(Circulation. 1999;99:348-353.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Shed Membrane Microparticles With Procoagulant Potential in Human Atherosclerotic Plaques
A Role for Apoptosis in Plaque Thrombogenicity
From the Institut National de la Santé et la Recherche Médicale, INSERM U141, IFR "Circulation," Hôpital Lariboisière, Paris, France (Z.M., A.T.); Institut d'Hématologie et d'Immunologie, Faculté de Médecine, Université Louis Pasteur, Strasbourg, France and INSERM U143, Le Kremlin-Bicêtne, France (B.H., J.-M.F.); and Service de Chirurgie Thoracique et Vasculaire, Hôpital Beaujon, Clichy, France (J.O., G.L.).
Background—The specific role of apoptosis in human atherosclerosis remains unknown. During apoptotic cell death, phosphatidylserine exposure on the cell surface confers a high tissue-factor (TF)–dependent procoagulant activity.
Methods and Results—In this study, we examined the role of apoptotic cell death in the promotion of plaque thrombogenicity. TF expression and its relation to apoptosis was analyzed in 16 human atherosclerotic plaques by the use of immunohistochemical techniques. The presence of shed membrane apoptotic microparticles was analyzed in extracts from 6 human atherosclerotic plaques and 3 underlying arterial walls. The microparticles were captured by annexin V and their amounts estimated with respect to their phospholipid content by use of a prothrombinase assay. The prothrombogenic potential of the microparticles was further assessed by the measurement of total and microparticle-dependent TF activity in the extracts. The cell origin of the microparticles was determined after capture by specific antibodies. We were able to detect marked TF expression in the plaques in close proximity to apoptotic cells and debris, suggesting a potential interaction between TF and the apoptotic cell surfaces. High levels of shed membrane apoptotic microparticles were detected in extracts from atherosclerotic plaques but not in the underlying arterial walls (29.5±3.7 nmol/L phosphatidylserine equivalent versus 1.3±0.4 nmol/L, respectively, P<0.02). The microparticles were mainly of monocytic and lymphocytic origin and retained 97±2% of total TF activity, indicating a direct causal relationship between shed membrane microparticles and procoagulant activity of plaque extracts.
Conclusions—These results indicate that shed membrane microparticles with procoagulant potential are produced in human atherosclerotic plaques. Apoptosis could be a critical determinant of plaque thrombogenicity after plaque rupture.
Key Words: apoptosis • thrombosis • atherosclerosis
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J. Huber, A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J. L. Witztum, B. R. Binder, and N. Leitinger Oxidized Membrane Vesicles and Blebs From Apoptotic Cells Contain Biologically Active Oxidized Phospholipids That Induce Monocyte-Endothelial Interactions Arterioscler Thromb Vasc Biol, January 1, 2002; 22(1): 101 - 107. [Abstract] [Full Text] [PDF]
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P. M. Yao and I. Tabas Free Cholesterol Loading of Macrophages Is Associated with Widespread Mitochondrial Dysfunction and Activation of the Mitochondrial Apoptosis Pathway J. Biol. Chem., November 2, 2001; 276(45): 42468 - 42476. [Abstract] [Full Text] [PDF]
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A. H. M. Hassan, I. M. Lang, M. Ignatescu, R. Ullrich, D. Bonderman, P. Wexberg, F. Weidinger, and H. D. Glogar Increased intimal apoptosis in coronary atherosclerotic vessel segments lacking compensatory enlargement J. Am. Coll. Cardiol., November 1, 2001; 38(5): 1333 - 1339. [Abstract] [Full Text] [PDF]
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Z. Mallat, A. Corbaz, A. Scoazec, P. Graber, S. Alouani, B. Esposito, Y. Humbert, Y. Chvatchko, and A. Tedgui Interleukin-18/Interleukin-18 Binding Protein Signaling Modulates Atherosclerotic Lesion Development and Stability Circ. Res., September 28, 2001; 89 (7): e41 - e45. [Abstract] [Full Text] [PDF]
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 L. Badimon, G. Vilahur, S. Sanchez, and X. Duran Atheromatous plaque formation and thrombogenesis: formation, risk factors and therapeutic approaches Eur. Heart J. Suppl., August 1, 2001; 3(suppl_I): I16 - I22. [Abstract] [PDF]
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Z. Mallat and A. Tedgui Current Perspective on the Role of Apoptosis in Atherothrombotic Disease Circ. Res., May 25, 2001; 88(10): 998 - 1003. [Abstract] [Full Text] [PDF]
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M. R. Bennett Reactive Oxygen Species and Death : Oxidative DNA Damage in Atherosclerosis Circ. Res., April 13, 2001; 88(7): 648 - 650. [Full Text] [PDF]
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 D M Braganza and M R Bennett New insights into atherosclerotic plaque rupture Postgrad. Med. J., February 1, 2001; 77(904): 94 - 98. [Full Text]
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F. D. Kolodgie, J. Narula, A. P. Burke, N. Haider, A. Farb, Y. Hui-Liang, J. Smialek, and R. Virmani Localization of Apoptotic Macrophages at the Site of Plaque Rupture in Sudden Coronary Death Am. J. Pathol., October 1, 2000; 157(4): 1259 - 1268. [Abstract] [Full Text] [PDF]
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M. M. Kockx, C. Seye, G. R. Y. De Meyer, M. W. M. Knaapen, M. Aikawa, S. J. Voglic, S. Sugiyama, E. Rabkin, P. Libby, M. B. Taubman, et al. Decreased Apoptosis and Tissue Factor Expression After Lipid Lowering Response Circulation, September 26, 2000; 102 (13): e99 - e99. [Full Text] [PDF]
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A. Tedgui and Z. Mallat Smooth Muscle Cells : Another Source of Tissue Factor-Containing Microparticles in Atherothrombosis? Circ. Res., July 21, 2000; 87(2): 81 - 82. [Full Text] [PDF]
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A. D. Schecter, B. Spirn, M. Rossikhina, P. L. A. Giesen, V. Bogdanov, J. T. Fallon, E. A. Fisher, L. M. Schnapp, Y. Nemerson, and M. B. Taubman Release of Active Tissue Factor by Human Arterial Smooth Muscle Cells Circ. Res., July 21, 2000; 87(2): 126 - 132. [Abstract] [Full Text] [PDF]
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O. Tricot, Z. Mallat, C. Heymes, J. Belmin, G. Leseche, and A. Tedgui Relation Between Endothelial Cell Apoptosis and Blood Flow Direction in Human Atherosclerotic Plaques Circulation, May 30, 2000; 101(21): 2450 - 2453. [Abstract] [Full Text] [PDF]
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E. Arnaud, V. Barbalat, V. Nicaud, F. Cambien, A. Evans, C. Morrison, D. Arveiler, G. Luc, J.-B. Ruidavets, J. Emmerich, et al. Polymorphisms in the 5' Regulatory Region of the Tissue Factor Gene and the Risk of Myocardial Infarction and Venous Thromboembolism : The ECTIM and PATHROS Studies Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 892 - 898. [Abstract] [Full Text] [PDF]
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Z. Mallat, H. Benamer, B. Hugel, J. Benessiano, P. G. Steg, J.-M. Freyssinet, and A. Tedgui Elevated Levels of Shed Membrane Microparticles With Procoagulant Potential in the Peripheral Circulating Blood of Patients With Acute Coronary Syndromes Circulation, February 29, 2000; 101(8): 841 - 843. [Abstract] [Full Text] [PDF]
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R. Nieuwland, R. J. Berckmans, S. McGregor, A. N. Boing, F. P. H. Th. M. Romijn, R. G. J. Westendorp, C. E. Hack, and A. Sturk Cellular origin and procoagulant properties of microparticles in meningococcal sepsis Blood, February 1, 2000; 95(3): 930 - 935. [Abstract] [Full Text] [PDF]
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W. L van Heerde, S. Robert-Offerman, E. Dumont, L. Hofstra, P. A Doevendans, J. F.M Smits, M. J.A.P Daemen, and C. P.M Reutelingsperger Markers of apoptosis in cardiovascular tissues: focus on Annexin V Cardiovasc Res, February 1, 2000; 45(3): 549 - 559. [Abstract] [Full Text] [PDF]
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M. M Kockx and A. G Herman Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res, February 1, 2000; 45(3): 736 - 746. [Abstract] [Full Text] [PDF]
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N. J. McCarthy and M. Bennett The regulation of vascular smooth muscle cell apoptosis Cardiovasc Res, February 1, 2000; 45(3): 747 - 755. [Abstract] [Full Text] [PDF]
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Z. Mallat, S. Besnard, M. Duriez, V. Deleuze, F. Emmanuel, M. F. Bureau, F. Soubrier, B. Esposito, H. Duez, C. Fievet, et al. Protective Role of Interleukin-10 in Atherosclerosis Circ. Res., October 15, 1999; 85 (8): e17 - e24. [Abstract] [Full Text] [PDF]
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M. Mesri and D. C. Altieri Leukocyte Microparticles Stimulate Endothelial Cell Cytokine Release and Tissue Factor Induction in a JNK1 Signaling Pathway J. Biol. Chem., August 13, 1999; 274(33): 23111 - 23118. [Abstract] [Full Text] [PDF]
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J.-R. Nofer, B. Levkau, I. Wolinska, R. Junker, M. Fobker, A. von Eckardstein, U. Seedorf, and G. Assmann Suppression of Endothelial Cell Apoptosis by High Density Lipoproteins (HDL) and HDL-associated Lysosphingolipids J. Biol. Chem., September 7, 2001; 276(37): 34480 - 34485. [Abstract] [Full Text] [PDF]
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V. A. Patel, Q.-J. Zhang, K. Siddle, M. A. Soos, M. Goddard, P. L. Weissberg, and M. R. Bennett Defect in Insulin-Like Growth Factor-1 Survival Mechanism in Atherosclerotic Plaque-Derived Vascular Smooth Muscle Cells Is Mediated by Reduced Surface Binding and Signaling Circ. Res., May 11, 2001; 88(9): 895 - 902. [Abstract] [Full Text] [PDF]
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