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. 1997 Jul 15;502(Pt 2):397–408. doi: 10.1111/j.1469-7793.1997.397bk.x

Hyperpolarization of isolated capillaries from guinea-pig heart induced by K+ channel openers and glucose deprivation.

U Langheinrich 1, J Daut 1
PMCID: PMC1159558  PMID: 9263919

Abstract

1. The present study was designed to test if microvascular coronary endothelial cells express ATP-sensitive K+ channels (KATP channels). We performed microfluorometric measurements of the membrane potential of freshly isolated guinea-pig coronary capillaries equilibrated with the voltage-sensitive dye bis-oxonol (bis-[1,3-dibutylbarbituric acid] trimethineoxonol, [DiBAC4(3)]). 2. The resting membrane potential of capillaries in physiological salt solution was -46 +/- 4.2 mV (n = 8) at room temperature (22 degrees C) as determined after calibration of the fluorescence using the Na(+)-K+ ionophore gramicidin in the presence of different K+ concentrations. Spontaneous membrane potential fluctuations of 10-20 mV amplitude were often observed. 3. A reversible, sustained hyperpolarization to a new membrane potential close to the K+ equilibrium potential (EK) could be induced by application of the K+ channel openers HOE 234 (100 nM to 1 microM), diazoxide (10 PM to 100 nM) or pinacidil (100 nM). Subsequent addition of glibenclamide (200 nM to 2 microM) reversed this hyperpolarization. 4. A glibenclamide-sensitive hyperpolarization of coronary capillaries to values near EK was also observed upon omission of D-glucose (10 mM) from the superfusing solution or by substituting L-glucose for D-glucose. Maximum hyperpolarization was reached in less than 10 min. 5. Our results suggest that microvascular coronary endothelial cells express KATP channels which may be activated during hypoglycaemia.

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Selected References

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

  1. Adams D. J., Barakeh J., Laskey R., Van Breemen C. Ion channels and regulation of intracellular calcium in vascular endothelial cells. FASEB J. 1989 Oct;3(12):2389–2400. doi: 10.1096/fasebj.3.12.2477294. [DOI] [PubMed] [Google Scholar]
  2. Ashcroft F. M. Adenosine 5'-triphosphate-sensitive potassium channels. Annu Rev Neurosci. 1988;11:97–118. doi: 10.1146/annurev.ne.11.030188.000525. [DOI] [PubMed] [Google Scholar]
  3. Ashcroft F. M., Ashcroft S. J., Harrison D. E. Properties of single potassium channels modulated by glucose in rat pancreatic beta-cells. J Physiol. 1988 Jun;400:501–527. doi: 10.1113/jphysiol.1988.sp017134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ashford M. L., Boden P. R., Treherne J. M. Glucose-induced excitation of hypothalamic neurones is mediated by ATP-sensitive K+ channels. Pflugers Arch. 1990 Jan;415(4):479–483. doi: 10.1007/BF00373626. [DOI] [PubMed] [Google Scholar]
  5. Berweck S., Thieme H., Helbig H., Lepple-Wienhues A., Wiederholt M. Effect of elevated glucose concentration on membrane voltage regulation in retinal capillary pericytes. Diabetes. 1993 Sep;42(9):1347–1350. doi: 10.2337/diab.42.9.1347. [DOI] [PubMed] [Google Scholar]
  6. Bräuner T., Hülser D. F., Strasser R. J. Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim Biophys Acta. 1984 Apr 11;771(2):208–216. doi: 10.1016/0005-2736(84)90535-2. [DOI] [PubMed] [Google Scholar]
  7. Cannell M. B., Sage S. O. Bradykinin-evoked changes in cytosolic calcium and membrane currents in cultured bovine pulmonary artery endothelial cells. J Physiol. 1989 Dec;419:555–568. doi: 10.1113/jphysiol.1989.sp017886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Daut J., Mehrke G., Nees S., Newman W. H. Passive electrical properties and electrogenic sodium transport of cultured guinea-pig coronary endothelial cells. J Physiol. 1988 Aug;402:237–254. doi: 10.1113/jphysiol.1988.sp017202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Dean P. M., Matthews E. K., Sakamoto Y. Pancreatic islet cells: effects of monosaccharides, glycolytic intermediates and metabolic inhibitors on membrane potential and electrical activity. J Physiol. 1975 Mar;246(2):459–478. doi: 10.1113/jphysiol.1975.sp010899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Edwards G., Weston A. H. The pharmacology of ATP-sensitive potassium channels. Annu Rev Pharmacol Toxicol. 1993;33:597–637. doi: 10.1146/annurev.pa.33.040193.003121. [DOI] [PubMed] [Google Scholar]
  12. Epps D. E., Wolfe M. L., Groppi V. Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3-dibutylbarbituric acid)trimethine oxonol (Dibac4(3)) in model systems and cells. Chem Phys Lipids. 1994 Feb;69(2):137–150. doi: 10.1016/0009-3084(94)90035-3. [DOI] [PubMed] [Google Scholar]
  13. He P., Curry F. E. Endothelial cell hyperpolarization increases [Ca2+]i and venular microvessel permeability. J Appl Physiol (1985) 1994 Jun;76(6):2288–2297. doi: 10.1152/jappl.1994.76.6.2288. [DOI] [PubMed] [Google Scholar]
  14. He P., Curry F. E. Measurement of membrane potential of endothelial cells in single perfused microvessels. Microvasc Res. 1995 Sep;50(2):183–198. doi: 10.1006/mvre.1995.1052. [DOI] [PubMed] [Google Scholar]
  15. Holevinsky K. O., Fan Z., Frame M., Makielski J. C., Groppi V., Nelson D. J. ATP-sensitive K+ channel opener acts as a potent Cl- channel inhibitor in vascular smooth muscle cells. J Membr Biol. 1994 Jan;137(1):59–70. doi: 10.1007/BF00234998. [DOI] [PubMed] [Google Scholar]
  16. Hutcheson I. R., Griffith T. M. Heterogeneous populations of K+ channels mediate EDRF release to flow but not agonists in rabbit aorta. Am J Physiol. 1994 Feb;266(2 Pt 2):H590–H596. doi: 10.1152/ajpheart.1994.266.2.H590. [DOI] [PubMed] [Google Scholar]
  17. Inagaki N., Gonoi T., Clement J. P., Wang C. Z., Aguilar-Bryan L., Bryan J., Seino S. A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels. Neuron. 1996 May;16(5):1011–1017. doi: 10.1016/s0896-6273(00)80124-5. [DOI] [PubMed] [Google Scholar]
  18. Janigro D., West G. A., Gordon E. L., Winn H. R. ATP-sensitive K+ channels in rat aorta and brain microvascular endothelial cells. Am J Physiol. 1993 Sep;265(3 Pt 1):C812–C821. doi: 10.1152/ajpcell.1993.265.3.C812. [DOI] [PubMed] [Google Scholar]
  19. Katnik C., Adams D. J. An ATP-sensitive potassium conductance in rabbit arterial endothelial cells. J Physiol. 1995 Jun 15;485(Pt 3):595–606. doi: 10.1113/jphysiol.1995.sp020755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Laskey R. E., Adams D. J., Cannell M., van Breemen C. Calcium entry-dependent oscillations of cytoplasmic calcium concentration in cultured endothelial cell monolayers. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1690–1694. doi: 10.1073/pnas.89.5.1690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lückhoff A., Busse R. Activators of potassium channels enhance calcium influx into endothelial cells as a consequence of potassium currents. Naunyn Schmiedebergs Arch Pharmacol. 1990 Jul;342(1):94–99. doi: 10.1007/BF00178979. [DOI] [PubMed] [Google Scholar]
  22. Lückhoff A., Busse R. Calcium influx into endothelial cells and formation of endothelium-derived relaxing factor is controlled by the membrane potential. Pflugers Arch. 1990 May;416(3):305–311. doi: 10.1007/BF00392067. [DOI] [PubMed] [Google Scholar]
  23. Marchenko S. M., Sage S. O. Electrical properties of resting and acetylcholine-stimulated endothelium in intact rat aorta. J Physiol. 1993 Mar;462:735–751. doi: 10.1113/jphysiol.1993.sp019579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mehrke G., Daut J. The electrical response of cultured guinea-pig coronary endothelial cells to endothelium-dependent vasodilators. J Physiol. 1990 Nov;430:251–272. doi: 10.1113/jphysiol.1990.sp018290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mehrke G., Pohl U., Daut J. Effects of vasoactive agonists on the membrane potential of cultured bovine aortic and guinea-pig coronary endothelium. J Physiol. 1991 Aug;439:277–299. doi: 10.1113/jphysiol.1991.sp018667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miao K., Joyner W. L. In situ study of the membrane potential in microvascular endothelial cells using a fluorescent probe. Microvasc Res. 1994 Jul;48(1):135–142. doi: 10.1006/mvre.1994.1044. [DOI] [PubMed] [Google Scholar]
  27. Neylon C. B., Avdonin P. V., Dilley R. J., Larsen M. A., Tkachuk V. A., Bobik A. Different electrical responses to vasoactive agonists in morphologically distinct smooth muscle cell types. Circ Res. 1994 Oct;75(4):733–741. doi: 10.1161/01.res.75.4.733. [DOI] [PubMed] [Google Scholar]
  28. Priebe L., Friedrich M., Benndorf K. Functional interaction between K(ATP) channels and the Na(+)-K(+) pump in metabolically inhibited heart cells of the guinea-pig. J Physiol. 1996 Apr 15;492(Pt 2):405–417. doi: 10.1113/jphysiol.1996.sp021317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Snetkov V. A., Hirst S. J., Ward J. P. Ion channels in freshly isolated and cultured human bronchial smooth muscle cells. Exp Physiol. 1996 Sep;81(5):791–804. doi: 10.1113/expphysiol.1996.sp003977. [DOI] [PubMed] [Google Scholar]
  30. Vanhoutte P. M., Rubanyi G. M., Miller V. M., Houston D. S. Modulation of vascular smooth muscle contraction by the endothelium. Annu Rev Physiol. 1986;48:307–320. doi: 10.1146/annurev.ph.48.030186.001515. [DOI] [PubMed] [Google Scholar]
  31. Voyta J. C., Via D. P., Butterfield C. E., Zetter B. R. Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J Cell Biol. 1984 Dec;99(6):2034–2040. doi: 10.1083/jcb.99.6.2034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weiss J. N., Lamp S. T. Glycolysis preferentially inhibits ATP-sensitive K+ channels in isolated guinea pig cardiac myocytes. Science. 1987 Oct 2;238(4823):67–69. doi: 10.1126/science.2443972. [DOI] [PubMed] [Google Scholar]
  33. al-Mehdi A. B., Ischiropoulos H., Fisher A. B. Endothelial cell oxidant generation during K(+)-induced membrane depolarization. J Cell Physiol. 1996 Feb;166(2):274–280. doi: 10.1002/(SICI)1097-4652(199602)166:2<274::AID-JCP4>3.0.CO;2-M. [DOI] [PubMed] [Google Scholar]

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