Research Article
Crystal-induced neutrophil activation: VIII. Immediate production of prostaglandin E2 mediated by constitutive cyclooxygenase 2 in human neutrophils stimulated by urate crystals
Caroline Gilbert, Patrice E. Poubelle, Pierre Borgeat, Marc Pouliot, Paul H. Naccache,
Corresponding Author
Paul H. Naccache
Laval University, Ste-Foy, Quebec, Canada
CHUL, Room T1-49, 2705 Boulevard Laurier, Ste-Foy, Quebec G1V 4G2, CanadaSearch for more papers by this authorCaroline Gilbert, Patrice E. Poubelle, Pierre Borgeat, Marc Pouliot, Paul H. Naccache,
Corresponding Author
Paul H. Naccache
Laval University, Ste-Foy, Quebec, Canada
CHUL, Room T1-49, 2705 Boulevard Laurier, Ste-Foy, Quebec G1V 4G2, CanadaSearch for more papers by this authorAbstract
Objective
To evaluate the impact of monosodium urate monohydrate (MSUM) crystals on the synthesis of prostaglandin E2 (PGE2) by human neutrophils, and to examine some of the mechanisms underlying these responses.
Methods
The amount of PGE2 released in the supernatants of stimulated human neutrophils was evaluated by enzyme immunoassay, and expression of cyclooxygenase 2 (COX-2) was monitored by immunoblot on cell lysates, as well as by cytofluorometry of buffy-coat cells.
Results
We observed that MSUM crystals rapidly stimulated the synthesis of PGE2, with levels peaking at 1 hour. This response was decreased by NS-398, a specific inhibitor of COX-2. We also detected a constitutive expression of COX-2 in unstimulated and unprimed neutrophils. This rapid COX-2–dependent PGE2 accumulation was independent of translation and transcription. We also observed that piceatannol, but not colchicine, blocked the synthesis of PGE2 stimulated by MSUM crystals.
Conclusion
These results show that the interaction of MSUM crystals with human neutrophils stimulates a significant synthesis of PGE2 mediated by constitutively expressed COX-2. The results of this study emphasize the potential importance of the neutrophil as a source of PGE2, which may modulate, positively or negatively, the inflammatory response.
REFERENCES
- 1 Ginsberg MH, Kozin F, Chow D, May J, Skosey JL. Adsorption of polymorphonuclear leukocyte lysosomal enzymes to monosodium urate crystals. Arthritis Rheum 1977; 20: 1538–42.
- 2 Guerne PA, Terkeltaub R, Zuraw B, Lotz M. Inflammatory microcrystals stimulate interleukin-6 production and secretion by human monocytes and synoviocytes. Arthritis Rheum 1989; 32: 1443–52.
- 3 Pouliot M, James MJ, McColl SR, Naccache PH, Cleland LG. Monosodium urate microcrystals induce cyclooxygenase-2 in human monocytes. Blood 1998; 91: 1769–76.
- 4 Bouchard L, de Medicis R, Lussier A, Naccache PH, Poubelle PE. Inflammatory microcrystals alter the functional phenotype of human osteoblast-like cells in vitro: synergism with IL-1 to overexpress cyclooxygenase-2. J Immunol 2002; 168: 5310–7.
- 5 McCarty DJ Jr. The inflammatory reaction to microcrystalline sodium urate. Arthritis Rheum 1965; 8: 726–35.
- 6 Seegmiller JE, Howell RR, Malawista SE. The inflammatory reaction to sodium urate. JAMA 1962; 180: 469–75.
- 7 Chang YH, Garalla EJ. Suppression of urate crystal–induced canine joint inflammation by heterologous anti–polymorphonuclear leukocyte serum. Arthritis Rheum 1968; 11: 145–50.
- 8 Phelps P, McCarty DJ. Crystal-induced inflammation in canine joints. II. Importance of polymorphonuclear leukocytes. J Exp Med 1966; 124: 115–26.
- 9 Rae SA, Davidson EM, Smith MJ. Leukotriene B4, an inflammatory mediator in gout. Lancet 1982; 2: 1122–4.
- 10 Serhan CN, Lundberg U, Weissmann G, Samuelsson B. Formation of leukotrienes and hydroxy acids by human neutrophils and platelets exposed to monosodium urate. Prostaglandins 1984; 27: 563–81.
- 11 Poubelle PE, de Medicis R, Naccache PH. Monosodium urate and calcium pyrophosphate crystals differentially activate the excitation-response coupling sequence of human neutrophils. Biochem Biophys Res Commun 1987; 149: 649–57.
- 12 Roberge CJ, de Medicis R, Dayer JM, Rola-Pleszczynski M, Naccache PH, Poubelle PE. Crystal-induced neutrophil activation. V. Differential production of biologically active IL-1 and IL-1 receptor antagonist. J Immunol 1994; 152: 5485–94.
- 13 Hachicha M, Naccache PH, McColl SR. Inflammatory microcrystals differentially regulate the secretion of macrophage inflammatory protein 1 and interleukin 8 by human neutrophils: a possible mechanism of neutrophil recruitment to sites of inflammation in synovitis. J Exp Med 1995; 182: 2019–25.
- 14 Simchowitz L, Atkinson JP, Spilberg I. Stimulation of the respiratory burst in human neutrophils by crystal phagocytosis. Arthritis Rheum 1982; 25: 181–8.
- 15 Naccache PH, Grimard M, Roberge CJ, Gilbert C, Lussier A, de Medicis R, et al. Crystal-induced neutrophil activation. I. Initiation and modulation of calcium mobilization and superoxide production by microcrystals. Arthritis Rheum 1991; 34: 333–42.
- 16 Bomalaski JS, Baker DG, Brophy LM, Clark MA. Monosodium urate crystals stimulate phospholipase A2 enzyme activities and the synthesis of a phospholipase A2–activating protein. J Immunol 1990; 145: 3391–7.
- 17 Naccache PH, Bourgoin S, Plante E, Roberge CJ, de Medicis R, Lussier A, et al. Crystal-induced neutrophil activation. II. Evidence for the activation of a phosphatidylcholine-specific phospholipase D. Arthritis Rheum 1993; 36: 117–25.
- 18 Burt HM, Jackson JK, Salari H. Inhibition of crystal-induced neutrophil activation by a protein tyrosine kinase inhibitor. J Leukoc Biol 1994; 55: 112–9.
- 19 Onello E, Traynor-Kaplan A, Sklar L, Terkeltaub R. Mechanism of neutrophil activation by an unopsonized inflammatory particulate: monosodium urate crystals induce pertussis toxin–insensitive hydrolysis of phosphatidylinositol 4,5-biphosphate. J Immunol 1991; 146: 4289–94.
- 20 Burt HM, Jackson JK, Dryden P, Salari H. Crystal-induced protein tyrosine phosphorylation in neutrophils and the effect of a tyrosine kinase inhibitor on neutrophil responses. Mol Pharmacol 1993; 43: 30–6.
- 21 Gaudry M, Roberge CJ, de Medicis R, Lussier A, Poubelle PE, Naccache PH. Crystal-induced neutrophil activation. III. Inflammatory microcrystals induce a distinct pattern of tyrosine phosphorylation in human neutrophils. J Clin Invest 1993; 91: 1649–55.
- 22 Desaulniers P, Fernandes M, Gilbert C, Bourgoin SG, Naccache PH. Crystal-induced neutrophil activation. VII. Involvement of Syk in the responses to monosodium urate crystals. J Leukoc Biol 2001; 70: 659–68.
- 23 Roberge CJ, Gaudry M, de Medicis R, Lussier A, Poubelle PE, Naccache PH. Crystal-induced neutrophil activation. IV. Specific inhibition of tyrosine phosphorylation by colchicine. J Clin Invest 1993; 92: 1722–9.
- 24 Barabe F, Gilbert C, Liao N, Bourgoin SG, Naccache PH. Crystal-induced neutrophil activation. VI. Involvement of FcγRIIIB (CD16) and CD11b in response to inflammatory microcrystals. FASEB J 1998; 12: 209–20.
- 25 McColl S, Naccache P. Crystal-induced arthropathies. In: JI Gallin, R Snyderman, editors. Inflammation: basic principles and clinical correlates. Vol. 65. Philadelphia: Lippincott Williams & Wilkins; 1999. p. 1039–45.
- 26 Wigley FM, Fine IT, Newcombe DS. The role of the human synovial fibroblast in monosodium urate crystal–induced synovitis. J Rheumatol 1983; 10: 602–11.
- 27 Weissmann G, Smolen JE, Korchak H. Prostaglandins and inflammation: receptor/cyclase coupling as an explanation of why PGEs and PGI2 inhibit functions of inflammatory cells. Adv Prostaglandin Thromboxane Res 1980; 8: 1637–53.
- 28 Weissmann G, Serhan C, Korchak HM, Smolen JE. Mechanisms of mediator release from neutrophils. Adv Exp Med Biol 1984; 172: 527–52.
- 29 Weissmann G, Hoffstein S, Korchak H, Smolen JE. The earliest membrane responses to phagocytosis: membrane potential changes and Ca++ loss in human granulocytes. Trans Assoc Am Physicians 1978; 91: 90–103.
- 30 Maloney CG, Kutchera WA, Albertine KH, McIntyre TM, Prescott SM, Zimmerman GA. Inflammatory agonists induce cyclooxygenase type 2 expression by human neutrophils. J Immunol 1998; 160: 1402–10.
- 31 Pouliot M, Gilbert C, Borgeat P, Poubelle PE, Bourgoin S, Créminon C, et al. Expression and activity of prostanglandin endoperoxide synthase-2 in agonist-activated human neutrophils. FASEB J 1998; 12: 1109–23.
- 32 Yu CL, Huang MH, Kung YY, Tsai CY, Tsai YY, Tsai ST, et al. Interleukin-13 increases prostaglandin E2 (PGE2) production by normal human polymorphonuclear neutrophils by enhancing cyclooxygenase 2 (COX-2) gene expression. Inflamm Res 1998; 47: 167–73.
- 33 Kim JS, Kim JM, Jung HC, Song IS. Expression of cyclooxygenase-2 in human neutrophils activated by Helicobacter pylori water-soluble proteins: possible involvement of NF-κB and MAP kinase signaling pathway. Dig Dis Sci 2001; 46: 2277–84.
- 34 Roberge CJ, Gaudry M, Gilbert C, Malawista SE, de Medicis R, Lussier A, et al. Paradoxical effects of colchicine on the activation of human neutrophils by chemotactic factors and inflammatory microcrystal. J Leukoc Biol 1996; 59: 864–71.
- 35
Borgeat P,
Picard S,
Dallaire N,
Pouliot M,
Surette ME.
Quantitative studies of the lipid mediators of inflammation using liquid chromatography-electrospray mass spectrometry. In:
CN Serhan,
PA Ward, editors.
Molecular and cellular basis of inflammation.
Humana Press:
Totowa (NJ);
1999. p.
275–88.
10.1007/978-1-59259-253-1_13 Google Scholar
- 36 Borgeat P, Picard S, Battistini B, Sirois P. Measurements of arachidonic acid metabolites derived from the lipoxygenase pathways by high-pressure liquid chromatography. In: IM Bird, editor. Phospholipid and cell signaling protocols. Vol. 105. Humana Press: Totowa (NJ); 1998. p. 209.
- 37 McCarty DJ. Pathogenesis and treatment of the acute attack of gout. Clin Orthop 1970; 71: 28–39.
- 38 Ehrenfeld M, Levy M, Bar Eli M, Gallily R, Eliakim M. Effect of colchicine on polymorphonuclear leucocyte chemotaxis in human volunteers. Br J Clin Pharmacol 1980; 10: 297–300.
- 39 McCarty DJ. Crystal-induced inflammation of the joints. Annu Rev Med 1970; 21: 357–66.
- 40 Ortiz-Bravo E, Schumacher HR Jr. Components generated locally as well as serum alter the phlogistic effect of monosodium urate crystals in vivo. J Rheumatol 1993; 20: 1162–6.
- 41 Ortiz-Bravo E, Sieck MS, Schumacher HR Jr. Changes in the proteins coating monosodium urate crystals during active and subsiding inflammation: immunogold studies of synovial fluid from patients with gout and of fluid obtained using the rat subcutaneous air pouch model. Arthritis Rheum 1993; 36: 1274–85.
- 42 Cherian PV, Schumacher HR Jr. Immunochemical and ultrastructural characterization of serum proteins associated with monosodium urate crystals in synovial fluid cells from patients with gout. Ultrastruct Pathol 1986; 10: 209–19.
- 43 Borgeat P, Samuelsson B. Metabolism of arachidonic acid in polymorphonuclear leukocytes: structural analysis of novel hydroxylated compounds. J Biol Chem 1979; 254: 7865–9.
- 44 Zurier RB. Prostaglandin release from human polymorphonuclear leukocytes. Adv Prostaglandin Thromboxane Res 1976; 2: 815–8.
- 45 Goldstein IM, Malmsten CL, Samuelsson B, Weissmann G. Prostaglandins, thromboxanes, and polymorphonuclear leukocytes: mediation and modulation of inflammation. Inflammation 1977; 2: 309–17.
- 46 Kaufmann WE, Worley PF, Pegg J, Bremer M, Isakson P. COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex. Proc Natl Acad Sci U S A 1996; 93: 2317–21.
- 47 Walenga RW, Kester M, Coroneos E, Butcher S, Dwivedi R, Statt C. Constitutive expression of prostaglandin endoperoxide G/H synthetase (PGHS)-2 but not PGHS-1 in human tracheal epithelial cells in vitro. Prostaglandins 1996; 52: 341–59.
- 48 Harris RC, McKanna JA, Akai Y, Jacobson HR, Dubois RN, Breyer MD. Cyclooxygenase-2 is associated with the macula densa of rat kidney and increases with salt restriction. J Clin Invest 1994; 94: 2504–10.
- 49 Margalit A, Hauser SD, Isakson PC. Regulation of in vivo prostaglandin biosynthesis by glutathione. Adv Exp Med Biol 1999; 469: 165–8.
- 50 Crowley MT, Costello PS, Fitzer-Attas CJ, Turner M, Meng F, Lowell C, et al. A critical role for Syk in signal transduction and phagocytosis mediated by Fcγ receptors on macrophages. J Exp Med 1997; 186: 1027–39.
- 51 Kiefer F, Brumell J, Al-Alawi N, Latour S, Cheng A, Veillette A, et al. The Syk protein tyrosine kinase is essential for Fcγ receptor signaling in macrophages and neutrophils. Mol Cell Biol 1998; 18: 4209–20.
- 52 Naccache PH, Jean N, Liao NW, Bator JM, McColl SR, Kubes P. Regulation of stimulated integrin surface expression in human neutrophils by tyrosine phosphorylation. Blood 1994; 84: 616–24.
- 53 Fuortes M, Jin WW, Nathan C. Adhesion-dependent protein tyrosine phosphorylation in neutrophils treated with tumor necrosis factor. J Cell Biol 1993; 120: 777–84.
- 54 Gaudry M, Caon AC, Gilbert C, Lille S, Naccache PH. Evidence for the involvement of tyrosine kinases in the locomotory responses of human neutrophils. J Leukoc Biol 1992; 51: 103–8.
- 55 Gaudry M, Gilbert C, Barabe F, Poubelle PE, Naccache PH. Activation of Lyn is a common element of the stimulation of human neutrophils by soluble and particulate agonists. Blood 1995; 86: 3567–74.
- 56 Naccache PH, Gilbert C, Barabe F, Al-Shami A, Mahana W, Bourgoin SG. Agonist-specific tyrosine phosphorylation of Cbl in human neutrophils. J Leukoc Biol 1997; 62: 901–10.
- 57 Gilbert C, Barabe F, Rollet-Labelle E, Bourgoin SG, McColl SR, Damaj BB, et al. Evidence for a role for SAM68 in the responses of human neutrophils to ligation of CD32 and to monosodium urate crystals. J Immunol 2001; 166: 4664–71.
- 58 Glaser KB, Sung A, Bauer J, Weichman BM. Regulation of eicosanoid biosynthesis in the macrophage: involvement of protein tyrosine phosphorylation and modulation by selective protein tyrosine kinase inhibitors. Biochem Pharmacol 1993; 45: 711–21.
- 59 Taylor JA, Karas JL, Ram MK, Green OM, Seidel-Dugan C. Activation of the high-affinity immunoglobulin E receptor Fc epsilon RI in RBL-2H3 cells is inhibited by Syk SH2 domains. Mol Cell Biol 1995; 15: 4149–57.
- 60 Hirasawa N, Scharenberg A, Yamamura H, Beaven MA, Kinet JP. A requirement for Syk in the activation of the microtubule-associated protein kinase/phospholipase A2 pathway by Fc epsilon R1 is not shared by a G protein–coupled receptor. J Biol Chem 1995; 270: 10960–7.
- 61 Shefler I, Sagi-Eisenberg R. Gi-mediated activation of the Syk kinase by the receptor mimetic basic secretagogues of mast cells: role in mediating arachidonic acid/metabolites release. J Immunol 2001; 167: 475–81.
- 62 Subbaramaiah K, Chung WJ, Michaluart P, Telang N, Tanabe T, Inoue H, et al. Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester–treated human mammary epithelial cells. J Biol Chem 1998; 273: 21875–82.
- 63 Waffo-Teguo P, Hawthorne ME, Cuendet M, Merillon JM, Kinghorn AD, Pezzuto JM, et al. Potential cancer-chemopreventive activities of wine stilbeonoids and flavans extracted from grape (Vitis vinifera) cell cultures. Nutr Cancer 2001; 40: 173–9.
- 64 Schumacher HR Jr, Boice JA, Daikh DI, Mukhopadhyay S, Malmstrom K, Ng J, et al. Randomised double blind trial of etoricoxib and indometacin in treatment of acute gouty arthritis. BMJ 2002; 324: 1488–92.
