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. 1992 Aug;60(8):3150–3155. doi: 10.1128/iai.60.8.3150-3155.1992

Induction of inflammatory mediator release (serotonin and 12-hydroxyeicosatetraenoic acid) from human platelets by Pseudomonas aeruginosa glycolipid.

B König 1, U Bergmann 1, W König 1
PMCID: PMC257295  PMID: 1639485

Abstract

Purified glycolipid from Pseudomonas aeruginosa induced the generation of significant amounts of 12-hydroxyeicosatetraenoic acid (12-HETE) and serotonin release from human platelets. The release of serotonin was first observed 2 min after addition of the glycolipid and increased with time. Significant serotonin release was obtained at glycolipid concentrations above 5 micrograms/ml and increased dose-dependently up to 100% at glycolipid concentrations above 40 micrograms/ml. Glycolipid induced 12-HETE in a time- and dose-dependent manner. 12-HETE formation was first measured after 10 min of incubation and increased with time. Optimal 12-HETE formation was obtained at a glycolipid concentration of 50 micrograms/ml; higher concentrations of glycolipid led to a decrease in 12-HETE formation, indicating a cytotoxic effect. Stimulation of platelets with glycolipid (12-HETE formation and serotonin release) was accompanied by calcium influx, translocation of protein kinase C, activation of guanylylimidodiphosphate binding, and increased GTPase activity in platelet membranes within the same concentration range.

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Selected References

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  1. Arturson G. Neutrophil granulocyte functions in severely burned patients. Burns Incl Therm Inj. 1985 Jun;11(5):309–319. doi: 10.1016/0305-4179(85)90093-2. [DOI] [PubMed] [Google Scholar]
  2. Bergmann U., Scheffer J., Köller M., Schönfeld W., Erbs G., Müller F. E., König W. Induction of inflammatory mediators (histamine and leukotrienes) from rat peritoneal mast cells and human granulocytes by Pseudomonas aeruginosa strains from burn patients. Infect Immun. 1989 Jul;57(7):2187–2195. doi: 10.1128/iai.57.7.2187-2195.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berka R. M., Gray G. L., Vasil M. L. Studies of phospholipase C (heat-labile hemolysin) in Pseudomonas aeruginosa. Infect Immun. 1981 Dec;34(3):1071–1074. doi: 10.1128/iai.34.3.1071-1074.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berka R. M., Vasil M. L. Phospholipase C (heat-labile hemolysin) of Pseudomonas aeruginosa: purification and preliminary characterization. J Bacteriol. 1982 Oct;152(1):239–245. doi: 10.1128/jb.152.1.239-245.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bigay J., Deterre P., Pfister C., Chabre M. Fluoride complexes of aluminium or beryllium act on G-proteins as reversibly bound analogues of the gamma phosphate of GTP. EMBO J. 1987 Oct;6(10):2907–2913. doi: 10.1002/j.1460-2075.1987.tb02594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bigby T. D., Meslier N. Transcellular lipoxygenase metabolism between monocytes and platelets. J Immunol. 1989 Sep 15;143(6):1948–1954. [PubMed] [Google Scholar]
  7. Bokoch G. M., Parkos C. A. Identification of novel GTP-binding proteins in the human neutrophil. FEBS Lett. 1988 Jan 18;227(1):66–70. doi: 10.1016/0014-5793(88)81415-7. [DOI] [PubMed] [Google Scholar]
  8. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 1990 Nov 8;348(6297):125–132. doi: 10.1038/348125a0. [DOI] [PubMed] [Google Scholar]
  9. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  10. Bray M. A. Leukotrienes in inflammation. Agents Actions. 1986 Oct;19(1-2):87–99. doi: 10.1007/BF01977263. [DOI] [PubMed] [Google Scholar]
  11. Brom C., Köller M., Brom J., König W. Effect of sodium fluoride on the generation of lipoxygenase products from human polymorphonuclear granulocytes, mononuclear cells and platelets--indication for the involvement of G proteins. Immunology. 1989 Oct;68(2):240–246. [PMC free article] [PubMed] [Google Scholar]
  12. Charo I. F., Feinman R. D., Detwiler T. C. Inhibition of platelet secretion by an antagonist of intracellular calcium. Biochem Biophys Res Commun. 1976 Oct 18;72(4):1462–1467. doi: 10.1016/s0006-291x(76)80178-7. [DOI] [PubMed] [Google Scholar]
  13. Chester I. R., Meadow P. M. Heterogeneity of the lipopolysaccharide from Pseudomonas aeruginosa. Eur J Biochem. 1975 Oct 15;58(2):273–282. doi: 10.1111/j.1432-1033.1975.tb02373.x. [DOI] [PubMed] [Google Scholar]
  14. Coussens L., Parker P. J., Rhee L., Yang-Feng T. L., Chen E., Waterfield M. D., Francke U., Ullrich A. Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. Science. 1986 Aug 22;233(4766):859–866. doi: 10.1126/science.3755548. [DOI] [PubMed] [Google Scholar]
  15. Coutinho I. R., Berk R. S., Mammen E. Platelet aggregation by a phospholipase C from Pseudomonas aeruginosa. Thromb Res. 1988 Sep 1;51(5):495–505. doi: 10.1016/0049-3848(88)90115-6. [DOI] [PubMed] [Google Scholar]
  16. Darveau R. P., Hancock R. E. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J Bacteriol. 1983 Aug;155(2):831–838. doi: 10.1128/jb.155.2.831-838.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Döring G. Host response to Pseudomonas aeruginosa. Acta Paediatr Scand Suppl. 1989;363:37–40. doi: 10.1111/apa.1989.78.s363.37. [DOI] [PubMed] [Google Scholar]
  18. Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  20. Goetzl E. J., Woods J. M., Gorman R. R. Stimulation of human eosinophil and neutrophil polymorphonuclear leukocyte chemotaxis and random migration by 12-L-hydroxy-5,8,10,14-eicosatetraenoic acid. J Clin Invest. 1977 Jan;59(1):179–183. doi: 10.1172/JCI108617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  22. HAUSER G., KARNOVSKY M. L. Studies on the production of glycolipide by Pseudomonas aeruginosa. J Bacteriol. 1954 Dec;68(6):645–654. doi: 10.1128/jb.68.6.645-654.1954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hamberg M., Samuelsson B. Prostaglandin endoperoxides. Novel transformations of arachidonic acid in human platelets. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3400–3404. doi: 10.1073/pnas.71.9.3400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hansbrough J. F., Carroll W. B., Zapata-Sirvent R. L., Reller B. R., Boswick J. A. Identification and antibiotic susceptibility of bacterial isolates from burned patients. Burns Incl Therm Inj. 1985 Aug;11(6):393–403. doi: 10.1016/0305-4179(85)90143-3. [DOI] [PubMed] [Google Scholar]
  25. Housey G. M., O'Brian C. A., Johnson M. D., Kirschmeier P., Weinstein I. B. Isolation of cDNA clones encoding protein kinase C: evidence for a protein kinase C-related gene family. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1065–1069. doi: 10.1073/pnas.84.4.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Houslay M. D., Bojanic D., Gawler D., O'Hagan S., Wilson A. Thrombin, unlike vasopressin, appears to stimulate two distinct guanine nucleotide regulatory proteins in human platelets. Biochem J. 1986 Aug 15;238(1):109–113. doi: 10.1042/bj2380109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Huang F. L., Yoshida Y., Nakabayashi H., Knopf J. L., Young W. S., 3rd, Huang K. P. Immunochemical identification of protein kinase C isozymes as products of discrete genes. Biochem Biophys Res Commun. 1987 Dec 31;149(3):946–952. doi: 10.1016/0006-291x(87)90500-6. [DOI] [PubMed] [Google Scholar]
  28. Johnson M. K., Boese-Marrazzo D. Production and properties of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun. 1980 Sep;29(3):1028–1033. doi: 10.1128/iai.29.3.1028-1033.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Knöller J., Schönfeld W., Köller M., Hensler T., König W. Arachidonic acid metabolites from polymorphonuclear leukocytes of healthy donors, severely burned patients and children with cystic fibrosis--routine monitoring by high-performance liquid chromatography. J Chromatogr. 1988 Jun 3;427(2):199–208. doi: 10.1016/0378-4347(88)80122-1. [DOI] [PubMed] [Google Scholar]
  30. Kosaka Y., Ogita K., Ase K., Nomura H., Kikkawa U., Nishizuka Y. The heterogeneity of protein kinase C in various rat tissues. Biochem Biophys Res Commun. 1988 Mar 30;151(3):973–981. doi: 10.1016/s0006-291x(88)80461-3. [DOI] [PubMed] [Google Scholar]
  31. Kurioka S., Liu P. V. Effect of the hemolysin of Pseudomonas aeruginosa on phosphatides and on phospholipase c activity. J Bacteriol. 1967 Feb;93(2):670–674. doi: 10.1128/jb.93.2.670-674.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Köller M., König W. 12-Hydroxyeicosatetraenoic acid (12-HETE) induces heat shock proteins in human leukocytes. Biochem Biophys Res Commun. 1991 Mar 29;175(3):804–809. doi: 10.1016/0006-291x(91)91636-q. [DOI] [PubMed] [Google Scholar]
  33. Köller M., König W., Brom J., Erbs G., Müller F. E. Studies on the mechanisms of granulocyte dysfunctions in severely burned patients--evidence for altered leukotriene generation. J Trauma. 1989 Apr;29(4):435–445. doi: 10.1097/00005373-198904000-00004. [DOI] [PubMed] [Google Scholar]
  34. König B., Schönfeld W., Scheffer J., König W. Signal transduction in human platelets and inflammatory mediator release induced by genetically cloned hemolysin-positive and -negative Escherichia coli strains. Infect Immun. 1990 Jun;58(6):1591–1599. doi: 10.1128/iai.58.6.1591-1599.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. König W., Schönfeld W., Raulf M., Köller M., Knöller J., Scheffer J., Brom J. The neutrophil and leukotrienes--role in health and disease. Eicosanoids. 1990;3(1):1–22. [PubMed] [Google Scholar]
  36. Marom Z., Shelhamer J. H., Kaliner M. Effects of arachidonic acid, monohydroxyeicosatetraenoic acid and prostaglandins on the release of mucous glycoproteins from human airways in vitro. J Clin Invest. 1981 Jun;67(6):1695–1702. doi: 10.1172/JCI110207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Massini P., Lüscher E. F. On the significance of the influx of calcium ions into stimulated human blood platelets. Biochim Biophys Acta. 1976 Jul 1;436(3):652–663. doi: 10.1016/0005-2736(76)90447-8. [DOI] [PubMed] [Google Scholar]
  38. Matsumoto T., Molski T. F., Kanaho Y., Becker E. L., Sha'afi R. I. G-protein dissociation, GTP-GDP exchange and GTPase activity in control and PMA treated neutrophils stimulated by fMet-Leu-Phe. Biochem Biophys Res Commun. 1987 Mar 13;143(2):489–498. doi: 10.1016/0006-291x(87)91380-5. [DOI] [PubMed] [Google Scholar]
  39. Meyers D. J., Berk R. S. Characterization of phospholipase C from Pseudomonas aeruginosa as a potent inflammatory agent. Infect Immun. 1990 Mar;58(3):659–666. doi: 10.1128/iai.58.3.659-666.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Moran K., Munster A. M. Alterations of the host defense mechanism in burned patients. Surg Clin North Am. 1987 Feb;67(1):47–56. doi: 10.1016/s0039-6109(16)44132-0. [DOI] [PubMed] [Google Scholar]
  41. Naka M., Nishikawa M., Adelstein R. S., Hidaka H. Phorbol ester-induced activation of human platelets is associated with protein kinase C phosphorylation of myosin light chains. Nature. 1983 Dec 1;306(5942):490–492. doi: 10.1038/306490a0. [DOI] [PubMed] [Google Scholar]
  42. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
  43. OSBORN M. J. STUDIES ON THE GRAM-NEGATIVE CELL WALL. I. EVIDENCE FOR THE ROLE OF 2-KETO- 3-DEOXYOCTONATE IN THE LIPOPOLYSACCHARIDE OF SALMONELLA TYPHIMURIUM. Proc Natl Acad Sci U S A. 1963 Sep;50:499–506. doi: 10.1073/pnas.50.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pedersen S. S., Kharazmi A., Espersen F., Høiby N. Pseudomonas aeruginosa alginate in cystic fibrosis sputum and the inflammatory response. Infect Immun. 1990 Oct;58(10):3363–3368. doi: 10.1128/iai.58.10.3363-3368.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Pier G. B. Pulmonary disease associated with Pseudomonas aeruginosa in cystic fibrosis: current status of the host-bacterium interaction. J Infect Dis. 1985 Apr;151(4):575–580. doi: 10.1093/infdis/151.4.575. [DOI] [PubMed] [Google Scholar]
  46. Sano K., Takai Y., Yamanishi J., Nishizuka Y. A role of calcium-activated phospholipid-dependent protein kinase in human platelet activation. Comparison of thrombin and collagen actions. J Biol Chem. 1983 Feb 10;258(3):2010–2013. [PubMed] [Google Scholar]
  47. Schächtele C., Seifert R., Osswald H. Stimulus-dependent inhibition of platelet aggregation by the protein kinase C inhibitors polymyxin B, H-7 and staurosporine. Biochem Biophys Res Commun. 1988 Feb 29;151(1):542–547. doi: 10.1016/0006-291x(88)90628-6. [DOI] [PubMed] [Google Scholar]
  48. Spector A. A., Gordon J. A., Moore S. A. Hydroxyeicosatetraenoic acids (HETEs). Prog Lipid Res. 1988;27(4):271–323. doi: 10.1016/0163-7827(88)90009-4. [DOI] [PubMed] [Google Scholar]
  49. Stenson W. F., Parker C. W. Monohydroxyeicosatetraenoic acids (HETEs) induce degranulation of human neutrophils. J Immunol. 1980 May;124(5):2100–2104. [PubMed] [Google Scholar]
  50. Syldatk C., Lang S., Wagner F., Wray V., Witte L. Chemical and physical characterization of four interfacial-active rhamnolipids from Pseudomonas spec. DSM 2874 grown on n-alkanes. Z Naturforsch C. 1985 Jan-Feb;40(1-2):51–60. doi: 10.1515/znc-1985-1-212. [DOI] [PubMed] [Google Scholar]
  51. Tapley P. M., Murray A. W. Evidence that treatment of platelets with phorbol ester causes proteolytic activation of Ca2+-activated, phospholipid-dependent protein kinase. Eur J Biochem. 1985 Sep 2;151(2):419–423. doi: 10.1111/j.1432-1033.1985.tb09118.x. [DOI] [PubMed] [Google Scholar]
  52. Tsien R. Y., Pozzan T., Rink T. J. Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol. 1982 Aug;94(2):325–334. doi: 10.1083/jcb.94.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wood R. E., Boat T. F., Doershuk C. F. Cystic fibrosis. Am Rev Respir Dis. 1976 Jun;113(6):833–878. doi: 10.1164/arrd.1976.113.6.833. [DOI] [PubMed] [Google Scholar]
  54. Woods D. E., Schaffer M. S., Rabin H. R., Campbell G. D., Sokol P. A. Phenotypic comparison of Pseudomonas aeruginosa strains isolated from a variety of clinical sites. J Clin Microbiol. 1986 Aug;24(2):260–264. doi: 10.1128/jcm.24.2.260-264.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yamanishi J., Takai Y., Kaibuchi K., Sano K., Castagna M., Nishizuka Y. Synergistic functions of phorbol ester and calcium in serotonin release from human platelets. Biochem Biophys Res Commun. 1983 Apr 29;112(2):778–786. doi: 10.1016/0006-291x(83)91529-2. [DOI] [PubMed] [Google Scholar]

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