Abstract
The properties of the voltage- and time-dependent outward current in single smooth muscle cells isolated from the rat anococcygeus were studied. The outward current was activated by depolarizations to membrane potentials positive to −40 mV. Activation followed third order kinetics; at + 20 mV, the time for the current to reach half its maximal amplitude was around 55 ms. The current inactivated with a time course that could best be described by a single exponential with a time constant around 1500 ms. The steady-state inactivation curve was voltage dependent over the range −110 to −30 mV, with a half-inactivation point of −67 mV. Recovery from inactivation followed an exponential time course with a time constant of around 770 ms at −90 mV. Deactivating tail current analysis revealed that a 10-fold change in the extracellular potassium ion concentration resulted in a 42 mV change in the reversal potential of the current. The current was blocked by 4-aminopyridine, tetraethylammonium, quinine and verapamil with IC50's — the concentrations producing 50% inhibition of the peak current — of 2 mM, 4 mM, 12 μM and 20 μM respectively. The current was not blocked by Toxin I (100 nM) or glibenclamide (10 μM). The current was still present in cells containing 5 mM EGTA; in these cells, replacing extracellular calcium with cadmium depressed the peak current by around 12%. This could be explained, at least in part, by a negative shift in the voltage dependence of inactivation.
Similar content being viewed by others
References
Adrian RH, Chandler WK, Hodgkin AL (1970) Voltage-clamp experiments in striated muscle fibres. J Physiol (Lond) 208:607–644
Amedee T, Benham CD, Bolton TB, Byrne NG, Large WA (1990) Potassium, chloride and non-selective cation conductances opened by noradrenaline in rabbit ear artery cells. J Physiol (Lond) 423:551–568
Beech DJ, Bolton TB (1989) Properties of the cromakaliminduced potassium conductance in smooth muscle cells isolated from the rabbit portal vein. Br J Pharmacol 98:851–864
Beech DJ, Bolton TB (1989) A voltage-dependent outward current with fast kinetics in single smooth muscle cells isolated from rabbit portal vein. J Physiol (Lond) 412:397–414
Beech DJ, Bolton TB (1989) Two components of potassium current activated by depolarization of single smooth muscle cells from the rabbit portal vein. J Physiol (Lond) 418:293–309
Byrne NG, Large WA (1987) Action of noradrenaline on single smooth muscle cells freshly dispersed from the rat anococcygeus muscle. J Physiol (Lond) 389:513–525
Castle NA, Haylett DG, Jenkinson DH (1989) Toxins in the characterization of potassium channels. Trends Neurosci 12:59–65
Catterall WA (1988) Structure and function of voltage-sensitive ion channels. Science 242:50–61
Fishman MC, Spector I (1981) Potassium current suppression by quinidine reveals additional calcium currents in neuroblastoma cells. Proc Natl Acad Sci USA 78:5245–5249
Gillespie JS (1972) The rat anococcygeus muscle and its response to nerve stimulation and to some drugs. Br J Pharmacol 45:404–416
Gillespie JS (1980) The physiology and pharmacology of the anococcygeus muscle. Trends Pharmacol Sci 1:453–457
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100
Hermann A, Gorman ALF (1984) Actions of quinidine on ionic currents of molluscan pacemaker neurons. J Gen Physiol 83:919–940
Hille B (1984) Ionic channels of excitable membranes. Sinauer, Massachusetts
Hisada T, Kurachi Y, Sugimoto T (1990) Properties of membrane currents in isolated smooth muscle cells from guinea-pig trachea. Pflügers Arch 416:151–161
Imaizumi Y, Muraki K, Watanabe M (1989) Ionic currents in single smooth muscle cells from the ureter of the guinea-pig. J Physiol (Lond) 411:131–159
Isacoff EY, Jan YN, Lan LY (1990) Evidence for the formation of heteromultimeric potassium channels in Xenopus oocytes. Nature 345:531–534
Kajioka S, Nahashima M, Kitamura K, Kuriyama H (1991) Mechanisms of vasodilation induced by potassium-channel activators. Clin Sci 81:129–139
Kotlikoff MI (1990) Potassium currents in canine airway smooth muscle cells. Am J Physiol 259:L384-L395
Lang RJ (1989) Identification of the major membrane currents in freshly dispersed single smooth muscle cells of guinea-pig ureter. J Physiol (Lond) 412:375–395
Lefevre IA, Coulombe A, Coraboeuf E (1991) The calcium antagonist D600 inhibits calcium-independent transient outward current in isolated rat ventricular myocytes. J Physiol (Lond) 432:65–80
Mayer ML, Sugiyama K (1988) A modulatory action of divalent cations on transient outward current in cultured rat sensory neurones. J Physiol (Lond) 396:417–433
McFadzean I, England S (1992) Properties of the inactivating outward current in single smooth muscle cells isolated from the rat anococcygeus. J Physiol (Lond) 446:248 P
Miyoshi H, Urabe T, Fujiwara A (1991) Electrophysiological properties of membrane currents in single myometrial cells isolated from pregnant rats. Pflügers Arch 419:386–393
Muraki K, Imaizumi Y, Kojima T, Watanabe M (1990) Effects of tetraethylammonium and 4-aminopyridine on outward currents and excitability in canine tracheal smooth muscle cells. Br J Pharmacol 100:507–515
Okabe K, Kitamura K, Kuriyama H (1987) Features of 4-aminopyridine sensitive outward current observed in single smooth muscle cells from the rabbit pulmonary artery. Pflügers Arch 409:561–568
Robbins J, Sim JA (1990) A transient outward current in NG108-15 neuroblastoma × glioma hybrid cells. Pflügers Arch 416:130–137
Rogawski MA (1985) The A-current: How ubiquitous a feature of excitable cells is it? Trends Neurosci 8:214–219
Ruppersberg JP, Schroter KH, Sakmann B, Stocker M, Sewing S, Pongs O (1990) Heteromultimeric channels formed by rat brain potassium-channel proteins. Nature 345:535–537
Terada K, Kitamura K, Kuriyama H (1987) Different inhibitions of the voltage-dependent K+ current by Ca2+ antagonists in the smooth muscle cell membrane of rabbit small intestine. Pflügers Arch 408:558–564
Thompson S (1982) Aminopyridine block of transient potassium current. J Gen Physiol 80:1–18
Volk KA, Matsuda JJ, Shibata EF (1991) A voltage-dependent potassium current in rabbit coronary artery smooth muscle cells. J Physiol (Lond) 439:751–768
Wong B (1981) Quinidine interactions with Myxicola giant axons. Mol Pharmacol 20:98–106
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
McFadzean, I., England, S. Properties of the inactivating outward current in single smooth muscle cells isolated from the rat anococcygeus. Pflügers Arch 421, 117–124 (1992). https://doi.org/10.1007/BF00374817
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00374817