Platelets promote coagulation factor XII-mediated proteolytic cascade systems in plasma
-
Julia Johne
Abstract
Blood coagulation factor XII (FXII, Hageman factor) is a plasma serine protease which is autoactivated following contact with negatively charged surfaces in a reaction involving plasma kallikrein and high-molecular-weight kininogen (contact phase activation). Active FXII has the ability to initiate blood clotting via the intrinsic pathway of coagulation and inflammatory reactions via the kallikrein-kinin system. Here we have determined FXII-mediated bradykinin formation and clotting in plasma. Western blotting analysis with specific antibodies against various parts of the contact factors revealed that limited activation of FXII is sufficient to promote plasma kallikrein activation, resulting in the conversion of high-molecular-weight kininogen and bradykinin generation. The presence of platelets significantly promoted FXII-initiated bradykinin formation. Similarly, in vitro clotting assays revealed that platelets critically promoted FXII-driven thrombin and fibrin formation. In summary, our data suggest that FXII-initiated protease cascades may proceed on platelet surfaces, with implications for inflammation and clotting.
References
Ahmad, S., Rawala-Sheikh, R., and Walsh, P. (1989). Comparative interactions of factor IX and factor IXa with human platelets. J. Biol. Chem.264, 3244–3251.10.1016/S0021-9258(18)94058-5Suche in Google Scholar
Aronson, D.L., Chang, P., and Kessler, C.M. (1992). Platelet-dependent thrombin generation after in vitro fibrinolytic treatment. Circulation85, 1706–1712.10.1161/01.CIR.85.5.1706Suche in Google Scholar
Baglia, F.A., Badellino, K.O., Li, C.Q., Lopez, J.A., and Walsh, P.N. (2002). Factor XI binding to the platelet glycoprotein Ib-IX-V complex promotes factor XI activation by thrombin. J. Biol. Chem.277, 1662–1668.10.1074/jbc.M108319200Suche in Google Scholar PubMed
Baird, T.R. and Walsh, P.N. (2002). Activated platelets but not endothelial cells participate in the initiation of the consolidation phase of blood coagulation. J. Biol. Chem.277, 28498–28503.10.1074/jbc.M203427200Suche in Google Scholar PubMed
Colman, R.W. (1998). The contact system: a proinflammatory pathway with antithrombotic activity. Nat. Med.4, 277–278.10.1038/nm0398-277Suche in Google Scholar PubMed
Colman, R.W. and Schmaier, A.H. (1997). Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood90, 3819–3843.10.1182/blood.V90.10.3819Suche in Google Scholar
Cool, D.E. and MacGillivray, R.T. (1987). Characterization of the human blood coagulation factor XII gene. Intron/exon gene organization and analysis of the 5'-flanking region. J. Biol. Chem.262, 13662–13673.Suche in Google Scholar
Gailani, D. and Broze, G.J. Jr. (1991). Factor XI activation in a revised model of blood coagulation. Science253, 909–912.10.1126/science.1652157Suche in Google Scholar PubMed
Girolami, A., Randi, M.L., Gavasso, S., Lombardi, A.M., and Spiezia, F. (2004). The occasional venous thromboses seen in patients with severe (homozygous) FXII deficiency are probably due to associated risk factors: a study of prevalence in 21 patients and review of the literature. J. Thromb. Thrombolysis17, 139–143.10.1023/B:THRO.0000037670.42776.cdSuche in Google Scholar
Haasemann, M., Buschko, J., Faussner, A., Roscher, A.A., Hoebeke, J., Burch, R.M., and Müller-Esterl, W. (1991). Anti-idiotypic antibodies bearing the internal image of a bradykinin epitope. Production, characterization, and interaction with the kinin receptor. J. Immunol.147, 3882–3892.Suche in Google Scholar
Henderson, L.M., Figueroa, C.D., Müller-Esterl, W., and Bhoola, K.D. (1994). Assembly of contact-phase factors on the surface of the human neutrophil membrane. Blood84, 474–482.10.1182/blood.V84.2.474.474Suche in Google Scholar
Herwald, H., Morgelin, M., Olsen, A., Rhen, M., Dahlback, B., Müller-Esterl, W., and Bjorck, L. (1998). Activation of the contact-phase system on bacterial surfaces – a clue to serious complications in infectious diseases. Nat. Med.4, 298–302.10.1038/nm0398-298Suche in Google Scholar PubMed
Joseph, K., Tholanikunnel, B.G., and Kaplan, A.P. (2002). Heat shock protein 90 catalyzes activation of the prekallikrein-kininogen complex in the absence of factor XII. Proc. Natl. Acad. Sci. USA99, 896–900.10.1073/pnas.022626899Suche in Google Scholar PubMed PubMed Central
Kaplan, A.P., Joseph, K., and Silverberg, M. (2002). Pathways for bradykinin formation and inflammatory disease. J. Allergy Clin. Immunol.109, 195–209.10.1067/mai.2002.121316Suche in Google Scholar PubMed
Leeb-Lundberg, L.M., Marceau, F., Müller-Esterl, W., Pettibone, D.J., and Zuraw, B.L. (2005). Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol. Rev.57, 27–77.10.1124/pr.57.1.2Suche in Google Scholar PubMed
Mackman, N. (2004). Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler. Thromb. Vasc. Biol.24, 1015–1022.10.1161/01.ATV.0000130465.23430.74Suche in Google Scholar PubMed
Mann, K.G. (2003). Thrombin formation. Chest124, 4–10.10.1378/chest.124.3_suppl.4SSuche in Google Scholar
Nieswandt, B., Schulte, V., Bergmeier, W., Mokhtari-Nejad, R., Rackebrandt, K., Cazenave, J.P., Ohlmann, P., Gachet, C., and Zirngibl, H. (2001). Long-term antithrombotic protection by in vivo depletion of platelet glycoprotein VI in mice. J. Exp. Med.193, 459–469.10.1084/jem.193.4.459Suche in Google Scholar PubMed PubMed Central
Osterud, B. and Rapaport, S.I. (1977). Activation of factor IX by the reaction product of tissue factor and factor VII: additional pathway for initiating blood coagulation. Proc. Natl. Acad. Sci. USA74, 5260–5264.10.1073/pnas.74.12.5260Suche in Google Scholar PubMed PubMed Central
Pauer, H.U., Renné, T., Hemmerlein, B., Legler, T., Fritzlar, S., Adham, I., Müller-Esterl, W., Emons, G., Sancken, U., Engel, W., and Burfeind, P. (2004). Targeted deletion of murine coagulation factor XII gene – a model for contact phase activation in vivo. Thromb. Haemost.92, 503–508.10.1160/TH04-04-0250Suche in Google Scholar PubMed
Pixley, R., DeLa Cadena, R., Page, J., Kauffman, N., Wyshock, E., Chang, A., Taylor, F., and Colman, R. (1993). The contact system contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia: in vivo use of a monoclonal anti-factor XII antibody to block contact activation in baboons. J. Clin. Invest.91, 61–68.10.1172/JCI116201Suche in Google Scholar PubMed PubMed Central
Polanowska-Grabowska, R. and Gear, A.R. (2000). Heat-shock proteins and platelet function. Platelets11, 6–22.10.1080/09537100075742Suche in Google Scholar PubMed
Ratnoff, O.D. and Colopy, J.E. (1955). A familial hemorrhagic trait associated with a deficiency of a clot-promoting fraction of plasma. J. Clin. Invest.34, 602–613.10.1172/JCI103109Suche in Google Scholar
Ratnoff, O.D. and Saito, H. (1979). Surface-mediated reactions. Curr. Top. Hematol.2, 1–57.Suche in Google Scholar
Renné, T., Dedio, J., Meijers, J.C., Chung, D., and Müller-Esterl, W. (1999). Mapping of the discontinuous H-kininogen binding site of plasma prekallikrein. Evidence for a critical role of apple domain-2. J. Biol. Chem.274, 25777–25784.10.1074/jbc.274.36.25777Suche in Google Scholar
Renné, T., Gailani, D., Meijers, J.C., and Müller-Esterl, W. (2002). Characterization of the H-kininogen-binding site on factor XI: a comparison of factor XI and plasma prekallikrein. J. Biol. Chem.277, 4892–4899.10.1074/jbc.M105221200Suche in Google Scholar
Renné, T., Pozgajova, M., Gruner, S., Schuh, K., Pauer, H.U., Burfeind, P., Gailani, D., and Nieswandt, B. (2005a). Defective thrombus formation in mice lacking coagulation factor XII. J. Exp. Med.202, 271–281.10.1084/jem.20050664Suche in Google Scholar
Renné, T., Schuh, K., and Müller-Esterl, W. (2005b). Local bradykinin formation is controlled by glycosaminoglycans. J. Immunol.175, 3377–3385.10.4049/jimmunol.175.5.3377Suche in Google Scholar
Seligsohn, U. and Griffin J.H. (1995). Contact activation and factor XI. In: The Metabolic and Molecular Bases of Inherited Disease, C. Scriver, A. Beaudet, W. Sly and D. Valle, eds. (New York, USA: McGraw-Hill), pp. 3289–3311.Suche in Google Scholar
Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (2002). Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J. Biol. Chem.277, 17962–17969.10.1074/jbc.M106101200Suche in Google Scholar
Shibayama, Y., Reddigari, S., and Kaplan, A.P. (1996). Interactions of factor XII with platelets and endothelial cells. Immunopharmacology32, 24–27.10.1016/0162-3109(96)00004-5Suche in Google Scholar
Sreedhar, A.S., Kalmar, E., Csermely, P., and Shen, Y.F. (2004). Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett.562, 11–15.10.1016/S0014-5793(04)00229-7Suche in Google Scholar
Tapper, H. and Herwald, H. (2000). Modulation of hemostatic mechanisms in bacterial infectious diseases. Blood96, 2329–2337.10.1182/blood.V96.7.2329Suche in Google Scholar
Walsh, P.N. (2001). Roles of platelets and factor XI in the initiation of blood coagulation by thrombin. Thromb. Haemost.86, 75–82.10.1055/s-0037-1616203Suche in Google Scholar
Zeerleder, S., Schloesser, M., Redondo, M., Wuillemin, W.A., Engel, W., Furlan, M., and Lammle, B. (1999). Reevaluation of the incidence of thromboembolic complications in congenital factor XII deficiency – a study on 73 subjects from 14 Swiss families. Thromb. Haemost.82, 1240–1246.10.1055/s-0037-1614368Suche in Google Scholar
©2006 by Walter de Gruyter Berlin New York
Artikel in diesem Heft
- Exploring the future of local vascular and inflammatory mediators
- Genetically altered animal models in the kallikrein-kinin system
- The kinin system mediates hyperalgesia through the inducible bradykinin B1 receptor subtype: evidence in various experimental animal models of type 1 and type 2 diabetic neuropathy
- Cross-talk of the renin-angiotensin and kallikrein-kinin systems
- Which endothelium-derived factors are really important in humans?
- Kinin- and angiotensin-converting enzyme (ACE) inhibitor-mediated nitric oxide production in endothelial cells
- Anti-inflammatory effects of kinins via microglia in the central nervous system
- Platelets promote coagulation factor XII-mediated proteolytic cascade systems in plasma
- Three-dimensional structure of an AMPA receptor without associated stargazin/TARP proteins
- Dual antagonists of the bradykinin B1 and B2 receptors based on a postulated common pharmacophore from existing non-peptide antagonists
- Generation and characterization of a humanized bradykinin B1 receptor mouse
- The role of bradykinin B1 receptor on cardiac remodeling in stroke-prone spontaneously hypertensive rats (SHR-SP)
- Molecular identification and pharmacological profile of the bovine kinin B1 receptor
- Interplay of human tissue kallikrein 4 (hK4) with the plasminogen activation system: hK4 regulates the structure and functions of the urokinase-type plasminogen activator receptor (uPAR)
- Cathepsin B localizes to plasma membrane caveolae of differentiating myoblasts and is secreted in an active form at physiological pH
Artikel in diesem Heft
- Exploring the future of local vascular and inflammatory mediators
- Genetically altered animal models in the kallikrein-kinin system
- The kinin system mediates hyperalgesia through the inducible bradykinin B1 receptor subtype: evidence in various experimental animal models of type 1 and type 2 diabetic neuropathy
- Cross-talk of the renin-angiotensin and kallikrein-kinin systems
- Which endothelium-derived factors are really important in humans?
- Kinin- and angiotensin-converting enzyme (ACE) inhibitor-mediated nitric oxide production in endothelial cells
- Anti-inflammatory effects of kinins via microglia in the central nervous system
- Platelets promote coagulation factor XII-mediated proteolytic cascade systems in plasma
- Three-dimensional structure of an AMPA receptor without associated stargazin/TARP proteins
- Dual antagonists of the bradykinin B1 and B2 receptors based on a postulated common pharmacophore from existing non-peptide antagonists
- Generation and characterization of a humanized bradykinin B1 receptor mouse
- The role of bradykinin B1 receptor on cardiac remodeling in stroke-prone spontaneously hypertensive rats (SHR-SP)
- Molecular identification and pharmacological profile of the bovine kinin B1 receptor
- Interplay of human tissue kallikrein 4 (hK4) with the plasminogen activation system: hK4 regulates the structure and functions of the urokinase-type plasminogen activator receptor (uPAR)
- Cathepsin B localizes to plasma membrane caveolae of differentiating myoblasts and is secreted in an active form at physiological pH