Control of cell volume and ion transport by beta-adrenergic catecholamines in erythrocytes of rainbow trout, Salmo gairdneri

J Physiol. 1987 Jan:382:123-44. doi: 10.1113/jphysiol.1987.sp016359.

Abstract

1. Trout red cells suspended in an isotonic medium containing beta-adrenergic catecholamines or adenosine 3',5'-phosphate (cyclic AMP) enlarge rapidly to reach a new steady-state volume which is maintained as long as hormone is present. The volume response is not changed by inhibition of the Na+-K+ pump with ouabain. The new steady-state volume was shown to result from a dynamic equilibrium involving the simultaneous functioning of two regulatory processes induced by hormone: a volume increase response that causes cells to enlarge by gaining Na+ and a volume decrease response that causes cells to shrink by losing K+. 2. As previously described, the volume increase response due to NaCl entry, is mediated by the activation by cyclic AMP of a Na+-H+ antiport operating in parallel to Cl(-)-OH- exchanges. In addition, it is shown in this paper that the Na+ uptake is a discontinuous, oscillatory process and that NaCl entry continues for several hours, i.e. as long as hormone is present. 3. The volume decrease response involves a passive, Cl(-)-dependent K+ loss. Na+ cannot use this pathway. The response is blocked by replacement of Cl- by NO3-, by loop diuretics (furosemide, bumetanide) but also by inhibitors of the anion exchanger (4,4'-diisothiocyanostilbene-2,2'-disulphonic acid (DIDS), niflumic acid). The activation of this ouabain-insensitive, Cl(-)-dependent K+ transport system is not directly triggered by cyclic AMP. It involves an all-or-none type of switching phenomenon which occurs when the cells swell to a certain volume. Thus it is a regulatory response to the increase in cell volume induced by stimulation of the Na+-H+ exchange by cyclic AMP. Inactivation is also volume dependent: when the cell size approaches the initial size the pathway shuts off. Thus the controlling mechanism of the K+ pathway acts like a reversible on-off switch that operates around a given volume. Ca2+ was not found to be involved in this control. Cyclic AMP is not necessary to keep the activated K+ pathway open but it could be one of the factors involved in the activating process. 4. There are several lines of evidence indicating that in trout red cells the volume decrease and the volume increase responses may not be brought about by the same transport mechanism operating in different modes. The movements of Na+, K+ and Cl- account for the water movements during volume increase and decrease. Thus movements of other solutes such as amino acids need not be considered.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amiloride / pharmacology
  • Animals
  • Biological Transport / drug effects
  • Chlorides / blood
  • Cyclic AMP / pharmacology
  • Erythrocytes / cytology
  • Erythrocytes / physiology*
  • In Vitro Techniques
  • Isoproterenol / pharmacology*
  • Ouabain / pharmacology
  • Potassium / blood
  • Salmonidae / blood*
  • Sodium / blood
  • Time Factors
  • Trout / blood*

Substances

  • Chlorides
  • Ouabain
  • Amiloride
  • Sodium
  • Cyclic AMP
  • Isoproterenol
  • Potassium