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Thromb Haemost 2019; 119(06): 860-870
DOI: 10.1055/s-0039-1681102
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Role of Cell Surface Lipids and Thiol-Disulphide Exchange Pathways in Regulating the Encryption and Decryption of Tissue Factor

Shabbir A. Ansari
1   Department of Cellular and Molecular Biology, The University of Texas Health Science Center at Tyler, Tyler, Texas, United States
,
Usha R. Pendurthi
1   Department of Cellular and Molecular Biology, The University of Texas Health Science Center at Tyler, Tyler, Texas, United States
,
L. Vijaya Mohan Rao
1   Department of Cellular and Molecular Biology, The University of Texas Health Science Center at Tyler, Tyler, Texas, United States
› Institutsangaben Funding This work was supported by the National Heart, Lung, and Blood Institute grants HL124055 and HL107483 to L.V.M.R. and American Heart Association’s post-doctoral fellowship award to S.A.A.
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Publikationsverlauf

30. November 2018

21. Januar 2019

Publikationsdatum:
12. März 2019 (online)

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Abstract

Tissue factor (TF), a transmembrane glycoprotein, is the cellular receptor of the coagulation factors VII (FVII) and VIIa (FVIIa). The formation of TF–FVIIa complex triggers the initiation of the blood coagulation pathway. TF plays an essential role in haemostasis, but an aberrant expression of TF activity contributes to thrombotic disorders. In health, TF pro-coagulant activity on cells is controlled tightly to allow sufficient coagulant activity to achieve haemostasis but not to cause thrombosis. It is achieved largely by selective localization of TF in the body and encryption of TF at the cell surface. A vast majority of TF on resting cells exists in an encrypted state with minimal pro-coagulant activity but becomes pro-thrombotic following cell injury or activation. At present, the mechanisms that are responsible for TF encryption and activation (decryption) are not entirely clear, but recent studies provide important mechanistic insights into these processes. To date, externalization of phosphatidylserine to the outer leaflet and thiol-disulphide exchange pathways that either turn on and off the allosteric disulphide bond in TF are shown to play a major role in regulating TF pro-coagulant activity on cell surfaces. Recent studies showed that sphingomyelin, a major phospholipid in the outer leaflet of plasma membrane, plays a critical role in the encryption of TF in resting cells. The present review provides an overview of recent literature on the above-described mechanisms of TF encryption and decryption with a particular emphasis on our recent findings.

Keywords

tissue factor - factor VIIa - encryption - decryption - sphingomyelin - phosphatidylserine - thiol-disulphide exchange pathways

Authors' Contributions

All authors contributed to the preparation and review of the article.


 

  • References

  • 1 Rapaport SI, Rao LVM. The tissue factor pathway: how it has become a “prima ballerina”. Thromb Haemost 1995; 74 (01) 7-17
    Thieme ConnectPubMedSuche in Google Scholar
  • 2 Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol 1989; 134 (05) 1087-1097
    PubMedSuche in Google Scholar
  • 3 Fleck RA, Rao LVM, Rapaport SI, Varki N. Localization of human tissue factor antigen by immunostaining with monospecific, polyclonal anti-human tissue factor antibody. Thromb Res 1990; 59 (02) 421-437
    CrossrefPubMedSuche in Google Scholar
  • 4 Giesen PL, Rauch U, Bohrmann B. , et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A 1999; 96 (05) 2311-2315
    CrossrefPubMedSuche in Google Scholar
  • 5 Butenas S, Bouchard BA, Brummel-Ziedins KE, Parhami-Seren B, Mann KG. Tissue factor activity in whole blood. Blood 2005; 105 (07) 2764-2770
    CrossrefPubMedSuche in Google Scholar
  • 6 Osterud B, Olsen JO, Bjørklid E. What is blood borne tissue factor?. Thromb Res 2009; 124 (05) 640-641
    CrossrefPubMedSuche in Google Scholar
  • 7 Osterud B, Bjorklid E. Tissue factor in blood cells and endothelial cells. Front Biosci (Elite Ed) 2012; 4: 289-299
    PubMedSuche in Google Scholar
  • 8 van der Poll T, Herwald H. The coagulation system and its function in early immune defense. Thromb Haemost 2014; 112 (04) 640-648
    Thieme ConnectPubMedSuche in Google Scholar
  • 9 Grover SP, Mackman N. Tissue factor: an essential mediator of hemostasis and trigger of thrombosis. Arterioscler Thromb Vasc Biol 2018; 38 (04) 709-725
    CrossrefPubMedSuche in Google Scholar
  • 10 Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006; 26 (03) 456-461
    CrossrefPubMedSuche in Google Scholar
  • 11 Kothari H, Pendurthi UR, Rao LV. Analysis of tissue factor expression in various cell model systems: cryptic vs. active. J Thromb Haemost 2013; 11 (07) 1353-1363
    CrossrefPubMedSuche in Google Scholar
  • 12 Rao LV, Pendurthi UR. Regulation of tissue factor coagulant activity on cell surfaces. J Thromb Haemost 2012; 10 (11) 2242-2253
    CrossrefPubMedSuche in Google Scholar
  • 13 Le DT, Rapaport SI, Rao LVM. Relations between factor VIIa binding and expression of factor VIIa/tissue factor catalytic activity on cell surfaces. J Biol Chem 1992; 267 (22) 15447-15454
    CrossrefPubMedSuche in Google Scholar
  • 14 Bach R, Rifkin DB. Expression of tissue factor procoagulant activity: regulation by cytosolic calcium. Proc Natl Acad Sci U S A 1990; 87 (18) 6995-6999
    CrossrefPubMedSuche in Google Scholar
  • 15 Ploplis VA, Edgington TS, Fair DS. Initiation of the extrinsic pathway of coagulation. Association of factor VIIa with a cell line expressing tissue factor. J Biol Chem 1987; 262 (20) 9503-9508
    CrossrefPubMedSuche in Google Scholar
  • 16 Maynard JR, Heckman CA, Pitlick FA, Nemerson Y. Association of tissue factor activity with the surface of cultured cells. J Clin Invest 1975; 55 (04) 814-824
    CrossrefPubMedSuche in Google Scholar
  • 17 Rao LVM, Kothari H, Pendurthi UR. Tissue factor: mechanisms of decryption. Front Biosci (Elite Ed) 2012; 4: 1513-1527
    PubMedSuche in Google Scholar
  • 18 Langer F, Ruf W. Synergies of phosphatidylserine and protein disulfide isomerase in tissue factor activation. Thromb Haemost 2014; 111 (04) 590-597
    Thieme ConnectPubMedSuche in Google Scholar
  • 19 Ruf W. Role of thiol pathways in TF procoagulant regulation. Thromb Res 2012; 129 (Suppl. 02) S11-S12
    CrossrefPubMedSuche in Google Scholar
  • 20 Chen VM, Hogg PJ. Encryption and decryption of tissue factor. J Thromb Haemost 2013; 11 (Suppl. 01) 277-284
    CrossrefPubMedSuche in Google Scholar
  • 21 Versteeg HH, Ruf W. Thiol pathways in the regulation of tissue factor prothrombotic activity. Curr Opin Hematol 2011; 18 (05) 343-348
    CrossrefPubMedSuche in Google Scholar
  • 22 Zelaya H, Rothmeier AS, Ruf W. Tissue factor at the crossroad of coagulation and cell signaling. J Thromb Haemost 2018; 16 (10) 1941-1952
    CrossrefPubMedSuche in Google Scholar
  • 23 Kiouptsi K, Reinhardt C. Protein disulfide-isomerase - a trigger of tissue factor-dependent thrombosis. Clin Hemorheol Microcirc 2016; 64 (03) 279-286
    PubMedSuche in Google Scholar
  • 24 Chargaff E. Remarks on the role of lipids in blood coagulation. Arch Sci Physiol (Paris) 1948; 2: 269-271
    PubMedSuche in Google Scholar
  • 25 Nemerson Y. The phospholipid requirement of tissue factor in blood coagulation. J Clin Invest 1968; 47 (01) 72-80
    CrossrefPubMedSuche in Google Scholar
  • 26 Bjorklid E, Storm E. Purification and some properties of the protein component of tissue thromboplastin from human brain. Biochem J 1977; 165 (01) 89-96
    CrossrefPubMedSuche in Google Scholar
  • 27 Krishnaswamy S, Field KA, Edgington TS, Morrissey JH, Mann KG. Role of the membrane surface in the activation of human coagulation factor X. J Biol Chem 1992; 267 (36) 26110-26120
    CrossrefPubMedSuche in Google Scholar
  • 28 Neuenschwander PF, Bianco-Fisher E, Rezaie AR, Morrissey JH. Phosphatidylethanolamine augments factor VIIa-tissue factor activity: enhancement of sensitivity to phosphatidylserine. Biochemistry 1995; 34 (43) 13988-13993
    CrossrefPubMedSuche in Google Scholar
  • 29 Shaw AW, Pureza VS, Sligar SG, Morrissey JH. The local phospholipid environment modulates the activation of blood clotting. J Biol Chem 2007; 282 (09) 6556-6563
    CrossrefPubMedSuche in Google Scholar
  • 30 Wang J, Pendurthi UR, Rao LVM. Sphingomyelin encrypts tissue factor: ATP-induced activation of A-SMase leads to tissue factor decryption and microvesicle shedding. Blood Adv 2017; 1 (13) 849-862
    CrossrefPubMedSuche in Google Scholar
  • 31 Morrissey JH, Neuenschwander PF, Huang Q, McCallum CD, Su B, Johnson AE. Factor VIIa-tissue factor: functional importance of protein-membrane interactions. Thromb Haemost 1997; 78 (01) 112-116
    Thieme ConnectPubMedSuche in Google Scholar
  • 32 Morrissey JH, Tajkhorshid E, Sligar SG, Rienstra CM. Tissue factor/factor VIIa complex: role of the membrane surface. Thromb Res 2012; 129 (Suppl. 02) S8-S10
    CrossrefPubMedSuche in Google Scholar
  • 33 Ohkubo YZ, Morrissey JH, Tajkhorshid E. Dynamical view of membrane binding and complex formation of human factor VIIa and tissue factor. J Thromb Haemost 2010; 8 (05) 1044-1053
    PubMedSuche in Google Scholar
  • 34 Ke K, Yuan J, Morrissey JH. Tissue factor residues that putatively interact with membrane phospholipids. PLoS One 2014; 9 (02) e88675
    CrossrefPubMedSuche in Google Scholar
  • 35 Mallik S, Prasad R, Bhattacharya A, Sen P. Synthesis of phosphatidylserine and its stereoisomers: their role in activation of blood coagulation. ACS Med Chem Lett 2018; 9 (05) 434-439
    CrossrefPubMedSuche in Google Scholar
  • 36 Zwaal RFA, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997; 89 (04) 1121-1132
    CrossrefPubMedSuche in Google Scholar
  • 37 Daleke DL. Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 2003; 44 (02) 233-242
    CrossrefPubMedSuche in Google Scholar
  • 38 Fadeel B, Xue D. The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit Rev Biochem Mol Biol 2009; 44 (05) 264-277
    CrossrefPubMedSuche in Google Scholar
  • 39 Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005; 62 (09) 971-988
    CrossrefPubMedSuche in Google Scholar
  • 40 Kodigepalli KM, Bowers K, Sharp A, Nanjundan M. Roles and regulation of phospholipid scramblases. FEBS Lett 2015; 589 (01) 3-14
    CrossrefPubMedSuche in Google Scholar
  • 41 van der Mark VA, Elferink RP, Paulusma CC. P4 ATPases: flippases in health and disease. Int J Mol Sci 2013; 14 (04) 7897-7922
    CrossrefPubMedSuche in Google Scholar
  • 42 Ruf W, Rehemtulla A, Morrissey JH, Edgington TS. Phospholipid-independent and -dependent interactions required for tissue factor receptor and cofactor function. J Biol Chem 1991; 266 (04) 2158-2166
    CrossrefPubMedSuche in Google Scholar
  • 43 Le DT, Rapaport SI, Rao LVM. Studies of the mechanism for enhanced cell surface factor VIIa/tissue factor activation of factor X on fibroblast monolayers after their exposure to N-ethylmaleimide. Thromb Haemost 1994; 72 (06) 848-855
    Thieme ConnectPubMedSuche in Google Scholar
  • 44 Ansari SA, Pendurthi UR, Sen P, Rao LV. The role of putative phosphatidylserine-interactive residues of tissue factor on its coagulant activity at the cell surface. PLoS One 2016; 11 (06) e0158377
    CrossrefPubMedSuche in Google Scholar
  • 45 Balasubramanian K, Mirnikjoo B, Schroit AJ. Regulated externalization of phosphatidylserine at the cell surface: implications for apoptosis. J Biol Chem 2007; 282 (25) 18357-18364
    CrossrefPubMedSuche in Google Scholar
  • 46 Leonarduzzi G, Chiarpotto E, Biasi F, Poli G. 4-Hydroxynonenal and cholesterol oxidation products in atherosclerosis. Mol Nutr Food Res 2005; 49 (11) 1044-1049
    CrossrefPubMedSuche in Google Scholar
  • 47 Mali VR, Palaniyandi SS. Regulation and therapeutic strategies of 4-hydroxy-2-nonenal metabolism in heart disease. Free Radic Res 2014; 48 (03) 251-263
    CrossrefPubMedSuche in Google Scholar
  • 48 Vatsyayan R, Kothari H, Pendurthi UR, Rao LV. 4-Hydroxy-2-nonenal enhances tissue factor activity in human monocytic cells via p38 mitogen-activated protein kinase activation-dependent phosphatidylserine exposure. Arterioscler Thromb Vasc Biol 2013; 33 (07) 1601-1611
    CrossrefPubMedSuche in Google Scholar
  • 49 Ansari SA, Pendurthi UR, Rao LVM. The lipid peroxidation product 4-hydroxy-2-nonenal induces tissue factor decryption via ROS generation and the thioredoxin system. Blood Adv 2017; 1 (25) 2399-2413
    CrossrefPubMedSuche in Google Scholar
  • 50 Ebert J, Wilgenbus P, Teiber JF. , et al. Paraoxonase-2 regulates coagulation activation through endothelial tissue factor. Blood 2018; 131 (19) 2161-2172
    CrossrefPubMedSuche in Google Scholar
  • 51 Hagmann H, Kuczkowski A, Ruehl M. , et al. Breaking the chain at the membrane: paraoxonase 2 counteracts lipid peroxidation at the plasma membrane. FASEB J 2014; 28 (04) 1769-1779
    CrossrefPubMedSuche in Google Scholar
  • 52 Liang HPH, Hogg PJ. Critical importance of the cell system when studying tissue factor de-encryption. Blood 2008; 112 (03) 912-913
    PubMedSuche in Google Scholar
  • 53 Langer F, Spath B, Fischer C. , et al. Rapid activation of monocyte tissue factor by antithymocyte globulin is dependent on complement and protein disulfide isomerase. Blood 2013; 121 (12) 2324-2335
    CrossrefPubMedSuche in Google Scholar
  • 54 Furlan-Freguia C, Marchese P, Gruber A, Ruggeri ZM, Ruf W. P2×7 receptor signaling contributes to tissue factor-dependent thrombosis in mice. J Clin Invest 2011; 121 (07) 2932-2944
    CrossrefPubMedSuche in Google Scholar
  • 55 Wolberg AS, Monroe DM, Roberts HR, Hoffman MR. Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and -independent mechanisms. Blood Coagul Fibrinolysis 1999; 10 (04) 201-210
    CrossrefPubMedSuche in Google Scholar
  • 56 Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, Hogg PJ. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 2006; 45 (39) 12020-12028
    CrossrefPubMedSuche in Google Scholar
  • 57 Lysov Z, Swystun LL, Kuruvilla S, Arnold A, Liaw PC. Lung cancer chemotherapy agents increase procoagulant activity via protein disulfide isomerase-dependent tissue factor decryption. Blood Coagul Fibrinolysis 2015; 26 (01) 36-45
    CrossrefPubMedSuche in Google Scholar
  • 58 Quinn PJ. Plasma membrane phospholipid asymmetry. Subcell Biochem 2002; 36: 39-60
    PubMedSuche in Google Scholar
  • 59 Truman JP, Al Gadban MM, Smith KJ, Hammad SM. Acid sphingomyelinase in macrophage biology. Cell Mol Life Sci 2011; 68 (20) 3293-3305
    CrossrefPubMedSuche in Google Scholar
  • 60 Milhas D, Clarke CJ, Hannun YA. Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett 2010; 584 (09) 1887-1894
    CrossrefPubMedSuche in Google Scholar
  • 61 Pavoine C, Pecker F. Sphingomyelinases: their regulation and roles in cardiovascular pathophysiology. Cardiovasc Res 2009; 82 (02) 175-183
    CrossrefPubMedSuche in Google Scholar
  • 62 Wong ML, Xie B, Beatini N. , et al. Acute systemic inflammation up-regulates secretory sphingomyelinase in vivo: a possible link between inflammatory cytokines and atherogenesis. Proc Natl Acad Sci U S A 2000; 97 (15) 8681-8686
    CrossrefPubMedSuche in Google Scholar
  • 63 Smith EL, Schuchman EH. The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J 2008; 22 (10) 3419-3431
    CrossrefPubMedSuche in Google Scholar
  • 64 Bianco F, Perrotta C, Novellino L. , et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 2009; 28 (08) 1043-1054
    CrossrefPubMedSuche in Google Scholar
  • 65 Cremesti AE, Goni FM, Kolesnick R. Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome?. FEBS Lett 2002; 531 (01) 47-53
    CrossrefPubMedSuche in Google Scholar
  • 66 Hancock JF. Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 2006; 7 (06) 456-462
    PubMedSuche in Google Scholar
  • 67 Mulder AB, Smit JW, Bom VJJ. , et al. Association of smooth muscle cell tissue factor with caveolae. Blood 1996; 88 (04) 1306-1313
    CrossrefPubMedSuche in Google Scholar
  • 68 Mulder AB, Smit JW, Bom VJJ, Blom NR, Halie MR, van der Meer J. Association of endothelial tissue factor and thrombomodulin with caveolae. Blood 1996; 88 (09) 3667-3670
    CrossrefPubMedSuche in Google Scholar
  • 69 Mandal SK, Pendurthi UR, Rao LVM. Cellular localization and trafficking of tissue factor. Blood 2006; 107 (12) 4746-4753
    CrossrefPubMedSuche in Google Scholar
  • 70 Awasthi V, Mandal SK, Papanna V, Rao LV, Pendurthi UR. Modulation of tissue factor-factor VIIa signaling by lipid rafts and caveolae. Arterioscler Thromb Vasc Biol 2007; 27 (06) 1447-1455
    CrossrefPubMedSuche in Google Scholar
  • 71 Sevinsky JR, Rao LVM, Ruf W. Ligand-induced protease receptor translocation into caveolae: a mechanism for regulating cell surface proteolysis of the tissue factor-dependent coagulation pathway. J Cell Biol 1996; 133 (02) 293-304
    CrossrefPubMedSuche in Google Scholar
  • 72 Dietzen DJ, Page KL, Tetzloff TA. Lipid rafts are necessary for tonic inhibition of cellular tissue factor procoagulant activity. Blood 2004; 103 (08) 3038-3044
    CrossrefPubMedSuche in Google Scholar
  • 73 Goñi FM, Alonso A. Membrane fusion induced by phospholipase C and sphingomyelinases. Biosci Rep 2000; 20 (06) 443-463
    CrossrefPubMedSuche in Google Scholar
  • 74 López-Montero I, Monroy F, Vélez M, Devaux PF. Ceramide: from lateral segregation to mechanical stress. Biochim Biophys Acta 2010; 1798 (07) 1348-1356
    PubMedSuche in Google Scholar
  • 75 Sevier CS, Kaiser CA. Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol 2002; 3 (11) 836-847
    PubMedSuche in Google Scholar
  • 76 Mamathambika BS, Bardwell JC. Disulfide-linked protein folding pathways. Annu Rev Cell Dev Biol 2008; 24: 211-235
    CrossrefPubMedSuche in Google Scholar
  • 77 Liang HP, Brophy TM, Hogg PJ. Redox properties of the tissue factor Cys186-Cys209 disulfide bond. Biochem J 2011; 437 (03) 455-460
    CrossrefPubMedSuche in Google Scholar
  • 78 Schmidt B, Ho L, Hogg PJ. Allosteric disulfide bonds. Biochemistry 2006; 45 (24) 7429-7433
    CrossrefPubMedSuche in Google Scholar
  • 79 Ahamed J, Versteeg HH, Kerver M. , et al. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci U S A 2006; 103 (38) 13932-13937
    CrossrefPubMedSuche in Google Scholar
  • 80 Reinhardt C, von Brühl ML, Manukyan D. , et al. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008; 118 (03) 1110-1122
    PubMedSuche in Google Scholar
  • 81 Ruf W, Versteeg HH. Tissue factor mutated at the allosteric Cys186-Cys209 disulfide bond is severely impaired in decrypted procoagulant activity. Blood 2010; 116 (03) 500-501
    PubMedSuche in Google Scholar
  • 82 van den Hengel LG, Kocatürk B, Reitsma PH, Ruf W, Versteeg HH. Complete abolishment of coagulant activity in monomeric disulfide-deficient tissue factor. Blood 2011; 118 (12) 3446-3448
    PubMedSuche in Google Scholar
  • 83 Kothari H, Nayak RC, Rao LV, Pendurthi UR. Cystine 186-cystine 209 disulfide bond is not essential for the procoagulant activity of tissue factor or for its de-encryption. Blood 2010; 115 (21) 4273-4283
    CrossrefPubMedSuche in Google Scholar
  • 84 van den Hengel LG, Osanto S, Reitsma PH, Versteeg HH. Murine tissue factor coagulant activity is critically dependent on the presence of an intact allosteric disulfide. Haematologica 2013; 98 (01) 153-158
    CrossrefPubMedSuche in Google Scholar
  • 85 Zhou B, Hogg PJ, Gräter F. One-way allosteric communication between the two disulfide bonds in tissue factor. Biophys J 2017; 112 (01) 78-86
    CrossrefPubMedSuche in Google Scholar
  • 86 Prasad R, Banerjee S, Sen P. Contribution of allosteric disulfide in the structural regulation of membrane-bound tissue factor-factor VIIa binary complex. J Biomol Struct Dyn 2018; 1-14
    PubMedSuche in Google Scholar
  • 87 Krudysz-Amblo J, Jennings II ME, Knight T, Matthews DE, Mann KG, Butenas S. Disulfide reduction abolishes tissue factor cofactor function. Biochim Biophys Acta 2013; 1830 (06) 3489-3496
    CrossrefPubMedSuche in Google Scholar
  • 88 Wilkinson B, Gilbert HF. Protein disulfide isomerase. Biochim Biophys Acta 2004; 1699 (1-2): 35-44
    CrossrefPubMedSuche in Google Scholar
  • 89 Jasuja R, Furie B, Furie BC. Endothelium-derived but not platelet-derived protein disulfide isomerase is required for thrombus formation in vivo. Blood 2010; 116 (22) 4665-4674
    PubMedSuche in Google Scholar
  • 90 Cho J, Furie BC, Coughlin SR, Furie B. A critical role for extracellular protein disulfide isomerase during thrombus formation in mice. J Clin Invest 2008; 118 (03) 1123-1131
    PubMedSuche in Google Scholar
  • 91 Popescu NI, Lupu C, Lupu F. Extracellular protein disulfide isomerase regulates coagulation on endothelial cells through modulation of phosphatidylserine exposure. Blood 2010; 116 (06) 993-1001
    PubMedSuche in Google Scholar
  • 92 Müller-Calleja N, Ritter S, Hollerbach A, Falter T, Lackner KJ, Ruf W. Complement C5 but not C3 is expendable for tissue factor activation by cofactor-independent antiphospholipid antibodies. Blood Adv 2018; 2 (09) 979-986
    CrossrefPubMedSuche in Google Scholar
  • 93 Rothmeier AS, Marchese P, Langer F. , et al. Tissue factor prothrombotic activity is regulated by integrin-arf6 trafficking. Arterioscler Thromb Vasc Biol 2017; 37 (07) 1323-1331
    CrossrefPubMedSuche in Google Scholar
  • 94 Wang P, Wu Y, Li X, Ma X, Zhong L. Thioredoxin and thioredoxin reductase control tissue factor activity by thiol redox-dependent mechanism. J Biol Chem 2013; 288 (05) 3346-3358
    CrossrefPubMedSuche in Google Scholar
  • 95 Rothmeier AS, Marchese P, Petrich BG. , et al. Caspase-1-mediated pathway promotes generation of thromboinflammatory microparticles. J Clin Invest 2015; 125 (04) 1471-1484
    CrossrefPubMedSuche in Google Scholar
  • 96 Lundström J, Holmgren A. Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. J Biol Chem 1990; 265 (16) 9114-9120
    CrossrefPubMedSuche in Google Scholar
  • 97 Bellisola G, Fracasso G, Ippoliti R. , et al. Reductive activation of ricin and ricin A-chain immunotoxins by protein disulfide isomerase and thioredoxin reductase. Biochem Pharmacol 2004; 67 (09) 1721-1731
    CrossrefPubMedSuche in Google Scholar