Complement Activation in Arterial and Venous Thrombosis is Mediated by Plasmin

EBioMedicine

Volumn 5, Issue , 2016, Pages 175-182

  Foley, Jonathan H ^a,b,c   Walton, Bethany L ^d   Aleman, Maria M ^d   O'Byrne, Alice M ^a   Lei, Victor ^a   Harrasser, Micaela ^b   Foley, Kimberley A ^e   Wolberg, Alisa S ^d   Conway, Edward M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c ROYAL FREE LONDON NHS FOUNDATION TRUST   (United Kingdom)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e QUEEN S UNIVERSITY   (Canada)

Author keywords

Complement; Fibrinolysis; Leukocytes; Thrombin; Thrombosis

Indexed keywords

COMPLEMENT; FERRIC CHLORIDE; PLASMIN; PROTHROMBIN; ANTITHROMBIN III; ANTITHROMBIN III-PROTEASE COMPLEX; BLOOD CLOTTING FACTOR 10A; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A; COMPLEMENT MEMBRANE ATTACK COMPLEX; PEPTIDE HYDROLASE; PLASMINOGEN ACTIVATOR; THROMBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY THROMBOSIS; ARTICLE; BLOOD FLOW; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMOLYSIS; INFERIOR CAVA VEIN; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VEIN THROMBOSIS; ANIMAL; ARTERY; BIOSYNTHESIS; COMPLEMENT ACTIVATION; DRUG EFFECT; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; ANTITHROMBIN III; ARTERIES; COMPLEMENT ACTIVATION; COMPLEMENT C3A; COMPLEMENT C5A; COMPLEMENT MEMBRANE ATTACK COMPLEX; FACTOR XA; FIBRINOLYSIN; HUMANS; MICE; PEPTIDE HYDROLASES; PLASMINOGEN ACTIVATORS; THROMBIN; VENOUS THROMBOSIS;

EID: 84957613158     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2016.02.011     Document Type: Article

References (46)

1. Aleman M.M., Walton B.L., Byrnes J.R., et al. Elevated prothrombin promotes venous, but not arterial, thrombosis in mice. Arterioscler. Thromb. Vasc. Biol. 2013, 33(8):1829-1836.
2. Amara U., Flierl M.A., Rittirsch D., et al. Molecular intercommunication between the complement and coagulation systems. J. Immunol. 2010, 185(9):5628-5636.
3. APEX AMI Investigators, Armstrong P.W., Granger C.B., et al. Pexelizumab for acute ST-elevation myocardial infarction in patients undergoing primary percutaneous coronary intervention: a randomized controlled trial. JAMA 2007, 297(1):43-51.
4. Auger J.L., Haasken S., Binstadt B.A. Autoantibody-mediated arthritis in the absence of C3 and activating Fcgamma receptors: C5 is activated by the coagulation cascade. Arthritis Res. Ther. 2012, 14(6):R269.
5. Barthel D., Schindler S., Zipfel P.F. Plasminogen is a complement inhibitor. J. Biol. Chem. 2012, 287(22):18831-18842.
6. Bennett W.R., Yawn D.H., Migliore P.J., et al. Activation of the complement system by recombinant tissue plasminogen activator. J. Am. Coll. Cardiol. 1987, 10(3):627-632.
7. Borkowska S., Suszynska M., Mierzejewska K., et al. Novel evidence that crosstalk between the complement, coagulation, and fibrinolysis proteolytic cascades is involved in mobilization of hematopoietic stem/progenitor cells (HSPCs). Leukemia 2014.
8. Brummel K.E., Paradis S.G., Butenas S., Mann K.G. Thrombin functions during tissue factor-induced blood coagulation. Blood 2002, 100(1):148-152.
9. Brummel-Ziedins K.E., Vossen C.Y., Butenas S., Mann K.G., Rosendaal F.R. Thrombin generation profiles in deep venous thrombosis. J. Thromb. Haemost. 2005, 3(11):2497-2505.
10. Cheung A.K., Faezi-Jenkin B., Leypoldt J.K. Effect of thrombosis on complement activation and neutrophil degranulation during in vitro hemodialysis. J. Am. Soc. Nephrol. 1994, 5(1):110-115.
11. Dielis A.W., Castoldi E., Spronk H.M., et al. Coagulation factors and the protein C system as determinants of thrombin generation in a normal population. J. Thromb. Haemost. 2008, 6(1):125-131.
12. Distelmaier K., Adlbrecht C., Jakowitsch J., et al. Local complement activation triggers neutrophil recruitment to the site of thrombus formation in acute myocardial infarction. Thromb. Haemost. 2009, 102(3):564-572.
13. Engelmann B., Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol. 2013, 13(1):34-45.
14. Fuchs T.A., Brill A., Wagner D.D. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32(8):1777-1783.
15. Hamilton K.K., Hattori R., Esmon C.T., Sims P.J. Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J. Biol. Chem. 1990, 265(7):3809-3814.
16. Horrevoets A.J., Pannekoek H., Nesheim M.E. A steady-state template model that describes the kinetics of fibrin-stimulated [Glu1]- and [Lys78]plasminogen activation by native tissue-type plasminogen activator and variants that lack either the finger or kringle-2 domain. J. Biol. Chem. 1997, 272(4):2183-2191.
17. Hoth J.J., Wells J.D., Jones S.E., Yoza B.K., McCall C.E. Complement mediates a primed inflammatory response after traumatic lung injury. J. Trauma Acute Care Surg. 2014, 76(3):601-608. (discussion 8-9).
18. Howes J.M., Richardson V.R., Smith K.A., et al. Complement C3 is a novel plasma clot component with anti-fibrinolytic properties. Diab. Vasc. Dis. Res. 2012, 9(3):216-225.
19. Huber-Lang M., Sarma J.V., Zetoune F.S., et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 2006, 12(6):682-687.
20. Kessel C., Nandakumar K.S., Peters F.B., Gauba V., Schultz P.G., Holmdahl R. A single functional group substitution in c5a breaks B cell and T cell tolerance and protects against experimental arthritis. Arthritis Rheum. 2014, 66(3):610-621.
21. Khan M.A., Maasch C., Vater A., et al. Targeting complement component 5a promotes vascular integrity and limits airway remodeling. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(15):6061-6066.
22. Krisinger M.J., Goebeler V., Lu Z., et al. Thrombin generates previously unidentified C5 products that support the terminal complement activation pathway. Blood 2012, 120(8):1717-1725.
23. Kyrle P.A., Mannhalter C., Beguin S., et al. Clinical studies and thrombin generation in patients homozygous or heterozygous for the G20210A mutation in the prothrombin gene. Arterioscler. Thromb. Vasc. Biol. 1998, 18(8):1287-1291.
24. 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.
25. Machlus K.R., Cardenas J.C., Church F.C., Wolberg A.S. Causal relationship between hyperfibrinogenemia, thrombosis, and resistance to thrombolysis in mice. Blood 2011, 117(18):4953-4963.
26. Machlus K.R., Lin F.C., Wolberg A.S. Procoagulant activity induced by vascular injury determines contribution of elevated factor VIII to thrombosis and thrombus stability in mice. Blood 2011, 118(14):3960-3968.
27. Mozaffarian D., Benjamin E.J., Go A.S., et al. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation 2015, 131(4):e29-322.
28. Oikonomopoulou K., Ricklin D., Ward P.A., Lambris J.D. Interactions between coagulation and complement-their role in inflammation. Semin. Immunopathol. 2012, 34(1):151-165.
29. 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. 2005, 52(7):2120-2124.
30. Raskob G.E., Angchaisuksiri P., Blanco A.N., et al. Thrombosis: a major contributor to global disease burden. Arterioscler. Thromb. Vasc. Biol. 2014, 34(11):2363-2371.
31. Rawal N., Pangburn M.K. C5 convertase of the alternative pathway of complement. Kinetic analysis of the free and surface-bound forms of the enzyme. J. Biol. Chem. 1998, 273(27):16828-16835.
32. Rawal N., Pangburn M. Formation of high-affinity C5 convertases of the alternative pathway of complement. J. Immunol. 2001, 166(4):2635-2642.
33. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010, 11(9):785-797.
34. Salmon J.E., Girardi G., Holers V.M. Complement activation as a mediator of antiphospholipid antibody induced pregnancy loss and thrombosis. Ann. Rheum. Dis. 2002, 61(Suppl. 2):ii46-ii50.
35. Sims P.J., Faioni E.M., Wiedmer T., Shattil S.J. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J. Biol. Chem. 1988, 263(34):18205-18212.
36. van den Eijnden-Schrauwen Y., Kooistra T., de Vries R.E., Emeis J.J. Studies on the acute release of tissue-type plasminogen activator from human endothelial cells in vitro and in rats in vivo: evidence for a dynamic storage pool. Blood 1995, 85(12):3510-3517.
37. von Bruhl M.L., Stark K., Steinhart A., et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med. 2012, 209(4):819-835.
38. Wada K., Takahashi H., Tatewaki W., Takizawa S., Shibata A. Plasmin-a2-plasmin inhibitor complex in plasma of patients with thromboembolic diseases. Thromb. Res. 1989, 56(6):661-665.
39. Wakefield T.W., Myers D.D., Henke P.K. Mechanisms of venous thrombosis and resolution. Arterioscler. Thromb. Vasc. Biol. 2008, 28(3):387-391.
40. Wat J., Foley J.H., Krisinger M.J., et al. Polyphosphate suppresses complement via the terminal pathway. Blood 2014, 123(5):768-776.
41. Wiedmer T., Esmon C.T., Sims P.J. Complement proteins C5b-9 stimulate procoagulant activity through platelet prothrombinase. Blood 1986, 68(4):875-880.
42. Wiggins R.C., Giclas P.C., Henson P.M. Chemotactic activity generated from the fifth component of complement by plasma kallikrein of the rabbit. J. Exp. Med. 1981, 153(6):1391-1404.
43. Wolberg A.S., Aleman M.M., Leiderman K., Machlus K.R. Procoagulant activity in hemostasis and thrombosis: Virchow's triad revisited. Anesth. Analg. 2012, 114(2):275-285.
44. Wong E.K., Kavanagh D. Anticomplement C5 therapy with eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria and atypical hemolytic uremic syndrome. Transl. Res. 2015, 165(2):306-320.
45. Yan C., Gao H. New insights for C5a and C5a receptors in sepsis. Front. Immunol. 2012, 3:368.
46. Zecher D., Cumpelik A., Schifferli J.A. Erythrocyte-derived microvesicles amplify systemic inflammation by thrombin-dependent activation of complement. Arterioscler. Thromb. Vasc. Biol. 2014, 34(2):313-320.