Abstract
Exposure of aortic strips from guinea-pigs to hypotonic extracellular fluid is followed by marked vasoconstriction, which is inhibited by D-600 (3 μM), a blocker of voltage-sensitive Ca2+ channels. Conventional electrophysiology, patch-clamp studies, pH determination with 2′, 7′ bis(2-carboxyethyl)-5, 6-carboxyfluorescein (BCECF) and Ca2+ measurements with Fura-2 have been performed on smooth muscle cells cultured either from rat or human aorta to further elucidate the underlying mechanisms. Exposure of the cells to a 25% hypotonic extracellular fluid leads to a rapid and fully reversible depolarization, paralleled by an increase of the selectivity and conductance of the cell membrane to Cl−, an acidification of the cytoplasm and an increase of intracellular Ca2+ concentration ([Ca2+]i). The latter is inhibited by the Ca2+ channel blocker D-600 (1–3 μM). It is concluded that osmotic cell swelling leads to the activation of an anion channel. The subsequent depolarization of the cell membrane activates voltage-sensitive Ca2+ channels which increases [Ca2+]i, thus stimulating the contraction of vascular smooth muscle cells.
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References
Almers W, Neher E (1985) The Ca signal from fura-2 loaded mast cells depends strongly on the method of dye-loading. FEBS Lett 192:13–18
Austin C, Wray S (1993) Changes of intracellular pH in rat mesenteric vascular smooth muscle with high-K+ depolarization. J Physiol (Lond) 469:1–10
Banderali U, Roy G (1992) Activation of K+ and Cl− channels in MDCK cells during volume regulation in hypotonic media. J Membr Biol 126:219–234
Banderali U, Roy G (1992) Anion channels for amino acids in MDCK cells. Am J Physiol 263:C1200-C1207
Bülow A, Johansson B (1994) Membrane stretch evoked by cell swelling increases contractile activity in vascular smooth muscle through dihydropyridine-sensitive pathways. Acta physiol Scand 152:419–427
Christensen O (1987) Mediation of cell volume regulation by Ca2+ influx through stretch-activated channels. Nature 330:66–68
Davis MJ, Donovitz JA, Hood JD (1992) Stretch-activated single-channel and whole cell currents in vascular smooth muscle cells. Am J Physiol 262:C1083-C1088
Doroshenko P, Neher E (1992) Volume-sensitive conductance in bovine chromaffin cell membrane. J physiol (Lond) 449:197–218
Ganz MB, Boyarsky G, Sterzel RB, Boron WF (1989) Arginine vasopressin enhances pHi regulation in the presence of HCO −3 by stimulating three acid-base transport systems. Nature 337:648–651
Graf J, Haddad P, Häussinger D, Lang F (1988) Cell volume regulation in liver. Renal Physiol Biochem 11:202–222
Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450
Johansson B, Jonsson O (1968) Cell volume as a factor influencing electrical and mechanical activity of vascular smooth muscle. Acta Physiol Scand 72:456–468
Jonsson O (1969) Changes in the activity of isolated vascular smooth muscle in response to reduced osmolarity. Acta Physiol Scand 77:191–200
Jonsson O (1969) Changes in the cell volume of isolated vascular smooth muscle in response to reduced osmolarity. Acta Physiol Scand 77:201–211
Lang F, Oberleithner H, Kolb HA, Paulmichl M, Völkl H, Wang W (1988) Interaction of intracellular pH and cell membrane potential. In: Häussinger D (ed) pH Homeostasis: mechanisms and control. Academic Press, London, pp 27–42
Lang F, Stehle T, Häussinger D (1989) Water, K+, H+, lactate and glucose fluxes during cell volume regulation in perfused rat liver. Pflügers Arch 413:209–216
Lang F, Friedrich F, Kahn E, Woell E, Hammerer M, Waldegger S, Maly K, Grunicke H (1991) Bradykinin induced oscillations of cell membrane potential in cells expressing the Ha-ras oncogene. J Biol Chem 266:4938–4942
Lang F, Ritter M, Wöll E, Weiss H, Häussinger D, Maly K, Grunicke H (1992) Altered cell volume regulation in ras oncogene expressing NIH fibroblasts. Pflügers Arch 420:424–427
Lansman JB, Hallam TJ, Rink TJ (1987) Single stretch-activated ion channels in vascular endothelial cells as mechanotransducers? Nature 325:81–813
Lau KR, Hudsen RL, Schultz SG (1984) Cell swelling increases a barium-inhibitable potassium conductance in the basolateral membrane of Necturus small intestine. Proc Natl Acad Sci USA 81:3591–3594
Linke AM, Betz E (1979) Excitability and NADH fluorescence of spontaneously active portal veins in relation to glucose withdrawal. Blood Vessels 16:295–301
Lopez AG, Guggino WB (1987) Volume regulation in the early proximal tubule of the Necturus kidney. J Membr Biol 97:117–125
Mendez F, Kolb HA (1995) Regulatory volume decrease of cultured kidney cells (OK): Dependence of calcium, ATP and GTP-γS and calcium signalling. Pflügers Arch (in press)
Nelson MT, Patlak JB, Worley JF, Standen NB (1990) Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol 259:C3-C18
Nilius B, Masahiro O, Zahradnik I, Droogmans G (1994) Activation of a Cl− current by hypotonic volume increase in human endothelial cells. J Gen Physiol 103:787–805
Nilius B, Sehrer J, Droogmans G (1994) Permeation properties and modulation of volume-activated Cl−-currents in human endothelial cells. Br J Pharmacol 112:1049–1056
Okada Y, Hazama A, Yuan W (1990) Stretch-induced activation of Ca2+-permeable ion channels is involved in the volume regulation of hypotonically swollen epithelial cells. Neurosci Res 12:5–13
Orlov SN, Resink TJ, Bernhardt J, Buhler FR (1992) Volume-dependent regulation of sodium and potassium fluxes in cultured vascular smooth muscle cells: dependence on medium osmolality and regulation by signalling systems. J Membr Biol 129:199–210
Ritter M, Paulmichl M, Lang F (1991) Further characterization of volume regulatory decrease in cultured renal epitheloid (MDCK) cells. Pflügers Arch 418:35–39
Roy G, Sauvé R (1987) Effect of anisotonic media on volume, ion and amino-acid content and membrane potential of kidney cells (MDCK) in culture. J Membr Biol 100:83–96
Ubl J, Murer H, Kolb HA (1988) Hypotonic shock evokes opening of Ca2+ activated K+ channels in opossum kidney cells. Pflügers Arch 412:551–553
Valverde MA, Diaz M, Sepulveda M, Gill DG, Hyde SC, Higgins CF (1992) Volume regulated chloride channels are associated with the human multidrug-resistance P-glycoprotein. Nature 355:830–833
Walker LN, Bowen-Pope DF, Ross R, Reidy MA (1986) Production of platelet-derived growth factor-like molecules by cultured arterial smooth muscle cells accompanies proliferation after arterial injury. Proc Natl Acad Sci USA 83:7311–7315
Weiss H, Lang F (1992) Ion channels activated by swelling of Madin Darby Canine Kidney (MDCK) cells. J Membr Biol 126:109–114
Yang XC, Sachs F (1989) Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243:1068–1071
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Lang, F., Busch, G.L., Zempel, G. et al. Ca2+ entry and vasoconstriction during osmotic swelling of vascular smooth muscle cells. Pflugers Arch. 431, 253–258 (1995). https://doi.org/10.1007/BF00410198
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DOI: https://doi.org/10.1007/BF00410198