Interaction of high molecular weight kininogen binding proteins on endothelial cells

Kusumam Joseph; Baby G. Tholanikunnel; Berhane Ghebrehiwet; Allen P. Kaplan

doi:10.1160/TH03-07-0471

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2004; 91(01): 61-70
DOI: 10.1160/TH03-07-0471

Blood Coagulation, Fibrinolysis and Cellular Haemostasis

Schattauer GmbH

Interaction of high molecular weight kininogen binding proteins on endothelial cells

Authors

Kusumam Joseph

¹Department of Medicine, Division of Pulmonary and Critical Care, Allergy and Clinical Immunology and Konishi-MUSC Institute for Inflammation Research
Baby G. Tholanikunnel

²Division of Nephrology, Medical University of South Carolina, Charleston, South Carolina, USA
Berhane Ghebrehiwet

³Department of Medicine, State University of New York, Stony Brook, New York, USA
Allen P. Kaplan

¹Department of Medicine, Division of Pulmonary and Critical Care, Allergy and Clinical Immunology and Konishi-MUSC Institute for Inflammation Research

Abstract

Summary

Cell surface proteins reported to participate in the binding and activation of the plasma kinin-forming cascade includes gC1qR, cytokeratin 1 and u-PAR. Each of these proteins binds high molecular weight kininogen (HK) as well as Factor XII. The studies on the interaction of these proteins, using dot-blot analysis, revealed that cytokeratin 1 binds to both gC1qR and u-PAR while gC1qR and u-PAR do not bind to each other. The binding properties of these proteins were further analyzed by gel filtration. When biotinylated cytokeratin 1 was incubated with either gC1qR or u-PAR and gel filtered, a new, higher molecular weight peak containing biotin was observed indicating complex formation. The protein shift was also similar to the biotin shift. Further, immunoprecipitation of solubilized endothelial cell plasma membrane proteins with anti-gC1qR recovered both gC1qR and cytokeratin 1, but not u-PAR. Immunoprecipitation with anti-u-PAR recovered only u-PAR and cytokeratin 1. By competitive ELISA, gC1qR inhibits u-PAR from binding to cytokeratin 1; u-PAR inhibits gC1qR binding to a lesser extent and requires a 10-fold molar excess. Our data suggest that formation of HK (and Factor XII) binding sites along endothelial cell membranes consists of bimolecular complexes of gC1qR-cytokeratin 1 and u-PAR-cytokeratin 1, with gC1qR binding being favored.

Keywords

Endothelial cells - high molecular weight kininogen - gC1qR - cytokeratin 1 - u-PAR

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Referenzen

References
1 Silverberg M, Dunn JT, Garen L. et al.. Autoactivation of human Hageman factor. Demonstration using a synthetic substrate. J Biol Chem 1980; 255: 7281-6.
2 Tankersley DL, Finlayson JS. Kinetics of activation and autoactivation of human Factor XII. Biochemistry 1984; 23: 273-9.
3 Griffin JH, Cochrane CG. Mechanisms for the involvement of high molecular weight kininogen in surface-dependent reactions of Hageman factor. Proc Natl Acad Sci USA 1978; 73: 2554-8.
4 Meier HL, Pierce JV, Colman RW. et al.. Activation and function of human Hageman factor. The role of high molecular weight kininogen and prekallikrein. J Clin Invest 1977; 60: 18-31.
5 Mandle Jr R, Colman RW, Kaplan AP. Identification of prekallikrein and high molecular weight kininogen as a complex in human plasma. Proc Natl Acad Sci USA 1976; 73: 4179-83.
6 Mori K, Nagasawa S. Studies on human high molecular weight (HMW) kininogen II. Structural change in HMW kininogen by the action of human plasma kallikrein. J Biochem 1981; 89: 1465-73.
7 Mori K, Sakamoto W, Nagasawa S. Studies on human high molecular weight (HMW) kininogen III. Cleavage of HMW kininogen by the action of salivary kallikrein. J Biochem 1981; 90: 503-9.
8 Schmaier AH, Kuo A, Lundberg D. et al.. The expression of high molecular weight kininogen on human umbilical vein endothelial cells. J Biol Chem 1988; 263: 16327-33.
9 Van Iwaarden F, deGroot PG, Bouma BN. The binding of high molecular weight kininogen to cultured human endothelial cells. J Biol Chem 1988; 263: 4698-703.
10 Reddigari SR, Kuna P, Miragliotta GF. et al.. Human high molecular weight kininogen binds to human umbilical vein endothelial cells via its heavy and light chains. Blood 1993; 81: 1306-11.
11 Hasan AAK, Cines DB, Herwald H. et al.. Mapping the cell binding site on high molecular weight kininogen domain 5. J Biol Chem 1995; 270: 19256-61.
12 Reddigari SR, Shibayama Y, Brunnee T. et al.. Human hagman factor (Factor XII) and high molecular weight kininogen compete for the same binding site on human umbilical vein endothelial cells. J Biol Chem 1993; 268: 11982-7.
13 Motta G, Rojkjaer R, Hasan AAK. et al.. High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: A novel mechanism for contact activation. Blood 1998; 91: 516-28.
14 Joseph K, Shibayama Y, Ghebrehiwet B. et al.. Factor XII-dependent contact activation on endothelial cells and binding proteins gC1qR and cytokeratin 1. Thromb Haemost 2001; 85: 119-24.
15 Joseph K, Tholanikunnel BG, Kaplan AP. Heat shock protein 90 catalyzes activation of the prekallikrein kininogen complex in the absence of factor XII. Proc Natl Acad Sci USA 2002; 99: 896-900.
16 Joseph K, Tholanikunnel BG, Kaplan AP. Activation of the bradykininforming cascade on endothelial cells: a role for heat shock protein 90. International Immunopharmacology 2002; 02: 1851-9.
17 Shariat-Madar Z, Mahdi F, Schmaier AH. Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J Biol Chem 2002; 277: 17962-9.
18 Joseph K, Ghebrehiwet B, Peerschke EIB. et al.. Identification of the zinc-dependent endothelial cell binding protein for high molecular weight kininogen and Factor XII: identity with the receptor that binds to the globular “heads” of C1q (gC1qR). Proc Natl Acad Sci USA 1996; 93: 8552-7.
19 Herwald H, Dedio J, Kellner R. et al.. Isolation and characterization of the kininogen binding protein p33 from endothelial cells. J Biol Chem 1996; 271: 13040-7.
20 Hasan AAK, Zisman T, Schmaier AH. Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc Natl Acad Sci USA 1998; 95: 3615-20.
21 Joseph K, Ghebrehiwet B, Kaplan AP. Cytokeratin 1 and gC1qR mediate high molecular weight kininogen binding to endothelial cells. Clinical Immunology 1999; 92: 246-55.
22 Shariat-Madar Z, Mahdi F, Schmaier AH. Mapping binding domains of kininogens on endothelial cell cytokeratin 1. J Biol Chem 1999; 274: 7137-45.
23 Colman RW, Pixley RA, Najamunnisa S. et al.. Binding of high molecular weight kininogen to human endothelial cells is mediated via a site within domains 2 and 3 of the urokinase receptor. J Clin Invest 1997; 100: 1481-7.
24 Renne T, Dedio J, David G. et al.. High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation on endothelial cells. J Biol Chem 2000; 275: 33688-96.
25 Renne T, Muller-Esterl W. Cell surface-associated chondroitin sulfate proteoglycans bind contact phase factor H-kininogen. FEBS Lett 2001; 500: 36-40.
26 Fernando LP, Fernando AN, Joseph K. et al.. Assesssment of the role of heparan sulfate in high molecular weight kininogen binding to endothelial cells. J Thromb Haemost. 2003 02. (In Press).
27 Colman RW, Schmaier AH. Contact system: A vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 1997; 90: 3819-43.
28 Ghebrehiwet B, Lim B-L, Peerschke EIB, Willis AC, Reid KBM. Isolation, cDNA cloning, and overexpression of a 33-kD cell surface glycoprotein that binds to the globular “heads” of C1q. J Exp Med 1994; 179: 1809-21.
29 Ban M, Yoneda K, Kitajima Y. Differentiation of eccrine poroma cells to cytokeratin 1- and 10-expressing cells, the intermediate layer cells of eccrine sweat duct, in the tumor cell nests. J Cutan Pathol 1997; 24: 246-8.
30 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilyzing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-54.
31 Jaffe EA. Synthesis of factor VIII by endothelial cells. Ann NY Acad Sci 1982; 401: 163-70.
32 Hertel C, Coulter SJ, Perkins JP. A comparison of catecholamine-induced internalization of b-adrenergic receptors and receptor-mediated endocytosis of epidermal growth factor in human astrocytoma cells. J Biol Chem 1985; 260: 12547-53.
33 Hertel C, Perkins JP. Sequential appearance of epidermal growth factor in plasma membraneassociated and intracellular vesicles during endocytosis. J Biol Chem 1987; 262: 11407-9.
34 Laemmli UK. Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 1970; 227: 680-5.
35 Nguyen T, Ghebrehiwet B, Peerschke EIB. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infection & Immunity 2000; 68: 2061-8.
36 Peerschke EIB, Smyth SS, Teng EI. et al.. Human umbilical vein endothelial cells possess binding sites for the globular domain of C1q. J Immunol 1996; 157: 4154-8.
37 Mahdi F, Shariat-Madar Z, Todd III RF. et al.. Expression and colocalization of cytokeratin 1 and urokinase plasminogen activator receptor on endothelial cells. Blood 2001; 97: 2342-50.
38 Joseph K, Ghebrehiwet B, Kaplan AP. Activation of the kinin-forming cascade on the surface of endothelial cells. Biol Chem 2001; 382: 71-5.
39 Feng X, Marcia GT, Peerschke EIB. et al.. Cooperation of C1q receptors and integrins in C1q-mediated endothelial cell adhesion and spreading. J Immunol 2002; 168: 2441-8.