Subscribe to RSS
DOI: 10.1160/TH03-04-0231
High molecular weight kininogen and factor XII binding to endothelial cells and astrocytes
Publication History
Received
16 April 2003
Accepted after resubmission
10 July 2003
Publication Date:
05 December 2017 (online)
Summary
We have quantitated the binding of high molecular weight kininogen (HK) to human microvascular endothelial cells of lung and dermal origin as well as to astrocytes and compared the results with those reported for human umbilical vein endothelial cells (HUVEC). We also reassessed parameters of binding to HUVEC employing cells in suspension as well as cells attached to the culture plate and report similar numbers of sites varying from 6.96x105to 7.71x105per cell. The present study shows that HK binds with high specificity and affinity to microvascular endothelial cells (Kd = 1.86 to 4.5 nM) compared to HUVEC (Kd = 10.35nM) but with lower affinity to astrocytes (Kd = 23.73 nM). Human cytokeratin 1, urokinase plasminogen activator receptor and gC1qR were found to be HK binding proteins present at the surface of microvascular endothelial cells and astrocytes analogous to that seen in HUVEC, as assessed by inhibition of binding with antibody to each protein. Lung microvascular endothelial cells had approximately half the number of HK binding sites as HUVEC while dermal micro vascular endothelial cells and astrocytes had only 8-10% of the sites/cell. The affinity of binding to the microvascular endothelial cells was greater than HUVEC, the affinity of binding to astrocytes was considerably less, nevertheless binding to each cell type involves gC1qR, cytokeratin 1 and u-PAR to varying degrees. We also demonstrate, for the first time, that factor XII binds to all of these cell types in a saturable and Zn+2dependent manner. Given that factor XII accelerates the interactions among cell surfaces and proteins of the contact activation cascade to generate bradykinin, binding of factor XII (and the prekallikrein-HK complex) may serve as a mechanism by which these proteins are concentrated locally to facilitate their interactions.
-
References
- 1 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.
- 2 Thompson RE, Mandle RJ, Kaplan AP. Association of factor XI and high molecular weight kininogen in human plasma. J Clin Invest 1977; 60: 1376-80.
- 3 Kaplan AP, Joseph K, Shibayama Y. et.al. Bradykinin formation-plasma and tissue pathways and cellular interactions. Clin Rev Allergy Immunol 1998; 16: 403-29.
- 4 Vavrek RJ, Stewart JM. Competitive antagonists of bradykinin. Peptides 1985; 6: 161-4.
- 5 Regoli D, Barabe J. Pharmacology of bradykinin and related kinins. Pharmacol Rev 1980; 32: 1-46.
- 6 Marceau F. Kinin B1 receptors: a review. Immunopharmacology 1995; 30: 1-26.
- 7 Davis AJ, Perkins MN. The involvement of bradykinin B1 and B2 receptor mechanisms in cytokine induced mechanical hyperalgesia in the rat. Br J Pharmacol 1994; 113: 63-8.
- 8 Schmaier AH, Kuo A, Lundberg D. et al The expression of high molecular weight kinino-gen on human umbilical vein endothelial cells. J Biol Chem 1988; 263: 16327-33.
- 9 Van Iwaarden F, De Groot PG, Bouma BN. The binding of high molecular weight kinino-gen to cultured human endothelial cells. J Biol Chem 1988; 263: 4698-703.
- 10 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.
- 11 Zhao Y, Qiu Q, Mahdi F. et al Assembly and activation of HK-PK complex on endothelial cells results in badykinin liberatin and NO formation. Am J Physiol 2001; 280: H1821-29.
- 12 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 CIq (gClq-R). Proc Natl Acad Sci USA 1996; 93: 8552-57.
- 13 Herwald H, Dedio J, Kellner R. et al Isolation and characterization of the kinino-gen-binding protein p33 from endothelial cells. J Biol Chem 1996; 271: 13040-47.
- 14 Joseph K, Ghebrehiwet B, Kaplan AP. Cytokeratin 1 and gC1qR mediate high molecular weight kininogen binding to endothelial cells. Clin Immunol 1999; 92: 246-55.
- 15 Hasan AAK, Zisman T, Schmaier AH. Identification of cytokeratin 1 as a binding protein and presentation receptor for kinino-gens on endothelial cells. Proc Natl Acad Sci USA 1998; 95: 3615-20.
- 16 Colman RW, Pixley RA, Najamunnisa S. et al Binding of high molecular weight kinino-gen to human endothelial cells is mediated via a site within domains 2 and 4 of the urokinase receptor. J Clin. Invest 1997; 100: 1481-7.
- 17 Renne T, Dedio J, David G. et al High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation of endothelial cells. J Biol Chem 2000; 275: 33688-96.
- 18 Kaplan AP, Joseph K, Silverberg M. Pathways for bradykinin formation and inflammatory disease. J Allergy Clin Immunol 2002; 109: 195-209.
- 19 Glenner CG, Wong CW. Alzheimer’s disease: Initial report of the purification and char-acterization of a novel cerebrovascular amyloid protein. Biochim Biophys Res Commun 1984; 120: 885-90.
- 20 Masters CL, Simms G, Weinman NA. et al Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 1985; 82: 4245-9.
- 21 Shibayama Y, Joseph K, Nakazawa Y, Ghebreihiwet B, Peerschke EIB, Kaplan AP. Zinc-dependent activation of the plasma kinin-forming cascade by aggregated β–Amyloid protein. Clin Immunol 1999; 90: 89-99.
- 22 Lesne S, Docagne F, Gabriel C. et al Transforming growth factor –B1 potentiates Amyloid β generation in astrocytes and in transgenic mice. J Biol Chem 2003; 278: 18408-18.
- 23 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.
- 24 Jaffe EA. Culture of human endothelial cells. Transplant Proc 1980; 12: 49-53.
- 25 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of the protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-54.
- 26 Joseph K, Nakazawa Y, Bahou WF. et al Platelet glycoprotein Ib: A zinc-dependent binding protein for the heavy chain of high molecular weight kininogen. Mol Med 1999; 5: 555-63.
- 27 Scatchard G. The attractions of proteins for small molecules and ions. Ann N Y Acad Sci 1949; 51: 660-72.
- 28 Munson PJ, Rodbard D. Ligand: A versatile computerized approach for characterization of ligand-binding systems. Anal Biochem 1980; 107: 220-39.
- 29 Reddigari SR, Shibayama Y, Brunnee T. et al Human Hageman 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.
- 30 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.
- 31 Baird TR, Walsh PN. The interaction of factor XIa with activated platelets but not endothelial cells promotes the activation of factor IX in the consolidation phase of blood coagulation. J Biol Chem 2002; 277: 38462-67.
- 32 Kuna P, Kaplan AP, Reddigari SR. Human high molecular weight kininogen binds to human umbilical cord endothelial cells through its heavy chain. Blood 1990; 76: 426a
- 33 Barnathan ES, Kuo A, Rosenfeld L. et al Interaction of single-chain urokinase-type plasminogen activator with human endothelial cells. J Biol Chem 1990; 265: 2865-72.
- 34 Hasan AAK, Cines DB, Herwald H. et al Mapping the cell binding sites in high molecular weight kininogen domain 5. J Biol Chem 1995; 270: 19256-61.
- 35 Moreira CR, Schmaier AH, Mahdi F. et al Identification of prolylcarboxypeptidase as the cell matrix-associated prekallikrein activator. FEBS Letters 2002; 523: 167-70.
- 36 Motta G, Shariat-Madar Z, Mahdi F. et al Assembly of high molecular weight kininogen and activation of prekallikrein on cell matrix. Thromb Haemost 2001; 86: 840-7.
- 37 Joseph K, Ghebrehiwet B, Kaplan AP. Cytokeratin 1 and gC1qR mediate high molecular weight kininogen binding to endothelial cells. Clinical Immunol 1999; 92: 246-55.
- 38 Fernando LP, Fernando AN, Joseph K, Kaplan AP. Assessment of the role of heparan sulfate in high molecular weight kininogen binding to human umbilical vein endothelial cells. J Thromb Haemost: (In Press);
- 39 Shariat-Madar Z, Mahdi F, Schmaier AH. Mapping binding domains of kininogens on endothelial cell cytokeratin 1. J Biol Chem 1999; 274: 7137-45.
- 40 Joseph K, Tholanikunnel BG, Ghebrehiwet B. et al Interaction of high molecular weight kininogen binding proteins with each other. Thromb Haemost 2001; 86: 2093
- 41 Salcedo R, Resau JH, Halverson D. et al Differential expression and responsiveness of chemokine receptors (CXCR1-3) by human microvascular endothelial cells and umbilical vein endothelial cells. FASEB J 2000; 14: 2055-64.
- 42 Takahashi K, Uwabe Y, Sawasaki Y. et al Increased secretion of urokinase-type plasminogen activator by human lung microvascular endothelial cells. Am J Physiol 1998; 275: I-47.-54.
- 43 Mason JC, Yarwood H, Sugars K. et al Human umbilical vein and dermal microvascular endothelial cels show hetergeneity in reponse to PKC activation. Am J Physiol 1997; 273: C1233-40.
- 44 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.
- 45 Mandle RJJ, Kaplan AP. Hageman factor substrates II. Human plasma prekallikrein. Mechanism of activation by hageman factor and participation in hageman factor dependent fibrinolysis. J Biol Chem 1977; 252: 6097-104.
- 46 Rojkjaer R, Hasan AAK, Motta M. et al Factor XII does not initiate prekallikrein activation on endothelial cells. Thromb Haemost 1998; 80: 74-81.
- 47 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.