Neutrophil P-selectin-glycoprotein-ligand-1 binding to platelet P-selectin enhances metalloproteinase 2 secretion and platelet-neutrophil aggregation

Summary

Platelets and neutrophils constitute a high source of metalloproteinases (MMPs), and their interactions via P-selectin and Pselectin- glycoprotein-ligand-1 (PSGL-1) are involved in thrombosis, vascular remodelling, and restenosis. We investigated the impact of these interactions on platelet MMP-2 secretion and function in platelet and neutrophil aggregation. The secretion of MMP-2 from human platelets was significantly increased threefold after thrombin activation, and enhanced two-fold in the presence of neutrophils. Neutrophil supernatant had no effect on platelet MMP-2 secretion. While no MMP-2 was detected in the supernatant of neutrophils, a high amount of MMP-9 was released by neutrophils, and remained unchanged upon thrombin activation or in the presence of platelets. Platelet P-selectin, which increased significantly after activation, triggered platelet binding to neutrophils that was completely inhibited by P-selectin or PSGL-1 antagonists, and was reduced by 50% with a GPIIb/ IIIa antagonist. P-selectin or PSGL-1 antagonism abolished the enhanced secretion of platelet MMP-2 in the presence of neutrophils and reduced platelet-neutrophil aggregation. Platelet activation and binding to neutrophils enhance the secretion of platelet MMP-2 via an adhesive interaction between P-selectin and PSGL-1, which contribute to increase platelet-neutrophil aggregation.

Keywords

Platelets - leukocytes - cell adhesion molecules - metalloproteinases

• References

• 1 Jang Y, Lincoff M, Plow EF. et al Cell adhesion molecules in coronary artery disease. J Am Coll Cardiol 1994; 24: 1591-601.
• 2 Nash GB. Adhesion between neutrophils and platelets: a modulator of thrombotic and inflammatory events?. Thromb Res 1994; 74 (Suppl. 01) S3-S11.
• 3 Freedman JE, Loscalzo J. Platelet-monocyte aggregates bridging thrombosis and inflammation. Circulation 2002; 105: 2130-2.
• 4 Cambien B, Wagner DD. A new role in hemostasis for the adhesion receptor P-selectin. Trends Mol Med 2004; 10: 179-86.
• 5 Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996; 88: 3259-87.
• 6 McEver RP, Cummings RD. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 1997; 100 (Suppl) S97-S103.
• 7 Moore KL. Structure and function of P-selectin glycoprotein ligand-1. Leuk Lymphoma 1998; 29: 1-15.
• 8 Marcus AJ, Broekman MJ, Safier LB. et al Formation of leukotrienes and other hydroxy acids during platelet-neutrophil interactions in vitro. Biochem Biophys Res Commun 1982; 109: 130-7.
• 9 Coeffier E, Delautier D, Le Couedic JP. et al Cooperation between platelets and neutrophils for PAFacether (platelet-activating factor) formation. J Leukoc Biol 1990; 47: 234-43.
• 10 Maugeri N, Evangelista V, Piccardoni P. et al Transcellular metabolism of arachidonic acid: increased platelet thromboxane generation in the presence of activated polymorphonuclear leukocytes. Blood 1992; 80: 447-51.
• 11 Cerletti C, Evangelista V, Molino M. et al Platelet activation by polymorphonuclear leukocytes: role of cathepsin G and P-selectin. Thromb Haemost 1995; 74: 218-23.
• 12 Bonomini M, Stuard S, Carreno MP. et al Neutrophil reactive oxygen species production during hemodialysis: role of activated platelet adhesion to neutrophils through P-selectin. Nephron 1997; 75: 402-11.
• 13 Neumann FJ, Marx N, Gawaz M. et al Induction of cytokine expression in leukocytes by binding of thrombin-stimulated platelets. Circulation 1997; 95: 2387-94.
• 14 Ostrovsky L, King AJ, Bond S. et al A juxtacrine mechanism for neutrophil adhesion on platelets involves platelet-activating factor and a selectin-dependent activation process. Blood 1998; 91: 3028-36.
• 15 Evangelista V, Manarini S, Sideri R. et al Platelet/ polymorphonuclear leukocyte interaction: Pselectin triggers protein-tyrosine phosphorylation-dependent CD11b/CD18 adhesion: role of PSGL-1 as a signaling molecule. Blood 1999; 93: 876-85.
• 16 Galt SW, Lindemann S, Medd D. et al Differential regulation of matrix metalloproteinase-9 by monocytes adherent to collagen and platelets. Circ Res 2001; 89: 509-16.
• 17 Ray JM, Stetler-Stevenson WG. The role of metalloproteinases and their inhibitors in tumour invasion, metastasis, and angiogenesis. Eur Respir J 1994; 7: 2062-72.
• 18 Fernandez-Patron C, Martinez-Cuesta MA, Salas E. et al Differential regulation of platelet aggregation by matrix metalloproteinases-9 and –2. Thromb Haemost 1999; 82: 1730-5.
• 19 Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17: 463-516.
• 20 Woessner Jr JF. The family matrix metalloproteinases. Ann NY Acad Sci 1994; 732: 11-21.
• 21 Vissers MC, Winterbourn CC. Activation of human neutrophil gelatinase by endogenous serine proteinases. Biochem J 1998; 249: 327-31.
• 22 Mazzieri R, Masiero L, Zanetta L. et al Control of type IV collagenase activity by components of the urokinase-plasmin system: a regulatory mechanism with cell-bound reactants. EMBO J 1997; 16: 2319-32.
• 23 Sawicki G, Sanders EJ, Salas E. et al Localization and translocation of MMP-2 during aggregation of human platelets. Thromb Haemost 1998; 80: 836-9.
• 24 Sawicki G, Salas E, Murat J. et al Release of gelatinase A during platelet activation mediates aggregation. Nature 1997; 386: 616-9.
• 25 Opdenakker G, Van den Steen PE, Dubois B. et al Gelatinase B functions as regulator and effector in leukocyte biology. J Leukoc Biol 2001; 69: 851-9.
• 26 Théorêt JF, Bienvenu JG, Kumar A. et al P-selectin antagonism with recombinant Pselectin glycoprotein ligand-1 (rPSGL-1g) inhibits circulating activated platelet binding to neutrophils induced by damaged arterial surfaces. J Pharmacol Exp Ther 2001; 298: 658-64.
• 27 Bienvenu JG, Tanguay JF, Théorêt JF. et al Recombinant soluble P-selectin glycoprotein ligand-1-Ig reduces restenosis through inhibition of platelet-neutrophil adhesion after double angioplasty in swine. Circulation 2001; 103: 1128-34.
• 28 Tanguay JF, Geoffroy P, Sirois MG. et al Prevention of in-stent restenosis via reduction of thrombo-inflammatory reactions with recombinant P-selectin glycoprotein ligand-1. Thromb Haemost 2004; 91: 1186-93.
• 29 Libersan D, Merhi Y. Platelet P-selectin expression: requirement for protein kinase C, but not protein tyrosine kinase or phosphoinositide 3-kinase. Thromb Haemost 2003; 89: 1016-23.
• 30 Caron A, Théorêt JF, Mousa SA. et al Anti-platelet effects of GPIIb/IIIa and Pselectin antagonism, platelet activation, and binding to neutrophils. Cardiovasc Pharmacol 2002; 40: 296-306.
• 31 Kazes I, Elalamy I, Sraer JD. et al Platelet release of trimolecular complex components MT1-MMP/ TIMP2/MMP2: involvement in MMP2 activation and platelet aggregation. Blood 2000; 96: 3064-9.
• 32 Oh LY, Larsen PH, Krekoski CA. et al Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 1999; 19: 8464-75.
• 33 Frenette PS, Denis CV, Weiss L. et al P-selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo . J Exp Med 2000; 191: 1413-22.
• 34 Sperandio M, Smith ML, Forlow SB. et al P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J Exp Med 2003; 197: 1355-63.
• 35 Spangenberg P, Redlich H, Bergmann I. et al The platelet glycoprotein IIb/IIIa complex is involved in the adhesion of activated platelets to leukocytes. Thromb Haemost 1993; 70: 515-21.
• 36 Diacovo TG, de Fourgerolles AR, Bainton DF. et al A functional integrin ligand on the surface of platelets: Intercellular adhesion molecule-2. J Clin Invest 1994; 94: 1243-51.
• 37 Bizzaro N, Goldschmeding R, von dem Borne AE. Platelet satellitism is Fc gamma RIII (CD16) receptormediated. Am J Clin Pathol 1995; 103: 740-4.
• 38 Simon DI, Chen Z, Xu H. et al Platelet glycoprotein ibalpha is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med 2000; 192: 193-204.
• 39 Santoso S, Sachs UJ, Kroll H. et al The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J Exp Med 2002; 196: 679-91.
• 40 Wize J, Sopata I, Smerdel A. et al Ligation of selectin L and integrin CD11b/CD18 (Mac-1) induces release of gelatinase B (MMP-9) from human neutrophils. Inflamm Res 1998; 47: 325-7.
• 41 Chung AWY, Radomski A. Alonso-Escolano et al Platelet-leukocyte aggregation induced by PAR agonists: regulation by nitric oxide and matrix metalloproteinases. Br J Pharamcol 2004; 143: 845-55.
• 42 Merten M, Thiagarajan P. P-selectin expression on platelets determines size and stability of platelet aggregates. Circulation 2000; 102: 1931-6.
• 43 Faraday N, Scharpf RB, Dodd-o JM. et al Leukocytes can enhance platelet-mediated aggregation and thromboxane release via interaction of P-selectin glycoprotein ligand 1 with P-selectin. Anesthesiology 2001; 94: 145-51.
• 44 Martinez MA, Salas E, Radomski A. et al Matrix metalloproteinase-2 in platelet adhesion to fibrinogen: interactions with nitric oxide. Med Sci Monit 2001; 7: 646-51.
• 45 Radomski A, Stewart MW, Jurasz P. et al Pharmacological characteristics of solid-phase von Willebrand factor in human platelets. Br J Pharmacol 2001; 134: 1013-20.
• 46 Bendeck MP, Nakada MT. The β3 integrin antagonist m7E3 reduces matrix metalloproteinase activity and smooth muscle cell migration. J Vasc Res 2001; 38: 590-9.
• 47 Sathish JG, Falati S, Croce K. et al Antibody crosslinking of human platelet P-selectin induces calcium entry by a mechanism dependent upon Fcgamma receptor IIA. Thromb Haemost 2004; 92: 598-605.
• 48 Kumar A, Hoover JL, Simmons CA. et al Remodeling and neointimal formation in the carotid artery of normal and P-selectin-deficient mice. Circulation 1997; 96: 4333-42.