Download PDF
Thromb Haemost 2008; 100(01): 60-68
DOI: 10.1160/TH07-03-0222
Platelets and Blood Cells
Schattauer GmbH

Effects of von Willebrand factor concentration and platelet collision on shear-induced platelet activation

Zhenyue Gao
1   Bioengineering Department of Beijing University of Aeronautics and Astronautics, Beijing, China
,
Fang Liu
2   Jiangsu Institute of Hematology, Suzhou, China
,
Ziqiang Yu
2   Jiangsu Institute of Hematology, Suzhou, China
,
Xia Bai
2   Jiangsu Institute of Hematology, Suzhou, China
,
Chun Yang
1   Bioengineering Department of Beijing University of Aeronautics and Astronautics, Beijing, China
,
Fengyuan Zhuang
1   Bioengineering Department of Beijing University of Aeronautics and Astronautics, Beijing, China
,
Changgeng Ruan
2   Jiangsu Institute of Hematology, Suzhou, China
› Author AffiliationsFinancial support: This work was supported by a grant from the National Natural Sciences Foundation of PR China (No. 10402002 and 30670904), and a Foundation for the Author of National Excellent Doctoral Dissertation of PR China (No. 200356).
Further Information

Publication History

Received 26 March 2007

Accepted after major revision 06 May 2008

Publication Date:
22 November 2017 (online)

    Permissions and Reprints

Summary

The binding of plasma von Willebrand factor (vWF) to platelet glycoprotein (GP) Ibα in a high shear stress field, and subsequent integrin-GPIIb/IIIa-vWF conjunction induces platelet aggregation (SIPA). However, the specific biomechanical mechanism of the vWF-GPIb interaction still remains to be elucidated. A parallel-plate rectangular flow chamber was built to simulate a stenopeic artery flow pattern. Using the flow chamber, we examined shear- induced platelet activation (SIPAct) at different vWF concentrations (5–25 µg/ml) and several simulated stenotic high shear rates. P-selectin expression on the platelets and annexin V binding to the platelets were used as two markers of platelet activation. At different localized shear rates (3,000 s-1–9,500 s-1), the percentage of annexin V and P-selectin positive cells increased from 8.3 ± 0.4% to 22.3 ± 1.8% ( p 0.05) and from 17.4 ± 0.5% to 33.5 ± 2.5% (p 0.05),respectively. As the vWF concentration increased from 5 µg/ml to 25 µg/ml, the annexinV binding rate increased from 7.2 ± 0.6% to 53.4 ± 3.8% (p 0.05), and P-selectin expression increased from 16.5 ± 1.2% to 65.9 ± 5.2% (p 0.05). A test in a uniform shear field using cone-plate viscometer rheometry showed that the platelet activation rate was proportional to the platelet concentration. This result suggests that platelet collision is one of the impact factors of SIPAct.

Keywords

vWF - SIPA(ct) - flow chamber - cone-plate viscometer - platelet collision
 

  • References

  • 1 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.
    CrossrefPubMedGoogle Scholar
  • 2 Kroll MH, Hellums JD, McIntire LV. et al. Platelets and shear stress. Blood 1996; 88: 1525-1541.
    PubMedGoogle Scholar
  • 3 Ikeda Y, Murata M, Goto S. Von Willebrand factordependent shear-induced platelet aggregation: basic mechanisms and clinical implications. Ann NY Acad Sci 1997; 811: 325-336.
    CrossrefPubMedGoogle Scholar
  • 4 Shankaran H, Alexandridis P, Neelamegham S. Aspects of hydrodynamic shear regulating shear-induced platelet activation and self-association of von Willebrand factor in suspension. Blood 2003; 101: 2637-2645.
    CrossrefPubMedGoogle Scholar
  • 5 Ikeda Y, Handa M, Kamata T. et al. Transmembrane calcium influx associated with von Willebrand factor binding to GP Ib in the initiation of shear-induced platelet aggregation. Thromb Haemost 1993; 69: 496-502.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 O'Brien JR, Salmon GP. Shear stress activation of platelet glycoprotein IIb/IIIa plus von Willebrand factor causes aggregation: filter blockage and the long bleeding time in von Willebrand's disease. Blood 1987; 70: 1354-1361.
    PubMedGoogle Scholar
  • 7 Peterson DM, Stathopoulos NA, Giorgio TD. et al. Shear-induced platelet aggregation requires von Willebrand factor and platelet membrane glycoproteins Ib and IIb-IIIa. Blood 1987; 69: 625-628.
    PubMedGoogle Scholar
  • 8 Andrew DB. Plasma von Willebrand factor, thrombosis, and the endothelium: The first 30 years. Thromb Haemost 2006; 95: 49-55.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Ruggeri ZM. von Willebrand factor. J Clin Invest 1997; 99: 559-563.
    CrossrefPubMedGoogle Scholar
  • 10 Sadler JE. Biochemistry and genetics of von Willebrand factor. Ann Rev Biochem 1998; 67: 395-424.
    CrossrefPubMedGoogle Scholar
  • 11 Ruggeri ZM. von Willebrand factor and the mechanisms of platelet function. Springer: 1998
    Google Scholar
  • 12 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.
    CrossrefPubMedGoogle Scholar
  • 13 James KH, Robert ES, Gwen AM. et al. Pharmacologic inhibition of platelet vWF-GPIbα interaction prevents coronary artery thrombosis. Thromb Haemost 2006; 95: 469-475.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Sakariassen KS, Bolhuis PA, Sixma JJ. Human blood platelet adhesion to artery subendothelium is mediated by factor VIII-Von Willebrand factor bound to the subendothelium. Nature 1979; 279: 636-638.
    CrossrefPubMedGoogle Scholar
  • 15 Schoenwaelder SM, Hughan SC, Boniface K. et al. RhoA sustains integrin αIIbβ3 adhesion contacts under high shear. J Biol Chem 2002; 277: 14738-14746.
    CrossrefPubMedGoogle Scholar
  • 16 Oury C, Sticker E, Cornelissen H. et al. ATP augments von Willebrand factor-dependent shear-induced platelet aggregation through Ca2+-calmodulin and myosin light chain kinase activation. J Biol Chem 2004; 279: 26266-26273.
    CrossrefPubMedGoogle Scholar
  • 17 Belval TK, Hellums JD. Analysis of shear-induced platelet aggregation with population balance mathematics. Biophys J 1986; 50: 479-487.
    CrossrefPubMedGoogle Scholar
  • 18 Holme PA, Ørvim 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.
    CrossrefPubMedGoogle Scholar
  • 19 Goto S, Ikeda Y, Saldívar E. et al. Distinct Mechanisms of Platelet Aggregation as a Consequence of Different Shearing Flow Conditions. J Clin Invest 1998; 101: 479-486.
    CrossrefPubMedGoogle Scholar
  • 20 Depraetere H, Ajzenberg N, Girma JP. et al. Platelet aggregation induced by a monoclonal antibody to the A1 domain of von Willebrand factor. Blood 1998; 91: 3792-3799.
    PubMedGoogle Scholar
  • 21 Pontiggia L, Steiner B, Ulrichts H. et al. Platelet microparticle formation and thrombin generation under high shear are effectively suppressed by a monoclonal antibody against GPIbα. Thromb Haemost 2006; 96: 774-780.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Wang JS. Intense exercise increases shear-induced platelet aggregation in men through enhancement of von Willbrand factor binding, glycoprotein IIb/IIIa activation, and P-selectin expression on platelets. Eur J Appl Physiol 2004; 91: 741-747.
    CrossrefPubMedGoogle Scholar
  • 23 van Mourik JA, Mochtar IA. Purification of human antihemophilic factor (factor VIII) by gel chromatography. Biochim Biophys Acta 1970; 221: 677-679.
    CrossrefPubMedGoogle Scholar
  • 24 Ruan CG, Du XP, Xi XD. et al. A murine antiglycoprotein Ib complex monoclonal antibody, SZ2, inhibits platelet aggregation induced by both ristocetin and collagen. Blood 1987; 69: 570-577.
    PubMedGoogle Scholar
  • 25 Kasirer-Friede A, Cozzi MR, Mazzucato M. et al. Signaling through GP Ib-IX-V activates αIIbβ3 independently of other receptors. Blood 2004; 103: 3403-3411.
    CrossrefPubMedGoogle Scholar
  • 26 Mazzucato M, Cozzi MR, Pradella P. et al. Distinct roles of ADP receptors in von Willebrand factor-mediated platelet signaling and activation under high flow. Blood 2004; 104: 3221-3227.
    CrossrefPubMedGoogle Scholar
  • 27 Oury C, Toth-Zsamboki E, Vermylen J. et al. P2X1-mediated activation of extracellular signal-regulated kinase 2 contributes to platelet secretion and aggregation induced by collagen. Blood 2002; 100: 2499-2505.
    CrossrefPubMedGoogle Scholar
  • 28 Mazzucato M, Pradella P, Cozzi MR. et al. Sequential cytoplasmic calcium signals in a 2-stage platelet activation process induced by the glycoprotein Ibamechanoreceptor. Blood 2002; 100: 2793-2800.
    CrossrefPubMedGoogle Scholar
  • 29 Dorsam RT, Kim S, Murugappan S. et al. Differential requirements for calcium and Src family kinases in platelet GPIIb/IIIa activation and thromboxane generation downstream of different G-protein pathways. Blood 2005; 105: 2749-2756.
    CrossrefPubMedGoogle Scholar
  • 30 Wunder B, Melzer S. Interlayer vacancy characterization of synthetic phlogopitic micas by IR spectroscopy. Eur J Mineral 2002; 14: 1129-1138.
    CrossrefPubMedGoogle Scholar
  • 31 Goto S, Salomon DR, Ikeda Y. et al. Characterization of the unique mechanism mediating the sheardependent binding of soluble von Willebrand factor to platelets. J Biol Chem 1995; 270: 23352-23361.
    CrossrefPubMedGoogle Scholar
  • 32 Dachary-Prigent J, Freyssinet JM, Pasquet JM. et al. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood 1993; 81: 2554-2565.
    PubMedGoogle Scholar
  • 33 Merten M, Chow T, Hellums TD. et al. A new role for P-selectin in shear-induced platelet aggregation. Circulation 2000; 102: 2045-2050.
    CrossrefPubMedGoogle Scholar
  • 34 Richter H. Rohrhydraulik. Springer-Verlag: 1971
    Google Scholar
  • 35 Muggli R, Baumgartner HR, Tschopp TB. et al. Automated microdensitometry and protein assays as a measure for platelet adhesion and aggregation on collagen-coated slides under controlled flow conditions. J Lab Clin Med 1980; 95: 195-207.
    PubMedGoogle Scholar
  • 36 Brian S. Perry's Chemical Engineer's Handbook. 6th Ed. New York: McGraw-Hill Book Co; 1984. 5 23-25.
    Google Scholar
  • 37 Fukuyama M, Sakai K, Itagaki I. et al. Continuous measurement of shear-induced platelet aggregation. Thromb Res 1989; 54: 253-260.
    CrossrefPubMedGoogle Scholar
  • 38 Chow TW, Hellums JD, Moake JL. et al. Shear stress-induced von Willebrand factor binding to platelet glycoprotein Ib initiates calcium influx associated with aggregation. Blood 1992; 80: 113-120.
    PubMedGoogle Scholar
  • 39 Osende JI, Fuster V, Lev EI. et al. Testing platelet activation with a shear-dependent platelet function test versus aggregation-based tests: Relevance for monitoring long-term glycoprotein IIb/IIIa inhibition. Circulation 2001; 103: 1488-1491.
    CrossrefPubMedGoogle Scholar
  • 40 Shenkman B, Schneiderman J, Tamarin I. et al. Testing the effect of GPIIb-IIIa antagonist in patients undergoing carotid stenting: correlation between standard aggregometry, flow cytometry and the cone and plate(let) analyzer (CPA) methods. Thromb Res 2001; 102: 311-317.
    CrossrefPubMedGoogle Scholar
  • 41 Sutera SP, Nowak MD, Joist JH. et al. A programmable, computer-controlled cone-plate viscometer for the application of pulsatile shear stress to platelet suspensions. Biorheology 1988; 25: 449-459.
    CrossrefPubMedGoogle Scholar
  • 42 Smoluchowski MV. Versuch einer mathematischen theorie der koagulationskinetik kolloider losungen. Z Phys Chem 1917; 92: 129-168.
    PubMedGoogle Scholar
  • 43 Levich VG. Physicochemical hydrodynamics. Englewood Cliffs, NJ: Prentice Hall; 1962
    Google Scholar
  • 44 Jansson JH, Nilsson TK, Johnson O. von Willebrand factor in plasma: a novel risk factor for recurrent myocardial infarction and death. Heart 1991; 66: 351-355.
    CrossrefPubMedGoogle Scholar
  • 45 Johansson L, Jansson JH, Boman K. et al. Prospective study on soluble thrombomodulin and von Willebrand factor and the risk of ischemic and hemorrhagic stroke. Thromb Haemost 2002; 87: 211-217.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 46 Elena IS, Dmitry AK, Nadezhda YP. et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost 2007; 97: 425-434.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 47 Zwaal RF, Schroit AJ. Pathophysiologic impli-cationsof membrane phospholipid asymmetry in blood cells. Blood 1997; 89: 1121-1132.
    PubMedGoogle Scholar
  • 48 Hsu-Lin S, Berman CL, Furie BC. et al. A platelet membrane protein expressed during platelet activation and secretion. Studies using a monoclonal antibody specific for thrombinactivated platelets. J Biol Chem 1984; 259: 9121-9126.
    PubMedGoogle Scholar
  • 49 Belval T, Hellums JD, Solis RT. The kinetics of platelet aggregation induced by fluidshearing stress. Microvasc Res 1984; 28: 279-288.
    CrossrefPubMedGoogle Scholar
  • 50 Belval TK, Hellums JD. Analysis of shear-induced platelet aggregation with population balance mathematics. Biophys J 1986; 50: 479-487.
    CrossrefPubMedGoogle Scholar