Platelets selectively enhance lymphocyte adhesion on subendothelial matrix under arterial flow conditions

Galia Spectre; Linjing Zhu; Maria Ersoy; Paul Hjemdahl; Naphtali Savion; David Varon; Nailin Li

doi:10.1160/TH12-02-0064

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2012; 108(02): 328-337
DOI: 10.1160/TH12-02-0064

Platelets and Blood Cells

Schattauer GmbH

Platelets selectively enhance lymphocyte adhesion on subendothelial matrix under arterial flow conditions

Authors

Galia Spectre^*

¹Department of Medicine-Solna, Clinical Pharmacology Unit, Karolinska Institute, Karolinska University Hospital-Solna, Stockholm, Sweden

²Department of Hematology, Hadassah Hebrew University Medical Center, Jerusalem, Israel
Linjing Zhu^*

¹Department of Medicine-Solna, Clinical Pharmacology Unit, Karolinska Institute, Karolinska University Hospital-Solna, Stockholm, Sweden
Maria Ersoy

¹Department of Medicine-Solna, Clinical Pharmacology Unit, Karolinska Institute, Karolinska University Hospital-Solna, Stockholm, Sweden
Paul Hjemdahl

¹Department of Medicine-Solna, Clinical Pharmacology Unit, Karolinska Institute, Karolinska University Hospital-Solna, Stockholm, Sweden
Naphtali Savion

³Goldschleger Eye Research Institute, Tel Aviv University, Tel Hashomer, Israel
David Varon

²Department of Hematology, Hadassah Hebrew University Medical Center, Jerusalem, Israel
Nailin Li

¹Department of Medicine-Solna, Clinical Pharmacology Unit, Karolinska Institute, Karolinska University Hospital-Solna, Stockholm, Sweden

Abstract

Summary

Platelet adhesion at sites of cardiovascular injury may facilitate leukocyte deposition. We asked if and how platelets enhance lymphocyte adhesion on different subendothelial matrix protein (SEMP)-coated surface at arterial shear stress. Hirudinised whole blood was subjected to an arterial shear rate (500 s⁻¹) in a Cone and Plate(let) analyser (CPA) for 5 minutes using plates coated with bovine serum albumin (BSA), collagen, fibrinogen, von Willebrand factor (vWF), or fibronectin. Platelet and lymphocyte adhesion were monitored by CPA and flow cytometry. Exposure of blood to collagen, fibrinogen, and vWF-coated surfaces induced platelet activation. The most marked effect was seen with collagen-coating, which markedly enhanced the adhesion of all lymphocyte subpopulations compared to BSA-coating. Fibrinogen-coating supported both T and NK cell adhesion, while vWF-coated surface only enhanced NK cell deposition. In contrast, fibronectin enhanced neither platelet activation nor lymphocyte adhesion. Moreover, platelets preferentially facilitated adhesion of large CD4⁺ and CD8⁺ T cells and NK cells, and of small B cells. Enhanced cell adhesion of larger lymphocytes was associated with elevated platelet conjugation and higher lymphocyte expression of PSGL-1, Mac-1, and CD40L. The enhancement of lymphocyte adhesion was totally platelet-dependent, and was abolished in platelet-depleted blood. Moreover, blockade of the platelet adhesion molecules P-selectin, GPIIb/IIIa, and CD40L attenuated platelet-dependent lymphocyte deposition. In conclusion, platelets support lymphocyte adhesion on SEMP-coated surfaces under arterial shear. The enhancement is selective for large T and NK cells and small B cells.

Keywords

Platelets - lymphocytes - arterial flow - subendothelial matrix proteins

Full Text

References

References
1 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.
2 Davi G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med 2007; 357: 2482-2494.
3 Li N. Platelet lymphocyte cross-talk. J Leukoc Biol 2008; 83: 1069-1078.
4 Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685-1695.
5 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: 887-896.
6 Massberg S, Schurzinger K, Lorenz M. et al. Pla telet adhesion via glycoprotein II b integrin is critical for atheroprogression and focal cerebral ischemia: an in vivo study in mice lacking glycoprotein IIb. Circulation 2005; 112: 1180-1188.
7 Rinder HM, Bonan JL, Rinder CS. et al. Dynamics of leukocyte-platelet adhesion in whole blood. Blood 1991; 78: 1730-1737.
8 Li N, Ji Q, Hjemdahl P. Platelet-lymphocyte conjugation differs between lymphocyte subpopulations. J Thromb Haemost 2006; 04: 874-881.
9 Diacovo TG, Puri KD, Warnock RA. et al. Platelet-mediated lymphocyte delivery to high endothelial venules. Science 1996; 273: 252-255.
10 Lalor P, Nash GB. Adhesion of flowing leucocytes to immobilized platelets. Br J Haematol 1995; 89: 725-732.
11 Elzey BD, Tian J, Jensen RJ. et al. Platelet-mediated modulation of adaptive immunity. A communication link between innate and adaptive immune compartments. Immunity 2003; 19: 9-19.
12 Gerdes N, Zhu L, Ersay M. et al. Platelets regulate CD4+ T cell differentiation via multiple chemokines in humans. Thromb Haemost 2011; 106: 353-362.
13 Elzey BD, Grant JF, Sinn HW. et al. Cooperation between platelet-derived CD154 and CD4+ T cells for enhanced germinal center formation. J Leukoc Biol 2005; 78: 80-84.
14 Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115: 3378-3384.
15 Butler LM, Metson-Scott T, Felix J. et al. Sequential adhesion of platelets and leukocytes from flowing whole blood onto a collagen-coated surface: requirement for a GPVI-binding site in collagen. Thromb Haemost 2007; 97: 814-821.
16 He S, Cao H, Magnusson CG. et al. Are increased levels of von Willebrand factor in chronic coronary heart disease caused by decrease in von Willebrand factor cleaving protease activity? A study by an immunoassay with antibody against intact bond 842Tyr-843Met of the von Willebrand factor protein. Thromb Res 2001; 103: 241-248.
17 Varon D, Dardik R, Shenkman B. et al. A new method for quantitative analysis of whole blood platelet interaction with extracellular matrix under flow conditions. Thromb Res 1997; 85: 283-294.
18 Li N, Wallén NH, Hjemdahl P. Evidence for prothrombotic effects of exercise and limited protection by aspirin. Circulation 1999; 100: 1374-1379.
19 Hu H, Li N, Yngen M. et al. Enhanced leukocyte-platelet cross-talk in type 1 diabetes mellitus: relationship to microangiopathy. J Thromb Haemost 2004; 02: 58-64.
20 Eriksson EE. Intravital microscopy on atherosclerosis in apolipoprotein e-defi-cient mice establishes microvessels as major entry pathways for leukocytes to advanced lesions. Circulation 2011; 124: 2129-2138.
21 Hu H, Zhu L, Huang Z. et al. Platelets enhance lymphocyte adhesion and infiltration into arterial thrombus. Thromb Haemost 2010; 104: 1184-1192.
22 Skilbeck C, Westwood SM, Walker PG. et al. Population of the vessel wall by leukocytes binding to P-selectin in a model of disturbed arterial flow. Arterioscler Thromb Vasc Biol 2001; 21: 1294-1300.
23 Solpov A, Shenkman B, Vitkovsky Y. et al. Platelets enhance CD4+ lymphocyte adhesion to extracellular matrix under flow conditions: role of platelet aggregation, integrins, and non-integrin receptors. Thromb Haemost 2006; 95: 815-821.
24 Savage B, Saldivar E, Ruggeri ZM. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 1996; 84: 289-297.
25 Mou Y, Ni H, Wilkins JA. The selective inhibition of beta 1 and beta 7 integrin-mediated lymphocyte adhesion by bacitracin. J Immunol 1998; 161: 6323-6329.
26 Ni H. Unveiling the new face of fibronectin in thrombosis and hemostasis. J Thromb Haemost 2006; 04: 940-942.
27 Ni H, Yuen PS, Papalia JM. et al. Plasma fibronectin promotes thrombus growth and stability in injured arterioles. Proc Natl Acad Sci USA 2003; 100: 2415-2419.
28 Beumer S, MJ IJ, de Groot PG. et al. Platelet adhesion to fibronectin in flow: dependence on surface concentration and shear rate, role of platelet membrane glycoproteins GP IIb/IIIa and VLA-5, and inhibition by heparin. Blood 1994; 84: 3724-3733.
29 Cho J, Mosher DF. Enhancement of thrombogenesis by plasma fibronectin crosslinked to fibrin and assembled in platelet thrombi. Blood 2006; 107: 3555-3563.
30 Lievens D, Eijgelaar WJ, Biessen EA. et al. The multi-functionality of CD40L and its receptor CD40 in atherosclerosis. Thromb Haemost 2009; 102: 206-214.
31 André P, Prasad KS, Denis CV. et al. CD40L stabilizes arterial thrombi by a beta3 integrin--dependent mechanism. Nat Med 2002; 08: 247-252.
32 McCarty OJ, Zhao Y, Andrew N. et al. Evaluation of the role of platelet integrins in fibronectin-dependent spreading and adhesion. J Thromb Haemost 2004; 02: 1823-1833.