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Apoptotic vascular endothelial cells become procoagulant
T Bombeli, A Karsan, JF Tait and JM Harlan
Department of Laboratory Medicine, University of Washington, Seattle 98195,
USA.
Whereas unperturbed endothelial cells provide potent anticoagulant
properties, exposure to inflammatory and atherogenic stimuli can rapidly
lead to a procoagulant behavior. Because recent studies provide evidence
that apoptosis of vascular cells may occur under conditions such as
atherosclerosis and inflammation, we investigated whether apoptotic
endothelial cells may contribute to the development of a prothrombotic
state. In this report, it is shown that both adherent and detached
apoptotic human umbilical vein endothelial cells (HUVECs) become
procoagulant. Apoptosis was induced by staurosporine, a nonspecific protein
kinase inhibitor, or by culture in suspension with serum deprivation. Both
methods resulted in similar findings. As assessed by flow cytometric
determination of annexin V binding, HUVECs undergoing cell death exhibited
typically a more rapid exposure of membrane phosphatidylserine (PS) than
DNA fragmentation. Depending on the stage of apoptosis, this redistribution
of phospholipids was found to induce an increase of the activity of the
intrinsic tenase complex by 25% to 60%. Although apoptotic cells did not
show antigenic or functional tissue factor (TF) activity, when preactivated
with lipopolysaccharide, TF procoagulant activity increased by 50% to 70%.
At 8 hours after apoptosis induction, antigenic thrombomodulin, heparan
sulfates, and TF pathway inhibitor decreased by about 83%, 80%, and 59%,
respectively. The functional activity of these components was reduced by
about 36%, 52%, and 39%, respectively. Moreover, the presence of apoptotic
HUVECs led to a significant increase of thrombin formation in recalcified
citrated plasma. In conclusion, apoptotic HUVECs, either adherent or in
suspension, become procoagulant by increased expression of PS and the loss
of anticoagulant membrane components.
Volume 89,
Issue 7,
pp. 2429-2442,
04/01/1997
Copyright © 1997 by The American Society of Hematology

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[Full Text]
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S. R. Goth and R. S. Stephens
Rapid, Transient Phosphatidylserine Externalization Induced in Host Cells by Infection with Chlamydia spp.
Infect. Immun.,
February 1, 2001;
69(2):
1109 - 1119.
[Abstract]
[Full Text]
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F. G. Blankenberg, L. Naumovski, J. F. Tait, A. M. Post, and H. W. Strauss
Imaging Cyclophosphamide-Induced Intramedullary Apoptosis in Rats Using 99mTc-Radiolabeled Annexin V
J. Nucl. Med.,
February 1, 2001;
42(2):
309 - 316.
[Abstract]
[Full Text]
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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.
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T. S. Kern, J. Tang, M. Mizutani, R. A. Kowluru, R. H. Nagaraj, G. Romeo, F. Podesta, and M. Lorenzi
Response of Capillary Cell Death to Aminoguanidine Predicts the Development of Retinopathy: Comparison of Diabetes and Galactosemia
Invest. Ophthalmol. Vis. Sci.,
November 1, 2000;
41(12):
3972 - 3978.
[Abstract]
[Full Text]
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S. S. DESHPANDE, P. ANGKEOW, J. HUANG, M. OZAKI, and K. IRANI
Rac1 inhibits TNF-{alpha}-induced endothelial cell apoptosis: dual regulation by reactive oxygen species
FASEB J,
September 1, 2000;
14(12):
1705 - 1714.
[Abstract]
[Full Text]
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K. Irani
Oxidant Signaling in Vascular Cell Growth, Death, and Survival : A Review of the Roles of Reactive Oxygen Species in Smooth Muscle and Endothelial Cell Mitogenic and Apoptotic Signaling
Circ. Res.,
August 4, 2000;
87(3):
179 - 183.
[Abstract]
[Full Text]
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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]
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A. Iwakura, M. Fujita, K. Hasegawa, T. Sawamura, R. Nohara, S. Sasayama, and M. Komeda
Pericardial fluid from patients with unstable angina induces vascular endothelial cell apoptosis
J. Am. Coll. Cardiol.,
June 1, 2000;
35(7):
1785 - 1790.
[Abstract]
[Full Text]
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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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T. Stefanec
Endothelial Apoptosis: Could It Have a Role in the Pathogenesis and Treatment of Disease?
Chest,
March 1, 2000;
117(3):
841 - 854.
[Abstract]
[Full Text]
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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]
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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]
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V. Pasceri, H. D. Wu, J. T. Willerson, and E. T. H. Yeh
Modulation of Vascular Inflammation In Vitro and In Vivo by Peroxisome Proliferator-Activated Receptor-{gamma} Activators
Circulation,
January 25, 2000;
101(3):
235 - 238.
[Abstract]
[Full Text]
[PDF]
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M.-L. Peyot, A.-P. Gadeau, F. Dandre, I. Belloc, F. Dupuch, and C. Desgranges
Extracellular Adenosine Induces Apoptosis of Human Arterial Smooth Muscle Cells via A2b-Purinoceptor
Circ. Res.,
January 7, 2000;
86(1):
76 - 85.
[Abstract]
[Full Text]
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N. Wang, L. Verna, S. Hardy, Y. Zhu, K.-S. Ma, M. J. Birrer, and M. B. Stemerman
c-Jun Triggers Apoptosis in Human Vascular Endothelial Cells
Circ. Res.,
September 3, 1999;
85(5):
387 - 393.
[Abstract]
[Full Text]
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C. B. Hansen, B. van Deurs, L. C. Petersen, and L. V. M. Rao
Discordant Expression of Tissue Factor and Its Activity in Polarized Epithelial Cells. Asymmetry in Anionic Phospholipid Availability as a Possible Explanation
Blood,
September 1, 1999;
94(5):
1657 - 1664.
[Abstract]
[Full Text]
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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]
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M. D. Silverman, C. R. Waters, G. T. Hayman, J. Wigboldus, M. M. Samet, and P. I. Lelkes
Tissue factor activity is increased in human endothelial cells cultured under elevated static pressure
Am J Physiol Cell Physiol,
August 1, 1999;
277(2):
C233 - C242.
[Abstract]
[Full Text]
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R. M. A. van Gorp, J. L. V. Broers, C. P. M. Reutelingsperger, N. M. H. J. Bronnenberg, G. Hornstra, M. C. E. van Dam-Mieras, and J. W. M. Heemskerk
Peroxide-induced membrane blebbing in endothelial cells associated with glutathione oxidation but not apoptosis
Am J Physiol Cell Physiol,
July 1, 1999;
277(1):
C20 - C28.
[Abstract]
[Full Text]
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T. Bombeli, B. R. Schwartz, and J. M. Harlan
Endothelial Cells Undergoing Apoptosis Become Proadhesive for Nonactivated Platelets
Blood,
June 1, 1999;
93(11):
3831 - 3838.
[Abstract]
[Full Text]
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G. Lizard, S. Monier, C. Cordelet, L. Gesquiere, V. Deckert, S. Gueldry, L. Lagrost, and P. Gambert
Characterization and Comparison of the Mode of Cell Death, Apoptosis Versus Necrosis, Induced by 7ß-Hydroxycholesterol and 7-Ketocholesterol in the Cells of the Vascular Wall
Arterioscler. Thromb. Vasc. Biol.,
May 1, 1999;
19(5):
1190 - 1200.
[Abstract]
[Full Text]
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E. J. Ackermann, J. K. Taylor, R. Narayana, and C. F. Bennett
The Role of Antiapoptotic Bcl-2 Family Members in Endothelial Apoptosis Elucidated with Antisense Oligonucleotides
J. Biol. Chem.,
April 16, 1999;
274(16):
11245 - 11252.
[Abstract]
[Full Text]
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B. R. Schwartz, A. Karsan, T. Bombeli, and J. M. Harlan
A Novel {beta}1 Integrin-Dependent Mechanism of Leukocyte Adherence to Apoptotic Cells
J. Immunol.,
April 15, 1999;
162(8):
4842 - 4848.
[Abstract]
[Full Text]
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C. T. Dang, M. S. Magid, B. Weksler, A. Chadburn, and J. Laurence
Enhanced Endothelial Cell Apoptosis in Splenic Tissues of Patients With Thrombotic Thrombocytopenic Purpura
Blood,
February 15, 1999;
93(4):
1264 - 1270.
[Abstract]
[Full Text]
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M. R Bennett
Apoptosis of vascular smooth muscle cells in vascular remodelling and atherosclerotic plaque rupture
Cardiovasc Res,
February 1, 1999;
41(2):
361 - 368.
[Abstract]
[Full Text]
[PDF]
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Z. Mallat, B. Hugel, J. Ohan, G. Leseche, J.-M. Freyssinet, and A. Tedgui
Shed Membrane Microparticles With Procoagulant Potential in Human Atherosclerotic Plaques : A Role for Apoptosis in Plaque Thrombogenicity
Circulation,
January 26, 1999;
99(3):
348 - 353.
[Abstract]
[Full Text]
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T. V. Byzova and E. F. Plow
Activation of alpha Vbeta 3 on Vascular Cells Controls Recognition of Prothrombin
J. Cell Biol.,
December 28, 1998;
143(7):
2081 - 2092.
[Abstract]
[Full Text]
[PDF]
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M. P. Soares, A. Muniappan, E. Kaczmarek, K. Koziak, C. J. Wrighton, F. Steinhauslin, C. Ferran, H. Winkler, F. H. Bach, and J. Anrather
Adenovirus-Mediated Expression of a Dominant Negative Mutant of p65/RelA Inhibits Proinflammatory Gene Expression in Endothelial Cells Without Sensitizing to Apoptosis
J. Immunol.,
November 1, 1998;
161(9):
4572 - 4582.
[Abstract]
[Full Text]
[PDF]
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A. Ortiz, T.H. Hughes-Davies, R. P. Hebbel, and A. Solovey
Circulating Endothelial Cells in Sickle Cell Anemia
N. Engl. J. Med.,
April 16, 1998;
338(16):
1162 - 1163.
[Full Text]
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