Download PDF
Thromb Haemost 2001; 85(03): 544-551
DOI: 10.1055/s-0037-1615619
Review Article
Schattauer GmbH

Factor XI Assembly and Activation on Human Umbilical Vein Endothelial Cells in Culture

Zia Shariat-Madar
1   Division of Hematology and Oncology, Department of Internal Medicine and Pathology
,
Fakhri Mahdi
1   Division of Hematology and Oncology, Department of Internal Medicine and Pathology
,
Alvin Schmaier
1   Division of Hematology and Oncology, Department of Internal Medicine and Pathology
2   University of Michigan, Ann Arbor, MI, USA
› Author Affiliations
Further Information

Publication History

Received 26 May 2000

Accepted after resubmission 28 September 2000

Publication Date:
08 December 2017 (online)

    Permissions and Reprints

Summary

Biotin-FXI optimally bound to HUVEC in the presence of 40 nM high molecular weight kininogen (HK) and ≥ ≥7 μM Zn2+. There was little specific FXI binding in the absence of added HK and at concentrations of Zn2+ <15 μM. FXI and prekallikrein, but not prothrombin, blocked biotin-FXI binding to HUVEC in the presence of HK with an IC50 of 18 nM and 180 nM, respectively. Monoclonal antibody HKL16 and peptide SDD31 also inhibited biotin-XI binding in the presence of HK with an IC50 of 4.7 nM and 50 μM, respectively. Alternatively, peptide T249-F260 of FXI’s apple domain 3 and heparin monosulfate were weak inhibitors of FXI binding to HUVEC. FXI bound to HUVEC with an apparent K d of 6.9 ± 3.0 nM and B max of 13 ± 2.6106 sites/cell. FXI bound to HK on HUVEC, but not prothrombin, became converted to FXIa. FXI activation on HUVEC resulted from tissue culture media bovine factor XIIa. HUVEC grown in human factor XII-deficient serum did not support FXI activation. FXI binding to HUVEC in culture was mostly mediated by HK and FXI activation on HUVEC is dependent on cell-associated factor XIIa.

Keywords

Factor XI - high molecular weight kininogen - factor XII - prekallikrein - prothrombin
 

  • References

  • 1 Thompson RE, Mandle Jr R, Kaplan AP. Association of factor XI and high molecular weight kininogen in human plasma. J Clin Invest 1977; 60: 1376-80.
    CrossrefPubMedGoogle Scholar
  • 2 Bouma BN, Griffin JH. Human blood coagulation factor XI. Purification, properties, and mechanism of activation by activated factor XII. J Biol Chem 1977; 252: 6432-7.
    PubMedGoogle Scholar
  • 3 Davie EW, Fujikawa K, Kurachi K, Kisiel W. The role of serine proteases in the blood coagulation cascade. Adv Enzymol Relat Areas Mol Biol. 1979; 48: 277-318.
    PubMedGoogle Scholar
  • 4 Ahmad SS, Rawala-Sheikh R, Walsh PN. Comparative interactions of factor IX and factor IXa with human platelets. J Biol Chem 1989; 264: 3244-51.
    PubMedGoogle Scholar
  • 5 Fujikawa K, Chung DW, Hendrickson LE, Davie EW. Amino acid sequence of human factor XI, a blood coagulation factor with four tandem repeats that are highly homologous with plasma prekallikrein. Biochemistry 1986; 25: 2417-24.
    CrossrefPubMedGoogle Scholar
  • 6 Baglia FA, Jameson BA, Walsh PN. Fine mapping of the high molecular weight kininogen binding site on blood coagulation factor XI through the use of rationally designed synthetic analogs. J Biol Chem 1992; 267: 4247-52.
    PubMedGoogle Scholar
  • 7 Baglia FA, Jameson BA, Walsh PN. Identification and chemical synthesis of a substrate-binding site for factor IX on coagulation factor XIa. J Biol Chem 1991; 266: 24190-7.
    PubMedGoogle Scholar
  • 8 Berrettini M, Schleef RR, Heeb MJ, Hopmeier P, Griffin JH. Assembly and expression of an intrinsic factor IX activator complex on the surface of cultured human endothelial cells. J Biol Chem 1992; 267: 19833-9.
    PubMedGoogle Scholar
  • 9 Sinha D, Seaman FS, Koshy A, Knight LC, Walsh PN. Blood coagulation factor XIa binds specifically to a site on activated human platelets distinct from that for factor XI. J Clin Invest 1984; 73: 1550-6.
    CrossrefPubMedGoogle Scholar
  • 10 Greengard JS, Heeb MJ, Ersdal E, Walsh PN, Griffin JH. Binding of coagulation factor XI to washed human platelets. Biochemistry 1986; 25: 3884-90.
    CrossrefPubMedGoogle Scholar
  • 11 Ho DH, Badellino K, Baglia FA, Walsh PN. A binding site for heparin in the apple 3 domain of factor XI. J Biol Chem 1998; 273: 16382-90.
    CrossrefPubMedGoogle Scholar
  • 12 Zhao M, Abel-Razek T, Sun M-F, Galani D. Characterization of a heparin binding site on the heavy chain of factor XI. J Biol Chem 1998; 273: 31153-9.
    CrossrefPubMedGoogle Scholar
  • 13 Baglia FA, Walsh PN. A binding site for thrombin in the apple 1 domain of factor XI J. Biol Chem 1996; 271: 3652-8.
    CrossrefPubMedGoogle Scholar
  • 14 Ho DH, Baglia FA, Walsh PN. Factor XI binding to activated platelets is mediated by residues R250, K255, F260, Q263 within the Apple 3 domain. Biochemistry 2000; 39: 316-23.
    CrossrefPubMedGoogle Scholar
  • 15 Baglia FA, Walsh PN. Prothrombin is a cofactor for the binding of factor XI to the platelet surface and for platelet-mediated factor XI activation by thrombin. Biochemistry 1998; 37: 2271-81.
    CrossrefPubMedGoogle Scholar
  • 16 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.
    CrossrefPubMedGoogle Scholar
  • 17 Shariat-Madar Z, Mahdi F, Schmaier AH. Mapping binding domains of kininogens on endothelial cell cytokeratin 1. J Biol Chem 1999; 274: 7137-45.
    CrossrefPubMedGoogle Scholar
  • 18 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.
    CrossrefPubMedGoogle Scholar
  • 19 Colman RW, Pixley RA, Najamunnisa S, Yan W, Wang J, Mazar A, McCrae KR. 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.
    CrossrefPubMedGoogle Scholar
  • 20 Joseph K, Ghebrehiwet B, Peerschke EI, Reid KB, Kaplan AP. 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 (gC1q-R). Proc Natl Acad Sci USA 1996; 93: 8552-7.
    CrossrefPubMedGoogle Scholar
  • 21 Herwald H, Dedio J, Kellner R, Loos M, Mueller-Esterl W. Isolation and Characterization of the Kininogen-binding Protein p33 from Endothelial Cells. Identity with the gC1q Receptor. J Biol Chem 1996; 271: 13040-7.
    CrossrefPubMedGoogle Scholar
  • 22 Colman RW, Bagdararian A, Talamo RC, Scott CF, Seavey M, Guimares JA, Pierce JV, Kaplan AP. Williams trait: human kininogen deficiency with diminished levels of plasminogen proactivator and prekallikrein associated with abnormalities of the Hageman-dependent pathways. J Clin Invest 1975; 56: 1650-62.
    CrossrefPubMedGoogle Scholar
  • 23 Chung DW, Fujikawa K, McMullen BA, Davie EW. Human plasma prekallikrein, a zymogen to a serine protease that contains four tandem repeats. Biochemistry 1986; 25: 2410-7.
    CrossrefPubMedGoogle Scholar
  • 24 Kitamura N, Kitagawa H, Fukushima D, Takagaki Y, Miyata T, Nakanishi S. Structural organization of the human kininogen gene and a model for its evolution. J Biol Chem 1985; 260: 8610-7.
    PubMedGoogle Scholar
  • 25 Tait JF, Fujikawa K. Primary structure requirements for the binding of human high molecular weight kininogen to plasma prekallikrein and factor XI. J Biol Chem 1987; 262: 11651-6.
    PubMedGoogle Scholar
  • 26 Kaufmann J, Haasemann M, Modrow S, Muller-Esterl W. Structural dissection of the multidomain kininogens. Fine mapping of the target epitopes of antibodies interfering with their functional properties. J Biol Chem 1993; 268: 9079-91.
    PubMedGoogle Scholar
  • 27 Motta G, Rojkjaer R, Hasan AAK, Cines DB, Schmaier AH. High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 1998; 91: 516-28.
    PubMedGoogle Scholar
  • 28 Scatchard G. The attraction for proteins for small molecules and ions. Ann NY Acad Sci 1949; 51: 660-72.
    CrossrefPubMedGoogle Scholar
  • 29 Meloni FJ, Gustafson EJ, Schmaier AH. High molecular weight kininogen binds to platelets by its heavy and light chains and when bound has altered susceptibility to kallikrein cleavage. Blood 1992; 79: 1233-44.
    PubMedGoogle Scholar
  • 30 Bock PE, Shore JD, Tans G, Griffin JH. Protein-Protein interactions in contact activation of blood coagulation. J Biol Chem 1985; 260: 12434-43.
    PubMedGoogle Scholar
  • 31 Warn-Cramer BJ, Bajaj SP. Stoichiometry of binding of high molecular weight kininogen to factor XI/Xia. Biochem Biophys Res Commun 1985; 133: 417-22.
    CrossrefPubMedGoogle Scholar
  • 32 Schmaier AH, Kuo A, Lundberg D, Murray S, Cines DB. The expression of high molecular weight kininogen on human umbilical vein endothelial cells. J Biol Chem 1988; 263: 16327-33.
    PubMedGoogle Scholar
  • 33 Rojkjaer R, Hasan AAK, Motta G, Schousboe I, Schmaier AH. Factor XII does not initiate prekallikrein activation on endothelial cells. Thromb Haemost 1998; 80: 74-81.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 34 Weisel JW, Nagaswami C, Woohead JL, DeLa Cadena RA, Page JD, Colman RW. The shape of high molecular weight kininogen: organization into structural domains, chnages with activation, and interactions with prekallikrein, as determined by electron microscopy. J Biol Chem 1994; 269: 10100-6.
    PubMedGoogle Scholar
  • 35 Naito K, Fujikawa K. Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J Biol Chem 1991; 266: 7353-8.
    PubMedGoogle Scholar
  • 36 Gailani D, Broze Jr GJ. Factor XI activation in a revised model of blood coagulation. Science 1991; 253: 909-12.
    CrossrefPubMedGoogle Scholar
  • 37 Scott CF, Silver LD, Purdon AD, Colman RW. Cleavage of human high molecular weight kininogen by factor XIa in vitro. Effect on structure and function. J Biol Chem 1985; 260: 10856-63.
    PubMedGoogle Scholar
  • 38 Brown NJ, Nadeau JH, Vaughan DE. Selective stimulation of tissue-type plasminogen activator (tPA) in vivo by infusion of bradykinin. Thromb Haemost 1997; 77: 522-5.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 39 Hong SL. Effect of bradykinin and thrombin on prostacyclin synthesis in endothelial cells from calf and pig aorta and human umbilical cord vein. Thromb Res 1980; 18: 787-95.
    CrossrefPubMedGoogle Scholar
  • 40 Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987; 327: 524-6.
    CrossrefPubMedGoogle Scholar