Download PDF
Thromb Haemost 2013; 109(01): 61-71
DOI: 10.1160/TH12-05-0279
Blood Coagulation, Fibrinolysis and Cellular Haemostasis
Schattauer GmbH

Enhanced binding of tissue factor-microparticles to collagen-IV and fibronectin leads to increased tissue factor activity in vitro

Camille Ettelaie   *
1   Biomedical Section, Department of Biological Sciences, University of Hull, Cottingham Road, Hull, UK
,
Mary E. W. Collier
1   Biomedical Section, Department of Biological Sciences, University of Hull, Cottingham Road, Hull, UK
,
Mah Pui Mei
1   Biomedical Section, Department of Biological Sciences, University of Hull, Cottingham Road, Hull, UK
,
Yu Pei Xiao
1   Biomedical Section, Department of Biological Sciences, University of Hull, Cottingham Road, Hull, UK
,
Anthony Maraveyas
2   Division of Cancer, Hull York Medical School, University of Hull, Cottingham Road, Hull, UK
› Author Affiliations
Further Information

Publication History

Received: 01 May 2012

Accepted after major revision: 09 October 2012

Publication Date:
27 November 2017 (online)

Also available at
    Permissions and Reprints

Summary

The role of tissue factor (TF)-containing microparticles in clot propagation has been established, but the ability of circulating microparticles to initiate coagulation has been disputed. However, TF-bearing microparticles, particularly endothelial-microparticles generated during disease, may interact with extracellular matrices which in turn can localise circulating TF to sites of injury. In order to examine this hypothesis in vitro, microparticles were isolated from human coronary artery endothelial cells transfected to overexpress TF, tumour-necrosis factor (TNF)α-treated cells or non-transfected cells lacking TF. The ability of microparticles to bind collagen-IV, fibronectin and fibrin was examined under static conditions and arterial shear rates (650 s-1), and also in the presence of inhibitory antibodies against β1-, β3-, α3-and αv-integrins or an anti-TF antibody. TF-microparticles showed increases of up to 43% and 24% in adherence to collagen-IV and fibronectin, respectively, compared to control microparticles under shear flow. Furthermore, TF-containing microparticles, but not the transfected parent cells had increased levels of β1-integrin compared to TF-deficient microparticles. Pre-incubation of microparticles with a β1-integrin-blocking antibody counteracted the additional adhesion of TFmicroparticles compared to control microparticles. Finally, adherence of TF microparticles to collagen-IV or fibronectin resulted in increased TF activity by concentrating TF onto the surface. In conclusion, the presence of TF within microparticles enhances the interactions of endothelial cell-derived microparticles with extracellular matrices in an integrin-dependent manner. Accumulation and localisation of these microparticles in turn results in the enhancement of TF activity. This may be an innate mechanism by which TF-bearing microparticles induce coagulation upon vascular injury.

Keywords

Tissue factor - endothelial-derived microparticles - extracellular matrices - integrins - procoagulant activity

* C.E. and M.E.W.C. contributed equally to this study.


 

  • References

  • 1 Chironi GN, Boulanger CM, Simon A. et al. Endothelial microparticles in diseases. Cell Tissue Res 2008; 335: 143-151. DOI:10.1007/s00441-008-0710-9.
    PubMedSearch in Google Scholar
  • 2 Rautou PE, Vion AC, Amabile N. et al. Microparticles, vascular function, and atherothrombosis. Circ Res 2011; 109: 593-606. DOI:10.1161/CIRCRESAHA.110.233163.
    CrossrefPubMedSearch in Google Scholar
  • 3 Morel O, Hugel B, Jesel L. et al. Procoagulant membranous microparticles and atherothrombotic complications in diabetics. Arch Mal Coeur Vaiss 2004; 97: 1006-1012.
    PubMedSearch in Google Scholar
  • 4 VanWijk MJ, VanBavel E, Struk A. et al. Microparticles in cardiovascular diseases. Cardiovasc Res 2003; 59: 277-287. DOI:10.1016/S0008-6363(03)00367-5.
    CrossrefPubMedSearch in Google Scholar
  • 5 Martínez MC, Tesse A, Zobairi F. et al. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol 2005; 288: H1004-1009. DOI:10.1152/ajpheart.00842.2004.
    CrossrefPubMedSearch in Google Scholar
  • 6 Jimenez JJ, Jy W, Mauro LM. et al. Endothelial microparticles (EMP) as vascular disease markers. Adv Clin Chem 2005; 39: 131-157.
    PubMedSearch in Google Scholar
  • 7 Gross PL, Furie BC, Merrill-Skoloff G. et al. Leukocyte-versus microparticle-mediated tissue factor transfer during arteriolar thrombus development. J Leukoc Biol 2005; 78: 1318-1326. DOI:10.1189/jlb.0405193.
    CrossrefPubMedSearch in Google Scholar
  • 8 Biró E, Sturk-Maquelin KN, Vogel GM. et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 2005; 01: 2561-2568. DOI:10.1046/j.1538-7836.2003.00456.x.
    PubMedSearch in Google Scholar
  • 9 Abid Hussein MN, Böing AN, Biró E. et al. Phospholipid composition of in vitro endothelial microparticles and their in vivo thrombogenic properties. Thromb Res 2008; 121: 865-871. DOI:10.1016/j.thromres.2007.08.005.
    CrossrefPubMedSearch in Google Scholar
  • 10 Horstman LL, Jy W, Jimenez JJ. et al. Endothelial microparticles as markers of endothelial dysfunction. Front Biosci 2004; 09: 1118-1135. DOI:10.2741/1270.
    CrossrefPubMedSearch in Google Scholar
  • 11 Mallat Z, Hugel B, Ohan J. et al. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99: 348-353. DOI:10.1161/01.CIR.99.3.348.
    CrossrefPubMedSearch in Google Scholar
  • 12 Leroyer AS, Isobe H, Lesèche G. et al. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J. Am. Coll. Cardiol 2007; 49: 772-777.
    CrossrefPubMedSearch in Google Scholar
  • 13 Biró E, Sturk-Maquelin KN, Vogel GM. et al. Microparticle-mediated thrombin generation assay: increased activity in patients with recurrent thrombosis. J Thromb Haemost 2008; 06: 913-919. DOI:10.1111/j.1538-7836.2008.02963.x.
    CrossrefPubMedSearch in Google Scholar
  • 14 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; 08: 1175-1181. DOI:10.1038/nm782.
    CrossrefPubMedSearch in Google Scholar
  • 15 Chou J, Mackman N, Merrill-Skoloff G. et al. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004; 104: 3190-3197. DOI:10.1182/blood-2004-03-0935.
    CrossrefPubMedSearch in Google Scholar
  • 16 Diamond SL. Tissue factor activity under flow. Thromb. Res 2010; 125 (Suppl. 01) S29-30.
    CrossrefPubMedSearch in Google Scholar
  • 17 Zwicker JI, Trenor 3rd CC, Furie BC. et al. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol 2011; 31: 728-733. DOI:10.1161/ATVBAHA.109.200964.
    CrossrefPubMedSearch in Google Scholar
  • 18 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. DOI:10.1084/jem.20021868.
    CrossrefPubMedSearch in Google Scholar
  • 19 Ramacciotti E, Hawley AE, Farris DM. et al. Leukocyte- and platelet-derived microparticles correlate with thrombus weight and tissue factor activity in an experimental mouse model of venous thrombosis. Thromb Haemost 2009; 101: 748-754.
    Thieme ConnectPubMedSearch in Google Scholar
  • 20 Furie B, Furie BC. In vivo thrombus formation. J Thromb Haemost 2007; 05 (Suppl. 01) 12-17. DOI:10.1111/j.1538-7836.2007.02482.x.
    PubMedSearch in Google Scholar
  • 21 Colace TV, Jobson J, Diamond SL. Relipidated tissue factor linked to collagen surfaces potentiates platelet adhesion and fibrin formation in a microfluidic model of vessel injury. Bioconjug Chem 2011; 22: 2104-2109. DOI:10.1021/bc200326v.
    CrossrefPubMedSearch in Google Scholar
  • 22 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. DOI:10.1111/j.1365-2141.2007.06650.x.
    CrossrefPubMedSearch in Google Scholar
  • 23 Merten M, Pakala R, Thiagarajan P. et al. Platelet microparticles promote platelet interaction with subendothelial matrix in a glycoprotein IIb/IIIa-dependent mechanism. Circulation 1999; 99: 2577-2582. DOI:10.1161/01.CIR.99.19.2577.
    CrossrefPubMedSearch in Google Scholar
  • 24 Collier ME, Ettelaie C. Regulation of the incorporation of tissue factor into microparticles by serine phosphorylation of the cytoplasmic domain of tissue factor. J Biol Chem 2011; 286: 11977-11984. DOI:10.1074/jbc.M110.195214.
    CrossrefPubMedSearch in Google Scholar
  • 25 Collier ME, Ettelaie C. Induction of endothelial cell proliferation by recombinant and microparticle-tissue factor involves beta1-integrin and extracellular signal regulated kinase activation. Arterioscler Thromb Vasc Biol 2010; 30: 1810-1817. DOI:10.1161/ATVBAHA.110.211854.
    CrossrefPubMedSearch in Google Scholar
  • 26 Ettelaie C, Fountain D, Collier MEW. et al. Low molecular weight heparin downregulates tissue factor expression and activity by modulating growth factor receptor-mediated induction of nuclear factor-κB. Biochim Biophys Acta Mol Basis Dis 2011; 1812: 591-600. DOI:10.1016/j.bbadis.2011.09.007.
    PubMedSearch in Google Scholar
  • 27 Ettelaie C, Su S, Li C. et al. Tissue factor-containing microparticles released from mesangial cells in response to high glucose and AGE induce tube formation in microvascular cells. Microvasc Res 2008; 76: 152-160. DOI:10.1016/j.mvr.2008.07.007.
    CrossrefPubMedSearch in Google Scholar
  • 28 Bonnekoh B, Wevers A, Jugert F. et al. Colorimetric growth assay for epidermal cell cultures by their crystal violet binding capacity. Arch Dermatol Res 1989; 281: 487-490. DOI:10.1007/BF00510085.
    CrossrefPubMedSearch in Google Scholar
  • 29 Collier ME, Li C, Ettelaie C. Influence of exogenous tissue factor on estrogen receptor alpha expression in breast cancer cells: involvement of beta1-integrin, PAR2, and mitogen-activated protein kinase activation. Mol Cancer Res 2008; 06: 1807-1818. DOI:10.1158/1541-7786.MCR-08-0109.
    CrossrefPubMedSearch in Google Scholar
  • 30 Kuharsky AL, Fogelson AL. Surface-mediated control of blood coagulation: the role of binding site densities and platelet deposition. Biophys J 2001; 80: 1050-1074. DOI:10.1016/S0006-3495(01)76085-7.
    CrossrefPubMedSearch in Google Scholar
  • 31 Pluskota E, Woody NM, Szpak D. et al. Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood 2008; 112: 2327-2335. DOI:10.1182/blood-2007-12-127183.
    CrossrefPubMedSearch in Google Scholar
  • 32 Versteeg HH, Schaffner F, Kerver M. et al. Inhibition of tissue factor signaling suppresses tumor growth. Blood 2008; 111: 190-199. DOI:10.1182/blood-2007-07-101048.
    CrossrefPubMedSearch in Google Scholar
  • 33 Schecter AD, Spirn B, Rossikhina M. et al. Release of active tissue factor by human arterial smooth muscle cells. Circ Res 2000; 87: 126-132. DOI:10.1161/01.RES.87.2.126.
    CrossrefPubMedSearch in Google Scholar
  • 34 Furlan-Freguia C, Marchese P, Gruber A. et al. P2X7 receptor signaling contributes to tissue factor-dependent thrombosis in mice. J Clin Invest 2011; 121: 2932-2944. DOI:10.1172/JCI46129.
    CrossrefPubMedSearch in Google Scholar
  • 35 Patchipulusu S, Turturro M, Hall CL. Monocyte-derived macrophage microparticles impart tissue factor activity to biomaterial surfaces. J Biomed Mater Res A 2010; 92: 724-732.
    PubMedSearch in Google Scholar