Secretory Phospholipases A2 Induce β-Glucuronidase Release and IL-6 Production from Human Lung Macrophages

Journal of Immunology - Tập 164 Số 9 - Trang 4908-4915 - 2000
Massimo Triggiani1, Francescopaolo Granata1, Alfonso Oriente1, Valeria De Marino1, Marco Gentile1, Cecilia Calabrese1, Cristiana Palumbo1, Gianni Marone1
1Division of Clinical Immunology and Allergy, University of Naples Federico II, Naples, Italy

Tóm tắt

Abstract

Secretory phospholipases A2 (sPLA2s) are a group of extracellular enzymes that release fatty acids at the sn-2 position of phospholipids. Group IIA sPLA2 has been detected in inflammatory fluids, and its plasma level is increased in inflammatory diseases. To investigate a potential mechanism of sPLA2-induced inflammation we studied the effect of group IA (from cobra venom) and group IIA (human synovial) sPLA2s on human macrophages. Both sPLA2s induced a concentration- and Ca2+-dependent, noncytotoxic release of β-glucuronidase (16.2 ± 2.4% and 13.1 ± 1.5% of the total content with groups IA and IIA, respectively). Both sPLA2s also increased the rate of secretion of IL-6 and enhanced the expression of IL-6 mRNA. Preincubation of macrophages with inhibitors of the hydrolytic activity of sPLA2 or cytosolic PLA2 did not influence the release of β-glucuronidase. Incubation of macrophages with p-aminophenyl-mannopyranoside-BSA (mp-BSA), a ligand of the mannose receptor, also resulted in β-glucuronidase release. However, while preincubation of macrophages with mp-BSA had no effect on β-glucuronidase release induced by group IIA sPLA2, it enhanced that induced by group IA sPLA2. A blocking Ab anti-mannose receptor inhibited both mp-BSA- and group IIA-induced β-glucuronidase release. Taken together, these data indicate that group IA and IIA sPLA2s activate macrophages with a mechanism independent from their enzymatic activities and probably related to the activation of the mannose receptor or sPLA2-specific receptors. The secretion of enzymes and cytokines induced by sPLA2s from human macrophages may play an important role in inflammation and tissue damage associated with the release of sPLA2s.

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Tài liệu tham khảo

Waite, M.. 1990. Biochemistry, molecular biology, and physiology of phospholipase A2 and its regulatory factors: phospholipases, enzymes that share a substrate class. Adv. Exp. Med. Biol. 279: 1

Mayer, R. J., L. A. Marshall. 1993. New insights on mammalian phospholipase A2(s): comparison of arachidonoyl-selective and -nonselective enzymes. FASEB J. 7: 339

Dennis, E. A.. 1994. Diversity of group types, regulation, and function of phospholipase A2. J. Biol. Chem. 269: 13057

Tischfield, J. A.. 1997. A reassessment of the low molecular weight phospholipase A2 gene family in mammals. J. Biol. Chem. 272: 17247

Kudo, I., M. Murakami, S. Hara, K. Inoue. 1993. Mammalian non-pancreatic phospholipase A2. Biochim. Biophys. Acta 117: 217

Kramer, R. M., C. Hession, B. Johansen, G. Hayes, P. McGray, E. P. Chow, R. Tizard, R. B. Pepinsky. 1988. Structure and properties of a human non-pancreatic phospholipase A2. J. Biol. Chem. 264: 5768

Seilhamer, J. J., W. Pruzansky, P. Vadas, S. Plant, J. A. Miller, J. Kloss, L. K. Johnson. 1989. Cloning and recombinant expression of phospholipase A2 present in rheumatoid arthritic synovial fluid. J. Biol. Chem. 264: 5335

Chilton, F. H., F. J. Averill, W. C. Hubbard, A. N. Fonteh, M. Triggiani, M. C. Liu. 1996. Antigen-induced generation of lyso-phospholipids in human airways. J. Exp. Med. 183: 2235

Vadas, P., S. Wasi, H. Z. Movat, J. B. Hay. 1981. Extracellular phospholipase A2 mediates inflammatory hyperaemia. Nature 293: 583

Kini, R. M., H. J. Evans. 1989. A model to explain the pharmacological effects of snake venom phospholipase A2. Toxicon 27: 613

Bomalaski, J. S., P. Lowton, J. L. Browning. 1991. Human extracellular recombinant phospholipase A2 induces an inflammatory response in rabbit joints. J. Immunol. 146: 3904

Edelson, J. D., P. Vadas, J. Villar, J. B. M. Mullen, W. Pruzanski. 1991. Acute lung injury induced by phospholipase A2: structural and functional changes. Am. Rev. Respir. Dis. 143: 1102

Foreman-Wykert, A. K., Y. Weinrauch, P. Elsbach, J. Weiss. 1999. Cell-wall determinants of the bactericidal action of group IIA phospholipase A2 against Gram-positive bacteria. J. Clin. Invest. 103: 715

Vadas, P., W. Pruzansky. 1986. Biology of disease: role of secretory phospholipase A2 in the pathobiology of disease. Lab. Invest. 55: 391

Fonteh, A. N., D. A. Bass, L. A. Marshall, M. Seeds, J. M. Samet, F. H. Chilton. 1994. Evidence that secretory phospholipase A2 plays a role in arachidonic acid release and eicosanoid biosynthesis by mast cells. J. Immunol. 152: 5438

Takasaki, J., Y. Kawauchi, Y. Masuho. 1998. Synergistic effect of type II phospholipase A2 and platelet-activating factor on Mac-1 surface expression and exocytosis of gelatinase granules in human neutrophils: evidence for the 5-lipoxygenase-dependent mechanism. J. Immunol. 160: 5066

Serafin, W. E., K. F. Austen. 1987. Mediators of immediate hypersensitivity reactions. N. Engl. J. Med. 317: 30

Kanemasa, T., A. Arimura, J. Kishino, M. Ohtani, H. Arita. 1992. Contraction of guinea pig lung parenchyma by pancreatic type phospholipase A2 via its specific binding site. FEBS Lett. 303: 217

Kanemasa, T., K. Hanasaki, H. Arita. 1992. Migration of vascular smooth muscle cells by phospholipase A2 via specific binding sites. Biochim. Biophys. Acta 1125: 210

Fonteh, A. N., J. M. Samet, M. Surette, W. Reed, F. H. Chilton. 1998. Mechanisms that account for the selective release of arachidonic acid from intact cells by secretory phospholipase A2. Biochim. Biophys. Acta 1393: 253

Lambeau, G., P. Ancian, J. Barhanin, M. Lazdunski. 1994. Cloning and expression of a membrane receptor for secretory phospholipase A2. J. Biol. Chem. 269: 1575

Ezekowitz, R. A., K. Sastry, P. Bailly, A. Warner. 1990. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 172: 1785

Yamamoto, Y., T. W. Klein, H. Friedman. 1997. Involvement of mannose receptor in cytokine interleukin-1β (IL-1β), IL-6, granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1β (MIP-1β), MIP-2, KC responses, caused by attachment of Candida albicans to macrophages. Infect. Immun. 65: 1077

Nathan, C. F.. 1987. Secretory products of macrophages. J. Clin. Invest. 79: 319

Koch, A. E., S. L. Kunkel, J. C. Burrows, H. L. Evanoff, G. K. Haines, R. M. Pope, R. M. Strieter. 1991. Synovial tissue macrophage as a source of the chemotactic cytokine IL-8. J. Immunol. 147: 2187

Chanez, P., I. Bousquet, L. Couret, G. Cornillac, G. Barneon, P. Vic, F. B. Michel, P. Godard. 1991. Increased numbers of hypodense alveolar macrophages in patients with bronchial asthma. Am. Rev. Respir. Dis. 144: 923

Marinò, I., M. Columbo, G. Marone. 1996. The releasability of lysosomal enzymes from neutrophil leukocytes in patients with rheumatoid arthritis. Clin. Exp. Rheum. 14: 387

Triggiani, M., A. Oriente, M. C. Seeds, D. A. Bass, G. Marone, F. H. Chilton. 1995. Migration of human inflammatory cells into the lung results in the remodelling of arachidonic acid into a triglyceride pool. J. Exp. Med. 182: 1181

Triggiani, M., V. De Marino, M. Sofia, S. Faraone, G. Ambrosio, L. Carratù, G. Marone. 1997. Characterization of platelet-activating factor acetylhydrolase in human bronchoalveolar lavage. Am. J. Respir. Crit. Care Med. 156: 94

Triggiani, M., A. Oriente, G. Marone. 1994. Differential roles for triglyceride and phospholipid pools of arachidonic acid in human lung macrophages. J. Immunol. 152: 1394

Triggiani, M., D. W. Goldman, F. H. Chilton. 1991. Biological effects of 1-acyl-2-acetyl-sn-glycero-3-phosphocholine in the human neutrophil. Biochim. Biophys. Acta 1084: 41

Lowry, O., A. Rosebrough, A. Farr, R. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265

Essayan, D. M., G. Krishnaswamy, S. K. Huang. 1997. Immunologic investigations of T-cell regulation of human IgE antibody secretion and allergic responses. Methods 13: 69

Snedecor, G. W.. 1980. Statistical Methods Iowa State University Press, Ames.

Weissler, J. C., C. R. Lyons, M. F. Lipscomb, G. B. Toews. 1986. Human pulmonary macrophages: functional comparison of cells obtained from whole lung and by bronchoalveolar lavage. Am. Rev. Respir. Dis. 133: 473

Kishimoto, T.. 1989. The biology of interleukin-6. Blood 74: 1

Fleisch, J. H., C. T. Armstrong, C. R. Roman, E. D. Mihelich, S. M. Spaethe, W. T. Jackson, J. L. Bobbit, S. Draheim, N. J. Bach, L. D. Dillard, et al 1996. Recombinant human secretory phospholipase A2 released thromboxane from guinea pig bronchoalveolar lavage cells: in vitro and ex vivo evaluation of a novel secretory phospholipase A2 inhibitor. J. Pharmacol. Exp. Ther. 278: 252

Murakami, M., S. Shimbara, T. Kambe, H. Kuwata, M. V. Winstead, J. A. Tischfield, I. Kudo. 1998. The functions of five distinct phospholipase A2s in regulating arachidonic acid release: type IIA and type V secretory phospholipase A2s are functionally redundant and act in concert with cytosolic phospholipase A2. J. Biol. Chem. 273: 14411

Dubois, C., E. Bissonnette, M. Rola-Pleszczynsky. 1989. Asbestos fibers and silica particles stimulates rat alveolar macrophages to release tumor necrosis factor: autoregulatory role of leukotriene B4. Am. Rev. Respir. Dis. 139: 1257

Bartoli, F., H. K. Lin, F. Ghomaschi, M. H. Gelb, M. K. Jain, R. Apiz-Castro. 1994. Tight binding inhibitors of 85-kDa phospholipase A2 but not 14-kDa phospholipase A2 inhibit release of free arachidonate in thrombin-stimulated human platelets. J. Biol. Chem. 269: 15625

Lambeau, G., J. Barhanin, H. Schweitz, J. Quar, M. Lazdunski. 1989. Identification and properties of very high affinity brain membrane-binding sites for a neurotoxic phospholipase from the taipan venom. J. Biol. Chem. 264: 11503

Lambeau, G., A. Schmid-Alliana, M. Lazdunski, J. Barhanin. 1990. Identification of a very high affinity binding protein for toxic phospholipase A2 in skeletal muscle. J. Biol. Chem. 265: 9526

Lambeau, G., J. Barhanin, M. Lazdunski. 1991. Identification of different receptor types for toxic phospholipase A2 in rabbit skeletal muscle. FEBS Lett. 293: 29

McNally, A. K., K. M. DeFife, J. M. Anderson. 1996. Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am. J. Pathol. 149: 975

Shepherd, V. L., Y. C. Lee, H. Schlesinger, P. D. Stahl. 1981. l-fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages. Proc. Natl. Acad. Sci. USA 78: 1019

Aderem, A., D. M. Underhill. 1999. Mechanism of phagocytosis in macrophages. Annu. Rev. Immunol. 17: 593

Murakami, M., Y. Nakatami, G. Atsumi, K. Inoue, I. Kudo. 1997. Regulatory functions of phospholipase A2. Crit. Rev. Immunol. 17: 225

Hack, C. E., G. J. Wolbink, C. Schalkwijk, H. Speijer, W. T. Hermens, H. van den Bosch. 1997. A role for secretory phospholipase A2 and C-reactive protein in the removal of injured cells. Immunol. Today 18: 111

Borregaard, N., J. B. Cowland. 1997. Granules of the neutrophilic polymorphonuclear leukocyte. Blood 89: 3503

Gauldie, J., C. Richards, D. Harnish, P. Lansdorp, H. Baumann. 1987. Interferon β2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc. Natl. Acad. Sci. USA 84: 7251

Crowl, R. M., T. J. Stoller, R. R. Conroy, C. R. Stoner. 1991. Induction of phospholipase A2 gene expression in human hepatoma cells by mediators of the acute phase response. J. Biol. Chem. 266: 2647

Gilman, S. C., J. Chang, P. R. Zeigler, J. Uhl, E. Mochan. 1988. Interleukin-1 activates phospholipase A2 in human synovial cells. Arthritis Rheum. 31: 126

Wada, A., H. Tojo, T. Sugiura, Y. Fujiwara, T. Kamada, N. Ueda, M. Okamoto. 1996. Group II phospholipase A2 as an autocrine growth factor mediating interleukin-1 action on mesangial cells. Biochim. Biophys. Acta 1345: 99

Nakae, H., S. Endo, K. Inada, H. Yamashita, Y. Yamada, T. Takakuwa, T. Kasai, M. Ogawa, K. Uchida. 1995. Plasma concentrations of type II phospholipase A2, cytokines and eicosanoids in patients with burns. Burns 21: 422

Nisijima, J., M. Okamoto, M. Ogawa, G. Kosaki, T. Yamano. 1983. Purification and characterization of human pancreatic phospholipase A2 and development of a radioimmunoassay. J. Biochem. 94: 137

Nakajima, M., K. Hanasaki, M. Ueda, H. Arita. 1992. Effect of pancreatic phospholipase A2 on isolated porcine cerebral arteries via its specific binding sites. FEBS Lett. 309: 261

Murakami, M., N. Hara, I. Kudo, K. Inoue. 1993. Triggering of degranulation in mast cells by exogenous type II phospholipase A2. J. Immunol. 151: 5675

Mourier, C., B. B. Vargaftig, P. A. Franken, H. M. Verheij, C. Bon, L. Touqui. 1994. Platelet secretory phospholipase A2 fails to induce rabbit platelet activation and to release arachidonic acid in contrast with venom phospholipases A2. Biochim. Biophys. Acta 1214: 88

Kishino, J., T. Masahiro, H. Arita. 1992. Proliferative effect of phospholipase A2 in rat chondrocyte via its specific binding sites. Biochem. Biophys. Res. Commun. 186: 1025

Reddy, S. T., H. R. Herschman. 1996. Transcellular prostaglandin production following mast cell activation is mediated by proximal secretory phospholipase A2 and distal prostaglandin synthase 1. J. Biol. Chem. 271: 186

Nicolas, J. P., G. Lambeau, M. Lazdunski. 1995. Identification of the binding domain for secretory phospholipases A2 on their M-type 180-kDa membrane receptor. J. Biol. Chem. 270: 28869

Jiang, W., W. J. Swiggard, C. Heufler, Y. Peng, A. Mirza, R. M. Steinman, M. C. Nussenzweig. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375: 151

Mukhopadhyay, A., P. Stahl. 1995. Bee venom phospholipase A2 is recognized by the macrophage mannose receptor. Arch. Biochem. Biophys. 324: 78