Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1996 Apr 15;492(Pt 2):419–430. doi: 10.1113/jphysiol.1996.sp021318

Extracellular K(+)-induced hyperpolarizations and dilatations of rat coronary and cerebral arteries involve inward rectifier K(+) channels.

H J Knot 1, P A Zimmermann 1, M T Nelson 1
PMCID: PMC1158837  PMID: 9019539

Abstract

1. The hypothesis that inward rectifier K(+) channels are involved in the vasodilatation of small coronary and cerebral arteries (100-200 microm diameter) in response to elevated [K+]o was tested. The diameters and membrane potentials of pressurized arteries from rat were measured using a video-imaging system and conventional microelectrodes, respectively. 2. Elevation of [K+]o from 6 to 16 mM caused the membrane potential of pressurized (60 mmHg) arteries to hyperpolarize by 12-14 mV. Extracellular Ba(2+) (Ba2+(o)) blocked K(+)-induced membrane potential hyperpolarizations at concentrations (IC(50), 6 microM) that block inward rectifier K(+) currents in smooth muscle cells isolated from these arteries. 3. Elevation of [K+]o from 6 to 16 mM caused sustained dilatations of pressurized coronary and cerebral arteries with diameters increasing from 125 to 192 microm and 110 to 180 microm in coronary and cerebral arteries, respectively. Ba2+(o) blocked K(+)-induced dilatations of pressurized coronary and cerebral arteries (IC50, 3-8 microM). 4. Elevated [K+]o-induced vasodilatation was not prevented by blockers of other types of K(+) channels (1 mM 4-aminopyridine, 1 mM TEA+, and 10 mu M glibenclamide), and blockers of Na(+)-K(+)-ATPase. Elevated [K+]o-induced vasodilatation was unaffected by removal of the endothelium. 5. These findings suggest that K+(o) dilates small rat coronary and cerebral arteries through activation of inward rectifier K(+) channels. Furthermore, these results support the hypothesis that inward rectifier K(+) channels may be involved in metabolic regulation of coronary and cerebral blood flow in response to changes in [K+]o.

Full text

PDF
419

Selected References

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

  1. Brayden J. E., Nelson M. T. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science. 1992 Apr 24;256(5056):532–535. doi: 10.1126/science.1373909. [DOI] [PubMed] [Google Scholar]
  2. Bünger R., Haddy R. J., Querengässer A., Gerlach E. Studies on potassium induced coronary dilation in the isolated guinea pig heart. Pflugers Arch. 1976 May 6;363(1):27–31. doi: 10.1007/BF00587398. [DOI] [PubMed] [Google Scholar]
  3. Cameron I. R., Caronna J. The effect of local changes in potassium and bicarbonate concentration on hypothalamic blood flow in the rabbit. J Physiol. 1976 Nov;262(2):415–430. doi: 10.1113/jphysiol.1976.sp011602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen W. T., Brace R. A., Scott J. B., Anderson D. K., Haddy F. J. The mechanism of the vasodilator action of potassium. Proc Soc Exp Biol Med. 1972 Jul;140(3):820–824. doi: 10.3181/00379727-140-36560. [DOI] [PubMed] [Google Scholar]
  5. Daut J., Standen N. B., Nelson M. T. The role of the membrane potential of endothelial and smooth muscle cells in the regulation of coronary blood flow. J Cardiovasc Electrophysiol. 1994 Feb;5(2):154–181. doi: 10.1111/j.1540-8167.1994.tb01156.x. [DOI] [PubMed] [Google Scholar]
  6. Edwards F. R., Hirst G. D. Inward rectification in submucosal arterioles of guinea-pig ileum. J Physiol. 1988 Oct;404:437–454. doi: 10.1113/jphysiol.1988.sp017298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edwards F. R., Hirst G. D., Silverberg G. D. Inward rectification in rat cerebral arterioles; involvement of potassium ions in autoregulation. J Physiol. 1988 Oct;404:455–466. doi: 10.1113/jphysiol.1988.sp017299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ficker E., Taglialatela M., Wible B. A., Henley C. M., Brown A. M. Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science. 1994 Nov 11;266(5187):1068–1072. doi: 10.1126/science.7973666. [DOI] [PubMed] [Google Scholar]
  9. Haddy F. J., Scott J. B. Metabolically linked vasoactive chemicals in local regulation of blood flow. Physiol Rev. 1968 Oct;48(4):688–707. doi: 10.1152/physrev.1968.48.4.688. [DOI] [PubMed] [Google Scholar]
  10. Harik S. I., Doull G. H., Dick A. P. Specific ouabain binding to brain microvessels and choroid plexus. J Cereb Blood Flow Metab. 1985 Mar;5(1):156–160. doi: 10.1038/jcbfm.1985.20. [DOI] [PubMed] [Google Scholar]
  11. Hexum T. D. Characterization of NaK-ATPase from vascular smooth muscle. Gen Pharmacol. 1981;12(5):393–396. doi: 10.1016/0306-3623(81)90098-7. [DOI] [PubMed] [Google Scholar]
  12. Hirst G. D., Edwards F. R. Sympathetic neuroeffector transmission in arteries and arterioles. Physiol Rev. 1989 Apr;69(2):546–604. doi: 10.1152/physrev.1989.69.2.546. [DOI] [PubMed] [Google Scholar]
  13. Hirst G. D., van Helden D. F. Ionic basis of the resting potential of submucosal arterioles in the ileum of the guinea-pig. J Physiol. 1982 Dec;333:53–67. doi: 10.1113/jphysiol.1982.sp014438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kléber A. G. Resting membrane potential, extracellular potassium activity, and intracellular sodium activity during acute global ischemia in isolated perfused guinea pig hearts. Circ Res. 1983 Apr;52(4):442–450. doi: 10.1161/01.res.52.4.442. [DOI] [PubMed] [Google Scholar]
  15. Knot H. J., Nelson M. T. Regulation of membrane potential and diameter by voltage-dependent K+ channels in rabbit myogenic cerebral arteries. Am J Physiol. 1995 Jul;269(1 Pt 2):H348–H355. doi: 10.1152/ajpheart.1995.269.1.H348. [DOI] [PubMed] [Google Scholar]
  16. Kuschinsky W., Wahl M., Bosse O., Thurau K. Perivascular potassium and pH as determinants of local pial arterial diameter in cats. A microapplication study. Circ Res. 1972 Aug;31(2):240–247. doi: 10.1161/01.res.31.2.240. [DOI] [PubMed] [Google Scholar]
  17. Lopatin A. N., Makhina E. N., Nichols C. G. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature. 1994 Nov 24;372(6504):366–369. doi: 10.1038/372366a0. [DOI] [PubMed] [Google Scholar]
  18. McCarron J. G., Halpern W. Potassium dilates rat cerebral arteries by two independent mechanisms. Am J Physiol. 1990 Sep;259(3 Pt 2):H902–H908. doi: 10.1152/ajpheart.1990.259.3.H902. [DOI] [PubMed] [Google Scholar]
  19. Nakao M., Gadsby D. C. [Na] and [K] dependence of the Na/K pump current-voltage relationship in guinea pig ventricular myocytes. J Gen Physiol. 1989 Sep;94(3):539–565. doi: 10.1085/jgp.94.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nelson M. T., Blaustein M. P. Properties of sodium pumps in internally perfused barnacle muscle fibers. J Gen Physiol. 1980 Feb;75(2):183–206. doi: 10.1085/jgp.75.2.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nelson M. T., Quayle J. M. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol. 1995 Apr;268(4 Pt 1):C799–C822. doi: 10.1152/ajpcell.1995.268.4.C799. [DOI] [PubMed] [Google Scholar]
  22. Nelson M. T., Worley J. F. Dihydropyridine inhibition of single calcium channels and contraction in rabbit mesenteric artery depends on voltage. J Physiol. 1989 May;412:65–91. doi: 10.1113/jphysiol.1989.sp017604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Paulson O. B., Newman E. A. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science. 1987 Aug 21;237(4817):896–898. doi: 10.1126/science.3616619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Quayle J. M., Bonev A. D., Brayden J. E., Nelson M. T. Pharmacology of ATP-sensitive K+ currents in smooth muscle cells from rabbit mesenteric artery. Am J Physiol. 1995 Nov;269(5 Pt 1):C1112–C1118. doi: 10.1152/ajpcell.1995.269.5.C1112. [DOI] [PubMed] [Google Scholar]
  25. Quayle J. M., McCarron J. G., Brayden J. E., Nelson M. T. Inward rectifier K+ currents in smooth muscle cells from rat resistance-sized cerebral arteries. Am J Physiol. 1993 Nov;265(5 Pt 1):C1363–C1370. doi: 10.1152/ajpcell.1993.265.5.C1363. [DOI] [PubMed] [Google Scholar]
  26. Robertson B. E., Nelson M. T. Aminopyridine inhibition and voltage dependence of K+ currents in smooth muscle cells from cerebral arteries. Am J Physiol. 1994 Dec;267(6 Pt 1):C1589–C1597. doi: 10.1152/ajpcell.1994.267.6.C1589. [DOI] [PubMed] [Google Scholar]
  27. Sakmann B., Trube G. Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol. 1984 Feb;347:641–657. doi: 10.1113/jphysiol.1984.sp015088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sieber F. E., Wilson D. A., Hanley D. F., Traystman R. J. Extracellular potassium activity and cerebral blood flow during moderate hypoglycemia in anesthetized dogs. Am J Physiol. 1993 Jun;264(6 Pt 2):H1774–H1780. doi: 10.1152/ajpheart.1993.264.6.H1774. [DOI] [PubMed] [Google Scholar]
  29. Somjen G. G. Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol. 1979;41:159–177. doi: 10.1146/annurev.ph.41.030179.001111. [DOI] [PubMed] [Google Scholar]
  30. Warner M. R., Kroeker T. S., Zipes D. P. Sympathetic stimulation and norepinephrine infusion modulate extracellular potassium concentration during acute myocardial ischemia. Circ Res. 1992 Nov;71(5):1078–1087. doi: 10.1161/01.res.71.5.1078. [DOI] [PubMed] [Google Scholar]
  31. Zlokovic B. V., Mackic J. B., Wang L., McComb J. G., McDonough A. Differential expression of Na,K-ATPase alpha and beta subunit isoforms at the blood-brain barrier and the choroid plexus. J Biol Chem. 1993 Apr 15;268(11):8019–8025. [PubMed] [Google Scholar]

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

RESOURCES