PDF herunterladen
Semin Thromb Hemost 2024; 50(07): 962-969
DOI: 10.1055/s-0043-1764469
Review Article

Substrates, Cofactors, and Cellular Targets of Coagulation Factor XIa

André L. Lira
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
,
Tia C.L. Kohs
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
,
Samantha A. Moellmer
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
,
Joseph J. Shatzel
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
2   Divison of Hematology and Medical Oncology, Department of Medicine, Oregon Health & Science University, Portland, Oregon
,
Owen J.T. McCarty
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
2   Divison of Hematology and Medical Oncology, Department of Medicine, Oregon Health & Science University, Portland, Oregon
,
Cristina Puy
1   Department of Biomedical Engineering, School of Medicine, Oregon Health & Science University, Portland, Oregon
2   Divison of Hematology and Medical Oncology, Department of Medicine, Oregon Health & Science University, Portland, Oregon
› Institutsangaben Funding This work was supported by grants from the National Institute of Health (R01HL151367 to J.J.S. and R01HL101972, R01GM116184, and R01HL151367 to O.J.T.M.).
› Weitere Informationen
    Lizenzen und Reprints

Abstract

Coagulation factor XI (FXI) has increasingly been shown to play an integral role in several physiologic and pathological processes. FXI is among several zymogens within the blood coagulation cascade that are activated by proteolytic cleavage, with FXI converting to the active serine protease form (FXIa). The evolutionary origins of FXI trace back to duplication of the gene that transcribes plasma prekallikrein, a key factor in the plasma kallikrein–kinin system, before further genetic divergence led to FXI playing a unique role in blood coagulation. While FXIa is canonically known for activating the intrinsic pathway of coagulation by catalyzing the conversion of FIX into FIXa, it is promiscuous in nature and has been shown to contribute to thrombin generation independent of FIX. In addition to its role in the intrinsic pathway of coagulation, FXI also interacts with platelets, endothelial cells, and mediates the inflammatory response through activation of FXII and cleavage of high-molecular-weight kininogen to generate bradykinin. In this manuscript, we critically review the current body of knowledge surrounding how FXI navigates the interplay of hemostasis, inflammatory processes, and the immune response and highlight future avenues for research. As FXI continues to be clinically explored as a druggable therapeutic target, understanding how this coagulation factor fits into physiological and disease mechanisms becomes increasingly important.

Keywords

factor XIa - inflammation - coagulation - barrier function - platelets

Note

The figure included in this manuscript was created using BioRender.com.




Publikationsverlauf

Artikel online veröffentlicht:
20. März 2023

© 2023. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Di Cera E. Serine proteases. IUBMB Life 2009; 61 (05) 510-515
    CrossrefPubMedSuche in Google Scholar
  • 2 López-Otín C, Bond JS. Proteases: multifunctional enzymes in life and disease. J Biol Chem 2008; 283 (45) 30433-30437
    CrossrefPubMedSuche in Google Scholar
  • 3 Khan AR, James MN. Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Protein Sci 1998; 7 (04) 815-836
    CrossrefPubMedSuche in Google Scholar
  • 4 Posma JJ, Posthuma JJ, Spronk HM. Coagulation and non-coagulation effects of thrombin. J Thromb Haemost 2016; 14 (10) 1908-1916
    CrossrefPubMedSuche in Google Scholar
  • 5 Di Cera E. Thrombin. Mol Aspects Med 2008; 29 (04) 203-254
    CrossrefPubMedSuche in Google Scholar
  • 6 Lakshmanan HHS, Estonilo A, Reitsma SE. et al. Revised model of the tissue factor pathway of thrombin generation: role of the feedback activation of FXI. J Thromb Haemost 2022; 20 (06) 1350-1363
    CrossrefPubMedSuche in Google Scholar
  • 7 Gailani D, Broze Jr GJ. Factor XI activation in a revised model of blood coagulation. Science 1991; 253 (5022): 909-912
    CrossrefPubMedSuche in Google Scholar
  • 8 Kravtsov DV, Matafonov A, Tucker EI. et al. Factor XI contributes to thrombin generation in the absence of factor XII. Blood 2009; 114 (02) 452-458
    CrossrefPubMedSuche in Google Scholar
  • 9 Gailani D, Geng Y, Verhamme I. et al. The mechanism underlying activation of factor IX by factor XIa. Thromb Res 2014; 133 (0 1, Suppl 1): S48-S51
    CrossrefPubMedSuche in Google Scholar
  • 10 Puy C, Rigg RA, McCarty OJT. The hemostatic role of factor XI. Thromb Res 2016; 141 (Suppl 2, Suppl 2): S8-S11
    CrossrefPubMedSuche in Google Scholar
  • 11 Doolittle RF. Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harb Symp Quant Biol 2009; 74: 35-40
    CrossrefPubMedSuche in Google Scholar
  • 12 Ponczek MB, Gailani D, Doolittle RF. Evolution of the contact phase of vertebrate blood coagulation. J Thromb Haemost 2008; 6 (11) 1876-1883
    CrossrefPubMedSuche in Google Scholar
  • 13 Jiang Y, Doolittle RF. The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci U S A 2003; 100 (13) 7527-7532
    CrossrefPubMedSuche in Google Scholar
  • 14 Ponczek MB, Shamanaev A, LaPlace A. et al. The evolution of factor XI and the kallikrein-kinin system. Blood Adv 2020; 4 (24) 6135-6147
    CrossrefPubMedSuche in Google Scholar
  • 15 Papagrigoriou E, McEwan PA, Walsh PN, Emsley J. Crystal structure of the factor XI zymogen reveals a pathway for transactivation. Nat Struct Mol Biol 2006; 13 (06) 557-558
    CrossrefPubMedSuche in Google Scholar
  • 16 Emsley J, McEwan PA, Gailani D. Structure and function of factor XI. Blood 2010; 115 (13) 2569-2577
    CrossrefPubMedSuche in Google Scholar
  • 17 Mohammed BM, Matafonov A, Ivanov I. et al. An update on factor XI structure and function. Thromb Res 2018; 161: 94-105
    CrossrefPubMedSuche in Google Scholar
  • 18 Gailani D, Emsley J. Toward a better understanding of factor XI activation. J Thromb Haemost 2019; 17 (12) 2016-2018
    CrossrefPubMedSuche in Google Scholar
  • 19 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 (09) 2417-2424
    CrossrefPubMedSuche in Google Scholar
  • 20 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 (08) 2056-2060
    CrossrefPubMedSuche in Google Scholar
  • 21 Baglia FA, Walsh PN. A binding site for thrombin in the apple 1 domain of factor XI. J Biol Chem 1996; 271 (07) 3652-3658
    CrossrefPubMedSuche in Google Scholar
  • 22 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 (06) 3838-3844
    CrossrefPubMedSuche in Google Scholar
  • 23 Cheng Q, Tucker EI, Pine MS. et al. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo . Blood 2010; 116 (19) 3981-3989
    CrossrefPubMedSuche in Google Scholar
  • 24 Zhao M, Abdel-Razek T, Sun MF, Gailani D. Characterization of a heparin binding site on the heavy chain of factor XI. J Biol Chem 1998; 273 (47) 31153-31159
    CrossrefPubMedSuche in Google Scholar
  • 25 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 (26) 16382-16390
    CrossrefPubMedSuche in Google Scholar
  • 26 Yang L, Sun MF, Gailani D, Rezaie AR. Characterization of a heparin-binding site on the catalytic domain of factor XIa: mechanism of heparin acceleration of factor XIa inhibition by the serpins antithrombin and C1-inhibitor. Biochemistry 2009; 48 (07) 1517-1524
    CrossrefPubMedSuche in Google Scholar
  • 27 Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011; 118 (26) 6963-6970
    CrossrefPubMedSuche in Google Scholar
  • 28 Geng Y, Verhamme IM, Smith SA. et al. Factor XI anion-binding sites are required for productive interactions with polyphosphate. J Thromb Haemost 2013; 11 (11) 2020-2028
    CrossrefPubMedSuche in Google Scholar
  • 29 Ivanov I, Shakhawat R, Sun MF. et al. Nucleic acids as cofactors for factor XI and prekallikrein activation: different roles for high-molecular-weight kininogen. Thromb Haemost 2017; 117 (04) 671-681
    Thieme ConnectPubMedSuche in Google Scholar
  • 30 Geng Y, Verhamme IM, Smith SB. et al. The dimeric structure of factor XI and zymogen activation. Blood 2013; 121 (19) 3962-3969
    CrossrefPubMedSuche in Google Scholar
  • 31 Choi SH, Smith SA, Morrissey JH. Polyphosphate accelerates factor V activation by factor XIa. Thromb Haemost 2015; 113 (03) 599-604
    Thieme ConnectPubMedSuche in Google Scholar
  • 32 Puy C, Tucker EI, Ivanov IS. et al. Platelet-derived short-chain polyphosphates enhance the inactivation of tissue factor pathway inhibitor by activated coagulation factor XI. PLoS One 2016; 11 (10) e0165172
    CrossrefPubMedSuche in Google Scholar
  • 33 Renné T, Sugiyama A, Gailani D, Jahnen-Dechent W, Walter U, Müller-Esterl W. Fine mapping of the H-kininogen binding site in plasma prekallikrein apple domain 2. Int Immunopharmacol 2002; 2 (13–14): 1867-1873
    CrossrefPubMedSuche in Google Scholar
  • 34 Renné T, Gailani D, Meijers JC, Müller-Esterl W. Characterization of the H-kininogen-binding site on factor XI: a comparison of factor XI and plasma prekallikrein. J Biol Chem 2002; 277 (07) 4892-4899
    CrossrefPubMedSuche in Google Scholar
  • 35 Bar Barroeta A, Marquart JA, Bakhtiari K, Meijer AB, Urbanus RT, Meijers JCM. Nanobodies against factor XI apple 3 domain inhibit binding of factor IX and reveal a novel binding site for high molecular weight kininogen. J Thromb Haemost 2022; 20 (11) 2538-2549
    CrossrefPubMedSuche in Google Scholar
  • 36 Moellmer SA, Puy C, McCarty OJT. HK is the apple of FXI's eye. J Thromb Haemost 2022; 20 (11) 2485-2487
    CrossrefPubMedSuche in Google Scholar
  • 37 Thompson RE, Mandle Jr R, Kaplan AP. Association of factor XI and high molecular weight kininogen in human plasma. J Clin Invest 1977; 60 (06) 1376-1380
    CrossrefPubMedSuche in Google Scholar
  • 38 Thompson RE, Mandle Jr R, Kaplan AP. Studies of binding of prekallikrein and Factor XI to high molecular weight kininogen and its light chain. Proc Natl Acad Sci U S A 1979; 76 (10) 4862-4866
    CrossrefPubMedSuche in Google Scholar
  • 39 Sinha D, Walsh PN. Binding of coagulation factor XIa to receptor on human platelets. Methods Enzymol 1992; 215: 361-369
    CrossrefPubMedSuche in Google Scholar
  • 40 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 (13) 3768-3775
    CrossrefPubMedSuche in Google Scholar
  • 41 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 (02) 316-323
    CrossrefPubMedSuche in Google Scholar
  • 42 Baglia FA, Gailani D, López JA, Walsh PN. Identification of a binding site for glycoprotein Ibalpha in the Apple 3 domain of factor XI. J Biol Chem 2004; 279 (44) 45470-45476
    CrossrefPubMedSuche in Google Scholar
  • 43 Morla S, Deguchi H, Zilberman-Rudenko J. et al. Skeletal muscle myosin promotes coagulation by binding factor XI via its A3 domain and enhancing thrombin-induced factor XI activation. J Biol Chem 2022; 298 (02) 101567
    CrossrefPubMedSuche in Google Scholar
  • 44 Matafonov A, Cheng Q, Geng Y. et al. Evidence for factor IX-independent roles for factor XIa in blood coagulation. J Thromb Haemost 2013; 11 (12) 2118-2127
    CrossrefPubMedSuche in Google Scholar
  • 45 Puy C, Tucker EI, Wong ZC. et al. Factor XII promotes blood coagulation independent of factor XI in the presence of long-chain polyphosphates. J Thromb Haemost 2013; 11 (07) 1341-1352
    CrossrefPubMedSuche in Google Scholar
  • 46 Whelihan MF, Orfeo T, Gissel MT, Mann KG. Coagulation procofactor activation by factor XIa. J Thromb Haemost 2010; 8 (07) 1532-1539
    CrossrefPubMedSuche in Google Scholar
  • 47 Puy C, Tucker EI, Matafonov A. et al. Activated factor XI increases the procoagulant activity of the extrinsic pathway by inactivating tissue factor pathway inhibitor. Blood 2015; 125 (09) 1488-1496
    CrossrefPubMedSuche in Google Scholar
  • 48 Muia J, Zhu J, Gupta G. et al. Allosteric activation of ADAMTS13 by von Willebrand factor. Proc Natl Acad Sci U S A 2014; 111 (52) 18584-18589
    CrossrefPubMedSuche in Google Scholar
  • 49 Zander CB, Cao W, Zheng XL. ADAMTS13 and von Willebrand factor interactions. Curr Opin Hematol 2015; 22 (05) 452-459
    CrossrefPubMedSuche in Google Scholar
  • 50 Garland KS, Reitsma SE, Shirai T. et al. Removal of the c-terminal domains of ADAMTS13 by activated coagulation factor XI induces platelet adhesion on endothelial cells under flow conditions. Front Med (Lausanne) 2017; 4: 232
    CrossrefPubMedSuche in Google Scholar
  • 51 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 (01) 171-174
    CrossrefPubMedSuche in Google Scholar
  • 52 Tillman BF, Gruber A, McCarty OJT, Gailani D. Plasma contact factors as therapeutic targets. Blood Rev 2018; 32 (06) 433-448
    CrossrefPubMedSuche in Google Scholar
  • 53 Seligsohn U. Factor XI deficiency in humans. J Thromb Haemost 2009; 7 (Suppl (Suppl. 01) 84-87
    CrossrefPubMedSuche in Google Scholar
  • 54 Gomez K, Bolton-Maggs P. Factor XI deficiency. Haemophilia 2008; 14 (06) 1183-1189
    CrossrefPubMedSuche in Google Scholar
  • 55 Pike GN, Cumming AM, Hay CR, Bolton-Maggs PH, Burthem J. Sample conditions determine the ability of thrombin generation parameters to identify bleeding phenotype in FXI deficiency. Blood 2015; 126 (03) 397-405
    CrossrefPubMedSuche in Google Scholar
  • 56 Gidley GN, Holle LA, Burthem J, Bolton-Maggs PHB, Lin FC, Wolberg AS. Abnormal plasma clot formation and fibrinolysis reveal bleeding tendency in patients with partial factor XI deficiency. Blood Adv 2018; 2 (10) 1076-1088
    CrossrefPubMedSuche in Google Scholar
  • 57 Zucker M, Seligsohn U, Salomon O, Wolberg AS. Abnormal plasma clot structure and stability distinguish bleeding risk in patients with severe factor XI deficiency. J Thromb Haemost 2014; 12 (07) 1121-1130
    CrossrefPubMedSuche in Google Scholar
  • 58 Guéguen P, Galinat H, Blouch MT. et al. Biological determinants of bleeding in patients with heterozygous factor XI deficiency. Br J Haematol 2012; 156 (02) 245-251
    CrossrefPubMedSuche in Google Scholar
  • 59 Bolton-Maggs PH, Patterson DA, Wensley RT, Tuddenham EG. Definition of the bleeding tendency in factor XI-deficient kindreds--a clinical and laboratory study. Thromb Haemost 1995; 73 (02) 194-202
    Thieme ConnectPubMedSuche in Google Scholar
  • 60 Gailani D. Factor XI as a target for preventing venous thromboembolism. J Thromb Haemost 2022; 20 (03) 550-555
    CrossrefPubMedSuche in Google Scholar
  • 61 Nopp S, Kraemmer D, Ay C. Factor XI inhibitors for prevention and treatment of venous thromboembolism: a review on the rationale and update on current evidence. Front Cardiovasc Med 2022; 9: 903029
    CrossrefPubMedSuche in Google Scholar
  • 62 DeLoughery EP, Olson SR, Puy C, McCarty OJT, Shatzel JJ. The safety and efficacy of novel agents targeting factors XI and XII in early phase human trials. Semin Thromb Hemost 2019; 45 (05) 502-508
    Thieme ConnectPubMedSuche in Google Scholar
  • 63 Brass S. Cardiovascular biology. Platelets and proteases. Nature 2001; 413 (6851): 26-27
    CrossrefPubMedSuche in Google Scholar
  • 64 Schoenwaelder SM, Yuan Y, Josefsson EC. et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114 (03) 663-666
    CrossrefPubMedSuche in Google Scholar
  • 65 Reddy EC, Rand ML. Procoagulant Phosphatidylserine-Exposing Platelets in vitro and in vivo . Front Cardiovasc Med 2020; 7: 15
    CrossrefPubMedSuche in Google Scholar
  • 66 Huang M, Rigby AC, Morelli X. et al. Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 2003; 10 (09) 751-756
    CrossrefPubMedSuche in Google Scholar
  • 67 Walsh PN, Mills DC, Pareti FI. et al. Hereditary giant platelet syndrome. Absence of collagen-induced coagulant activity and deficiency of factor-XI binding to platelets. Br J Haematol 1975; 29 (04) 639-655
    PubMedSuche in Google Scholar
  • 68 White-Adams TC, Berny MA, Tucker EI. et al. Identification of coagulation factor XI as a ligand for platelet apolipoprotein E receptor 2 (ApoER2). Arterioscler Thromb Vasc Biol 2009; 29 (10) 1602-1607
    CrossrefPubMedSuche in Google Scholar
  • 69 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 (08) 2271-2281 [Retracted in: Walsh PN. Biochemistry. 2007 Nov 6;46(44):12886–12887]
    CrossrefPubMedSuche in Google Scholar
  • 70 Yun TH, Baglia FA, Myles T. et al. 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. J Biol Chem 2003; 278 (48) 48112-48119
    CrossrefPubMedSuche in Google Scholar
  • 71 Kossmann S, Lagrange J, Jäckel S. et al. Platelet-localized FXI promotes a vascular coagulation-inflammatory circuit in arterial hypertension. Sci Transl Med 2017; 9 (375) eaah4923
    CrossrefPubMedSuche in Google Scholar
  • 72 Döhrmann M, Makhoul S, Gross K. et al. CD36-fibrin interaction propagates FXI-dependent thrombin generation of human platelets. FASEB J 2020; 34 (07) 9337-9357
    CrossrefPubMedSuche in Google Scholar
  • 73 Verhoef JJ, Barendrecht AD, Nickel KF. et al. Polyphosphate nanoparticles on the platelet surface trigger contact system activation. Blood 2017; 129 (12) 1707-1717
    CrossrefPubMedSuche in Google Scholar
  • 74 Miller TN, Sinha D, Baird TR, Walsh PN. A catalytic domain exosite (Cys527-Cys542) in factor XIa mediates binding to a site on activated platelets. Biochemistry 2007; 46 (50) 14450-14460
    CrossrefPubMedSuche in Google Scholar
  • 75 Reitsma SE, Pang J, Raghunathan V. et al. Role of platelets in regulating activated coagulation factor XI activity. Am J Physiol Cell Physiol 2021; 320 (03) C365-C374
    CrossrefPubMedSuche in Google Scholar
  • 76 Rodrigues SF, Granger DN. Blood cells and endothelial barrier function. Tissue Barriers 2015; 3 (1–2): e978720
    CrossrefPubMedSuche in Google Scholar
  • 77 Yau JW, Teoh H, Verma S. Endothelial cell control of thrombosis. BMC Cardiovasc Disord 2015; 15: 130
    CrossrefPubMedSuche in Google Scholar
  • 78 van Hinsbergh VW. Endothelium--role in regulation of coagulation and inflammation. Semin Immunopathol 2012; 34 (01) 93-106
    CrossrefPubMedSuche in Google Scholar
  • 79 Long AT, Kenne E, Jung R, Fuchs TA, Renné T. Contact system revisited: an interface between inflammation, coagulation, and innate immunity. J Thromb Haemost 2016; 14 (03) 427-437
    CrossrefPubMedSuche in Google Scholar
  • 80 Pathak M, Kaira BG, Slater A, Emsley J. Cell receptor and cofactor interactions of the contact activation system and factor XI. Front Med (Lausanne) 2018; 5: 66
    CrossrefPubMedSuche in Google Scholar
  • 81 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 (28) 19833-19839
    CrossrefPubMedSuche in Google Scholar
  • 82 Shariat-Madar Z, Mahdi F, Schmaier AH. Factor XI assembly and activation on human umbilical vein endothelial cells in culture. Thromb Haemost 2001; 85 (03) 544-551
    Thieme ConnectPubMedSuche in Google Scholar
  • 83 Mohammed BM, Cheng Q, Matafonov A. et al. A non-circulating pool of factor XI associated with glycosaminoglycans in mice. J Thromb Haemost 2019; 17 (09) 1449-1460
    CrossrefPubMedSuche in Google Scholar
  • 84 Mahdi F, Shariat-Madar Z, Schmaier AH. The relative priority of prekallikrein and factors XI/XIa assembly on cultured endothelial cells. J Biol Chem 2003; 278 (45) 43983-43990
    CrossrefPubMedSuche in Google Scholar
  • 85 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 (41) 38462-38467
    CrossrefPubMedSuche in Google Scholar
  • 86 Baird TR, Walsh PN. Activated platelets but not endothelial cells participate in the initiation of the consolidation phase of blood coagulation. J Biol Chem 2002; 277 (32) 28498-28503
    CrossrefPubMedSuche in Google Scholar
  • 87 Puy C, Ngo ATP, Pang J. et al. Endothelial PAI-1 (plasminogen activator inhibitor-1) blocks the intrinsic pathway of coagulation, inducing the clearance and degradation of FXIa (activated factor XI). Arterioscler Thromb Vasc Biol 2019; 39 (07) 1390-1401
    CrossrefPubMedSuche in Google Scholar
  • 88 Ngo ATP, Jordan KR, Mueller PA. et al. Pharmacological targeting of coagulation factor XI mitigates the development of experimental atherosclerosis in low-density lipoprotein receptor-deficient mice. J Thromb Haemost 2021; 19 (04) 1001-1017
    CrossrefPubMedSuche in Google Scholar
  • 89 Foley JH, Conway EM. Cross talk pathways between coagulation and inflammation. Circ Res 2016; 118 (09) 1392-1408
    CrossrefPubMedSuche in Google Scholar
  • 90 Schmaier AH. The contact activation and kallikrein/kinin systems: pathophysiologic and physiologic activities. J Thromb Haemost 2016; 14 (01) 28-39
    CrossrefPubMedSuche in Google Scholar
  • 91 Bryant JW, Shariat-Madar Z. Human plasma kallikrein-kinin system: physiological and biochemical parameters. Cardiovasc Hematol Agents Med Chem 2009; 7 (03) 234-250
    CrossrefPubMedSuche in Google Scholar
  • 92 Schmaier AH. The physiologic basis of assembly and activation of the plasma kallikrein/kinin system. Thromb Haemost 2004; 91 (01) 1-3
    Thieme ConnectPubMedSuche in Google Scholar
  • 93 Silasi R, Keshari RS, Lupu C. et al. Inhibition of contact-mediated activation of factor XI protects baboons against S. aureus-induced organ damage and death. Blood Adv 2019; 3 (04) 658-669
    CrossrefPubMedSuche in Google Scholar
  • 94 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 (19) 10856-10863
    CrossrefPubMedSuche in Google Scholar
  • 95 Bane Jr CE, Ivanov I, Matafonov A. et al. Factor XI deficiency alters the cytokine response and activation of contact proteases during polymicrobial sepsis in mice. PLoS One 2016; 11 (04) e0152968
    CrossrefPubMedSuche in Google Scholar
  • 96 Rawish E, Sauter M, Sauter R, Nording H, Langer HF. Complement, inflammation and thrombosis. Br J Pharmacol 2021; 178 (14) 2892-2904
    CrossrefPubMedSuche in Google Scholar
  • 97 Ghebrehiwet B, Silverberg M, Kaplan AP. Activation of the classical pathway of complement by Hageman factor fragment. J Exp Med 1981; 153 (03) 665-676
    CrossrefPubMedSuche in Google Scholar
  • 98 Irmscher S, Döring N, Halder LD. et al. Kallikrein cleaves C3 and activates complement. J Innate Immun 2018; 10 (02) 94-105
    CrossrefPubMedSuche in Google Scholar
  • 99 Puy C, Pang J, Reitsma SE. et al. Cross-talk between the complement pathway and the contact activation system of coagulation: activated factor XI neutralizes complement factor H. J Immunol 2021; 206 (08) 1784-1792
    CrossrefPubMedSuche in Google Scholar
  • 100 Heal SL, Hardy LJ, Wilson CL. et al. Novel interaction of properdin and coagulation factor XI: Crosstalk between complement and coagulation. Res Pract Thromb Haemost 2022; 6 (04) e12715
    CrossrefPubMedSuche in Google Scholar
  • 101 Shi T, Giannakopoulos B, Iverson GM, Cockerill KA, Linnik MD, Krilis SA. Domain V of β2-glycoprotein I binds factor XI/XIa and is cleaved at Lys317-Thr318. J Biol Chem 2005; 280 (02) 907-912
    CrossrefPubMedSuche in Google Scholar
  • 102 Ge X, Yamaguchi Y, Zhao L. et al. Prochemerin cleavage by factor XIa links coagulation and inflammation. Blood 2018; 131 (03) 353-364
    CrossrefPubMedSuche in Google Scholar
  • 103 Shi T, Iverson GM, Qi JC. et al. Beta 2-Glycoprotein I binds factor XI and inhibits its activation by thrombin and factor XIIa: loss of inhibition by clipped beta 2-glycoprotein I. Proc Natl Acad Sci U S A 2004; 101 (11) 3939-3944
    CrossrefPubMedSuche in Google Scholar
  • 104 Horbach DA, van Oort E, Lisman T, Meijers JC, Derksen RH, de Groot PG. Beta2-glycoprotein I is proteolytically cleaved in vivo upon activation of fibrinolysis. Thromb Haemost 1999; 81 (01) 87-95
    Thieme ConnectPubMedSuche in Google Scholar
  • 105 Itoh Y, Inuzuka K, Kohno I. et al. Highly increased plasma concentrations of the nicked form of beta(2) glycoprotein I in patients with leukemia and with lupus anticoagulant: measurement with a monoclonal antibody specific for a nicked form of domain V. J Biochem 2000; 128 (06) 1017-1024
    CrossrefPubMedSuche in Google Scholar
  • 106 Mattern A, Zellmann T, Beck-Sickinger AG. Processing, signaling, and physiological function of chemerin. IUBMB Life 2014; 66 (01) 19-26
    CrossrefPubMedSuche in Google Scholar
  • 107 Lorentz CU, Tucker EI, Verbout NG. et al. The contact activation inhibitor AB023 in heparin-free hemodialysis: results of a randomized phase 2 clinical trial. Blood 2021; 138 (22) 2173-2184
    CrossrefPubMedSuche in Google Scholar
  • 108 Pallares Robles A, Ten Cate V, Schulz A. et al. Association of FXI activity with thrombo-inflammation, extracellular matrix, lipid metabolism and apoptosis in venous thrombosis. Sci Rep 2022; 12 (01) 9761
    CrossrefPubMedSuche in Google Scholar
  • 109 Cao Y, Wang Y, Zhou Z. et al. Liver-heart cross-talk mediated by coagulation factor XI protects against heart failure. Science 2022; 377 (6613): 1399-1406
    CrossrefPubMedSuche in Google Scholar