Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1990 Mar;422:103–126. doi: 10.1113/jphysiol.1990.sp017975

Modulation of potassium channels in human T lymphocytes: effects of temperature.

P A Pahapill 1, L C Schlichter 1
PMCID: PMC1190123  PMID: 2352174

Abstract

1. The predominant channels found in lymphocytes with patch-clamp whole-cell recordings are voltage-gated K+ channels. Several lines of evidence suggest that these channels are involved in lymphocyte function. Most lymphocyte functions are temperature sensitive and have not been correlated with electrophysiology at different temperatures. We have examined the effect of temperature on the voltage-dependent K+ channel in normal human T lymphocytes. Both macroscopic current and single-channel events were studied with whole-cell recordings at temperatures from 5 to 42 degrees C. 2. Peak conductance, activation rate, inactivation rate and rate of recovery from inactivation all increased progressively as the temperature increased. The effect of temperature on channel opening processes was greater at low temperatures. In contrast, the inactivation process was most sensitive to temperature changes above room temperature. Arrhenius plots of conductance and kinetic parameters were curvilinear with no obvious break-points. 3. The increase in whole-cell conductance at 37 degrees C was due to both an increase in the single-channel conductance and in the probability that each channel is open at any time. 4. K+ currents were fitted by Hodgkin-Huxley equations with n4j kinetics providing the best description of the currents at all temperatures tested. 5. Steady-state activation- and inactivation-voltage curves shifted in opposite directions with warming, resulting in a greater area of overlap of the curves ('window' current). The increase in resting K+ channel activity predicted by a greater window current was confirmed with single-channel measurements. 6. The present study has shown that the behaviour of K+ channels in human T lymphocytes is temperature dependent.

Full text

PDF
103

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aldrich R. W. Inactivation of voltage-gated delayed potassium current in molluscan neurons. A kinetic model. Biophys J. 1981 Dec;36(3):519–532. doi: 10.1016/S0006-3495(81)84750-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beam K. G., Donaldson P. L. A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C. J Gen Physiol. 1983 Apr;81(4):485–512. doi: 10.1085/jgp.81.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bregestovski P., Redkozubov A., Alexeev A. Elevation of intracellular calcium reduces voltage-dependent potassium conductance in human T cells. 1986 Feb 27-Mar 5Nature. 319(6056):776–778. doi: 10.1038/319776a0. [DOI] [PubMed] [Google Scholar]
  4. Cahalan M. D., Chandy K. G., DeCoursey T. E., Gupta S. A voltage-gated potassium channel in human T lymphocytes. J Physiol. 1985 Jan;358:197–237. doi: 10.1113/jphysiol.1985.sp015548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chen J. H., Schulman H., Gardner P. A cAMP-regulated chloride channel in lymphocytes that is affected in cystic fibrosis. Science. 1989 Feb 3;243(4891):657–660. doi: 10.1126/science.2464852. [DOI] [PubMed] [Google Scholar]
  6. Cheung R. K., Grinstein S., Dosch H. M., Gelfand E. W. Volume regulation by human lymphocytes: characterization of the ionic basis for regulatory volume decrease. J Cell Physiol. 1982 Aug;112(2):189–196. doi: 10.1002/jcp.1041120206. [DOI] [PubMed] [Google Scholar]
  7. Choquet D., Korn H. Dual effects of serotonin on a voltage-gated conductance in lymphocytes. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4557–4561. doi: 10.1073/pnas.85.12.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Choquet D., Sarthou P., Primi D., Cazenave P. A., Korn H. Cyclic AMP-modulated potassium channels in murine B cells and their precursors. Science. 1987 Mar 6;235(4793):1211–1214. doi: 10.1126/science.2434998. [DOI] [PubMed] [Google Scholar]
  9. DeCoursey T. E., Chandy K. G., Gupta S., Cahalan M. D. Voltage-gated K+ channels in human T lymphocytes: a role in mitogenesis? Nature. 1984 Feb 2;307(5950):465–468. doi: 10.1038/307465a0. [DOI] [PubMed] [Google Scholar]
  10. Decoursey T. E., Chandy K. G., Gupta S., Cahalan M. D. Mitogen induction of ion channels in murine T lymphocytes. J Gen Physiol. 1987 Mar;89(3):405–420. doi: 10.1085/jgp.89.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deutsch C., Krause D., Lee S. C. Voltage-gated potassium conductance in human T lymphocytes stimulated with phorbol ester. J Physiol. 1986 Mar;372:405–423. doi: 10.1113/jphysiol.1986.sp016016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deutsch C., Slater L., Goldstein P. Volume regulation of human peripheral blood lymphocytes and stimulated proliferation of volume-adapted cells. Biochim Biophys Acta. 1982 Nov 17;721(3):262–267. doi: 10.1016/0167-4889(82)90078-7. [DOI] [PubMed] [Google Scholar]
  13. Eisen S. A., Wedner H. J., Parker C. W. Isolation of pure human peripheral blood T-lymphocytes using nylon wool columns. Immunol Commun. 1972;1(6):571–577. doi: 10.3109/08820137209022965. [DOI] [PubMed] [Google Scholar]
  14. Fukushima Y., Hagiwara S., Henkart M. Potassium current in clonal cytotoxic T lymphocytes from the mouse. J Physiol. 1984 Jun;351:645–656. doi: 10.1113/jphysiol.1984.sp015268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grinstein S., Dixon S. J. Ion transport, membrane potential, and cytoplasmic pH in lymphocytes: changes during activation. Physiol Rev. 1989 Apr;69(2):417–481. doi: 10.1152/physrev.1989.69.2.417. [DOI] [PubMed] [Google Scholar]
  16. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krause D., Lee S. C., Deutsch C. Forskolin effects on the voltage-gated K+ conductance of human T cells. Pflugers Arch. 1988 Jul;412(1-2):133–140. doi: 10.1007/BF00583742. [DOI] [PubMed] [Google Scholar]
  18. Kuno M., Goronzy J., Weyand C. M., Gardner P. Single-channel and whole-cell recordings of mitogen-regulated inward currents in human cloned helper T lymphocytes. Nature. 1986 Sep 18;323(6085):269–273. doi: 10.1038/323269a0. [DOI] [PubMed] [Google Scholar]
  19. Lee S. C., Price M., Prystowsky M. B., Deutsch C. Volume response of quiescent and interleukin 2-stimulated T-lymphocytes to hypotonicity. Am J Physiol. 1988 Feb;254(2 Pt 1):C286–C296. doi: 10.1152/ajpcell.1988.254.2.C286. [DOI] [PubMed] [Google Scholar]
  20. Lewis R. S., Cahalan M. D. The plasticity of ion channels: parallels between the nervous and immune systems. Trends Neurosci. 1988 May;11(5):214–218. doi: 10.1016/0166-2236(88)90129-4. [DOI] [PubMed] [Google Scholar]
  21. Mahaut-Smith M. P., Schlichter L. C. Ca2(+)-activated K+ channels in human B lymphocytes and rat thymocytes. J Physiol. 1989 Aug;415:69–83. doi: 10.1113/jphysiol.1989.sp017712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martz E. Mechanism of specific tumor-cell lysis by alloimmune T lymphocytes: resolution and characterization of discrete steps in the cellular interaction. Contemp Top Immunobiol. 1977;7:301–361. doi: 10.1007/978-1-4684-3054-7_9. [DOI] [PubMed] [Google Scholar]
  23. Matteson D. R., Deutsch C. K channels in T lymphocytes: a patch clamp study using monoclonal antibody adhesion. Nature. 1984 Feb 2;307(5950):468–471. doi: 10.1038/307468a0. [DOI] [PubMed] [Google Scholar]
  24. Romey G., Chicheportiche R., Lazdunski M. Transition temperatures of the electrical activity of ion channels in the nerve membrane. Biochim Biophys Acta. 1980 Nov 18;602(3):610–620. doi: 10.1016/0005-2736(80)90339-9. [DOI] [PubMed] [Google Scholar]
  25. Schlichter L., Sidell N., Hagiwara S. K channels are expressed early in human T-cell development. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5625–5629. doi: 10.1073/pnas.83.15.5625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schlichter L., Sidell N., Hagiwara S. Potassium channels mediate killing by human natural killer cells. Proc Natl Acad Sci U S A. 1986 Jan;83(2):451–455. doi: 10.1073/pnas.83.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sidell N., Schlichter L. C., Wright S. C., Hagiwara S., Golub S. H. Potassium channels in human NK cells are involved in discrete stages of the killing process. J Immunol. 1986 Sep 1;137(5):1650–1658. [PubMed] [Google Scholar]
  28. Sidell N., Schlichter L. Retinoic acid blocks potassium channels in human lymphocytes. Biochem Biophys Res Commun. 1986 Jul 31;138(2):560–567. doi: 10.1016/s0006-291x(86)80533-2. [DOI] [PubMed] [Google Scholar]
  29. Trinchieri G., Perussia B. Human natural killer cells: biologic and pathologic aspects. Lab Invest. 1984 May;50(5):489–513. [PubMed] [Google Scholar]
  30. Walsh K. B., Kass R. S. Regulation of a heart potassium channel by protein kinase A and C. Science. 1988 Oct 7;242(4875):67–69. doi: 10.1126/science.2845575. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES