The Journal of Membrane Biology

, Volume 73, Issue 3, pp 237–246 | Cite as

Thiol-dependent passive K/Cl transport in sheep red cells: I. Dependence on chloride and external K+[Rb+] ions

  • P. K. Lauf
Articles

Summary

Treatment with 2mm N-ethylmaleimide (NEM) caused a marked increase in K+ permeability of low K+ but not of high K+ sheep red cells suspended in isosmotic Cl media with 10−4m ouabain. The Na+ permeability was unaltered. Kinetic analysis by K+ efflux and K+ or Rb+ influx measurements suggests that NEM primarily increased the bidirectional fluxes of K+ and Rb+, since (a) no significant change in the apparent external affinities of these ions was found, and (b) below unity, the observed flux ratios were close to those calculated from the Ussing relationship. Replacement of Cl by NO 3 abolished the NEM-stimulated and reduced the basal K+ flux rates. Similarly, 10−3m furosemide inhibited Cl-dependent K+ fluxes in both control and NEM-treated LK red cells. Exposure of LK cells to hyposmotic but not to hyperosmotic salt solutions increased the basal Cl dependent K+ flux twofold as reported by Dunham and Ellory (J. Physiol. (London)318:511–530, 1981) but did not affect its fractional stimulation by NEM. The action of NEM is interpreted as a stimulation of a temperature-dependent and Cl-requiring K+ transport pathway genetically preserved in adult LK but turned off in HK sheep red cells. In addition, common to both LK and HK sheep red cells was a basal K+ flux that operated in the presence of either Cl or NO 3 .

Key Words

sheep erythrocytes passive K+Cl cotransport sulfhydryl (SH) groups 

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References

  1. 1.
    Aiton, J.F., Brown, C.D.A., Ogden, P., Simmons, N.J., 1982. K+ transport in ‘tight’ epithelial monolayers of MDCK cells.J. Membrane Biol. 65:99–109Google Scholar
  2. 2.
    Aiton, J.F., Chipperfield, A.R., Lamb, J.F., Ogden, P., Simmons, N.L. 1981. Occurrence of passive furosemide-sensitive transmembrane potassium transport in cultured cells.Biochim. Biophys. Acta 646:389–398Google Scholar
  3. 3.
    Aull, F. 1981. Potassium chloride cotransport in steadystate ascites tumor Cells. Does bumetanide inhibit?Biochim. Biophys. Acta 643:339Google Scholar
  4. 4.
    Bakker-Grunwald, T. 1978. Effect of anions on potassium self-exchange in ascites tumor cells.Biochim. Biophys. Acta 513:292–295Google Scholar
  5. 5.
    Bakker-Grunwald, T. 1981. Hormone induced diuretic-sensitive potassium transport in turkey erythrocytes is anion dependent.Biochim. Biophys. Acta 641:427–431Google Scholar
  6. 6.
    Brown, A.M., Ellory, J.C., Young, J.D., Lew, V.L. 1978. A calcium-activated potassium channel present in foetal red cells of the sheep but absent from reticulocytes and mature red cells.Biochim. Biophys. Acta 511:163–175Google Scholar
  7. 7.
    Chipperfield, A.R. 1980. An effect of chloride on (Na+K) co-transport in human red blood cells.Nature 286:281–282Google Scholar
  8. 8.
    Chipperfield, A.R. 1981. Chloride dependence of frusemideand phloretin-sensitive passive sodium and potassium fluxes in human red cells.J. Physiol. (London) 312:435–444Google Scholar
  9. 9.
    Dunham, P.B. 1976. Passive potassium transport in LK sheep red cells. Effect of anti-L antibody and intracellular potassium.J. Gen. Physiol. 68:567–581Google Scholar
  10. 10.
    Dunham, P.B. 1976. Two populations of antibodies affecting cation transport in LK erythrocytes of sheep and goats.Biochim. Biophys. Acta 443:219–226Google Scholar
  11. 11.
    Dunham, P.B., Ellory, J.C. 1981. Passive potassium transport in low potassium sheep red cells: Dependence upon cell volume and chloride.J. Physiol. (London) 318:511–530Google Scholar
  12. 12.
    Dunham, P.B., Hoffman, J.F. 1971. Active cation transport and ouabain binding in high potassium and low potassium red blood cells of sheep.J. Gen. Physiol. 58:94Google Scholar
  13. 13.
    Dunham, P.B., Stewart, G.W., Ellory, J.C. 1980. Chlorideactivated passive potassium transport in human erythrocytes.Proc. Natl. Acad. Sci. USA 77:1711–1715Google Scholar
  14. 14.
    Ellory, J.C., Dunham, P.B. 1980. Volume-dependent passive potassium transport in LK sheep red cells.In: Membrane Transport in Erythrocytes. Alfred Benzon Symposium 14. U.V. Lassen, H.H. Ussing, and J.O. Wieth, editors. pp. 409–427. Munksgaard, CopenhagenGoogle Scholar
  15. 15.
    Ellory, J.C., Tucker, EM. 1969. Stimulation of the potassium transport system in low potassium type sheep red cells by a specific antigen-antibody reaction.Nature (London) 222:477–478Google Scholar
  16. 16.
    Funder, J., Wieth, J.O. 1967. Effects of some monovalent anions on fluxes of Na and K, and on glucose metabolism of ouabain treated human red cells.Acta Physiol. Scand. 71:168–185Google Scholar
  17. 17.
    Garay, R., Adragna, N., Canessa, M., Tosteson, D. 1981. Outward sodium and potassium cotransport in human red cells.J. Membrane Biol. 62:169–174Google Scholar
  18. 18.
    Geck, P., Pietrzyk, C., Burckhardt, B.C., Pfeiffer, B., Heinz, E. 1980. Electrically silent cotransport of Na+, K+, and Cl in Ehrlich cells.Biochim. Biophys. Acta 600:432Google Scholar
  19. 19.
    Grinstein, S., Dupre, A., Rothstein, A. 1982. Volume regulation by human lymphocytes.J. Gen. Physiol. 79:849–868Google Scholar
  20. 20.
    Guggino, W.B., Boulpaep, E.L., Giebisch, G. 1982. Electrical properties of chloride transport across theNecturus proximal tubule.J. Membrane Biol. 65:185–196Google Scholar
  21. 21.
    Haas, M., Schmidt, W.F., III., McManus, T.J. 1982. Catecholamine stimulated ion transport in duck red cells: gradient effects in electrically neutral (Na+K+2Cl) co-transport.J. Gen. Physiol. 80:125–147Google Scholar
  22. 22.
    Haest, C.W.M., Kamp, D., Deuticke, B. 1981. Topology of membrane sulfhydryl groups in the human erythrocyte. Demonstration of a non-reactive population in intrinsic proteins.Biochim. Biophys. Acta 643:319–326Google Scholar
  23. 23.
    Hoffman, E.K., Sjoholm, G., Simonsen, L.O. 1981. Anioncation co-transport and volume regulation in Ehrlich ascites tumour cells.J. Physiol. (London) 319:94–95Google Scholar
  24. 24.
    Hoffman, P.G., Tosteson, D.C. 1971. Active sodium and potassium transport in high potassium and low potassium sheep red cells.J. Gen. Physiol. 58:438–466Google Scholar
  25. 25.
    Joiner, C.H., Lauf, P.K. 1978. The correlation between ouabain binding and K+ pump inhibition in human and sheep erythrocytes.J. Physiol. (London) 283:155–175Google Scholar
  26. 26.
    Joiner, C.H., Lauf, P.K. 1978. Modulation of ouabain binding and K+ pump flux by cellular Na+ and K+ in human and sheep erythrocytes.J. Physiol. (London) 283:177–196Google Scholar
  27. 27.
    Kregenow, F.M. 1981. Osmoregulatory salt transport mechanisms: Control of cell volume in anisotonic media.Annu. Rev. Physiol. 43:493–505Google Scholar
  28. 28.
    Lauf, P.K. 1981. A chemically unmasked, chloride dependent K+ transport in low K+ sheep red cells: Genetic and evolutionary aspects.In: Erythrocyte Membranes 2: Recent Clinical and Experimental Advances. W.C. Kruckeberg, T.W. Eaton, and P.J. Brewer, editors. pp. 13–30. Alan R. Liss, New YorkGoogle Scholar
  29. 29.
    Lauf, P.K. 1982. Evidence for chloride dependent potassium and water transport induced by hyposmotic stress in erythrocytes of the marine teleost,Opsanus Tau.J. Comp. Physiol. 146:9–16Google Scholar
  30. 30.
    Lauf, P.K. 1982. Active and passive cation transport and its association with membrane antigens in sheep erythrocytes: Developments and trends.In: Membranes and Transport. A. Martonosi, editor. Vol. 1. pp. 553–558. Plenum Press, New York-LondonGoogle Scholar
  31. 31.
    Lauf, P.K. 1982. Kinetics of the SH-group dependent, chloride activated passive K+ transport in low K+ sheep red cells.Fed. Proc. 41:974Google Scholar
  32. 32.
    Lauf, P.K., Rasmusen, B.A., Hoffman, P.G., Dunham, P.B., Cook, P.H., Parmelee, M.L., Tosteson, D.C. 1970. Stimulation of active potassium transport in LK sheep red cells by blood group L-antiserum.J. Membrane Biol. 3:1–13Google Scholar
  33. 33.
    Lauf, P.K., Stiehl, B.J., Joiner, C.H. 1977. Active and passive cation transport and L antigen heterogeneity in low potassium sheep red cells.J. Gen. Physiol. 70:221–242Google Scholar
  34. 34.
    Lauf, P.K., Sun, W.W. 1976. The binding characteristics of M and L isoantibodies to high and low potassium sheep red cells.J. Membrane Biol. 28:351–372Google Scholar
  35. 35.
    Lauf, P.K., Theg, B.E. 1980. A chloride dependent K+ flux induced by N-ethylmaleimide in genetically low K+ sheep and goat erythrocytes.Biochem. Biophys. Res. Commun. 92:1422–1428Google Scholar
  36. 36.
    Lauf, P.K., Theg, B.E. 1980. N-Ethylmaleimide enhances selectively passive K+ permeability in low potassium sheep red cells.In: Advances in Physiological Science. Vol. 6. Genetics, Structure and Function of Blood Cells. S.R. Hollan, G. Gardos, and B. Sarkadi, editors. pp. 285–291. Pergamon Press, BudapestGoogle Scholar
  37. 37.
    McRoberts, J.A., Erlinger, S., Rindler, M.J., Saier, M.H., Jr. 1982. Furosemide-sensitive salt transport in the Madin-Darby canine kidney cell line. Evidence for the co-transport of Na+, K+, and Cl.J. Biol. Chem. 257:2260Google Scholar
  38. 38.
    Rao, A. 1979. Disposition of the band 3 polypeptide in the human erythrocyte membrane.J. Biol. Chem. 254:3503–3511Google Scholar
  39. 39.
    Rasmusen, B.A. 1969. A blood group antibody which reacts exclusively with LK sheep red blood cells.Genetics 61:49Google Scholar
  40. 40.
    Rasmusen, B.A., Hall, J.G. 1966. Association between potassium concentration and serological type of sheep red blood cells.Science 151:1551–1552Google Scholar
  41. 41.
    Reichstein, E., Rothstein, A. 1981. Effects of quinine on Ca++-induced K+ efflux from human red blood cells.J. Membrane Biol. 59:57–63Google Scholar
  42. 42.
    Sims, P.J., Lauf, P.K. 1978. Steady state analysis of tracer exchange across the C5b-9 complement lesion in a biological membrane.Proc. Natl. Acad. Sci. USA 75:5669–5673Google Scholar
  43. 43.
    Spring, K.R., Ericson, A.C. 1982. Epithelial cell volume modulation and regulation.J. Membrane Biol. 69:167–176Google Scholar
  44. 44.
    Stewart, G.W., Ellory, J.C., Klein, R.A. 1980. Increased human red cell cation passive permeability below 12°C.Nature (London) 286:403–404Google Scholar
  45. 45.
    Tosteson, D.C., Hoffman, J.F. 1960. Regulation of cell volume by active cation transport in high and low potassium sheep red cells.J. Gen. Physiol. 44:169–194Google Scholar
  46. 46.
    Tucker, E.M., Ellory, J.C., Wooding, F.B.P., Morgan, G., Herbert, J. 1976. The number and specificity of L antigen sites on low potassium type sheep red cells.Proc. R. Soc. London. B 194:271–277Google Scholar
  47. 47.
    Ussing, H.H. 1978. Interpretation of tracer fluxes.In: Membrane Transport Biology. Vol. I., pp. 115–140. Springer-Verlag, New YorkGoogle Scholar
  48. 48.
    Wiley, J.S., Cooper, R.S. 1974. A furosemide-sensitive cotransport of sodium plus potassium in the human red cell.J. Clin. Invest. 53:745–755Google Scholar
  49. 49.
    Wright, E.M., Diamond, J.M. 1977. Anion selectivity in biological systems.Physiol. Rev. 57:109–156Google Scholar
  50. 50.
    Zade-Oppen, A.M.M., Schooler, J.M., Cook, P., Tosteson, D.C. 1979. Effect of membrane potential and internal pH on active sodium — potassium transport and on ATP content in high-potassium sheep erythrocytes.Biochim. Biophys. Acta 55:285–298Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1983

Authors and Affiliations

  • P. K. Lauf
    • 1
  1. 1.Department of PhysiologyDuke University Medical CenterDurham

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