(Circulation. 2000;101:841.)
© 2000 American Heart Association, Inc.
Brief Rapid Communications |
Elevated Levels of Shed Membrane Microparticles With Procoagulant Potential in the Peripheral Circulating Blood of Patients With Acute Coronary Syndromes
From the Institut National de la Santé et la Recherche Médicale, INSERM U141, IFR Circulation, Hôpital Lariboisière, Paris (Z.M., A.T.); Service de Cardiologie (H.B., P.G.S.) and Service de Biochimie (J.B.), Hôpital Bichat, Paris; Institut d’Hématologie et d’Immunologie, Faculté de Médecine, Université Louis Pasteur, Strasbourg; and INSERM U143, Le Kremlin-Bicêtre (B.H., J.-M.F.), France.
Correspondence to Alain Tedgui, PhD, INSERM U 141, 41 boulevard de la Chapelle, 75475 Paris Cedex 10, France. E-mail tedgui{at}infobiogen.fr
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Abstract |
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Background—Apoptotic microparticles are responsible for almost all tissue factor activity of the plaque lipid core. We hypothesized that elevated levels of procoagulant microparticles could also circulate in the peripheral blood of patients with recent clinical signs of plaque disruption and thrombosis.
Methods and Results—We studied 39 patients with coronary heart disease, including 12 patients with stable angina and 27 patients with acute coronary syndromes (ACS), and 12 patients with noncoronary heart disease. We isolated the circulating microparticles by capture with annexin V and determined their procoagulant potential with a prothrombinase assay. The cell origins of microparticles were determined in an additional 22 patients by antigenic capture with specific antibodies. The level of procoagulant microparticles did not differ between stable angina patients and noncoronary patients (10.1±1.6 nmol/L phosphatidylserine [PS] equivalent versus 9.9±1.6 nmol/L PS equivalent, respectively). However, procoagulant microparticles were significantly elevated in patients with ACS (22.2±2.7 nmol/L PS equivalent) compared with other coronary (P<0.01) or noncoronary (P<0.01) patients. Microparticles of endothelial origin were significantly elevated in patients with ACS (P<0.01), which suggests an important role for endothelial injury in inducing the procoagulant potential.
Conclusions—High levels of procoagulant endothelial microparticles are present in the circulating blood of patients with ACS and may contribute to the generation and perpetuation of intracoronary thrombi.
Key Words: atherosclerosis • complications • thrombosis • microparticles • endothelium.
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Introduction |
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Acute coronary syndromes (ACS) are severe clinical manifestations of coronary artery lumen occlusion by a thrombus formed on the contact of a ruptured or eroded atherosclerotic plaque.1 2 Tissue factor (TF) is highly expressed in atherosclerotic plaques,3 and TF activity of plaques retrieved from patients with unstable angina (UA) is significantly higher than that found in the plaques of patients with stable angina (SA),4 which suggests that it may significantly determine thrombus formation after plaque disruption. TF activity is highly dependent on the presence of phosphatidylserine (PS),5 and it has been shown that this anionic phospholipid is redistributed on the cell surface during apoptotic death,6 conferring to the cell a potent procoagulant activity.7 8 Interestingly, shed membrane apoptotic microparticles rich in PS are produced in considerable amounts within human atherosclerotic plaques and carry almost all TF activity of the plaque lipid core,9 indicating that they may largely determine plaque thrombogenicity. In the present study, we hypothesized that high levels of cell-derived microparticles with procoagulant potential could also be detectable in the circulating blood of patients with recent clinical signs of plaque disruption and thrombosis and may therefore contribute to the initiation and perpetuation of the thrombotic process.
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Methods |
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Patient Selection
To isolate the circulating microparticles and determine their procoagulant potential, we prospectively included 39 patients with angina and angiographic documentation of coronary artery disease (CAD) and 12 controls. Among patients with CAD, 12 (9 men; mean age 62±3 years) had SA with no signs of myocardial ischemia at rest, and 27 had ACS: 13 (8 men; mean age 62±4 years) had UA (Braunwald class III) with documented signs of recent myocardial ischemia at rest, and 14 (10 men; mean age 61±4 years) had acute myocardial infarction (MI). Cardiovascular risk factors were not significantly different between the 3 groups of patients with CAD, except for hypercholesterolemia, which was more prevalent in patients with SA (P<0.02).
All coronary patients were receiving aspirin. Patients with ACS received additional standard antithrombotic therapy before blood sampling. Anti-ischemic medications were equally distributed between groups. Programmed primary coronary angioplasty (85% with stent placement) was performed after blood sampling in 9 patients with SA (75%), 12 patients with UA (92%), and 14 patients with MI (100%).
Controls (9 men and 3 women, mean age 58±4 years) were patients with angiographic documentation of absence of CAD (4 patients with chest pain, 4 patients with valvular disease, and 4 patients with dilated cardiomyopathy).
To characterize the cell origins of the microparticles, we included 16 additional consecutive patients with angina and angiographic documentation of CAD (5 with SA, mean age 63±5 years, and 11 with ACS, mean age 62±4 years) and 6 noncoronary patients (5 with valvular disease and 1 with dilated cardiomyopathy, mean age 65±8 years).
Isolation of the Circulating Microparticles and Determination of
Their Procoagulant Potential
Blood samples were collected before any mechanical intervention
at admission (day 0), except in 6 patients with MI, in whom blood
sampling was performed at day 8 after the coronary event.
Microparticles were captured by immobilized annexin V, and
the anionic phospholipid content was determined by a prothrombinase
assay as previously described in detail.9 10 We verified
that the method used for the capture of microparticles did not allow
the capture of PS-containing lipoproteins.
Determination of the Cell Origins of Circulating
Microparticles
Microparticles were captured by specific antibodies (anti-CD3,
anti-CD11a, anti-CD31, anti-CD146, and anti-GP Ib).9 10
The morphology of circulating microparticles was recently
published.11 12
Statistical Analysis
Results are expressed as mean±SEM. Comparisons between groups
were made by a 1-way ANOVA. Simple regression analysis was
performed to analyze the relation between values of
microparticles captured with anti-CD31, anti-CD146, or anti-GP Ib
antibodies. A value of P<0.05 was considered statistically
significant.
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Results |
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The level of circulating microparticles in patients admitted with a diagnosis of SA was not significantly different from that in patients admitted for noncoronary heart disease (10.1±1.6 versus 9.9±1.6 nmol/L PS equivalent, respectively). However, the level of procoagulant microparticles was significantly elevated in the circulating blood of patients with UA (18.6±1.9 nmol/L PS) or MI (25.6±4.8 nmol/L PS) compared with patients who presented with signs of SA (P<0.01) or with noncoronary patients (P<0.01). In the patients with ACS, no difference was found in the level of circulating microparticles between those with UA and those with MI (Figure
).
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Two patients experienced recurrent ischemic syndromes during hospitalization: 1 patient in the UA group developed recurrent documented myocardial ischemia, and 1 in the MI group had reocclusion of his stented culprit coronary artery. Interestingly, these 2 patients had very high baseline levels of circulating procoagulant microparticles (35.6 and 62.3 nmol/L PS, respectively).
Circulating microparticles captured with anti-CD146 or anti-CD31
antibody were elevated in patients with ACS (compared with both stable
coronary and noncoronary patients), whereas those
captured with anti-GP Ib, anti-CD3, or anti-CD11a were not
(Table). The values obtained with
anti-CD31 antibody were not correlated with those obtained with anti-GP
Ib antibody but were highly correlated with those obtained with
anti-CD146 antibody (P<0.001). Given that there were almost
no CD3-bearing microparticles, these findings indicate that
microparticles captured with anti-CD31 or anti-CD146 were most likely
of endothelial origin.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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In the present study, the levels of circulating procoagulant microparticles in patients who presented with SA were not different from those found in noncoronary patients. However, we found significantly elevated levels of circulating procoagulant microparticles in the patients who presented with ACS in comparison with both SA patients and noncoronary patients. These results suggest that an increase in circulating microparticles more specifically reflects the complications of atherosclerosis (ie, thrombus formation occurring on the contact of a disrupted atheromatous plaque). Because only patients with ACS received heparin, it could be argued that differences in levels of microparticles reflect differences in medications. This is unlikely, however, because heparin has been reported either to have no effect or to decrease microparticle generation from thrombin-activated platelets.13
Soejima et al14 recently reported that plasma TF antigen levels are significantly elevated in patients with UA compared with those measured in patients with SA and are associated with a poor prognosis. However, these authors did not measure TF activity, nor did they determine the origin of the TF antigen. Our findings extend those of Soejima et al and suggest that the procoagulant potential of the circulating blood is, at least in part, related to the presence of elevated levels of circulating procoagulant microparticles. Moreover, the prevalence of microparticles bearing CD146 and CD31 suggests a potentially important role for acute endothelial injury in this process. This may reflect the endothelial erosion at the site of plaque disruption, the endothelial injury on exposure of plaque microvessels to inflammatory cells, and/or the endothelial injury associated with myocardial ischemia. It should be noted that our data do not exclude the possibility that a certain amount of circulating microparticles may also originate from other cell types, including smooth muscle cells and cardiomyocytes.
The detection of elevated levels of circulating procoagulant microparticles 8 days after the acute ischemic syndrome is in line with the observation of persistent intracoronary thrombi 24 hours to 30 days after the ischemic episode.15 In the present study, the 2 patients who experienced documented recurrent myocardial ischemia or coronary reocclusion with reinfarction had very high basal levels of circulating microparticles. This observation suggests that the level of circulating microparticles could be useful as an indicator of the persistence or recurrence of thrombus and therefore as a prognostic marker of the recurrence of ischemic events. This hypothesis needs to be tested in a large multicenter study.
In addition to their direct effect in promotion and amplification of the coagulation cascade, the circulating microparticles may also act in a variety of inflammatory processes16 17 and may be responsible for dissemination of the procoagulant and proinflammatory potentials to sites remote from the microenvironment of their formation.8
In conclusion, high levels of procoagulant microparticles are present in the circulating blood of patients with ACS and may participate in the generation and perpetuation of intracoronary thrombi. The high levels of circulating microparticles of endothelial origin suggest an important role for endothelial injury in thrombus formation.
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Acknowledgments |
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This work was supported by a grant from Fondation pour la Recherche Médicale-Action Recherche Santé 2000.
Received October 29, 1999; revision received December 31, 1999; accepted January 10, 2000.
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References |
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C. Mineo, H. Deguchi, J. H. Griffin, and P. W. Shaul Endothelial and Antithrombotic Actions of HDL Circ. Res., June 9, 2006; 98(11): 1352 - 1364. [Abstract] [Full Text] [PDF]
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J.-J. Stampfuss, P. Censarek, J. W. Fischer, K. Schror, and A.-A. Weber Rapid Release of Active Tissue Factor From Human Arterial Smooth Muscle Cells Under Flow Conditions Arterioscler Thromb Vasc Biol, May 1, 2006; 26(5): e34 - e37. [Abstract] [Full Text] [PDF]
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J. Steffel, T. F. Luscher, and F. C. Tanner Tissue Factor in Cardiovascular Diseases: Molecular Mechanisms and Clinical Implications Circulation, February 7, 2006; 113(5): 722 - 731. [Abstract] [Full Text] [PDF]
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N. Werner, S. Wassmann, P. Ahlers, S. Kosiol, and G. Nickenig Circulating CD31+/Annexin V+ Apoptotic Microparticles Correlate With Coronary Endothelial Function in Patients With Coronary Artery Disease Arterioscler Thromb Vasc Biol, January 1, 2006; 26(1): 112 - 116. [Abstract] [Full Text] [PDF]
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J. Herrmann Peri-procedural myocardial injury: 2005 update Eur. Heart J., December 1, 2005; 26(23): 2493 - 2519. [Abstract] [Full Text] [PDF]
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A. Tesse, M. C. Martinez, B. Hugel, K. Chalupsky, C. D. Muller, F. Meziani, D. Mitolo-Chieppa, J.-M. Freyssinet, and R. Andriantsitohaina Upregulation of Proinflammatory Proteins Through NF-{kappa}B Pathway by Shed Membrane Microparticles Results in Vascular Hyporeactivity Arterioscler Thromb Vasc Biol, December 1, 2005; 25(12): 2522 - 2527. [Abstract] [Full Text] [PDF]
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A. Malarstig, T. Tenno, N. Johnston, B. Lagerqvist, T. Axelsson, A.-C. Syvanen, L. Wallentin, and A. Siegbahn Genetic Variations in the Tissue Factor Gene Are Associated With Clinical Outcome in Acute Coronary Syndrome and Expression Levels in Human Monocytes Arterioscler Thromb Vasc Biol, December 1, 2005; 25(12): 2667 - 2672. [Abstract] [Full Text] [PDF]
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Z. Mallat, Ph. G. Steg, J. Benessiano, M.-L. Tanguy, K. A. Fox, J.-P. Collet, O. H. Dabbous, P. Henry, K. F. Carruthers, A. Dauphin, et al. Circulating Secretory Phospholipase A2 Activity Predicts Recurrent Events in Patients With Severe Acute Coronary Syndromes J. Am. Coll. Cardiol., October 4, 2005; 46(7): 1249 - 1257. [Abstract] [Full Text] [PDF]
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T. Hattori, M. M.H. Khan, R. W. Colman, and L. H. Edmunds Jr Plasma Tissue Factor Plus Activated Peripheral Mononuclear Cells Activate Factors VII and X in Cardiac Surgical Wounds J. Am. Coll. Cardiol., August 16, 2005; 46(4): 707 - 713. [Abstract] [Full Text] [PDF]
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C. M. Boulanger and A. Tedgui Dying for attention: Microparticles and angiogenesis Cardiovasc Res, July 1, 2005; 67(1): 1 - 3. [Full Text] [PDF]
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I. Ott Soluble Tissue Factor Emerges From Inflammation Circ. Res., June 24, 2005; 96(12): 1217 - 1218. [Full Text] [PDF]
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H. Koga, S. Sugiyama, K. Kugiyama, K. Watanabe, H. Fukushima, T. Tanaka, T. Sakamoto, M. Yoshimura, H. Jinnouchi, and H. Ogawa Elevated Levels of VE-Cadherin-Positive Endothelial Microparticles in Patients With Type 2 Diabetes Mellitus and Coronary Artery Disease J. Am. Coll. Cardiol., May 17, 2005; 45(10): 1622 - 1630. [Abstract] [Full Text] [PDF]
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V. Llorente-Cortes and L. Badimon LDL Receptor-Related Protein and the Vascular Wall: Implications for Atherothrombosis Arterioscler Thromb Vasc Biol, March 1, 2005; 25(3): 497 - 504. [Abstract] [Full Text] [PDF]
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M. C. Martinez, A. Tesse, F. Zobairi, and R. Andriantsitohaina Shed membrane microparticles from circulating and vascular cells in regulating vascular function Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1004 - H1009. [Abstract] [Full Text] [PDF]
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J. L. Yu, L. May, V. Lhotak, S. Shahrzad, S. Shirasawa, J. I. Weitz, B. L. Coomber, N. Mackman, and J. W. Rak Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis Blood, February 15, 2005; 105(4): 1734 - 1741. [Abstract] [Full Text] [PDF]
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G. Busch, I. Seitz, B. Steppich, S. Hess, R. Eckl, A. Schomig, and I. Ott Coagulation Factor Xa Stimulates Interleukin-8 Release in Endothelial Cells and Mononuclear Leukocytes: Implications in Acute Myocardial Infarction Arterioscler Thromb Vasc Biol, February 1, 2005; 25(2): 461 - 466. [Abstract] [Full Text] [PDF]
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S. M. Day, J. L. Reeve, B. Pedersen, D. M Farris, D. D. Myers, M. Im, T. W. Wakefield, N. Mackman, and W. P. Fay Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall Blood, January 1, 2005; 105(1): 192 - 198. [Abstract] [Full Text] [PDF]
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P. R. Moreno and V. Fuster New aspects in the pathogenesis of diabetic atherothrombosis J. Am. Coll. Cardiol., December 21, 2004; 44(12): 2293 - 2300. [Abstract] [Full Text] [PDF]
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A. C. Ferreira, A. A. Peter, A. J. Mendez, J. J. Jimenez, L. M. Mauro, J. A. Chirinos, R. Ghany, S. Virani, S. Garcia, L. L. Horstman, et al. Postprandial Hypertriglyceridemia Increases Circulating Levels of Endothelial Cell Microparticles Circulation, December 7, 2004; 110(23): 3599 - 3603. [Abstract] [Full Text] [PDF]
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M. Hristov, W. Erl, S. Linder, and P. C. Weber Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro Blood, November 1, 2004; 104(9): 2761 - 2766. [Abstract] [Full Text] [PDF]
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K. G. Birukov, V. N. Bochkov, A. A. Birukova, K. Kawkitinarong, A. Rios, A. Leitner, A. D. Verin, G. M. Bokoch, N. Leitinger, and Joe. G.N. Garcia Epoxycyclopentenone-Containing Oxidized Phospholipids Restore Endothelial Barrier Function via Cdc42 and Rac Circ. Res., October 29, 2004; 95(9): 892 - 901. [Abstract] [Full Text] [PDF]
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O. Gasser and J. A. Schifferli Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis Blood, October 15, 2004; 104(8): 2543 - 2548. [Abstract] [Full Text] [PDF]
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V. Llorente-Cortes, M. Otero-Vinas, S. Camino-Lopez, O. Llampayas, and L. Badimon Aggregated Low-Density Lipoprotein Uptake Induces Membrane Tissue Factor Procoagulant Activity and Microparticle Release in Human Vascular Smooth Muscle Cells Circulation, July 27, 2004; 110(4): 452 - 459. [Abstract] [Full Text] [PDF]
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O. Aras, A. Shet, R. R. Bach, J. L. Hysjulien, A. Slungaard, R. P. Hebbel, G. Escolar, B. Jilma, and N. S. Key Induction of microparticle- and cell-associated intravascular tissue factor in human endotoxemia Blood, June 15, 2004; 103(12): 4545 - 4553. [Abstract] [Full Text] [PDF]
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T. Suhara, K. Fukuo, O. Yasuda, M. Tsubakimoto, Y. Takemura, H. Kawamoto, T. Yokoi, M. Mogi, T. Kaimoto, and T. Ogihara Homocysteine Enhances Endothelial Apoptosis via Upregulation of Fas-Mediated Pathways Hypertension, June 1, 2004; 43(6): 1208 - 1213. [Abstract] [Full Text] [PDF]
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E. Durand, A. Scoazec, A. Lafont, J. Boddaert, A. Al Hajzen, F. Addad, M. Mirshahi, M. Desnos, A. Tedgui, and Z. Mallat In Vivo Induction of Endothelial Apoptosis Leads to Vessel Thrombosis and Endothelial Denudation: A Clue to the Understanding of the Mechanisms of Thrombotic Plaque Erosion Circulation, June 1, 2004; 109(21): 2503 - 2506. [Abstract] [Full Text] [PDF]
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S. Rajagopalan, E. C. Somers, R. D. Brook, C. Kehrer, D. Pfenninger, E. Lewis, A. Chakrabarti, B. C. Richardson, E. Shelden, W. J. McCune, et al. Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity Blood, May 15, 2004; 103(10): 3677 - 3683. [Abstract] [Full Text] [PDF]
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S. Martin, A. Tesse, B. Hugel, M. C. Martinez, O. Morel, J.-M. Freyssinet, and R. Andriantsitohaina Shed Membrane Particles From T Lymphocytes Impair Endothelial Function and Regulate Endothelial Protein Expression Circulation, April 6, 2004; 109(13): 1653 - 1659. [Abstract] [Full Text] [PDF]
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L. M. L. Bezerra and S. G. Filler Interactions of Aspergillus fumigatus with endothelial cells: internalization, injury, and stimulation of tissue factor activity Blood, March 15, 2004; 103(6): 2143 - 2149. [Abstract] [Full Text] [PDF]
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H J Ankersmit, T Weber, J Auer, G Roth, M Brunner, E Kvas, B Moser, S Spreitzer, E Lassnig, E Maurer, et al. Increased serum concentrations of soluble CD95/Fas and caspase 1/ICE in patients with acute angina Heart, February 1, 2004; 90(2): 151 - 154. [Abstract] [Full Text] [PDF]
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F. D. Kolodgie, A. Petrov, R. Virmani, N. Narula, J. W. Verjans, D. K. Weber, D. Hartung, N. Steinmetz, J. L. Vanderheyden, M. A. Vannan, et al. Targeting of Apoptotic Macrophages and Experimental Atheroma With Radiolabeled Annexin V: A Technique With Potential for Noninvasive Imaging of Vulnerable Plaque Circulation, December 23, 2003; 108(25): 3134 - 3139. [Abstract] [Full Text] [PDF]
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A. Sambola, J. Osende, J. Hathcock, M. Degen, Y. Nemerson, V. Fuster, J. Crandall, and J. J. Badimon Role of Risk Factors in the Modulation of Tissue Factor Activity and Blood Thrombogenicity Circulation, February 25, 2003; 107(7): 973 - 977. [Abstract] [Full Text] [PDF]
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P. K. Shah Mechanisms of plaque vulnerability and rupture J. Am. Coll. Cardiol., February 19, 2003; 41(4_Suppl_S): 15S - 22S. [Abstract] [Full Text] [PDF]
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R. A. Preston, W. Jy, J. J. Jimenez, L. M. Mauro, L. L. Horstman, M. Valle, G. Aime, and Y. S. Ahn Effects of Severe Hypertension on Endothelial and Platelet Microparticles Hypertension, February 1, 2003; 41(2): 211 - 217. [Abstract] [Full Text] [PDF]
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D. Proudfoot, J.D. Davies, J.N. Skepper, P.L. Weissberg, and C.M. Shanahan Acetylated Low-Density Lipoprotein Stimulates Human Vascular Smooth Muscle Cell Calcification by Promoting Osteoblastic Differentiation and Inhibiting Phagocytosis Circulation, December 10, 2002; 106(24): 3044 - 3050. [Abstract] [Full Text] [PDF]
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V. Schachinger and A. M. Zeiher Atherogenesis--recent insights into basic mechanisms and their clinical impact Nephrol. Dial. Transplant., December 1, 2002; 17(12): 2055 - 2064. [Full Text] [PDF]
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M. Diamant, R. Nieuwland, R. F. Pablo, A. Sturk, J. W.A. Smit, and J. K. Radder Elevated Numbers of Tissue-Factor Exposing Microparticles Correlate With Components of the Metabolic Syndrome in Uncomplicated Type 2 Diabetes Mellitus Circulation, November 5, 2002; 106(19): 2442 - 2447. [Abstract] [Full Text] [PDF]
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V. Balasubramanian, E. Grabowski, A. Bini, and Y. Nemerson Platelets, circulating tissue factor, and fibrin colocalize in ex vivo thrombi: real-time fluorescence images of thrombus formation and propagation under defined flow conditions Blood, September 26, 2002; 100(8): 2787 - 2792. [Abstract] [Full Text] [PDF]
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F. Sabatier, P. Darmon, B. Hugel, V. Combes, M. Sanmarco, J.-G. Velut, D. Arnoux, P. Charpiot, J.-M. Freyssinet, C. Oliver, et al. Type 1 And Type 2 Diabetic Patients Display Different Patterns of Cellular Microparticles Diabetes, September 1, 2002; 51(9): 2840 - 2845. [Abstract] [Full Text] [PDF]
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R. Gonzalez-Conejero, J. Corral, V. Roldan, C. Martinez, F. Marin, J. Rivera, J. A. Iniesta, M. L. Lozano, P. Marco, and V. Vicente A common polymorphism in the annexin V Kozak sequence (-1C>T) increases translation efficiency and plasma levels of annexin V, and decreases the risk of myocardial infarction in young patients Blood, August 28, 2002; 100(6): 2081 - 2086. [Abstract] [Full Text] [PDF]
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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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C. M. Boulanger, A. Scoazec, T. Ebrahimian, P. Henry, E. Mathieu, A. Tedgui, and Z. Mallat Circulating Microparticles From Patients With Myocardial Infarction Cause Endothelial Dysfunction Circulation, November 27, 2001; 104(22): 2649 - 2652. [Abstract] [Full Text] [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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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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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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