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Science 23 August 1991:
Vol. 253. no. 5022, pp. 909 - 912
DOI: 10.1126/science.1652157
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Articles

Science, Vol 253, Issue 5022, 909-912
Copyright © 1991 by American Association for the Advancement of Science

articles

Factor XI activation in a revised model of blood coagulation

D Gailani and GJ Broze Jr

Department of Medicine, Jewish Hospital, Washington University Medical Center, St. Louis, MO 63110.

Coagulation factor XI is activated in vitro by factor XIIa in the presence of high molecular weight kininogen (HMWK) and a negatively charged surface. Factor XII deficiency is not associated with bleeding, which suggests that another mechanism for factor XI activation exists in vivo. A revised model of coagulation is proposed in which factor XI is activated by thrombin. In the absence of cofactors, thrombin is more effective (kcat/Km = 1.6 x 10(5)) than factor XIIa (1.7 x 10(4)) in activating factor XI. Dextran sulfate enhances activation of factor XI by thrombin 2000-fold; part of this effect is due to autoactivation of factor XI by activated factor XI.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Factor XI Homodimer Structure Is Essential for Normal Proteolytic Activation by Factor XIIa, Thrombin, and Factor XIa.
W. Wu, D. Sinha, S. Shikov, C. K. Yip, T. Walz, P. C. Billings, J. D. Lear, and P. N. Walsh (2008)
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Detailed Mechanisms of the Inactivation of Factor VIIIa by Activated Protein C in the Presence of Its Cofactors, Protein S and Factor V.
A. J. Gale, T. J. Cramer, D. Rozenshteyn, and J. R. Cruz (2008)
J. Biol. Chem. 283, 16355-16362
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Characterization of Novel Forms of Coagulation Factor XIa: INDEPENDENCE OF FACTOR XIa SUBUNITS IN FACTOR IX ACTIVATION.
S. B. Smith, I. M. Verhamme, M.-f. Sun, P. E. Bock, and D. Gailani (2008)
J. Biol. Chem. 283, 6696-6705
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Intrinsic Pathway of Coagulation and Arterial Thrombosis.
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Arterioscler. Thromb. Vasc. Biol. 27, 2507-2513
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Feedback activation of factor XI by thrombin does not occur in plasma.
D. L. Pedicord, D. Seiffert, and Y. Blat (2007)
PNAS 104, 12855-12860
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Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation.
C. Kannemeier, A. Shibamiya, F. Nakazawa, H. Trusheim, C. Ruppert, P. Markart, Y. Song, E. Tzima, E. Kennerknecht, M. Niepmann, et al. (2007)
PNAS 104, 6388-6393
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Thrombin During Cardiopulmonary Bypass.
L. H. Edmunds Jr and R. W. Colman (2006)
Ann. Thorac. Surg. 82, 2315-2322
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Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis.
C. Kleinschnitz, G. Stoll, M. Bendszus, K. Schuh, H.-U. Pauer, P. Burfeind, C. Renne, D. Gailani, B. Nieswandt, and T. Renne (2006)
J. Exp. Med. 203, 513-518
   Abstract »    Full Text »    PDF »
Are hemostasis and thrombosis two sides of the same coin?.
R. W. Colman (2006)
J. Exp. Med. 203, 493-495
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Spatial Propagation and Localization of Blood Coagulation Are Regulated by Intrinsic and Protein C Pathways, Respectively.
M. A. Panteleev, M. V. Ovanesov, D. A. Kireev, A. M. Shibeko, E. I. Sinauridze, N. M. Ananyeva, A. A. Butylin, E. L. Saenko, and F. I. Ataullakhanov (2006)
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Positive Feedbacks of Coagulation: Their Role in Threshold Regulation.
J. Jesty and E. Beltrami (2005)
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The Prothrombotic Paradox of Hypertension: Role of the Renin-Angiotensin and Kallikrein-Kinin Systems.
A. W.J.H. Dielis, M. Smid, H. M.H. Spronk, K. Hamulyak, A. A. Kroon, H. ten Cate, and P. W. de Leeuw (2005)
Hypertension 46, 1236-1242
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Tissue-Specific Hemostasis in Mice.
N. Mackman (2005)
Arterioscler. Thromb. Vasc. Biol. 25, 2273-2281
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Directing thrombin.
D. A. Lane, H. Philippou, and J. A. Huntington (2005)
Blood 106, 2605-2612
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Defective thrombus formation in mice lacking coagulation factor XII.
T. Renne, M. Pozgajova, S. Gruner, K. Schuh, H.-U. Pauer, P. Burfeind, D. Gailani, and B. Nieswandt (2005)
J. Exp. Med. 202, 271-281
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Crystal Structures of the FXIa Catalytic Domain in Complex with Ecotin Mutants Reveal Substrate-like Interactions.
L. Jin, P. Pandey, R. E. Babine, J. C. Gorga, K. J. Seidl, E. Gelfand, D. T. Weaver, S. S. Abdel-Meguid, and J. E. Strickler (2005)
J. Biol. Chem. 280, 4704-4712
   Abstract »    Full Text »    PDF »
Factor XI Interacts with the Leucine-rich Repeats of Glycoprotein Ib{alpha} on the Activated Platelet.
F. A. Baglia, C. N. Shrimpton, J. Emsley, K. Kitagawa, Z. M. Ruggeri, J. A. Lopez, and P. N. Walsh (2004)
J. Biol. Chem. 279, 49323-49329
   Abstract »    Full Text »    PDF »
Identification of a Binding Site for Glycoprotein Ib{alpha} in the Apple 3 Domain of Factor XI.
F. A. Baglia, D. Gailani, J. A. Lopez, and P. N. Walsh (2004)
J. Biol. Chem. 279, 45470-45476
   Abstract »    Full Text »    PDF »
Structural Role of Gly193 in Serine Proteases: INVESTIGATIONS OF A G555E (GLY193 IN CHYMOTRYPSIN) MUTANT OF BLOOD COAGULATION FACTOR XI.
A. E. Schmidt, T. Ogawa, D. Gailani, and S. P. Bajaj (2004)
J. Biol. Chem. 279, 29485-29492
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Factor XI-Dependent Reciprocal Thrombin Generation Consolidates Blood Coagulation when Tissue Factor Is Not Available.
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Arterioscler. Thromb. Vasc. Biol. 24, 1138-1142
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Review: The plasma kallikrein/kinin and renin angiotensin systems in blood pressure regulation in sepsis.
Z. Shariat-Madar and A. H. Schmaier (2004)
Innate Immunity 10, 3-13
   Abstract »    PDF »
A Brief Historical Review of the Waterfall/Cascade of Blood Coagulation.
E. W. Davie (2003)
J. Biol. Chem. 278, 50819-50832
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Thrombin Activation of Factor XI on Activated Platelets Requires the Interaction of Factor XI and Platelet Glycoprotein Ib{alpha} with Thrombin Anion-binding Exosites I and II, Respectively.
T. H. Yun, F. A. Baglia, T. Myles, D. Navaneetham, J. A. Lopez, P. N. Walsh, and L. L. K. Leung (2003)
J. Biol. Chem. 278, 48112-48119
   Abstract »    Full Text »    PDF »
Thrombin Formation.
K. G. Mann (2003)
Chest 124, 4S-10S
   Abstract »    Full Text »    PDF »
Prevalence, causes, and characterization of factor XI inhibitors in patients with inherited factor XI deficiency.
O. Salomon, A. Zivelin, T. Livnat, R. Dardik, R. Loewenthal, O. Avishai, D. M. Steinberg, M. H. Rosove, N. O'Connell, C. A. Lee, et al. (2003)
Blood 101, 4783-4788
   Abstract »    Full Text »    PDF »
The Glycoprotein Ib-IX-V Complex Mediates Localization of Factor XI to Lipid Rafts on the Platelet Membrane.
F. A. Baglia, C. N. Shrimpton, J. A. Lopez, and P. N. Walsh (2003)
J. Biol. Chem. 278, 21744-21750
   Abstract »    Full Text »    PDF »
Factor XI, but Not Prekallikrein, Blocks High Molecular Weight Kininogen Binding to Human Umbilical Vein Endothelial Cells.
T. R. Baird and P. N. Walsh (2003)
J. Biol. Chem. 278, 20618-20623
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The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome.
W. C. Aird (2003)
Blood 101, 3765-3777
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Mutations in Autolytic Loop-2 and at Asp554 of Human Prothrombin That Enhance Protein C Activation by Meizothrombin.
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J. Biol. Chem. 278, 15015-15022
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The Fourth Epidermal Growth Factor-like Domain of Thrombomodulin Interacts with the Basic Exosite of Protein C.
L. Yang and A. R. Rezaie (2003)
J. Biol. Chem. 278, 10484-10490
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Neutrophil Cathepsin G Promotes Prothrombinase and Fibrin Formation under Flow Conditions by Activating Fibrinogen-adherent Platelets.
M. S. Goel and Scott. L. Diamond (2003)
J. Biol. Chem. 278, 9458-9463
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Femoral Pseudoaneurysms: Management with Percutaneous Thrombin Injections--Success Rates and Effects on Systemic Coagulation.
K. Kruger, M. Zahringer, F.-D. Sohngen, A. Gossmann, O. Schulte, C. Feldmann, D. Strohe, and K. Lackner (2003)
Radiology 226, 452-458
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Unusual Proteolytic Activation of Pro-hepatocyte Growth Factor by Plasma Kallikrein and Coagulation Factor XIa.
M. Peek, P. Moran, N. Mendoza, D. Wickramasinghe, and D. Kirchhofer (2002)
J. Biol. Chem. 277, 47804-47809
   Abstract »    Full Text »    PDF »
Congenital Factor XI Deficiency in a Domestic Shorthair Cat.
M. T. Troxel, M. B. Brooks, and M. L. Esterline (2002)
J. Am. Anim. Hosp. Assoc. 38, 549-553
   Abstract »    Full Text »    PDF »
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.
T. R. Baird and P. N. Walsh (2002)
J. Biol. Chem. 277, 38462-38467
   Abstract »    Full Text »    PDF »
Activated Platelets but Not Endothelial Cells Participate in the Initiation of the Consolidation Phase of Blood Coagulation.
T. R. Baird and P. N. Walsh (2002)
J. Biol. Chem. 277, 28498-28503
   Abstract »    Full Text »    PDF »
Coagulation, fibrinolysis, and cell activation in patients and shed mediastinal blood during coronary artery bypass grafting with a new heparin-coated surface.
M. Johnell, G. Elgue, R. Larsson, A. Larsson, S. Thelin, and A. Siegbahn (2002)
J. Thorac. Cardiovasc. Surg. 124, 321-332
   Abstract »    Full Text »    PDF »
Thrombin functions during tissue factor-induced blood coagulation.
K. E. Brummel, S. G. Paradis, S. Butenas, and K. G. Mann (2002)
Blood 100, 148-152
   Abstract »    Full Text »    PDF »
Factor XI deficiency in French Basques is caused predominantly by an ancestral Cys38Arg mutation in the factor XI gene.
A. Zivelin, F. Bauduer, L. Ducout, H. Peretz, N. Rosenberg, R. Yatuv, and U. Seligsohn (2002)
Blood 99, 2448-2454
   Abstract »    Full Text »    PDF »
Characterization of the H-kininogen-binding Site on Factor XI. A COMPARISON OF FACTOR XI AND PLASMA PREKALLIKREIN.
T. Renne, D. Gailani, J. C. M. Meijers, and W. Muller-Esterl (2002)
J. Biol. Chem. 277, 4892-4899
   Abstract »    Full Text »    PDF »
Hemostatic Abnormalities in Cardiopulmonary Bypass: Pathophysiologic and Transfusion Considerations.
K. Kottke-Marchant and S. Sapatnekar (2001)
Seminars in Cardiothoracic and Vascular Anesthesia 5, 187-206
   Abstract »    PDF »
Defective binding of factor XI-N248 to activated human platelets.
M.-F. Sun, F. A. Baglia, D. Ho, D. Martincic, R. E. Ware, P. N. Walsh, and D. Gailani (2001)
Blood 98, 125-129
   Abstract »    Full Text »    PDF »
arboxypeptidase U at the Interface Between Coagulation and Fibrinolysis.
K. Schatteman, F. Goossens, J. Leurs, R. Verkerk, S. Scharpe, J. J. Michiels, and D. Hendriks (2001)
Clinical and Applied Thrombosis/Hemostasis 7, 93-101
   Abstract »    PDF »
Endothelial cell protein C receptor plays an important role in protein C activation in vivo.
F. B. Taylor Jr, G. T. Peer, M. S. Lockhart, G. Ferrell, and C. T. Esmon (2001)
Blood 97, 1685-1688
   Abstract »    Full Text »    PDF »
Activation of Clotting Factors XI and IX in Patients With Acute Myocardial Infarction.
M. C. Minnema, R. J. G. Peters, R. de Winter, Y. P. T. Lubbers, S. Barzegar, K. A. Bauer, R. D. Rosenberg, C. E. Hack, and H. t. Cate (2000)
Arterioscler. Thromb. Vasc. Biol. 20, 2489-2493
   Abstract »    Full Text »    PDF »
High Levels of Coagulation Factor XI as a Risk Factor for Venous Thrombosis.
J. C.M. Meijers, W. L.H. Tekelenburg, B. N. Bouma, R. M. Bertina, and F. R. Rosendaal (2000)
N. Engl. J. Med. 342, 696-701
   Abstract »    Full Text »    PDF »
C1-Esterase Inhibitor: An Anti-Inflammatory Agent and Its Potential Use in the Treatment of Diseases Other Than Hereditary Angioedema.
C. Caliezi, W. A. Wuillemin, S. Zeerleder, M. Redondo, B. Eisele, and C. E. Hack (2000)
Pharmacol. Rev. 52, 91-112
   Abstract »    Full Text »    PDF »
Identification of Amino Acids in the Factor XI Apple 3 Domain Required for Activation of Factor IX.
M.-F. Sun, M. Zhao, and D. Gailani (1999)
J. Biol. Chem. 274, 36373-36378
   Abstract »    Full Text »    PDF »
Activation of the Contact System of Coagulation Does Not Contribute to the Hemostatic Imbalance in Hypertriglyceridemia.
M. C. Minnema, M. E. Wittekoek, N. Schoonenboom, J. J. P. Kastelein, C. E. Hack, and H. t. Cate (1999)
Arterioscler. Thromb. Vasc. Biol. 19, 2548-2553
   Abstract »    Full Text »    PDF »
Commentary.
A. M. Schmidt, E. A. Rose, and D. M. Stern (1999)
J. Thorac. Cardiovasc. Surg. 118, 429-431
   Full Text »    PDF »
Thrombin Activates Factor XI on Activated Platelets in the Absence of Factor XII.
J. A. Oliver, D. M. Monroe, H. R. Roberts, and M. Hoffman (1999)
Arterioscler. Thromb. Vasc. Biol. 19, 170-177
   Abstract »    Full Text »    PDF »
Characterization of a Heparin Binding Site on the Heavy Chain of Factor XI.
M. Zhao, T. Abdel-Razek, M.-F. Sun, and D. Gailani (1998)
J. Biol. Chem. 273, 31153-31159
   Abstract »    Full Text »    PDF »
Activation of Clotting Factor XI Without Detectable Contact Activation in Experimental Human Endotoxemia.
M.C. Minnema, D. Pajkrt, W.A. Wuillemin, D. Roem, W.K. Bleeker, M. Levi, S.J.H. van Deventer, C.E. Hack, and H. ten Cate (1998)
Blood 92, 3294-3301
   Abstract »    Full Text »    PDF »
Identification of Mutations and Polymorphisms in the Factor XI Genes of an African American Family by Dideoxyfingerprinting.
D. Martincic, S. A. Zimmerman, R. E. Ware, M.-F. Sun, J. A. Whitlock, and D. Gailani (1998)
Blood 92, 3309-3317
   Abstract »    Full Text »    PDF »
A Binding Site for Heparin in the Apple 3 Domain of Factor XI.
D. H. Ho, K. Badellino, F. A. Baglia, and P. N. Walsh (1998)
J. Biol. Chem. 273, 16382-16390
   Abstract »    Full Text »    PDF »
Rapid Activation of Protein C by Factor Xa and Thrombin in the Presence of Polyanionic Compounds.
A. R. Rezaie (1998)
Blood 91, 4572-4580
   Abstract »    Full Text »    PDF »
Blood Coagulation in Hemophilia A and Hemophilia C.
K. M. Cawthern, C. van `t Veer, J. B. Lock, M. E. DiLorenzo, R. F. Branda, and K. G. Mann (1998)
Blood 91, 4581-4592
   Abstract »    Full Text »    PDF »
Molecular Cloning of Platelet Factor XI, an Alternative Splicing Product of the Plasma Factor XI Gene.
T.-C. Hsu, S. K. Shore, T. Seshsmma, O. Bagasra, and P. N. Walsh (1998)
J. Biol. Chem. 273, 13787-13793
   Abstract »    Full Text »    PDF »
Protein C Inhibitor Acts as a Procoagulant by Inhibiting the Thrombomodulin-Induced Activation of Protein C in Human Plasma.
M. G.L.M. Elisen, P. A.Kr. von dem Borne, B. N. Bouma, and J. C.M. Meijers (1998)
Blood 91, 1542-1547
   Abstract »    Full Text »    PDF »
Antithrombotic Efficacy of Inactivated Active Site Recombinant Factor VIIa Is Shear Dependent in Human Blood.
U. Orvim, R. M. Barstad, L. Orning, L. B. Petersen, M. Ezban, U. Hedner, and K. S. Sakariassen (1997)
Arterioscler. Thromb. Vasc. Biol. 17, 3049-3056
   Abstract »    Full Text »
Evaluation of the Initiation Phase of Blood Coagulation Using Ultrasensitive Assays for Serine Proteases.
S. Butenas, C. van `t Veer, and K. G. Mann (1997)
J. Biol. Chem. 272, 21527-21533
   Abstract »    Full Text »    PDF »
A Comparison of Murine and Human Factor XI.
D. Gailani, M.-F. Sun, and Y. Sun (1997)
Blood 90, 1055-1064
   Abstract »    Full Text »    PDF »
Functional Requirements for Inhibition of Thrombin by Antithrombin III in the Presence and Absence of Heparin.
M. Tsiang, A. K. Jain, and C. S. Gibbs (1997)
J. Biol. Chem. 272, 12024-12029
   Abstract »    Full Text »    PDF »
Regulation of Tissue Factor Initiated Thrombin Generation by the Stoichiometric Inhibitors Tissue Factor Pathway Inhibitor, Antithrombin-III, and Heparin Cofactor-II.
C. van `t Veer and K. G. Mann (1997)
J. Biol. Chem. 272, 4367-4377
   Abstract »    Full Text »    PDF »
Identification of a Factor IX Binding Site on the Third Apple Domain of Activated Factor XI.
Y. Sun and D. Gailani (1996)
J. Biol. Chem. 271, 29023-29028
   Abstract »    Full Text »    PDF »
Sustained Inhibition of Whole-Blood Clot Procoagulant Activity by Inhibition of Thrombus-Associated Factor Xa.
C. R. McKenzie, D. R. Abendschein, and P. R. Eisenberg (1996)
Arterioscler. Thromb. Vasc. Biol. 16, 1285-1291
   Abstract »    Full Text »
Enhanced Thrombin Sensitivity of a Factor VIII-Heparin Cofactor II Hybrid.
J. Voorberg, G. van Stempvoort, J. M.K. Bos, K. Mertens, J. A. van Mourik, and M.-J. S.H. Donath (1996)
J. Biol. Chem. 271, 20985-20988
   Abstract »    Full Text »    PDF »
Tissue Factor Mediates Prolonged Procoagulant Activity on the Luminal Surface of Balloon-Injured Aortas in Rabbits.
C. M. Speidel, P. R. Eisenberg, W. Ruf, T. S. Edgington, and D. R. Abendschein (1995)
Circulation 92, 3323-3330
   Abstract »    Full Text »
Von Willebrand Factor Antigen and Factor XI Activity Levels As Predictors of Bleeding Tendency in Israeli Patients with Von Willebrand's Disease.
B. Brenner, T. Stemberg, A. Laor, S. Tavori, I. Tatarsky, and N. Lanir (1995)
Clinical and Applied Thrombosis/Hemostasis 1, 260-264
   Abstract »    PDF »
Evaluation of Factor XIa–{alpha}1-Antitrypsin in Plasma, a Contact Phase–Activated Coagulation Factor–Inhibitor Complex, in Patients With Coronary Artery Disease.
T. Murakami, Y. Komiyama, M. Masuda, M. Karakawa, T. Iwasaka, and H. Takahashi (1995)
Arterioscler. Thromb. Vasc. Biol. 15, 1107-1113
   Abstract »    Full Text »
Functional Mapping of the Surface Residues of Human Thrombin.
M. Tsiang, A. K. Jain, K. E. Dunn, M. E. Rojas, L. L. K. Leung, and C. S. Gibbs (1995)
J. Biol. Chem. 270, 16854-16863
   Abstract »    Full Text »    PDF »
Regulation of the Tertiary Structure and Function of Coagulation Factor IX by Magnesium(II) Ions.
F. Sekiya, T. Yamashita, H. Atoda, Y. Komiyama, and T. Morita (1995)
J. Biol. Chem. 270, 14325-14331
   Abstract »    Full Text »    PDF »
Expression and Folding of Recombinant Bovine Prethrombin-2 and Its Activation to Thrombin.
E. E. DiBella, M. C. Maurer, and H. A. Scheraga (1995)
J. Biol. Chem. 270, 163-169
   Abstract »    Full Text »    PDF »
Factor XII deficiency and cardiopulmonary bypass.
M. Wallock, C. Arentzen, and J. Perkins (1995)
Perfusion 10, 13-16
   Abstract »    PDF »
Thrombin-mediated Feedback Activation of Factor XI on the Activated Platelet Surface Is Preferred over Contact Activation by Factor XIIa or Factor XIa.
F. A. Baglia and P. N. Walsh (2000)
J. Biol. Chem. 275, 20514-20519
   Abstract »    Full Text »    PDF »
The Role of High Molecular Weight Kininogen and Prothrombin as Cofactors in the Binding of Factor XI A3 Domain to the Platelet Surface.
D. H. Ho, K. Badellino, F. A. Baglia, M.-F. Sun, M.-M. Zhao, D. Gailani, and P. N. Walsh (2000)
J. Biol. Chem. 275, 25139-25145
   Abstract »    Full Text »    PDF »
A Binding Site for the Kringle II Domain of Prothrombin in the Apple 1 Domain of Factor XI.
F. A. Baglia, K. O. Badellino, D. H. Ho, V. R. Dasari, and P. N. Walsh (2000)
J. Biol. Chem. 275, 31954-31962
   Abstract »    Full Text »    PDF »
Factor XI Binding to the Platelet Glycoprotein Ib-IX-V Complex Promotes Factor XI Activation by Thrombin.
F. A. Baglia, K. O. Badellino, C. Q. Li, J. A. Lopez, and P. N. Walsh (2002)
J. Biol. Chem. 277, 1662-1668
   Abstract »    Full Text »    PDF »


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Science. ISSN 0036-8075 (print), 1095-9203 (online)