Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

An enhanced incorporation of fatty acid into phosphatidyl choline that parallels histamine discharge in mast cells

Summary

Purified rat peritoneal and pleural mast cells preincubated briefly with radioactively labeled fatty acid were treated with A23187, which bypasses primary receptors in stimulating exocytosis. An enhanced incorporation of fatty acid into phosphatidyl choline (PC) that occurred in parallel with histamine release at 24–25°C was observed and was initially proportional to the total amount of histamine discharged. Enhanced PC labeling and histamine secretion were also proportional at temperatures ranging from 17–37°C. Both radioactive linoleic and palmitic acids were incorporated selectively at the β-position of the glycerol backbone of PC. PC labeling by [3H]choline was not detectably different in control and stimulated cells, and phosphatidic acid did not exhibit selectively enhanced β-acylation. Thus, the stimulated labeling in A23187-treated cells may occur secondary to the action of a phospholipase A2 that favors PC as a substrate.

Other peritoneal cell types exhibit a very similar A23187-stimulated selective labeling of PC. Therefore, autoradiography has been used to provide a direct demonstration that in purified preparations, mast cells are the principal cell type engaged in A23187-elicited incorporation of fatty acid into PC. The efficacy of this approach has relied on special procedures devised to obtain significantly different autoradiographic grain densities between control and stimulated preparations that can be attributed to differences in the level of [3H]palmitate-labeled PC.

Preliminary tests using compound 48/80 as a secretory stimulus for mast cells have identified a similar selectively enhanced PC labeling. In either case, however, consideration of possible relationships between PC metabolism and the secretory process are premature since they have not been tested directly.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Akesson, B. 1970. Initial esterification and conversion of intraportally injected (1-14C) linoleic acid in rat liver.Biochim. Biophys. Acta 218:57–70

  2. 2.

    Akesson, B., Elovson, J., Arvidson, G. 1970. Initial incorporation into rat liver glycerolipids of intraportally injected (9, 10-3H)palmitic acid.Biochim. Biophys. Acta 218:44–56

  3. 3.

    Apitz-Castro, R.J., Mas, M.A., Cruz, M.R., Jain, M.K. 1979. Isolation of homogenous phospholipase A2 from human platelets.Biochem. Biophys. Res. Commun. 91:63–71

  4. 4.

    Bell, R.L., Majerus, P.W. 1980. Thrombin-induced hydrolysis of phosphatidyl inositol in human platelets.J. Biol. Chem. 255:1790–1792

  5. 5.

    Billah, M.M., Lapetina, E.G. 1982. Rapid decrease of phosphatidyl inositol 4, 5-bisphosphate in thrombin-stimulated platelets.J. Biol. Chem. 257:12705–12708

  6. 6.

    Billah, M.M., Lapetina, E., Cuatrecasas, P. 1981. Phospholipase A2 activity specific for phosphatidic acid.J. Biol. Chem. 256:5399–5403

  7. 7.

    Bligh, E.G., Dyer, W.J. 1959. A rapid method of total lipid extraction and purification.Can. J. Biochem. 37:911–917

  8. 8.

    Brandt, A.E., Lands, W.E.M. 1967. The effect of acyl-group composition on the rate of acyltransferase-catalyzed synthesis of lecithin.Biochim. Biophys. Acta 144:605–612

  9. 9.

    Caro, L.G., Van Tubergen, R.P. 1962. High resolution autoradiography. I. Methods.J. Cell Biol. 15:173–188

  10. 10.

    Castagna, M., Takai, Y., Kaibuchi, K., Sano, K., Kikkawa, V., Nishizuka, Y. 1982. Direct activation of calcium-activated phospholipid-dependent protein kinase by tumor-promoting phorbol esters.J. Biol. Chem. 257:7847–7851

  11. 11.

    Castle, A.M., Castle, J.D. 1981. The purification and partial characterization of phospholipase A2—a secretory protein of rabbit parotid gland.Biochim. Biophys. Acta 666:259–274

  12. 12.

    Cochrane, D.E., Douglas, W.W. 1974. Calcium-induced extrusion of secretory granules (exocytosis) in mast cells exposed to 48/80 or the ionophore A23187 and X537A.Proc Natl. Acad. Sci. USA 71:408–412

  13. 13.

    Cockroft, S., Gomperts, B.D. 1979. Evidence for a role of phosphatidyl inositol turnover in stimulus-secretion coupling.Biochem. J. 178:681–687

  14. 14.

    Crews, F.T., Morita, Y., McGiyney, A., Hirata, F., Siraganian, R.P., Axelrod, J. 1981. Ig-E-Mediated histamine release in rat basophilic leukemia cells: Receptor activation, phospholipid methylation, Ca2+ flux, and release of arachidonic acid.Arch. Biochem. Biophys. 212:561–571

  15. 15.

    DeHaas, G.H., Postema, N.M., Nieuwenhuizen, W., Deenen, L.L.M. van 1968. Purification and properties of phospholipase A from porcine pancreas.Biochim. Biophys. Acta 159:103–117

  16. 16.

    Deutsch, J.W., Kelly, R.B. 1981. Lipids of synaptic vesicles: Relevance to the mechanism of membrane fusion.Biochemistry 20:378–385

  17. 17.

    Ferber, E., Resch, K. 1973. Phospholipid metabolism of stimulated lymphocytes: Activation of acyl coA: Lysolecithin acyltransferases in microsomal membranes.Biochim. Biophys. Acta 296:355

  18. 18.

    Fisher, K.A. 1976. Analysis of membrane halves: Cholesterol.Proc. Natl. Acad. Sci. USA 73:173–177

  19. 19.

    Foreman, J.D., Monger, J.L., Gomperts, B.D. 1973. Calcium ionophores and movement of calcium ions following the physiological stimulus to a secretory process.Nature (London) 245:249–251

  20. 20.

    Franson, R., Waite, M. 1978. Relation between calcium requirement, substrate charge, and rabbit polymorphonuclear leukocyte phospholipase A2 activity.Biochemistry 17:4029–4033

  21. 21.

    Frei, E., Zahler, D. 1979. Phospholipase A2 from sheep erythrocyte membranes: Ca2+ dependence and localization.Biochim. Biophys. Acta 550:450–463

  22. 22.

    Groot, P.H.E., Scholte, H.R., Hulsmann, W.C. 1975. Fatty acid activation: Specificity, localization and function.In: Advance in Lipid Research. R. Paolette and D. Kutcheoski, editors. Vol. 14, pp. 75–126. Academic, New York

  23. 23.

    Helander, H.F., Bloom, G.D. 1974. Quantitative analysis of mast cell structure.J. Microsc. 100:315–321

  24. 24.

    Hirata, F., Axelrod, J., Crews, F.T. 1979. Concanavalin A stimulates phospholipid methylation and phosphatidylserine decarboxylation in rat mast cells.Proc. Natl. Acad. Sci. USA,76:4813–4816

  25. 25.

    Hirata, F., Corcoran, B.A., Vankatasubramanian, K., Schiffmann, E., Axelrod, J. 1979. Chemoattractants stimulate degradation of methylated phospholipids and release of arachidonic acid in rabbit leukocytes.Proc. Natl. Acad. Sci. USA 76:2640–2643

  26. 26.

    Hirata, F., Toyoshima, S., Axelrod, J., Waxdal, M.J. 1980. Phospholipid methylation: A biochemical signal modulating lymphocyte mitogenesis.Proc. Natl. Acad. Sci. USA 77:862–865

  27. 27.

    Ho, P.C., Orange, R.P. 1978. Indirect evidence of phospholipase A activation in purified mast cells during reverse anaphylactic challenge.Fed. Proc. 37:1667

  28. 28.

    Hokin, L.E. 1968. Dynamic aspects of phospholipids during protein secretion.Int. Rev. Cytol. 23:187–208

  29. 29.

    Ishizaka, T., Hirata, F., Ishizaka, K., Axelrod, J. 1980. Stimulation of phospholipid methylation. Ca2+ influx. and histamine release by bridging IgE receptors on rat mast cells.Proc. Natl. Acad. Sci. USA 77:1903–1906

  30. 30.

    Kalina, M., Pease, D.C. 1977. The preservation of ultrastructure in saturated phosphatidyl cholines by tannic acid model systems and Type II pneumocytes.J. Cell Biol. 74:726–741

  31. 31.

    Kennerly, D.A., Sullivan, T.J., Parker, C.W. 1979. Activation of phospholipid metabolism during mediator release from stimulated rat mast cells.J. Immunol. 122:152–159

  32. 32.

    Kennerly, D.A., Sullivan, T.J., Sylwester, P., Parker, C.W. 1979. Diacylglycerol metabolism in mast cells: A potential role in membrane fusion and arachidonic acid release.J. Exp. Med. 150:1039–1044

  33. 33.

    Lagunoff, D., Wan, H. 1974. Temperature dependence of mast cell histamine secretion.J. Cell. Biol. 61:809–811

  34. 34.

    Lewis, R.A., Austen, K.F. 1981. Mediation of local homeostasis and inflammation by leukotrienes and other mast cell dependent compounds.Nature (London) 293:103–108

  35. 35.

    Lewis, R.A., Soter, N.A., Diamond, P.T., Austen, K.F., Oates, J.A., Roberts, L.J. 1982. Prostaglandin D2 generation after activation of rat and human mast cells with antiIgE.J. Immunol. 129:1627–1631

  36. 36.

    Luft, J.H. 1961. Improvements in epoxy resin embedding methods.J. Biochem. Biophys. Cytol. 9:409–414

  37. 37.

    Martin, T.W., Lagunoff, D. 1982. Rat mast cell phospholipase A2: activity toward exogenous phosphatidyl serine and inhibition by N-(7-nitro-2, 1, 3-benzoxadiaxol-4-yl) phosphatidyl serine.Biochemistry 21:1254–1260

  38. 38.

    McGivney, A., Crews, F.T., Hirata, F., Axelrod, J., Siraganian, R.P. 1981. Rat basophilic leukemia cell lines defective in phospholipid methyltransferase enzymes, Ca2+ influx, and histamine release: Reconstitution by hybridization.Proc. Natl. Acad. Sci. USA 78:6176–6180

  39. 39.

    McGivney, A., Morita, Y., Crews, F.T., Hirata, F., Axelrod, J., Siraganian, R.P. 1981. Phospholipase activation in the IgE-mediated and Ca2+ ionophore A23187-induced release of histamine from rat basophilic leukemia cells.Arch. Biochem. Biophys. 212:572–580

  40. 40.

    Michell, R.H. 1975. Inositol phospholipids and cell surface receptor function.Biochim. Biophys. Acta 425:81–147

  41. 41.

    Morrison, D.C., Roser, J.F., Henson, P.M., Cochrane, C.G. 1974. Activation of rat mast cells by low molecular weight stimuli.J. Immunol. 112:573–582

  42. 42.

    Palade, G.E. 1975. Intracellular aspects of the process of protein synthesis.Science 189:347–358

  43. 43.

    Pfenninger, K.H., Johnson, M.P. 1981. Nerve growth factor stimulates phospholipid methylation in growing neurites.Proc. Natl. Acad. Sci. USA 78:7797–7800

  44. 44.

    Richardson, K.C., Jarett, J., Finke, E.H. 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy.Stain Technol. 35:313–323

  45. 45.

    Rittenhouse-Simmons, S. 1979. Production of diglyceride from phosphatidyl inositol in activated human platelets.J. Clin. Invest. 63:580–587

  46. 46.

    Roberts, L.J., Lewis, R.A., Oates, J.A., Austen, K.F. 1979. Prostaglandin, thromboxane and 12-hydroxy-5,8,10,14-eicosatetraenoic acid production by ionophore-stimulated rat serosal mast cells.Biochim. Biophys. Acta 575:185–192

  47. 47.

    Roelofsen, B., Zwaal, R.F.A. 1976. The use of phospholipase in the determination of asymmetric phospholipid distribution in membranes.In: Methods in Membrane Biology. K.D. Korn, editor. Vol. 7, pp. 147–177. Plenum, New York

  48. 48.

    Rohlich, P., Anderson, P., Uvnas, B. 1971. Electron microscope observations on compound 48/80-induced degranulation in rat mast cells: Evidence for sequential exocytosis of storage granules.J. Cell Biol. 51:465–483

  49. 49.

    Rutten, W.J., DePont, J.H.M., Bonting, S.L., Daeman, F.M. 1975. Lysophospholipids in pig pancreatic zymogen granules in relation to exocytosis.Eur. J. Biochem. 54:259–265

  50. 50.

    Saffitz, J.E., Gross, R.W., Williamson, J.R., Sobel, B.E. 1981. Autoradiography of phosphatidyl choline.J. Histochem. Cytochem. 29:371–378

  51. 51.

    Salpeter, M.M., Bachmann, L. 1965. Assessment of technical steps in electron microscope autoradiography.In: Use of Radioautography in Investigation of Protein Synthesis. C.P. LeBond and E. Warren, editors. pp. 23–41. Academic, New York

  52. 52.

    Schnar, R., Weigel, P., Kuhlenschmidt, M., Lee, Y., Roseman, S. 1978. Adhesion of chicken hepatocytes to polyacrylamide gels derivatized with N-acetyglucosamine.J. Biol. Chem. 253:7940–7951

  53. 53.

    Schrey, M.P., Rubin, R.P. 1979. Characterization of a calcium-mediated activation of arachidonic acid turnover in adrenal phospholipids by corticotropin.J. Biol. Chem. 254:11234–11241

  54. 54.

    Shore, P.A., Burkhalter, A., Cohn, V.H. Jr. 1959. A method for fluorometric assay of histamine in tissues.J. Pharmacol. Exp. Ther. 127:182–186

  55. 55.

    Sokal, R.R., Rohlf, F.J. 1981.In: Biometry. pp. 429–450. W. H. Freeman, San Francisco

  56. 56.

    Spector, A.A. 1968. The transport and utilization of free fatty acid.Ann. N.Y. Acad. Sci. 149:768–783

  57. 57.

    Strandberg, K., Sydbom, A., Uvnas, B. 1975. Incorporation of choline, serine, ethanolamine, and inositol into phospholipids of isolated rat mast cells.Acta Physiol. Scand 94:54–62

  58. 58.

    Strandberg, K., Westerberg, S. 1976. Composition of phospholipids and phospholipid fatty acids in rat mast cells.Molec. Cell Biochem. 11:103–107

  59. 59.

    Uvnas, B. 1974. The isolation of secretory granules from mast cells.Methods Enzymol. 51:395–402

  60. 60.

    Uvnas, B., Thon, I. 1961. Evidence for enzymatic histamine release from isolated rat mast cells.Exp. Cell Res. 23:45–57

  61. 61.

    Van den Bosch, H. 1980. Intracellular phospholipases A.Biochim. Biophys. Acta 604:191–246

  62. 62.

    Van den Bosch, H. 1974. Phosphoglyceride metabolism.Annu. Rev. Biochem. 43:243–277

  63. 63.

    Van den Bosch, H., Deenen, L.L.M. van 1965. Chemical structure and biochemical significance of lysolecithins from rat liver.Biochim. Biophys. Acta. 106:326–337

  64. 64.

    Van Golde, L.M.G., Van den Bergh, S.G. 1977. The liver.In: Lipid Metabolism in Mammals. F. Snyder, editor. pp. 35–149. Plenum, New York

  65. 65.

    Wells, M., Hanahan, D. 1968. Phospholipase A fromCrotalus adamanteus venom.Methods Enzymol. 14:178–184

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Castle, J.D., Castle, A.M., Ma, A.K. et al. An enhanced incorporation of fatty acid into phosphatidyl choline that parallels histamine discharge in mast cells. J. Membrain Biol. 79, 215–230 (1984). https://doi.org/10.1007/BF01871061

Download citation

Key Words

  • mast cells
  • exocytosis
  • calcium ionophore
  • phospholipid labeling
  • autoradiography