Skip to main content
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1993 Oct;110(2):573–582. doi: 10.1111/j.1476-5381.1993.tb13849.x

K channel activation by nucleotide diphosphates and its inhibition by glibenclamide in vascular smooth muscle cells.

D J Beech 1, H Zhang 1, K Nakao 1, T B Bolton 1
PMCID: PMC2175936  PMID: 8242232

Abstract

1. Whole-cell and inside-out patch recordings were made from single smooth muscle cells that had been isolated enzymatically and mechanically from the rabbit portal vein. 2. In whole-cells the inclusion in the recording pipette solution of nucleotide diphosphates (NDPs), but not tri- or monophosphates, induced a K-current that developed gradually over 5 to 15 min. Intracellular 1 mM guanosine 5'-diphosphate (GDP) induced a slowly developing outward K-current at -37 mV that reached a maximum on average of 72 +/- 4 pA (n = 40). Half maximal effect was estimated to occur with about 0.2 mM GDP. Except for ADP, other NDPs had comparable effects. At 0.1 mM, ADP was equivalent to GDP but at higher concentration ADP was less effective. ADP induced its maximum effect at 1 mM but had almost no effect at 10 mM. 3. In 14% of inside-out patches exposed to 1 mM GDP at the intracellular surface, characteristic K channel activity was observed which showed long (> 1 s) bursts of openings separated by longer closed periods. The current-voltage relationship for the channel was linear in a 60 mM:130 mM K-gradient and the unitary conductance was 24 pS. 4. Glibenclamide applied via the extracellular solution was found to be a potent inhibitor of GDP-induced K-current (IK(GDP)) in the whole-cell. The Kd was 25 nM and the inhibition was fully reversible on wash-out. 5. IK(GDP) was not evoked if Mg ions were absent from the pipette solution. In contrast the omission of extracellular Mg ions had no effect on outward or inward IK(GDP). 6. Inclusion of 1 mM ATP in the recording pipette solution reduced IK(GDP) and also attenuated its decline during long (25 min) recordings. 7. When perforated-patch whole-cell recording was used, metabolic poisoning with cyanide and 2-deoxy-D-glucose induced a glibenclamide-sensitive K-current. This current was not observed when conventional whole-cell recording was used. Possible reasons for this difference are discussed. 8. These K channels appear similar to ATP-sensitive K channels but we refer to them as nucleotide diphosphate-dependent K channels (KNDP) to emphasise what seems to be a primary role for nucleotide diphosphates in their regulation.

Full text

PDF
573

Selected References

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

  1. Allard B., Lazdunski M. Nucleotide diphosphates activate the ATP-sensitive potassium channel in mouse skeletal muscle. Pflugers Arch. 1992 Nov;422(2):185–192. doi: 10.1007/BF00370419. [DOI] [PubMed] [Google Scholar]
  2. Ashcroft S. J., Ashcroft F. M. Properties and functions of ATP-sensitive K-channels. Cell Signal. 1990;2(3):197–214. doi: 10.1016/0898-6568(90)90048-f. [DOI] [PubMed] [Google Scholar]
  3. Ashcroft S. J., Ashcroft F. M. The sulfonylurea receptor. Biochim Biophys Acta. 1992 Dec 15;1175(1):45–59. doi: 10.1016/0167-4889(92)90008-y. [DOI] [PubMed] [Google Scholar]
  4. Beech D. J., Bolton T. B. Properties of the cromakalim-induced potassium conductance in smooth muscle cells isolated from the rabbit portal vein. Br J Pharmacol. 1989 Nov;98(3):851–864. doi: 10.1111/j.1476-5381.1989.tb14614.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beech D. J., Zhang H., Nakao K., Bolton T. B. Single channel and whole-cell K-currents evoked by levcromakalim in smooth muscle cells from the rabbit portal vein. Br J Pharmacol. 1993 Oct;110(2):583–590. doi: 10.1111/j.1476-5381.1993.tb13850.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brayden J. E. Membrane hyperpolarization is a mechanism of endothelium-dependent cerebral vasodilation. Am J Physiol. 1990 Sep;259(3 Pt 2):H668–H673. doi: 10.1152/ajpheart.1990.259.3.H668. [DOI] [PubMed] [Google Scholar]
  7. Clapp L. H., Gurney A. M. ATP-sensitive K+ channels regulate resting potential of pulmonary arterial smooth muscle cells. Am J Physiol. 1992 Mar;262(3 Pt 2):H916–H920. doi: 10.1152/ajpheart.1992.262.3.H916. [DOI] [PubMed] [Google Scholar]
  8. Daut J., Maier-Rudolph W., von Beckerath N., Mehrke G., Günther K., Goedel-Meinen L. Hypoxic dilation of coronary arteries is mediated by ATP-sensitive potassium channels. Science. 1990 Mar 16;247(4948):1341–1344. doi: 10.1126/science.2107575. [DOI] [PubMed] [Google Scholar]
  9. Davis N. W., Standen N. B., Stanfield P. R. ATP-dependent potassium channels of muscle cells: their properties, regulation, and possible functions. J Bioenerg Biomembr. 1991 Aug;23(4):509–535. doi: 10.1007/BF00785809. [DOI] [PubMed] [Google Scholar]
  10. Dunne M. J., Petersen O. H. Intracellular ADP activates K+ channels that are inhibited by ATP in an insulin-secreting cell line. FEBS Lett. 1986 Nov 10;208(1):59–62. doi: 10.1016/0014-5793(86)81532-0. [DOI] [PubMed] [Google Scholar]
  11. Ekmehag B. L. Electrical and mechanical responses to inhibition of cell respiration in vascular smooth muscle of the rat portal vein. Acta Physiol Scand. 1989 Sep;137(1):41–51. doi: 10.1111/j.1748-1716.1989.tb08719.x. [DOI] [PubMed] [Google Scholar]
  12. Fan Z., Nakayama K., Hiraoka M. Multiple actions of pinacidil on adenosine triphosphate-sensitive potassium channels in guinea-pig ventricular myocytes. J Physiol. 1990 Nov;430:273–295. doi: 10.1113/jphysiol.1990.sp018291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garland C. J., McPherson G. A. Evidence that nitric oxide does not mediate the hyperpolarization and relaxation to acetylcholine in the rat small mesenteric artery. Br J Pharmacol. 1992 Feb;105(2):429–435. doi: 10.1111/j.1476-5381.1992.tb14270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Horn R., Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol. 1988 Aug;92(2):145–159. doi: 10.1085/jgp.92.2.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishida Y., Paul R. J. Effects of hypoxia on high-energy phosphagen content, energy metabolism and isometric force in guinea-pig taenia caeci. J Physiol. 1990 May;424:41–56. doi: 10.1113/jphysiol.1990.sp018054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kajioka S., Kitamura K., Kuriyama H. Guanosine diphosphate activates an adenosine 5'-triphosphate-sensitive K+ channel in the rabbit portal vein. J Physiol. 1991 Dec;444:397–418. doi: 10.1113/jphysiol.1991.sp018885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kajioka S., Oike M., Kitamura K. Nicorandil opens a calcium-dependent potassium channel in smooth muscle cells of the rat portal vein. J Pharmacol Exp Ther. 1990 Sep;254(3):905–913. [PubMed] [Google Scholar]
  19. Kakei M., Noma A., Shibasaki T. Properties of adenosine-triphosphate-regulated potassium channels in guinea-pig ventricular cells. J Physiol. 1985 Jun;363:441–462. doi: 10.1113/jphysiol.1985.sp015721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kamouchi M., Kajioka S., Sakai T., Kitamura K., Kuriyama H. A target K+ channel for the LP-805-induced hyperpolarization in smooth muscle cells of the rabbit portal vein. Naunyn Schmiedebergs Arch Pharmacol. 1993 Mar;347(3):329–335. doi: 10.1007/BF00167453. [DOI] [PubMed] [Google Scholar]
  21. Kovacs R. J., Nelson M. T. ATP-sensitive K+ channels from aortic smooth muscle incorporated into planar lipid bilayers. Am J Physiol. 1991 Aug;261(2 Pt 2):H604–H609. doi: 10.1152/ajpheart.1991.261.2.H604. [DOI] [PubMed] [Google Scholar]
  22. Lazdunski M., Bernardi H., de Weille J. R., Mourre C., Fosset M. Agonists and antagonists of ATP-sensitive potassium channels. Adv Nephrol Necker Hosp. 1992;21:195–202. [PubMed] [Google Scholar]
  23. Lorenz J. N., Schnermann J., Brosius F. C., Briggs J. P., Furspan P. B. Intracellular ATP can regulate afferent arteriolar tone via ATP-sensitive K+ channels in the rabbit. J Clin Invest. 1992 Sep;90(3):733–740. doi: 10.1172/JCI115945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lydrup M. L., Hellstrand P. Metabolic correlates to pacemaker activity in the smooth muscle of guinea-pig mesotubarium. Acta Physiol Scand. 1991 Feb;141(2):263–272. doi: 10.1111/j.1748-1716.1991.tb09076.x. [DOI] [PubMed] [Google Scholar]
  25. Nakayama S., Tomita T. Regulation of intracellular free magnesium concentration in the taenia of guinea-pig caecum. J Physiol. 1991 Apr;435:559–572. doi: 10.1113/jphysiol.1991.sp018525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nelson M. T., Huang Y., Brayden J. E., Hescheler J., Standen N. B. Arterial dilations in response to calcitonin gene-related peptide involve activation of K+ channels. Nature. 1990 Apr 19;344(6268):770–773. doi: 10.1038/344770a0. [DOI] [PubMed] [Google Scholar]
  27. Nichols C. G., Lederer W. J. Adenosine triphosphate-sensitive potassium channels in the cardiovascular system. Am J Physiol. 1991 Dec;261(6 Pt 2):H1675–H1686. doi: 10.1152/ajpheart.1991.261.6.H1675. [DOI] [PubMed] [Google Scholar]
  28. Noack T., Edwards G., Deitmer P., Weston A. H. Potassium channel modulation in rat portal vein by ATP depletion: a comparison with the effects of levcromakalim (BRL 38227). Br J Pharmacol. 1992 Dec;107(4):945–955. doi: 10.1111/j.1476-5381.1992.tb13390.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8;305(5930):147–148. doi: 10.1038/305147a0. [DOI] [PubMed] [Google Scholar]
  30. Noma A., Shibasaki T. Membrane current through adenosine-triphosphate-regulated potassium channels in guinea-pig ventricular cells. J Physiol. 1985 Jun;363:463–480. doi: 10.1113/jphysiol.1985.sp015722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pfründer D., Anghelescu I., Kreye V. A. Intracellular ADP activates ATP-sensitive K+ channels in vascular smooth muscle cells of the guinea pig portal vein. Pflugers Arch. 1993 Apr;423(1-2):149–151. doi: 10.1007/BF00374972. [DOI] [PubMed] [Google Scholar]
  32. Quast U., Cook N. S. In vitro and in vivo comparison of two K+ channel openers, diazoxide and cromakalim, and their inhibition by glibenclamide. J Pharmacol Exp Ther. 1989 Jul;250(1):261–271. [PubMed] [Google Scholar]
  33. Robertson B. E., Corry P. R., Nye P. C., Kozlowski R. Z. Ca2+ and Mg-ATP activated potassium channels from rat pulmonary artery. Pflugers Arch. 1992 Jun;421(2-3):94–96. [PubMed] [Google Scholar]
  34. Robertson D. W., Steinberg M. I. Potassium channel modulators: scientific applications and therapeutic promise. J Med Chem. 1990 Jun;33(6):1529–1541. doi: 10.1021/jm00168a001. [DOI] [PubMed] [Google Scholar]
  35. Silberberg S. D., van Breemen C. A potassium current activated by lemakalim and metabolic inhibition in rabbit mesenteric artery. Pflugers Arch. 1992 Jan;420(1):118–120. doi: 10.1007/BF00378653. [DOI] [PubMed] [Google Scholar]
  36. Standen N. B., Quayle J. M., Davies N. W., Brayden J. E., Huang Y., Nelson M. T. Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science. 1989 Jul 14;245(4914):177–180. doi: 10.1126/science.2501869. [DOI] [PubMed] [Google Scholar]
  37. Sun H. T., Yoshida Y., Imai S. A Ca2(+)-activated, Mg2(+)-dependent ATPase with high affinities for both Ca2+ and Mg2+ in vascular smooth muscle microsomes: comparison with plasma membrane Ca2(+)-pump ATPase. J Biochem. 1990 Nov;108(5):730–736. doi: 10.1093/oxfordjournals.jbchem.a123273. [DOI] [PubMed] [Google Scholar]
  38. Tomita T. Ionic channels in smooth muscle studied with patch-clamp methods. Jpn J Physiol. 1988;38(1):1–18. doi: 10.2170/jjphysiol.38.1. [DOI] [PubMed] [Google Scholar]
  39. Tung R. T., Kurachi Y. On the mechanism of nucleotide diphosphate activation of the ATP-sensitive K+ channel in ventricular cell of guinea-pig. J Physiol. 1991 Jun;437:239–256. doi: 10.1113/jphysiol.1991.sp018593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Van Breemen C., Wuytack F., Casteels R., Martinelli B., Campailla E., Ferrari G. Stimulation of 45Ca efflux from smooth muscle cells by metabolic inhibition and high K depolarization. Pflugers Arch. 1975 Sep 9;359(3):183–196. doi: 10.1007/BF00587378. [DOI] [PubMed] [Google Scholar]
  41. Wakatsuki T., Nakaya Y., Inoue I. Vasopressin modulates K(+)-channel activities of cultured smooth muscle cells from porcine coronary artery. Am J Physiol. 1992 Aug;263(2 Pt 2):H491–H496. doi: 10.1152/ajpheart.1992.263.2.H491. [DOI] [PubMed] [Google Scholar]
  42. Weston A. H., Edwards G. Recent progress in potassium channel opener pharmacology. Biochem Pharmacol. 1992 Jan 9;43(1):47–54. doi: 10.1016/0006-2952(92)90659-7. [DOI] [PubMed] [Google Scholar]
  43. Zilberter Y., Burnashev N., Papin A., Portnov V., Khodorov B. Gating kinetics of ATP-sensitive single potassium channels in myocardial cells depends on electromotive force. Pflugers Arch. 1988 May;411(5):584–589. doi: 10.1007/BF00582382. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES