Transendothelial migration drives dissociation of plateletmonocyte complexes

Janine M. van Gils; Paula A. da Costa Martins; Anita Mol; Peter L. Hordijk; Jaap Jan Zwaginga

doi:10.1160/TH08-03-0165

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2008; 100(02): 271-279
DOI: 10.1160/TH08-03-0165

Platelets and Blood Cells

Schattauer GmbH

Transendothelial migration drives dissociation of plateletmonocyte complexes

Janine M. van Gils

¹Department of Molecular Cell Biology, Sanquin Research and Landsteiner Laboratory, Academical Medical Center, University of Amsterdam, Amsterdam, The Netherlands

,

Paula A. da Costa Martins

²Department of Experimental Immunohematology, Sanquin Research and Landsteiner Laboratory, Academical Medical Center, University of Amsterdam, Amsterdam, The Netherlands

,

Anita Mol

¹Department of Molecular Cell Biology, Sanquin Research and Landsteiner Laboratory, Academical Medical Center, University of Amsterdam, Amsterdam, The Netherlands

,

Peter L. Hordijk

¹Department of Molecular Cell Biology, Sanquin Research and Landsteiner Laboratory, Academical Medical Center, University of Amsterdam, Amsterdam, The Netherlands

,

Jaap Jan Zwaginga

²Department of Experimental Immunohematology, Sanquin Research and Landsteiner Laboratory, Academical Medical Center, University of Amsterdam, Amsterdam, The Netherlands

³Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands

› Author Affiliations

Abstract

Summary

Monocytes and platelets are both crucially involved in atherogenesis. Importantly, activated platelets bound to circulating monocytes increase adhesion of the monocytes and thus mediate colocalization of both cell types at the vessel wall. We examined the fate of the platelets upon migration of these potentially pro-atherogenic platelet-monocyte complexes (PMC) across activated endothelium. Platelet-monocyte complex migration was studied both quantitatively by means of Transwell filters coated with endothelial cells, as well as qualitatively with different imaging techniques, and in the absence or presence of flow. Upon PMC transendothelial migration, platelets relocate with monocytic P-selectin glycoprotein ligand-1 (PSGL-1) to the rear of the monocyte, detach,and remain at the endothelial surface. Platelet dissociation appeared not to be due to reduced PSGL-1 expression or reduced platelet-binding capacity of the migrated monocytes. In addition, different endothelial matrix proteins with different platelet-binding capacities coated on the Transwell filter, instead of endothelial cells, did not affect PMC dissociation. In contrast, lowering the mechanical stress that PMC experience during transmigration prevented dissociation of platelets. In conclusion, PMC dissociate during transendothelial migration as a result of monocytic PSGL-1 redistribution and mechanical stress. PMC-mediated deposition of activated platelets at sites of vascular inflammation is likely relevant for cardiovascular disease progression or vascular regeneration.

Keywords

Monocytes - platelet immunology - cell migration - endothelial cells

Full Text

References

References
1 Munro JM, Cotran RS. The pathogenesis of atherosclerosis: atherogenesis and inflammation. Lab Invest 1988; 58: 249-261.
2 Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999; 340: 115-126.
3 Huo Y, Schober A, Forlow SB. et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003; 09: 61-67.
4 Langer HF, Gawaz M. Platelet-vessel wall interactions in atherosclerotic disease. Thromb Haemost 2008; 99: 480-486.
5 Zwaginga JJ, Torres HI, Lammers J. et al. Minimal platelet deposition and activation in models of injured vessel wall ensure optimal neutrophil adhesion under flow conditions. Arterioscler Thromb Vasc Biol 1999; 19: 1549-1554.
6 Rinder HM, Bonan JL, Rinder CS. et al. Dynamics of leukocyte-platelet adhesion in whole blood. Blood 1991; 78: 1730-1737.
7 Sarma J, Laan CA, Alam S. et al. Increased platelet binding to circulating monocytes in acute coronary syndromes. Circulation 2002; 105: 2166-2171.
8 McCabe DJ, Harrison P, Mackie IJ. et al. Platelet degranulation and monocyte-platelet complex formation are increased in the acute and convalescent phases after ischaemic stroke or transient ischaemic attack. Br J Haematol 2004; 125: 777-787.
9 Furman MI, Benoit SE, Barnard MR. et al. Increased platelet reactivity and circulating monocyte-platelet aggregates in patients with stable coronary artery disease. J Am Coll Cardiol 1998; 31: 352-358.
10 Shoji T, Koyama H, Fukumoto S. et al. Platelet activation is associated with hypoadiponectinemia and carotid atherosclerosis. Atherosclerosis 2006; 188: 190-195.
11 Rinder CS, Bonan JL, Rinder HM. et al. Cardiopul-monary bypass induces leukocyte-platelet adhesion. Blood 1992; 79: 1201-1205.
12 da Costa Martins P, Zwaginga JJ. Leukocyte-platelet aggregates: new particles reflecting and effecting cardiovascular disease. Thromb Haemost 2005; 94: 1120-1121.
13 Dong ZM, Brown AA, Wagner DD. Prominent role of P-selectin in the development of advanced atherosclerosis in ApoE-deficient mice. Circulation 2000; 101: 2290-2295.
14 da Costa Martins P, van den Berk N, Ulfman LH. et al. Platelet-monocyte complexes support monocyte adhesion to endothelium by enhancing secondary tethering and cluster formation. Arterioscler Thromb Vasc Biol 2004; 24: 193-199.
15 Theilmeier G, Lenaerts T, Remacle C. et al. Circulating activated platelets assist THP-1 monocytoid/en-dothelial cell interaction under shear stress. Blood 1999; 94: 2725-2734.
16 Weyrich AS, McIntyre TM, McEver RP. et al. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B trans-location. J Clin Invest 1995; 95: 2297-2303.
17 Weyrich AS, Elstad MR, McEver RP. et al. Activated platelets signal chemokine synthesis by human monocytes. J Clin Invest 1996; 97: 1525-1534.
18 Celi A, Pellegrini G, Lorenzet R. et al. P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci USA 1994; 91: 8767-8771.
19 da Costa Martins PA, van Gils JM, Mol A. et al. Platelet binding to monocytes increases the adhesive properties of monocytes by up-regulating the expression and functionality of beta1 and beta2 integrins. J Leukoc Biol 2006; 79: 499-507.
20 Yago T, Tsukuda M, Minami M. P-selectin binding promotesthe adhesion of monocytestoVCAM-1 under flow conditions. J Immunol 1999; 163: 367-373.
21 We ber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res 2005; 96: 612-616.
22 von Hundelshausen P, Petersen F, Brandt E. Platelet-derived chemokines in vascular biology. Thromb Haemost 2007; 97: 704-713.
23 Jaffe EA, Nachman RL, Becker CG. et al. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 1973; 52: 2745-2756.
24 Houdijk WP, de Groot PG, Nievelstein PF. et al. Subendothelial proteins and platelet adhesion. von Willebrand factor and fibronectin, not thrombospon-din, are involved in platelet adhesion to extracellular matrix of human vascular endothelial cells. Arteriosclerosis 1986; 06: 24-33.
25 Campanero MR, Sanchez-Mateos P, del Pozo MA. et al. ICAM-3 regulates lymphocyte morphology and integrin-mediated T cell interaction with endothelial cell and extracellular matrix ligands. J Cell Biol 1994; 127: 867-878.
26 Lang D, Dohle F, Terstesse M. et al. Down-regulation of monocyte apoptosis by phagocytosis of platelets: involvement of a caspase-9, caspase-3, and heat shock protein 70-dependent pathway. J Immunol 2002; 168: 6152-6158.
27 Bradfield PF, Scheiermann C, Nourshargh S. et al. JAM-C regulates unidirectional monocyte trans-endothelial migration in inflammation. Blood 2007; 110: 2545-2555.
28 Bruehl RE, Moore KL, Lorant DE. et al. Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1. J Leukoc Biol 1997; 61: 489-499.
29 Lorant DE, McEver RP, McIntyre TM. et al. Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces. J Clin Invest 1995; 96: 171-182.
30 Dore M, Burns AR, Hughes BJ. et al. Chemoattract-ant-induced changes in surface expression and redistribution of a functional ligand for P-selectin on neutrophils. Blood 1996; 87: 2029-2037.
31 Davenpeck KL, Brummet ME, Hudson SA. et al. Activation of human leukocytes reduces surface P-se-lectin glycoprotein ligand-1 (PSGL-1, CD162) and adhesion to P-selectin in vitro. J Immunol 2000; 165: 2764-2772.
32 von Hundelshausen P, We ber C. Platelets as immune cells: bridging inflammation and cardiovascular disease. Circ Res 2007; 100: 27-40.
33 May AE, Seizer P, Gawaz M. Platelets: inflammatory firebugs of vascular walls. Arterioscler Thromb Vasc Biol 2008; 28: s5-10.
34 Dole VS, Bergmeier W, Patten IS. et al. PSGL-1 regulates platelet P-selectin-mediated endothelial activation and shedding of P-selectin from activated platelets. Thromb Haemost 2007; 98: 806-812.
35 Celik S, Langer H, Stellos K. et al. Platelet-associated LIGHT (TNFSF14) mediates adhesion of platelets to human vascular endothelium. Thromb Haemost 2007; 98: 798-805.
36 de Boer HC, Verseyden C, Ulfman LH. et al. Fibrin and activated platelets cooperatively guide stem cells to a vascular injury and promote differentiation towards an endothelial cell phenotype. Arterioscler Thromb Va sc Biol 2006; 26: 1653-1659.
37 Lev EI, Estrov Z, Aboulfatova K. et al. Potential role of activated platelets in homing of human endothelial progenitor cells to subendothelial matrix. Thromb Haemost 2006; 96: 498-504.
38 Massberg S, Brand K, Gruner S. et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med 2002; 196: 887-96.
39 Schmitt-Sody M, Klose A, Gottschalk O. et al. Pla-telet-endothelial cell interactions in murine antigen-induced arthritis. Rheumatology (Oxford) 2005; 44: 885-889.
40 Pitchford SC. Novel uses for anti-platelet agents as anti-inflammatory drugs. Br J Pharmacol 2007; 152: 987-1002.