Platelet function under high shear conditions

A. J. Reininger

doi:10.1055/s-0037-1616934

Hämostaseologie, Table of Contents

Hamostaseologie 2009; 29(01): 21-24
DOI: 10.1055/s-0037-1616934

Original article

Schattauer GmbH

Platelet function under high shear conditions

A. J. Reininger

¹Dept. of Transfusion Medicine, Haemostaseology and Immunogenetics, Clinic for Anaesthesiology, University Clinic Munich, Germany

› Author Affiliations

Abstract

Summary

Blood platelets are the first line of defense against bleeding and as such involved in the haemostatic repair of damaged vasculature. Their true prowess seems to be displayed under high shear conditions where platelets interact with a variety of plasma proteins, all of which are tightly regulated to close the leak but at the same time prevent lumen occlusion and thromboembolism. The first task is to arrest fast flowing platelets on exposed collagen of the damaged subendothelial surface. Although platelets are endowed with several collagen receptors, most notably integrin ╒2b®1 and the immunoglobulin superfamily member GPVI, they can not arrest platelets at high shear rates. The latter requires binding of the platelet receptor GPIb╒to the A1-binding domain of von Willebrand factor (VWF), which first has to be immobilized from the flowing blood onto the site of injury. Under high shear conditions further accrual of newly arriving platelets again requires VWF, which has to bridge platelets not only to the exposed collagen but also to each other by being sandwiched between the multiple platelet layers of the haemostatic plug.

Keywords

Platelet function - shear stress

Full Text

References

References
1 Reininger AJ, Heijnen HF, Schumann H. et al. Mechanism of platelet adhesion to von Willebrand factor and microparticle formation under high shear stress. Blood 2006; 107: 3537-3545.
2 Bergmeier W, Piffath CL, Goerge T. et al. The role of platelet adhesion receptor GPIbalpha far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. Proc Natl Acad Sci USA 2006; 103: 16900-16905.
3 Kato K, Kanaji T, Russell S. et al. The contribution of glycoprotein VI to stable platelet adhesion and thrombus formation illustrated by targeted gene deletion. Blood 2003; 102: 1701-1707.
4 Jurk K, Clemetson KJ, de Groot PG. et al. Thrombospondin- 1 mediates platelet adhesion at high shear via glycoprotein Ib (GPIb): an alternative/ backup mechanism to von Willebrand factor. FASEB J 2003; 17: 1490-1492.
5 Siedlecki CA, Lestini BJ, Kottke-Marchant KK. et al. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 1996; 88: 2939-2950.
6 Schneider SW, Nuschele S, Wixforth A. et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci USA 2007; 104: 7899-7903.
7 Nesbitt WS, Kulkarni S, Giuliano S. et al. Distinct glycoprotein Ib/V/IX and integrin alphaIIbbeta3- dependent calcium signals cooperatively regulate platelet adhesion under flow. J Biol Chem 2002; 277: 2965-2972.
8 Ruggeri ZM, De ML, Gatti L. et al. Platelets have more than one binding site for von Willebrand factor. J Clin Invest 1983; 72: 1-12.
9 Goto S, Salomon DR, Ikeda Y, Ruggeri ZM. Characterization of the unique mechanism mediating the shear-dependent binding of soluble von Willebrand factor to platelets. J Biol Chem 1995; 270: 23352-23361.
10 Kasirer-Friede A, Ware J, Leng L. et al. Lateral clustering of platelet GP Ib-IX complexes leads to upregulation of the adhesive function of integrin alpha IIbbeta 3. J Biol Chem 2002; 277: 11949-11956.
11 Kasirer-Friede A, Cozzi MR, Mazzucato M. et al. Signaling through GP Ib-IX-V activates alpha IIb beta 3 independently of other receptors. Blood 2004; 103: 3403-3411.
12 Mazzucato M, Pradella P, Cozzi MR. et al. Sequential cytoplasmic calcium signals in a 2-stage platelet activation process induced by the glycoprotein Ibalpha mechanoreceptor. Blood 2002; 100: 2793-2800.
13 Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4: 517-529.
14 Feske S. Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 2007; 7: 690-702.
15 Grosse J, Braun A, Varga-Szabo D. et al. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest 2007; 117: 3540-3550.
16 Varga-Szabo D, Braun A, Kleinschnitz C. et al. The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 2008; 205: 1583-1591.
17 Braun A, Varga-Szabo D, Kleinschnitz C. et al. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood. 2008 Prepublished online DOI: 10.1182/blood-2008-07-171611.
18 Bergmeier W, Oh-Hora M, McCarl CA. et al. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood. 2008 Prepublished online DOI: 10.1182/blood-2008-08-174516.
19 Ruggeri ZM, Orje JN, Habermann R. et al. Activation- independent platelet adhesion and aggregation under elevated shear stress. Blood 2006; 108: 1903-1910.
20 Savage B, Almus-Jacobs F, Ruggeri ZM. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 1998; 94: 657-666.
21 Donadelli R, Orje JN, Capoferri C. et al. Size regulation of von Willebrand factor-mediated platelet thrombi by ADAMTS13 in flowing blood. Blood 2006; 107: 1943-1950.
22 Penz S, Reininger AJ, Brandl R. et al. Human atheromatous plaques stimulate thrombus formation by activating platelet glycoprotein VI. FASEB J 2005; 19: 898-909.
23 Lefkovits J, Plow EF, Topol E. Platelet glycoprotein IIb/IIIa receptors in cardiovascular medicine. New Engl J Med 1995; 332: 1553-1559.
24 Weisel JW, Nagaswami C, Vilaire G, Bennett JS. Examination of the platelet membrane glycoprotein IIb-IIIa complex and its interaction with fibrinogen and other ligands by electron microscopy. J Biol Chem 1992; 267: 16637-16643.
25 Polgar J, Matuskova J, Wagner DD. The P-selectin, tissue factor, coagulation triad. J Thromb Haemost 2005; 3: 1590-1596.
26 Ruggeri ZM, Dent JA, Saldivar E. Contribution of distinct adhesive interactions to platelet aggregation in flowing blood. Blood 1999; 94: 172-178.
27 Ni H, Denis CV, Subbarao S. et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest 2000; 106: 385-392.
28 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.
29 Andre P, Prasad KS, Denis CV. et al. CD40L stabilizes arterial thrombi by a beta3 integrin--dependent mechanism. Nat Med 2002; 8: 247-252.
30 Shida Y, Nishio K, Sugimoto M. et al. Functional imaging of shear-dependent activity of ADAMTS13 in regulating mural thrombus growth under whole blood flow conditions. Blood 2008; 111: 1295-1298.
31 Muller I, Klocke A, Alex M. et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 2003; 17: 476-478.
32 Holme PA, Orvim U, Hamers MJAG. et al. Shearinduced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis. Arterioscler Thromb Vasc Biol 1997; 17: 646-653.
33 Keuren JF, Magdeleyns EJ, Bennaghmouch A. et al. Microparticles adhere to collagen type I, fibrinogen, von Willebrand factor and surface immobilised platelets at physiological shear rates. Br J Haematol 2007; 138: 527-533.
34 Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106: 1604-1611.