1932

Abstract

The vasculature is a dynamic environment in which blood platelets constantly survey the endothelium for sites of vessel damage. The formation of a mechanically coherent hemostatic plug to prevent blood loss relies on a coordinated series of ligand–receptor interactions governing the recruitment, activation, and aggregation of platelets. The physical biology of each step is distinct in that the recruitment of platelets depends on the mechanosensing of the platelet receptor glycoprotein Ib for the adhesive protein von Willebrand factor, whereas platelet activation and aggregation are responsive to the mechanical forces sensed at adhesive junctions between platelets and at the platelet–matrix interface. Herein we take a biophysical perspective to discuss the current understanding of platelet mechanotransduction as well as the measurement techniques used to quantify the physical biology of platelets in the context of thrombus formation under flow.

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2018-06-04
2024-04-21
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Literature Cited

  1. 1.  Qiu Y, Ciciliano J, Myers DR, Tran R, Lam WA 2015. Platelets and physics: how platelets “feel” and respond to their mechanical microenvironment. Blood Rev 29:377–86
    [Google Scholar]
  2. 2.  Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL 1996. Platelets and shear stress. Blood 88:1525
    [Google Scholar]
  3. 3.  Tschopp TB, Weiss HJ, Baumgartner HR 1974. Decreased adhesion of platelets to subendothelium in von Willebrand's disease. J. Lab. Clin. Med. 83:296–300
    [Google Scholar]
  4. 4.  Sakariassen KS, Nievelstein PFEM, Coller BS, Sixma JJ 1986. The role of platelet membrane glycoproteins Ib and IIb-IIIa in platelet adherence to human artery subendothelium. Br. J. Haematol. 63:681–91
    [Google Scholar]
  5. 5.  Weiss HJ, Tschopp TB, Baumgartner HR 1975. Impaired interaction (adhesion-aggregation) of platelets with the subendothelium in storage-pool disease and after aspirin ingestion. N. Engl. J. Med. 293:619–23
    [Google Scholar]
  6. 6.  Chen C, Ofenloch JC, Yianni YP, Hanson SR, Lumsden AB 1998. Phosphorylcholine coating of ePTFE reduces platelet deposition and neointimal hyperplasia in arteriovenous grafts. J. Surg. Res. 77:119–25
    [Google Scholar]
  7. 7.  Hanson SR, Kotze HF, Savage B, Harker LA 1985. Platelet interactions with Dacron vascular grafts. A model of acute thrombosis in baboons. Arterioscler. Thromb. Vasc. Biol. 5:595–603
    [Google Scholar]
  8. 8.  Roald HE, Barstad RM, Bakken IJ, Roald B, Lyberg T, Sakariassen KS 1994. Initial interactions of platelets and plasma proteins in flowing non-anticoagulated human blood with the artificial surfaces Dacron and PTFE. Blood Coagul. Fibrinolysis 5:355–63
    [Google Scholar]
  9. 9.  Chow TW, Hellums JD, Moake JL, Kroll MH 1992. Shear stress–induced von Willebrand factor binding to platelet glycoprotein Ib initiates calcium influx associated with aggregation. Blood 80:113–20
    [Google Scholar]
  10. 10.  Furukawa K, Ushida T, Sugano H, Ohshima N, Tateishi T 1999. Real time observation of platelet adhesion to opaque biomaterial surfaces under shear flow conditions. J. Biomed. Mater. Res. 46:93–102
    [Google Scholar]
  11. 11.  Panzer S, Badr Eslam R, Schneller A, Kaider A, Koren D et al. 2010. Loss of high-molecular-weight von Willebrand factor multimers mainly affects platelet aggregation in patients with aortic stenosis. Thromb. Haemost. 103:408–14
    [Google Scholar]
  12. 12.  Hubbell JA, McIntire LV 1986. Visualization and analysis of mural thrombogenesis on collagen, polyurethane and nylon. Biomaterials 7:354–63
    [Google Scholar]
  13. 13.  Sakariassen KS, Aarts PA, de Groot PG, Houdijk WP, Sixma JJ 1983. 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. 102:522–35
    [Google Scholar]
  14. 14.  Sakariassen KS, Kuhn H, Muggli R, Baumgartner HR 1988. Growth and stability of thrombi in flowing citrated blood: assessment of platelet–surface interactions with computer-assisted morphometry. Thromb. Haemost. 60:392–98
    [Google Scholar]
  15. 15.  Zilberman-Rudenko J, McCarty OJT 2017. Utility and development of microfluidic platforms for platelet research. Platelets 28:425–26
    [Google Scholar]
  16. 16.  Feghhi S, Sniadecki NJ 2011. Mechanobiology of platelets: techniques to study the role of fluid flow and platelet retraction forces at the micro- and nano-scale. Int. J. Mol. Sci. 12:9009–30
    [Google Scholar]
  17. 17.  Schoeman RM, Lehmann M, Neeves KB 2017. Flow chamber and microfluidic approaches for measuring thrombus formation in genetic bleeding disorders. Platelets 28:463–71
    [Google Scholar]
  18. 18.  McCarty OJT, Ku D, Sugimoto M, King MR, Cosemans JMEM et al. 2016. Dimensional analysis and scaling relevant to flow models of thrombus formation: communication from the SSC of the ISTH. J. Thromb. Haemost. 14:619–22
    [Google Scholar]
  19. 19.  Colace T, Fogarty PF, Panckeri KA, Li R, Diamond SL 2014. Microfluidic assay of hemophilic blood clotting: distinct deficits in platelet and fibrin deposition at low factor levels. J. Thromb. Haemost. 12:147–58
    [Google Scholar]
  20. 20.  Neeves KB, Maloney SF, Fong KP, Schmaier AA, Kahn ML et al. 2008. Microfluidic focal thrombosis model for measuring murine platelet deposition and stability: PAR4 signaling enhances shear resistance of platelet aggregates. J. Thromb. Haemost. 6:2193–201
    [Google Scholar]
  21. 21.  de Witt SM, Swieringa F, Cavill R, Lamers MME, van Kruchten R et al. 2014. Identification of platelet function defects by multi-parameter assessment of thrombus formation. Nat. Commun. 5:4257
    [Google Scholar]
  22. 22.  Branchford BR, Ng CJ, Neeves KB, Di Paola J 2015. Microfluidic technology as an emerging clinical tool to evaluate thrombosis and hemostasis. Thromb. Res. 136:13–19
    [Google Scholar]
  23. 23.  Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS 2003. Cells lying on a bed of microneedles: an approach to isolate mechanical force. PNAS 100:1484–89
    [Google Scholar]
  24. 24.  Liang XM, Han SJ, Reems J-A, Gao D, Sniadecki NJ 2010. Platelet retraction force measurements using flexible post force sensors. Lab Chip 10:991–98
    [Google Scholar]
  25. 25.  Casuso I, Rico F, Scheuring S 2011. Biological AFM: where we come from—where we are—where we may go. J. Mol. Recognit. 24:406–13
    [Google Scholar]
  26. 26.  Lam WA, Chaudhuri O, Crow A, Webster KD, Li T-D et al. 2011. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat. Mater. 10:61–66
    [Google Scholar]
  27. 27.  Yago T, Lou J, Wu T, Yang J, Miner JJ et al. 2008. Platelet glycoprotein Ibα forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J. Clin. Investig. 118:3195–3207
    [Google Scholar]
  28. 28.  Hanley W, McCarty OJT, Jadhav S, Tseng Y, Wirtz D, Konstantopoulos K 2003. Single molecule characterization of P-selectin/ligand binding. J. Biol. Chem. 278:10556–61
    [Google Scholar]
  29. 29.  Gourier C, Jegou A, Husson J, Pincet F 2008. A nanospring named erythrocyte. The biomembrane force probe. Cell. Mol. Bioeng. 1:263
    [Google Scholar]
  30. 30.  Ju L, Chen Y, Xue L, Du X, Zhu C 2016. Cooperative unfolding of distinctive mechanoreceptor domains transduces force into signals. eLife 5:e15447
    [Google Scholar]
  31. 31.  Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG et al. 2014. Platelet mechanosensing of substrate stiffness during clot formation mediates adhesion, spreading, and activation. PNAS 111:14430–35
    [Google Scholar]
  32. 32.  Kee MF, Myers DR, Sakurai Y, Lam WA, Qiu Y 2015. Platelet mechanosensing of collagen matrices. PLOS ONE 10:e0126624
    [Google Scholar]
  33. 33.  Myers DR, Qiu Y, Fay ME, Tennenbaum M, Chester D et al. 2016. Single-platelet nanomechanics measured by high-throughput cytometry. Nat. Mater. 16:230–35
    [Google Scholar]
  34. 34.  Sadler JE 1998. Biochemistry and genetics of von Willebrand factor. Annu. Rev. Biochem. 67:395–424
    [Google Scholar]
  35. 35.  Sporn LA, Marder VJ, Wagner DD 1986. Inducible secretion of large, biologically potent von Willebrand factor multimers. Cell 46:185–90
    [Google Scholar]
  36. 36.  Kanaji S, Fahs SA, Shi Q, Haberichter SL, Montgomery RR 2012. Contribution of platelet versus endothelial VWF to platelet adhesion and hemostasis. J. Thromb. Haemost. 10:1646–52
    [Google Scholar]
  37. 37.  Wagner DD 1982. Immunolocalization of von Willebrand protein in Weibel–Palade bodies of human endothelial cells. J. Cell Biol. 95:355–60
    [Google Scholar]
  38. 38.  Cramer EM, Meyer D, le Menn R, Breton-Gorius J 1985. Eccentric localization of von Willebrand factor in an internal structure of platelet α-granule resembling that of Weibel–Palade bodies. Blood 66:710
    [Google Scholar]
  39. 39.  Nightingale T, Cutler D 2013. The secretion of von Willebrand factor from endothelial cells: an increasingly complicated story. J. Thromb. Haemost. 11:Suppl. 1192–201
    [Google Scholar]
  40. 40.  Padilla A 2004. P-selectin anchors newly released ultralarge von Willebrand factor multimers to the endothelial cell surface. Blood 103:2150–56
    [Google Scholar]
  41. 41.  Springer TA 2014. Von Willebrand factor, Jedi knight of the bloodstream. Blood 124:1412–25
    [Google Scholar]
  42. 42.  Pareti FI, Niiya K, McPherson JM, Ruggeri ZM 1987. Isolation and characterization of two domains of human von Willebrand factor that interact with fibrillar collagen types I and III. J. Biol. Chem. 262:13835–41
    [Google Scholar]
  43. 43.  Siediecki CA, Lestini BJ, Kottke-Marchant KK, Eppell SJ, Wilson DL, Marchant RE 1996. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 88:2939–50
    [Google Scholar]
  44. 44.  Schneider SW, Nuschele S, Wixforth A, Gorzelanny C, Alexander-Katz A et al. 2007. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. PNAS 104:7899–903
    [Google Scholar]
  45. 45.  Sing CE, Alexander-Katz A 2010. Elongational flow induces the unfolding of von Willebrand factor at physiological flow rates. Biophys. J. 98:L35–37
    [Google Scholar]
  46. 46.  Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A et al. 2009. A shear gradient–dependent platelet aggregation mechanism drives thrombus formation. Nat. Med. 15:665–73
    [Google Scholar]
  47. 47.  Fu H, Jiang Y, Yang D, Scheiflinger F, Wong WP, Springer TA 2017. Flow-induced elongation of von Willebrand factor precedes tension-dependent activation. Nat. Commun. 8:324
    [Google Scholar]
  48. 48.  Dong JF 2002. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 100:4033–39
    [Google Scholar]
  49. 49.  Crawley JTB, de Groot R, Xiang Y, Luken BM, Lane DA 2011. Unraveling the scissile bond: how ADAMTS13 recognizes and cleaves von Willebrand factor. Blood 118:3212–21
    [Google Scholar]
  50. 50.  Zhang X, Halvorsen K, Zhang C-Z, Wong WP, Springer TA 2009. Mechanoenzymatic cleavage of the ultralarge vascular protein, von Willebrand factor. Science 324:1330–34
    [Google Scholar]
  51. 51.  Furlan M, Robles R, Lamie B 1996. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood 87:4223
    [Google Scholar]
  52. 52.  Soejima K, Mimura N, Hirashima M, Maeda H, Hamamoto T et al. 2001. A novel human metalloprotease synthesized in the liver and secreted into the blood: possibly, the von Willebrand factor–cleaving protease?. J. Biochem. 130:475–80
    [Google Scholar]
  53. 53.  Savage B, Saldívar E, Ruggeri ZM 1996. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84:289–97
    [Google Scholar]
  54. 54.  Li R, Emsley J 2013. The organizing principle of platelet glycoprotein Ib–IX–V complex. J. Thromb. Haemost. 11:605–14
    [Google Scholar]
  55. 55.  Bergmeier W, Piffath CL, Goerge T, Cifuni SM, Ruggeri ZM et al. 2006. The role of platelet adhesion receptor GPIbα far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. PNAS 103:16900–5
    [Google Scholar]
  56. 56.  Huizinga EG 2002. Structures of glycoprotein Ibα and its complex with von Willebrand factor A1 domain. Science 297:1176–79
    [Google Scholar]
  57. 57.  Deng W, Xu Y, Chen W, Paul DS, Syed AK et al. 2016. Platelet clearance via shear-induced unfolding of a membrane mechanoreceptor. Nat. Commun. 7:12863
    [Google Scholar]
  58. 58.  Kim J, Zhang C-Z, Zhang X, Springer TA 2010. A mechanically stabilized receptor–ligand flex-bond important in the vasculature. Nature 466:992–95
    [Google Scholar]
  59. 59.  Ju L, Lou J, Chen Y, Li Z, Zhu C 2015. Force-induced unfolding of leucine-rich repeats of glycoprotein Ibα strengthens ligand interaction. Biophys. J. 109:1781–84
    [Google Scholar]
  60. 60.  Ruggeri ZM, Orje JN, Habermann R, Federici AB, Reininger AJ 2006. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108:1903–10
    [Google Scholar]
  61. 61.  Aslan JE, Itakura A, Gertz JM, McCarty OJT 2012. Platelet shape change and spreading. Platelets and Megakaryocytes, vol. 3: Additional Protocols and Perspectives JM Gibbins, MP Mahaut-Smith 91–100 New York: Springer
    [Google Scholar]
  62. 62.  Zhang W, Deng W, Zhou L, Xu Y, Yang W et al. 2015. Identification of a juxtamembrane mechanosensitive domain in the platelet mechanosensor glycoprotein Ib–IX complex. Blood 125:562–69
    [Google Scholar]
  63. 63.  Deng W, Li R 2015. Juxtamembrane contribution to transmembrane signaling. Biopolymers 104:317–22
    [Google Scholar]
  64. 64.  Dai K, Bodnar R, Berndt MC, Du X 2005. A critical role for 14–3–3ζ protein in regulating the VWF binding function of platelet glycoprotein Ib–IX and its therapeutic implications. Blood 106:1975–81
    [Google Scholar]
  65. 65.  Senis YA, Mazharian A, Mori J 2014. Src family kinases: at the forefront of platelet activation. Blood 124:2013–24
    [Google Scholar]
  66. 66.  Yin H, Liu J, Li Z, Berndt MC, Lowell CA, Du X 2008. Src family tyrosine kinase Lyn mediates vWF/GPIb-IX-induced platelet activation via the cGMP signaling pathway. Blood 112:1139–46
    [Google Scholar]
  67. 67.  Delaney MK, Liu J, Zheng Y, Berndt MC, Du X 2012. A role for Rac1 in glycoprotein Ib-IX-mediated signal transduction and integrin activation. Arterioscler. Thromb. Vasc. Biol. 32:2761–68
    [Google Scholar]
  68. 68.  Stojanovic A, Marjanovic JA, Brovkovych VM, Peng X, Hay N et al. 2006. A phosphoinositide 3-kinase–AKT–nitric oxide–cGMP signaling pathway in stimulating platelet secretion and aggregation. J. Biol. Chem. 281:16333–39
    [Google Scholar]
  69. 69.  Yin H, Stojanovic A, Hay N, Du X 2008. The role of Akt in the signaling pathway of the glycoprotein Ib-IX-induced platelet activation. Blood 111:658–65
    [Google Scholar]
  70. 70.  Li Z, Zhang G, Feil R, Han J, Du X 2006. Sequential activation of p38 and ERK pathways by cGMP-dependent protein kinase leading to activation of the platelet integrin αIIbβ3. Blood 107:965–72
    [Google Scholar]
  71. 71.  Falati S, Edmead CE, Poole AW 1999. Glycoprotein Ib-V-IX, a receptor for von Willebrand factor, couples physically and functionally to the Fc receptor γ-chain, Fyn, and Lyn to activate human platelets. Blood 94:1648
    [Google Scholar]
  72. 72.  McCarty OJT, Calaminus SDJ, Berndt MC, Machesky LM, Watson SP 2006. Von Willebrand factor mediates platelet spreading through glycoprotein Ib and αIIbβ3 in the presence of botrocetin and ristocetin, respectively. J. Thromb. Haemost. 4:1367–78
    [Google Scholar]
  73. 73.  Okorie UM, Diamond SL 2006. Matrix protein microarrays for spatially and compositionally controlled microspot thrombosis under laminar flow. Biophys. J. 91:3474–81
    [Google Scholar]
  74. 74.  Santoro SA, Walsh JJ, Staatz WD, Baranski KJ 1991. Distinct determinants on collagen support α2β1 integrin–mediated platelet adhesion and platelet activation. Cell Regul 2:905–13
    [Google Scholar]
  75. 75.  Inoue O, Suzuki-Inoue K, McCarty OJT, Moroi M, Ruggeri ZM et al. 2006. Laminin stimulates spreading of platelets through integrin α6β1–dependent activation of GPVI. Blood 107:1405–12
    [Google Scholar]
  76. 76.  Nuyttens BP, Thijs T, Deckmyn H, Broos K 2011. Platelet adhesion to collagen. Thromb. Res. 127:S26–29
    [Google Scholar]
  77. 77.  Tsuji M, Ezumi Y, Arai M, Takayama H 1997. A novel association of Fc receptor γ-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. J. Biol. Chem. 272:23528–31
    [Google Scholar]
  78. 78.  Quek LS, Pasquet J-M, Hers I, Cornall R, Knight G et al. 2000. Fyn and Lyn phosphorylate the Fc receptor γ chain downstream of glycoprotein VI in murine platelets, and Lyn regulates a novel feedback pathway. Blood 96:4246
    [Google Scholar]
  79. 79.  Watson SP, Auger JM, McCarty OJT, Pearce AC 2005. GPVI and integrin αIIbβ3 signaling in platelets. J. Thromb. Haemost. 3:1752–62
    [Google Scholar]
  80. 80.  Carrim N, Walsh TG, Consonni A, Torti M, Berndt MC, Metharom P 2014. Role of focal adhesion tyrosine kinases in GPVI-dependent platelet activation and reactive oxygen species formation. PLOS ONE 9:e113679
    [Google Scholar]
  81. 81.  Stefanini L, Bergmeier W 2010. CalDAG-GEFI and platelet activation. Platelets 21:239–43
    [Google Scholar]
  82. 82.  Cifuni SM, Wagner DD, Bergmeier W 2008. CalDAG-GEFI and protein kinase C represent alternative pathways leading to activation of integrin αIIbβ3 in platelets. Blood 112:1696–1703
    [Google Scholar]
  83. 83.  Akbar H, Shang X, Perveen R, Berryman M, Funk K et al. 2011. Gene targeting implicates Cdc42 GTPase in GPVI and non-GPVI mediated platelet filopodia formation, secretion and aggregation. PLOS ONE 6:e22117
    [Google Scholar]
  84. 84.  Aslan JE, Itakura A, Haley KM, Tormoen GW, Loren CP et al. 2013. P21 activated kinase signaling coordinates glycoprotein receptor VI–mediated platelet aggregation, lamellipodia formation, and aggregate stability under shear. Arterioscler. Thromb. Vasc. Biol. 33:1544–51
    [Google Scholar]
  85. 85.  Calaminus SD, McCarty OJT, Auger JM, Pearce AC, Insall RH et al. 2007. A major role for Scar/WAVE-1 downstream of GPVI in platelets. J. Thromb. Haemost. 5:535–41
    [Google Scholar]
  86. 86.  Siljander PRM, Hamaia S, Peachey AR, Slatter DA, Smethurst PA et al. 2004. Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J. Biol. Chem. 279:47763–72
    [Google Scholar]
  87. 87.  Inoue O, Suzuki-Inoue K, Dean WL, Frampton J, Watson SP 2003. Integrin α2β1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLCγ2. J. Cell Biol. 160:769–80
    [Google Scholar]
  88. 88.  Manganaro D, Consonni A, Guidetti GF, Canobbio I, Visconte C et al. 2015. Activation of phosphatidylinositol 3-kinase β by the platelet collagen receptors integrin α2β1 and GPVI: the role of Pyk2 and c-Cbl. Biochim. Biophys. Acta 1853:1879–88
    [Google Scholar]
  89. 89.  Consonni A, Cipolla L, Guidetti G, Canobbio I, Ciraolo E et al. 2012. Role and regulation of phosphatidylinositol 3-kinase in platelet integrin α2β1 signaling. Blood 119:847–56
    [Google Scholar]
  90. 90.  Marjoram RJ, Li Z, He L, Tollefsen DM, Kunicki TJ et al. 2014. α2β1 integrin, GPVI receptor, and common FcRγ chain on mouse platelets mediate distinct responses to collagen in models of thrombosis. PLOS ONE 9:e114035
    [Google Scholar]
  91. 91.  Mazzucato M, Cozzi MR, Battiston M, Jandrot-Perrus M, Mongiat M et al. 2009. Distinct spatio-temporal Ca2+ signaling elicited by integrin α2β1 and glycoprotein VI under flow. Blood 114:2793–801
    [Google Scholar]
  92. 92.  McCarty OJT, Zhao Y, Andrew N, Machesky LM, Staunton D et al. 2004. Evaluation of the role of platelet integrins in fibronectin-dependent spreading and adhesion. J. Thromb. Haemost. 2:1823–33
    [Google Scholar]
  93. 93.  Lee D, Fong KP, King MR, Brass LF, Hammer DA 2012. Differential dynamics of platelet contact and spreading. Biophys. J. 102:472–82
    [Google Scholar]
  94. 94.  Weisel JW 2007. Structure of fibrin: impact on clot stability. J. Thromb. Haemost. 5:116–24
    [Google Scholar]
  95. 95.  Litvinov RI, Farrell DH, Weisel JW, Bennett JS 2016. The platelet integrin αIIbβ3 differentially interacts with fibrin versus fibrinogen. J. Biol. Chem. 291:7858–67
    [Google Scholar]
  96. 96.  Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, Shattil SJ 2003. Src kinase activation by direct interaction with the integrin β cytoplasmic domain. PNAS 100:13298–302
    [Google Scholar]
  97. 97.  Naik MU, Naik TU, Summer R, Naik UP 2017. Binding of CIB1 to the αIIb tail of αIIbβ3 is required for FAK recruitment and activation in platelets. PLOS ONE 12:e0176602
    [Google Scholar]
  98. 98.  Wonerow P, Pearce AC, Vaux DJ, Watson SP 2003. A critical role for phospholipase Cγ2 in αIIbβ3-mediated platelet spreading. J. Biol. Chem. 278:37520–29
    [Google Scholar]
  99. 99.  Giuliano S, Nesbitt WS, Rooney M, Jackson SP 2003. Bidirectional integrin αIIbβ3 signalling regulating platelet adhesion under flow: contribution of protein kinase C. Biochem. J. 372:163–72
    [Google Scholar]
  100. 100.  Pelletier AJ, Bodary SC, Levinson AD 1992. Signal transduction by the platelet integrin αIIbβ3: induction of calcium oscillations required for protein-tyrosine phosphorylation and ligand-induced spreading of stably transfected cells. Mol. Biol. Cell. 3:989–98
    [Google Scholar]
  101. 101.  Pearce AC, McCarty OJT, Calaminus SDJ, Vigorito E, Turner M, Watson SP 2007. Vav family proteins are required for optimal regulation of PLCγ2 by integrin αIIbβ3. Biochem. J. 401:753–61
    [Google Scholar]
  102. 102.  McCarty OJT, Larson MK, Auger JM, Kalia N, Atkinson BT et al. 2005. Rac1 is essential for platelet lamellipodia formation and aggregate stability under flow. J. Biol. Chem. 280:39474–84
    [Google Scholar]
  103. 103.  Aslan JE, Tormoen GW, Loren CP, Pang J, McCarty OJT 2011. S6K1 and mTOR regulate Rac1-driven platelet activation and aggregation. Blood 118:3129–36
    [Google Scholar]
  104. 104.  Stefanini L, Boulaftali Y, Ouellette TD, Holinstat M, Desire L et al. 2012. Rap1–Rac1 circuits potentiate platelet activation. Arterioscler. Thromb. Vasc. Biol. 32:434–41
    [Google Scholar]
  105. 105.  Goncalves I, Nesbitt WS, Yuan Y, Jackson SP 2005. Importance of temporal flow gradients and integrin αIIbβ3 mechanotransduction for shear activation of platelets. J. Biol. Chem. 280:15430–37
    [Google Scholar]
  106. 106.  Munnix ICA, Cosemans JMEM, Auger JM, Heemskerk JWM 2009. Platelet response heterogeneity in thrombus formation. Thromb. Haemost. 102:1149–56
    [Google Scholar]
  107. 107.  Nguyen T-H, Palankar R, Bui V-C, Medvedev N, Greinacher A, Delcea M 2016. Rupture forces among human blood platelets at different degrees of activation. Sci. Rep. 6:25402
    [Google Scholar]
  108. 108.  Colace T, Falls E, Zheng XL, Diamond SL 2011. Analysis of morphology of platelet aggregates formed on collagen under laminar blood flow. Ann. Biomed. Eng. 39:922–29
    [Google Scholar]
  109. 109.  Pinar IP, Arthur JF, Andrews RK, Gardiner EE, Ryan K, Carberry J 2015. Methods to determine the Lagrangian shear experienced by platelets during thrombus growth. PLOS ONE 10:e0144860
    [Google Scholar]
  110. 110.  Shi X, Yang J, Huang J, Long Z, Ruan Z et al. 2016. Effects of different shear rates on the attachment and detachment of platelet thrombi. Mol. Med. Rep. 13:2447–56
    [Google Scholar]
  111. 111.  Jen CJ, McIntire LV 2005. The structural properties and contractile force of a clot. Cell Motil 2:445–55
    [Google Scholar]
  112. 112.  Sylman JL, Daalkhaijav U, Zhang Y, Gray EM, Farhang PA et al. 2017. Differential roles for the coagulation factors XI and XII in regulating the physical biology of fibrin. Ann. Biomed. Eng. 45:1328–40
    [Google Scholar]
  113. 113.  Wufsus AR, Rana K, Brown A, Dorgan JR, Liberatore MW, Neeves KB 2015. Elastic behavior and platelet retraction in low- and high-density fibrin gels. Biophys. J. 108:173–83
    [Google Scholar]
  114. 114.  Muthard RW, Diamond SL 2012. Blood clots are rapidly assembled hemodynamic sensors: Flow arrest triggers intraluminal thrombus contraction. Arterioscler. Thromb. Vasc. Biol. 32:2938–45
    [Google Scholar]
  115. 115.  Brown AEX, Litvinov RI, Discher DE, Purohit PK, Weisel JW 2009. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325:741–44
    [Google Scholar]
  116. 116.  Feghhi S, Tooley WW, Sniadecki NJ 2016. Nonmuscle myosin IIA regulates platelet contractile forces through Rho kinase and myosin light-chain kinase. J. Biomech. Eng. 138:104506
    [Google Scholar]
  117. 117.  Feghhi S, Munday AD, Tooley WW, Rajsekar S, Fura AM et al. 2016. Glycoprotein Ib–IX–V complex transmits cytoskeletal forces that enhance platelet adhesion. Biophys. J. 111:601–8
    [Google Scholar]
  118. 118.  Jones CM, Baker-Groberg SM, Cianchetti FA, Glynn JJ, Healy LD et al. 2014. Measurement science in the circulatory system. Cell. Mol. Bioeng. 7:1–14
    [Google Scholar]
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