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Inhibition of the histamine-induced Ca2+ influx in primary human endothelial cells (HUVEC) by volatile anaesthetics

Published online by Cambridge University Press:  01 December 2008

P. W. L. Tas ,
C. Stößel  and
N. Roewer
P. W. L. Tas*
Affiliation:
University of Würzburg, Center of Operative Medicine, Department of Anesthesiology, Oberdürrbacher Strasse 6, Würzburg, Germany
C. Stößel
Affiliation:
University of Würzburg, Center of Operative Medicine, Department of Anesthesiology, Oberdürrbacher Strasse 6, Würzburg, Germany
N. Roewer
Affiliation:
University of Würzburg, Center of Operative Medicine, Department of Anesthesiology, Oberdürrbacher Strasse 6, Würzburg, Germany
*
Correspondence to: Piet Tas, Klinik und Poliklinik für Anesthesiologie, Zentrum für Operative Medizin, der Universität Würzburg, Oberdürrbacher Strasse 6, 97080 Würzburg, Germany. E-mail: tas_p@klinik.uni-wuerzburg.de; Tel: +49 931 20130065; Fax: +49 931 20130019
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Summary

Background and objective

Vasoactive substances such as histamine, acetylcholine or ATP increase the [Ca2+]i of endothelial cells, which leads to the activation of nitric oxide synthase (eNOS). The NO produced by this enzyme relaxes the underlying smooth muscle. Evidence suggests that eNOS activation is dependent on agonist-induced Ca2+ entry. Recently we have shown that in human endothelial cells (HUVEC), this Ca2+ entry is sensitive to isoflurane. The objective here was to study the mechanism by which volatile anaesthetics can depress the histamine-induced Ca2+ entry into HUVEC cells.

Methods

HUVECs on coverslips were loaded with the Ca2+ indicator Fluo-3 and inserted in a gastight, temperature-controlled perfusion chamber. Excitation was at 488 nm and fluorescence signals were monitored with a confocal laser scanning microscope (MRC1024, Biorad). Direct measurement of the Ca2+ influx was with Mn2+ as surrogate for calcium at 360 nm in cells loaded with Fura-2.

Results

Addition of histamine induces a biphasic [Ca2+]i increase consisting of Ca2+ release from internal stores and a Ca2+ influx from the external medium (plateau phase). The plateau phase was dose-dependently inhibited by enflurane and sevoflurane (13.7 resp. 21.9% inhibition by 1 MAC anaesthetic). Direct measurement of the Ca2+ influx using the Mn2+ quench of the Fura-2 fluorescence gave similar results. The inhibition of the anaesthetics was not reduced by inhibition of the cGMP pathway, inactivation of protein kinase C, depolarization of the cells or the presence of specific Ca2+-dependent K+ channel inhibitors. Interestingly, unsaturated fatty acids inhibit the histamine-induced Ca2+ influx in a similar way as the volatile anaesthetics.

Conclusions

Volatile anaesthetics dose-dependently inhibit the histamine-induced Ca2+ influx in HUVECs by a mechanism that may involve unspecific perturbation of the lipid bilayer.

Keywords

ENDOTHELIUMCALCIUMENFLURANEISOFLURANEFLUO-3FURA-2
Type
Original Article
Information
European Journal of Anaesthesiology , Volume 25 , Issue 12 , December 2008 , pp. 976 - 985
Copyright
Copyright © European Society of Anaesthesiology 2008

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References

1.Johns, RA. Endothelium, anesthetics and vascular control. Anesthesiology 1993; 79: 1381–1391.CrossRefGoogle ScholarPubMed
2.Garland, CJ, Plane, F, Kemp, BK, Cocks, TM. Endothelium-dependent hyperpolarisation: a role in the control of vascular tone. Trends Pharmacol Sci 1995; 16: 23–30.CrossRefGoogle Scholar
3.Busse, R, Adwards, G, Félétou, M, Fleming, I, Vanhoutte, PM, Weston, AH. EDHF: bringing the concepts together. Trends Pharmacol Sci 2002; 23: 374–380.CrossRefGoogle ScholarPubMed
4.Mombouli, JV, Vanhoutte, PM. Endothelial dysfunction: a novel therapeutic target. Endothelial dysfunction: from physiology to therapy. J Mol Cell Cardiol 1999; 31: 61–74.CrossRefGoogle Scholar
5.Muldoon, SM, Hart, JL, Bowen, KA, Freas, W. Attenuation of endothelium-mediated vasodilation by halothane. Anesthesiology 1988; 68: 31–37.CrossRefGoogle ScholarPubMed
6.Todo, H, Nakamura, K, Hatano, Y, Nishiwada, M, Kakuyama, M, Mori, K. Halothane and isoflurane inhibit endothelium-dependent relaxation elicited by acetylcholine. Anesth Analg 1992; 75: 198–203.Google Scholar
7.Uggeri, MJ, Proctor, GJ, Johns, RA. Halothane, enflurane, and isoflurane attenuate both receptor and non-receptor mediated EDRF production in rat thoracic aorta. Anesthesiology 1992; 76: 1012–1017.CrossRefGoogle ScholarPubMed
8.Johns, RA, Tichotski, A, Muro, M, Spaeth, JP, Le Cras, TD, Rengasamy, A. Halothane and isoflurane inhibit endothelium dependent cyclic guanosine monophosphate accumulation in endothelial cell-vascular smooth muscle co-cultures independent of an effect on guanylyl cyclase activation. Anesthesiology 1995; 83: 823–834.CrossRefGoogle ScholarPubMed
9.Adams, DJ, Barakeh, J, Laskey, R, van Breemen, C. Ion channels and regulation of intracellular calcium in vascular endothelial cells. FASEB J 1989; 3: 2389–2400.CrossRefGoogle ScholarPubMed
10.Oike, M, Gericke, M, Droogmans, G, Nilius, B. Calcium entry activated by store depletion in human umbilical vein endothelial cells. Cell Calcium 1994; 16: 367–376.CrossRefGoogle ScholarPubMed
11.Nilius, B, Viana, F, Droogmans, G. Ion channels in vascular endothelium. Ann Rev Physiol 1997; 59: 145–170.CrossRefGoogle ScholarPubMed
12.Cheng, GF, Cheung, DW. Characterization of acetylcholine-induced membrane hyperpolarization in endothelial cells. Circ Res 1992; 70: 257–263.CrossRefGoogle Scholar
13.Faehling, M, Koch, ED, Raithel, J, Trischler, G, Waltenberger, J. Vascular endothelial growth factor-A activates Ca2+-activated K+ channels in human endothelial cells in culture. Int J Biochem Cell Biol 2001; 33: 337–346.CrossRefGoogle ScholarPubMed
14.Muraki, K, Imaizumi, Y, Ohya, S et al. Apamin sensitive Ca2+-dependent K+ current and hyperpolarisation in human endothelial cells. Biochem Biophys Res Commun 1997; 236: 340–343.CrossRefGoogle Scholar
15.Putney, JW. A model for receptor-regulated Ca2+-entry. Cell Calcium 1986; 7: 1–12.CrossRefGoogle Scholar
16.Lin, S, Fagan, KA, Li, KX, Shaul, PW, Cooper, DMF, Rodman, DM. Sustained endothelial nitric-oxide synthase activation requires capacitative Ca2+-entry. J Biol Chem 2000; 275: 17979–17985.CrossRefGoogle ScholarPubMed
17.Lückhoff, A, Pohl, U, Mülsch, A, Busse, R. Differential role of extra- and intracellular calcium in the release of EDRF and prostacyclin from cultured endothelial cells. Br J Pharmacol 1988; 95: 189–196.CrossRefGoogle ScholarPubMed
18.Pajewski, TN, Miao, N, Lynch, C, Johns, RA. Volatile anesthetics affect calcium mobilization in bovine endothelial cells. Anesthesiology 1996; 85: 1147–1156.CrossRefGoogle ScholarPubMed
19.Loeb, AL, Longnecker, DE, Williamson, JR. Alteration of calcium mobilization in endothelial cells by volatile anesthetics. Biochem Pharmacol 1993; 45: 1137–1142.CrossRefGoogle ScholarPubMed
20.Simoneau, C, Thuringer, D, Cai, S, Garneau, L, Blaise, G, Sauvé, R. Effects of halothane and isoflurane on bradykinin evoked Ca2+-influx in bovine aortic endothelial cells. Anesthesiology 1996; 85: 366–379.CrossRefGoogle Scholar
21.Kanna, T, Akata, T, Izumi, K et al. Sevoflurane and bradykinin-induced calcium mobilization in pulmonary arterial valvular endothelial cells in situ: sevoflurane stimulates plasmalemmal calcium influx into endothelial cells. J Cardiovasc Pharmacol 2002; 40: 714–724.CrossRefGoogle ScholarPubMed
22.Az-ma, T, Fujii, K, Yuge, O. Inhibitory effect of sevoflurane on nitric oxide release from cultured endothelial cells. Eur J Pharmacol 1995; 289: 33–39.CrossRefGoogle ScholarPubMed
23.Tas, PWL, Stößel, C, Roewer, N. The volatile anesthetic isoflurane inhibits the histamine-induced Ca2+-influx in primary human endothelial cells. Anesth Analg 2003; 97: 430–435.CrossRefGoogle ScholarPubMed
24.Jaffe, EA, Nachman, RL, Becker, CG, Minick, CR. Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria. J Clin Invest 1973; 52: 2745–2756.CrossRefGoogle ScholarPubMed
25.D`Amore, PA, Klagsbrun, M. Endothelial cell mitogens derived from retina and hypothalamus: biochemical and biological similarities. J Cell Biol 1984; 99: 1545–1549.CrossRefGoogle ScholarPubMed
26.Tas, PWL, Koschel, K. Volatile anesthetics stimulate the phorbol ester evoked neurotransmitter release from PC12 cells through an increase of the cytoplasmic Ca2+-ion concentration. Biochim Biophys Acta 1991; 1091: 401–404.CrossRefGoogle ScholarPubMed
27.Merritt, JE, Jacob, R, Hallam, TJ. Use of manganese to discriminate between calcium influx and mobilization from internal stores in stimulated human neutrophils. J Biol Chem 1989; 264: 1522–1527.CrossRefGoogle ScholarPubMed
28.Fasolato, C, Hoth, M, Matthews, G, Penner, R. Ca2+ and Mn2+ influx through receptor-mediated activation of non-specific cation channels in mast cells. Proc Natl Acad Sci USA 1993; 90: 3068–3072.CrossRefGoogle Scholar
29.Ethier, MF, Yamaguchi, H, Madison, JM. Effects of cyclopiazonic acid on cytoplasmic calcium in bovine airway smooth muscle. Am J Physiol 2001; 281: L126–L133.Google ScholarPubMed
30.Iouzalen, L, David-Dufilho, M, Devynck, MA. Refilling state of internal Ca2+ stores is not the only intracellular signal stimulating Ca2+ influx in human endothelial cells. Biochem Pharmacol 1995; 49: 893–899.CrossRefGoogle Scholar
31.Frieden, M, Graier, WF. Subplasmalemmal ryanodine-sensitive Ca2+ release contributes to Ca2+-dependent K+ channel activation in a human umbilical vein endothelial cell line. J Physiol 2000; 524: 715–724.CrossRefGoogle Scholar
32.Su, JY, Vo, AC. Role of protein kinase C, Ca2+/calmodulin-dependent protein kinase II, and mitogen-activated protein kinases in volatile anesthetic-induced relaxation in newborn rabbit pulmonary artery. Anesthesiology 2003; 99: 131–137.CrossRefGoogle ScholarPubMed
33.Marinovic, J, Bosnjak, ZJ, Stadnicka, A. Preconditioning by isoflurane induces lasting sensitization of the cardiac sarcolemmal adenosine triphosphate-sensitive potassium channel by a protein kinase C-delta-mediated mechanism. Anesthesiology 2005; 103: 540–547.CrossRefGoogle ScholarPubMed
34.Groschner, K, Hingel, S, Lintschinger, B et al. Trp proteins form store-operated cation channels in human vascular endothelial cells. FEBS Lett 1998; 437: 101–106.CrossRefGoogle ScholarPubMed
35.Minke, B, Cook, B. TRP channel proteins and signal transduction. Physiol Rev 2002; 82: 429–472.CrossRefGoogle ScholarPubMed
36.Freichel, M, Suh, SH, Pfeifer, A et al. Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4−/− mice. Nat Cell Biol 2001; 3: 121–127.CrossRefGoogle ScholarPubMed
37.Osanai, T, Fujita, N, Fujiwara, N et al. Cross talk of shear-induced production of prostacyclin and nitric oxide in endothelial cells. Am J Physiol 2000; 278: H233–H238.Google ScholarPubMed
38.Heller, R, Bussolino, F, Ghigo, D et al. Protein kinase C and cyclic AMP modulate thrombin-induced platelet-activating factor synthesis in human endothelial cells. Biochim Biophys Acta 1991; 1093: 55–64.CrossRefGoogle ScholarPubMed
39.Kwan, HY, Huang, Y, Yao, X. Store-operated calcium entry in vascular endothelial cells is inhibited by cGMP via a protein kinase G dependent mechanism. J Biol Chem 2000; 275: 6758–6763.CrossRefGoogle Scholar
40.Draijer, R, Vaandrager, AB, Nolte, C et al. Expression of cGMP-dependent protein kinase I and phosphorylation of its substrate, vasodilator stimulated phosphoprotein, in human endothelial cells. Circ Res 1995; 77: 897–905.CrossRefGoogle ScholarPubMed
41.Gamberucci, A, Fulceri, R, Benedetti, A. Inhibition of store-dependent capacitative Ca2+ influx by unsaturated fatty acids. Cell Calcium 1997; 21: 375–385.CrossRefGoogle ScholarPubMed