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. 1995 Mar 28;92(7):2815–2819. doi: 10.1073/pnas.92.7.2815

Endogenously opsonized particles divert prostanoid action from lethal to protective in models of experimental endotoxemia.

D F Eierman 1, M Yagami 1, S M Erme 1, S R Minchey 1, P A Harmon 1, K J Pratt 1, A S Janoff 1
PMCID: PMC42309  PMID: 7708730

Abstract

We report that, in rats, the lethal consequences of high-dose endotoxin challenge are exacerbated by the intravascular administration of prostaglandin E1 but attenuated by the intravascular administration of endocytosable particles. This protection is mediated by opsonins. Nonopsonizable particles were unable to provide protection unless first pseudoopsonized with antibody directed against the CR3 (CD11b/CD18) phagocyte receptor. We show that endogenously opsonized particles can act in concert with prostaglandin E1 (putatively by elevation of neutrophil intracellular cAMP and the resultant downregulation of CR3) to completely rescue animals from the lethal late-stage sequelae of experimental endotoxemia. These data illustrate that the interaction of particles with cellular receptors can transform the overall systemic response to prostaglandin E1 from pro- to antiinflammatory. This suggests a role for multiple receptor engagement events in defining the systemic prostaglandin response and offers a rationale for developing new therapeutic modalities in the treatment of sepsis and other inflammatory diseases.

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Selected References

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

  1. Barclay A. N. The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology. 1981 Apr;42(4):593–600. [PMC free article] [PubMed] [Google Scholar]
  2. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  3. Cronstein B. N., Naime D., Ostad E. The antiinflammatory mechanism of methotrexate. Increased adenosine release at inflamed sites diminishes leukocyte accumulation in an in vivo model of inflammation. J Clin Invest. 1993 Dec;92(6):2675–2682. doi: 10.1172/JCI116884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Devine D. V., Wong K., Serrano K., Chonn A., Cullis P. R. Liposome-complement interactions in rat serum: implications for liposome survival studies. Biochim Biophys Acta. 1994 Apr 20;1191(1):43–51. doi: 10.1016/0005-2736(94)90231-3. [DOI] [PubMed] [Google Scholar]
  5. Doerr T. A., Rosolia D. L., Peters S. P., Gee M. H., Albertine K. H. PGE1 inhibited PMN attachment to air emboli in vivo during infusion of ZAP without preventing lung injury. J Appl Physiol (1985) 1992 Jan;72(1):340–351. doi: 10.1152/jappl.1992.72.1.340. [DOI] [PubMed] [Google Scholar]
  6. Dunn D. L. Use of novel therapeutic agents for the treatment of serious infection. Am J Surg. 1993 Nov;166(5):449–455. doi: 10.1016/s0002-9610(05)81141-9. [DOI] [PubMed] [Google Scholar]
  7. Fällman M., Andersson R., Andersson T. Signaling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complement-opsonized particles. J Immunol. 1993 Jul 1;151(1):330–338. [PubMed] [Google Scholar]
  8. Grant M. M., Burnett C. M., Fein A. M. Effect of prostaglandin E1 infusion on leukocyte traffic and fibrosis in acute lung injury induced by bleomycin in hamsters. Crit Care Med. 1991 Feb;19(2):211–217. doi: 10.1097/00003246-199102000-00017. [DOI] [PubMed] [Google Scholar]
  9. Kearney J. F., Radbruch A., Liesegang B., Rajewsky K. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol. 1979 Oct;123(4):1548–1550. [PubMed] [Google Scholar]
  10. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  11. Lu D. J., Furuya W., Grinstein S. Involvement of multiple kinases in neutrophil activation. Blood Cells. 1993;19(2):343–351. [PubMed] [Google Scholar]
  12. Löfgren R., Ng-Sikorski J., Sjölander A., Andersson T. Beta 2 integrin engagement triggers actin polymerization and phosphatidylinositol trisphosphate formation in non-adherent human neutrophils. J Cell Biol. 1993 Dec;123(6 Pt 1):1597–1605. doi: 10.1083/jcb.123.6.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Madden T. D., Bally M. B., Hope M. J., Cullis P. R., Schieren H. P., Janoff A. S. Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents. Biochim Biophys Acta. 1985 Jul 11;817(1):67–74. doi: 10.1016/0005-2736(85)90069-0. [DOI] [PubMed] [Google Scholar]
  14. Mayer L. D., Hope M. J., Cullis P. R. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim Biophys Acta. 1986 Jun 13;858(1):161–168. doi: 10.1016/0005-2736(86)90302-0. [DOI] [PubMed] [Google Scholar]
  15. Mårtensson L., Davidsson B., Hultkvist U. Model of pulmonary extravasation as an effect of neutropenia in endotoxic shock in guinea pigs. Eur Surg Res. 1989;21(6):319–326. doi: 10.1159/000129045. [DOI] [PubMed] [Google Scholar]
  16. Nathan C., Sanchez E. Tumor necrosis factor and CD11/CD18 (beta 2) integrins act synergistically to lower cAMP in human neutrophils. J Cell Biol. 1990 Nov;111(5 Pt 1):2171–2181. doi: 10.1083/jcb.111.5.2171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ney P., Braun M., Szymanski C., Bruch L., Schrör K. Antiplatelet, antineutrophil and vasodilating properties of 13,14-dihydro-PGE1 (PGE0)--an in vivo metabolite of PGE1 in man. Eicosanoids. 1991;4(3):177–184. [PubMed] [Google Scholar]
  18. Novogrodsky A., Vanichkin A., Patya M., Gazit A., Osherov N., Levitzki A. Prevention of lipopolysaccharide-induced lethal toxicity by tyrosine kinase inhibitors. Science. 1994 May 27;264(5163):1319–1322. doi: 10.1126/science.8191285. [DOI] [PubMed] [Google Scholar]
  19. Ohlsson K., Björk P., Bergenfeldt M., Hageman R., Thompson R. C. Interleukin-1 receptor antagonist reduces mortality from endotoxin shock. Nature. 1990 Dec 6;348(6301):550–552. doi: 10.1038/348550a0. [DOI] [PubMed] [Google Scholar]
  20. Perkins W. R., Minchey S. R., Ahl P. L., Janoff A. S. The determination of liposome captured volume. Chem Phys Lipids. 1993 Sep;64(1-3):197–217. doi: 10.1016/0009-3084(93)90066-c. [DOI] [PubMed] [Google Scholar]
  21. Robinson A. P., White T. M., Mason D. W. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology. 1986 Feb;57(2):239–247. [PMC free article] [PubMed] [Google Scholar]
  22. Rossignon M. D., Khayat D., Royer C., Rouby J. J., Jacquillat C., Viars P. Functional and metabolic activity of polymorphonuclear leukocytes from patients with adult respiratory distress syndrome: results of a randomized double-blind placebo-controlled study on the activity of prostaglandin E1. Anesthesiology. 1990 Feb;72(2):276–281. doi: 10.1097/00000542-199002000-00012. [DOI] [PubMed] [Google Scholar]
  23. Schade U. F. Pentoxifylline increases survival in murine endotoxin shock and decreases formation of tumor necrosis factor. Circ Shock. 1990 Jun;31(2):171–181. [PubMed] [Google Scholar]
  24. Sevetson B. R., Kong X., Lawrence J. C., Jr Increasing cAMP attenuates activation of mitogen-activated protein kinase. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10305–10309. doi: 10.1073/pnas.90.21.10305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Smith S. R., Terminelli C., Kenworthy-Bott L., Calzetta A., Donkin J. The cooperative effects of TNF-alpha and IFN-gamma are determining factors in the ability of IL-10 to protect mice from lethal endotoxemia. J Leukoc Biol. 1994 Jun;55(6):711–718. doi: 10.1002/jlb.55.6.711. [DOI] [PubMed] [Google Scholar]
  26. Spink C. H., Yeager M. D., Feigenson G. W. Partitioning behavior of indocarbocyanine probes between coexisting gel and fluid phases in model membranes. Biochim Biophys Acta. 1990 Mar 30;1023(1):25–33. doi: 10.1016/0005-2736(90)90005-9. [DOI] [PubMed] [Google Scholar]
  27. Vane J. R. Prostaglandins as mediators of inflammation. Adv Prostaglandin Thromboxane Res. 1976;2:791–801. [PubMed] [Google Scholar]
  28. Weissmann G., Dukor P., Zurier R. B. Effect of cyclic AMP on release of lysosomal enzymes from phagocytes. Nat New Biol. 1971 Jun 2;231(22):131–135. doi: 10.1038/newbio231131a0. [DOI] [PubMed] [Google Scholar]
  29. Weissmann G., Zurier R. B., Spieler P. J., Goldstein I. M. Mechanisms of lysosomal enzyme release from leukocytes exposed to immune complexes and other particles. J Exp Med. 1971 Sep 1;134(3 Pt 2):149s–165s. [PubMed] [Google Scholar]
  30. Wu J., Dent P., Jelinek T., Wolfman A., Weber M. J., Sturgill T. W. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3',5'-monophosphate. Science. 1993 Nov 12;262(5136):1065–1069. doi: 10.1126/science.7694366. [DOI] [PubMed] [Google Scholar]
  31. Yokota M., Kambayashi J., Sakon M., Tahara H., Shiba E., Kawasaki T., Mori T. The possible involvement of platelet activation in endotoxin-induced renal insufficiency in a rabbit model. Jpn J Surg. 1991 Sep;21(5):542–546. doi: 10.1007/BF02470992. [DOI] [PubMed] [Google Scholar]
  32. Zurier R. B., Weissmann G., Hoffstein S., Kammerman S., Tai H. H. Mechanisms of lysosomal enzyme release from human leukocytes. II. Effects of cAMP and cGMP, autonomic agonists, and agents which affect microtubule function. J Clin Invest. 1974 Jan;53(1):297–309. doi: 10.1172/JCI107550. [DOI] [PMC free article] [PubMed] [Google Scholar]

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