Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:488-496
© 1996 American Heart Association, Inc.
Articles |
Thrombin-Induced Increase in Endothelial Permeability Is Associated With Changes in Cell-to-Cell Junction Organization
From CEA, Laboratoire d'Hématologie, INSERM U217, Département de Biologie Moléculaire et Structurale, Grenoble, France, and Istituto di Ricerche Farmacologiche Mario Negri, Milano, Italy (M.-G.L.).
Correspondence to Dr M.-J. Rabiet, Laboratoire d'Hématologie, INSERM U 217, Département de Biologie Moléculaire et Structurale, CEN-G, 17 rue des Martyrs, 38054 Grenoble Cedex, France.
Abstract Thrombin increases endothelial permeability in a rapid and reversible way. This effect requires the catalytic activity of the enzyme and thrombin receptor engagement. Endothelial cell permeability is mostly regulated by intercellular junction organization. In the present study, we investigated whether opening of intercellular gaps after thrombin treatment could be related to changes in adherence-junction molecular organization. By immunofluorescence analysis, we found that thrombin stimulation of endothelial cells caused a marked alteration of the distribution of vascular endothelial (VE)-cadherin and of the associated catenins. These molecules, which are strictly localized at intercellular boundaries in confluent resting cells, were absent in the areas of intercellular retraction. Immunoprecipitation analysis indicated that thrombin disrupted the VE-cadherin/catenin complex. This effect was reversible and correlated with the increase in endothelial permeability. The use of a protein kinase C inhibitor (calphostin C) blocked both thrombin-induced permeability and disassembly of adherence-junction components. We propose that thrombin's effect on endothelial cell junction organization is an important determinant in the increase in endothelial permeability induced by this agent.
Key Words: endothelial monolayer • thrombin • cadherin • catenins
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
V. Vouret-Craviari, D. Grall, G. Flatau, J. Pouyssegur, P. Boquet, and E. Van Obberghen-Schilling Effects of Cytotoxic Necrotizing Factor 1 and Lethal Toxin on Actin Cytoskeleton and VE-Cadherin Localization in Human Endothelial Cell Monolayers Infect. Immun., June 1, 1999; 67(6): 3002 - 3008. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Hurst IV, P. L. Goldberg, F. L. Minnear, R. L. Heimark, and P. A. Vincent Rearrangement of adherens junctions by transforming growth factor-beta 1: role of contraction Am J Physiol Lung Cell Mol Physiol, April 1, 1999; 276(4): L582 - L595. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Hordijk, E Anthony, F. Mul, R Rientsma, L. Oomen, and D Roos Vascular-endothelial-cadherin modulates endothelial monolayer permeability J. Cell Sci., January 6, 1999; 112(12): 1915 - 1923. [Abstract] [PDF]
|
|
|
|
|
|
G. P. v. N. Amerongen, R. Draijer, M. A. Vermeer, and V. W. M. van Hinsbergh Transient and Prolonged Increase in Endothelial Permeability Induced by Histamine and Thrombin : Role of Protein Kinases, Calcium, and RhoA Circ. Res., November 30, 1998; 83(11): 1115 - 1123. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Essler, K. Hermann, M. Amano, K. Kaibuchi, J. Heesemann, P. C. Weber, and M. Aepfelbacher Pasteurella multocida Toxin Increases Endothelial Permeability via Rho Kinase and Myosin Light Chain Phosphatase J. Immunol., November 15, 1998; 161(10): 5640 - 5646. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Gulino, E. Delachanal, E. Concord, Y. Genoux, B. Morand, M.-O. Valiron, E. Sulpice, R. Scaife, M. Alemany, and T. Vernet Alteration of Endothelial Cell Monolayer Integrity Triggers Resynthesis of Vascular Endothelium Cadherin J. Biol. Chem., November 6, 1998; 273(45): 29786 - 29793. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Vouret-Craviari, P. Boquet, J. Pouysségur, and E. Van Obberghen-Schilling Regulation of the Actin Cytoskeleton by Thrombin in Human Endothelial Cells: Role of Rho Proteins in Endothelial Barrier Function Mol. Biol. Cell, September 1, 1998; 9(9): 2639 - 2653. [Abstract] [Full Text]
|
|
|
|
|
|
M. Essler, M. Amano, H.-J. Kruse, K. Kaibuchi, P. C. Weber, and M. Aepfelbacher Thrombin Inactivates Myosin Light Chain Phosphatase via Rho and Its Target Rho Kinase in Human Endothelial Cells J. Biol. Chem., August 21, 1998; 273(34): 21867 - 21874. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Saito, Y. Minamiya, M. Kitamura, S. Saito, K. Enomoto, K. Terada, and J.-i. Ogawa Endothelial Myosin Light Chain Kinase Regulates Neutrophil Migration Across Human Umbilical Vein Endothelial Cell Monolayer J. Immunol., August 1, 1998; 161(3): 1533 - 1540. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
S Esser, M. Lampugnani, M Corada, E Dejana, and W Risau Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells J. Cell Sci., January 7, 1998; 111(13): 1853 - 1865. [Abstract] [PDF]
|
|
|
|
|
|
R. A. Henriksen, G. P. Samokhin, and P. B. Tracy Thrombin-Induced Thromboxane Synthesis by Human Platelets : Properties of an Anion Binding Exosite I– Independent Receptor Arterioscler Thromb Vasc Biol, December 1, 1997; 17(12): 3519 - 3526. [Abstract] [Full Text]
|
|
|
|
|
|
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|
|
|
|
|
|
M. Lampugnani, M Corada, P Andriopoulou, S Esser, W Risau, and E Dejana Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells J. Cell Sci., January 9, 1997; 110(17): 2065 - 2077. [Abstract] [PDF]
|
|
|
|
|
|
A. Gilchrist, J. F. Vanhauwe, A. Li, T. O. Thomas, T. Voyno-Yasenetskaya, and H. E. Hamm Galpha Minigenes Expressing C-terminal Peptides Serve as Specific Inhibitors of Thrombin-mediated Endothelial Activation J. Biol. Chem., July 6, 2001; 276(28): 25672 - 25679. [Abstract] [Full Text] [PDF]
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