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. 1995 Feb 1;305(Pt 3):859–864. doi: 10.1042/bj3050859

Arachidonic acid is functioning as a second messenger in activating the Ca2+ entry process on H1-histaminoceptor stimulation in DDT1 MF-2 cells.

L van der Zee 1, A Nelemans 1, A den Hertog 1
PMCID: PMC1136338  PMID: 7848286

Abstract

This study was carried out to identify the cellular component activating the histamine-stimulated Ca2+ entry in vas-deferens-derived DDT1 MF-2 cells. H1-histaminoceptor stimulation resulted in a rise in intracellular Ca2+ concentration, caused by Ca2+ release from inositol phosphate-sensitive Ca2+ stores and Ca2+ entry from the extracellular space, accompanied by a transient Ca(2+)-activated outward K+ current. The histamine-evoked K+ current was still observed after preventing inositol phosphate-induced Ca2+ mobilization by intracellularly applied heparin. This current was activated by Ca2+ entry from the extracellular space, because it was abolished in the presence of the Ca(2+)-channel blocker La3+ or under Ca(2+)-free conditions. H1-histaminoceptor-activated Ca2+ entry was also observed in the presence of intracellularly applied Ins(1,4,5)P3 and Ins(1,3,4,5)P4, depleting their respective Ca2+ stores and pre-activating the inositol phosphate-regulated Ca2+ entry. Thus the ability of histamine to activate Ca2+ entry independently of Ca2+ mobilization and the formation of inositol phosphates suggests that another component is involved to initiate the Ca(2+)-entry process. It was observed that H1-histaminoceptor stimulation resulted in a pronounced release of arachidonic acid (AA) in DDT1 MF-2 cells. Exogenously applied AA induced a concentration-dependent increase in internal Ca2+ due to activation of Ca2+ entry from the extracellular space. Slow inactivation of the AA-sensitive Ca2+ channels is suggested by the slow decline in Ca2+ entry. In accord, the histamine-induced Ca2+ entry was not observed with AA-pre-activated Ca2+ channels. Inhibition of the lipoxygenase and cyclo-oxygenase pathway did not affect the AA-induced Ca2+ and the concomitant K+ current were decreased in the presence of AA and caused by Ca2+ mobilization from internal stores. Blocking this internal Ca2+ release by heparin, in the presence of AA, resulted in abolition of the histamine-induced Ca(2+)-regulated K+ current. These observations show that AA, released on H1-histaminoceptor stimulation in DDT1 MF-2 cells, is functioning as a second messenger to activate plasma-membrane Ca2+ channels promoting Ca2+ entry from the extracellular space.

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Selected References

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  1. Axelrod J. Receptor-mediated activation of phospholipase A2 and arachidonic acid release in signal transduction. Biochem Soc Trans. 1990 Aug;18(4):503–507. doi: 10.1042/bst0180503. [DOI] [PubMed] [Google Scholar]
  2. Benham C. D., Tsien R. W. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature. 1987 Jul 16;328(6127):275–278. doi: 10.1038/328275a0. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  4. Bonventre J. V. Phospholipase A2 and signal transduction. J Am Soc Nephrol. 1992 Aug;3(2):128–150. doi: 10.1681/ASN.V32128. [DOI] [PubMed] [Google Scholar]
  5. Brown A. M., Birnbaumer L. Ionic channels and their regulation by G protein subunits. Annu Rev Physiol. 1990;52:197–213. doi: 10.1146/annurev.ph.52.030190.001213. [DOI] [PubMed] [Google Scholar]
  6. Cullen P. J., Irvine R. F., Dawson A. P. Synergistic control of Ca2+ mobilization in permeabilized mouse L1210 lymphoma cells by inositol 2,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate. Biochem J. 1990 Oct 15;271(2):549–553. doi: 10.1042/bj2710549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Den Hertog A., Hoiting B., Molleman A., Van den Akker J., Duin M., Nelemans A. Calcium release from separate receptor-specific intracellular stores induced by histamine and ATP in a hamster cell line. J Physiol. 1992 Aug;454:591–607. doi: 10.1113/jphysiol.1992.sp019281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ely J. A., Hunyady L., Baukal A. J., Catt K. J. Inositol 1,3,4,5-tetrakisphosphate stimulates calcium release from bovine adrenal microsomes by a mechanism independent of the inositol 1,4,5-trisphosphate receptor. Biochem J. 1990 Jun 1;268(2):333–338. doi: 10.1042/bj2680333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Engels F., Willems H., Nijkamp F. P. Cyclooxygenase-catalyzed formation of 9-hydroxylinoleic acid by guinea pig alveolar macrophages under non-stimulated conditions. FEBS Lett. 1986 Dec 15;209(2):249–253. doi: 10.1016/0014-5793(86)81121-8. [DOI] [PubMed] [Google Scholar]
  10. Ferguson J. E., Han J. K., Kao J. P., Nuccitelli R. The effects of inositol trisphosphates and inositol tetrakisphosphate on Ca2+ release and Cl- current pattern in the Xenopus laevis oocyte. Exp Cell Res. 1991 Feb;192(2):352–365. doi: 10.1016/0014-4827(91)90052-v. [DOI] [PubMed] [Google Scholar]
  11. Graier W. F., Schmidt K., Kukovetz W. R. Bradykinin-induced Ca(2+)-influx into cultured aortic endothelial cells is not regulated by inositol 1,4,5-trisphosphate or inositol 1,3,4,5-tetrakisphosphate. Second Messengers Phosphoproteins. 1991;13(4):187–197. [PubMed] [Google Scholar]
  12. Graier W. F., Schmidt K., Kukovetz W. R. Is the bradykinin-induced Ca2+ influx and the formation of endothelium-derived relaxing factor mediated by a G protein? Eur J Pharmacol. 1992 Jan 14;225(1):43–49. doi: 10.1016/0922-4106(92)90037-v. [DOI] [PubMed] [Google Scholar]
  13. Hallam T. J., Rink T. J. Receptor-mediated Ca2+ entry: diversity of function and mechanism. Trends Pharmacol Sci. 1989 Jan;10(1):8–10. doi: 10.1016/0165-6147(89)90092-8. [DOI] [PubMed] [Google Scholar]
  14. Hazen S. L., Zupan L. A., Weiss R. H., Getman D. P., Gross R. W. Suicide inhibition of canine myocardial cytosolic calcium-independent phospholipase A2. Mechanism-based discrimination between calcium-dependent and -independent phospholipases A2. J Biol Chem. 1991 Apr 15;266(11):7227–7232. [PubMed] [Google Scholar]
  15. Henzi V., MacDermott A. B. Characteristics and function of Ca(2+)- and inositol 1,4,5-trisphosphate-releasable stores of Ca2+ in neurons. Neuroscience. 1992;46(2):251–273. doi: 10.1016/0306-4522(92)90049-8. [DOI] [PubMed] [Google Scholar]
  16. Hertelendy F., Molnár M., Jamaluddin M. Dual action of arachidonic acid on calcium mobilization in avian granulosa cells. Mol Cell Endocrinol. 1992 Feb;83(2-3):173–181. doi: 10.1016/0303-7207(92)90157-2. [DOI] [PubMed] [Google Scholar]
  17. Hesketh T. R., Smith G. A., Moore J. P., Taylor M. V., Metcalfe J. C. Free cytoplasmic calcium concentration and the mitogenic stimulation of lymphocytes. J Biol Chem. 1983 Apr 25;258(8):4876–4882. [PubMed] [Google Scholar]
  18. Hoiting B., Molleman A., Duin M., den Hertog A., Nelemans A. P2 purinoceptor-mediated inositol phosphate formation in relation to cytoplasmic calcium in DDT1 MF-2 smooth muscle cells. Eur J Pharmacol. 1990 Jul 31;189(1):31–39. doi: 10.1016/0922-4106(90)90227-o. [DOI] [PubMed] [Google Scholar]
  19. Irvine R. F. Inositol phosphates and Ca2+ entry: toward a proliferation or a simplification? FASEB J. 1992 Sep;6(12):3085–3091. doi: 10.1096/fasebj.6.12.1325932. [DOI] [PubMed] [Google Scholar]
  20. Irvine R. F., Moor R. M. Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986 Dec 15;240(3):917–920. doi: 10.1042/bj2400917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jacob R. Agonist-stimulated divalent cation entry into single cultured human umbilical vein endothelial cells. J Physiol. 1990 Feb;421:55–77. doi: 10.1113/jphysiol.1990.sp017933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Keyser D. O., Alger B. E. Arachidonic acid modulates hippocampal calcium current via protein kinase C and oxygen radicals. Neuron. 1990 Oct;5(4):545–553. doi: 10.1016/0896-6273(90)90092-t. [DOI] [PubMed] [Google Scholar]
  23. Lückhoff A., Clapham D. E. Inositol 1,3,4,5-tetrakisphosphate activates an endothelial Ca(2+)-permeable channel. Nature. 1992 Jan 23;355(6358):356–358. doi: 10.1038/355356a0. [DOI] [PubMed] [Google Scholar]
  24. Merritt J. E., Rink T. J. Regulation of cytosolic free calcium in fura-2-loaded rat parotid acinar cells. J Biol Chem. 1987 Dec 25;262(36):17362–17369. [PubMed] [Google Scholar]
  25. Molleman A., Hoiting B., Duin M., van den Akker J., Nelemans A., Den Hertog A. Potassium channels regulated by inositol 1,3,4,5-tetrakisphosphate and internal calcium in DDT1 MF-2 smooth muscle cells. J Biol Chem. 1991 Mar 25;266(9):5658–5663. [PubMed] [Google Scholar]
  26. Molleman A., Nelemans A., Den Hertog A. P2-purinoceptor-mediated membrane currents in DDT1 MF-2 smooth muscle cells. Eur J Pharmacol. 1989 Oct 4;169(1):167–174. doi: 10.1016/0014-2999(89)90829-7. [DOI] [PubMed] [Google Scholar]
  27. Molleman A., Nelemans A., van den Akker J., Duin M., den Hertog A. Voltage-dependent sodium and potassium, but no calcium conductances in DDT1 MF-2 smooth muscle cells. Pflugers Arch. 1991 Jan;417(5):479–484. doi: 10.1007/BF00370943. [DOI] [PubMed] [Google Scholar]
  28. Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
  29. Needleman P., Turk J., Jakschik B. A., Morrison A. R., Lefkowith J. B. Arachidonic acid metabolism. Annu Rev Biochem. 1986;55:69–102. doi: 10.1146/annurev.bi.55.070186.000441. [DOI] [PubMed] [Google Scholar]
  30. Putney J. W., Jr Capacitative calcium entry revisited. Cell Calcium. 1990 Nov-Dec;11(10):611–624. doi: 10.1016/0143-4160(90)90016-n. [DOI] [PubMed] [Google Scholar]
  31. Ramanadham S., Gross R., Turk J. Arachidonic acid induces an increase in the cytosolic calcium concentration in single pancreatic islet beta cells. Biochem Biophys Res Commun. 1992 Apr 30;184(2):647–653. doi: 10.1016/0006-291x(92)90638-2. [DOI] [PubMed] [Google Scholar]
  32. Shimada T., Somlyo A. P. Modulation of voltage-dependent Ca channel current by arachidonic acid and other long-chain fatty acids in rabbit intestinal smooth muscle. J Gen Physiol. 1992 Jul;100(1):27–44. doi: 10.1085/jgp.100.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Soliven B., Takeda M., Shandy T., Nelson D. J. Arachidonic acid and its metabolites increase Cai in cultured rat oligodendrocytes. Am J Physiol. 1993 Mar;264(3 Pt 1):C632–C640. doi: 10.1152/ajpcell.1993.264.3.C632. [DOI] [PubMed] [Google Scholar]
  34. Vacher P., McKenzie J., Dufy B. Arachidonic acid affects membrane ionic conductances of GH3 pituitary cells. Am J Physiol. 1989 Aug;257(2 Pt 1):E203–E211. doi: 10.1152/ajpendo.1989.257.2.E203. [DOI] [PubMed] [Google Scholar]
  35. Vindlacheruvu R. R., Rink T. J., Sage S. O. Lack of evidence for a role for the lipoxygenase pathway in increases in cytosolic calcium evoked by ADP and arachidonic acid in human platelets. FEBS Lett. 1991 Nov 4;292(1-2):196–200. doi: 10.1016/0014-5793(91)80866-2. [DOI] [PubMed] [Google Scholar]
  36. Wolf R. A., Gross R. W. Identification of neutral active phospholipase C which hydrolyzes choline glycerophospholipids and plasmalogen selective phospholipase A2 in canine myocardium. J Biol Chem. 1985 Jun 25;260(12):7295–7303. [PubMed] [Google Scholar]
  37. von Tscharner V., Prod'hom B., Baggiolini M., Reuter H. Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration. 1986 Nov 27-Dec 3Nature. 324(6095):369–372. doi: 10.1038/324369a0. [DOI] [PubMed] [Google Scholar]

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