Thrombin activatable fibrinolysis inhibitor (TAFI) — A possible link between coagulation and complement activation in the antiphospholipid syndrome (APS)

Thrombosis Research

Volumn 158, Issue , 2017, Pages 168-173

  Grosso, Giorgia ^a   Vikerfors, Anna ^a   Woodhams, Barry ^b   Adam, Mariette ^c   Bremme, Katarina ^a   Holmström, Margareta ^d   Ågren, Anna ^d   Eelde, Anna ^d   Bruzelius, Maria ^d   Svenungsson, Elisabet ^a   Antovic, Aleksandra ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b HaemaCon Ltd   (United Kingdom)

^c Stago Instruments   (France)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Antiphospholipid antibodies; Antiphospholipid syndrome; Arterial thrombosis; Complement C5a; Thrombin activatable fibrinolysis inhibitor (TAFI)

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C5; FIBRINOGEN; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBOMODULIN; COMPLEMENT COMPONENT C5A; FIBRIN; THROMBOPLASTIN;

ADULT; AGED; ANAPHYLAXIS; ANTIPHOSPHOLIPID SYNDROME; ARTERIAL PRESSURE; ARTICLE; BLOOD CLOTTING; BLOOD SAMPLING; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; EUGLOBULIN LYSIS TEST; FEMALE; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MORBIDITY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; QUESTIONNAIRE; TURBIDIMETRY; YOUNG ADULT; BLOOD; COMPLEMENT ACTIVATION; IMMUNOLOGY; METABOLISM;

ADULT; ANTIPHOSPHOLIPID SYNDROME; CARBOXYPEPTIDASE B2; COMPLEMENT ACTIVATION; COMPLEMENT C5A; FEMALE; FIBRIN; HUMANS; MALE; THROMBOPLASTIN;

EID: 85021333476     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2017.06.028     Document Type: Article

References (38)

1. Miyakis, S., Lockshin, M.D., Atsumi, T., Branch, D.W., Brey, R.L., Cervera, R., et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J. Thromb. Haemost. 4:2 (2006), 295–306.
2. Cervera, R., Piette, J.C., Font, J., Khamashta, M.A., Shoenfeld, Y., Camps, M.T., et al. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum. 46:4 (2002), 1019–1027.
3. de Groot, P.G., Derksen, R.H., Pathophysiology of the antiphospholipid syndrome. J. Thromb. Haemost. 3:8 (2005), 1854–1860.
4. Meroni, P.L., Borghi, M.O., Raschi, E., Tedesco, F., Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat. Rev. Rheumatol. 7:6 (2011), 330–339.
5. Pierangeli, S.S., Colden-Stanfield, M., Liu, X., Barker, J.H., Anderson, G.L., Harris, E.N., Antiphospholipid antibodies from antiphospholipid syndrome patients activate endothelial cells in vitro and in vivo. Circulation, 99(15), 1999, 1997.
6. Pierangeli, S.S., Girardi, G., Vega-Ostertag, M., Liu, X., Espinola, R.G., Salmon, J., Requirement of activation of complement C3 and C5 for antiphospholipid antibody-mediated thrombophilia. Arthritis Rheum. 52:7 (2005), 2120–2124.
7. Pierangeli, S.S., Vega-ostertag, M., Liu, X., Girardi, G., Complement activation: a novel pathogenic mechanism in the antiphospholipid syndrome. Ann. N. Y. Acad. Sci. 1051:1 (2005), 413–420.
8. Girardi, G., Berman, J., Redecha, P., Spruce, L., Thurman, J.M., Kraus, D., et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J. Clin. Investig. 112:11 (2003), 1644–1654.
9. Salmon, J.E., Girardi, G., Holers, V.M., Complement activation as a mediator of antiphospholipid antibody induced pregnancy loss and thrombosis. Ann. Rheum. Dis., 61(Suppl. 2), 2002, ii46.
10. Salmon, J.E., Girardi, G., Lockshin, M.D., The antiphospholipid syndrome as a disorder initiated by inflammation: implications for the therapy of pregnant patients. Nat. Clin. Pract. Rheumatol. 3:3 (2007), 140–147 (quiz 1 pp. following 87).
11. Avalos, I., Tsokos, G.C., The role of complement in the antiphospholipid syndrome-associated pathology. Clin Rev Allergy Immunol 36:2–3 (2009), 141–144.
12. Cavazzana, I., Nebuloni, M., Cetin, I., Acaia, B., Saino, S., Borghi, M.O., et al. Complement activation in anti-phospholipid syndrome: a clue for an inflammatory process?. J. Autoimmun. 28:2–3 (2007), 160–164.
13. Oku, K., Amengual, O., Atsumi, T., Pathophysiology of thrombosis and pregnancy morbidity in the antiphospholipid syndrome. Eur. J. Clin. Investig. 42:10 (2012), 1126–1135.
14. Oku, K., Atsumi, T., Bohgaki, M., Amengual, O., Kataoka, H., Horita, T., et al. Complement activation in patients with primary antiphospholipid syndrome. Ann. Rheum. Dis. 68:6 (2009), 1030–1035.
15. Shapira, I., Andrade, D., Allen, S.L., Salmon, J.E., Brief report: induction of sustained remission in recurrent catastrophic antiphospholipid syndrome via inhibition of terminal complement with eculizumab. Arthritis Rheum. 64:8 (2012), 2719–2723.
16. Campbell, W.D., Lazoura, E., Okada, N., Okada, H., Inactivation of C3a and C5a octapeptides by carboxypeptidase R and carboxypeptidase N. Microbiol. Immunol. 46:2 (2002), 131–134.
17. Bajzar, L., Morser, J., Nesheim, M., TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J. Biol. Chem., 271(28), 1996, 16603.
18. Foley, J.H., Kim, P.Y., Mutch, N.J., Gils, A., Insights into thrombin activatable fibrinolysis inhibitor function and regulation. J. Thromb. Haemost. 11:Suppl. 1 (2013), 306–315.
19. Colucci, M., Semeraro, N., Thrombin activatable fibrinolysis inhibitor: at the nexus of fibrinolysis and inflammation. Thromb. Res. 129:3 (2012), 314–319.
20. He, S., Cao, H., Antovic, A., Blombäck, M., Modifications of flow measurement to determine fibrin gel permeability and the preliminary use in research and clinical materials. Blood Coagul. Fibrinolysis, 16(1), 2005, 61.
21. Vikerfors, A., Svenungsson, E., Agren, A., Mobarrez, F., Bremme, K., Holmstrom, M., et al. Studies of fibrin formation and fibrinolytic function in patients with the antiphospholipid syndrome. Thromb. Res. 133:5 (2014), 936–944.
22. Carter, A.M., Cymbalista, C.M., Spector, T.D., Grant, P.J., Euro, C.I., Heritability of clot formation, morphology, and lysis: the EuroCLOT study. Arterioscler. Thromb. Vasc. Biol. 27:12 (2007), 2783–2789.
23. Devreese, K.M., Antiphospholipid antibodies: evaluation of the thrombotic risk. Thromb. Res. 130:Suppl. 1 (2012), S37–S40.
24. Ames, P.R., Antinolfi, I., Ciampa, A., Batuca, J., Scenna, G., Lopez, L.R., et al. Primary antiphospholipid syndrome: a low-grade auto-inflammatory disease?. Rheumatology (Oxford) 47:12 (2008), 1832–1837.
25. de Groot, P.G., Urbanus, R.T., Antiphospholipid syndrome-not a noninflammatory disease. Semin. Thromb. Hemost. 41:6 (2015), 607–614.
26. Ritis, K., Doumas, M., Mastellos, D., Micheli, A., Giaglis, S., Magotti, P., et al. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J. Immunol. 177:7 (2006), 4794–4802.
27. Romay-Penabad, Z., Liu, X.X., Montiel-Manzano, G., De Martinez, E.P., Pierangeli, S.S., C5a receptor-deficient mice are protected from thrombophilia and endothelial cell activation induced by some antiphospholipid antibodies. (Author abstract) (Report) Ann. N. Y. Acad. Sci., 1108, 2007, 554.
28. Meroni, P.L., Macor, P., Durigutto, P., De Maso, L., Gerosa, M., Ferraresso, M., et al. Complement activation in antiphospholipid syndrome and its inhibition to prevent rethrombosis after arterial surgery. Blood 127:3 (2016), 365–367.
29. Heylen, E., Willemse, J., Hendriks, D., An update on the role of carboxypeptidase U (TAFIa) in fibrinolysis. Front. Biosci., 16, 2011, 2427 (Landmark edition).
30. Tregouet, D.A., Schnabel, R., Alessi, M.C., Godefroy, T., Declerck, P.J., Nicaud, V., et al. Activated thrombin activatable fibrinolysis inhibitor levels are associated with the risk of cardiovascular death in patients with coronary artery disease: the AtheroGene study. J. Thromb. Haemost. 7:1 (2009), 49–57.
31. Martinez-Zamora, M.A., Tassies, D., Carmona, F., Espinosa, G., Cervera, R., Reverter, J.C., et al. Original article: thrombin activatable fibrinolysis inhibitor and clot lysis time in pregnant patients with antiphospholipid syndrome: relationship with pregnancy outcome and thrombosis. Am. J. Reprod. Immunol. 62:6 (2009), 381–389.
32. Martínez-Zamora, M.A., Tassies, D., Carmona, F., Espinosa, G., Cervera, R., Reverter, J.C., et al. Clot lysis time and thrombin activatable fibrinolysis inhibitor in severe preeclampsia with or without associated antiphospholipid antibodies. J. Reprod. Immunol. 86:2 (2010), 133–140.
33. Giannakopoulos, B., Krilis, S.A., The pathogenesis of the antiphospholipid syndrome. N. Engl. J. Med. 368:11 (2013), 1033–1044.
34. Amaya-Amaya, J., Rojas-Villarraga, A., Anaya, J.-M., Cardiovascular disease in the antiphospholipid syndrome. Lupus 23:12 (2014), 1288–1291.
35. Martin, F.A., Murphy, R.P., Cummins, P.M., Thrombomodulin and the vascular endothelium: insights into functional, regulatory, and therapeutic aspects. Am. J. Physiol. Heart Circ. Physiol. 304:12 (2013), H1585–H1597.
36. Andreoli, L., Chighizola, C.B., Banzato, A., Pons-estel, G.J., Jesus, G.R., Erkan, D., Estimated frequency of antiphospholipid antibodies in patients with pregnancy morbidity, stroke, myocardial infarction, and deep vein thrombosis: a critical review of the literature. Arthritis Care Res. 65:11 (2013), 1869–1873.
37. Ambrosino, P., Lupoli, R., Di Minno, A., Iervolino, S., Peluso, R., Di Minno, M.N., Markers of cardiovascular risk in patients with antiphospholipid syndrome: a meta-analysis of literature studies. Ann. Med. 46:8 (2014), 693–702.
38. Matyja-Bednarczyk, A., Swadzba, J., Iwaniec, T., Sanak, M., Dziedzina, S., Cmiel, A., et al. Risk factors for arterial thrombosis in antiphospholipid syndrome. Thromb. Res. 133:2 (2014), 173–176.