Abstract
Type l voltage-gated K+ channels in murine lymphocytes were studied under voltage clamp in cell-attached patches and in the whole-cell configuration. The kinetics of activation of whole-cell currents during depolarizing pulses could be fit by a single exponential after an initial delay. Deactivation upon repolarization of both macroscopic and microscopic currents was mono-exponential, except in Rb-Ringer or Cs- Ringer solution in which tail currents often displayed "hooks," wherein the current first increased or remained constant before decaying. In some cells type l currents were contaminated by a small component due to type n K+ channels, which deactivate approximately 10 times slower than type l channels. Both macroscopic and single channel currents could be dissected either kinetically or pharmacologically into these two K+ channel types. The ionic selectivity and conductance of type l channels were studied by varying the internal and external permeant ion. With 160 mM K+ in the cell, the relative permeability calculated from the reversal potential with the Goldman-Hodgkin-Katz equation was K+ (identical to 1.0) greater than Rb+ (0.76) greater than NH4+ = Cs+ (0.12) much greater than Na+ (less than 0.004). Measured 30 mV negative to the reversal potential, the relative conductance sequence was quite different: NH4+ (1.5) greater than K+ (identical to 1.0) greater than Rb+ (0.5) greater than Cs+ (0.06) much greater than Na+, Li+, TMA+ (unmeasurable). Single channel current rectification resembled that of the whole-cell instantaneous I-V relation. Anomalous mole-fraction dependence of the relative permeability PNH4/PK was observed in NH4(+)- K+ mixtures, indicating that the type l K+ channel is a multi-ion pore. Compared with other K+ channels, lymphocyte type l K+ channels are most similar to "g12" channels in myelinated nerve.
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- Adams D. J., Nonner W., Dwyer T. M., Hille B. Block of endplate channels by permeant cations in frog skeletal muscle. J Gen Physiol. 1981 Dec;78(6):593–615. doi: 10.1085/jgp.78.6.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Almers W., Armstrong C. M. Survival of K+ permeability and gating currents in squid axons perfused with K+-free media. J Gen Physiol. 1980 Jan;75(1):61–78. doi: 10.1085/jgp.75.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altman A., Theofilopoulos A. N., Weiner R., Katz D. H., Dixon F. J. Analysis of T cell function in autoimmune murine strains. Defects in production and responsiveness to interleukin 2. J Exp Med. 1981 Sep 1;154(3):791–808. doi: 10.1084/jem.154.3.791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Bezanilla F. Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol. 1974 May;63(5):533–552. doi: 10.1085/jgp.63.5.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Lopez-Barneo J. External calcium ions are required for potassium channel gating in squid neurons. Science. 1987 May 8;236(4802):712–714. doi: 10.1126/science.2437654. [DOI] [PubMed] [Google Scholar]
- Armstrong C. M., Matteson D. R. The role of calcium ions in the closing of K channels. J Gen Physiol. 1986 May;87(5):817–832. doi: 10.1085/jgp.87.5.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M. Potassium pores of nerve and muscle membranes. Membranes. 1975;3:325–358. [PubMed] [Google Scholar]
- Bezanilla F., Armstrong C. M. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J Gen Physiol. 1972 Nov;60(5):588–608. doi: 10.1085/jgp.60.5.588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Chandler W. K., Meves H. Sodium and potassium currents in squid axons perfused with fluoride solutions. J Physiol. 1970 Dec;211(3):623–652. doi: 10.1113/jphysiol.1970.sp009297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chandy K. G., DeCoursey T. E., Fischbach M., Talal N., Cahalan M. D., Gupta S. Altered K+ channel expression in abnormal T lymphocytes from mice with the lpr gene mutation. Science. 1986 Sep 12;233(4769):1197–1200. doi: 10.1126/science.2426784. [DOI] [PubMed] [Google Scholar]
- Clay J. R., Shlesinger M. F. Effects of external cesium and rubidium on outward potassium currents in squid axons. Biophys J. 1983 Apr;42(1):43–53. doi: 10.1016/S0006-3495(83)84367-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coronado R., Latorre R., Mautner H. G. Single potassium channels with delayed rectifier behavior from lobster axon membranes. Biophys J. 1984 Jan;45(1):289–299. doi: 10.1016/S0006-3495(84)84155-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- DeCoursey T. E., Jacobs E. R., Silver M. R. Potassium currents in rat type II alveolar epithelial cells. J Physiol. 1988 Jan;395:487–505. doi: 10.1113/jphysiol.1988.sp016931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Decoursey T. E., Chandy K. G., Gupta S., Cahalan M. D. Two types of potassium channels in murine T lymphocytes. J Gen Physiol. 1987 Mar;89(3):379–404. doi: 10.1085/jgp.89.3.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drouin H., The R. The effect of reducing extracellular pH on the membrane currents of the ranvier node. Pflugers Arch. 1969;313(1):80–88. doi: 10.1007/BF00586331. [DOI] [PubMed] [Google Scholar]
- Dubois J. M. Capsaicin blocks one class of K+ channels in the frog node of Ranvier. Brain Res. 1982 Aug 12;245(2):372–375. doi: 10.1016/0006-8993(82)90820-4. [DOI] [PubMed] [Google Scholar]
- Dubois J. M. Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J Physiol. 1981 Sep;318:297–316. doi: 10.1113/jphysiol.1981.sp013865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dubois J. M. Simultaneous changes in the equilibrium potential and potassium conductance in voltage clamped Ranvier node in the frog. J Physiol. 1981 Sep;318:279–295. doi: 10.1113/jphysiol.1981.sp013864. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gay L. A., Stanfield P. R. The selectivity of the delayed potassium conductance of frog skeletal muscle fibers. Pflugers Arch. 1978 Dec 28;378(2):177–179. doi: 10.1007/BF00584453. [DOI] [PubMed] [Google Scholar]
- Gilbert D. L., Ehrenstein G. Effect of divalent cations on potassium conductance of squid axons: determination of surface charge. Biophys J. 1969 Mar;9(3):447–463. doi: 10.1016/S0006-3495(69)86396-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilly W. F., Armstrong C. M. Slowing of sodium channel opening kinetics in squid axon by extracellular zinc. J Gen Physiol. 1982 Jun;79(6):935–964. doi: 10.1085/jgp.79.6.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grissmer S., Cahalan M. D., Chandy K. G. Abundant expression of type l K+ channels. A marker for lymphoproliferative diseases? J Immunol. 1988 Aug 15;141(4):1137–1142. [PubMed] [Google Scholar]
- 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]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Hille B. Charges and potentials at the nerve surface. Divalent ions and pH. J Gen Physiol. 1968 Feb;51(2):221–236. doi: 10.1085/jgp.51.2.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hille B. Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J Gen Physiol. 1975 Nov;66(5):535–560. doi: 10.1085/jgp.66.5.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hille B. Potassium channels in myelinated nerve. Selective permeability to small cations. J Gen Physiol. 1973 Jun;61(6):669–686. doi: 10.1085/jgp.61.6.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hille B., Schwarz W. Potassium channels as multi-ion single-file pores. J Gen Physiol. 1978 Oct;72(4):409–442. doi: 10.1085/jgp.72.4.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hu S., Rubly N. Effects of morphine on ionic currents in frog node of Ranvier. Eur J Pharmacol. 1983 Nov 25;95(3-4):185–192. doi: 10.1016/0014-2999(83)90633-7. [DOI] [PubMed] [Google Scholar]
- Ilyin V. I., Katina I. E., Lonskii A. V., Makovsky V. S., Polishchuk E. V. The Cole-Moore effect in nodal membrane of the frog Rana ridibunda: evidence for fast and slow potassium channels. J Membr Biol. 1980 Dec 30;57(3):179–193. doi: 10.1007/BF01869586. [DOI] [PubMed] [Google Scholar]
- Jonas P., Bräu M. E., Hermsteiner M., Vogel W. Single-channel recording in myelinated nerve fibers reveals one type of Na channel but different K channels. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7238–7242. doi: 10.1073/pnas.86.18.7238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawa K. Transient outward currents and changes of their gating properties after cell activation in thrombocytes of the newt. J Physiol. 1987 Apr;385:189–205. doi: 10.1113/jphysiol.1987.sp016491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis R. S., Cahalan M. D. Subset-specific expression of potassium channels in developing murine T lymphocytes. Science. 1988 Feb 12;239(4841 Pt 1):771–775. doi: 10.1126/science.2448877. [DOI] [PubMed] [Google Scholar]
- Lucero M. T., Pappone P. A. Voltage-gated potassium channels in brown fat cells. J Gen Physiol. 1989 Mar;93(3):451–472. doi: 10.1085/jgp.93.3.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Matteson D. R., Swenson R. P., Jr External monovalent cations that impede the closing of K channels. J Gen Physiol. 1986 May;87(5):795–816. doi: 10.1085/jgp.87.5.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mozhaeva G. N., Naumov A. P. Vliianie poverkhnostnogo zariada na statsionarnuiu kalievuiu provodimost' membrany perekhvata Ranv'e. 3. Deistvie dvukhvalentnykh kationov. Biofizika. 1972 Sep-Oct;17(5):801–808. [PubMed] [Google Scholar]
- PICKARD W. F., LETTVIN J. Y., MOORE J. W., TAKATA M., POOLER J., BERNSTEIN T. CAESUM IONS DO NOT PASS THE MEMBRANE OF THE GIANT AXON. Proc Natl Acad Sci U S A. 1964 Nov;52:1177–1183. doi: 10.1073/pnas.52.5.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palti Y., Ganot G., Stämpfli R. Effect of conditioning potential on potassium current kinetics in the frog node. Biophys J. 1976 Mar;16(3):261–273. doi: 10.1016/S0006-3495(76)85686-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plant T. D. The effects of rubidium ions on components of the potassium conductance in the frog node of Ranvier. J Physiol. 1986 Jun;375:81–105. doi: 10.1113/jphysiol.1986.sp016107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reuter H., Stevens C. F. Ion conductance and ion selectivity of potassium channels in snail neurones. J Membr Biol. 1980 Dec 15;57(2):103–118. doi: 10.1007/BF01868997. [DOI] [PubMed] [Google Scholar]
- Röper J., Schwarz J. R. Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. J Physiol. 1989 Sep;416:93–110. doi: 10.1113/jphysiol.1989.sp017751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sands S. B., Lewis R. S., Cahalan M. D. Charybdotoxin blocks voltage-gated K+ channels in human and murine T lymphocytes. J Gen Physiol. 1989 Jun;93(6):1061–1074. doi: 10.1085/jgp.93.6.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwarz J. R., Vogel W. Potassium inactivation in single myelinated nerve fibres of Xenopus laevis. Pflugers Arch. 1971;330(1):61–73. doi: 10.1007/BF00588735. [DOI] [PubMed] [Google Scholar]
- Shapiro B. I. Effects of strychnine on the potassium conductance of the frog node of Ranvier. J Gen Physiol. 1977 Jun;69(6):897–914. doi: 10.1085/jgp.69.6.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shapiro M. S., DeCoursey T. E. Permeant ion effects on the gating kinetics of the type L potassium channel in mouse lymphocytes. J Gen Physiol. 1991 Jun;97(6):1251–1278. doi: 10.1085/jgp.97.6.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shibasaki T. Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol. 1987 Jun;387:227–250. doi: 10.1113/jphysiol.1987.sp016571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spruce A. E., Standen N. B., Stanfield P. R. Rubidium ions and the gating of delayed rectifier potassium channels of frog skeletal muscle. J Physiol. 1989 Apr;411:597–610. doi: 10.1113/jphysiol.1989.sp017593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swenson R. P., Jr, Armstrong C. M. K+ channels close more slowly in the presence of external K+ and Rb+. Nature. 1981 Jun 4;291(5814):427–429. doi: 10.1038/291427a0. [DOI] [PubMed] [Google Scholar]
- Wagoner P. K., Oxford G. S. Cation permeation through the voltage-dependent potassium channel in the squid axon. Characteristics and mechanisms. J Gen Physiol. 1987 Aug;90(2):261–290. doi: 10.1085/jgp.90.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wofsy D., Murphy E. D., Roths J. B., Dauphinée M. J., Kipper S. B., Talal N. Deficient interleukin 2 activity in MRL/Mp and C57BL/6J mice bearing the lpr gene. J Exp Med. 1981 Nov 1;154(5):1671–1680. doi: 10.1084/jem.154.5.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woodhull A. M. Ionic blockage of sodium channels in nerve. J Gen Physiol. 1973 Jun;61(6):687–708. doi: 10.1085/jgp.61.6.687. [DOI] [PMC free article] [PubMed] [Google Scholar]