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Transcellular Metabolism of Arachidonic Acid in Platelets and Polymorphonuclear Leukocytes Activated by Physiological Agonists: Enhancement of Leukotriene B4Synthesis

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Cell-Cell Interactions in the Release of Inflammatory Mediators

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 314))

Abstract

Polymorphonuclear leukocytes (PMNL) are known to play a major role in the inflammatory process in part through their ability to produce and respond to chemotactic factors. Leukotriene (LT) B4, a metabolite of arachidonic acid derived from the 5-lipoxygenase pathway, is produced by phagocytes and has potent chemotactic and chemokinetic effects on these cells1. PMNL stimulated with the ionophore A23187 synthesize large amounts of LTB4 2, while receptor-mediated activation of PMNL and monocytes-macrophages by agonists such as the chemotactic peptide N-formyl-Met-Leu-Phe (fMLP), the complement fragment C5a, platelet-activating factor (paf-acether) or by phagocytosis also leads to LTB4 synthesis3–7. However LTB4 synthesis induced by natural agonists is of lower magnitude as it is often not detectable by HPLC procedures8. Evidence has accumulated during the last decade, supporting that platelet/leukocyte interactions occur in several pathophysiological situations9, and in particular that platelets might modulate inflammation. Indeed, activated platelets release arachidonic acid metabolites, pafacether, platelet-derived growth factor (PDGF), platelet factor 4 (PF4), serotonin and adenine nucleotides which could affect PMNL functions such as migration, degranulation, adherence and production of superoxide anion10–13.

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References

  1. A.W. Ford-Hutchinson, Leukotriene B4 in inflammation, Crit.Rev.Immunol. 10: 1 (1990).

    PubMed  CAS  Google Scholar 

  2. P. Borgeat, Biochemistry of the lipoxygenase pathways in neutrophils, Can, J. of Physiol. Pharmacol. 67: 936 (1989)

    Article  CAS  Google Scholar 

  3. P. Borgeat, M. Nadeau, G. Rouleau, P. Sirois, P. Braquet and P. Poubelle, PAF-induced leukotriene synthesis in human polymorphonuclear leukocytes: inhibition by Ginkgolide B (BN52021), in: “The Ginkgolides: Chemistry, Biology, Pharmacology and Clinical Aspects,” P. Braquet, ed., J.R. Prous Science Publishers, Barcelone (1988).

    Google Scholar 

  4. H.E. Claesson, U. Lundberg and C. Malmsten, Serum-coated zymosan stimulates the synthesis of leukotriene B4 in human polymorphonuclear leukocytes. Inhibition by cyclic AMP. Biochem. Biophys. Res. Commun. 99: 1230 (1981).

    Article  PubMed  CAS  Google Scholar 

  5. R.M. Clancy, C.A. Dahinden and T.E. Hugli, Arachidonate metabolism by human polymorphonuclear leukocytes stimulated by N-formyl-Met-Leu-Phe or complement component C5a is independent of phospholipase activation. Proc. Natl. Acad. Sci. USA 80: 7200 (1983).

    Article  PubMed  CAS  Google Scholar 

  6. A.H. Lin, D.R. Morton and R.R. Gorman, Acetyl glyceryl ether phosphorylcholine stimulates leukotriene B4 synthesis in human polymorphonuclear leukocytes J.Clin.Invest. 70: 1058 (1982).

    Article  PubMed  CAS  Google Scholar 

  7. H. Salari, P. Braquet, P. Naccache and P. Borgeat, Characterization of effect of N-formyl-methionyl-leucyl-phenylalanine on leukotriene synthesis in human polymorphonuclear leukocytes, Inflammation 9: 127 (1985).

    Article  PubMed  CAS  Google Scholar 

  8. S.R. McColl, E. Krump, P.H. Naccache, P. Poubelle, P. Braquet, M. Braquet and P. Borgeat, Granulocyte-macrophage colony-stimulating factor increases the synthesis of leukotriene B4 by human neutrophils in response to platelet-activating factor: enhancement of both arachidonic acid avaibility and 5-lipoxygenase activation, J. Immunol. in press.

    Google Scholar 

  9. B. B. Weksler, Platelets, in: “Inflammation: Basic Principles and Clinical Correlates,” J.I. Gallin, I.M. Goldstein & R. Snyderman, ed., Raven Press, New York (1988).

    Google Scholar 

  10. T.F. Deuel, R.M. Senior and D. Chang, Platelet factor 4 is chemotactic for neutrophils and monocytes, Proc. Nat. Acad. Sci. USA. 78: 4584 (1981).

    Article  PubMed  CAS  Google Scholar 

  11. T.F. Deuel, R.M. Senior and J.S. Huang, Chemotaxis of monocytes and neutrophils to platelet derived growth factor, J. Clin. Invest. 69: 1046 (1982).

    Article  PubMed  CAS  Google Scholar 

  12. P.A. Ward, T.W. Cunningham, K.K. McCulloch, S.H. Phan, J. Powel and K.J. Johnson, Platelets enhancement of O 2 responses in stimulated human neutrophils, Lab.Inv. 58: 37 (1988).

    CAS  Google Scholar 

  13. M.A. Boogaert, O. Yamada, H.S. Jacob and C.F. Moldow, Enhancement of granulocytes-endothelial cell adherence and granulocyte-induced cytotoxicity by platelet release products, Proc. Natl. Acad. Sci. USA. 79: 7019 (1982).

    Article  Google Scholar 

  14. A.J. Marcus, M.J. Broekman, L.B. Safier, H.L. Ullman, N. Islam, C.N. Serhan, L.E. Rutherford, H.M. Korchak and G. Weissman, Formation of leukotrienes and other hydroxy acids during platelet-neutrophil interactions in vitro, Biochem. BioPhys. fies. Commun. 109: 130 (1982).

    Article  CAS  Google Scholar 

  15. P. Borgeat, B. Fruteau-de-Laclos, S. Picard, J. Drapeau, P. Vallerand and E.J. Corey, Studies on the mechanism of formation of the 5S, 12S-dihydroxy-6, 8, 10, 14(E, Z, E, Z) acid in leukocytes, Prostaglandins 23: 713 (1982).

    Article  PubMed  CAS  Google Scholar 

  16. A.J. Marcus, L.B. Safier, H.L. Ullman, M.J. Broekman, N. Islam, T.D. Oglesby and R.R. Gorman, 12S, 20-Dihydroxy-icosatetraenoic acid: A new icosanoid synthesized by neutrophils from 12S-hydroxyicosatetraenoic acid produced by thrombin-or collagen-stimulated platelets. Proc. Nat. Acad. Sci. USA 81: 903 (1984).

    Article  PubMed  CAS  Google Scholar 

  17. J. Maclouf, F.A. Fitzpatrick and R.C. Murphy, Transcellular biosynthesis of eicosanoids, Pharmacol.Res. 21: 1 (1989).

    Article  PubMed  CAS  Google Scholar 

  18. C.N. Serhan, K.A. Sheppard, Lipoxin formation during human neutrophil-platelet interactions — evidence for the transformation of leukotriene-A4 by platelet 12-lipoxygenase in vitro, J. Clin. Invest. 85: 772 (1990).

    Article  PubMed  CAS  Google Scholar 

  19. J. Maclouf, B. Fruteau de Laclos and P. Borgeat, Stimulation of leukotriene biosynthesis in human blood leukocytes by platelet-derived 12-hydroperoxy-icosatetraenoic acid. Proc. Natl. Acad. Sci. USA. 79: 6042 (1982).

    Article  PubMed  CAS  Google Scholar 

  20. A. Del Maschio, J. Maclouf, E. Corvazier, M.J. Grange, P. Borgeat, Activated platelets stimulate human neutrophils functions, Nouv. Rev. Fr. Hematol. 27: 275 (1985).

    PubMed  CAS  Google Scholar 

  21. S. Fiore and C.N. Serhan, Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils, J. Exp. Med. 172: 1451 (1990).

    Article  PubMed  CAS  Google Scholar 

  22. R. Palmantier and P. Borgeat, Thrombin-activated platelets amplify leukotriene B4 synthesis by neutrophils, Clinical and investigative medicine, 12:B7, Abst.#R-17 (1989).

    Google Scholar 

  23. R. Palmantier and P. Borgeat, Amplification of leukotriene B4 synthesis in neutrophils by thrombin activated platelets, FASEB J. 4:A2231. Abst.#3102 (1990).

    Google Scholar 

  24. M. Lagarde, P.A. Bryon, M. Guichardant, M. Dechavanne, A simple and efficient method for platelet isolation from their plasma, Thromb.Res. 17: 581 (1980).

    Article  PubMed  CAS  Google Scholar 

  25. A. Boyum, Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1g. Scand. J. Clin. Lab. Invest. 21: 77 (1968).

    Article  CAS  Google Scholar 

  26. P. Borgeat and S. Picard, 19-Hydroxyprostaglandin B2 as an internal standard for on-line extraction-high-performance liquid chromatography analysis of lipoxygenase products. Anal. Biochem. 171: 283 (1988).

    Article  PubMed  CAS  Google Scholar 

  27. M. Chignard, C. Lalau Keraly, D. Nunez, E. Coëffier and J. Benveniste, PAF-acether and platelets, in: “Platelets in biology and pathology III” MacIntyre & Gordon, ed., Elsevier Science Publisher, B.V., (1987).

    Google Scholar 

  28. W.S. Powell, Properties of leukotriene B4 20-hydroxylase from polymorphonuclear leukocytes. J. Biol. Chem. 259: 3082 (1984).

    PubMed  CAS  Google Scholar 

  29. J.A. Lindgren, G. Hansson, B. Samuelsson, Formation of novel hydroxylated eicosatetraenoic acids in preparations of human polymorphonuclear leukocytes. FEBS. Lett. 128: 329 (1981).

    Article  PubMed  CAS  Google Scholar 

  30. C. Ruef and D.L. Coleman, Granulocyte-Macrophage Colony-Stimulating Factor: Pleitropic Cytokine With Potential Usefulness, Reviews of infectious diseases. 12: 41 (1990).

    Article  PubMed  CAS  Google Scholar 

  31. R.H. Weisbart, L. Kwan, D.W. Golde, J.C. Gasson, Human GM-CSF primes neutrophils for enhanced oxidative metabolism in response to the major physiological chemoattractants. Blood. 69: 18 (1987).

    PubMed  CAS  Google Scholar 

  32. S.E. Kaufman, J.F. Dipersio, J.C. Gasson, Effects of Human GM-CSF on Neutrophil Degranulation In Vitro. Exp. Hematol. 17: 800 (1989).

    PubMed  CAS  Google Scholar 

  33. A.F. Lopez, D.J. Williamson, J.R. Gamble, C.G. Begley, J.M. Harlan, S.J. Klebanoff, A. Waltersdorph, G. Wong, S.C. Clark and M.A. Vadas, Recombinant human granulocyte-macrophage colony-stimulating factor stimulates in vitro mature human neutrophil and eosinophil function, surface receptor expression and survival, J. Clin. Invest. 78: 1222 (1986).

    Article  Google Scholar 

  34. D.S. Silberstein, W.F. Owen, J.C. Gasson, J.F. DiPersio and D.W. Golde, Enhancement of human eosinophil cytotoxicity and leukotriene synthesis by biosynthetic (recombinant) granulocyte-macrophage colony-stimulating factor. J. Immunol. 137: 3290 (1986).

    PubMed  CAS  Google Scholar 

  35. C.A. Dahinden, J. Zingg, F.E. Maly and A.L. De Weck, Leukotriene production in human neutrophils primed by recombinant human granulocyte/macrophage colony-stimulating factor and stimulated with the complement component C5a and FMLP as second signals. J. Exp. Med. 167: 1281 (1988).

    Article  PubMed  CAS  Google Scholar 

  36. J.F. DiPersio, P.H. Naccache, P. Borgeat, J.C. Gasson, M-H. Nguyen and S.R. McColl, Characterization of the priming effects of human granulocyte-macrophage colony-stimulating factor on human neutrophil leukotriene synthesis, Prostaglandins. 36: 673 (1988).

    Article  Google Scholar 

  37. R.L. Maas and A.R. Brash, Evidence for a lipoxygenase mechanism in the biosynthesis of epoxide and dihydroxy leukotrienes from 15(S)-hydroperoxyicosatetraenoic acid by human platelets and porcine leukocytes. Proc. Nat. Acad. Sci. USA. 80: 2884 (1983).

    Article  PubMed  CAS  Google Scholar 

  38. P.Y-K. Wong, P. Westlund, M. Hamberg, E. Granstrom, P.H-W. Chao and B. Samuelsson, 15-Lipoxygenase in human platelets. J. Biol. Chem. 260: 9162 (1985).

    PubMed  CAS  Google Scholar 

  39. A.J. Marcus, L.B. Safier, H.L. Ullman, N. Islam, M.J. Broekman and C. von Schacky, Studies on the mechanism of omega-hydroxylation of platelet 12-hydroxyeicosatetraenoic acid (12-HETE) by unstimulated neutrophils. J. Clin. Invest. 79: 179 (1987).

    Article  PubMed  CAS  Google Scholar 

  40. J. Maclouf, R.C. Murphy and P.M. Henson, Transcellular Biosynthesis of sulfidopeptide leukotrienes during receptor-mediated stimulation of human neutrophil/platelet mixtures, Blood. 76: 1838 (1990).

    PubMed  CAS  Google Scholar 

  41. K. Schror, V. Neuhaus, B. Ahland, S. Sauerland, A. Kuhn, H. Darius and K. Bussmann, Actions of tiaprofenic acid on vascular prostacyclin biosynthesis and thromboxane and 12-HPETE formation of human platelets in vitro and ex vivo. Rheumatology. 7: 88 (1982).

    Google Scholar 

  42. H. Salari, P. Braquet, P. Borgeat, Comparative effects of indomethacin, acetylenic acids, 15-HETE, nordihydroguaiaretic acid and BW755C on the metabolism of arachidonic acid in human leukocytes and platelets. Prostaglandins Leukotrienes Med. 13: 53 (1984).

    Article  CAS  Google Scholar 

  43. J.B. Smith, C. Dangelmaier and G. Mauco, Measurement of arachidonic acid liberation in thrombin-stimulated human platelets. Use of agents that inhibit both the cyclooxygenase and lipoxygenase enzymes. Biochim. Biophys. Acta. 835: 344 (1985).

    PubMed  CAS  Google Scholar 

  44. E. Coeffier, D. Delautier, J.P. Lecouedic, M. Chignard, Y. Denizot and J. Benveniste, Cooperation between platelets and neutrophils for PAF-acether (Platelet-Activating Factor) formation. J. Leukocyte Biol. 47: 234 (1990).

    PubMed  CAS  Google Scholar 

  45. P. Borgeat and B. Samuelsson, Arachidonic acid metabolism in polymorphonuclear leukocytes: effects of ionophore A23187. Proc. Natl, Acad, Sci. USA. 76: 2148 (1979).

    Article  CAS  Google Scholar 

  46. K.A. Haines, K.N. Giedd, A.M. Rich, H.M. Korchak and G. Weissmann, The leukotriene B4 paradox: neutrophils can, but will not, respond to ligand-receptor interactions by forming leukotriene B4 or its omega-metabolites. Biochem. J. 241: 55 (1987).

    PubMed  CAS  Google Scholar 

  47. A. Hatzelmann and V. Ullrich, Regulation of 5-lipoxygenase activity by the glutathione status in human polymorphonuclear leukocytes. Eur.J.Biochem. 169: 175 (1987).

    Article  PubMed  CAS  Google Scholar 

  48. A.D. Purdon and A.K. Rao, Interaction of albumin, Arachidonic acid and prostanoids in platelets. Prostagland. Leuk. Essent. Fatty. 35: 213 (1989).

    Article  CAS  Google Scholar 

  49. T.W. Jungi, M.O. Spycher, U.E. Nydegger and S. Barandun, Platelet-leukocyte interaction: selective binding of thrombin-stimulated platelets to human monocytes, polymorphonuclear leukocytes, and related cell lines, Blood. 67: 629 (1986).

    PubMed  CAS  Google Scholar 

  50. E. Larsen, A. Celi, G.E. Gilbert, B.C. Furie, J.K. Erban, R. Bonfanti, D.D. Wagner, B. Furie, PADGEM protein — A receptor that mediates the interaction of activated platelets with neutrophils and monocytes, Cell. 59: 305 (1989).

    Article  PubMed  CAS  Google Scholar 

  51. S.A. Hamburger, R.P. Mcever, GMP-140 Mediates Adhesion of Stimulated Platelets to Neutrophils, Blood. 75: 550 (1990).

    PubMed  CAS  Google Scholar 

  52. E. Larsen, T. Palabrica, S. Sajer, G.E Gilbert, D.D. Wagner, B.C. Furie and B. Furie, PADGEM-dependant adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15), Cell. 63: 467 (1990).

    Article  PubMed  CAS  Google Scholar 

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© 1991 Plenum Press, New York

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Palmantier, R., Borgeat, P. (1991). Transcellular Metabolism of Arachidonic Acid in Platelets and Polymorphonuclear Leukocytes Activated by Physiological Agonists: Enhancement of Leukotriene B4Synthesis. In: Wong, P.YK., Serhan, C.N. (eds) Cell-Cell Interactions in the Release of Inflammatory Mediators. Advances in Experimental Medicine and Biology, vol 314. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-6024-7_4

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  • DOI: https://doi.org/10.1007/978-1-4684-6024-7_4

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