Platelet Associated Fibrinogen and ICAM-2 Induce Firm Adhesion of Neutrophils under Flow Conditions

P. H. M. Kuijper; H. I. Gallardo Torres; J.-W. J. Lammers; J. J. Sixma; L. Koenderman; J. J. Zwaginga

doi:10.1055/s-0037-1615227

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 1998; 80(03): 443-448
DOI: 10.1055/s-0037-1615227

Rapid Communications

Schattauer GmbH

Platelet Associated Fibrinogen and ICAM-2 Induce Firm Adhesion of Neutrophils under Flow Conditions

P. H. M. Kuijper

¹From the Departments of Pulmonary Diseases, Utrecht, The Netherlands

,

H. I. Gallardo Torres

¹From the Departments of Pulmonary Diseases, Utrecht, The Netherlands

,

J.-W. J. Lammers

¹From the Departments of Pulmonary Diseases, Utrecht, The Netherlands

,

J. J. Sixma

²From the Haematology, University Hospital Utrecht, Utrecht, The Netherlands

,

L. Koenderman

¹From the Departments of Pulmonary Diseases, Utrecht, The Netherlands

,

J. J. Zwaginga

²From the Haematology, University Hospital Utrecht, Utrecht, The Netherlands

› Author Affiliations

Abstract

Summary

Surface-bound platelets support selectin-mediated rolling and β_2-integrin-mediated firm adhesion of neutrophils (PMN) under flow conditions. We examined which ligands on platelets mediate this firm adhesion. Surface-bound platelets express ICAM-2 and GPIIbIIIa-bound fibrinogen, which are ligands for LFA-1 and MAC-1. In a well defined model for vessel wall injury, blood from an afibrinogenemic patient was perfused over ECM-coated coverslips to obtain fibrinogen-free platelet surfaces. At high shear rates, PMN-adhesion to fibrinogen-free platelet surfaces decreased compared to fibrinogen-containing controls. Under these conditions, firm adhesion and not rolling was blocked demonstrating the importance of fibrinogen in this process. In addition, MAC-1 and LFA-1 on PMN and ICAM-2 on platelets played a role in firm adhesion; the effect of blocking antibodies was most evident at high shear. The effects of fibrinogen depletion and ICAM-2 blocking were additive. In conclusion, multiple redundant ligands, like ICAM-2 and fibrinogen, induce firm and shear resistant PMN adhesion to platelets under flow conditions. Individually these ligands become critical at higher shear. Blocking of two or more interactions also interferes with low shear adhesion.

Full Text

References

References
1 Palabrica TM, Lobb RR, Furie BC, Aronovitz M, Benjamin CD, Hsu YM, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-51.
2 Munro JM, Cotran RS. The pathogenesis of atherosclerosis: atherogenesis and inflammation. Lab Invest 1988; 58: 249-61.
3 Buttrum SM, Hatton R, Nash GB. Selectin-mediated rolling of neutrophils on immobilized platelets. Blood 1993; 82: 1165-74.
4 Yeo EL, Sheppard JA, Feuerstein IA. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood 1994; 83: 2498-507.
5 Kuijper PHM, Gallardo Torres HI, van der Linden JAM, Lammers J-WJ, Sixma JJ, Koenderman L, Zwaginga JJ. Platelet-dependent primary hemostasis promotes selectin- and integrin-mediated neutrophil adhesion to damaged endothelium under flow conditions. Blood 1996; 87: 3271-81.
6 Kuijper PHM, Gallardo Torres HI, van der Linden JAM, Lammers J-WJ, Sixma JJ, Zwaginga JJ, Koenderman L. Neutrophil adhesion to fibrin(ogen) under flow conditions is diminished by activation and L-selectin shedding. Blood. 1997 (Abstract).
7 Walcheck B, Moore KL, McEver RP, Kishimoto TK. Neutrophil-neutro-phil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1. J Clin Invest 1996; 98: 1081-7.
8 Diacovo TG, Roth SJ, Buccola JM, Bainton DF, Springer TA. Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the β₂-integrin CD11b/CD18. Blood 1996; 88: 146-57.
9 Evangelista V, Manarini S, Rotondo S, Martelli N, Polischuk R, McGregor JL, de Gaetano G, Cerletti C. Platelet/polymorphonuclear leukocyte interaction in dynamic conditions: Evidence of adhesion cascade and cross talk between P-selectin and the β2 integrin CD11b/CD18. Blood 1996; 88: 4183-94.
10 Ruf A, Schlenk RF, Maras A, Morgenstern E, Patscheke H. Contact-induced neutrophil activation by platelets in human cell suspensions and whole blood. Blood 1992; 80: 1238-46.
11 Spangenberg P, Redlich H, Bergmann I, Losche W, Gotzrath M, Kehrel B. The platelet glycoprotein IIb/IIIa complex is involved in the adhesion of activated platelets to leukocytes. Thromb Haemost 1993; 70: 514-21.
12 Ruf A, Patscheke H. Platelet-induced neutrophil activation: platelet-expressed fibrinogen induces the oxidative burst in neutrophils by an interaction with CD11C/CD18. Br J Haematol 1995; 90: 791-6.
13 Kuijper PHM, Gallardo Torres HI, Lammers J-WJ, Sixma JJ, Koenderman L, Zwaginga JJ. Platelet- and fibrin-deposition at the damaged vessel wall: cooperative substrates for neutrophil adhesion under flow conditions. Blood. 1997 (Abstract).
14 Wright SD, Weitz JI, Huang AJ, Levin SM, Silverstein SC, Loike JD. Complement receptor type three (CD11c/CD18) of human polymorphonu-clear leukocytes recognizes fibrinogen. Proc Natl Acad Sci USA 1988; 85: 7734-8.
15 Diacovo TG, deFougerolles AR, Bainton DF, Springer TA. A functional integrin ligand on the surface of platelets: intercellular adhesion molecule-2. J Clin Invest 1994; 94: 1243-51.
16 Sanchez-Madrid F, Krensky AM, Ware CF, Robbins E, Strominger JL, Burakoff SJ, Springer TA. Three distinct antigens associated with human T-lymphocyte- mediated cytolysis: LFA-1, LFA-2, and LFA-3. Proc Natl Acad Sci USA 1982; 79: 7489-93.
17 Xie J, Li R, Kotovuori P, Vermot-Desroches C, Wijdenes J, Arnaout MA, Nortamo P, Gahmberg CG. Intercellular adhesion molecule-2 (ICAM-2) binds to the leukocyte integrin CD11b/CD18 through the A-domain. J Immunol 1995; 155: 3619-28.
18 Sakariassen KS, Aarts PAMM, de Groot PG, Houdijk WPM, Sixma JJ. A perfusion chamber developed to investigate platelet interaction in flowing blood with human vessel wall cells, their extracellular matrix and purified components. J Lab Clin Med 1983; 102: 522-35.
19 Zwaginga JJ, Sixma JJ, de Groot PG. Activation of endothelial cells with phorbol myristate acetate, tumor necrosis factor or endotoxin induces platelet thombus formation on their matrix. Studies of a new model using low molecular weight heparin anticoagulant. Arteriosclerosis 1990; 10: 49.
20 Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical cord veins. Identification of morphology and immunologic criteria. J Clin Invest 1973; 52: 2745-56.
21 Willems C, Astaldi GCB, de Groot PG, Janssen MC, Gonsalves MD, Zeyle-maker WP, van Mourik JA. Media conditioned by cultured human vascular endothelial cells inhibit the growth of vascular smooth muscle cells. Exp Cell Res 1982; 139: 191-7.
22 Zwaginga JJ, IJsseldijk MJ, de Groot PG, Kooistra M, Vos J, van Es A, Koomans HA, Struyvenberg A, Sixma JJ. Treatment of uremic anemia with recombinant erythropoietin also reduces the defects in platelet adhesion and aggregation caused by uremic plasma. Thromb Haemost 1991; 66: 638-47.
23 Koenderman L, Kok PTM, Hamelink ML, Verhoeven AJ, Bruijnzeel PLB. An improved method for the isolation of eosinophilic granulocytes from peripheral blood of normal individuals. J Leuk Bio 1988; 44: 79.
24 Takada Y, Puzon W. Identification of a regulatory region of integrin beta 1 subunit using activating and inhibiting antibodies. J Biol Chem 1993; 268: 17597-601.
25 Alon R, Kassner PD, Carr MW, Finger EB, Hemler ME, Springer TA. The integrin VLA-4 supports tethering and rolling in flow on VCAM-1. J Cell Biol 1995; 128: 1243-53.
26 Lalor P, Nash GB. Adhesion of flowing leukocytes to immobilized platelets. Br J Haematol 1995; 89: 725-32.
27 Weber C, Springer TA. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J Clin Invest 1997; 100: 2085-93.
28 Wachtfogel YT, DeLa Cadena RA, Kunapuli SP, Rick L, Miller M, Schultze RL, Altieri DC, Edgington TS, Colman RW. High molecular weight kininogen binds to Mac-1 on neutrophils by its heavy chain (domain 3) and its light chain (domain 5). J Biol Chem 1994; 269: 19307-12.
29 Coombe DR, Watt SM, Parish CR. Mac-1 (CD11b/CD18) and CD45 mediate the adhesion of hematopoietic progenitor cells to stromal cell elements via recognition of stromal heparan sulfate. Blood 1994; 84: 739-52.
30 Diamond MS, Alon R, Parkos CA, Quinn MT, Springer TA. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J Cell Biol 1995; 130: 1473-82.
31 Hynes RO. Integrins: versatility, modulation and signaling in cell adhesion. Cell 1992; 69: 11-25.
32 Gresham HD, Adams SP, Brown EJ. Ligand binding specificity of the leukocyte response integrin expressed by human neutrophils. J Biol Chem 1992; 267: 13895-902.
33 Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 1991; 65: 859-73.