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. 1990 Jun;58(6):1591–1599. doi: 10.1128/iai.58.6.1591-1599.1990

Signal transduction in human platelets and inflammatory mediator release induced by genetically cloned hemolysin-positive and -negative Escherichia coli strains.

B König 1, W Schönfeld 1, J Scheffer 1, W König 1
PMCID: PMC258683  PMID: 1971256

Abstract

Incubation of human platelets with the hemolysin-producing Escherichia coli strain K-12 (pANN5211) induced the activation of protein kinase C, aggregation of platelets, calcium influx, low amounts of 12-hydroxyeicosatetraenoic acid (12-HETE), and release of serotonin from dense granules. Nonhemolytic isogenic strains of E. coli 536/21 which differed only in their types of adhesins (MSH+ MS-Fim+; S-MRH+ S-Fim+; P-MRH+ P-Fim+) released neither serotonin nor 12-HETE from human platelets nor induced platelet aggregation. All hemolysin-negative bacteria except E. coli 536/21, without any adhesins, were able to activate protein kinase C reversibly but did not induce calcium influx. Activation of platelets with fluoride, an activator of the GTP-binding protein, was associated with protein kinase C activation, calcium influx, platelet aggregation, serotonin release, and 12-HETE formation. The simultaneous stimulation of platelets with NaF and the nonhemolytic E. coli strains suppressed several of the NaF-induced platelet responses. Membrane preparations isolated from stimulated platelets with hemolysin-negative and hemolysin-positive E. coli showed increased binding of guanylylimidodiphosphate, a nonhydrolyzable GTP analog, and enhanced GTPase activity.

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Selected References

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  1. 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]
  2. Bruns C., Schächtele C., Marmé D. Synthetic diacylglycerols induce a rise of quin2-detectable free intracellular calcium in human platelets. FEBS Lett. 1987 Aug 31;221(1):23–27. doi: 10.1016/0014-5793(87)80345-9. [DOI] [PubMed] [Google Scholar]
  3. Cavalieri S. J., Bohach G. A., Snyder I. S. Escherichia coli alpha-hemolysin: characteristics and probable role in pathogenicity. Microbiol Rev. 1984 Dec;48(4):326–343. doi: 10.1128/mr.48.4.326-343.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Christiansen N. O., Larsen C. S., Juhl H., Esmann V. Membrane-associated protein kinases in phorbol ester-activated human polymorphonuclear leukocytes. Biochim Biophys Acta. 1986 Oct 29;884(1):54–59. doi: 10.1016/0304-4165(86)90226-6. [DOI] [PubMed] [Google Scholar]
  6. Cochet C., Keramidas M., Souvignet C., Chambaz E. M. Phorbol ester-induced alteration of protein kinase C catalytic properties occurs at the membrane level and is not reproduced by physiological stimuli. Biochem Biophys Res Commun. 1986 Aug 14;138(3):1283–1290. doi: 10.1016/s0006-291x(86)80422-3. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hacker J., Hughes C., Hof H., Goebel W. Cloned hemolysin genes from Escherichia coli that cause urinary tract infection determine different levels of toxicity in mice. Infect Immun. 1983 Oct;42(1):57–63. doi: 10.1128/iai.42.1.57-63.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hallam T. J., Daniel J. L., Kendrick-Jones J., Rink T. J. Relationship between cytoplasmic free calcium and myosin light chain phosphorylation in intact platelets. Biochem J. 1985 Dec 1;232(2):373–377. doi: 10.1042/bj2320373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Helfman D. M., Appelbaum B. D., Vogler W. R., Kuo J. F. Phospholipid-sensitive Ca2+-dependent protein kinase and its substrates in human neutrophils. Biochem Biophys Res Commun. 1983 Mar 29;111(3):847–853. doi: 10.1016/0006-291x(83)91376-1. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Kaibuchi K., Takai Y., Sawamura M., Hoshijima M., Fujikura T., Nishizuka Y. Synergistic functions of protein phosphorylation and calcium mobilization in platelet activation. J Biol Chem. 1983 Jun 10;258(11):6701–6704. [PubMed] [Google Scholar]
  14. Kikkawa U., Takai Y., Tanaka Y., Miyake R., Nishizuka Y. Protein kinase C as a possible receptor protein of tumor-promoting phorbol esters. J Biol Chem. 1983 Oct 10;258(19):11442–11445. [PubMed] [Google Scholar]
  15. Kishimoto A., Kajikawa N., Shiota M., Nishizuka Y. Proteolytic activation of calcium-activated, phospholipid-dependent protein kinase by calcium-dependent neutral protease. J Biol Chem. 1983 Jan 25;258(2):1156–1164. [PubMed] [Google Scholar]
  16. 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]
  17. Kraft A. S., Anderson W. B. Phorbol esters increase the amount of Ca2+, phospholipid-dependent protein kinase associated with plasma membrane. Nature. 1983 Feb 17;301(5901):621–623. doi: 10.1038/301621a0. [DOI] [PubMed] [Google Scholar]
  18. Köller M., Schönfeld W., Knöller J., Bremm K. D., König W., Spur B., Crea A., Peters W. The metabolism of leukotrienes in blood plasma studied by high-performance liquid chromatography. Biochim Biophys Acta. 1985 Jan 9;833(1):128–134. doi: 10.1016/0005-2760(85)90260-7. [DOI] [PubMed] [Google Scholar]
  19. König B., König W., Scheffer J., Hacker J., Goebel W. Role of Escherichia coli alpha-hemolysin and bacterial adherence in infection: requirement for release of inflammatory mediators from granulocytes and mast cells. Infect Immun. 1986 Dec;54(3):886–892. doi: 10.1128/iai.54.3.886-892.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. König W., König B., Scheffer J., Hacker J., Goebel W. Role of cloned virulence factors (mannose-resistant haemagglutination, mannose-resistant adhesions) from uropathogenic Escherichia coli strains in the release of inflammatory mediators from neutrophils and mast cells. Immunology. 1989 Jul;67(3):401–407. [PMC free article] [PubMed] [Google Scholar]
  21. Marre R., Hacker J., Henkel W., Goebel W. Contribution of cloned virulence factors from uropathogenic Escherichia coli strains to nephropathogenicity in an experimental rat pyelonephritis model. Infect Immun. 1986 Dec;54(3):761–767. doi: 10.1128/iai.54.3.761-767.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Melloni E., Pontremoli S., Michetti M., Sacco O., Sparatore B., Horecker B. L. The involvement of calpain in the activation of protein kinase C in neutrophils stimulated by phorbol myristic acid. J Biol Chem. 1986 Mar 25;261(9):4101–4105. [PubMed] [Google Scholar]
  25. Melloni E., Pontremoli S., Michetti M., Sacco O., Sparatore B., Salamino F., Horecker B. L. Binding of protein kinase C to neutrophil membranes in the presence of Ca2+ and its activation by a Ca2+-requiring proteinase. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6435–6439. doi: 10.1073/pnas.82.19.6435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Northup J. K., Smigel M. D., Sternweis P. C., Gilman A. G. The subunits of the stimulatory regulatory component of adenylate cyclase. Resolution of the activated 45,000-dalton (alpha) subunit. J Biol Chem. 1983 Sep 25;258(18):11369–11376. [PubMed] [Google Scholar]
  29. Parkkinen J., Finne J., Achtman M., Väisänen V., Korhonen T. K. Escherichia coli strains binding neuraminyl alpha 2-3 galactosides. Biochem Biophys Res Commun. 1983 Mar 16;111(2):456–461. doi: 10.1016/0006-291x(83)90328-5. [DOI] [PubMed] [Google Scholar]
  30. Rink T. J., Sanchez A., Hallam T. J. Diacylglycerol and phorbol ester stimulate secretion without raising cytoplasmic free calcium in human platelets. Nature. 1983 Sep 22;305(5932):317–319. doi: 10.1038/305317a0. [DOI] [PubMed] [Google Scholar]
  31. Sanchez A., Hallam T. J., Rink T. J. Trifluoperazine and chlorpromazine block secretion from human platelets evoked at basal cytoplasmic free calcium by activators of C-kinase. FEBS Lett. 1983 Nov 28;164(1):43–46. doi: 10.1016/0014-5793(83)80015-5. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Scheffer J., König W., Hacker J., Goebel W. Bacterial adherence and hemolysin production from Escherichia coli induces histamine and leukotriene release from various cells. Infect Immun. 1985 Oct;50(1):271–278. doi: 10.1128/iai.50.1.271-278.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Sternweis P. C., Gilman A. G. Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4888–4891. doi: 10.1073/pnas.79.16.4888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Väisänen-Rhen V., Elo J., Väisänen E., Siitonen A., Orskov I., Orskov F., Svenson S. B., Mäkelä P. H., Korhonen T. K. P-fimbriated clones among uropathogenic Escherichia coli strains. Infect Immun. 1984 Jan;43(1):149–155. doi: 10.1128/iai.43.1.149-155.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Väisänen V., Elo J., Tallgren L. G., Siitonen A., Mäkelä P. H., Svanborg-Edén C., Källenius G., Svenson S. B., Hultberg H., Korhonen T. Mannose-resistant haemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet. 1981 Dec 19;2(8260-61):1366–1369. doi: 10.1016/s0140-6736(81)92796-3. [DOI] [PubMed] [Google Scholar]
  40. Waalwijk C., MacLaren D. M., de Graaff J. In vivo function of hemolysin in the nephropathogenicity of Escherichia coli. Infect Immun. 1983 Oct;42(1):245–249. doi: 10.1128/iai.42.1.245-249.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ware J. A., Johnson P. C., Smith M., Salzman E. W. Aequorin detects increased cytoplasmic calcium in platelets stimulated with phorbol ester or diacylglycerol. Biochem Biophys Res Commun. 1985 Nov 27;133(1):98–104. doi: 10.1016/0006-291x(85)91846-7. [DOI] [PubMed] [Google Scholar]
  42. 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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