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Anion-dependent transport of thallous ions through human erythrocyte membrane

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Unidirectional fluxes of 204Tl+ through the human red blood cell membrane were measured. The inward rate coefficient measured in a K+-free saline was 15.6±0.6 hr−1. The influx of Tl+ could be partially inhibited with 0.1mm ouabain (by 28%), 0.1mm DIDS (by 50%) or 1mm furosemide (by 51%). The inhibitory effects of ouabain and DIDS or furosemide were additive. Half-maximal responses were seen at 0.72 μ m and 0.22mm concentrations of DIDS and furosemide, respectively. A similar action of these blockers on Tl+ influx was observed in the erythrocytes incubated in MgCl2-sucrose media. The outward rate coefficient of 204Tl was also inhibited by DIDS and furosemide (by 65 and 52%, respectively). Rate coefficients of 204Tl influx and efflux decreased significantly in the red cells exposed to Cl-free media (NaNO3 or Mg(NO3)2-sucrose). Under these conditions addition of DIDS and furosemide led to only a small inhibition of Tl+ fluxes. There was a linear increase in Tl+ influx with rising of external Cl concentration within 80–155mm or HCO 3 concentration from 20 to 40mm when the sum of anions was kept constant (155mm) with NO 3 . The HCO 3 -stimulated Tl+ influx was completely blocked by 0.05mm DIDS but only 67% by 1mm furosemide. The present study provides direct evidence for the occurrence of Cl (HCO 3 )-dependent, DIDS-sensitive movement of Tl+ across the human erythrocyte membrane in both directions. Under physiological conditions, about half of net Tl+ fluxes occurs due to an anion exchange mechanism. Our data fail to detect a contribution of the Na-K-Cl cotransport system to Tl+ transport in human erythrocytes.

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  1. 1.

    Aickin, C.C., Brading, A.F. 1990. The effect of loop diuretics on Cl transport in smooth muscle of the guinea-pig vas deferens and taenia from the caecum. J. Physiol. 421:33–53

  2. 2.

    Alda, J.O., Garay, R. 1990. Chloride (or bicarbonate)-dependent copper uptake through the anion exchanger in human red blood cells. Am. J. Physiol. 259:C570-C576

  3. 3.

    Bakker-Grunwald, T. 1979. Movement of thallous ion across the ascites cell membrane. J. Membrane Biol. 47:171–183

  4. 4.

    Barrera, H., Gomez-Puyou, A. 1975. Characteristics of the movement of K+ across the mitochondrial membrane and the inhibitory action of Tl+. J. Biol. Chem. 250:5370–5374

  5. 5.

    Becker, B.F., Duhm, J. 1978. Evidence for anionic cation transport of lithium, sodium and potassium across the human erythrocyte membrane induced by divalent anions. J. Physiol. 282:149–168

  6. 6.

    Boron, W.F., Boulpeap, E.L. 1989. The electrogenic Na/HCO3 cotransporter. Kidney Int. 36:392–402

  7. 7.

    Brazy, P.C., Gunn, R.B. 1976. Furosemide inhibition of chloride transport in human red blood cells. J. Gen. Physiol. 68:583–599

  8. 8.

    Brismar, T., Coffins, V.P., Kesselberg, M. 1989. Thallium-201 uptake relates to membrane potential and potassium permeability in human glioma cells. Brain Res. 500:30–36

  9. 9.

    Britten, J.S., Blank, M. 1968. Thallium activation of the (Na+ + K+)-activated ATPase of rabbit kidney. Biochim. Biophys. Acta 159:160–166

  10. 10.

    Callahan, T.J., Goldstein, D.A. 1978. Anion inhibitor-sensitive unidirectional sodium movements in the human erythrocyte. J. Gen. Physiol. 72:87–100

  11. 11.

    Cavieres, J.D., Ellory, J.C. 1974. Thallium and the sodium pump in human red cells. J. Physiol. 243:243–266

  12. 12.

    Deepak, K., Zeidel, M.L., Ballermann, B.J., Brenner, B.M., Hebert, S.C. 1990. pH regulation and response to ANP in A10 cells differ markedly in the presence vs. absence of CO2-HCO 3 . Am. J. Physiol. 259:C471-C483

  13. 13.

    Diwan, J.J., Dase, M., Richardson, R., Aronson, D. 1979. Kinetics of Mg2+ flux into rat liver mitochondria. Biochemistry 18:2590–2595

  14. 14.

    Edwards, C., Vyskočil, F. 1984. The effects of the replacement of K+ by Tl+, Rb+ and NH 4 + on the muscle membrane potential. Gen. Physiol. Biophys. 3:259–264

  15. 15.

    Fitz, J.G., Persico, M., Scharschmidt, B.F. 1989. Electrophysiological evidence for Na+-coupled bicarbonate transport in cultured rat hepatocytes. Am. J. Physiol. 256:G491-G500

  16. 16.

    Funder, J. 1980. Alkali metal cation transport through the human erythrocyte membrane by the anion exchange mechanism. Acta Physiol. Scand. 108:31–37

  17. 17.

    Funder, J., Tosteson, D.C., Wieth, J.O. 1978. Effects of bicarbonate on lithium transport in human red cells. J. Gen. Physiol. 71:721–746

  18. 18.

    Hagiwara, S., Eaton, D.C., Stuart, A.E., Rosenthal, N.P. 1972. Cation selectivity of the resting membrane of squid axon. J. Membrane Biol. 9:373–384

  19. 19.

    Hagiwara, S., Miyazaki, S., Krasne, S., Ciani, S. 1977. Anomalous permeabilities of the egg cell membrane of a starfish in K+-Tl+ mixtures. J. Gen. Physiol. 70:269–281

  20. 20.

    Hoffmann, E.K. 1986. Anion transport systems in the plasma membrane of vertebrate cells. Biochim. Biophys. Acta 864:1–31

  21. 21.

    Johns, A., Cutshaw, S.V. 1983. Furosemide-sensitive thallium fluxes in smooth muscle of rabbit uterus. Am. J. Physiol. 245:F778-F783

  22. 22.

    Kalfakakou, V., Simons, T.J.B. 1990. Anionic mechanisms of zinc uptake across the human red cell membrane. J. Physiol. 421:485–497

  23. 23.

    Knauf, P. 1979. Erythrocyte anion exchange and the band 3 protein: Transport kinetics and molecular structure. Curr. Top. Membr. Transp. 12:251–363

  24. 24.

    Kreye, V.A.W., Bauer, P.K., Villhauer, I. 1981. Evidence for furosemide-sensitive active chloride transport in vascular smooth muscle. Eur. J. Pharmacol. 73:91–95

  25. 25.

    Lee, A.G. 1971. The Chemistry of Thallium. p. 336. Elsevier, Amsterdam

  26. 26.

    Lee, A.G. 1972. The coordination chemistry of thallium (I). Coordin. Chem. Rev. 8:289–349

  27. 27.

    McCall, D., Zimmer, L.J., Katz, A.M. 1985. Kinetics of thallium exchange in cultured rat myocardial cells. Circ. Res. 56:370–376

  28. 28.

    Nancollas, G.H. 1957. Thermodynamics of ion association. Faraday Discuss. Chem. Soc. 24:108–113

  29. 29.

    Nicoll, R.A. 1978. The blockade of GABA mediated responses in the frog spinal cord by ammonium ions and furosemide. J. Physiol. 283:121–132

  30. 30.

    Rangachari, P.K., McWade, D. 1986. Ouabain-insensitive, halide-sensitive Tl+ uptake by canine iliac arteries. Biochim. Biophys. Acta 854:251–256

  31. 31.

    Sherstobitov, A.O., Gusev, G.P., Skulskii, I.A. 1990. Transport of univalent thallium across the human red cell membrane. Cytology 32:239–244 (in Russian)

  32. 32.

    Simons, T.J.B. 1986. The role of anion transport in the passive movement of lead across the human red cell membrane. J. Physiol. 378:287–312

  33. 33.

    Skulskii, I.A., Manninen, V., Ġlasunov, V.V. 1990. Thallium and rubidium permeability of human and rat erythrocyte membrane. Gen. Physiol. Biophys. 9:39–44

  34. 34.

    Skulskii, I.A., Manninen, V., Järnefelt, J. 1978. Factors affecting the relative magnitude of the ouabain-sensitive and ouabain-insensitive fluxes of thallium ion in erythrocytes. Biochim. Biophys. Acta 506:233–241

  35. 35.

    Soleimani, M., Aronson, P.S. 1989. Ionic mechanism of a Na+-HCO 3 cotransport in rabbit renal basolateral membrane vesicles. J. Biol. Chem. 264:18302–18308

  36. 36.

    Torrubia, J.O.A., Garay, R. 1989. Evidence for a major route for zinc uptake in human red blood cells: (Zn(HCO3)2Cl) influx through the (Cl/HCO 3 ) anion exchanger. J. Cell. Physiol. 138:316–322

  37. 37.

    Townsley, M.C., Machen, T.E. 1989. Na-HCO3 cotransport in rabbit parietal cells. Am. J. Physiol. 257:G350-G356

  38. 38.

    Wieth, J.O. 1979. Bicarbonate exchange through the human red blood cell membrane determined with (14C) bicarbonate. J. Physiol. 294:521–539

  39. 39.

    Zerahn, K. 1983. Comparison between active transport of Tl+, K+ and Rb+ across the isolated short-circuited frog skin. J. Exp. Biol. 107:65–72

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Skulskii, I.A., Gusev, G.P., Sherstobitov, A.O. et al. Anion-dependent transport of thallous ions through human erythrocyte membrane. J. Membarin Biol. 130, 219–225 (1992). https://doi.org/10.1007/BF00240479

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Key words

  • thallium transport
  • anion exchanger
  • human erythrocytes