Histidine-rich glycoprotein binds DNA and RNA and attenuates their capacity to activate the intrinsic coagulation pathway

Thrombosis and Haemostasis

Volumn 115, Issue 1, 2016, Pages 89-98

  Vu, Trang T ^a,b   Leslie, Beverly A ^a,b   Stafford, Alan R ^a,b   Zhou, Ji ^a,b   Fredenburgh, James C ^a,b   Weitz, Jeffrey I ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Coagulation; DNA; Histidine rich glycoprotein; Intrinsic pathway; RNA

Indexed keywords

BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 11A; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12A; HISTIDINE; KININOGEN; PREKALLIKREIN; THROMBIN; DNA; HIGH MOLECULAR WEIGHT KININOGEN; HISTIDINE-RICH PROTEINS; PROTEIN; PROTEIN BINDING; RNA;

ARTICLE; ASSAY; BLOOD CLOTTING; CLOTTING ASSAY; CONTROLLED STUDY; FACTOR ACTIVATION ASSAY; FLUORESCENCE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; PRIORITY JOURNAL; PROTEIN BINDING; SURFACE PLASMON RESONANCE; THROMBIN GENERATION ASSAY; BINDING COMPETITION; BLOOD; BLOOD CLOTTING TIME; ENZYME ACTIVATION; METABOLISM;

BINDING, COMPETITIVE; BLOOD COAGULATION; DNA; ENZYME ACTIVATION; FACTOR XIA; FACTOR XIIA; HUMANS; KININOGEN, HIGH-MOLECULAR-WEIGHT; PREKALLIKREIN; PROTEIN BINDING; PROTEINS; RNA; SURFACE PLASMON RESONANCE; THROMBIN; WHOLE BLOOD COAGULATION TIME;

EID: 84951304886     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH15-04-0336     Document Type: Article

References (43)

1. Colman RW, Schmaier AH. Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 1997; 90: 3819-3843.
2. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011; 118: 6963-6970.
3. Kannemeier C, Shibamiya A, Nakazawa F, et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci USA 2007; 104: 6388-6393.
4. Gailani D, Renne T. Intrinsic pathway of coagulation and arterial thrombosis. Arterioscler Thromb Vasc Biol 2007; 27: 2507-2513.
5. Muller F, Gailani D, Renne T. Factor XI and XII as antithrombotic targets. Curr Opin Hematol 2011; 18: 349-355.
6. Gailani D, Broze GJ, Jr. Factor XI activation in a revised model of blood coagulation. Science 1991; 253: 909-912.
7. Renne T, Pozgajova M, Gruner S, et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med 2005; 202: 271-281.
8. Wang X, Smith PL, Hsu MY, et al. Effects of factor XI deficiency on ferric chloride-induced vena cava thrombosis in mice. J Thromb Haemost 2006; 4: 1982-1988.
9. Wang X, Cheng Q, Xu L, et al. Effects of factor IX or factor XI deficiency on ferric chloride-induced carotid artery occlusion in mice. J Thromb Haemost 2005; 3: 695-702.
10. Crosby JR, Marzec U, Revenko AS, et al. Antithrombotic effect of antisense factor XI oligonucleotide treatment in primates. Arterioscler Thromb Vasc Biol 2013; 33: 1670-1678.
11. Yau JW, Liao P, Fredenburgh JC, et al. Selective depletion of factor XI or factor XII with antisense oligonucleotides attenuates catheter thrombosis in rabbits. Blood 2014; 123: 2102-2107.
12. Larsson M, Rayzman V, Nolte MW, et al. A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci Transl Med 2014; 6: 222ra17.
13. Renne T, Schmaier AH, Nickel KF, et al. In vivo roles of factor XII. Blood 2012; 120: 4296-4303.
14. Muller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-1156.
15. Brill A, Fuchs TA, Savchenko AS, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012; 10: 136-144.
16. von Bruhl ML, 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: 819-835.
17. Gould TJ, Vu TT, Swystun LL, et al. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms. Arterioscler Thromb Vasc Biol 2014; 34: 1977-1984.
18. Semeraro F, Ammollo CT, Esmon NL, et al. Histones induce phosphatidylserine exposure and a procoagulant phenotype in human red blood cells. J Thromb Haemost 2014; 12: 1697-1702.
19. Semeraro F, Ammollo CT, Morrissey JH, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 2011; 118: 1952-1961.
20. Smith SA, Choi SH, Collins JN, et al. Inhibition of polyphosphate as a novel strategy for preventing thrombosis and inflammation. Blood 2012; 120: 5103-5110.
21. Jain S, Pitoc GA, Holl EK, et al. Nucleic acid scavengers inhibit thrombosis without increasing bleeding. Proc Natl Acad Sci USA 2012; 109: 12938-12943.
22. MacQuarrie JL, Stafford AR, Yau JW, et al. Histidine-rich glycoprotein binds factor XIIa with high affinity and inhibits contact-initiated coagulation. Blood 2011; 117: 4134-4141.
23. Jones AL, Hulett MD, Parish CR. Histidine-rich glycoprotein: A novel adaptor protein in plasma that modulates the immune, vascular and coagulation systems. Immunol Cell Biol 2005; 83: 106-118.
24. Gorgani NN, Smith BA, Kono DH, et al. Histidine-rich glycoprotein binds to DNA and Fc gamma RI and potentiates the ingestion of apoptotic cells by macrophages. J Immunol 2002; 169: 4745-4751.
25. Vu TT, Stafford AR, Leslie BA, et al. Histidine-rich glycoprotein binds fibrin(ogen) with high affinity and competes with thrombin for binding to the gamma’-chain. J Biol Chem 2011; 286: 30314-30323.
26. Leung LL, Harpel PC, Nachman RL, et al. Histidine-rich glycoprotein is present in human platelets and is released following thrombin stimulation. Blood 1983; 62: 1016-1021.
27. Vu TT, Zhou J, Leslie BA, et al. Arterial thrombosis is accelerated in mice deficient in histidine-rich glycoprotein. Blood 2015; 125: 2712-2719.
28. Petrera NS, Stafford AR, Leslie BA, et al. Long range communication between exosites 1 and 2 modulates thrombin function. J Biol Chem 2009; 284: 25620-25629.
29. Kretz CA, Cuddy KK, Stafford AR, et al. HD1, a thrombin-and prothrombinbinding DNA aptamer, inhibits thrombin generation by attenuating prothrombin activation and thrombin feedback reactions. Thromb Haemost 2010; 103: 83-93.
30. Yau JW, Stafford AR, Liao P, et al. Mechanism of catheter thrombosis: comparison of the antithrombotic activities of fondaparinux, enoxaparin, and heparin in vitro and in vivo. Blood 2011; 118: 6667-6674.
31. Swystun LL, Mukherjee S, Liaw PC. Breast cancer chemotherapy induces the release of cell-free DNA, a novel procoagulant stimulus. J Thromb Haemost 2011; 9: 2313-2321.
32. Mandle RJ, Colman RW, Kaplan AP. Identification of prekallikrein and highmolecular-weight kininogen as a complex in human plasma. Proc Natl Acad Sci USA 1976; 73: 4179-4183.
33. Scott CF, Colman RW. Fibrinogen blocks the autoactivation and thrombin-mediated activation of factor XI on dextran sulfate. Proc Natl Acad Sci USA 1992; 89: 11189-11193.
34. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880-15885.
35. de Maat S, van Dooremalen S, de Groot PG, et al. A nanobody-based method for tracking factor XII activation in plasma. Thromb Haemost 2013; 110: 458-468.
36. Gansler J, Jaax M, Leiting S, et al. Structural requirements for the procoagulant activity of nucleic acids. PLoS One 2012; 7: e50399.
37. Pixley RA, Cassello A, De La Cadena RA, et al. Effect of heparin on the activation of factor XII and the contact system in plasma. Thromb Haemost 1991; 66: 540-547.
38. de Agostini A, Lijnen HR, Pixley RA, et al. Inactivation of factor XII active fragment in normal plasma. Predominant role of C-1-inhibitor. J Clin Invest 1984; 73: 1542-1549.
39. Olson ST, Gettins PG. Regulation of proteases by protein inhibitors of the serpin superfamily. Prog Mol Biol Transl Sci 2011; 99: 185-240.
40. Wagenaar-Bos IG, Hack CE. Structure and function of C1-inhibitor. Immunol Allergy Clin North Am 2006; 26: 615-632.
41. Pixley RA, Schmaier A, Colman RW. Effect of negatively charged activating compounds on inactivation of factor XIIa by Cl inhibitor. Arch Biochem Biophys 1987; 256: 490-498.
42. Pixley RA, Schapira M, Colman RW. The regulation of human factor XIIa by plasma proteinase inhibitors. J Biol Chem 1985; 260: 1723-1729.
43. Marx G, Korner G, Mou X, et al. Packaging zinc, fibrinogen, and factor XIII in platelet alpha-granules. J Cell Physiol 1993; 156: 437-442.