubMed] [Google Scholar]
  23. Medbø J. I., Sejersted O. M. Plasma potassium changes with high intensity exercise. J Physiol. 1990 Feb;421:105–122. doi: 10.1113/jphysiol.1990.sp017935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ruff R. L., Simoncini L., Stühmer W. Comparison between slow sodium channel inactivation in rat slow- and fast-twitch muscle. J Physiol. 1987 Feb;383:339–348. doi: 10.1113/jphysiol.1987.sp016412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sjøgaard G., Adams R. P., Saltin B. Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. Am J Physiol. 1985 Feb;248(2 Pt 2):R190–R196. doi: 10.1152/ajpregu.1985.248.2.R190. [DOI] [PubMed] [Google Scholar]
  26. Vyskocil F., Hník P., Rehfeldt H., Vejsada R., Ujec E. The measurement of K+e concentration changes in human muscles during volitional contractions. Pflugers Arch. 1983 Nov;399(3):235–237. doi: 10.1007/BF00656721. [DOI] [PubMed] [Google Scholar]
  27. 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]

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