Download PDF
Thromb Haemost 2001; 86(01): 75-82
DOI: 10.1055/s-0037-1616203
Research Article
Schattauer GmbH

Roles of Platelets and Factor XI in the Initiation of Blood Coagulation by Thrombin[*]

Peter N. Walsh
1   The Sol Sherry Thrombosis Research Center, Departments of Medicine and Biochemistry, Temple University School of Medicine, Philadelphia, PA, USA
› Author Affiliations
Further Information

Publication History

Publication Date:
12 December 2017 (online)

Also available at
    Permissions and Reprints

Summary

To account for the variable hemostatic defect in patients with factor XI (FXI) deficiency, with normal hemostasis in contact factor deficiencies, a coagulation paradigm is presented whereby trace quantities of thrombin, generated transiently by exposure of tissue factor at sites of vascular injury, activates FXI bound to the platelet surface in the presence of prothrombin or high Mr kininogen (HK). Tissue factor pathway inhibitor (TFPI) limits the flux of thrombin generated by the tissue factor pathway, and protease nexin II (PNII), released from activated platelets, inhibits solution phase FXIa and localizes FIX activation to the platelet surface where FXIa is protected from inactivation by PNII. Either prothrombin or HK binds to the Apple 1 (A1) domain of FXI, thereby exposing a platelet-binding site in the FXI A3 domain. Dimeric FXI binds to activated platelets directly through the A3 domain of one monomer. After proteolytic activation of platelet-bound FXI by thrombin (or FXIIa), a substrate binding site for FIX is exposed in the opposite monomer that promotes FIX activation on the platelet surface resulting in the local explosive generation of thrombin and the formation of hemostatic thrombi at sites of vascular injury.

Key words

Factor XI - factor IX - protease nexin II - factor XII - high Mr kininogen

* This study was supported by research grants from the National Institute of Health (HL46213, HL56914, and HL64943)


 

  • References

  • 1 MacFarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature 1964; 202: 498-99.
    CrossrefPubMedGoogle Scholar
  • 2 Davie EW, Ratnoff OD. Waterfall sequence for intrinsic blood clotting. Science 1964; 145: 1310-2.
    CrossrefPubMedGoogle Scholar
  • 3 Colman RW. Contact activation pathway: inflammatory, fibrinolytic, anticoagulant, antiadhesive and antiangiogenic activities. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN. eds. Philadelphia: J. B. Lippincott Williams & Wilkins; 2001: 103-22.
    Google Scholar
  • 4 Morrissey JH. Tissue factor and factor VII initiation of coagulation. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN. eds. Philadelphia: J. B. Lippincott Williams & Wilkins; 2001: 89-102.
    Google Scholar
  • 5 Walsh PN. Platelet coagulant activities and hemostasis: a hypothesis. Blood 1974; 43: 597-605.
    PubMedGoogle Scholar
  • 6 Walsh PN. Factor XI. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN. eds. Philadelphia: J. B. Lippincott Williams & Wilkins; 2001: 191-202.
    Google Scholar
  • 7 Asakai R, Chung DW, Davie EW, Seligsohn U. Factor XI deficiency in Ashkenazi Jews in Israel. N Engl J Med 1991; 325: 153-8.
    CrossrefPubMedGoogle Scholar
  • 8 Bolton-Maggs PH, Young Wan-Yin B, McCraw AH, Slack J, Kernoff PB. Inheritance and bleeding in factor XI deficiency. Br J Haematol 1988; 69: 521-8.
    CrossrefPubMedGoogle Scholar
  • 9 Hu CJ, Baglia FA, Mills DC, Konkle BA, Walsh PN. Tissue-specific expression of functional platelet factor XI is independent of plasma factor XI expression. Blood 1998; 91: 3800-7.
    PubMedGoogle Scholar
  • 10 Leiba H, Ramot B, Many A. Hereditary and coagulation studies in ten families with factor XI (plasma thromboplastin antecedent) deficiency. Br J Haematol 1965; 11: 654-65.
    CrossrefPubMedGoogle Scholar
  • 11 Ragni MV, Sinha D, Seaman F, Lewis JH, Spero JA, Walsh PN. Comparison of bleeding tendency, factor XI coagulant activity, and factor XI antigen in 25 factor XI-deficient kindreds. Blood 1985; 65: 719-24.
    PubMedGoogle Scholar
  • 12 Rapaport SI, Proctor RR, Patch MJ, Yettra M. The mode of inheritance of PTA deficiency: evidence for the existence of a major PTA deficiency and a minor PTA deficiency. Blood 1961; 18: 149-55.
    PubMedGoogle Scholar
  • 13 Rosenthal RL, Dreskin OH, Rosenthal N. New hemophilia-like disease caused by deficiency of a third plasma thromboplastin factor. Proc Soc Exp Biol Med 1953; 82: 171-4.
    CrossrefPubMedGoogle Scholar
  • 14 Sidi A, Seligsohn U, Jonas P, Many M. Factor XI deficiency: detection and management during urologic surgery. J Urol 1978; 119: 528-30.
    CrossrefPubMedGoogle Scholar
  • 15 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
  • 16 Gailani D, Broze Jr GJ. Factor XI activation in a revised model of blood coagulation. Science 1991; 253: 909-12.
    CrossrefPubMedGoogle Scholar
  • 17 Broze GJJ, Miletich JP. Isolation of the tissue factor inhibitor produced by HepG2 hepatoma cells. Proc Natl Acad Sci USA 1987; 84: 1886-90.
    CrossrefPubMedGoogle Scholar
  • 18 Broze GJJ, Miletich JP. Characterization of the inhibition of tissue factor in serum. Blood 1987; 69: 150-5.
    PubMedGoogle Scholar
  • 19 Hubbard AR, Jennings CA. Inhibition of tissue thromboplastin-mediated blood coagulation. Thromb Res 1986; 42: 489-98.
    CrossrefPubMedGoogle Scholar
  • 20 Hubbard AR, Jennings CA. Inhibition of the tissue factor-factor VII complex: involvement of factor Xa and lipoproteins. Thromb Res 1987; 46: 527-37.
    CrossrefPubMedGoogle Scholar
  • 21 Morrison SA, Jesty J. Tissue factor-dependent activation of tritium labeled factor IX and factor X in human plasma. Blood 1984; 63: 1338-47.
    PubMedGoogle Scholar
  • 22 Rao LVM, Rapaport SI. Studies on the mechanisms of inactivation of the extrinsic pathway of coagulation. Blood 1987; 69: 645-51.
    PubMedGoogle Scholar
  • 23 Sanders NL, Bajaj SP, Zivelin A, Rapaport SI. Inhibition of tissue factor/ factor VIIa activity in plasma requires factor X and an additional plasma component. Blood 1985; 66: 204-12.
    PubMedGoogle Scholar
  • 24 Ahmad SS, Rawala-Sheikh R, Ashby B, Walsh PN. Platelet receptor-mediated factor X activation by factor IXa. High-affinity factor IXa receptors induced by factor VIII are deficient on platelets in Scott syndrome. J Clin Invest 1989; 84: 824-8.
    CrossrefPubMedGoogle Scholar
  • 25 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
  • 26 Ahmad SS, Rawala-Sheikh R, Walsh PN. Platelet receptor occupancy with factor IXa promotes factor X activation. J Biol Chem 1989; 264: 20012-6.
    PubMedGoogle Scholar
  • 27 Baglia FA, Jameson BA, Walsh PN. Identification and characterization of a binding site for platelets in the Apple 3 domain of coagulation factor XI. J Biol Chem 1995; 270: 6734-40.
    CrossrefPubMedGoogle Scholar
  • 28 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
  • 29 Oliver JA, Monroe DM, Roberts HR, Hoffman M. Thrombin activates factor XI on activated platelets in the absence of factor XII. Arterioscler Thromb Vasc Biol 1999; 19: 170-7.
    CrossrefPubMedGoogle Scholar
  • 30 Baglia FA, Walsh PN. Thrombin-mediated feedback activation of factor XI on the activated platelet surface is preferred over contact activation by factor XIIa or factor XIa. J Biol Chem 2000; 275: 20514-9.
    CrossrefPubMedGoogle Scholar
  • 31 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
  • 32 Rawala-Sheikh R, Ahmad SS, Ashby B, Walsh PN. Kinetics of coagulation factor X activation by platelet-bound factor IXa. Biochemistry 1990; 29: 2606-11.
    CrossrefPubMedGoogle Scholar
  • 33 Walsh PN. The effects of collagen and kaolin on the intrinsic coagulant activity of platelets. Evidence for an alternative pathway in intrinsic coagulation not requiring factor XII. Br J Haematol 1972; 22: 393-405.
    CrossrefPubMedGoogle Scholar
  • 34 Walsh PN. The role of platelets in the contact phase of blood coagulation. Br J Haematol 1972; 22: 237-54.
    CrossrefPubMedGoogle Scholar
  • 35 Walsh PN, Biggs R. The role of platelets in intrinsic factor-Xa formation. Br J Haematol 1972; 22: 743-60.
    CrossrefPubMedGoogle Scholar
  • 36 Walsh PN, Griffin JH. Contributions of human platelets to the proteolytic activation of blood coagulation factors XII and XI. Blood 1981; 57: 106-18.
    PubMedGoogle Scholar
  • 37 Hsu TC, Shore SK, Seshsmma T, Bagasra O, Walsh PN. Molecular cloning of platelet factor XI, an alternative splicing product of the plasma factor XI gene. J Biol Chem 1998; 273: 13787-93.
    CrossrefPubMedGoogle Scholar
  • 38 Lipscomb MS, Walsh PN. Human platelets and factor XI. Localization in platelet membranes of factor XI-like activity and its functional distinction from plasma factor XI. J Clin Invest 1979; 63: 1006-14.
    CrossrefPubMedGoogle Scholar
  • 39 Walsh PN. Albumin density gradient separation and washing of platelets and the study of platelet coagulant activities. Br J Haematol 1972; 22: 205-17.
    CrossrefPubMedGoogle Scholar
  • 40 Badellino K, Walsh PN. Localization of the heparin binding site on the catalytic domain of factor XIa. Blood 1998; 92: 39a (abstr.).
    PubMedGoogle Scholar
  • 41 Badellino KO, Walsh PN. Protease nexin II interactions with coagulation factor XIa are contained within the Kunitz protease inhibitor domain of protease nexin II and the factor XIa catalytic domain. Biochemistry 2000; 39: 4769-77.
    CrossrefPubMedGoogle Scholar
  • 42 Scandura JM, Zhang Y, Van Nostrand WE, Walsh PN. Progress curve analysis of the kinetics with which blood coagulation factor XIa is inhibited by protease nexin-2. Biochemistry 1997; 36: 412-20.
    CrossrefPubMedGoogle Scholar
  • 43 Zhang Y, Scandura JM, Van Nostrand WE, Walsh PN. The mechanism by which heparin promotes the inhibition of coagulation factor XIa by protease nexin-2. J Biol Chem 1997; 272: 26139-44.
    CrossrefPubMedGoogle Scholar
  • 44 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
  • 45 Heck LW, Kaplan AP. Substrates of Hageman factor. I. Isolation and characterization of human factor XI (PTA) and inhibition of the activated enzyme by alpha 1-antitrypsin. J Exp Med 1974; 140: 1615-30.
    CrossrefPubMedGoogle Scholar
  • 46 Kurachi K, Davie EW. Activation of human factor XI (plasma thromboplastin antecedent) by factor XIIa (activated Hageman factor). Biochemistry 1977; 16: 5831-9.
    CrossrefPubMedGoogle Scholar
  • 47 Movat HZ, Ozge-Anwar AH. The contact phase of blood coagulation: clotting factors XI and XII, their isolation and interaction. J Lab Clin Med 1974; 84: 861-78.
    PubMedGoogle Scholar
  • 48 Saito H, Goldsmith Jr GH. Plasma thromboplastin antecedent (PTA, factor XI): a specific and sensitive radioimmunoassay. Blood 1977; 50: 377-85.
    PubMedGoogle Scholar
  • 49 Asakai R, Davie EW, Chung DW. Organization of the gene for human factor XI. Biochemistry 1987; 26: 7221-8.
    CrossrefPubMedGoogle Scholar
  • 50 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
  • 51 Kato A, Asakai R, Davie EW, Aoki N. Factor XI gene (F11) is located on the distal end of the long arm of human chromosome 4. Cytogenet Cell Genet 1989; 52: 77-8.
    CrossrefPubMedGoogle Scholar
  • 52 Tordai H, Banyai L, Patthy L. The PAN module: the N-terminal domains of plasminogen and hepatocyte growth factor are homologous with the apple domains of the prekallikrein family and with a novel domain found in numerous nematode proteins. FEBS Lett 1999; 461: 63-7.
    CrossrefPubMedGoogle Scholar
  • 53 Brown PJ, Billington KJ, Bumstead JM, Clark JD, Tomley FM. A micro-neme protein from Eimeria tenella with homology to the Apple domains of coagulation factor XI and plasma pre-kallikrein. Mol Biochem Parasitol 2000; 107: 91-102.
    CrossrefPubMedGoogle Scholar
  • 54 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
  • 55 Wiggins RC, Bouma BN, Cochrane CG, Griffin JH. Role of high-molecular-weight kininogen in surface-binding and activation of coagulation Factor XI and prekallikrein. Proc Natl Acad Sci USA 1977; 74: 4636-40.
    CrossrefPubMedGoogle Scholar
  • 56 Baglia FA, Jameson BA, Walsh PN. Localization of the high molecular weight kininogen binding site in the heavy chain of human factor XI to amino acids phenylalanine 56 through serine 86. J Biol Chem 1990; 265: 4149-54.
    PubMedGoogle Scholar
  • 57 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
  • 58 Seaman FS, Baglia FA, Gurr JA, Jameson BA, Walsh PN. Binding of high-molecular-mass kininogen to the Apple 1 domain of factor XI is mediated in part by Val64 and Ile77. Biochem J 1994; 304: 715-21.
    CrossrefPubMedGoogle Scholar
  • 59 Castaldi PA, Larrieu MJ, Caen J. Availability of platelet Factor 3 and activation of factor XII in thrombasthenia. Nature 1965; 207: 422-4.
    CrossrefPubMedGoogle Scholar
  • 60 Mustard JF, Hegardt B, Roswell HC, MacMillan RL. Effect of adenosine nucleotides on platelet aggregation and clotting time. J Lab Clin Med 1964; 65: 548-59.
    PubMedGoogle Scholar
  • 61 Mustard JF, Rowsell HC, Lotz F, Hegardt B, Murphy EA. The effect of adenine nucleotides on thrombus formation, platelet count, and blood coagulation. Exp Mol Pathol 1966; 5: 43-60.
    CrossrefPubMedGoogle Scholar
  • 62 Pizzuto J, Giorgio AJ, Didisheim P. The clot-promoting effect of adenosine-5′-diphosphate (ADP). I. Mechanisms of action. Thromb Diath Haemorrh 1966; 15: 428-35.
    PubMedGoogle Scholar
  • 63 Weiss HJ, Kochwa S. Studies of platelet function and proteins in 3 patients with Glanzmann’s thrombasthenia. J Lab Clin Med 1968; 71: 153-65.
    PubMedGoogle Scholar
  • 64 Baglia FA, Seaman FS, Walsh PN. The Apple 1 and Apple 4 domains of factor XI act synergistically to promote the surface-mediated activation of factor XI by factor XIIa. Blood 1995; 85: 2078-83.
    PubMedGoogle Scholar
  • 65 Ho DH, Badellino K, Baglia FA, Sun MF, Zhao MM, Gailani D, Walsh PN. The role of high molecular weight kininogen and prothrombin as cofactors in the binding of factor XI A3 domain to the platelet surface. J Biol Chem 2000; 275: 25139-45.
    CrossrefPubMedGoogle Scholar
  • 66 Ho DH, Baglia FA, Walsh PN. Factor XI binding to activated platelets is mediated by residues R(250), K(255), F(260), and Q(263) within the Apple 3 domain. Biochemistry 2000; 39: 316-23.
    CrossrefPubMedGoogle Scholar
  • 67 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
  • 68 Zhao M, Abdel-Razek TT, Sun M-F, Gailani D. Characterization of the inter-action between heparin and coagulation factor XI. Blood 1998; 92: 39a (abstr.).
    PubMedGoogle Scholar
  • 69 Baglia FA, Badellino KO, Ho DH, Dasari VR, Walsh PN. A binding site for the kringle II domain of prothrombin in the apple 1 domain of factor XI. J Biol Chem 2000; 275: 31954-62.
    CrossrefPubMedGoogle Scholar
  • 70 Gailani D, Broze Jr GJ. Factor XII-independent activation of factor XI in plasma: effects of sulfatides on tissue factor-induced coagulation. Blood 1993; 82: 813-9.
    PubMedGoogle Scholar
  • 71 Scott CF, Colman RW. Fibrinogen blocks the autoactivation and thrombin-mediated activation of factor XI on dextran sulfate. Proc Natl Acad Sci USA 1992; 89: 11189-93.
    CrossrefPubMedGoogle Scholar
  • 72 Baglia FA, Jameson BA, Walsh PN. Identification and characterization of a binding site for factor XIIa in the Apple 4 domain of coagulation factor XI. J Biol Chem 1993; 268: 3838-44.
    PubMedGoogle Scholar
  • 73 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
  • 74 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
  • 75 Walsh PN, Sinha D, Koshy A, Seaman FS, Bradford H. Functional characterization of platelet-bound factor XIa: retention of factor XIa activity on the platelet surface. Blood 1986; 68: 225-30.
    PubMedGoogle Scholar
  • 76 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
  • 77 Sinha D, Koshy A, Seaman FS, Walsh PN. Functional characterization of human blood coagulation factor XIa using hybridoma antibodies. J Biol Chem 1985; 260: 10714-9.
    PubMedGoogle Scholar
  • 78 Sinha D, Seaman FS, Walsh PN. Role of calcium ions and the heavy chain of factor XIa in the activation of human coagulation factor IX. Biochemistry 1987; 26: 3768-75.
    CrossrefPubMedGoogle Scholar
  • 79 van der Graaf F, Greengard JS, Bouma BN, Kerbiriou DM, Griffin JH. Isolation and functional characterization of the active light chain of activated human blood coagulation factor XI. J Biol Chem 1983; 258: 9669-75.
    PubMedGoogle Scholar
  • 80 Sun MF, Zhao M, Gailani D. Identification of amino acids in the factor XI apple 3 domain required for activation of factor IX. J Biol Chem 1999; 274: 36373-8.
    CrossrefPubMedGoogle Scholar
  • 81 Sun Y, Gailani D. Identification of a factor IX binding site on the third apple domain of activated factor XI. J Biol Chem 1996; 271: 29023-8.
    CrossrefPubMedGoogle Scholar
  • 82 Meijers JC, Davie EW, Chung DW. Expression of human blood coagulation factor XI: characterization of the defect in factor XI type III deficiency. Blood 1992; 79: 1435-40.
    PubMedGoogle Scholar
  • 83 Meijers JC, Mulvihill ER, Davie EW, Chung DW. Apple four in human blood coagulation factor XI mediates dimer formation. Biochemistry 1992; 31: 4680-4.
    CrossrefPubMedGoogle Scholar
  • 84 McMullen BA, Fujikawa K, Davie EW. Location of the disulfide bonds in human coagulation factor XI: the presence of tandem apple domains. Biochemistry 1991; 30: 2056-60.
    CrossrefPubMedGoogle Scholar
  • 85 Dorfman R, Walsh PN. Noncovalent Interactions of the Apple 4 Domain that Mediate Coagulation Factor XI Homodimerization. J Biol Chem 2001; 276: 6429-38.
    CrossrefPubMedGoogle Scholar
  • 86 Gailani D, Sun MF, Zhao M, Walsh PN. A model for the activation of factor IX by factor XIa on the surface of activated platelets. Blood 1999; 94: 621a (abstr.).
    PubMedGoogle Scholar
  • 87 Tracy PB. Role of platelets and leukocytes in coagulation. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN. eds. Philadelphia: J. B. Lippincott Williams & Wilkins; 2001: 575-96.
    Google Scholar
  • 88 Beeler DL, Marcum JA, Schiffman S, Rosenberg RD. Interaction of factor XIa and antithrombin in the presence and absence of heparin. Blood 1986; 67: 1488-92.
    PubMedGoogle Scholar
  • 89 Berrettini M, Schleef RR, Espana F, Loskutoff DJ, Griffin JH. Interaction of type 1 plasminogen activator inhibitor with the enzymes of the contact activation system. J Biol Chem 1989; 264: 11738-43.
    PubMedGoogle Scholar
  • 90 Damus PS, Hicks M, Rosenberg RD. Anticoagulant action of heparin. Nature 1973; 246: 355-7.
    CrossrefPubMedGoogle Scholar
  • 91 Espana F, Berrettini M, Griffin JH. Purification and characterization of plasma protein C inhibitor. Thromb Res 1989; 55: 369-84.
    CrossrefPubMedGoogle Scholar
  • 92 Forbes CD, Pensky J, Ratnoff OD. Inhibition of activated Hageman factor and activated plasma thromboplastin antecedent by purified serum C1 inactivator. J Lab Clin Med 1970; 76: 809-15.
    PubMedGoogle Scholar
  • 93 Meijers JC, Vlooswijk RA, Bouma BN. Inhibition of human blood coagulation factor XIa by C-1 inhibitor. Biochemistry 1988; 27: 959-63.
    CrossrefPubMedGoogle Scholar
  • 94 Saito H, Goldsmith GH, Moroi M, Aoki N. Inhibitory spectrum of alpha 2-plasmin inhibitor. Proc Natl Acad Sci USA 1979; 76: 2013-7.
    CrossrefPubMedGoogle Scholar
  • 95 Scott CF, Colman RW. Factors influencing the acceleration of human factor XIa inactivation by antithrombin III. Blood 1989; 73: 1873-9.
    PubMedGoogle Scholar
  • 96 Scott CF, Schapira M, Colman RW. Effect of heparin on the inactivation rate of human factor XIa by antithrombin-III. Blood 1982; 60: 940-7.
    PubMedGoogle Scholar
  • 97 Scott CF, Schapira M, James HL, Cohen AB, Colman RW. Inactivation of factor XIa by plasma protease inhibitors: predominant role of alpha 1-protease inhibitor and protective effect of high molecular weight kininogen. J Clin Invest 1982; 69: 844-52.
    CrossrefPubMedGoogle Scholar
  • 98 Soons H, Janssen-Claessen T, Tans G, Hemker HC. Inhibition of factor XIa by antithrombin III. Biochemistry 1987; 26: 4624-9.
    CrossrefPubMedGoogle Scholar
  • 99 Walsh PN, Sinha D, Kueppers F, Seaman FS, Blankstein KB. Regulation of factor XIa activity by platelets and alpha 1-protease inhibitor. J Clin Invest 1987; 80: 1578-86.
    CrossrefPubMedGoogle Scholar
  • 100 Bush AI, Martins RN, Rumble B, Moir R, Fuller S, Milward E, Currie J, Ames D, Weidemann A, Fischer P, Multhaup G, Beyreuther K, Masters CL. The amyloid precursor protein of Alzheimer’s disease is released by human platelets. J Biol Chem 1990; 265: 15977-83.
    PubMedGoogle Scholar
  • 101 Cronlund AL, Walsh PN. A low molecular weight platelet inhibitor of factor XIa: purification, characterization, and possible role in blood coagulation. Biochemistry 1992; 31: 1685-94.
    CrossrefPubMedGoogle Scholar
  • 102 Smith RP, Higuchi DA, Broze Jr GJ. Platelet coagulation factor XIa-inhibitor, a form of Alzheimer amyloid precursor protein. Science 1990; 248: 1126-8.
    CrossrefPubMedGoogle Scholar
  • 103 Soons H, Janssen-Claessen T, Hemker HC, Tans G. The effect of platelets in the activation of human blood coagulation factor IX by factor XIa. Blood 1986; 68: 140-8.
    PubMedGoogle Scholar
  • 104 Van Nostrand WE, Schmaier AH, Farrow JS, Cunningham DD. Protease nexin-II (amyloid beta-protein precursor): a platelet alpha-granule protein. Science 1990; 248: 745-8.
    CrossrefPubMedGoogle Scholar
  • 105 Berliner S, Horowitz I, Martinowitz U, Brenner B, Seligsohn U. Dental surgery in patients with severe factor XI deficiency without plasma replacement. Blood Coagul Fibrinolysis 1992; 3: 465-8.
    CrossrefPubMedGoogle Scholar
  • 106 Gailani D. Advances and dilemmas in factor XI. Current Opin Hematol 1994; 1: 347-53.
    PubMedGoogle Scholar
  • 107 Kitchens CS. Factor XI: a review of its biochemistry and deficiency. Semin Thromb Hemost 1991; 17: 55-72.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 108 Seligsohn U. Factor XI deficiency. Thromb Haemost 1993; 70: 68-71.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 109 von dem Borne PA, Meijers JC, Bouma BN. Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood 1995; 86: 3035-42.
    PubMedGoogle Scholar
  • 110 Bajzar L, Manuel R, Nesheim ME. Purification and characterization of TAFI, a thrombin-activatable fibrinolysis inhibitor. J Biol Chem 1995; 270: 14477-84.
    CrossrefPubMedGoogle Scholar
  • 111 Hendriks D, Scharpe S, Van Sande M, Lommaert MP. Characterization of a carboxypeptidase in human serum distinct from carboxypeptidase. Clin Chem Clin Biochem 1989; 27: 277-85.
    PubMedGoogle Scholar
  • 112 Redlitz A, Tan AK, Eaton DL, Plow EF. Plasma carboxypeptidases as regulators of the plasminogen system. J Clin Invest 1995; 96: 2534-8.
    CrossrefPubMedGoogle Scholar
  • 113 Tan AK, Eaton DL. Activation and characterization of procarboxypeptidase B from human plasma. Biochemistry 1995; 34: 5811-6.
    CrossrefPubMedGoogle Scholar
  • 114 Wang W, Hendriks D, Scharpe S. Carboxypeptidase U a plasma carboxypeptidase with high affinity for plasminogen. J Biol Chem 1994; 269: 15937-44.
    PubMedGoogle Scholar
  • 115 Bouma BN, Meijers JC. Fibrinolysis and the contact system: a role for factor XI in the down-regulation of fibrinolysis. Thromb Haemost 1999; 82: 243-50.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 116 Tuszynski GP, Bevacqua SJ, Schmaier AH, Colman RW, Walsh PN. Factor XI antigen and activity in human platelets. Blood 1982; 59: 1148-56.
    PubMedGoogle Scholar
  • 117 Walsh PN, Mills DC, Pareti FI, Stewart GJ, Macfarlane DE, Johnson MM, Egan JJ. Hereditary giant platelet syndrome. Absence of collagen-induced coagulant activity and deficiency of factor-XI binding to platelets. Br J Haematol 1975; 29: 639-55.
    CrossrefPubMedGoogle Scholar
  • 118 Komiyama Y, Nomura S, Murakami T, Masuda M, Egawa H, Murata K, Okubo S, Kokawa T, Yasunaga K. Purification and characterization of platelet-type factor XI from human platelets. Thromb Haemost 1993; 69: 1238 (abstract).
    PubMedGoogle Scholar
  • 119 Schiffman S, Rapaport SI, Chong MM. Platelets and initiation of intrinsic clotting. Br J Haematol 1973; 24: 633-42.
    CrossrefPubMedGoogle Scholar
  • 120 Schiffman S, Yeh CH. Purification and characterization of platelet factor XI. Thromb Res 1990; 60: 87-97.
    CrossrefPubMedGoogle Scholar
  • 121 Martincic D, Kravtsov V, Gailani D. Factor XI messenger RNA in human platelets. Blood 1999; 94: 3397-404.
    CrossrefPubMedGoogle Scholar
  • 122 Asakai R, Chung DW, Ratnoff OD, Davie EW. Factor XI (plasma thromboplastin antecedent) deficiency in Ashkenazi Jews is a bleeding disorder that can result from three types of point mutations. Proc Natl Acad Sci USA 1989; 86: 7667-71.
    CrossrefPubMedGoogle Scholar
  • 123 Giannelli F, Green PM, Sommer SS, Poon M, Ludwig M, Schwaab R, Reitsma PH, Goossens M, Yoshioka A, Figueiredo MS, Brownlee GG. Haemophilia B: database of point mutations and short additions and deletions – eighth edition. Nucleic Acids Res 1998; 26: 265-8.
    CrossrefPubMedGoogle Scholar
  • 124 Hancock JF, Wieland K, Pugh RE, Martinowitz U, Schulman S, Kakkar VV, Kernoff PB, Cooper DN. A molecular genetic study of factor XI deficiency. Blood 1991; 77: 1942-8.
    PubMedGoogle Scholar
  • 125 Martincic D, Zimmerman SA, Ware RE, Sun MF, Whitlock JA, Gailani D. Identification of mutations and polymorphisms in factor XI genes of an African-American family by dideoxyfingerprinting. Blood 1998; 92: 3309-17.
    PubMedGoogle Scholar
  • 126 Peretz H, Zivelin A, Usher S, Seligsohn U. A 14-bp deletion (codon 554 del AAGgtaacagagtg) at exon 14/intron N junction of the coagulation factor XI gene disrupts splicing and causes severe factor XI deficiency. Hum Mutat 1996; 8: 77-8.
    CrossrefPubMedGoogle Scholar
  • 127 Pugh RE, McVey JH, Tuddenham EG, Hancock JF. Six point mutations that cause factor XI deficiency. Blood 1995; 85: 1509-16.
    PubMedGoogle Scholar
  • 128 Seligsohn U, Weiss E, Kulka T, Eichel R, Zwang E, Pereta H. The frequency of the type II and type III mutations causing factor XI deficiency in the general Jewish population. Thromb Haemost 1993; 69: 1296 (abstract).
    PubMedGoogle Scholar
  • 129 Wistinghausen B, Reischer A, Oddoux C, Ostrer H, Nardi M, Karpatkin M. Severe factor XI deficiency in an Arab family associated with a novel mutation in exon 11. Br J Haematol 1997; 99: 575-7.
    CrossrefPubMedGoogle Scholar
  • 130 Shirk RA, Konkle BA, Walsh PN. Nonsense mutation in exon V of the factor XI gene does not abolish platelet factor XI expression. Br J Haematol 2000; 111: 91-5.
    CrossrefPubMedGoogle Scholar