Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Catecholamine- and volume-dependent ion fluxes in carp (Cyprinus carpio) red blood cells

  • 22 Accesses

  • 11 Citations

Abstract

In carp erythrocytes, noradrenaline (10-6 mol·l-1) induces a 30- to 40-fold activation of Na+/H+ exchange (the ethylisopropylamiloride-inhibited component of the 22Na influx) and a fourfold stimulation of the Na+, K+ pump (ouabain-inhibited component of 86Rb influx). In both cases the effect of noradrenaline is blocked by propranolol but not phentolamine and is imitated by forskolin. An activator of protein kinase C (β-phorbol 12-myristate, 13-acetate) increases Na+/H+ exchange by 10 times and decreases the Na+, K+ pump activity by 20–30 percent. In the presence of ethylisopropylamiloride the increment of the Na+, K+ pump activity induced by noradrenaline is reduced by 35–45 percent, indicating the existence of a Na+/H+ exchange-independent mechanism of the Na+, K+ pump regulation by β-adrenergic catecholamines. Hypertonic shrinkage of carp erythrocytes results in a 40- to 80-fold activation of Na+/H+ exchange, whereas hypotonic swelling induces an increase in the rate of 86Rb+ efflux which is inhibited by furosemide by about 30–40 percent. The rate of pH0 recovery in response to acidification or alkalinization in rat erythrocytes is approximately 15 times as fast as in carp erythrocytes. Unlike in rat erythrocytes, valinomycin does not cause an alkalinization of incubation medium in carp erythrocytes indicating the absence of conductive pathway in the operation of anion transporter protein. A scheme is suggested which describes the interrelation of Na+/H+ exchange, Na+, K+ pump and a non-identified system providing for K+ efflux in cell swelling, regulation of cell volume and cytoplasmic pH in fish erythrocytes under conditions of deep hypoxia and high activity.

This is a preview of subscription content, log in to check access.

Abbreviations

cAMP:

cyclic adenosine monophosphate

CCCP:

carbonylcyamide m-chlorophenylhydrazone

DMSO:

dimethylsulphoxide

EIPA:

ethylisopropylamiloride

NA:

noradrenaline

PMA:

β-phorbol 12-myristate, 13-acetate

RVD:

regulatory volume decrease

RVI:

regulatory volume increase

References

  1. Baroin A, Garcia-Romeu F, La Marret T, Motais R (1984) A transient sodium-hydrogen exchange system induced by catecholamine in erythrocytes of rainbow trout. J Physiol (London) 1356:21–31

  2. Borgese F, Garcia-Romeu F, Motais R (1986) Catecholamineinduced transport systems in the trout erythrocyte: Na+/H+ counter-transport or Na/Cl co-transport? J Gen Physiol 87:551–556

  3. Borgese F, Garcia-Romeu F, Motais R (1987a) Control of cell volume and ion transport by β-adrenergic catecholamines in erythrocytes of rainbow trout, Salmo gairdneri. J Physiol (London) 382:123–144

  4. Borgese F, Garcia-Romeu F, Motais R (1987b) Ion movements and volume changes induced by catecholamines in erythrocytes of rainbow trout: effect of pH. J Physiol (London) 382:145–157

  5. Bourne PK, Cossins AR (1982) On the instability of K+ influx in erythrocytes of the rainbow trout, Salmo gairdneri, and role of catecholamine hormones in maintaining in vivo influx activity. J Exp Biol 101:93–104

  6. Cabantchik ZI, Knauf PA, Rothstein A (1978) The anion transport system of red blood cell. The role of membrane protein evaluated by the use of probes. Biochim Biophys Acta 515:239–302

  7. Cossins A (1989) Intracellular pH. Regulation by fish red cells. Nature 340:20–21

  8. Cossins A, Richardson PA (1985) Adrenalin-induced Na+/H+-exchange in trout erythrocytes and its effects upon oxygencarrying capacity. J Exp Biol 118:229–246

  9. Dickman K, Goldstein L (1990) Cell volume regulation by skate erythrocytes: role of potassium. Am J Physiol 258:R1217-R1223

  10. Fievet B, Caroff J, Motais R (1990) Catecholamine release controlled by blood oxygen tension during deep hypoxia in trout: effect on red blood cell Na/H exchanger activity. Respir Physiol 79:81–90

  11. Freedman K, Hoffman JF (1979) Ionic and osmotic equilibria of human red blood cells treated with nystatin. J Gen Physiol 74:157–185

  12. Garay R, Nazaret C, Hannaert R, Cragoe E (1988) Demonstration of a [K, Cl]-cotransport system in human red cells by its sensitivity to [(dihydroindenyl) oxy] alcanoic acids regulation of cell swelling and distinction from the bumetanide-sensitive [Na,K,Cl] cotransport system. Mol Pharmacol 33:696–701

  13. Garcia-Romeu F, Motais R, Borgese F (1988) Desensitization by external Na of the cyclic AMP-dependent Na+/H+-antiporter in trout red cells. J Gen Physiol 91:529–548

  14. Gurlo TG, Orlov SN, Aksentsev SL, Okun IM, Konev SV (1991) Inward and outward potassium (86Rb+) fluxes in human and rat erythrocytes: volume change regulation (in Russian). Biological Membranes (Moscow) 8:727–735

  15. Hall AC, Ellory JC (1986) Evidence for the presence of volumesensitive KCl cotransport in young human red cells. Biochim Biophys Acta 858:317

  16. Jennings ML, Douglas SM, McAndrew PE (1986) Amiloridesensitive sodium-hydrogen exchange in osmotically shrunken rabbit red blood cells. Am J Physiol 251:C32-C40

  17. Kaji D (1986) Volume-sensitive K-transport in human erythrocytes. J Gen Physiol 88:718–738

  18. Knauf PA, Fuhrmann GF, Rothstein A (1977) The relationship between anion exchange and net anion flow across the human red blood cell membrane. J Gen Physiol 69:363–368

  19. Lauf PK (1982) Evidence for chloride-dependent potassium and water transport induced by hyposmotic stress in erythrocytes of the marine teleost Ospanus tau. J Comp Physiol 146:9–16

  20. Leite MV, Goldstein L (1987) Ca2+ ionophore and phorbol ester stimulate taurine efflux from skate erythrocyte. J Exp Zool 242:95–97

  21. Lowe AG, Lambert A (1982) Chloride-bicarbonate exchange and related transport processes. Biochim Biophys Acta 694:353–374

  22. Mahe J, Garcia-Romeu F, Motais R (1985) Inhibition by amiloride of both adenylate cyclase activity and the Na+/H+ antiporter in fish erythrocytes. Eur J Pharmacol 116:199–206

  23. Motais R, Garcia-Romeu F, Borgese F (1987) The control of Na+/H+-exchange by molecular oxygen in trout erythrocytes. A possible role of hemoglobin as a transducer. J Gen Physiol 90:197–207

  24. Motais R, Fievet B, Garcia-Romeu F, Thomas S (1989) Na+/H+-exchange and pH regulation in red blood cells: role of uncatalyzed H2CO3 dehydration. Am J Physiol 256:728–735

  25. Nikinmaa M (1982) Effect of adrenaline on red cell volume and concentration gradient of proton across the red cell membrane in the rainbow trout, Salmo gairdneri. Mol Physiol 2:287–297

  26. Nikinmaa M (1983) Adrenergic regulation of haemoglobin oxygen affinity in rainbow trout red cell. J Comp Physiol 152:67–72

  27. Nikinmaa M (1992) Membrane transport and control of hemoglobin oxygen affinity in nucleated erythrocytes. Physiol Rev 72:301–321

  28. Nikinmaa M, Railo E (1987) Anion movements across lamprey (Lampetra fluviatilis) red cell membrane. Biochim Biophys Acta 899:134–136

  29. Orlov SN, Pokudin NI, Gulak PV, Postnov YuV (1990) Volume-dependent regulation of cation transport and polyphosphoinositide metabolism in human and rat erythrocytes: features revealed in primary hypertension. Physiol Bohemoslov 39:15–26

  30. Orlov SN, Pokudin NI, Kotelevtsev YuV, Gulak PV (1989) Volume-dependent regulation of ion transport and membrane phosphorylation in human and rat erythrocytes. J Membr Biol 107:105–117

  31. Orlov SN, Pokudin NI, Ryazkski GG, Kotelevtsev YuV (1987) Valinomycin induces Na+/H+ exchange in rat erythrocytes: effect of protein kinase A and C activators (in Russian). Biological Membranes (Moscow) 4:1036–1046

  32. Orlov SN, Skryabin GA, Kotelevtsev SV, Kozlov YuP (1989) Univalent ion transport in carp erythrocytes: mechanism and regulation (in Russian). Biological Membranes (Moscow) 6:1261–1277

  33. Orlov SN, Skryabin GA (1991) β-adrenergic catecholamine activates Na+, K+-pump in carp erythrocytes independently of stimulation of Na+/H+-exchange. Doklady Biophysics (Proc Acad Sci USSR) Consultants Burcau, NY, pp 10–12

  34. Parker JC (1983) Volume-responsive sodium movements in dog red blood cells. Am J Physiol 244:C324-C330

  35. Postnov YuV, Kravtsov GM, Orlov SN, Pokudin NI, Postnov IYu, Kotelevtsev YuU (1988) Effect of protein kinase C activation on cytoskeleton and cation transport in human erythrocytes: reproduction of some abnormalitics revealed in essential hypertension. Hypertension 12:267–273

  36. Salama M, Nikinmaa M (1988) The adrenergic responses of carp (Cyprinus carpio) red blood cells: effects of PO2 and pH. J Exp Biol 136:405–416

  37. Salama M, Nikinmaa M (1989) Species differences in the adrenergic responses of fish red blood cells: studies on whitefish, pikeperch, trout and carp. Fish Physiol Biochem 6:167–173

  38. Salama A, Nikinmaa M (1990) Effect of oxygen tension on catecholamine-induced formation of cAMP and on swelling of carp red blood cells. Am J Physiol 259:C723-C726

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Orlov, S.N., Skryabin, G.A. Catecholamine- and volume-dependent ion fluxes in carp (Cyprinus carpio) red blood cells. J Comp Physiol B 163, 413–420 (1993). https://doi.org/10.1007/BF00265647

Download citation

Key words

  • Na+, K+-pump
  • Na+/H+-exchange
  • Anion transport
  • Erythrocytes
  • Carp, Cyprinus carpio