Arachidonic acid-induced calcium influx in human platelets. Comparison with the effect of thrombin (original) (raw)

Abstract

The effects of arachidonic acid and thrombin on calcium movements have been studied in fura-2-loaded platelets by a procedure which allows simultaneous monitoring of the uptake of manganese, a calcium surrogate for Ca2+ channels, and the release of Ca2+ from intracellular stores. Arachidonic acid induced both Ca2+ (Mn2+) entry through the plasma membrane and Ca2+ release from the intracellular stores. The release of Ca2+ was prevented by cyclo-oxygenase inhibitors and mimicked by the prostaglandin H2/thromboxane A2 receptor agonist U46619. Ca2+ (Mn2+) entry required higher concentrations of arachidonic acid and was not prevented by either cyclo-oxygenase or lipoxygenase inhibitors. Several polyunsaturated fatty acids reproduced the effect of arachidonic acid on Ca2+ (Mn2+) entry, but higher concentrations were required. The effects of maximal concentrations of arachidonic acid and thrombin on the uptake of Mn2+ were not additive. Both agonists induced the entry of Ca2+, Mn2+, Co2+ and Ba2+, but not Ni2+, which, in addition, blocked the entry of the other divalent cations. However, arachidonic acid, but not thrombin, increased a Ni2(+)-sensitive permeability to Mg2+. The effect of thrombin but not that of arachidonic acid was prevented either by pretreatment with phorbol ester or by an increase in cyclic-AMP levels. Arachidonic acid also accelerated the uptake of Mn2+ by human neutrophils, rat thymocytes and Ehrlich ascites-tumour cells.

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Selected References

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  1. Alonso M. T., Sanchez A., García-Sancho J. Monitoring of the activation of receptor-operated calcium channels in human platelets. Biochem Biophys Res Commun. 1989 Jul 14;162(1):24–29. doi: 10.1016/0006-291x(89)91956-6. [DOI] [PubMed] [Google Scholar]
  2. Arslan P., Di Virgilio F., Beltrame M., Tsien R. Y., Pozzan T. Cytosolic Ca2+ homeostasis in Ehrlich and Yoshida carcinomas. A new, membrane-permeant chelator of heavy metals reveals that these ascites tumor cell lines have normal cytosolic free Ca2+. J Biol Chem. 1985 Mar 10;260(5):2719–2727. [PubMed] [Google Scholar]
  3. Baran D. T., Peck W. A., Frengley P. A., Lichtman M. A. Cortisol-induced inhibition of amino acid transport in thymic lymphocytes: kinetic parameters; relation to ATP levels and protein synthesis; and specificity. Biochim Biophys Acta. 1973 May 25;307(3):627–639. doi: 10.1016/0005-2736(73)90307-6. [DOI] [PubMed] [Google Scholar]
  4. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  5. Crouch M. F., Lapetina E. G. No direct correlation between Ca2+ mobilization and dissociation of Gi during platelet phospholipase A2 activation. Biochem Biophys Res Commun. 1988 May 31;153(1):21–30. doi: 10.1016/s0006-291x(88)81184-7. [DOI] [PubMed] [Google Scholar]
  6. DeRiemer S. A., Strong J. A., Albert K. A., Greengard P., Kaczmarek L. K. Enhancement of calcium current in Aplysia neurones by phorbol ester and protein kinase C. Nature. 1985 Jan 24;313(6000):313–316. doi: 10.1038/313313a0. [DOI] [PubMed] [Google Scholar]
  7. Eisenberg M., Hall J. E., Mead C. A. The nature of the voltage-dependent conductance induced by alamethicin in black lipid membranes. J Membr Biol. 1973 Dec 31;14(2):143–176. doi: 10.1007/BF01868075. [DOI] [PubMed] [Google Scholar]
  8. Fischer T. H., Griffin A. M., Barton D. W., White G. C., 2nd Kinetic evidence that arachidonate-induced calcium efflux from platelet microsomes involves a carrier-type ionophoric mechanism. Biochim Biophys Acta. 1990 Feb 28;1022(2):215–228. doi: 10.1016/0005-2736(90)90117-7. [DOI] [PubMed] [Google Scholar]
  9. Garcia-Sancho J., Alonso M. T., Sanchez A. Receptor-operated calcium channels in human platelets. Biochem Soc Trans. 1989 Dec;17(6):980–982. doi: 10.1042/bst0170980. [DOI] [PubMed] [Google Scholar]
  10. Goligorsky M. S., Menton D. N., Laszlo A., Lum H. Nature of thrombin-induced sustained increase in cytosolic calcium concentration in cultured endothelial cells. J Biol Chem. 1989 Oct 5;264(28):16771–16775. [PubMed] [Google Scholar]
  11. Grinstein S., Rothstein A. Mechanisms of regulation of the Na+/H+ exchanger. J Membr Biol. 1986;90(1):1–12. doi: 10.1007/BF01869680. [DOI] [PubMed] [Google Scholar]
  12. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  13. Hallam T. J., Rink T. J. Agonists stimulate divalent cation channels in the plasma membrane of human platelets. FEBS Lett. 1985 Jul 8;186(2):175–179. doi: 10.1016/0014-5793(85)80703-1. [DOI] [PubMed] [Google Scholar]
  14. Hashimoto Y., Naito C., Kume S., Kato H., Watanabe T., Kawamura M., Teramoto T., Oka H. High concentrations of arachidonic acid induce platelet aggregation and serotonin release independent of prostaglandin endoperoxides and thromboxane A2. Biochim Biophys Acta. 1985 Sep 6;841(3):283–291. doi: 10.1016/0304-4165(85)90070-4. [DOI] [PubMed] [Google Scholar]
  15. Hosey M. M., Lazdunski M. Calcium channels: molecular pharmacology, structure and regulation. J Membr Biol. 1988 Sep;104(2):81–105. doi: 10.1007/BF01870922. [DOI] [PubMed] [Google Scholar]
  16. Inui Y., Christensen H. N. Discrimination of single transport systems. The Na plus-sensitive transport of neutral amino acids in the Ehrlich cell. J Gen Physiol. 1966 Sep;50(1):203–224. doi: 10.1085/jgp.50.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kowalska M. A., Rao A. K., Disa J. High concentrations of exogenous arachidonate inhibit calcium mobilization in platelets by stimulation of adenylate cyclase. Biochem J. 1988 Jul 1;253(1):255–262. doi: 10.1042/bj2530255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Krueger B. K. Toward an understanding of structure and function of ion channels. FASEB J. 1989 Jun;3(8):1906–1914. doi: 10.1096/fasebj.3.8.2470631. [DOI] [PubMed] [Google Scholar]
  19. Kurachi Y., Ito H., Sugimoto T., Shimizu T., Miki I., Ui M. Arachidonic acid metabolites as intracellular modulators of the G protein-gated cardiac K+ channel. Nature. 1989 Feb 9;337(6207):555–557. doi: 10.1038/337555a0. [DOI] [PubMed] [Google Scholar]
  20. MacIntyre D. E., McNicol A., Drummond A. H. Tumour-promoting phorbol esters inhibit agonist-induced phosphatidate formation and Ca2+ flux in human platelets. FEBS Lett. 1985 Jan 28;180(2):160–164. doi: 10.1016/0014-5793(85)81063-2. [DOI] [PubMed] [Google Scholar]
  21. Maclouf J., Levy-Toledano S., Savariau E., Hardisty R., Caen J. P. Arachidonic acid-induced human platelet aggregation independent of cyclooxygenase and lipoxygenase. Prostaglandins. 1984 Sep;28(3):383–398. doi: 10.1016/0090-6980(84)90024-8. [DOI] [PubMed] [Google Scholar]
  22. Merritt J. E., Hallam T. J. Platelets and parotid acinar cells have different mechanisms for agonist-stimulated divalent cation entry. J Biol Chem. 1988 May 5;263(13):6161–6164. [PubMed] [Google Scholar]
  23. Mollinedo F., Schneider D. L. Subcellular localization of cytochrome b and ubiquinone in a tertiary granule of resting human neutrophils and evidence for a proton pump ATPase. J Biol Chem. 1984 Jun 10;259(11):7143–7150. [PubMed] [Google Scholar]
  24. Nishikawa M., Hidaka H., Shirakawa S. Possible involvement of direct stimulation of protein kinase C by unsaturated fatty acids in platelet activation. Biochem Pharmacol. 1988 Aug 15;37(16):3079–3089. doi: 10.1016/0006-2952(88)90304-8. [DOI] [PubMed] [Google Scholar]
  25. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature. 1988 Aug 25;334(6184):661–665. doi: 10.1038/334661a0. [DOI] [PubMed] [Google Scholar]
  26. Piomelli D., Volterra A., Dale N., Siegelbaum S. A., Kandel E. R., Schwartz J. H., Belardetti F. Lipoxygenase metabolites of arachidonic acid as second messengers for presynaptic inhibition of Aplysia sensory cells. Nature. 1987 Jul 2;328(6125):38–43. doi: 10.1038/328038a0. [DOI] [PubMed] [Google Scholar]
  27. Putney J. W., Jr, Takemura H., Hughes A. R., Horstman D. A., Thastrup O. How do inositol phosphates regulate calcium signaling? FASEB J. 1989 Jun;3(8):1899–1905. doi: 10.1096/fasebj.3.8.2542110. [DOI] [PubMed] [Google Scholar]
  28. Rink T. J. A real receptor-operated calcium channel? Nature. 1988 Aug 25;334(6184):649–650. doi: 10.1038/334649a0. [DOI] [PubMed] [Google Scholar]
  29. Rink T. J., Sanchez A. Effects of prostaglandin I2 and forskolin on the secretion from platelets evoked at basal concentrations of cytoplasmic free calcium by thrombin, collagen, phorbol ester and exogenous diacylglycerol. Biochem J. 1984 Sep 15;222(3):833–836. doi: 10.1042/bj2220833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rink T. J., Tsien R. Y., Pozzan T. Cytoplasmic pH and free Mg2+ in lymphocytes. J Cell Biol. 1982 Oct;95(1):189–196. doi: 10.1083/jcb.95.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rittenhouse S. E., Sasson J. P. Mass changes in myoinositol trisphosphate in human platelets stimulated by thrombin. Inhibitory effects of phorbol ester. J Biol Chem. 1985 Jul 25;260(15):8657–8660. [PubMed] [Google Scholar]
  32. Sage S. O., Merritt J. E., Hallam T. J., Rink T. J. Receptor-mediated calcium entry in fura-2-loaded human platelets stimulated with ADP and thrombin. Dual-wavelengths studies with Mn2+. Biochem J. 1989 Mar 15;258(3):923–926. doi: 10.1042/bj2580923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sanchez A., Alonso M. T., Collazos J. M. Thrombin-induced changes of intracellular [Ca2+] and pH in human platelets. Cytoplasmic alkalinization is not a prerequisite for calcium mobilization. Biochim Biophys Acta. 1988 Mar 3;938(3):497–500. doi: 10.1016/0005-2736(88)90149-6. [DOI] [PubMed] [Google Scholar]
  34. Sanchez A. Ca2+-independent secretion is dependent on cytoplasmic ATP in human platelets. FEBS Lett. 1985 Oct 28;191(2):283–286. doi: 10.1016/0014-5793(85)80025-9. [DOI] [PubMed] [Google Scholar]
  35. Sekiya K., Okuda H. Selective inhibition of platelet lipoxygenase by baicalein. Biochem Biophys Res Commun. 1982 Apr 14;105(3):1090–1095. doi: 10.1016/0006-291x(82)91081-6. [DOI] [PubMed] [Google Scholar]
  36. Siegel M. I., McConnell R. T., Abrahams S. L., Porter N. A., Cuatrecasas P. Regulation of arachidonate metabolism via lipoxygenase and cyclo-oxygenase by 12-HPETE, the product of human platelet lipoxygenase. Biochem Biophys Res Commun. 1979 Aug 28;89(4):1273–1280. doi: 10.1016/0006-291x(79)92146-6. [DOI] [PubMed] [Google Scholar]
  37. Siegl A. M., Daly J. W., Smith J. B. Inhibition of aggregation and stimulation of cyclic AMP generation in intact human platelets by the diterpene forskolin. Mol Pharmacol. 1982 May;21(3):680–687. [PubMed] [Google Scholar]
  38. Siess W. Molecular mechanisms of platelet activation. Physiol Rev. 1989 Jan;69(1):58–178. doi: 10.1152/physrev.1989.69.1.58. [DOI] [PubMed] [Google Scholar]
  39. Tapley P. M., Murray A. W. Platelet Ca2+-activated, phospholipid-dependent protein kinase: evidence for proteolytic activation of the enzyme in cells treated with phospholipase C1. Biochem Biophys Res Commun. 1984 Feb 14;118(3):835–841. doi: 10.1016/0006-291x(84)91470-0. [DOI] [PubMed] [Google Scholar]
  40. Thomas J. A., Buchsbaum R. N., Zimniak A., Racker E. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry. 1979 May 29;18(11):2210–2218. doi: 10.1021/bi00578a012. [DOI] [PubMed] [Google Scholar]
  41. Thomas R. C. Experimental displacement of intracellular pH and the mechanism of its subsequent recovery. J Physiol. 1984 Sep;354:3P–22P. doi: 10.1113/jphysiol.1984.sp015397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tohmatsu T., Nakashima S., Nozawa Y. Evidence of Ca2+ mobilizing action of arachidonic acid in human platelets. Biochim Biophys Acta. 1989 Jun 15;1012(1):97–102. doi: 10.1016/0167-4889(89)90016-5. [DOI] [PubMed] [Google Scholar]
  43. Tsukuda M., Asaoka Y., Sekiguchi K., Kikkawa U., Nishizuka Y. Properties of protein kinase C subspecies in human platelets. Biochem Biophys Res Commun. 1988 Sep 30;155(3):1387–1395. doi: 10.1016/s0006-291x(88)81295-6. [DOI] [PubMed] [Google Scholar]
  44. Zavoico G. B., Cragoe E. J., Jr, Feinstein M. B. Regulation of intracellular pH in human platelets. Effects of thrombin, A23187, and ionomycin and evidence for activation of Na+/H+ exchange and its inhibition by amiloride analogs. J Biol Chem. 1986 Oct 5;261(28):13160–13167. [PubMed] [Google Scholar]
  45. Zavoico G. B., Halenda S. P., Sha'afi R. I., Feinstein M. B. Phorbol myristate acetate inhibits thrombin-stimulated Ca2+ mobilization and phosphatidylinositol 4,5-bisphosphate hydrolysis in human platelets. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3859–3862. doi: 10.1073/pnas.82.11.3859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zschauer A., van Breemen C., Bühler F. R., Nelson M. T. Calcium channels in thrombin-activated human platelet membrane. Nature. 1988 Aug 25;334(6184):703–705. doi: 10.1038/334703a0. [DOI] [PubMed] [Google Scholar]