Lymphocyte Adhesion to Human Endothelial Cells Induces Tissue Factor Expression via a Juxtacrine Pathway

Summary

To study the effect of lymphocyte adhesion on the procoagulant activity of endothelial cells, we have stimulated HUVECs with interferon-γ to upregulate adhesion molecules. Subsequent addition of lymphocytes induced the expression of tissue factor (TF) by HUVECs. Both CD4⁺ and CD8⁺ T-cells promoted this TF synthesis via distinct adhesion molecules (CD4⁺ T-cells: E-selectin and ICAM-1; CD8⁺ T-cells: MHC-I molecules). In addition, tumor necrosis factor-α and -β (TNFα, TNFβ) and platelet-activating factor (PAF) were involved in lymphocyte-mediated TF expression on HUVECs. We demonstrate that PAF plays a pivotal role in this process. Adhesion of lymphocytes to endothelial cell surface molecules induced the release of PAF. PAF, in turn, caused the production of T.NFα and TNFβ, both of which are potent stimulators of TF expression.

• References

• 1 Sakai T, Kisiel W. Formation of tissue factor activity following incubation of recombinant human tissue factor apoprotein with plasma lipoproteins. Thromb Res 1990; 60: 213-222
• 2 Guha A, Bach R, Konigsberg W. Affinity purification of human tissue factor: interaction of factor VII and tissue factor in detergent micelles. Proc Natl Acad Sci USA 1986; 83: 299-302
• 3 Bauer KA, Kass BL, Cate HT, Hawiger JJ, Rosenberg RD. Factor IX is activated in vivo by the tissue factor mechanism. Blood 1990; 76: 731-6
• 4 Komiyama Y, Pedersen AH, Kisiel W. Proteolytic activation of human factors IX and X by recombinant human factor Vila: effects of calcium, phospholipids, and tissue factor. Biochemistry 1990; 29: 9418-9425
• 5 Warr T, Rao L, Rapaport S. Disseminated intravascular coagulation in rabbits induced by administration of endotoxin or tissue factor: effect of antitissue factor antibodies and measurement of plasma extrinsic pathway inhibitor activity. Blood 1990; 75: 1481-1489
• 6 Noguchi M, Sakai T, Kisiel W. Correlation between antigenic and functional expression of tissue factor on the surface of cultured human endothelial cells following stimulation by lipopolysaccharide endotoxin. Thromb Res 1989; 55: 87-97
• 7 Bevilacqua MP, Pober JS, Majean GR. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1. Proc Natl Acad Sci USA 1986; 83: 4533-4537
• 8 Tannenbaum SH, Finko R, Cines DB. Antibody and immune complexes induce tissue factor production by human endothelial cells. J Immunol 1986; 137: 1532-1535
• 9 Lyberg T, Gaidai KS, Evensen SA, Prydz H. Cellular cooperation in endothelial cell thromboplastin synthesis. Br J Haematol 1982; 53: 85-95
• 10 Galdal KS. Thromboplastin synthesis in endothelial cells. Haemostasis 1984; 14: 378-385
• 11 Binder K, Schmid E, Müller TH. Effect of peripheral blood lymphocytes on procoagulant activity of human endothelial cells pretreated with lipopolysaccharide. In DIC: Pathogenesis, Diagnosis and Therapy of Disseminated Intravascular Fibrin Formation. Müller-Berghaus G. et al. (ed) Amsterdam: Excerpta Medica, Elsevier Science Publishers BV; 1993. pp 55-61
• 12 Leeuwenberg JF M, von Asmuth EJ U, Jeunhomme TM A A, Buurman WA. IFN-γ regulates the expression of the adhesion molecule ELAM-1 and IL-6 production by human endothelial cells in vitro. J Immunol 1990; 145: 2110-2114
• 13 Pober JS. Cytokine-mediated activation of vascular endothelium. Am J Pathol 1988; 133: 426-433
• 14 Pober JS, Cotran RS. The role of endothelial cells in inflammation. Transplantation 1990; 50: 537-541
• 15 Bevilacqua MP, Stengelin S, Gimbrone MA J, Seed B. Endothelial leukocyte adhesion molecule 1 : an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 1989; 243: 1160-1165
• 16 Dobrina A, Schwartz BR, Carlos TM, Ochs HD, Beatty PG, Harlan JM. CD 11 /CD 18-independent neutrophil adherence to inducible endothelial- leukocyte adhesion molecules (E-LAM) in vitro. Immunology 1989; 67: 502-508
• 17 Carlos T, Kovach N, Schwartz B, Rosa M, Newman B, Wayner E, Benjamin C, Osborn L, Lobb R, Harlan J. Human monocytes bind to cytokine- induced adhesive ligands on cultured human endothelial cells: endothelial- leukocyte adhesion molecule-1 and vascular cell adhesion molecule-1. Blood 1991; 77: 2266-2271
• 18 Picker LJ, Kishimoto TK, Smith CW, Wamock RA, Butcher EC. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature 1991; 349: 796-799
• 19 Shimizu Y, Shaw S, Gräber N, Gopal TV, Horgan KJ, van Seventer GA, Newman W. Activation-independent binding of human memory T cells to adhesion molecule ELAM-1. Nature 1991; 349: 799-802
• 20 Pober JS, Cotran RS. What can be learned from the expression of endothelial adhesion molecules in tissues?. Lab Invest 1991; 64: 301-305
• 21 Pober JS, Gimbrone MA J, Lapierre LA, Mendrick DL, Fiers W, Rothlein R, Springer TA. Overlapping patterns of activation by human endothelial cells by interleukin 1, tumor necrosis factor and immune interferon. J Immunol 1986; 137: 1893-1897
• 22 Adams PW, Lee HS, Waldman WJ, Sedmak DD, Morgan CJ, Ward JS, Orosz CG. Alloantigenicity of human endothelial cells. J Immunol 1992; 148: 3753-3760
• 23 Hahne M, Jäger U, Isenmann S, Hallmann R, Vestweber D. Five tumor necrosis factor-inducible cell adhesion mechanisms on the surface of mouse endothelioma cells mediate the binding of leukocytes. J Cell Biol 1993; 121: 655-664
• 24 Doukas J, Mordes JP. T Jymphocytes capable of activating endothelial cells are present in rats with autoimmune diabetes. J Immunol 1993; 150: 1036-1046
• 25 Kishimoto TK, Larson AL, Corbi ML, Dustin DE, Staunton DE, Springer TA. The leukocyte integrins. Adv Immunol 1989; 46: 149-182
• 26 Norment AM, Salter RD, Parham P, Engelhard VH, Littman DR. Cell-cell adhesion mediated by CD8 and MHC class I molecules. Nature 1988; 336: 79-82
• 27 Carlsen E, Stinessen MB, Prydz H. Differential effect of a-interferon and γ-interferon on thromboplastin response in monocytes and endothelial cells. Clin Exp Immunol 1987; 70: 471-478
• 28 Zuckerman SH, Surprenant YM. Induction of endothelial cell/macrophage procoagulant activity: synergistic stimulation by gamma interferon and, granulocyte-macrophage colony stimulating factor. Thromb Haemost 1989; 61: 178-182
• 29 Gregory SA, Morrissey JH, Edgington TS. Regulation of tissue factor gene expression in the monocyte response to endotoxin. Molec Cell Biol 1989; 9: 2752-2755
• 30 Rothlein R, Dustin ML, Marlin SD, Springer TA. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol 1986; 137: 1270-1274
• 31 Kishimoto TK, Warnock RA, Jutila MA, Butcher EC, Lane C, Anderson DC, Smith CW. Antibodies against human neutrophil LECAM-1 (LAM-l/Leu-8/DREG-56 antigen) and endothelial cell ELAM-1 inhibit a common CD 18-independent adhesion pathway in vitro. Blood 1991; 78: 805-811
• 32 Hanisch F-G, Hanski C, Hasegawa A. Sialyl Lewis^x antigen as defined by monoclonal antibody AM-3 is a marker of dysplasia in the colonic adenoma-carcinoma sequence. Cancer Res 1992; 52: 3138-3144
• 33 Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. J Clin Invest 1973; 52: 2745-2756
• 34 Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159
• 35 Rivers RP A, Hathaway WE, Weston WL. The endotoxin-induced coagulant activity of human monocytes. Br J Haematol 1975; 30: 311-316
• 36 Dustin ML, Springer TA. Lymphocyte function associated antigen-1 (LFA-1) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells. J Cell Biol 1988; 107: 321-325
• 37 Smith CW, Martin SD, Rothlein R, Toman C, Anderson DC. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J Clin Invest 1989; 83: 2008-2011
• 38 Bosman FT. Integrins: cell adhesives and modulators of cell function. Histochem J 1993; 25: 469-477
• 39 Diamond MS, Springer TA. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J Cell Biol 1993; 120: 545-556
• 40 Munro JM, Lo SK, Corless C, Robertson MJ, Lee NC, Barnhill RL, Weinberg DS, Bevilacqua MP. Expression of sialyl-Lewis X, an E-selectin ligand, in inflammation, immune processes, and lymphoid tissues. Am J Pathol 1992; 141: 1397-1408
• 41 Yong K, Khwaja A. Leucocyte cellular adhesion molecules. Blood Rev 1990; 4: 211-225
• 42 Smiley PL, Stremler KE, Prescott SM, Zimmerman GA, McIntyre TM. Oxidatively fragmented phosphatidylcholines activate human neutrophils through the receptor for platelet-activating factor. J Biol Chem 1990; 266: 11104-11110
• 43 Gouvello S, Vivier E, Debre P, Thomas Y, Colard O. CD2 triggering stimulates the formation of platelet-activating factor-acether from alkyl- arachidonoyl-glycerophosphocholine in a human CD⁴+ T-lymphocyte clone. J Immunol 1992; 149: 1289-1293
• 44 Bussolino F, Breviario F, Tetta C, Aglietta M, Mantovani A, Dejana E. Interleukin-1 stimulates platelet activating factor production in cultured human endothelial cells. J Clin Invest 1986; 77: 2027-2033
• 45 Bevilacqua MP, Gimbrone MA. Inducible endothelial functions in inflammation and coagulation. Semin Thromb Hemost 1987; 13: 425-433
• 46 Crowe PD, VanArsdale TL, Walter BN, Ware CF, Hession C, Ehrenfels B, Browning JL, Din WS, Goodwin RG, Smith CA. A lymphotoxin-β-specific receptor. Science 1994; 264: 707-710
• 47 Carlsen E, Fiatmark A, Prydz H. Cytokine-induced procoagulant activity in monocytes and endothelial cells. Further enhancement by cyclosporine Transplantation 1988; 46: 575-580
• 48 Adamthwaite D, Cooley MA. CD8⁺ T-cell subsets defined by expression of CD45 isoforms differ in their capacity to produce II-2, IFN-γ and TNF-β. Immunology 1994; 81: 253-260
• 49 Nagura H, Ohtani H. Expression of major histocompatibility class-II antigens by vascular endothelial cells leads to amplified immunoinflammatory processes. Acta Histochem Cytochem 1992; 25: 653-660
• 50 Kahaleh MB, Zhou S. Induction of tumor necrosis factor synthesis by endothelial cells upon exposure to R-TNF. Arthritis and Rheumatism 1989; 32: 124-127
• 51 Marceau F, Grassi J, Frobert Y, Bergeron C, Poubelle PE. Effects of experimental conditions on the production of interleukin-lα and -lβ by human endothelial cells cultured in vitro. Int J Immunopharmacol 1992; 14: 525-534
• 52 Cabre F, Tost D, Suesa N, Gutierrez M, Ucedo P, Mauleon D, Carganico G. Synthesis and release of platelet-activating factor and eicosanoids in human endothelial cells induced by different agonists. Agents Actions 1993; 38: 212-219
• 53 More L, Sim R, Hudson M, Dhillon AP, Pounder R, Wakefield AJ. Immunohistochemical study of tissue factor expression in normal intestine and idiopathic inflammatory bowel disease. J Clin Pathol 1993; 46: 703-708
• 54 Drake TA, Cheng J, Chang A, Taylor Jr FB. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. Am J Pathol 1993; 142: 458-470
• 55 Xu H, Gonzalo JA, St Pierre Y, Williams IR, Küpper TS, Cotran RS, Springer TA, Gutierrez-Ramos J-C. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J Exp Med 1994; 180: 95-109
• 56 Ogata M, Matsumoto T, Koga K, Takenaka I, Kamochi M, Sata T, Yoshida S, Shigematsu A. An antagonist of platelet-activating factor suppressed endotoxin-induced tumor necrosis factor and mortality in mice pretreated with carrageenan. Infect Immunol 1993; 61: 699-703
• 57 Tracey KJ, Fong Y, Hesse DG. Anti-cachectin/TNF monoclonal antibodies prevent septic schock during lethal bacteremia. Nature 1987; 330: 662-665
• 58 Tracey KJ, Lowry SF. The role of cytokine mediators in septic shock. Adv Surg 1990; 23: 21-26
• 59 Beutler B, Milsark IW, Cerami A. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effects of endotoxin. Science 1985; 229: 869-873