The Sodium Gradient, Potassium Channels, and Regulation of Calcium in Pulmonary and Mesenteric Arterial Smooth Muscles: Effects of Hypoxia

  • Xiao-Jian Yuan
  • Carmen G. Salvaterra
  • Mary L. Tod
  • Magdalena Juhaszova
  • William F. Goldman
  • Lewis J. Rubin
  • Mordecai P. Blaustein
Part of the NATO ASI Series book series (NSSA, volume 251)

Abstract

Contraction in vascular smooth muscle (VSM) is generally initiated by the membrane excitation that triggers an increase in cytoplasmic free Ca2+ ([Ca2+]i) which then activates the contractile apparatus (19, 26). In general, [Ca2+]i can be increased by i) Ca2+ influx, through voltage-gated Ca2+ channels by depolarization of the plasma membrane, and/or through receptor-operated Ca2+ channels by vasoconstrictive mediators; ii) Ca2+ release from sarcoplasmic reticulum (SR), mitochondrial, and other intracellular Ca2+ stores; iii) decreased Ca2+ extrusion (via Na-Ca exchange, Ca2+-ATPase) and sequestration (via mitochondria, SR, Ca2+-binding proteins); and iv) increased Ca2+ entry via Na-Ca exchange. Ca2+ influx through voltage-gated Ca2+ channels is controlled mainly by the membrane potential (Em) (35) that is dominated by K+ channel permeability and the transmembrane K+ distribution (14). The smooth muscle cell membrane possesses a high membrane input resistance (13, 35, 56); thus, a small decrease in K+ conductance should cause a relatively large depolarization, which should, in turn, open voltage-gated Ca2+ channels and thereby increase [Ca2+]i.

Keywords

Tungsten MgCl CaCl Cytosol HEPES 

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References

  1. 1.
    Ambesi, A., E.E. Bagwell, and G.E. Lindenmayer. Purification and identification of the cardiac sarcolemma Na/Ca exchanger. Biophys. J. 59:138A, 1991.Google Scholar
  2. 2.
    Archer, S.L., J.A. Will, and E.K. Weir. Redox status in the control of pulmonary vascular tone. He 11(3):127–141, 1986.Google Scholar
  3. 3.
    Ashford, M.L.J. ATP-regulated K+ channels in rat hypothalamic neurones. J. Physiol. Lond. in press, 1992.Google Scholar
  4. 4.
    Beech, D.J. and T.B. Bolton. Two components of potassium current activated by depolarization of single smooth muscle cells from the rabbit portal vein. J. Physiol. Lond. 418:293–309, 1989.PubMedGoogle Scholar
  5. 5.
    Bennie, R.E., C.S. Packer, D.R. Powell, N. Jin, and R.A. Rhoades. Biphasic contractile response of pulmonary artery to hypoxia. Am. J. Physiol. 261:L156–L163, 1PubMedGoogle Scholar
  6. 6.
    Bergofsky, E.H. and S. Holtzman. A study of the mechanisms involved in the pulmonary arterial pressor response to hypoxia. Circ. Res. 20:506–519, 1967.PubMedCrossRefGoogle Scholar
  7. 7.
    Blaustein, M.P., W.F. Goldman, G. Fontana, B.K. Krueger, E.M. Santiago, T.D. Steele, D.N. Weis, and P.J. Yarowsky. Physiological roles of the sodium-calcium exchanger in nerve and muscle. Ann. NY Acad. Sci. 639:254–274, 1PubMedCrossRefGoogle Scholar
  8. 8.
    Bonnet, P., D. Gebremedhin, N.J. Rush, and D.R. Harder. Effects of hypoxia on a potassium channel in cat cerebral arterial muscle cells. Zeitschrift für Kardiologie 80(Suppl. 7):25–27, 1991.PubMedGoogle Scholar
  9. 9.
    Bova, S., W.F. Goldman, X.-J. Yuan, and M.P. Blaustein. Influence of Na+ gradient on Ca2+ transients and contraction in vascular smooth muscle. Am. J. Physiol. 259:H409–H423, 1990.PubMedGoogle Scholar
  10. 10.
    Bradford, J.R. and H.P. Dean. The pulmonary circulation. J. Physiol. Lond. 16:34–96, 1894.PubMedGoogle Scholar
  11. 11.
    Brayden, J.E. and M.T. Nelson. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science Wash. DC 256:532–535, 1992.CrossRefGoogle Scholar
  12. 12.
    Buescher, P.C., D.B. Pearse, R.P. Pillai, M.C. Litt, M.C. Mitchell, and J.T. Sylvester. Energy state and vasomotor tone in hypoxic pig lungs. J. Appl. Physiol. 70(4): 1874–1881, 1991.PubMedGoogle Scholar
  13. 13.
    Clapp, L.H. and A.M. Gurney. ATP-sensitive K+ channels regulate resting potential of pulmonary arterial smooth muscle cells. Am. J. Physiol. 262:H916–H920, 1992.PubMedGoogle Scholar
  14. 14.
    Cox, R.H. Potassium channel activators in vascular smooth muscle. In: Cellular and Molecular Mechanisms in Hypertension, edited by R.H. Cox. New York: Plenum Press, 1991, p. 27–43.CrossRefGoogle Scholar
  15. 15.
    Daut, J., W. Maier-Rudolph, N. von Beckerath, G. Mehrke, K. Guntherk and L. Goedel-Meinen. Hypoxic dilation of coronary arteries in mediated by ATP-sensitive potassium channels. Science Wash. DC 247:1341–1344, 1990.CrossRefGoogle Scholar
  16. 16.
    Davies, N.W., N.B. Standen and P.R. Stanfield. ATP-dependent potassium channels of muscle cells:their properties, regulation, and possible function. J. Bioenergetics and Biomembranes 23(4):509–535, 1991.CrossRefGoogle Scholar
  17. 17.
    Duchen, M. R. Effects of metabolic inhibition of the membrane properties of isolated mouse primary sensory neurones. J. Physiol. Lond. 424:387–409, 1990.PubMedGoogle Scholar
  18. 18.
    Farrukh, I.S. and J.R. Michael. Cellular mechanisms that control pulmonary vascular tone during hypoxia and normoxia. Am. Rev. Respir. Dis., 145:1389–1397, 1992.PubMedGoogle Scholar
  19. 19.
    Filo, R.S., D.F. Bohr, and J.C. Ruegg. Glycerinated skeletal and smooth muscle: calcium and magnesium dependence. Science Wash. DC 147:1581–1583, 1972.CrossRefGoogle Scholar
  20. 20.
    Frank, J.S., G. Mottino, D. Reid, R.S. Molday, and K.D. Philipson. Distribution of the Na+-Ca2+ exchange protein in mammalian cardiac myocytes: An immunofluorescence and immunocolloidal gold-labeling study. J. Cell Biol. 117:337–345, 1992.PubMedCrossRefGoogle Scholar
  21. 21.
    Ganfornina, M.D. and J. Lopez-Barneo. Potassium channel types in arterial chemoreceptor cells and their selective modulation by oxygen. J. Gen. Physiol. 100:401–426, 1992.PubMedCrossRefGoogle Scholar
  22. 22.
    Goldman, W.F., S. Bova, and M.P. Blaustein. Measurement of intracellular Ca2+ in cultured arterial smooth muscle cells using fura-2 and digital imaging microscopy. Cell Calcium 11:221–231, 1990.PubMedCrossRefGoogle Scholar
  23. 23.
    Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:85–100, 1981.PubMedCrossRefGoogle Scholar
  24. 24.
    Harder, D.R., J.A. Madden, and C. Dawson. Hypoxic induction of Ca2+-dependent action potentials in small pulmonary arteries of the cat. J. Appl. Physiol. 59(5): 1389–1393, 1985.PubMedGoogle Scholar
  25. 25.
    Hasunuma, K., D.M. Rodman, and I.F. McMurtry. Effects of K+ channel blockers on vascular tone in the perfused rat lung. Am. Rev. Respir. Dis. 144:884–887, 1991.PubMedCrossRefGoogle Scholar
  26. 26.
    Kamm, K.E., and J.T. Stull. The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Ann. Rev. Pharmacol. Toxicol. 25:593–620, 1989.Google Scholar
  27. 27.
    Kieval, R.S., R.J. Bloch, G.E. Lindenmayer, A. Ambesi, W.J. Lederer. Immunofluorescence localization of the Na-Ca exchanger in heart cells. Am. J. Physiol. 263:C545–C550, 1992.PubMedGoogle Scholar
  28. 28.
    Levitan, I.B., S. Chung, and P.H. Reinhart. Modulation of a single ion channel by several different protein kinases. Advances in Second Messenger and Phosphoprotein Research 24:36–40, 1990.PubMedGoogle Scholar
  29. 29.
    Lichtheim. Die Stoerungen des Lungenkreislaufes und ihr Einfluss auf den. Blutdruck. Inaug. Dissert. Berlin, 1876.Google Scholar
  30. 30.
    Lopez-Lopez, J., C. Gonzalez, J. Urena, and J. Lopez-Barneo. Low pO2 selectively inhibits K channel activity in chemoreceptor cells of the mammalian carotid body. J. Gen. Physiol. 93:1001–1015, 1989.PubMedCrossRefGoogle Scholar
  31. 31.
    Luther, P.W., R.K. Yip, R.J. Bloch, A. Ambesi, G.E. Lindenmayer, and M.P. Blaustein. Presynaptic localization of sodium/calcium exchangers in neuromuscular preparations. J. Neurosci., in press, 1992.Google Scholar
  32. 32.
    Madden, J.A., M.S. Vadula, and V.P. Kurup. Effects of hypoxia and other vasoactive agents on pulmonary and cerebral artery smooth muscle cells. Am. J. Physiol. 263:L384–L393, 1992.PubMedGoogle Scholar
  33. 33.
    McMurtry, I.F., A.B. Davidson, J.T. Reeves, and R.F. Grover. Inhibition of hypoxic pulmonary vasoconstriction by calcium antagonists in isolated rat lungs. Circ. Res. 38:99–104, 1976.PubMedCrossRefGoogle Scholar
  34. 34.
    Murray, T.R., L. Chen, B.E. Marshall, and E.J. Macarak. Hypoxic contraction of cultured pulmonary vascular smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 3:457–465, 1990.PubMedGoogle Scholar
  35. 35.
    Nelson, M.T., J.B. Patlak, J.F. Worley, and N.B. Standen. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am. J. Physiol. 259:C3–C18, 1990.PubMedGoogle Scholar
  36. 36.
    Ohe, M., T. Mimata, T. Haneda and T. Takishima. Time course of pulmonary vasoconstriction with repeated hypoxia and glucose depletion. Respir. Physiol. 63:177–186, 1986.PubMedCrossRefGoogle Scholar
  37. 37.
    Okabe, K., K. Kitamura, and H. Kuriyama. Features of 4-aminopyridine sensitive outward current observed in single smooth muscle cells from the rabbit pulmonary artery. Pflügers Arch. 409:561–568, 1987.PubMedCrossRefGoogle Scholar
  38. 38.
    Plumier, P.L. La circulation pulmonaire chez le chien. Arch. Int. Physiol. 1:176–213, 1904.Google Scholar
  39. 39.
    Post, J.M., J.R. Hume, S.L. Archer, and E.K. Weir. Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction. Am. J. Physiol. 262:C882–C890, 1992.PubMedGoogle Scholar
  40. 40.
    Robertson, B.E., P.R. Corry, P.C.G. Nye, and R.Z. Kozloswski. Ca2+ and Mg-ATP activated potassium channels from rat pulmonary artery. Pflügers Arch 421:94–96, 1992.PubMedCrossRefGoogle Scholar
  41. 41.
    Rodman, D.M. and N.F. Voelkel. Regulation of vascular tone. In: The Lung, Scientific Foundations. R.G. Crystal, J.B. West, P.J. Barnes, N.S. Cherniack, and E.R. Weibel, editors. Raven Press, Ltd., New York, 1991, p. 1105–1119.Google Scholar
  42. 42.
    Rodman, D.M., T. Yamaguchi, K. Hasunuma, R.F. O’Brien, and I.F. McMurtry. Hypoxic contraction of isolated rat pulmonary artery. J. Pharmacol. Exp. Ther. 248:952–959, 1988.Google Scholar
  43. 43.
    Salvaterra, C.G. and W.F. Goldman. Acute hypoxia increases cytosolic calcium in cultured pulmonary arterial myocytes. Am. J. Physiol., in press, 1992.Google Scholar
  44. 44.
    Salvaterra, C.G., L.J. Rubin, J. Schaeffer, and M.P. Blaustein. The influence of the transmembrane sodium gradient on the responses of pulmonary arteries to decreases in oxygen tension. Am. Rev. Respir. Dis. 139:933–939, 1989.PubMedGoogle Scholar
  45. 45.
    See, K.L., I.J. Forbes and W.H. Betts. Oxygen dependency of phototoxicity with hematoporphyrin derivative. Biochem. Photobiol. 39(5):631–634, 1984.CrossRefGoogle Scholar
  46. 46.
    Stanbrook, H.S. and I.F. McMurtry. Inhibition of glycolysis potentiates hypoxic vasoconstriction in rat lung. J. Appl. Physiol. 55:1467–1473, 1983.PubMedGoogle Scholar
  47. 47.
    Standen, N.B., J.M. Quayle, N.W. Davies, J.E. Brayden, Y. Huang, and M.T. Nelson. Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science Wash. DC 245:177–190, 1989.CrossRefGoogle Scholar
  48. 48.
    Suzuki, H. and B.M. Twarog. Membrane properties of smooth muscle cells in pulmonary hypertensive rats. Am. J. Physiol. 242:H907–H915, 1982.PubMedGoogle Scholar
  49. 49.
    Voelkel, N.F., I.F. McMurtry, and J.T. Reeves. Hypoxia impairs vasodilation in the lung. J. Clin. Invest. 67:238–246, 1981.PubMedCrossRefGoogle Scholar
  50. 50.
    Volk, K.A., J.J. Matsuda, and E.F. Shibata. A voltage-dependent potassium current in rabbit coronary artery smooth muscle cells. J. Physiol. Lond. 439:751–768, 1991.PubMedGoogle Scholar
  51. 51.
    Von Beckerath, N., S. Cyrys, A. Dischner, and J. Daut. Hypoxic vasodilation in isolated, perfused guinea-pig heart: an analysis of the underlying mechanisms. J. Physiol. Lond. 442:297–319, 1991.PubMedGoogle Scholar
  52. 52.
    Von Euler, U.S. and G. Liljestrand. Observations on the pulmonary arterial blood pressure in the cat. Acta Physiol. Scand. 12:301–320, 1946.CrossRefGoogle Scholar
  53. 53.
    Yuan, X.-J. The cellular mechanisms of hypoxia pulmonary vasoconstriction. Progress in Physiol. Sci. 20(4):301–306, 1989.Google Scholar
  54. 54.
    Yuan, X.-J and Y.N. Cai. Effects of calcium antagonists on pulmonary hypertension during acute hypoxia in rats. Chinese J. Appl. Physiol. 2(2): 136–141, 1989.Google Scholar
  55. 55.
    Yuan, X.-J., W.F. Goldman, MX Tod, L.J. Rubin, and M.P. Blaustein. Hypoxia reduced potassium currents in cultured rat pulmonary but not mesenteric arterial myocytes. Am. J. Physiol. in press, 1992.Google Scholar
  56. 56.
    Yuan, X.-J., W.F. Goldman, M.L. Tod, L.J. Rubin, and M.P. Blaustein. Ionic currents in rat pulmonary and mesenteric arterial myocytes in primary culture and subculture. Am. J. Physiol. in press, 1992.Google Scholar
  57. 57.
    Yuan, X.-J., MX. Tod, L.J. Rubin, and M.P. Blaustein. Contrasting effects of hypoxia on tension in rat pulmonary and mesenteric arteries. Am. J. Physiol. 259:H281–H289, 1990.PubMedGoogle Scholar
  58. 58.
    Yuan, X.-J., T. Sugiyama, W.F. Goldman, L.J. Rubin, and M.P. Blaustein. A mitochondrial uncoupler, FCCP, increases K+ current in rat pulmonary arterial myocytes. Biophys. J. in press, 1993.Google Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Xiao-Jian Yuan
    • 1
    • 2
    • 3
    • 4
  • Carmen G. Salvaterra
    • 2
    • 3
    • 4
  • Mary L. Tod
    • 1
    • 2
    • 3
    • 4
  • Magdalena Juhaszova
    • 1
    • 4
  • William F. Goldman
    • 1
    • 4
  • Lewis J. Rubin
    • 1
    • 2
    • 3
    • 4
  • Mordecai P. Blaustein
    • 1
    • 3
    • 4
  1. 1.Department of PhysiologyUniversity of Maryland School of MedicineBaltimoreUSA
  2. 2.Division of Pulmonary and Critical Care MedicineUniversity of Maryland School of MedicineBaltimoreUSA
  3. 3.Department of MedicineUniversity of Maryland School of MedicineBaltimoreUSA
  4. 4.Hypertension CenterUniversity of Maryland School of MedicineBaltimoreUSA

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