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Thromb Haemost 2003; 89(01): 3-8
DOI: 10.1055/s-0037-1613535
Review Article
Schattauer GmbH

Intravascular tissue factor pathway – a model for rapid initiation of coagulation within the blood vessel

Bernd Engelmann
2   Vaskuläre Biologie und Hämostase, Institut für Klinische Chemie, Ludwig-Maximilians-Universität München, Munich, Germany
,
Thomas Luther
1   Institut für Pathologie, Technische Universität Dresden, Dresden, Germany
,
Ingrid Müller
2   Vaskuläre Biologie und Hämostase, Institut für Klinische Chemie, Ludwig-Maximilians-Universität München, Munich, Germany
› Author Affiliations Financial support The investigations in the author’s laboratory have been supported by grants from the Deutsche Forschungsgemeinschaft.
Further Information

Publication History

Received 25 October 2002

Accepted 04 November 2002

Publication Date:
09 December 2017 (online)

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Summary

The loss of blood through vessel wall ruptures is initially prevented by the rapid adhesion of platelets to the subendothelium, and the formation of a thrombus consisting of platelets and different types of leukocytes. Concomitantly, the coagulation process is thought to be activated by vascular wall tissue factor (TF). Here, a new model for the initiation of coagulation is presented, based on unexpected findings on the presence and functional activation of TF within the blood itself. TF was recently found to be stored in the α-granules of resting platelets under physiological conditions. Activation by collagen exposes TF on the platelet cell membrane and on platelet derived microvesicles. Adhesive interactions of the TF bearing platelets and microvesicles to neutrophils and monocytes support the functional activation of the blood based TF. The intravascular TF pathway is proposed to play a significant role during hemostasis by enabling the generation of fibrin at the site of the developing thrombus.

Keywords

P-selectin - PSGL-1 - circulating microvesicles - factor VIIa - factor Xa
 

  • References

  • 1 Dahlback B. Blood coagulation. Lancet 2000; 355: 1627-32.
    CrossrefPubMedGoogle Scholar
  • 2 Morrissey JH. Tissue factor: an enzyme cofactor and a true receptor. Thromb Haemost 2001; 86: 66-74.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 3 Kannemeier C, Feussner A, Stohr HA, Weisse J, Preissner KT, Romisch J. Factor VII and single-chain plasminogen activator-activating protease: activation and autoactivation of the proenzyme. Eur J Biochem 2001; 268: 3789-96.
    CrossrefPubMedGoogle Scholar
  • 4 Bajaj MS, Birktoft JJ, Steer SA, Bajaj SP. Structure and biology of tissue factor pathway inhibitor. Thromb Haemost 2001; 86: 959-72.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Camerer E, Kolsto AB, Prydz H. Cell biology of tissue factor, the principal initiator of blood coagulation. Thromb Res 1996; 81: 1-41.
    CrossrefPubMedGoogle Scholar
  • 6 Zhang Y, Deng Y, Luther T, Müller M, Ziegler R, Waldherr R, Stern DM, Nawroth PP. Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest 1994; 94: 1320-7.
    CrossrefPubMedGoogle Scholar
  • 7 Contrino J, Hair G, Kreutzer DL, Rickles FR. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996; 2: 209-15.
    CrossrefPubMedGoogle Scholar
  • 8 Osterud B, Bjorklid E. The tissue factor pathway in disseminated intravascular coagulation. Semin Thromb Hemost 2001; 27: 605-17.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Zillmann A, Luther T, Muller I, Kotzsch M, Spannagl M, Kauke T, Oelschlagel U, Zahler S, Engelmann B. Platelet-associated tissue factor contributes to the collagen-triggered activation of blood coagulation. Biochem Biophys Res Commun 2001; 281: 603-9.
    CrossrefPubMedGoogle Scholar
  • 10 Koyama T, Nishida K, Ohdama S, Sawada M, Murakami N, Hirosawa S, Kuriyama R, Matsuzawa K, Hasegawa R, Aoki N. Determination of plasma tissue factor antigen and its clinical significance. Br J Haematol 1994; 87: 343-7.
    CrossrefPubMedGoogle Scholar
  • 11 Fareed J, Callas DD, Hoppensteads D, Bermes EW. Tissue factor antigen levels in various biological fluids. Blood Coagul Fibrinolysis 1995; 6 (Suppl. 01) (Suppl.) S32-S36.
    PubMedGoogle Scholar
  • 12 Zumbach M, Hofmann M, Borcea V, Luther T, Kotzsch M, Muller M, Hergesell O, Andrassy K, Ritz E, Ziegler R, Wahl P, Nawroth PP. Tissue factor antigen is elevated in patients with microvascular complications of diabetes mellitus. Exp Clin Endocrinol 1997; 105: 206-12.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Suefuji H, Ogawa H, Yasue H, Kaikita K, Soejima H, Motoyama T, Mizuno Y, Oshima S, Saito T, Tsuji I, Kumeda K, Kamikubo Y, Nakamura S. Increased plasma tissue factor levels in acute myocardial infarction. Am Heart J 1997; 134: 253-9.
    CrossrefPubMedGoogle Scholar
  • 14 Misumi K, Ogawa H, Yasue H, Soejima H, Suefuji H, Nishiyama K, Takazoe K, Kugiyama K, Tsuji I, Kumeda K, Nakamura S. Comparison of plasma tissue factor levels in unstable and stable angina pectoris. Am J Cardiol 1998 81: 22-6.
    PubMedGoogle Scholar
  • 15 Müller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E, Zieseniss S, Zahler S, Preissner K, Engelmann B. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J (in press).
    PubMedGoogle Scholar
  • 16 Neuenschwander PF, Morrissey JH. Deletion of the membrane anchoring region of tissue factor abolishes autoactivation of factor VII but not cofactor function. J Biol Chem 1992; 267: 14477-82.
    PubMedGoogle Scholar
  • 17 Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 1999; 96: 2311-5.
    CrossrefPubMedGoogle Scholar
  • 18 Osterud B. The role of platelets in decrypting monocyte tissue factor. Semin Hematol 2001; 38 (Suppl. 04) (Suppl 12) 2-5.
    PubMedGoogle Scholar
  • 19 Hoffman M, Monroe DM. 3rd A cell-based model of hemostasis. Thromb Haemost 2001; 85: 958-65.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 20 Rauch U, Bonderman D, Bohrmann B, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96: 170-5.
    PubMedGoogle Scholar
  • 21 Ott I, Andrassy M, Zieglgansberger D, Geith S, Schomig A, Neumann FJ. Regulation of monocyte procoagulant activity in acute myocardial infarction: role of tissue factor and tissue factor pathway inhibitor-1. Blood 2001; 97: 3721-6.
    CrossrefPubMedGoogle Scholar
  • 22 Siddiqui FA, Desai H, Amirkhosravi A, Amaya M, Francis JL. The presence and release of tissue factor from human platelets. Platelets 2002; 13: 247-53.
    CrossrefPubMedGoogle Scholar
  • 23 Berckmans RJ, Nieuwland R, Boing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 2001; 85: 639-46.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 24 McEver RP. Adhesive interactions of leukocytes, platelets, and the vessel wall during hemostasis and inflammation. Thromb Haemost 2001; 86: 746-56.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu YM, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-51.
    CrossrefPubMedGoogle Scholar
  • 26 Kirchhofer D, Sakariassen KS, Clozel M, Tschopp TB, Hadvary P, Nemerson Y, Baumgartner HR. Relationship between tissue factor expression and deposition of fibrin, platelets, and leukocytes on cultured endothelial cells under venous blood flow conditions. Blood 1993; 81: 2050-8.
    CrossrefPubMedGoogle Scholar
  • 27 Goel MS, Diamond SL. Neutrophil enhancement of fibrin deposition under flow through platelet-dependent and -independent mechanisms. Arterioscler Thromb Vasc Biol 2001; 21: 2093-8.
    CrossrefPubMedGoogle Scholar
  • 28 Michelson AD, Barnard MR, Krueger LA, Valeri CR, Furman MI. Circulating monocyteplatelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001; 104: 1533-7.
    CrossrefPubMedGoogle Scholar
  • 29 Cerletti C, Evangelista V, de Gaetano G. Pselectin-beta 2-integrin cross-talk: a molecular mechanism for polymorphonuclear leukocyte recruitment at the site of vascular damage. Thromb Haemost 1999; 82: 787-93.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 30 Weber C, Springer TA. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J Clin Invest 1997; 100: 2085-93.
    CrossrefPubMedGoogle Scholar
  • 31 Simon DI, Chen Z, Xu H. et al. Platelet glycoprotein Ib is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med 2000; 192: 193-204.
    CrossrefPubMedGoogle Scholar
  • 32 Santoso S, Sachs UJ, Kroll H, Linder M, Ruf A, Preissner KT, Chavakis T. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J Exp Med 2002; 196: 679-91.
    CrossrefPubMedGoogle Scholar
  • 33 Mallat Z, Benamer H, Hugel B, Benessiano J, Steg PG, Freyssinet JM, Tedgui A. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 2000; 101: 41-3.
    CrossrefPubMedGoogle Scholar
  • 34 Vidal C, Spaulding C, Picard F, Schaison F, Melle J, Weber S, Fontenay-Roupie M. Flow cytometry detection of platelet procoagulation activity and microparticles in patients with unstable angina treated by percutaneous coronary angioplasty and stent implantation. Thromb Haemost 2001; 86: 784-90.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Evangelista V, Rajtar G, de Gaetano G, White JG, Cerletti C. Platelet activation by fMLPstimulated polymorphonuclear leukocytes: the activity of cathepsin G is not prevented by antiproteinases. Blood 1991; 77: 2379-88.
    PubMedGoogle Scholar
  • 36 Clark RA, Klebanoff SJ. Neutrophil-platelet interaction mediated by myeloperoxidase and hydrogen peroxide. J Immunol 1980; 124: 399-405.
    PubMedGoogle Scholar
  • 37 Tsuji T, Nagata K, Koike J, Todoroki N, Irimura T. Induction of superoxide anion production from monocytes and neutrophils by activated platelets through the P-selectin-sialyl Lewis X interaction. J Leukoc Biol 1994; 56: 583-7.
    CrossrefPubMedGoogle Scholar
  • 38 Lesnik P, Dentan C, Vonica A, Moreau M, Chapman MJ. Tissue factor pathway inhibitor activity associated with LDL is inactivated by cell- and copper-mediated oxidation. Arterioscler Thromb Vasc Biol 1995; 15: 1121-30.
    CrossrefPubMedGoogle Scholar
  • 39 Novotny WF, Girard TJ, Miletich JP, Broze Jr GJ. Platelets secrete a coagulation inhibitor functionally and antigenically similar to the lipoprotein associated coagulation inhibitor. Blood 1988; 72: 2020-5.
    PubMedGoogle Scholar
  • 40 Libby P. Changing concepts of atherogenesis. J Intern Med 2000; 247: 349-58.
    CrossrefPubMedGoogle Scholar
  • 41 Mallat Z, Hugel B, Ohan J, Leseche G, Freyssinet JM, Tedgui A.. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99: 348-53.
    CrossrefPubMedGoogle Scholar
  • 42 Zieseniss S, Zahler S, Muller I, Hermetter A, Engelmann B. Modified phosphatidylethanolamine as the active component of oxidized low density lipoprotein promoting platelet prothrombinase activity. J Biol Chem 2001; 276: 19828-35.
    CrossrefPubMedGoogle Scholar
  • 43 Siess W. Athero- and thrombogenic actions of lysophosphatidic acid and sphingosine-1-phosphate. Biochim Biophys Acta 2002; 1582: 204-15.
    CrossrefPubMedGoogle Scholar
  • 44 Lawson CA, Yan SD, Yan SF, Liao H, Zhou YS, Sobel J, Kisiel W, Stern DM, Pinsky DJ. Monocytes and tissue factor promote thrombosis in a murine model of oxygen deprivation. J Clin Invest 1997; 99: 1729-38.
    CrossrefPubMedGoogle Scholar