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Ion channels in lymphocytes

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Abstract

The advent of the gigaohm-seal recording technique has enabled the study of the electrical properties of small cells, such as individual lymphocytes. Recent studies using this technique in combination with standard immunological and biochemical techniques indicate that cells of the immune system may utilize ion channels, similar in properties to those described in nerve and muscle, in the process of activation. For example, potassium channels may be required for T-lymphocyte mitogenesis and calcium channels for antibody production. This article summarizes these recent reports.

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References

  1. Currie GA: Effect of phytohemagglutinin on the surface charge of human and murine lymphocytes. Nature 216:694–695, 1967

    Google Scholar 

  2. Kiefer H, Blume AJ, Kaback HR: Membrane potential changes during mitogenic stimulation of mouse spleen lymphocytes. Proc Natl Acad Sci USA 77:2200–2204, 1980

    Google Scholar 

  3. Felber SM, Brand MD: Early plasma-membrane-potential changes during stimulation of lymphocytes by concanavalin A. Biochem J 210:885–891, 1983

    Google Scholar 

  4. Shapiro HM, Natale PJ, Kamentsky LA: Estimation of membrane potentials of individual lymphocytes by flow cytometry. Proc Natl Acad Sci USA 76:5728–5730, 1979

    Google Scholar 

  5. Tsien RY, Pozzan T, Rink T: T-cell mitogens cause early changes in cytoplasmic free Ca2+ and membrane potential in lymphocytes. Nature 295:68–71, 1982

    Google Scholar 

  6. Quastel MR, Kaplan JG: Early stimulation of potassium uptake in lymphocytes treated with phytochemagglutinin. Exp Cell Res 63:230–233, 1970

    Google Scholar 

  7. Segel GB, Simon W, Lichtman MA: Regulation of sodium and potassium transport in phytohemagglutinin-stimulated human blood lymphocytes. J Clin Invest 64:834–841, 1979

    Google Scholar 

  8. Metcalfe JC, Pozzan T, Smith GA, Hesketh TR: A calcium hypothesis for the control of cell growth. Biochem Soc Symp 45:1–26, 1980

    Google Scholar 

  9. Freedman MH: Investigations on the nature and significance of early calcium fluxes observed in mitogen induced T and B lymphocytes. Cell Immunol 44:290–313, 1979

    Google Scholar 

  10. Kaplan JG: Membrane cation transport and the control of proliferation of mammalian cells. Annu Rev Physiol 40:19–41, 1978

    Google Scholar 

  11. Hesketh TR, Bavetta S, Smith GA, Metcalfe JC: Duration of the calcium signal in the mitogenic stimulation of thymocytes. Biochem J 214:575–579, 1983

    Google Scholar 

  12. Bryant SH: The electrophysiology of myotonia with a review of congenital myotonia of goats.In New Developments in Electromyography and Clinical Neurophysiology, Vol. 1, JE Desmedt (ed). Basel, Karger, 1973, pp 420–450

    Google Scholar 

  13. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ: Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch Physiol 391:85–100, 1981

    Google Scholar 

  14. DeCoursey TE, Chandy KG, Gupta S, Cahalan MD: Volt-age-gated K+ channels in human T lymphocytes: A role in mitogenesis? Nature 307:465–468, 1984

    Google Scholar 

  15. Matteson DR, Deutsch C: K channels in T-lymphocytes: A patch clamp study using monoclonal antibody adhesion. Nature 307:468–471, 1984

    Google Scholar 

  16. Cahalan MD, Chandy KG, DeCoursey TE, Gupta S: A voltage-gated potassium channel in human T lymphocytes. J Physiol (Lond), 1985 (in press)

  17. Fukushima Y, Hagiwara S, Henkart M: (1984). Potassium current in clonal cytotoxic T lymphocytes from the mouse. J Physiol (Lond) 351:645–656, 1984

    Google Scholar 

  18. Ypey DL, Clapham DE: Development of a delayed outward-rectifying K+ conductance in cultured mouse peritoneal macrophages. Proc Natl Acad Sci USA 81:3083–3087, 1984

    Google Scholar 

  19. Hamilton LJ, Kaplan JG: Flux of86Rb in activated human lymphocytes. Can J Biochem 55:774–778, 1977

    Google Scholar 

  20. Segel GB, Gordon BR, Lichtman MA, Hollander MM, Klemperer MR: Exodus of42K+ and86Rb+ from rat thymic and human blood lymphocytes exposed to phytohemagglutinin. J Cell Physiol 87:337–344, 1975

    Google Scholar 

  21. Segel GB, Lichtman MA: Potassium transport in human blood lymphocytes treated with phytohemagglutinin. J Clin Invest 58:1358–1369, 1976

    Google Scholar 

  22. Owens T, Kaplan JG: Increased cationic ion fluxes in stimulated lymphocytes of the mouse: Response of enriched B- and T-cell subpopulations to B- and T-cell mitogens. Can J Biochem 58:831–839, 1980

    Google Scholar 

  23. Chandy KG, DeCoursey TE, Cahalan MD, McLaughlin C, Gupta S: Voltage-gated potassium channels are required for T lymphocyte activation. J Exp Med 160:369–385, 1984

    Google Scholar 

  24. DeCoursey TE, Chandy KG, Gupta S, Cahalan MD: Pharmacology of human T lymphocyte K channels. Biophys J 45:144a, 1984

    Google Scholar 

  25. Blitstein-Willinger E, Diamantstein T: Inhibition by Isoptin (a calcium antagonist) of the mitogenic stimulation of lymphocytes prior to the S phase. Immunology 34:303–307, 1978

    Google Scholar 

  26. Murphy ED, Roths JB:In Genetic Control of Autoimmune Diseases, NR Rose, PE Bigazzi, NL Warner (eds). New York, Elsevier/North-Holland, 1978, pp 207–221

    Google Scholar 

  27. Theofilopoulos AN, Eisenberg RA, Bourdon MA, Crowell JS, Dixon FJ: Distribution of lymphocytes identified by surface markers in murine strains with systemic lupus-like syndromes. J Exp Med 149:516–534, 1979

    Google Scholar 

  28. Wofsy DE, Murphy ED, Roths JB, Dauphinee MJ, Kipper SB, Talal N: Deficient interleukin 2 activity in MRL/Mp and C57BL/6J mice bearing the lpr gene. J Exp Med 154:1671–1680, 1981

    Google Scholar 

  29. Rupert BL, Ford RJ, Maizel AL: T-cell mediated suppression in the MRL mouse. Cell Immunol 61:40–51, 1981

    Google Scholar 

  30. DeCoursey TE, Chandy KG, Fischbach M, Talal N, Cahalan MD, Gupta S: Differences in ion channel expression in T lymphocytes from MRL-lpr and MRL-+/+ mice. Fed Proc 43:1736, 1984

    Google Scholar 

  31. Russel JH, Dobos CB: Accelerated86Rb+ (K+) release from the cytotoxic T lymphocyte is a physiologic event associated with delivery of lethal hit. J Immunol 131:1138–1141, 1983

    Google Scholar 

  32. Grinstein S, Dupre A, Rothstein A: Volume regulation by human lymphocytes. J Gen Physiol 79:849–868, 1982

    Google Scholar 

  33. Cheung RK, Grinstein S, Gelfand EW: Volume regulation by human lymphocytes. J Clin Invest 70:632–638, 1982

    Google Scholar 

  34. Grinstein S, Clarke CA, Rothstein A, Gelfand EW: Volume-induced anion conductance in human B lymphocytes is cation independent. Am J Physiol 245:C160-C163, 1983

    Google Scholar 

  35. Sarkadi B, Mack E, Rothstein A: Ionic events during the volume response of human peripheral blood lymphocytes to hypotonic media. J Gen Physiol 83:497–512, 1984

    Google Scholar 

  36. Allwood G, Asherson GL, Davey MJ, Goodford PJ: The early uptake of radioactive calcium by human lymphocytes treated with phytohaemagglutinin. Immunology 21:509–516, 1971

    Google Scholar 

  37. Freedman MH, Raff MC, Gomperts B: Induction of increased calcium uptake in mouse T lymphocytes by concanavalin A and its modulation by cyclic nucleotides. Nature (Lond) 255:378–382, 1975

    Google Scholar 

  38. Freedman MH, Gelfand EW: Post recognition ion dependent events in mitogen induced lymphocyte proliferation and in cytotoxic effector cell responses.In Immunology of Receptors, B Cinader (ed). New York, Marcel Dekker, 1977, pp 97–114

    Google Scholar 

  39. Whitney RB, Sutherland RM: Enhanced uptake of calcium by transforming lymphocytes. Cell Immunol 5:137–147, 1972

    Google Scholar 

  40. Greene WC, Parker CM, Parker CW: Calcium and lymphocyte activation. Cell Immunol 25:74–89, 1976

    Google Scholar 

  41. Hesketh TR, Smith GA, Houslay MD, Warren GB, Metcalfe JC: Is an early calcium influx necessary to stimulate lymphocytes? Nature 267:490–492, 1977

    Google Scholar 

  42. Luckasen JR, White JG, Kersey JH: Mitogenic properties of calcium ionophore A23187. Proc Natl Acad Sci USA 71:5088–5090, 1974

    Google Scholar 

  43. Hesketh TR, Smith GA, Moore JP, Taylor MV, Metcalfe JC: Free cytoplasmic calcium concentration and the mitogenic stimulation of lymphocytes. J Biol Chem 258:4876–4882, 1983

    Google Scholar 

  44. Weiss A, Imboden J, Shoback D, Stobo J: Role of T3 surface molecules in human T-cell activation: T3-dependent activation results in a rise of cytoplasmic calcium. Proc Natl Acad Sci USA 81:4169–4173, 1984

    Google Scholar 

  45. Imboden J, Weiss A, Shoback D, Stobo J: Perturbation of the T cell antigen receptor complex increases cytoplasmic free calcium. Clin Res 32:505A, 1984

    Google Scholar 

  46. Fukushima Y, Hagiwara S: Voltage-gated Ca2+ channel in mouse myeloma cells. Proc Natl Acad Sci USA 80:2240–2242, 1983

    Google Scholar 

  47. Fukushima Y, Hagiwara S: Parallel changes of Ca current and immunoglobulin secretion during the tissue culture cycle. Biophys J 45:35a, 1984

    Google Scholar 

  48. Inoue I: Activation-inactivation of potassium channels and development of the potassium-channel spike in internally perfused squid giant axons. J Gen Physiol 78:43–61, 1981

    Google Scholar 

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Authors and Affiliations

  1. Division of Basic and Clinical Immunology, Department of Medicine, University of California, 92717, Irvine, California

    K. G. Chandy & S. Gupta

  2. Department of Physiology and Biophysics, University of California, 92717, Irvine, California

    T. E. Decoursey & M. D. Cahalan

Authors
  1. K. G. Chandy
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  2. T. E. Decoursey
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  3. M. D. Cahalan
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  4. S. Gupta
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Chandy, K.G., Decoursey, T.E., Cahalan, M.D. et al. Ion channels in lymphocytes. J Clin Immunol 5, 1–6 (1985). https://doi.org/10.1007/BF00915161

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