Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1985 May 1;85(5):649–667. doi: 10.1085/jgp.85.5.649

Effect of norepinephrine on swelling-induced potassium transport in duck red cells. Evidence against a volume-regulatory decrease under physiological conditions

PMCID: PMC2215820  PMID: 3998706

Abstract

Duck red cells exhibit specific volume-sensitive ion transport processes that are inhibited by furosemide, but not by ouabain. Swelling cells in a hypotonic synthetic medium activates a chloride- dependent, but sodium-independent, potassium transport. Shrinking cells in a hypertonic synthetic medium stimulates an electrically neutral co- transport of [Na + K + 2 Cl] with an associated 1:1 K/K (or K/Rb) exchange. These shrinkage-induced modes can also be activated in both hypo- and hypertonic solutions by beta-adrenergic catecholamines (e.g., norepinephrine). Freshly drawn cells spontaneously shrink approximately 4-5% when removed from the influence of endogenous plasma catecholamines, either by incubation in a catecholamine-free, plasma- like synthetic medium, or in plasma to which a beta-receptor blocking dose of propranolol has been added. This spontaneous shrinkage resembles the response of hypotonically swollen cells in that it is due to a net loss of KCl with no change in cell sodium. Norepinephrine abolishes the net potassium transport seen in both fresh and hypotonically swollen cells. Moreover, cells swollen in diluted plasma, at physiological pH and extracellular potassium, show no net loss of KCl and water ("volume-regulatory decrease") unless propranolol is added. Examination of the individual cation fluxes in the presence of catecholamines demonstrates that activation of [Na + K + 2Cl] co- transport with its associated K/Rb exchange prevents, or overrides, swelling-induced [K + Cl] co-transport. These results, therefore, cast doubt on whether the swelling-induced [K + Cl] system can serve a volume-regulatory function under in vivo conditions.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Adragna N. C., Tosteson D. C. Effect of volume changes on ouabain-insensitive net outward cation movements in human red cells. J Membr Biol. 1984;78(1):43–52. doi: 10.1007/BF01872531. [DOI] [PubMed] [Google Scholar]
  2. Alper S. L., Beam K. G., Greengard P. Hormonal control of Na+-K+ co-transport in turkey erythrocytes. Multiple site phosphorylation of goblin, a high molecular weight protein of the plasma membrane. J Biol Chem. 1980 May 25;255(10):4864–4871. [PubMed] [Google Scholar]
  3. Bia M. J., DeFronzo R. A. Extrarenal potassium homeostasis. Am J Physiol. 1981 Apr;240(4):F257–F268. doi: 10.1152/ajprenal.1981.240.4.F257. [DOI] [PubMed] [Google Scholar]
  4. Bilezikian J. P., Aurbach G. D. A beta-adrenergic receptor of the turkey erythrocyte. I. Binding of catecholamine and relationship to adenylate cyclase activity. J Biol Chem. 1973 Aug 25;248(16):5577–5583. [PubMed] [Google Scholar]
  5. Bourne P. K., Cossins A. R. On the instability of K+ influx in erythrocytes of the rainbow trout, Salmo gairdneri, and the role of catecholamine hormones in maintaining in vivo influx activity. J Exp Biol. 1982 Dec;101:93–104. doi: 10.1242/jeb.101.1.93. [DOI] [PubMed] [Google Scholar]
  6. Brown M. J., Brown D. C., Murphy M. B. Hypokalemia from beta2-receptor stimulation by circulating epinephrine. N Engl J Med. 1983 Dec 8;309(23):1414–1419. doi: 10.1056/NEJM198312083092303. [DOI] [PubMed] [Google Scholar]
  7. Cala P. M. Cell volume regulation by Amphiuma red blood cells. The role of Ca+2 as a modulator of alkali metal/H+ exchange. J Gen Physiol. 1983 Dec;82(6):761–784. doi: 10.1085/jgp.82.6.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cass A., Dalmark M. Equilibrium dialysis of ions in nystatin-treated red cells. Nat New Biol. 1973 Jul 11;244(132):47–49. doi: 10.1038/newbio244047a0. [DOI] [PubMed] [Google Scholar]
  9. DAVOREN P. R., SUTHERLAND E. W. THE CELLULAR LOCATION OF ADENYL CYCLASE IN THE PIGEON ERYTHROCYTE. J Biol Chem. 1963 Sep;238:3016–3023. [PubMed] [Google Scholar]
  10. Duhm J., Göbel B. O. Role of the furosemide-sensitive Na+/K+ transport system in determining the steady-state Na+ and K+ content and volume of human erythrocytes in vitro and in vivo. J Membr Biol. 1984;77(3):243–254. doi: 10.1007/BF01870572. [DOI] [PubMed] [Google Scholar]
  11. Epstein F. H., Rosa R. M. Adrenergic control of serum potassium. N Engl J Med. 1983 Dec 8;309(23):1450–1451. doi: 10.1056/NEJM198312083092308. [DOI] [PubMed] [Google Scholar]
  12. Gardner J. D., Klaeveman H. L., Bilezikian J. P., Aurbach G. D. Stimulation of sodium transport in turkey erythrocytes by cyclic 3',5'-AMP. Endocrinology. 1974 Aug;95(2):499–507. doi: 10.1210/endo-95-2-499. [DOI] [PubMed] [Google Scholar]
  13. Haas M., McManus T. J. Bumetanide inhibits (Na + K + 2Cl) co-transport at a chloride site. Am J Physiol. 1983 Sep;245(3):C235–C240. doi: 10.1152/ajpcell.1983.245.3.C235. [DOI] [PubMed] [Google Scholar]
  14. Haas M., Schmidt W. F., 3rd, McManus T. J. Catecholamine-stimulated ion transport in duck red cells. Gradient effects in electrically neutral [Na + K + 2Cl] Co-transport. J Gen Physiol. 1982 Jul;80(1):125–147. doi: 10.1085/jgp.80.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kregenow F. M. Functional separation of the Na-K exchange pump from the volume controlling mechanism in enlarged duck red cells. J Gen Physiol. 1974 Oct;64(4):393–412. doi: 10.1085/jgp.64.4.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kregenow F. M. Osmoregulatory salt transporting mechanisms: control of cell volume in anisotonic media. Annu Rev Physiol. 1981;43:493–505. doi: 10.1146/annurev.ph.43.030181.002425. [DOI] [PubMed] [Google Scholar]
  17. Kregenow F. M. The response of duck erythrocytes to hypertonic media. Further evidence for a volume-controlling mechanism. J Gen Physiol. 1971 Oct;58(4):396–412. doi: 10.1085/jgp.58.4.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kregenow F. M. The response of duck erythrocytes to nonhemolytic hypotonic media. Evidence for a volume-controlling mechanism. J Gen Physiol. 1971 Oct;58(4):372–395. doi: 10.1085/jgp.58.4.372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leskovac V., Pericin D., Trivić S., Stupar M., Murgul L. Inhibition by isoproterenol of the passive potassium efflux from pigeon erythrocytes. Comp Biochem Physiol C. 1984;78(2):475–478. doi: 10.1016/0742-8413(84)90117-8. [DOI] [PubMed] [Google Scholar]
  20. Manninen V. Movements of sodium and potassium ions and their tracers in propranolol-treated red cells and diaphragm muscle. Acta Physiol Scand Suppl. 1970;355:1–76. [PubMed] [Google Scholar]
  21. Palfrey H. C., Feit P. W., Greengard P. cAMP-stimulated cation cotransport in avian erythrocytes: inhibition by "loop" diuretics. Am J Physiol. 1980 Mar;238(3):C139–C148. doi: 10.1152/ajpcell.1980.238.3.C139. [DOI] [PubMed] [Google Scholar]
  22. Porzig H. Comparative study of the effects of propranolol and tetracaine on cation movements in resealed human red cell ghosts. J Physiol. 1975 Jul;249(1):27–49. doi: 10.1113/jphysiol.1975.sp011001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rasmussen H., Lake W., Allen J. E. The effect of catecholamines and prostaglandins upon human and rat erythrocytes. Biochim Biophys Acta. 1975 Nov 10;411(1):63–73. doi: 10.1016/0304-4165(75)90285-8. [DOI] [PubMed] [Google Scholar]
  24. Riddick D. H., Kregenow F. M., Orloff J. The effect of norepinephrine and dibutyryl cyclic adenosine monophosphate on cation transport in duck erythrocytes. J Gen Physiol. 1971 Jun;57(6):752–766. doi: 10.1085/jgp.57.6.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rosa R. M., Silva P., Young J. B., Landsberg L., Brown R. S., Rowe J. W., Epstein F. H. Adrenergic modulation of extrarenal potassium disposal. N Engl J Med. 1980 Feb 21;302(8):431–434. doi: 10.1056/NEJM198002213020803. [DOI] [PubMed] [Google Scholar]
  26. Rudolph S. A., Greengard P. Regulation of protein phosphorylation and membrane permeability by beta-adrenergic agents and cyclic adenosine 3':5'-monophosphate in the avian erythrocyte. J Biol Chem. 1974 Sep 10;249(17):5684–5687. [PubMed] [Google Scholar]
  27. Schmidt W. F., 3rd, McManus T. J. Ouabain-insensitive salt and water movements in duck red cells. I. Kinetics of cation transport under hypertonic conditions. J Gen Physiol. 1977 Jul;70(1):59–79. doi: 10.1085/jgp.70.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schmidt W. F., 3rd, McManus T. J. Ouabain-insensitive salt and water movements in duck red cells. II. Norepinephrine stimulation of sodium plus potassium cotransport. J Gen Physiol. 1977 Jul;70(1):81–97. doi: 10.1085/jgp.70.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmidt W. F., 3rd, McManus T. J. Ouabain-insensitive salt and water movements in duck red cells. III. The role of chloride in the volume response. J Gen Physiol. 1977 Jul;70(1):99–121. doi: 10.1085/jgp.70.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Wiley J. S., Cooper R. A. A furosemide-sensitive cotransport of sodium plus potassium in the human red cell. J Clin Invest. 1974 Mar;53(3):745–755. doi: 10.1172/JCI107613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. ØRSKOV S. L. The potassium absorption by pigeon blood cells; a considerable potassium absorption by pigeon- and hen blood cells in observed when a hypertonic sodium chloride solution is added. Acta Physiol Scand. 1954 Jul 18;31(2-3):221–229. doi: 10.1111/j.1748-1716.1954.tb01133.x. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES