Skip to main content
SpringerLink
Log in

Interaction of Platelets and Neutrophils in the Generation of Sulfidopeptide Leukotrienes

  • Chapter
Cell-Cell Interactions in the Release of Inflammatory Mediators

Part of the book series: Advances in Experimental Medicine and Biology ((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).

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  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. R. P. Orange and K. F. Austen, Slow reacting substance of anaphylaxis, Adv. Immunol. 10: 105 (1969).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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. 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).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  7. T. Shimizu, Enzymes functional in the synthesis of leukotrienes and related compounds, Int. J. Biochem. 20: 661 (1988).

    Article  PubMed  CAS  Google Scholar 

  8. B. Samuelsson, and C. D. Funk, Enzymes involved in the biosynthesis of leukotriene B4, J. Biol. Chem. 264: 19469 (1989).

    PubMed  CAS  Google Scholar 

  9. A. Jorg, W. R. Henderson, R. C. Murphy, and S. J. Klebanoff, Leukotriene generation by eosinophils, J. Exp. Med. 155: 390 (1982).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  12. S. E. Dahlen, P. Hedqvist, S. Hammarstrom, and B. Samuelsson, Leukotrienes are potent constrictors of human bronchi, Nature 288: 484 (1980).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  16. C. P. Page, Platelets as inflammatory cell, Immunopharmacol. 17: 51 (1989).

    Article  CAS  Google Scholar 

  17. P. M. Henson, Interactions between neutrophils and platelets, Editorial, Lab. Invest. 62: 391 (1990).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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. M. A. Selak, M. Chignard, and J. B. Smith, Cathepsin G is a strong platelet agonist released by neutrophils, Biochem. J. 251: 293 (1988).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    CAS  Google Scholar 

  25. S. M. Albelda and C. A. Buck, Integrins and other cell adhesion molecules, FASEB J. 4: 2868–2880 (1990).

    PubMed  CAS  Google Scholar 

  26. T. A. Springer, Adhesion receptors of the immune system, Nature 346: 425 (1990).

    Article  PubMed  CAS  Google Scholar 

  27. T. A. Springer and L. A. Lasky, Sticky sugars for selectins, Nature 349: 196 (1991).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  30. S. A. Hamburger and R. P. McEver, GMP-140 mediates adhesion of stimulated platelets to neutrophils, Blood 75: 550 (1990).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  36. P. Borgeat and B. Samuelsson, Transformation of arachidonic acid by rabbit polymorphonuclear leukocytes, J. Biol. Chem. 254: 2643 (1979).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  41. F. A. Fitzpatrick, D. R. Morton, and M. A. Wynalda, Albumin stabilizes leukotriene A4, J. Biol. Chem. 257: 4680 (1982).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  44. J. Maclouf and R. C. Murphy, Transcellular metabolism of neutrophil-derived leukotriene A4 by human platelets, J. Biol. Chem. 263: 174 (1988).

    PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  47. J. Maclouf, R. C. Murphy, and P. M. Henson, Transcellular sulfidopeptide leukotriene biosynthetic capacity of vascular cells, Blood 74: 703 (1989).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  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).

    PubMed  CAS  Google Scholar 

  50. R. A. Lewis, and K. F. Austen, The biologically active leukotrienes. Biosynthesis, metabolism, receptors, functions, and pharmacology, J. Clin. Invest. 73: 889 (1984).

    Article  PubMed  CAS  Google Scholar 

  51. A. J. Marcus, Thrombosis and inflammation as multicellular processes: Pathophysiological significance of transcellular metabolism, Blood 76: 1903 (1990).

    PubMed  CAS  Google Scholar 

  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 

Download references

Author information

Authors and Affiliations

  1. National Jewish Center for Immunology and Respiratory Medicine, 1400 Jackson Street, Denver, CO, 80206, USA

    Robert C. Murphy & Peter M. Henson

  2. INSERM Unit 150, Hopital Lariboisiere, 75475, Paris Cedex 10, France

    Jacques Maclouf

Authors
  1. Robert C. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacques Maclouf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter M. Henson
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. New York Medical College, Valhalla, New York, USA

    Patrick Y.-K. Wong

  2. Harvard Medical School, Boston, Massachusetts, USA

    Charles N. Serhan

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Plenum Press, New York

About this chapter

Cite this chapter

Murphy, R.C., Maclouf, J., Henson, P.M. (1991). Interaction of Platelets and Neutrophils in the Generation of Sulfidopeptide Leukotrienes. 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_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-6024-7_5

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-6026-1

  • Online ISBN: 978-1-4684-6024-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation