Thromb Haemost 2002; 87(06): 1062-1068
DOI: 10.1055/s-0037-1613133
Review Article
Schattauer GmbH

Tissue Factor Activity Is Upregulated in Human Endothelial Cells Exposed to Oscillatory Shear Stress

Lucia Mazzolai
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
,
Paolo Silacci
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
,
Karima Bouzourene
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
,
François Daniel
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
,
Hans Brunner
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
,
Daniel Hayoz
1   Division of Hypertension and Vascular Medicine, CHUV, Lausanne, Switzerland
› Author Affiliations
Further Information

Publication History

Received 19 November 2001

Accepted after revision 20 February 2002

Publication Date:
08 December 2017 (online)

Summary

Hemodynamic forces play a critical role in the pathogenesis of atherosclerosis as evidenced by the focal nature of the disease. Oscillatory shear stress characterizes the hemodynamic environment of plaque-prone areas as opposed to unidirectional shear stress typical of plaque-free areas. These particular flow conditions modulate atherosclerosis-related genes. Tissue factor (TF) initiates blood coagulation, contributes to vascular remodeling, and is therefore a potential contributor in the development/progression of atherosclerosis. We investigated the effect of oscillatory and unidirectional flows on TF using an in vitro perfusion system. Human endothelial cells exposed for 24 h to oscillatory shear stress, significantly increased TF mRNA, and TF protein expression (1.5-and 1.75-fold, respectively, p <0.01), and surface TF activity (twofolds-increase). Expression of TF inhibitor (TFPI), mRNA and protein, remained unchanged as compared to static conditions. Conversely, cells exposed to unidirectional shear, showed a decrease in TF activity with a significant increase in TFPI mRNA and protein expression (1.5-and 1.8-fold, respectively, p <0.01). These results show for the first time that pulsatile oscillatory shear stress induces a procoagulant phenotype of endothelial cells which may favor formation/progression of atherothrombotic lesions.

 
  • References

  • 1 Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcationPositive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 1985; 05 (03) 293-302.
  • 2 Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999; 282 (21) 2035-42.
  • 3 Mackman N. Regulation of the tissue factor gene. Thromb Haemost 1997; 78 (01) 747-54.
  • 4 Nemerson Y. Tissue factor and hemostasis. Blood 1988; 71 (01) 1-8.
  • 5 Osterud B. Tissue factor: a complex biological role. Thromb Haemost 1997; 78 (01) 755-8.
  • 6 Thiruvikraman SV, Guha A, Roboz J, Taubman MB, Nemerson Y, Fallon JT. In situ localization of tissue factor in human atherosclerotic plaques by binding of digoxigenin-labeled factors VIIa and X. Lab Invest 1996; 75 (04) 451-61.
  • 7 Hatakeyama K, Asada Y, Marutsuka K, Sato Y, Kamikubo Y, Sumiyoshi A. Localization and activity of tissue factor in human aortic atherosclerotic lesions. Atherosclerosis 1997; 133 (02) 213-9.
  • 8 Ardissino D, Merlini PA, Bauer KA, Bramucci E, Ferrario CM, Coppola R, Fetiveau R, Lucreziotti S, Rosenberg RD, Mannucci PM. Thrombogenic potential of human coronary atherosclerotic plaques. Blood 2001; 98 (09) 2726-9.
  • 9 Contrino J, Hair G, Kreutzer DL, Rickles FR. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996; 02 (02) 209-15.
  • 10 Lin MC, Almus-Jacobs F, Chen HH, Parry GC, Mackman N, Shyy JY, Chien S. Shear stress induction of the tissue factor gene. J Clin Invest 1997; 99 (04) 737-44.
  • 11 Grabowski EF, Lam FP. Endothelial cell function, including tissue factor expression, under flow conditions. Thromb Haemost 1995; 74 (01) 123-8.
  • 12 Grabowski EF, Zuckerman DB, Nemerson Y. The functional expression of tissue factor by fibroblasts and endothelial cells under flow conditions. Blood 1993; 81 (12) 3265-70.
  • 13 Houston P, Dickson MC, Ludbrook V, White B, Schwachtgen JL, McVey JH, Mackman N, Reese JM, Gorman DG, Campbell C, Braddock M. Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arterioscler Thromb Vasc Biol 1999; 19 (02) 281-9.
  • 14 Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 1998; 18 (05) 677-85.
  • 15 Resnick N, Yahav H, Schubert S, Wolfovitz E, Shay A. Signalling pathways in vascular endothelium activated by shear stress: relevance to atherosclerosis. Curr Op Lipidol 2000; 11 (02) 167-77.
  • 16 Gimbrone MAJ, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann NY Acad Sci 2000; 902: 230-9 discussion 239-40.
  • 17 Ballermann BJ, Dardik A, Eng E, Liu A. Shear stress and the endothelium. Kidney Int Suppl 1998; 67: S100-8.
  • 18 Chien S, Li S, Shyy YJ. Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension 1998; 31 (1 Pt 2) 162-9.
  • 19 Bouis D, Hospers G, Meijer C, Molema G, Mulder N. Endothelium in vitro: A review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis 2001; 04: 91-102.
  • 20 Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, Hayoz D. Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler Thromb Vasc Biol 1998; 18 (05) 686-92.
  • 21 Hayoz D, Tardy Y, Rutschmann B, Mignot JP, Achakri H, Feihl F, Meister JJ, Waeber B, Brunner HR. Spontaneous diameter oscillations of the radial artery in humans. Am J Physiol 1993; 264 (6 Pt 2) H2080-H2084.
  • 22 He X, Ku DN, Moore JEJ. Simple calculation of the velocity profiles for pulsatile flow in a blood vessel using Mathematica. Ann Biomed Eng 1993; 21 (01) 45-9.
  • 23 Strandness DEJ, Sumner DS. In: Hemodynamics for surgeons. Grune and Stratton. New York: 1975. Ref Type: Serial (Book, Monograph).
  • 24 Westmuckett AD, Lupu C, Roquefeuil S, Krausz T, Kakkar VV, Lupu F. Fluid flow induces upregulation of synthesis and release of tissue factor pathway inhibitor in vitro. Arterioscler Thromb Vasc Biol 2000; 20 (11) 2474-82.
  • 25 Silverman MD, Manolopoulos VG, Unsworth BR, Lelkes PI. Tissue factor expression is differentially modulated by cyclic mechanical strain in various human endothelial cells. Blood Coag Fibrinol 1996; 07 (03) 281-8.
  • 26 Silacci P, Desgeorges A, Mazzolai L, Chambaz C, Hayoz D. Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension 2001; 38 (05) 1162-6.
  • 27 Bombeli T, Karsan A, Tait JF, Harlan JM. Apoptotic vascular endothelial cells become procoagulant. Blood 1997; 89 (07) 2429-42.
  • 28 Mallat Z, Hugel B, Ohan J, Leseche G, Freyssinet JM, Tedgui A. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99 (03) 348-53.
  • 29 Grabowski EF, Reninger AJ, Petteruti PG, Tsukurov O, Orkin RW. Shear stress decreases endothelail cell tissue factor activity by augmenting secretion of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol 2001; 21: 157-62.
  • 30 Matsumoto A, Kaway Y, Watanabe K, Murata M, Handa M, Nakamura S, Ikeda Y. Fluid shear stress attenuates tumor necrosis factor-ex-induced tissue factor expression in cultures of human endothelial cells. Blood 1998; 91: 4164-72.
  • 31 Ye S, Humphries S, Henney A. Matrix metalloproteinases: implication in vascular matrix remodelling during atherogenesis. Clin Sci 1998; 94 (02) 103-10.
  • 32 Zucker S, Mirza H, Conner CE, Lorenz AF, Drews MH, Bahou WF, Jesty J. Vascular endothelial growth factor induces tissue factor and matrix metalloproteinase production in endothelial cells: conversion of prothrombin to thrombin results in progelatinase A activation and cell proliferation. Int J Cancer 1998; 75 (05) 780-6.
  • 33 Hasenstab D, Lea H, Hart CE, Lok S, Clowes AW. Tissue factor overexpression in rat arterial neointima models thrombosis and progression of advanced atherosclerosis. Circulation 101 (22) 2651-7.