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Methods Paper

Measurement of whole blood thrombus formation using parallel-plate flow chambers – a practical guide

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Pages 229-242 | Received 22 Jun 2011, Accepted 06 Oct 2011, Published online: 13 Apr 2012

References

  • Gibbins JM. Platelet adhesion signalling and the regulation of thrombus formation. J Cell Sci 2004; 117: 3415–3425
  • Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res 2007; 100: 1673–1685
  • Munnix IC, Cosemans JM, Auger JM, Heemskerk JW. Platelet response heterogeneity in thrombus formation. Thromb Haemost 2009; 102: 1149–1156
  • Zwaginga JJ, Nash G, King MR, Heemskerk JW, Frojmovic M, Hoylaerts MF, Sakariassen KS. Flow-based assays for global assessment of hemostasis. Part 1: Biorheologic considerations. J Thromb Haemost 2006; 4: 2486–2487
  • Zwaginga JJ, Sakariassen KS, Nash G, King MR, Heemskerk JW, Frojmovic M, Hoylaerts MF. Flow-based assays for global assessment of hemostasis. Part 2: Current methods and considerations for the future. J Thromb Haemost 2006, 4:2716–2717
  • Sakariassen KS, Aarts PA, de Groot PG, Houdijk WP, 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: 522–535
  • De Groot PG, IJsseldijk MJW, Sixma JJ. Platelet adhesion to the subendothelium under flow. Methods Mol Biol 1999; 96: 159–170
  • Sakariassen KS, Hanson SR, Cadroy Y. Methods and models to evaluate shear-dependent and surface reactivity-dependent antithrombotic efficacy. Thromb Res 2001; 104: 149–174
  • Neeves KB, Maloney SF, Fong KP, Schmaier AA, Kahn ML, Brass LF, Diamond SL. Microfluidic focal thrombosis model for measuring murine platelet deposition and stability: PAR4 signaling enhances shear-resistance of platelet aggregates. J Thromb Haemost 2008; 6: 2193–2201
  • Roest M, Reininger A, Zwaginga JJ, King MR, Heemskerk JWM, the Biorheology Subcommittee of the SSC of the ISTH. Flow chamber-based assays to measure thrombus formation in vitro: Requirements for standardization. J Thromb Haemost 2011, [Epub ahead of print]
  • Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mohtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fässler R. Glycoprotein VI but not a2b1 integrin is essential for platelet interaction with collagen. EMBO J 2001; 20: 2120–2130
  • Lecut C, Schoolmeester A, Kuijpers MJ, Broers JL, van Zandvoort MA, Vanhoorelbeke K, Deckmyn H, Jandrot-Perrus M, Heemskerk JW. Principal role of glycoprotein VI in a2b1 and aIIbb3 activation during collagen-induced thrombus formation. Arterioscler Thromb Vasc Biol 2004; 24: 1727–1733
  • Kuijpers MJ, Schulte V, Bergmeier W, Lindhout T, Brakebusch C, Offermanns S, Fassler R, Heemskerk JW, Nieswandt B. Complementary roles of glycoprotein VI and a2b1 integrin in collagen-induced thrombus formation in flowing whole blood ex vivo. FASEB J 2003; 17: 685–687
  • Bergmeier W, Oh-Hora M, McCarl CA, Roden RC, Bray PF, Feske S. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 2009; 113: 675–678
  • Savage B, Ginsberg MH, Ruggeri ZM. Influence of fibrillar collagen structure on the mechanisms of platelet thrombus formation under flow. Blood 1999; 94: 2704–2715
  • Wu YP, de Groot PG, Sixma JJ. Shear-stress-induced detachment of blood platelets from various surfaces. Arterioscler Thromb Vasc Biol 1997; 17: 3202–3207
  • Cosemans JM, Kuijpers MJ, Lecut C, Loubele ST, Heeneman S, Jandrot-Perrus M, Heemskerk JW. Contribution of platelet glycoprotein VI to the thrombogenic effect of collagens in fibrous atherosclerotic lesions. Atherosclerosis 2005; 181: 19–27
  • Zhao XM, Wu YP, Cai HX, Wei R, Lisman T, Han JJ, Xia ZL, de Groot PG. The influence of the pulsatility of the blood flow on the extent of platelet adhesion. Thromb Res 2008; 121: 821–825
  • Munnix IC, Gilio K, Siljander PR, Raynal N, Feijge MA, Hackeng TM, Deckmyn H, Smethurst PA, Farndale RW, Heemskerk JW. Collagen-mimetic peptides mediate flow-dependent thrombus formation by high- or low-affinity binding of integrin a2b1 and glycoprotein VI. J Thromb Haemost 2008; 6: 2132–2142
  • Pugh N, Simpson AM, Smethurst PA, de Groot PG, Raynal N, Farndale RW. Synergism between platelet collagen receptors defined using receptor-specific collagen-mimetic peptide substrata in flowing blood. Blood 2010; 115: 5069–5079
  • Lisman T, Raynal N, Groeneveld D, Maddox B, Peachey AR, Huizinga EG, de Groot PG, Farndale RW. A single high-affinity binding site for von Willebrand factor in collagen III, identified using synthetic triple-helical peptides. Blood 2006; 108: 3753–3756
  • 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
  • Maxwell MJ, Dopheide SM, Turner SJ, Jackson SP. Shear induces a unique series of morphological changes in translocating platelets: Effects of morphology on translocation dynamics. Arterioscler Thromb Vasc Biol 2006; 26: 663–669
  • Elvers M, Stegner D, Hagedorn I, Kleinschnitz C, Braun A, Kuijpers ME, Boesl M, Chen Q, Heemskerk JW, Stoll G, et al. Impaired aIIbb3 integrin activation and shear-dependent thrombus formation in mice lacking phospholipase D1. Sci Signal 2010; 3: ra1
  • Beumer S, IJsseldijk MJ, de Groot PG, Sixma JJ. 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
  • Zaidi TN, McIntire LV, Farrell DH, Thiagarajan P. Adhesion of platelets to surface-bound fibrinogen under flow. Blood 1996; 88: 2967–2972
  • Kuijpers MJ, Nieuwenhuys CM, Feijge MA, Kloots W, Giesen PL, Jerling JC, oude Egbrink MG, Heemskerk JW. Regulation of tissue factor-induced coagulation and platelet aggregation in flowing whole blood. Thromb Haemost 2005; 93: 97–105
  • Jen CJ, Lin JS. Direct observation of platelet adhesion to fibrinogen- and fibrin-coated surfaces. Am J Physiol 1991; 261: H1457–H1463
  • Endenburg SC, Hantgan RR, Lindeboom-Blokzijl L, Lankhof H, Jerome WG, Lewis JC, Sixma JJ, de Groot PG. On the role of von Willebrand factor in promoting platelet adhesion to fibrin in flowing blood. Blood 1995; 86: 4158–4165
  • Keuren JF, Baruch D, Legendre P, Denis CV, Lenting PJ, Girma JP, Lindhout T. von Willebrand factor C1C2 domain is involved in platelet adhesion to polymerized fibrin at high shear rate. Blood 2004; 103: 1741–1746
  • Hindriks G, IJsseldijk MJ, Sonnenberg A, Sixma JJ, de Groot PG. Platelet adhesion to laminin: Role of Ca2+ and Mg2+ ions, shear rate, and platelet membrane glycoproteins. Blood 1992; 79: 928–935
  • Inoue O, Suzuki-Inoue K, Ozaki Y. Redundant mechanism of platelet adhesion to laminin and collagen under flow: Involvement of von Willebrand factor and glycoprotein Ib-IX-V. J Biol Chem 2008; 283: 16279–16282
  • Penz SM, Reininger AJ, Toth O, Deckmyn H, Brandl R, Siess W. Glycoprotein Ibalpha inhibition and ADP receptor antagonists, but not aspirin, reduce platelet thrombus formation in flowing blood exposed to atherosclerotic plaques. Thromb Haemost 2007; 97: 435–443
  • Reininger AJ, Bernlochner I, Penz SM, Ravanat C, Smethurst P, Farndale RW, Gachet C, Brandl R, Siess W. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol 2011; 55: 1147–1158
  • Nergiz-Unal R, Cosemans JM, Feijge MA, van der Meijden PE, Storey RF, van Giezen JJ, oude Egbrink MG, Heemskerk JW, Kuijpers MJ. Stabilizing role of platelet P2Y12 receptors in shear-dependent thrombus formation on ruptured plaques. Plos One 2010; 5: e10130
  • Saelman EU, Kehrel B, Hese KM, de Groot PG, Sixma JJ, Nieuwenhuis HK. Platelet adhesion to collagen and endothelial cell matrix under flow conditions is not dependent on platelet glycoprotein IV. Blood 1994; 83: 3240–3244
  • Nieswandt B, Watson SP. Platelet-collagen interaction: Is GPVI the central receptor?. Blood 2003; 102: 449–461
  • Auger JM, Kuijpers MJ, Senis YA, Watson SP, Heemskerk JW. Adhesion of human and mouse platelets to collagen under shear: A unifying model. FASEB J 2005; 19: 825–827
  • Jackson SP, Mistry N, Yuan YP. Platelets and the injured vessel wall: Rolling into action. Focus on glycoprotein Ib/V/IX and the platelet cytoskeleton. Trends Cardiovasc Med 2000; 10: 192–197
  • Kuijpers MJ, Schulte V, Oury C, Lindhout T, Broers J, Hoylaerts MF, Nieswandt B, Heemskerk JW. Facilitating roles of murine platelet glycoprotein Ib and aIIbb3 in phosphatidylserine exposure during vWF-collagen-induced thrombus formation. J Physiol 2004; 558: 403–415
  • Jackson SP. The growing complexity of platelet aggregation. Blood 2007; 109: 5087–5095
  • Heemskerk JW, Sakariassen KS, Zwaginga JJ, Brass LF, Jackson SP, Farndale RW, the Biorheology Subcommittee of the SSC, of the ISTH. Collagen surfaces to measure thrombus formation under flow: Possibilities for standardization. J Thromb Haemost 2011; 9: 856–858
  • Sixma JJ, de Groot PG. Regulation of platelet adhesion to the vessel wall. Ann N Y Acad Sci 1994; 714: 190–199
  • Ruggeri ZM. Platelet adhesion under flow. Microcirculation 2009; 16: 58–83
  • Lisman T, Adelmeijer J, Cauwenberghs S, Van Pampus EC, Heemskerk JW, De Groot PG. Recombinant factor VIIa enhances platelet adhesion and activation under flow conditions at normal and reduced platelet count. J Thromb Haemost 2005; 3: 742–751
  • Okorie UM, Diamond SL. Matrix protein microarrays for spatially and compositionally controlled microspot thrombosis under laminar flow. Biophys J 2006; 91: 3474–3481
  • Berny MA, Munnix IC, Auger JM, Schols SE, Cosemans JM, Panizzi P, Bock PE, Watson SP, McCarty OJ, Heemskerk JW. Spatial distribution of factor Xa, thrombin, and fibrin(ogen) on thrombi at venous shear. PLoS One 2010; 5: e10415
  • Munnix IC, Kuijpers MJ, Auger J, Thomassen CM, Panizzi P, van Zandvoort MA, Rosing J, Bock PE, Watson SP, Heemskerk JW. Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation: Regulation by transient integrin activation. Arterioscler Thromb Vasc Biol 2007; 27: 2484–2490
  • Cosemans JM, Iserbyt BF, Deckmyn H, Heemskerk JW. Multiple pathways to switch platelet integrins on and off. J Thromb Haemost 2008; 6: 1253–1261
  • Heemskerk JW, Bevers EM, Lindhout T. Platelet activation and blood coagulation. Thromb Haemost 2002; 88: 186–193
  • Brass LF. Thrombin and platelet activation. Chest 2003; 124: 18S–25S
  • Van der Meijden PE, Munnix IC, Auger JM, Govers-Riemslag JW, Cosemans JM, Kuijpers MJ, Spronk HM, Watson SP, Renne T, Heemskerk JW. Dual role of collagen in factor XII-dependent thrombus formation. Blood 2009; 114: 881–890
  • Munnix IC, Strehl A, Kuijpers MJ, Auger JM, van der Meijden PE, van Zandvoort MA, oude Egbrink MG, Nieswandt B, Heemskerk JW. The glycoprotein VI-phospholipase Cg2 signaling pathway controls thrombus formation induced by collagen and tissue factor in vitro and in vivo. Arterioscler Thromb Vasc Biol 2005; 25: 2673–2678
  • Diamond SL. Tissue factor activity under flow. Thromb Res 2010; 125: S29–S30
  • Cosemans JM, Munnix IC, Wetzker R, Heller R, Jackson SP, Heemskerk JW. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood 2006; 108: 3045–3052
  • Maxwell MJ, Westein E, Nesbitt WS, Giuliano S, Dopheide SM, Jackson SP. Identification of a 2-stage platelet aggregation process mediating shear-dependent thrombus formation. Blood 2007; 109: 566–576
  • Meyer dos Santos S, Klinkhardt U, Schneppenheim R, Harder S. Using ImageJ for the quantitative analysis of flow-based adhesion assays in real-time under physiologic flow conditions. Platelets 2010; 21: 60–66
  • Heemskerk JW, Willems GM, Rook MB, Sage SO. Ragged spiking of free calcium in ADP-stimulated human platelets: Regulation of puff-like calcium signals in vitro and ex vivo. J Physiol 2001; 535: 625–635
  • Nesbitt WS, Giuliano S, Kulkarni S, Dopheide SM, Harper IS, Jackson SP. Intercellular calcium communication regulates platelet aggregation and thrombus growth. J Cell Biol 2003; 160: 1151–1161
  • Gilio K, Munnix IC, Mangin P, Cosemans JM, Feijge MA, van der Meijden PE, Olieslagers S, Chrzanowska-Wodnicka MB, Lillian R, Schoenwaelder S, et al. Non-redundant roles of phosphoinositide 3-kinase isoforms alpha and beta in glycoprotein VI-induced platelet signaling and thrombus formation. J Biol Chem 2009; 284: 33750–33762
  • Siljander PR, Munnix IC, Smethurst PA, Deckmyn H, Lindhout T, Ouwehand WH, Farndale RW, Heemskerk JW. Platelet receptor interplay regulates collagen-induced thrombus formation in flowing human blood. Blood 2004; 103: 1333–1341
  • Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, Fu J, Carberry J, Fouras A, Jackson SP. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 2009; 15: 665–673
  • Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood 2001; 98: 1456–1463
  • Ono A, Westein E, Hsiao S, Nesbitt WS, Hamilton JR, Schoenwaelder SM, Jackson SP. Identification of a fibrin-independent platelet contractile mechanism regulating primary hemostasis and thrombus growth. Blood 2008; 112: 90–99
  • Auger JM, Watson SP. Dynamic tyrosine kinase-regulated signaling and actin polymerisation mediate aggregate stability under shear. Arterioscler Thromb Vasc Biol 2008; 28: 1499–1504
  • Goto S, Tamura N, Ishida H, Ruggeri ZM. Dependence of platelet thrombus stability on sustained glycoprotein IIb/IIIa activation through adenosine 5′-diphosphate receptor stimulation and cyclic calcium signaling. J Am Coll Cardiol 2006; 47: 155–162
  • Cosemans JM, Van Kruchten R, Olieslagers S, Schurgers LJ, Verheyen FK, Munnix IC, Waltenberger J, Angelillo-Scherrer A, Hoylaerts MF, Carmeliet P, et al. Potentiating role of Gas6 and Tyro3, Axl and Mer (TAM) receptors in human and murine platelet activation and thrombus stabilization. J Thromb Haemost 2010; 8: 1797–1808
  • Kuijpers MJ, Pozgajova M, Cosemans JM, Munnix IC, Eckes B, Nieswandt B, Heemskerk JW. Role of murine integrin a2b1 in thrombus stabilization and embolization: Contribution of thromboxane A2. Thromb Haemost 2007; 98: 1072–1080
  • Cosemans JM, Schols SE, Stefanini L, de Witt S, Feijge MA, Hamulyak K, Deckmyn H, Bergmeier W, Heemskerk JW. Key role of glycoprotein Ib/V/IX and von Willebrand factor in platelet activation-dependent fibrin formation at low shear flow. Blood 2011; 117: 651–660
  • Mizuno T, Sugimoto M, Matsui H, Hamada M, Shida Y, Yoshioka A. Visual evaluation of blood coagulation during mural thrombogenesis under high shear blood flow. Thromb Res 2008; 121: 855–864
  • Van de Walle G, Schoolmeester A, Iserbyt BF, Cosemans JM, Heemskerk JW, Hoylaerts MF, Nurden A, Vanhoorelbeke K, Deckmyn H. Activation of aIIbb3 is sufficient but also an imperative prerequisite to activate a2b1 on platelets. Blood 2007; 109: 595–602
  • Gilio K, Harper MT, Cosemans JM, Konopatskaya O, Munnix IC, Prinzen L, Leitges M, Liu Q, Molkentin JD, Heemskerk JW, et al. Functional divergence of platelet protein kinase C (PKC) isoforms in thrombus formation on collagen. J Biol Chem 2010; 285: 23410–23419
  • Kulkarni S, Woollard KJ, Thomas S, Oxley D, Jackson SP. Conversion of platelets from a proaggregatory to a proinflammatory adhesive phenotype: Role of PAF in spatially regulating neutrophil adhesion and spreading. Blood 2007; 110: 1879–1886
  • Hu H, Zhu L, Huang Z, Ji Q, Chatterjee M, Zhang W, Li N. Platelets enhance lymphocyte adhesion and infiltration into arterial thrombus. Thromb Haemost 2011; 104: 1184–1192
  • Cattaneo M. Bleeding manifestations of congenital and drug-induced defects of the platelet P2Y12 receptor for adenosine diphosphate. Thromb Haemost 2011; 105(Suppl. 1)S67–S74
  • Storey RF. Pharmacology and clinical trials of reversibly-binding P2Y12 inhibitors. Thromb Haemost 2011; 105(Suppl. 1)S75–S81
  • Gurbel PA, Tantry US. Clopidogrel response variability and the advent of personalised antiplatelet therapy. A bench to bedside journey. Thromb Haemost 2011; 106: 265–271
  • Siller-Matula JM, Krumphuber J, Jilma B. Pharmacokinetic, pharmacodynamic and clinical profile of novel antiplatelet drugs targeting vascular diseases. Br J Pharmacol 2010; 159: 502–517
  • Bossavy JP, Thalamas C, Sagnard L, Barret A, Sakariassen K, Boneu B, Cadroy Y. A double-blind randomized comparison of combined aspirin and ticlopidine therapy versus aspirin or ticlopidine alone on experimental arterial thrombogenesis in humans. Blood 1998; 92: 1518–1525
  • Cadroy Y, Bossavy JP, Thalamas C, Sagnard L, Sakariassen K, Boneu B. Early potent antithrombotic effect with combined aspirin and a loading dose of clopidogrel on experimental arterial thrombogenesis in humans. Circulation 2000; 101: 2823–2828
  • Mendolicchio GL, Zavalloni D, Bacci M, Corrada E, Marconi M, Lodigiani C, Presbitero P, Rota L, Ruggeri ZM. Variable effect of P2Y12 inhibition on platelet thrombus volume in flowing blood. J Thromb Haemost 2011; 9: 373–382
  • Sakakibara M, Goto S, Eto K, Tamura N, Isshiki T, Handa S. Application of ex vivo flow chamber system for assessment of stent thrombosis. Arterioscler Thromb Vasc Biol 2002; 22: 1360–1364
  • Andre P, LaRocca T, Delaney SM, Lin PH, Vincent D, Sinha U, Conley PB, Phillips DR. Anticoagulants (thrombin inhibitors) and aspirin synergize with P2Y12 receptor antagonism in thrombosis. Circulation 2003; 108: 2697–2703
  • Favaloro EJ. Clinical utility of the PFA-100. Semin Thromb Hemost 2008; 34: 709–733
  • Michelson AD. Methods for the measurement of platelet function. Am J Cardiol 2009; 103: 20A–26A
  • Tsuji S, Sugimoto M, Miyata S, Kuwahara M, Kinoshita S, Yoshioka A. Real-time analysis of mural thrombus formation in various platelet aggregation disorders: Distinct shear-dependent roles of platelet receptors and adhesive proteins under flow. Blood 1999; 94: 968–975
  • Sugimoto M, Matsui H, Mizuno T, Tsuji S, Miyata S, Matsumoto M, Matsuda M, Fujimura Y, Yoshioka A. Mural thrombus generation in type 2A and 2B von Willebrand disease under flow conditions. Blood 2003; 101: 915–920
  • Zwaginga JJ, Sakariassen KS, King MR, Diacovo TG, Grabowski EF, Nash G, Hoylaerts M, Heemskerk JW. Can blood flow assays help to identify clinically relevant differences in von Willebrand factor functionality in von Willebrand disease types 1–3?. J Thromb Haemost 2007; 5: 2547–2549

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