Advertisement

Interaction of Platelets and Neutrophils in the Generation of Sulfidopeptide Leukotrienes

  • Robert C. Murphy
  • Jacques Maclouf
  • Peter M. Henson
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 314)

Abstract

For approximately 50 years the mediator termed slow reacting substance of anaphylaxis (SRS-A) was suspected to play an important role in human allergic reactions, prolonged bronchoconstriction and asthma yet its chemical structure remained elusive (1, 2). Details concerning the biosynthetic origin of this molecule as well as the regulatory mechanisms involved in controlling production and degradation of SRS-A were unknown. In 1979, the structure of SRS-A was elucidated (3) as a family of three novel compounds, having both a lipid portion derived from arachidonic acid and a peptide portion derived from glutathione (4). These molecules are now termed sulfidopeptide leukotrienes (leukotriene C4, D4, E4), which differ in the number of amino acid residues resident in the peptide portion as either gamma-glutamylcysteinylglycine, cysteinylglycine, or cysteine respectively. During the past decade, a great deal of information has been obtained describing the biosynthesis of these molecules, the activation of phospholipase A2 in liberating free arachidonic acid esterified to storage phospholipids (5), the importance of 5-lipoxygenase in generating the reactive intermediate leukotriene A4 (6) and LTC4 synthase which catalyzes the condensation of glutathione with leukotriene A4 yielding LTC4 (7). Furthermore, it is now recognized that sulfidopeptide leukotrienes can be synthesized in a variety of cells including mast cells (8), eosinophils (9), macrophages (10), and basophils (11). Interest in these molecules continues because of the potent biological activities which they possess including bronchoconstriction (12), vasoconstriction (13), and increased vascular permeability (14). Metabolism of LTC4 is known to take place rapidly and includes sequential peptide cleavage reactions (leading to the sulfidopeptide leukotriene described above) as well as ω- and β-oxidation with ultimate elimination of metabolites into the urine (15).

Keywords

Human Neutrophil Lipid Mediator Calcium Ionophore Calcium Ionophore A23187 Human Polymorphonuclear Leukocyte 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    C. H. Kelloway and E. R. Trethewie, The liberation of a slow-reacting smooth muscle-stimulating substance in anaphylaxis, J. Exptl. Phvsiol. 30: 121 (1940).Google Scholar
  2. 2.
    R. P. Orange and K. F. Austen, Slow reacting substance of anaphylaxis, Adv. Immunol. 10: 105 (1969).PubMedCrossRefGoogle Scholar
  3. 3.
    R. C. Murphy, S. Hammarstrom, and B. Samuelsson, Leukotriene C: A slow reacting substance (SRS) from murine mastocytoma cells, Proc. Natl. Acad. Sci. USA 76: 4275 (1979).PubMedCrossRefGoogle Scholar
  4. 4.
    B. Samuelsson, P. Borgeat, S. Hammarstrom, and R. C. Murphy, Leukotrienes: A new group of biologically active compounds, in: “Advances in Prostaglandins and Thromboxane Research,” B. Samuelsson, P. W. Ramwell, and R. Paoletti, eds., Raven Press, New York (1980).Google Scholar
  5. 5.
    C. C. Leslie, D. R. Voelker, J. Y. Channon, M. W. Wall, and P. T. Zelarney, Properties and purification of an arachidonoyl-hydrolyzing phospholipase A2 from a macrophage cell line, RAW204.7, Biochim. Biophys. Acta 963: 476 (1988).PubMedGoogle Scholar
  6. 6.
    P. Borgeat and B. Samuelsson, Arachidonic acid metabolism and polymorphonuclear leukocytes: Unstable intermediate in formation of dihydroxy acids, Proc. Natl. Acad. Sci. USA 76: 3213 (1979).PubMedCrossRefGoogle Scholar
  7. 7.
    T. Shimizu, Enzymes functional in the synthesis of leukotrienes and related compounds, Int. J. Biochem. 20: 661 (1988).PubMedCrossRefGoogle Scholar
  8. 8.
    B. Samuelsson, and C. D. Funk, Enzymes involved in the biosynthesis of leukotriene B4, J. Biol. Chem. 264: 19469 (1989).PubMedGoogle Scholar
  9. 9.
    A. Jorg, W. R. Henderson, R. C. Murphy, and S. J. Klebanoff, Leukotriene generation by eosinophils, J. Exp. Med. 155: 390 (1982).PubMedCrossRefGoogle Scholar
  10. 10.
    C. A. Rouzer, W. A. Scott, A. L. Hamill, and F. A. Cohn, Dynamics of leukotriene C production by macrophages, J. Exp. Med. 152: 1236 (1980).PubMedCrossRefGoogle Scholar
  11. 11.
    P. T. Peachell, L. M. Lichtenstein, and R. P. Schleimer, Inhibition by adenosine of histamine and leukotriene release from human basophils, Biochem. Pharm. 38: 1717 (1989).PubMedCrossRefGoogle Scholar
  12. 12.
    S. E. Dahlen, P. Hedqvist, S. Hammarstrom, and B. Samuelsson, Leukotrienes are potent constrictors of human bronchi, Nature 288: 484 (1980).PubMedCrossRefGoogle Scholar
  13. 13.
    N. A. Soter, R. A. Lewis, E. J. Corey, and K. F. Austen, Local effects of synthetic leukotrienes (LTC4, LTD4, LTE4, and LTB4) in human skin, J. Invest. Dermatol. 80: 115 (1983).PubMedCrossRefGoogle Scholar
  14. 14.
    Z. Marom, J. H. Shelhamer, M. K. Bach, D. R. Morton, and M. Kaliner, Slow reacting substances LTC4 and D4 increase the release of mucus from human airways in vitro, Am. Rev. Respir. Dis. 126: 449 (1982).PubMedGoogle Scholar
  15. 15.
    A. Sala, N. Voelkel, J. Maclouf, and R. C. Murphy, LTE4 elimination and metabolism in normal human subjects, J. Biol. Chem. 265: 21771 (1990).PubMedGoogle Scholar
  16. 16.
    C. P. Page, Platelets as inflammatory cell, Immunopharmacol. 17: 51 (1989).CrossRefGoogle Scholar
  17. 17.
    P. M. Henson, Interactions between neutrophils and platelets, Editorial, Lab. Invest. 62: 391 (1990).PubMedGoogle Scholar
  18. 18.
    J. Wester, J. J. Sixma, J. J. Geuze, and H. J. G. Heijin, Morphology of the hemostatic plug in human skin wounds. Transformation of the healing, Lab. Invest. 41: 182 (1979).PubMedGoogle Scholar
  19. 19.
    P. M. Henson and C. G. Cochrane, Immunological induction of increased vascular permeability. I. A rabbit passive cutaneous anaphylactic reaction requiring complement, platelets and neutrophils, J. Exp. Med. 129: 153 (1969).PubMedCrossRefGoogle Scholar
  20. 20.
    P. M. Henson, Mechanisms of release of constituents from rabbit platelets by antigen-antibody complexes and complement II. Interaction of platelets with neutrophils, J. Immunol. 105: 490 (1970).PubMedGoogle Scholar
  21. 21.
    A. Del Maschio, V. Evangelista, G. Rajtar, Z.-M. Chen, C. Cerletti, and G. De Gaetano, Platelet activation by polymorphonuclear leukocytes exposed to chemotactic agents, Am. J. Phvsiol. 258: H870 (1990).Google Scholar
  22. 22.
    M. A. Selak, M. Chignard, and J. B. Smith, Cathepsin G is a strong platelet agonist released by neutrophils, Biochem. J. 251: 293 (1988).PubMedGoogle Scholar
  23. 23.
    D. Y. Tzeng, T. F. Deuel, J. S. Huang, R. M. Senior, L. A. Boxer, and R. L. Baehner, Platelet-derived growth factor promotes polymorphonuclear leukocyte activation, Blood 64: 1123 (1984).PubMedGoogle Scholar
  24. 24.
    S. T. McGarrity, T. M. Hyers, and R. O. Webster, Inhibition of neutrophil functions by platelets and platelet-derived products: Description of multiple inhibitory properties, J. Leuk. Biol. 44: 93 (1988).Google Scholar
  25. 25.
    S. M. Albelda and C. A. Buck, Integrins and other cell adhesion molecules, FASEB J. 4: 2868–2880 (1990).PubMedGoogle Scholar
  26. 26.
    T. A. Springer, Adhesion receptors of the immune system, Nature 346: 425 (1990).PubMedCrossRefGoogle Scholar
  27. 27.
    T. A. Springer and L. A. Lasky, Sticky sugars for selectins, Nature 349: 196 (1991).PubMedCrossRefGoogle Scholar
  28. 28.
    E. Larsen, A. Celi, G. E. Gilbert, B. C. Furie, J. K. Erban, R. Bonfanti, D. D. Wagner, and B. Furie, PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes, Cell 59: 305 (1989).PubMedCrossRefGoogle Scholar
  29. 29.
    L. Corral, M. S. Singer, B. A. Macher, and S. D. Rosen, Requirement for sialic acid on neutrophils in a GMP-140 (PADGEM) mediated adhesive interaction with activated platelets, Biochem. Biophys. Res. Commun. 172: 1349 (1990).PubMedCrossRefGoogle Scholar
  30. 30.
    S. A. Hamburger and R. P. McEver, GMP-140 mediates adhesion of stimulated platelets to neutrophils, Blood 75: 550 (1990).PubMedGoogle Scholar
  31. 31.
    J. Maclouf, B. Fruteau de Laclos, and P. Borgeat, Stimulation of leukotriene biosynthesis in human blood leukocytes by platelet-derived 12-hydroxyperoxy-eicosatetraenoic acids, Proc. Natl. Acad. Sci. USA 79: 6042 (1982).PubMedCrossRefGoogle Scholar
  32. 32.
    A. J. Marcus, L. B. Safier, H. L. Ullman, N. Islam, M. J. Broekman, N. Islam, T. D. Oglesby, and R. R. Gorman, 12S,20-Dihydroxyicosatetraenoic acid: A new eicosanoid synthesized by neutrophils from 12S-hydroxyicosatetraenoic acid produced by thrombin-or collagen-stimulated platelets, Proc. Natl. Acad. Sci. USA 81: 903 (1984).PubMedCrossRefGoogle Scholar
  33. 33.
    P. Wong, Y. K. Westlund, M. Hamberg, E. Granstrom, P. H. W. Chao, and B. Samuelsson, ω-Hydroxylation of 12-L-hydroxy-5, 8, 10, 14-eicosatetraenoic acid in human polymorphonuclear leukocytes, J. Biol. Chem. 259: 2683 (1984).PubMedGoogle Scholar
  34. 34.
    A. J. Marcus, L. B. Safier, H. L. Ullman, N. Islam, M. J. Broekman, J. R. Falck, S. Fischer, and C. von Schacky, Platelet-neutrophil interactions: (12S)-hydroxy-eicosatetraen-l, 20-dioic acid: A new eicosanoid synthesized by unstimulated neutrophils from (12S)-20-dihydroxyeicosatetraenoic acid, J. Biol. Chem. 263: 2223 (1988).PubMedGoogle Scholar
  35. 35.
    P. Borgeat, M. Hamberg, and B. Samuelsson, Transformation of arachidonic acid in dihomo-7-linolenic acid by rabbit PMN leukocytes, J. Biol. Chem. 251: 7816 (1976).PubMedGoogle Scholar
  36. 36.
    P. Borgeat and B. Samuelsson, Transformation of arachidonic acid by rabbit polymorphonuclear leukocytes, J. Biol. Chem. 254: 2643 (1979).PubMedGoogle Scholar
  37. 37.
    T. Shimizu, O. Radmar, and B. Samuelsson, Enzyme with dual lipoxygenase activities catalyze leukotriene A4 synthesis from arachidonic acid, Proc. Natl. Acad. Sci. USA 81: 689 (1984).PubMedCrossRefGoogle Scholar
  38. 38.
    R. A. F. Dixon, R. E. Diehl, E. Opas, E. Rands, P. J. Vickers, J. F. Evans, J. W. Gillard, and D. K. Miller, Requirement of a 5-lipoxygenase-activating protein for leukotriene synthesis, Nature 343: 282 (1990).PubMedCrossRefGoogle Scholar
  39. 39.
    C. A. Rouzer and S. Kargman, Translocation of 5-lipoxygenase to the membrane in human leukocytes challenged with ionophore A23187, J. Biol. Chem. 263: 10980 (1988).PubMedGoogle Scholar
  40. 40.
    C. A. Dahinden, R. M. Clancy, M. Gross, J. M. Chiller, and T. E. Hugli, Leukotriene C4 production by murine mast cells: Evidence of a role for extracellular leukotriene A4, Proc. Natl. Acad. Sci. USA 82: 6632 (1985).PubMedCrossRefGoogle Scholar
  41. 41.
    F. A. Fitzpatrick, D. R. Morton, and M. A. Wynalda, Albumin stabilizes leukotriene A4, J. Biol. Chem. 257: 4680 (1982).PubMedGoogle Scholar
  42. 42.
    B. K. Lam, W. F. Owen, K. F. Austen, and R. J. Soberman, The identification of a distinct export step following the biosynthesis of leukotriene C4 by human eosinophils, J. Biol. Chem. 264: 12885 (1989).PubMedGoogle Scholar
  43. 43.
    B. K. Lam, W. F. Owen, K. F. Austen, and R. J. Soberman, The mechanism of leukotriene B4 export from human polymorphonuclear leukocytes, J. Biol. Chem. 265: 13438 (1990).PubMedGoogle Scholar
  44. 44.
    J. Maclouf and R. C. Murphy, Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets, J. Biol. Chem. 263: 174 (1988).PubMedGoogle Scholar
  45. 45.
    H. E. Claesson and J. Haeggstrom, Human endothelial cells stimulate leukotriene synthesis and convert granulocyte released leukotriene A4 into leukotrienes B4, C4, D4, and E4, Eur. J. Biochem. 173: 93 (1988).PubMedCrossRefGoogle Scholar
  46. 46.
    C. Edenius, K. Heidvall, and J.A. Lindgren, Novel transformation of granulocyte-derived leukotriene A4 into cysteinyl-containing leukotrienes by human platelets, Eur. J. Biochem. 178: 81 (1988).PubMedCrossRefGoogle Scholar
  47. 47.
    J. Maclouf, R. C. Murphy, and P. M. Henson, Transcellular sulfidopeptide leukotriene biosynthetic capacity of vascular cells, Blood 74: 703 (1989).PubMedGoogle Scholar
  48. 48.
    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).PubMedGoogle Scholar
  49. 49.
    A. Fradin, J. A. Zirrolli, J. Maclouf, L. Vausbinder, P. M. Henson, and R. C. Murphy, PAF and leukotriene biosynthesis in whole blood: A model for the study of transcellular arachidonate metabolism, J. Immunol. 143: 3680 (1989).PubMedGoogle Scholar
  50. 50.
    R. A. Lewis, and K. F. Austen, The biologically active leukotrienes. Biosynthesis, metabolism, receptors, functions, and pharmacology, J. Clin. Invest. 73: 889 (1984).PubMedCrossRefGoogle Scholar
  51. 51.
    A. J. Marcus, Thrombosis and inflammation as multicellular processes: Pathophysiological significance of transcellular metabolism, Blood 76: 1903 (1990).PubMedGoogle Scholar
  52. 52.
    R. C. Murphy and P. M. Henson, Mediator network, in: “Annales de l’Institut Pasteur/Immunologie,” Institut Pasteur, ed., Institut Pasteur (1985).Google Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Robert C. Murphy
    • 1
  • Jacques Maclouf
    • 2
  • Peter M. Henson
    • 1
  1. 1.National Jewish Center for Immunology and Respiratory MedicineDenverUSA
  2. 2.INSERM Unit 150, Hopital LariboisiereParis Cedex 10France

Personalised recommendations