Abstract
Human neutrophils from peripheral blood may physically interact with platelets in several settings including hemostasis, inflammation, and a variety of vascular disorders. A role for lipoxygenase (LO)-derived products has been implicated in each of these events; therefore, we investigated the formation of lipoxins during coincubation of human neutrophils and platelets. Simultaneous addition of FMLP and thrombin to coincubations of these cells led to formation of both lipoxin A4 and lipoxin B4, which were monitored by reversed-phase high pressure liquid chromatography. Neither stimulus nor cell type alone induced the formation of these products. When leukotriene A4 (LTA4), a candidate for the transmitting signal, was added to platelets, lipoxins were formed. In cell-free 100,000 g supernatants of platelet lysates, which displayed 12-LO activity, LTA4 was also transformed to lipoxins. Platelet formation of lipoxins was inhibited by the LO inhibitor esculetin and partially sensitive to chelation of Ca2+, while neither acetylsalicylic acid nor indomethacin significantly inhibited their generation. In contrast, neutrophils did not transform LTA4 to lipoxins. Cell-free 100,000 g supernatants of neutrophil lysates converted LTA4 to LTB4. These results indicate that neutrophil-platelet interactions can lead to the formation of lipoxins from endogenous sources and provide a role for platelet 12-LO in the formation of lipoxins from LTA4.
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- Audera C., Rocklin R., Vaillancourt R., Jakubowski J. A., Deykin D. Altered arachidonic acid metabolism and platelet size in atopic subjects. Clin Immunol Immunopathol. 1988 Mar;46(3):352–359. doi: 10.1016/0090-1229(88)90054-2. [DOI] [PubMed] [Google Scholar]
- Badr K. F., DeBoer D. K., Schwartzberg M., Serhan C. N. Lipoxin A4 antagonizes cellular and in vivo actions of leukotriene D4 in rat glomerular mesangial cells: evidence for competition at a common receptor. Proc Natl Acad Sci U S A. 1989 May;86(9):3438–3442. doi: 10.1073/pnas.86.9.3438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Badr K. F., Serhan C. N., Nicolaou K. C., Samuelsson B. The action of lipoxin-A on glomerular microcirculatory dynamics in the rat. Biochem Biophys Res Commun. 1987 May 29;145(1):408–414. doi: 10.1016/0006-291x(87)91337-4. [DOI] [PubMed] [Google Scholar]
- Baranes D., Matzner J., Razin E. Thrombin-induced calcium-independent degranulation of human neutrophils. Inflammation. 1986 Dec;10(4):455–461. doi: 10.1007/BF00915829. [DOI] [PubMed] [Google Scholar]
- Bizios R., Lai L., Fenton J. W., 2nd, Malik A. B. Thrombin-induced chemotaxis and aggregation of neutrophils. J Cell Physiol. 1986 Sep;128(3):485–490. doi: 10.1002/jcp.1041280318. [DOI] [PubMed] [Google Scholar]
- Brezinski M. E., Gimbrone M. A., Jr, Nicolaou K. C., Serhan C. N. Lipoxins stimulate prostacyclin generation by human endothelial cells. FEBS Lett. 1989 Mar 13;245(1-2):167–172. doi: 10.1016/0014-5793(89)80214-5. [DOI] [PubMed] [Google Scholar]
- Busija D. W., Armstead W., Leffler C. W., Mirro R. Lipoxins A4 and B4 dilate cerebral arterioles of newborn pigs. Am J Physiol. 1989 Feb;256(2 Pt 2):H468–H471. doi: 10.1152/ajpheart.1989.256.2.H468. [DOI] [PubMed] [Google Scholar]
- 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]
- Dahinden C. A., Clancy R. M., Gross M., Chiller J. M., Hugli T. E. Leukotriene C4 production by murine mast cells: evidence of a role for extracellular leukotriene A4. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6632–6636. doi: 10.1073/pnas.82.19.6632. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dahlén S. E., Raud J., Serhan C. N., Björk J., Samuelsson B. Biological activities of lipoxin A include lung strip contraction and dilation of arterioles in vivo. Acta Physiol Scand. 1987 Aug;130(4):643–647. doi: 10.1111/j.1748-1716.1987.tb08187.x. [DOI] [PubMed] [Google Scholar]
- Del Maschio A., Maclouf J., Corvazier E., Grange M. J., Borgeat P. Activated platelets stimulate human neutrophils functions. Nouv Rev Fr Hematol. 1985;27(4):275–278. [PubMed] [Google Scholar]
- Edenius C., Haeggström J., Lindgren J. A. Transcellular conversion of endogenous arachidonic acid to lipoxins in mixed human platelet-granulocyte suspensions. Biochem Biophys Res Commun. 1988 Dec 15;157(2):801–807. doi: 10.1016/s0006-291x(88)80320-6. [DOI] [PubMed] [Google Scholar]
- Feinmark S. J., Cannon P. J. Endothelial cell leukotriene C4 synthesis results from intercellular transfer of leukotriene A4 synthesized by polymorphonuclear leukocytes. J Biol Chem. 1986 Dec 15;261(35):16466–16472. [PubMed] [Google Scholar]
- Feinstein M. B., Halenda S. P. Arachidonic acid mobilization in platelets: the possible role of protein kinase C and G-proteins. Experientia. 1988 Feb 15;44(2):101–104. doi: 10.1007/BF01952189. [DOI] [PubMed] [Google Scholar]
- Funk M. O., Jr, Andre J. C., Otsuki T. Oxygenation of trans polyunsaturated fatty acids by lipoxygenase reveals steric features of the catalytic mechanism. Biochemistry. 1987 Oct 20;26(21):6880–6884. doi: 10.1021/bi00395a043. [DOI] [PubMed] [Google Scholar]
- Garrick R., Shen S. Y., Ogunc S., Wong P. Y. Transformation of leukotriene A4 to lipoxins by rat kidney mesangial cell. Biochem Biophys Res Commun. 1989 Jul 31;162(2):626–633. doi: 10.1016/0006-291x(89)92356-5. [DOI] [PubMed] [Google Scholar]
- Hamberg M., Hamberg G. On the mechanism of the oxygenation of arachidonic acid by human platelet lipoxygenase. Biochem Biophys Res Commun. 1980 Aug 14;95(3):1090–1097. doi: 10.1016/0006-291x(80)91584-3. [DOI] [PubMed] [Google Scholar]
- Jungi T. W., Spycher M. O., Nydegger U. E., Barandun S. Platelet-leukocyte interaction: selective binding of thrombin-stimulated platelets to human monocytes, polymorphonuclear leukocytes, and related cell lines. Blood. 1986 Mar;67(3):629–636. [PubMed] [Google Scholar]
- Knauer K. A., Lichtenstein L. M., Adkinson N. F., Jr, Fish J. E. Platelet activation during antigen-induced airway reactions in asthmatic subjects. N Engl J Med. 1981 Jun 4;304(23):1404–1407. doi: 10.1056/NEJM198106043042307. [DOI] [PubMed] [Google Scholar]
- Kühn H., Wiesner R., Alder L., Fitzsimmons B. J., Rokach J., Brash A. R. Formation of lipoxin B by the pure reticulocyte lipoxygenase via sequential oxygenation of the substrate. Eur J Biochem. 1987 Dec 15;169(3):593–601. doi: 10.1111/j.1432-1033.1987.tb13650.x. [DOI] [PubMed] [Google Scholar]
- Lagarde M., Croset M., Authi K. S., Crawford N. Subcellular localization and some properties of lipoxygenase activity in human blood platelets. Biochem J. 1984 Sep 1;222(2):495–500. doi: 10.1042/bj2220495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lam B. K., Serhan C. N., Samuelsson B., Wong P. Y. A phospholipase A2 isoenzyme provokes lipoxin B formation from endogenous sources of arachidonic acid in porcine leukocytes. Biochem Biophys Res Commun. 1987 Apr 14;144(1):123–131. doi: 10.1016/s0006-291x(87)80484-9. [DOI] [PubMed] [Google Scholar]
- Lefer A. M., Stahl G. L., Lefer D. J., Brezinski M. E., Nicolaou K. C., Veale C. A., Abe Y., Smith J. B. Lipoxins A4 and B4: comparison of icosanoids having bronchoconstrictor and vasodilator actions but lacking platelet aggregatory activity. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8340–8344. doi: 10.1073/pnas.85.21.8340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis R. A., Austen K. F. The biologically active leukotrienes. Biosynthesis, metabolism, receptors, functions, and pharmacology. J Clin Invest. 1984 Apr;73(4):889–897. doi: 10.1172/JCI111312. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maas R. L., Brash A. R. Evidence for a lipoxygenase mechanism in the biosynthesis of epoxide and dihydroxy leukotrienes from 15(S)-hydroperoxyicosatetraenoic acid by human platelets and porcine leukocytes. Proc Natl Acad Sci U S A. 1983 May;80(10):2884–2888. doi: 10.1073/pnas.80.10.2884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marcus A. J., Broekman M. J., Safier L. B., Ullman H. L., Islam N., Sherhan C. N., Rutherford L. E., Korchak H. M., Weissmann G. Formation of leukotrienes and other hydroxy acids during platelet-neutrophil interactions in vitro. Biochem Biophys Res Commun. 1982 Nov 16;109(1):130–137. doi: 10.1016/0006-291x(82)91575-3. [DOI] [PubMed] [Google Scholar]
- Marcus A. J., Safier L. B., Ullman H. L., Islam N., Broekman M. J., von Schacky C. Studies on the mechanism of omega-hydroxylation of platelet 12-hydroxyeicosatetraenoic acid (12-HETE) by unstimulated neutrophils. J Clin Invest. 1987 Jan;79(1):179–187. doi: 10.1172/JCI112781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Needleman P., Turk J., Jakschik B. A., Morrison A. R., Lefkowith J. B. Arachidonic acid metabolism. Annu Rev Biochem. 1986;55:69–102. doi: 10.1146/annurev.bi.55.070186.000441. [DOI] [PubMed] [Google Scholar]
- Nicolaou K. C., Marron B. E., Veale C. A., Webber S. E., Dahlén S. E., Samuelsson B., Serhan C. N. Identification of a novel 7-cis-11-trans-lipoxin A4 generated by human neutrophils: total synthesis, spasmogenic activities and comparison with other geometric isomers of lipoxins A4 and B4. Biochim Biophys Acta. 1989 May 15;1003(1):44–53. doi: 10.1016/0005-2760(89)90096-9. [DOI] [PubMed] [Google Scholar]
- Pace-Asciak C. R., Klein J., Spielberg S. P. Metabolism of leukotriene A4 into C4 by human platelets. Biochim Biophys Acta. 1986 Jun 11;877(1):68–74. doi: 10.1016/0005-2760(86)90119-0. [DOI] [PubMed] [Google Scholar]
- Palmblad J., Gyllenhammar H., Ringertz B., Serhan C. N., Samuelsson B., Nicolaou K. C. The effects of lipoxin A and lipoxin B on functional responses of human granulocytes. Biochem Biophys Res Commun. 1987 May 29;145(1):168–175. doi: 10.1016/0006-291x(87)91302-7. [DOI] [PubMed] [Google Scholar]
- Rouzer C. A., Shimizu T., Samuelsson B. On the nature of the 5-lipoxygenase reaction in human leukocytes: characterization of a membrane-associated stimulatory factor. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7505–7509. doi: 10.1073/pnas.82.22.7505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rådmark O., Malmsten C., Samuelsson B., Goto G., Marfat A., Corey E. J. Leukotriene A. Isolation from human polymorphonuclear leukocytes. J Biol Chem. 1980 Dec 25;255(24):11828–11831. [PubMed] [Google Scholar]
- Rådmark O., Shimizu T., Jörnvall H., Samuelsson B. Leukotriene A4 hydrolase in human leukocytes. Purification and properties. J Biol Chem. 1984 Oct 25;259(20):12339–12345. [PubMed] [Google Scholar]
- Samuelsson B., Dahlén S. E., Lindgren J. A., Rouzer C. A., Serhan C. N. Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science. 1987 Sep 4;237(4819):1171–1176. doi: 10.1126/science.2820055. [DOI] [PubMed] [Google Scholar]
- Schafer A. I., Turner N. A., Handin R. I. Platelet lipoxygenase-dependent oxygen burst. Evidence for differential activation of lipoxygenase in intact and disrupted human platelets. Biochim Biophys Acta. 1982 Sep 14;712(3):535–541. doi: 10.1016/0005-2760(82)90281-8. [DOI] [PubMed] [Google Scholar]
- Sekiya K., Okuda H., Arichi S. Selective inhibition of platelet lipoxygenase by esculetin. Biochim Biophys Acta. 1982 Oct 14;713(1):68–72. [PubMed] [Google Scholar]
- Sellmayer A., Strasser T., Weber P. C. Differences in arachidonic acid release, metabolism and leukotriene B4 synthesis in human polymorphonuclear leukocytes activated by different stimuli. Biochim Biophys Acta. 1987 Mar 11;927(3):417–422. doi: 10.1016/0167-4889(87)90107-8. [DOI] [PubMed] [Google Scholar]
- Serhan C. N., Hamberg M., Samuelsson B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5335–5339. doi: 10.1073/pnas.81.17.5335. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Serhan C. N., Hamberg M., Samuelsson B., Morris J., Wishka D. G. On the stereochemistry and biosynthesis of lipoxin B. Proc Natl Acad Sci U S A. 1986 Apr;83(7):1983–1987. doi: 10.1073/pnas.83.7.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Serhan C. N., Hirsch U., Palmblad J., Samuelsson B. Formation of lipoxin A by granulocytes from eosinophilic donors. FEBS Lett. 1987 Jun 15;217(2):242–246. doi: 10.1016/0014-5793(87)80671-3. [DOI] [PubMed] [Google Scholar]
- Serhan C. N., Nicolaou K. C., Webber S. E., Veale C. A., Dahlén S. E., Puustinen T. J., Samuelsson B. Lipoxin A. Stereochemistry and biosynthesis. J Biol Chem. 1986 Dec 15;261(35):16340–16345. [PubMed] [Google Scholar]
- Serhan C. N. On the relationship between leukotriene and lipoxin production by human neutrophils: evidence for differential metabolism of 15-HETE and 5-HETE. Biochim Biophys Acta. 1989 Aug 8;1004(2):158–168. doi: 10.1016/0005-2760(89)90264-6. [DOI] [PubMed] [Google Scholar]
- Shearman M. S., Naor Z., Sekiguchi K., Kishimoto A., Nishizuka Y. Selective activation of the gamma-subspecies of protein kinase C from bovine cerebellum by arachidonic acid and its lipoxygenase metabolites. FEBS Lett. 1989 Jan 30;243(2):177–182. doi: 10.1016/0014-5793(89)80125-5. [DOI] [PubMed] [Google Scholar]
- Soberman R. J., Harper T. W., Betteridge D., Lewis R. A., Austen K. F. Characterization and separation of the arachidonic acid 5-lipoxygenase and linoleic acid omega-6 lipoxygenase (arachidonic acid 15-lipoxygenase) of human polymorphonuclear leukocytes. J Biol Chem. 1985 Apr 10;260(7):4508–4515. [PubMed] [Google Scholar]
- Ueda N., Yokoyama C., Yamamoto S., Fitzsimmons B. J., Rokach J., Oates J. A., Brash A. R. Lipoxin synthesis by arachidonate 12-lipoxygenase purified from porcine leukocytes. Biochem Biophys Res Commun. 1987 Dec 31;149(3):1063–1069. doi: 10.1016/0006-291x(87)90516-x. [DOI] [PubMed] [Google Scholar]
- Walstra P., Verhagen J., Veldink G. A., Vliegenthart J. F. 12-Lipoxygenase from bovine polymorphonuclear leukocytes, an enzyme with leukotriene A4-synthase activity. Biochem Biophys Res Commun. 1987 Nov 30;149(1):258–265. doi: 10.1016/0006-291x(87)91633-0. [DOI] [PubMed] [Google Scholar]
- Walstra P., Verhagen J., Vermeer M. A., Klerks J. P., Veldink G. A., Vliegenthart J. F. Evidence for lipoxin formation by bovine polymorphonuclear leukocytes via triple dioxygenation of arachidonic acid. FEBS Lett. 1988 Feb 8;228(1):167–171. doi: 10.1016/0014-5793(88)80609-4. [DOI] [PubMed] [Google Scholar]
- Wong P. Y., Westlund P., Hamberg M., Granström E., Chao P. H., Samuelsson B. 15-Lipoxygenase in human platelets. J Biol Chem. 1985 Aug 5;260(16):9162–9165. [PubMed] [Google Scholar]
- Yokoyama C., Shinjo F., Yoshimoto T., Yamamoto S., Oates J. A., Brash A. R. Arachidonate 12-lipoxygenase purified from porcine leukocytes by immunoaffinity chromatography and its reactivity with hydroperoxyeicosatetraenoic acids. J Biol Chem. 1986 Dec 15;261(35):16714–16721. [PubMed] [Google Scholar]