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. 1990 Feb 15;266(1):157–163. doi: 10.1042/bj2660157

Relationship between arachidonate generation and exocytosis in permeabilized mast cells.

Y Churcher 1, D Allan 1, B D Gomperts 1
PMCID: PMC1131109  PMID: 2138015

Abstract

Using rat mast cells permeabilized with streptolysin O we show that release of arachidonate generally occurs under similar but not identical conditions to those that cause exocytosis of beta-N-acetylglucosaminidase (hexosaminidase). Thus, hexosaminidase secretion and arachidonate release both require provision of Ca2+ together with a guanine nucleotide but exocytosis occurs at lower concentrations of both effectors. The kinetics of both processes are similar, with a delay in onset only when ATP is present. Arachidonate release occurs largely from a pool of arachidonyl phosphatidylcholine which appears to represent less than 1% of the total phosphatidylcholine of the cells. Despite the general similarity of the conditions causing exocytosis and arachidonate release, our results show that under some circumstances it is possible to obtain exocytosis without measurable release of arachidonate and that therefore phospholipase A2 activation is not an essential precursor of secretion.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan D., Cockcroft S. A modified procedure for thin-layer chromatography of phospholipids. J Lipid Res. 1982 Dec;23(9):1373–1374. [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Burch R. M., Axelrod J. Dissociation of bradykinin-induced prostaglandin formation from phosphatidylinositol turnover in Swiss 3T3 fibroblasts: evidence for G protein regulation of phospholipase A2. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6374–6378. doi: 10.1073/pnas.84.18.6374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burch R. M., Luini A., Axelrod J. Phospholipase A2 and phospholipase C are activated by distinct GTP-binding proteins in response to alpha 1-adrenergic stimulation in FRTL5 thyroid cells. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7201–7205. doi: 10.1073/pnas.83.19.7201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chi E. Y., Henderson W. R., Klebanoff S. J. Phospholipase A2-induced rat mast cell secretion. Role of arachidonic acid metabolites. Lab Invest. 1982 Dec;47(6):579–585. [PubMed] [Google Scholar]
  6. Cockcroft S., Howell T. W., Gomperts B. D. Two G-proteins act in series to control stimulus-secretion coupling in mast cells: use of neomycin to distinguish between G-proteins controlling polyphosphoinositide phosphodiesterase and exocytosis. J Cell Biol. 1987 Dec;105(6 Pt 1):2745–2750. doi: 10.1083/jcb.105.6.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cockcroft S., Stutchfield J. G-proteins, the inositol lipid signalling pathway, and secretion. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 26;320(1199):247–265. doi: 10.1098/rstb.1988.0075. [DOI] [PubMed] [Google Scholar]
  8. Frye R. A., Holz R. W. Arachidonic acid release and catecholamine secretion from digitonin-treated chromaffin cells: effects of micromolar calcium, phorbol ester, and protein alkylating agents. J Neurochem. 1985 Jan;44(1):265–273. doi: 10.1111/j.1471-4159.1985.tb07140.x. [DOI] [PubMed] [Google Scholar]
  9. Frye R. A., Holz R. W. The relationship between arachidonic acid release and catecholamine secretion from cultured bovine adrenal chromaffin cells. J Neurochem. 1984 Jul;43(1):146–150. doi: 10.1111/j.1471-4159.1984.tb06690.x. [DOI] [PubMed] [Google Scholar]
  10. Gomperts B. D., Tatham P. E. GTP-binding proteins in the control of exocytosis. Cold Spring Harb Symp Quant Biol. 1988;53(Pt 2):983–992. doi: 10.1101/sqb.1988.053.01.113. [DOI] [PubMed] [Google Scholar]
  11. Henderson W. R., Chi E. Y., Jörg A., Klebanoff S. J. Horse eosinophil degranulation induced by the ionophore A23187. Ultrastructure and role of phospholipase A2. Am J Pathol. 1983 Jun;111(3):341–349. [PMC free article] [PubMed] [Google Scholar]
  12. Howell T. W., Cockcroft S., Gomperts B. D. Essential synergy between Ca2+ and guanine nucleotides in exocytotic secretion from permeabilized rat mast cells. J Cell Biol. 1987 Jul;105(1):191–197. doi: 10.1083/jcb.105.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Howell T. W., Gomperts B. D. Rat mast cells permeabilised with streptolysin O secrete histamine in response to Ca2+ at concentrations buffered in the micromolar range. Biochim Biophys Acta. 1987 Feb 18;927(2):177–183. doi: 10.1016/0167-4889(87)90132-7. [DOI] [PubMed] [Google Scholar]
  14. Howell T. W., Kramer I. M., Gomperts B. D. Protein phosphorylation and the dependence on Ca2+ and GTP-gamma-S for exocytosis from permeabilised mast cells. Cell Signal. 1989;1(2):157–163. doi: 10.1016/0898-6568(89)90005-3. [DOI] [PubMed] [Google Scholar]
  15. Knight D. E., Scrutton M. C. Gaining access to the cytosol: the technique and some applications of electropermeabilization. Biochem J. 1986 Mar 15;234(3):497–506. doi: 10.1042/bj2340497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lee T. H., Hoover R. L., Williams J. D., Sperling R. I., Ravalese J., 3rd, Spur B. W., Robinson D. R., Corey E. J., Lewis R. A., Austen K. F. Effect of dietary enrichment with eicosapentaenoic and docosahexaenoic acids on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N Engl J Med. 1985 May 9;312(19):1217–1224. doi: 10.1056/NEJM198505093121903. [DOI] [PubMed] [Google Scholar]
  17. Lerner M., Samuni A., Razin E. Stimulation of murine cultured mast cells under anaerobic conditions: inhibition of arachidonic acid release. Immunol Lett. 1987 Nov;16(2):121–124. doi: 10.1016/0165-2478(87)90118-0. [DOI] [PubMed] [Google Scholar]
  18. Masini E., Giannella E., Bani-Sacchi T., Fantozzi R., Palmerani B., Mannaioni P. F. Histamine release from serosal mast cells by intermediate products of arachidonic acid metabolism. Agents Actions. 1987 Apr;20(3-4):202–205. doi: 10.1007/BF02074669. [DOI] [PubMed] [Google Scholar]
  19. Peters S. P., MacGlashan D. W., Jr, Schleimer R. P., Hayes E. C., Adkinson N. F., Jr, Lichtenstein L. M. The pharmacologic modulation of the release of arachidonic acid metabolites from purified human lung mast cells. Am Rev Respir Dis. 1985 Aug;132(2):367–373. doi: 10.1164/arrd.1985.132.2.367. [DOI] [PubMed] [Google Scholar]
  20. Razin E., Marx G. Thrombin-induced degranulation of cultured bone marrow-derived mast cells. J Immunol. 1984 Dec;133(6):3282–3285. [PubMed] [Google Scholar]
  21. Schleimer R. P., MacGlashan D. W., Jr, Peters S. P., Pinckard R. N., Adkinson N. F., Jr, Lichtenstein L. M. Characterization of inflammatory mediator release from purified human lung mast cells. Am Rev Respir Dis. 1986 Apr;133(4):614–617. doi: 10.1164/arrd.1986.133.4.614. [DOI] [PubMed] [Google Scholar]
  22. Shaw R. J., Cromwell O., Kay A. B. Preferential generation of leukotriene C4 by human eosinophils. Clin Exp Immunol. 1984 Jun;56(3):716–722. [PMC free article] [PubMed] [Google Scholar]
  23. Skipski V. P., Peterson R. F., Barclay M. Quantitative analysis of phospholipids by thin-layer chromatography. Biochem J. 1964 Feb;90(2):374–378. doi: 10.1042/bj0900374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Smith J. B., Ingerman C., Kocsis J. J., Silver M. J. Formation of prostaglandins during the aggregation of human blood platelets. J Clin Invest. 1973 Apr;52(4):965–969. doi: 10.1172/JCI107262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tatham P. E., Gomperts B. D. ATP inhibits onset of exocytosis in permeabilised mast cells. Biosci Rep. 1989 Feb;9(1):99–109. doi: 10.1007/BF01117516. [DOI] [PubMed] [Google Scholar]
  26. Turk J., Wolf B. A., Lefkowith J. B., Stump W. T., McDaniel M. L. Glucose-induced phospholipid hydrolysis in isolated pancreatic islets: quantitative effects on the phospholipid content of arachidonate and other fatty acids. Biochim Biophys Acta. 1986 Dec 5;879(3):399–409. doi: 10.1016/0005-2760(86)90232-8. [DOI] [PubMed] [Google Scholar]
  27. Walsh C. E., Dechatelet L. R., Chilton F. H., Wykle R. L., Waite M. Mechanism of arachidonic acid release in human polymorphonuclear leukocytes. Biochim Biophys Acta. 1983 Jan 7;750(1):32–40. doi: 10.1016/0005-2760(83)90201-1. [DOI] [PubMed] [Google Scholar]

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