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

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Ion Flux in Pulmonary Vascular Control

Part of the book series: NATO ASI 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.

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References

  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. 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.

    CAS  Google Scholar 

  3. Ashford, M.L.J. ATP-regulated K+ channels in rat hypothalamic neurones. J. Physiol. Lond. in press, 1992.

    Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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, 1

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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, 1

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  10. Bradford, J.R. and H.P. Dean. The pulmonary circulation. J. Physiol. Lond. 16:34–96, 1894.

    PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Chapter  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  29. Lichtheim. Die Stoerungen des Lungenkreislaufes und ihr Einfluss auf den. Blutdruck. Inaug. Dissert. Berlin, 1876.

    Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  38. Plumier, P.L. La circulation pulmonaire chez le chien. Arch. Int. Physiol. 1:176–213, 1904.

    Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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. 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. 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.

    PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  46. Stanbrook, H.S. and I.F. McMurtry. Inhibition of glycolysis potentiates hypoxic vasoconstriction in rat lung. J. Appl. Physiol. 55:1467–1473, 1983.

    PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  48. Suzuki, H. and B.M. Twarog. Membrane properties of smooth muscle cells in pulmonary hypertensive rats. Am. J. Physiol. 242:H907–H915, 1982.

    PubMed  CAS  Google Scholar 

  49. Voelkel, N.F., I.F. McMurtry, and J.T. Reeves. Hypoxia impairs vasodilation in the lung. J. Clin. Invest. 67:238–246, 1981.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  53. Yuan, X.-J. The cellular mechanisms of hypoxia pulmonary vasoconstriction. Progress in Physiol. Sci. 20(4):301–306, 1989.

    CAS  Google Scholar 

  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. 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. 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. 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.

    PubMed  CAS  Google Scholar 

  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 

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Authors and Affiliations

  1. Department of Physiology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Xiao-Jian Yuan, Mary L. Tod, Magdalena Juhaszova, William F. Goldman, Lewis J. Rubin & Mordecai P. Blaustein

  2. Division of Pulmonary and Critical Care Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Xiao-Jian Yuan, Carmen G. Salvaterra, Mary L. Tod & Lewis J. Rubin

  3. Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Xiao-Jian Yuan, Carmen G. Salvaterra, Mary L. Tod, Lewis J. Rubin & Mordecai P. Blaustein

  4. Hypertension Center, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Xiao-Jian Yuan, Carmen G. Salvaterra, Mary L. Tod, Magdalena Juhaszova, William F. Goldman, Lewis J. Rubin & Mordecai P. Blaustein

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  1. Xiao-Jian Yuan
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Editor information

Editors and Affiliations

  1. Veterans Administration Medical Center, Minneapolis, Minnesota, USA

    E. Kenneth Weir

  2. University of Nevada, Reno, Nevada, USA

    Joseph R. Hume

  3. University of Colorado, Denver, Colorado, USA

    John T. Reeves

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Yuan, XJ. et al. (1993). The Sodium Gradient, Potassium Channels, and Regulation of Calcium in Pulmonary and Mesenteric Arterial Smooth Muscles: Effects of Hypoxia. In: Weir, E.K., Hume, J.R., Reeves, J.T. (eds) Ion Flux in Pulmonary Vascular Control. NATO ASI Series, vol 251. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2397-0_16

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  • DOI: https://doi.org/10.1007/978-1-4615-2397-0_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6016-2

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