Extracellular histones promote thrombin generation through platelet-dependent mechanisms: Involvement of platelet TLR2 and TLR4

Blood

Volumn 118, Issue 7, 2011, Pages 1952-1961

  Semeraro, Fabrizio ^a   Ammollo, Concetta T ^a   Morrissey, James H ^b,c   Dale, George L ^d   Friese, Paul ^d   Esmon, Naomi L ^a,d   Esmon, Charles T ^a,d,e  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 5A; HEPARIN; HISTONE; MONOCLONAL ANTIBODY; PADGEM PROTEIN; PHOSPHATASE; PHOSPHATIDYLSERINE; POLYPHOSPHATE; THROMBIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANTIGEN PRESENTING CELL; ARTICLE; AUTOMATED THROMBINOGRAPHY; AUTOMATION; BLOOD CLOTTING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RICH PLASMA;

EID: 80051884192     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-03-343061     Document Type: Article

References (51)

1. Jahr S., Hentze H., Englisch S., et al. DNA fragments in the blood plasma of cancer patients: Quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001; 61(4):1659-1665. (Pubitemid 34292602)
2. Brinkmann V., Laube B., Abu Abed U., et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535. (Pubitemid 38314426)
3. Von Köckritz-Blickwede M., Goldmann O., Thulin P., et al. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood. 2008;111(6):3070-3080.
4. Holdenrieder S., Stieber P. Clinical use of circulating nucleosomes. Crit Rev Clin Lab Sci. 2009; 46(1):1-24.
5. Zeerleder S., Zwart B., Wuillemin W.A., et al. Elevated nucleosome levels in systemic inflammation and sepsis. Crit Care Med. 2003;31(7):1947- 1951.
6. Kawasaki H., Iwamuro S. Potential roles of histones in host defense as antimicrobial agents. Infect Disord Drug Targets. 2008;8(3):195-205.
7. Kleine T.J., Gladfelter A., Lewis P.N., Lewis S.A. Histone-induced damage of a mammalian epithelium: The conductive effect. Am J Physiol. 1995; 268(5):C1114-C1125.
8. Xu J., Zhang X., Pelayo R., et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318-1321.
9. Fuchs T.A., Brill A., Duerschmied D., et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci U S A. 2010;107(36):15880-15885.
10. Elzey B.D., Tian J., Jensen R.J., et al. Platelet-mediated modulation of adaptive immunity.Acommunication link between innate and adaptive immune compartments. Immunity. 2003;19(1):9-19. (Pubitemid 36859897)
11. Semple J.W., Freedman J. Platelets and innate immunity. Cell Mol Life Sci. 2010;67(4):499-511.
12. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805- 820.
13. Shiraki R., Inoue N., Kawasaki S., et al. Expression of Toll-like receptors on human platelets. Thromb Res. 2004;113(6):379-385. (Pubitemid 38844368)
14. Cognasse F., Hamzeh H., Chavarin P., et al. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol. 2005;83(2):196-198. (Pubitemid 40469328)
15. Blair P., Rex S., Vitseva O., et al. Stimulation of Tolllike receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ Res. 2009; 104(3):346-354.
16. Zhang G., Han J., Welch E.J., et al. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. 2009;182(12):7997-8004.
17. Andonegui G., Kerfoot S.M., McNagny K., et al. Platelets express functional Toll-like receptor-4. Blood. 2005;106(7):2417-2423. (Pubitemid 41510815)
18. Aslam R., Speck E.R., Kim M., et al. Platelet Toll-like receptor expression modulates lipopolysaccharide- induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood. 2006; 107(2):637-641. (Pubitemid 43076388)
19. Xu J., Zhang X., Monestier M., Esmon N.L., Esmon C.T. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury [published online ahead of print July 22, 2011]. J Immunol. doi: 10.4049/jimmunol.1003930.
20. Smirnov M.D., Esmon C.T. Phosphatidylethanolamine incorporation into vesicles selectively enhances factor Va inactivation by activated protein C. J Biol Chem. 1994;269(2):816-819. (Pubitemid 24032448)
21. Esmon C.T., Esmon N.L., Le Bonniec B.F., Johnson A.E. Protein C activation. Meth Enzymol. 1993;222:359-385. (Pubitemid 23303245)
22. Alberio L., Safa O., Clemetson K.J., Esmon C.T., Dale G.L. Surface expression and functional characterization of α-granule factor V in human platelets: Effects of ionophore A23187, thrombin, collagen, and convulxin. Blood. 2000;95(5):1694-1702. (Pubitemid 30120831)
23. Hemker H.C., Al Dieri R., De Smedt E., Beguin S. Thrombin generation, a function test of the haemostatic- thrombotic system. Thromb Haemost. 2006;96(5):553-561. (Pubitemid 44782533)
24. Luddington R., Baglin T. Clinical measurement of thrombin generation by calibrated automated thrombography requires contact factor inhibition. J Thromb Haemost. 2004;2(11):1954-1959. (Pubitemid 40192749)
25. Bäck J., Lang M.H., Elgue G., et al. Distinctive regulation of contact activation by antithrombin and C1-inhibitor on activated platelets and material surfaces. Biomaterials. 2009;30(34):6573-6580.
26. Panes O., Matus V., Sáez C.G., et al. Human platelets synthesize and express functional tissue factor. Blood. 2007;109(12):5242-5250. (Pubitemid 46890544)
27. Smith S.A., Mutch N.J., Baskar D., et al. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci U S A. 2006;103(4):903- 908.
28. Müller F., Mutch N.J., Schenk W.A., et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009;139(6): 1143-1156.
29. Pal P.K., Starr T., Gertler M.M. Neutralization of heparin by histone and its subfractions. Thromb Res. 1983;31(1):69-79. (Pubitemid 13035236)
30. Mosnier L.O. Platelet factor 4 inhibits thrombomodulin- dependent activation of thrombinactivatable fibrinolysis inhibitor (TAFI) by thrombin. J Biol Chem. 2011;286(1):502-510.
31. Gerotziafas G.T., Depasse F., Busson J., et al. Towards a standardization of thrombin generation assessment: The influence of tissue factor, platelets and phospholipids concentration on the normal values of Thrombogram- Thrombinoscope assay. Thromb J. 2005;3:16.
32. Vanschoonbeek K., Feijge M.A., Van Kampen R.J., et al. Initiating and potentiating role of platelets in tissue factor-induced thrombin generation in the presence of plasma: Subject-dependent variation in thrombogram characteristics. J Thromb Haemost. 2004;2(3):476-484. (Pubitemid 40185661)
33. Bouchard B.A., Mann K.G., Butenas S. No evidence for tissue factor on platelets. Blood. 2010;116(5): 854-855.
34. Ratnoff O.D., Busse R.J., Sheon R.P. The demise of John Hageman. N Engl J Med. 1968;279(14): 760-761.
35. Renné T., Pozgajová M., Grüner S., et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202(2):271-281. (Pubitemid 41043823)
36. Kannemeier C., Shibamiya A., Nakazawa F., et al. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A. 2007;104(15):6388-6393. (Pubitemid 47186104)
37. Smith S.A., Choi S.H., Davis-Harrison R., et al. Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood. 2010; 116(20):4353-4359.
38. André P. P-selectin in haemostasis. Br J Haematol. 2004;126(3):298-306. (Pubitemid 39005709)
39. Ohashi K., Burkart V., Flohé S., Kolb H. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J Immunol. 2000;164(2):558-561. (Pubitemid 30043672)
40. Asea A., Rehli M., Kabingu E., et al. Novel signal transduction pathway utilized by extracellular HSP70: Role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem. 2002;277(17):15028-15034. (Pubitemid 34952579)
41. Park J.S., Svetkauskaite D., He Q., et al. Involvement of Toll like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem. 2004;279(9):7370-7377. (Pubitemid 38294612)
42. Klune J.R., Dhupar R., Cardinal J., Billiar T.R., Tsung A. HMGB1: Endogenous danger signaling. Mol Med. 2008;14(7-8):476-484.
43. Park J.S., Gamboni-Robertson F., He Q., et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol. 2006;290(3):C917-C924.
44. Termeer C., Benedix F., Sleeman J., et al. Oligosaccharides of hyaluronan activate dendritic cells via Toll-like receptor 4. J Exp Med. 2002;195(1): 99-111. (Pubitemid 34074500)
45. Johnson G.B., Brunn G.J., Kodaira Y., Platt J.L. Receptor- mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Tolllike receptor 4. J Immunol. 2002;168(10):5233- 5239.
46. Smiley S.T., King J.A., Hancock W.W. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol. 2001; 167(5):2887-2894. (Pubitemid 32768923)
47. Biragyn A., Ruffini P.A., Leifer C.A., et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science. 2002;298(5595): 1025-1029. (Pubitemid 35247310)
48. Karikó K., Ni H., Capodici J., Lamphier M., Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem. 2004;279(13): 12542-12550. (Pubitemid 38445825)
49. Leadbetter E.A., Rifkin I.R., Hohlbaum A.M., et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 2002;416(6881):603-607. (Pubitemid 34406754)
50. Barrat F.J., Meeker T., Gregorio J., et al. Nucleic acids of mammalian origin can act as endogenous ligands for toll-like receptors and may promote systemic lupus erythematosus. J Exp Med. 2005;202(8):1131-1139. (Pubitemid 41464506)
51. Zeerleder S., Zwart B., te Velthuis H., et al. Nucleosome- releasing factor: A new role for factor VIIactivating protease (FSAP). FASEB J. 2008; 22(12):4077-4084.