Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1989 Apr;411:131–159. doi: 10.1113/jphysiol.1989.sp017565

Ionic currents in single smooth muscle cells from the ureter of the guinea-pig.

Y Imaizumi 1, K Muraki 1, M Watanabe 1
PMCID: PMC1190516  PMID: 2482352

Abstract

1. Ionic currents underlying the action potential were recorded from enzymatically isolated smooth muscle cells of guinea-pig ureter. 2. The action potential recorded from a single cell was similar to that from a multicellular preparation. It showed repetitive spikes on a plateau potential which followed the first spike. Treatment with 10 mM-tetraethylammonium (TEA) increased the amplitude and duration of the plateau phase and abolished the repetitive spikes. 3. Under voltage clamp mode, at least two (maybe three) kinds of outward currents were activated during depolarizing pulses. The main outward current was Ca2+-dependent K+ current (IK(Ca], which was mostly blocked in Ca2+-free solution, or by application of 1 mM-cadmium (Cd2+) or 2 mM-tetraethylammonium (TEA). IK(Ca) was greatly decreased by treatment with 5 mM-caffeine or an addition of 10 mM-EGTA in a pipette solution. 4. In the presence of 1 mM-Cd2+ and 2 mM-TEA, a small transient outward current remained. 4-Aminopyridine (1 mM) suppressed the transient outward current by about 40%. Time- and voltage-dependent delayed rectifier outward currents were small in ureter cells. An inwardly rectifying K+ current was not detected. 5. An application of 1 mM-Cd2+, 5 mM-cobalt (Co2+), 1 mM-lanthanum (La3+) or 0.1 microM-nifedipine completely blocked the action potential. Replacement of 80-90% of extracellular Na+ with Li+ or Tris almost abolished the plateau potential and repetitive spikes but did not change significantly the first spike. 6. In the presence of 30 mM-TEA, the inward current elicited by depolarization was monophasic and lasted for more than 1 s. Application of 1 mM-Cd2+, 1 mM-La3+, 0.1 microM-nifedipine, or 5 mM-Co2+ completely blocked inward current. The replacement (87%) of extracellular Na+ ions with Li+, Tris, sucrose or TEA speeded up the decay of inward current; the inward current decreased by 10-60% at the end of a 500 ms pulse. 7. Even in low-Na+ solution (120 mM-TEA), the inactivation of ICa had a quite slow component (tau = 1 s), in addition to another faster component (tau = 100 ms) at 0 mV. When short depolarizing clamp pulses (50 ms) were repetitively applied at short intervals (50 ms) and with interpulse voltage of -10 or -20 mV to mimic the repetitive spikes on the plateau of the action potential, the decline of peak Ca2+ current during the train of pulses was smaller than the decay of Ca2+ current during a long pulse.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
131

Selected References

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

  1. Aickin C. C., Brading A. F., Walmsley D. An investigation of sodium-calcium exchange in the smooth muscle of guinea-pig ureter. J Physiol. 1987 Oct;391:325–346. doi: 10.1113/jphysiol.1987.sp016741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aldrich R. W., Jr, Getting P. A., Thompson S. H. Inactivation of delayed outward current in molluscan neurone somata. J Physiol. 1979 Jun;291:507–530. doi: 10.1113/jphysiol.1979.sp012828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Attwell D., Eisner D., Cohen I. Voltage clamp and tracer flux data: effects of a restricted extra-cellular space. Q Rev Biophys. 1979 Aug;12(3):213–261. doi: 10.1017/s0033583500005448. [DOI] [PubMed] [Google Scholar]
  4. Bean B. P., Sturek M., Puga A., Hermsmeyer K. Calcium channels in muscle cells isolated from rat mesenteric arteries: modulation by dihydropyridine drugs. Circ Res. 1986 Aug;59(2):229–235. doi: 10.1161/01.res.59.2.229. [DOI] [PubMed] [Google Scholar]
  5. Bean B. P. Two kinds of calcium channels in canine atrial cells. Differences in kinetics, selectivity, and pharmacology. J Gen Physiol. 1985 Jul;86(1):1–30. doi: 10.1085/jgp.86.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bechem M., Pott L. Removal of Ca current inactivation in dialysed guinea-pig atrial cardioballs by Ca chelators. Pflugers Arch. 1985 May;404(1):10–20. doi: 10.1007/BF00581485. [DOI] [PubMed] [Google Scholar]
  7. Benham C. D., Bolton T. B., Lang R. J., Takewaki T. The mechanism of action of Ba2+ and TEA on single Ca2+-activated K+ -channels in arterial and intestinal smooth muscle cell membranes. Pflugers Arch. 1985 Feb;403(2):120–127. doi: 10.1007/BF00584088. [DOI] [PubMed] [Google Scholar]
  8. Benham C. D., Bolton T. B. Patch-clamp studies of slow potential-sensitive potassium channels in longitudinal smooth muscle cells of rabbit jejunum. J Physiol. 1983 Jul;340:469–486. doi: 10.1113/jphysiol.1983.sp014774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Benham C. D., Bolton T. B. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986 Dec;381:385–406. doi: 10.1113/jphysiol.1986.sp016333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bilbaut A., Hernandez-Nicaise M. L., Leech C. A., Meech R. W. Membrane currents that govern smooth muscle contraction in a ctenophore. Nature. 1988 Feb 11;331(6156):533–535. doi: 10.1038/331533a0. [DOI] [PubMed] [Google Scholar]
  11. Bolton T. B., Lang R. J., Takewaki T., Benham C. D. Patch and whole-cell voltage clamp of single mammalian visceral and vascular smooth muscle cells. Experientia. 1985 Jul 15;41(7):887–894. doi: 10.1007/BF01970006. [DOI] [PubMed] [Google Scholar]
  12. Caffrey J. M., Josephson I. R., Brown A. M. Calcium channels of amphibian stomach and mammalian aorta smooth muscle cells. Biophys J. 1986 Jun;49(6):1237–1242. doi: 10.1016/S0006-3495(86)83753-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Casteels R., Raeymaekers L., Droogmans G., Wuytack F. Na+-K+ ATPase, Na-Ca exchange, and excitation-contraction coupling in smooth muscle. J Cardiovasc Pharmacol. 1985;7 (Suppl 3):S103–S110. [PubMed] [Google Scholar]
  14. Clark R. B., Giles W. R., Imaizumi Y. Properties of the transient outward current in rabbit atrial cells. J Physiol. 1988 Nov;405:147–168. doi: 10.1113/jphysiol.1988.sp017326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Clark R. B., Giles W. Sodium current in single cells from bullfrog atrium: voltage dependence and ion transfer properties. J Physiol. 1987 Oct;391:235–265. doi: 10.1113/jphysiol.1987.sp016736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  18. Fedida D., Noble D., Shimoni Y., Spindler A. J. Inward current related to contraction in guinea-pig ventricular myocytes. J Physiol. 1987 Apr;385:565–589. doi: 10.1113/jphysiol.1987.sp016508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gabella G. Quantitative morphological study of smooth muscle cells of the guinea-pig taenia coli. Cell Tissue Res. 1976 Jul 26;170(2):161–186. doi: 10.1007/BF00224297. [DOI] [PubMed] [Google Scholar]
  20. Ganitkevich VYa, Shuba M. F., Smirnov S. V. Calcium-dependent inactivation of potential-dependent calcium inward current in an isolated guinea-pig smooth muscle cell. J Physiol. 1987 Nov;392:431–449. doi: 10.1113/jphysiol.1987.sp016789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ganitkevich VYa, Shuba M. F., Smirnov S. V. Potential-dependent calcium inward current in a single isolated smooth muscle cell of the guinea-pig taenia caeci. J Physiol. 1986 Nov;380:1–16. doi: 10.1113/jphysiol.1986.sp016268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Giles W. R., Imaizumi Y. Comparison of potassium currents in rabbit atrial and ventricular cells. J Physiol. 1988 Nov;405:123–145. doi: 10.1113/jphysiol.1988.sp017325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hagiwara S., Ozawa S., Sand O. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol. 1975 May;65(5):617–644. doi: 10.1085/jgp.65.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Hume J. R., Giles W. Ionic currents in single isolated bullfrog atrial cells. J Gen Physiol. 1983 Feb;81(2):153–194. doi: 10.1085/jgp.81.2.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Inoue R., Kitamura K., Kuriyama H. Two Ca-dependent K-channels classified by the application of tetraethylammonium distribute to smooth muscle membranes of the rabbit portal vein. Pflugers Arch. 1985 Oct;405(3):173–179. doi: 10.1007/BF00582557. [DOI] [PubMed] [Google Scholar]
  27. Jmari K., Mironneau C., Mironneau J. Inactivation of calcium channel current in rat uterine smooth muscle: evidence for calcium- and voltage-mediated mechanisms. J Physiol. 1986 Nov;380:111–126. doi: 10.1113/jphysiol.1986.sp016275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kimura J., Miyamae S., Noma A. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol. 1987 Mar;384:199–222. doi: 10.1113/jphysiol.1987.sp016450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Klöckner U., Isenberg G. Action potentials and net membrane currents of isolated smooth muscle cells (urinary bladder of the guinea-pig). Pflugers Arch. 1985 Dec;405(4):329–339. doi: 10.1007/BF00595685. [DOI] [PubMed] [Google Scholar]
  30. Klöckner U., Isenberg G. Calcium currents of cesium loaded isolated smooth muscle cells (urinary bladder of the guinea pig). Pflugers Arch. 1985 Dec;405(4):340–348. doi: 10.1007/BF00595686. [DOI] [PubMed] [Google Scholar]
  31. Kuriyama H., Osa T., Toida N. Membrane properties of the smooth muscle of guinea-pig ureter. J Physiol. 1967 Jul;191(2):225–238. doi: 10.1113/jphysiol.1967.sp008247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kuriyama H., Tomita T. The action potential in the smooth muscle of the guinea pig taenia coli and ureter studied by the double sucrose-gap method. J Gen Physiol. 1970 Feb;55(2):147–162. doi: 10.1085/jgp.55.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lansman J. B. Calcium current and calcium-activated inward current in the oocyte of the starfish Leptasterias hexactis. J Physiol. 1987 Sep;390:397–413. doi: 10.1113/jphysiol.1987.sp016708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Loirand G., Pacaud P., Mironneau C., Mironneau J. Evidence for two distinct calcium channels in rat vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 1986 Nov;407(5):566–568. doi: 10.1007/BF00657519. [DOI] [PubMed] [Google Scholar]
  35. Mitra R., Morad M. Ca2+ and Ca2+-activated K+ currents in mammalian gastric smooth muscle cells. Science. 1985 Jul 19;229(4710):269–272. doi: 10.1126/science.2409600. [DOI] [PubMed] [Google Scholar]
  36. Momose K., Gomi Y. Studies on isolated smooth muscle cells. I. Continuous observation of contraction of single smooth muscle cells isolated from vas deferens of guinea pig. Chem Pharm Bull (Tokyo) 1977 Sep;25(9):2449–2451. doi: 10.1248/cpb.25.2449. [DOI] [PubMed] [Google Scholar]
  37. Momose K., Gomi Y. [Studies on isolated smooth muscle cells. VI. Dispersion procedures for acetylcholine-sensitive smooth muscle cells of guinea pig (author's transl)]. Nihon Heikatsukin Gakkai Zasshi. 1980 Mar;16(1):29–36. doi: 10.1540/jsmr1965.16.29. [DOI] [PubMed] [Google Scholar]
  38. Mullins L. J. The generation of electric currents in cardiac fibers by Na/Ca exchange. Am J Physiol. 1979 Mar;236(3):C103–C110. doi: 10.1152/ajpcell.1979.236.3.C103. [DOI] [PubMed] [Google Scholar]
  39. Nakazawa K., Matsuki N., Shigenobu K., Kasuya Y. Contractile response and electrophysiological properties in enzymatically dispersed smooth muscle cells of rat vas deferens. Pflugers Arch. 1987 Feb;408(2):112–119. doi: 10.1007/BF00581338. [DOI] [PubMed] [Google Scholar]
  40. Ohya Y., Kitamura K., Kuriyama H. Cellular calcium regulates outward currents in rabbit intestinal smooth muscle cell. Am J Physiol. 1987 Apr;252(4 Pt 1):C401–C410. doi: 10.1152/ajpcell.1987.252.4.C401. [DOI] [PubMed] [Google Scholar]
  41. Okabe K., Kitamura K., Kuriyama H. Features of 4-aminopyridine sensitive outward current observed in single smooth muscle cells from the rabbit pulmonary artery. Pflugers Arch. 1987 Aug;409(6):561–568. doi: 10.1007/BF00584654. [DOI] [PubMed] [Google Scholar]
  42. Okabe K., Kitamura K., Kuriyama H. The existence of a highly tetrodotoxin sensitive Na channel in freshly dispersed smooth muscle cells of the rabbit main pulmonary artery. Pflugers Arch. 1988 Apr;411(4):423–428. doi: 10.1007/BF00587722. [DOI] [PubMed] [Google Scholar]
  43. Partridge L. D., Swandulla D. Calcium-activated non-specific cation channels. Trends Neurosci. 1988 Feb;11(2):69–72. doi: 10.1016/0166-2236(88)90167-1. [DOI] [PubMed] [Google Scholar]
  44. Robinson K., Giles W. A data acquisition, display and plotting program for the IBM PC. Comput Methods Programs Biomed. 1986 Dec;23(3):319–327. doi: 10.1016/0169-2607(86)90067-2. [DOI] [PubMed] [Google Scholar]
  45. Shuba M. F. The effect of sodium-free and potassium-free solutions, ionic current inhibitors and ouabain on electrophysiological properties of smooth muscle of guinea-pig ureter. J Physiol. 1977 Jan;264(3):837–851. doi: 10.1113/jphysiol.1977.sp011697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Singer J. J., Walsh J. V., Jr Characterization of calcium-activated potassium channels in single smooth muscle cells using the patch-clamp technique. Pflugers Arch. 1987 Feb;408(2):98–111. doi: 10.1007/BF00581337. [DOI] [PubMed] [Google Scholar]
  47. Sturek M., Hermsmeyer K. Calcium and sodium channels in spontaneously contracting vascular muscle cells. Science. 1986 Jul 25;233(4762):475–478. doi: 10.1126/science.2425434. [DOI] [PubMed] [Google Scholar]
  48. Terada K., Kitamura K., Kuriyama H. Different inhibitions of the voltage-dependent K+ current by Ca2+ antagonists in the smooth muscle cell membrane of rabbit small intestine. Pflugers Arch. 1987 May;408(6):558–564. doi: 10.1007/BF00581156. [DOI] [PubMed] [Google Scholar]
  49. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tsien R. W. Calcium channels in excitable cell membranes. Annu Rev Physiol. 1983;45:341–358. doi: 10.1146/annurev.ph.45.030183.002013. [DOI] [PubMed] [Google Scholar]
  51. Van Breemen C., Aaronson P., Loutzenhiser R. Sodium-calcium interactions in mammalian smooth muscle. Pharmacol Rev. 1978 Jun;30(2):167–208. [PubMed] [Google Scholar]
  52. Walsh J. V., Jr, Singer J. J. Identification and characterization of major ionic currents in isolated smooth muscle cells using the voltage-clamp technique. Pflugers Arch. 1987 Feb;408(2):83–97. doi: 10.1007/BF00581336. [DOI] [PubMed] [Google Scholar]
  53. Warshaw D. M., Szarek J. L., Hubbard M. S., Evans J. N. Pharmacology and force development of single freshly isolated bovine carotid artery smooth muscle cells. Circ Res. 1986 Mar;58(3):399–406. doi: 10.1161/01.res.58.3.399. [DOI] [PubMed] [Google Scholar]
  54. Yatani A., Seidel C. L., Allen J., Brown A. M. Whole-cell and single-channel calcium currents of isolated smooth muscle cells from saphenous vein. Circ Res. 1987 Apr;60(4):523–533. doi: 10.1161/01.res.60.4.523. [DOI] [PubMed] [Google Scholar]

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

RESOURCES