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Thromb Haemost 2011; 105(05): 776-782
DOI: 10.1160/TH10-12-0771
Theme Issue Article
Schattauer GmbH

Imaging fibrin formation and platelet and endothelial cell activation in vivo

Lola Bellido-Martin   *
1   Division of Hemostasis and Thrombosis, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Massachussetts, USA
,
Vivien Chen   *
1   Division of Hemostasis and Thrombosis, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Massachussetts, USA
,
Reema Jasuja   *
1   Division of Hemostasis and Thrombosis, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Massachussetts, USA
,
Bruce Furie
2   Harvard Medical School, Boston, Massachussetts, USA
,
Barbara C. Furie
2   Harvard Medical School, Boston, Massachussetts, USA
› Institutsangaben Financial support:This work was supported by grants from the National Institutes of Health to B.F. and B.C.F. R.J. is a recipient of a fellowship from the American Heart Association and V.M.C. is a recipient of a grant from the National Health and Medical Research Council of Australia.
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Publikationsverlauf

Received: 04. Dezember 2010

Accepted after minor revision: 04. Februar 2011

Publikationsdatum:
28. November 2017 (online)

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Summary

Over the past six decades research employing in vitro assays has identified enzymes, cofactors, cell receptors and associated ligands important to the haemostatic process and its regulation. These studies have greatly advanced our understanding of the molecular and cellular bases of haemostasis and thrombosis. However, in vitro assays cannot simultaneously reproduce the interactions of all of the components of the haemostatic process that occur in vivo nor do they reflect the importance of haemodynamic factors resulting from blood flow. To overcome these limitations investigators have increasingly turned to animal models of haemostasis and thrombosis. In this article we describe some advances in the visualisation of platelet and endothelial cell activation and blood coagulation in vivo and review what we have learned from our intravital microscopy experiments using primarily the laser-induced injury model for thrombosis.

Keywords

Animal models - thrombosis - intravital imaging

* These authors contributed equally to the preparation of this review.


 

  • References

  • 1 Day SM, Reeve JL, Myers DD. et al. Murine thrombosis models. Thromb Haemost 2004; 92: 486-494.
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 2 Westrick RJ, Winn ME, Eitzman DT. Murine models of vascular thrombosis (Eitzman series). Arterioscler Thromb Vasc Biol 2007; 27: 2079-2093.
    CrossrefPubMedGoogle Scholar
  • 3 Sachs UJ, Nieswandt B. In vivo thrombus formation in murine models. Circ Res 2007; 100: 979-991.
    CrossrefPubMedGoogle Scholar
  • 4 Reimann-Hunziger G. Uber experimentelle Thrombose und ihre Behandlung mit Heparin. Schweizerische Medizinische Wochenschrift 1944; 74: 66-69.
    PubMedGoogle Scholar
  • 5 Kurz KD, Main BW, Sandusky GE. Rat model of arterial thrombosis induced by ferric chloride. Thromb Res 1990; 60: 269-280.
    CrossrefPubMedGoogle Scholar
  • 6 Denis C, Methia N, Frenette PS. et al. A mouse model of severe von Willebrand disease: defects in haemostasis and thrombosis. Proc Natl Acad Sci USA 1998; 95: 9524-9529.
    CrossrefPubMedGoogle Scholar
  • 7 Dubois C, Panicot-Dubois L, Merrill-Skoloff G. et al. Glycoprotein VI-dependent and -independent pathways of thrombus formation in vivo. Blood 2006; 107: 3902-3906.
    CrossrefPubMedGoogle Scholar
  • 8 Balla G, Vercellotti GM, Eaton JW. et al. Iron loading of endothelial cells augments oxidant damage. J Lab Clin Med 1990; 116: 546-554.
    PubMedGoogle Scholar
  • 9 Tseng MT, Dozier A, Haribabu B. et al. Transendothelial migration of ferric ion in FeCl3 injured murine common carotid artery. Thromb Res 2006; 118: 275-280.
    CrossrefPubMedGoogle Scholar
  • 10 Kawamura Y, Takahari Y, Tamura N. et al. Imaging of structural changes in endothelial cells and thrombus formation at the site of FeCl(3)-induced injuries in mice cremasteric arteries. J Atheroscler Thromb 2009; 16: 807-814.
    PubMedGoogle Scholar
  • 11 Arfors KE, Dhall DP, Engeset J. et al. In vivo quantitation of platelet activity using biolaser-induced endothelial injury. Bibl Anat 1969; 10: 502-506.
    PubMedGoogle Scholar
  • 12 Rosen ED, Raymond S, Zollman A. et al. Laser-induced noninvasive vascular injury models in mice generate platelet- and coagulation-dependent thrombi. Am J Pathol 2001; 158: 1613-1622.
    CrossrefPubMedGoogle Scholar
  • 13 Falati S, Gross P, Merrill-Skoloff G. et al. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med 2002; 8: 1175-1181.
    CrossrefPubMedGoogle Scholar
  • 14 Nonne C, Lenain N, Hechler B. et al. Importance of platelet phospholipase Cgamma2 signaling in arterial thrombosis as a function of lesion severity. Arterioscler Thromb Vasc Biol 2005; 25: 1293-1298.
    CrossrefPubMedGoogle Scholar
  • 15 Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med 2008; 359: 938-949.
    CrossrefPubMedGoogle Scholar
  • 16 Hechler B, Nonne C, Eckly A. et al. Arterial thrombosis: relevance of a model with two levels of severity assessed by histologic, ultrastructural and functional characterization. J Thromb Haemost 2010; 8: 173-184.
    CrossrefPubMedGoogle Scholar
  • 17 Kulkarni S, Nesbitt WS, Dopheide SM. et al. Techniques to examine platelet adhesive interactions under flow. Methods Mol Biol 2004; 272: 165-186.
    PubMedGoogle Scholar
  • 18 Celi A, Merrill-Skoloff G, Gross P. et al. Thrombus formation: Direct real time observation and digital analysis of thrombus assembly in a living mouse by confocal and widefield intravital microscopy. J Thromb Haemost 2003; 1: 60-68.
    CrossrefPubMedGoogle Scholar
  • 19 Flaumenhaft R, Tanaka E, Graham GJ. et al. Localization and quantification of platelet-rich thrombi in large blood vessels with near-infrared fluorescence imaging. Circulation 2007; 115: 84-93.
    PubMedGoogle Scholar
  • 20 Frenette PS, Johnson RC, Hynes RO. et al. Platelets roll on stimulated endothelium in vivo: an interaction mediated by endothelial P-selectin. Proc Natl Acad Sci USA 1995; 92: 7450-7454.
    CrossrefPubMedGoogle Scholar
  • 21 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.
    CrossrefPubMedGoogle Scholar
  • 22 Bergmeier W, Schulte V, Brockhoff G. et al. Flow cytometric detection of activated mouse integrin alphaIIbbeta3 with a novel monoclonal antibody. Cytometry 2002; 48: 80-86.
    CrossrefPubMedGoogle Scholar
  • 23 Berny MA, Munnix IC, Auger JM. et al. Spatial distribution of factor Xa, thrombin, and fibrin(ogen) on thrombi at venous shear. PLoS One 2010; 5: e10415.
    CrossrefPubMedGoogle Scholar
  • 24 Hayashi T, Mogami H, Murakami Y. et al. Real-time analysis of platelet aggregation and procoagulant activity during thrombus formation in vivo. Pflugers Arch 2008; 456: 1239-1251.
    CrossrefPubMedGoogle Scholar
  • 25 Yang J, Wu J, Kowalska M. et al. Loss of signaling through the G protein, Gz, results in abnormal platelet activation and altered responses to psychoactive drugs. Proc Natl Acad Sci USA 2000; 97: 9984-9989.
    CrossrefPubMedGoogle Scholar
  • 26 Prinzen L, Miserus RJ, Dirksen A. et al. Optical and magnetic resonance imaging of cell death and platelet activation using annexin a5-functionalized quantum dots. Nano Lett 2007; 7: 93-100.
    CrossrefPubMedGoogle Scholar
  • 27 Mangin P, Yap CL, Nonne C. et al. Thrombin overcomes the thrombosis defect associated with platelet GPVI/FcRgamma deficiency. Blood 2006; 107: 4346-4353.
    CrossrefPubMedGoogle Scholar
  • 28 Cho J, Furie BC, Coughlin SR. et al. A critical role for extracellular protein disulfide isomerase during thrombus formation in mice. J Clin Invest 2008; 118: 1123-1131.
    PubMedGoogle Scholar
  • 29 Chou J, Mackman N, Merrill-Skoloff G. et al. Hematopoietic Cell-Derived Micro-particle Tissue Factor Contributes to Fibrin Formation During Thrombus Propagation. Blood 2004; 104: 3190-3197.
    CrossrefPubMedGoogle Scholar
  • 30 Dubois C, Panicot-Dubois L, Gainor JF. et al. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J Clin Invest 2007; 117: 953-960.
    CrossrefPubMedGoogle Scholar
  • 31 Vandendries ER, Hamilton JR, Coughlin SR. et al. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc Natl Acad Sci USA 2007; 104: 288-292.
    CrossrefPubMedGoogle Scholar
  • 32 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.
    CrossrefPubMedGoogle Scholar
  • 33 Massberg S, Gawaz M, Gruner S. et al. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197: 41-49.
    CrossrefPubMedGoogle Scholar
  • 34 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.
    CrossrefPubMedGoogle Scholar
  • 35 Jasuja R, Furie B, Furie BC. Endothelium-derived but not platelet-derived protein disulfide isomerase is required for thrombus formation in vivo. Blood 2010; 116: 4665-4674.
    CrossrefPubMedGoogle Scholar
  • 36 Falati S, Liu Q, Gross P. et al. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003; 197: 1585-1598.
    CrossrefPubMedGoogle Scholar
  • 37 Atkinson BT, Jasuja R, Chen VM. et al. Laser-induced endothelial cell activation supports fibrin formation. Blood 2010; 116: 4675-4683.
    CrossrefPubMedGoogle Scholar
  • 38 Chen VM, Hogg PJ. Allosteric disulfide bonds in thrombosis and thrombolysis. J Thromb Haemost 2006; 4: 2533-2541.
    CrossrefPubMedGoogle Scholar
  • 39 Chen K, Detwiler TC, Essex DW. Characterization of protein disulphide isomerase released from activated platelets. Br J Haematol 1995; 90: 425-431.
    CrossrefPubMedGoogle Scholar
  • 40 Essex DW, Chen K, Swiatkowska M. Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood 1995; 86: 2168-2173.
    PubMedGoogle Scholar
  • 41 Hotchkiss KA, Matthias LJ, Hogg PJ. Exposure of the cryptic Arg-Gly-Asp sequence in thrombospondin-I by protein disulfide isomerase. Biochem Biophys Acta 1998; 1388: 478-488.
    CrossrefPubMedGoogle Scholar
  • 42 Reinhardt C, von Bruhl ML, Manukyan D. et al. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008; 118: 1110-1122.
    PubMedGoogle Scholar
  • 43 Ahamed J, Versteeg HH, Kerver M. et al. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 2006; 103: 13932-13937.
    CrossrefPubMedGoogle Scholar
  • 44 Chen VM, Ahamed J, Versteeg HH. et al. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 2006; 45: 12020-12028.
    CrossrefPubMedGoogle Scholar
  • 45 Liang HP, Hogg PJ. Critical importance of the cell system when studying tissue factor de-encryption. Blood 2008; 112: 912-913.
    CrossrefPubMedGoogle Scholar
  • 46 Versteeg H, Ruf WR. Tissue factor coagulant function is enhanced by protein-disulfide isomerase independent of oxidoreductase activity. J Biol Chem 2007; 282: 25416-25424.
    CrossrefPubMedGoogle Scholar
  • 47 Ruf W, Versteeg HH. Tissue factor mutated at the allosteric Cys186-Cys209 disulfide bond is severely impaired in decrypted procoagulant activity. Blood 2010; 116: 500-501.
    PubMedGoogle Scholar
  • 48 Kothari H, Nayak RC, Rao LV. et al. Cystine 186-cystine 209 disulfide bond is not essential for the procoagulant activity of tissue factor or for its de-encryption. Blood 2010; 115: 4273-4283.
    CrossrefPubMedGoogle Scholar
  • 49 Pendurthi U, Ghosh S, Mandal S. et al. Tissue factor activation: is disulfide bond switching a regulatory mechanism?. Blood 2007; 110: 3900-3908.
    CrossrefPubMedGoogle Scholar
  • 50 Bach RR, Monroe D. What is wrong with the allosteric disulfide bond hypothesis?. Arterioscler Thromb Vasc Biol 2009; 29: 1997-1998.
    CrossrefPubMedGoogle Scholar
  • 51 Popescu NI, Lupu C, Lupu F. Extracellular protein disulfide isomerase regulates coagulation on endothelial cells through modulation of phosphatidylserine exposure. Blood 2010; 116: 993-1001.
    CrossrefPubMedGoogle Scholar
  • 52 Kothari H, Rao L, Pendurthi UR. Cys186-Cys209 disulfide-mutated tissue factor does not equal cryptic tissue factor: no impairment in decryption of disulfide mutated tissue factor. Blood 2010; 116: 502-503.
    CrossrefPubMedGoogle Scholar
  • 53 Kamocka MM, Mu J, Liu X. et al. Two-photon intravital imaging of thrombus development. J Biomed Opt 2010; 15: 016020.
    CrossrefPubMedGoogle Scholar