Histones link inflammation and thrombosis through the induction of Weibel–Palade body exocytosis

Journal of Thrombosis and Haemostasis

Volumn 14, Issue 11, 2016, Pages 2274-2286

  Michels, A ^a   Albanez S ^a   Mewburn, J ^b   Nesbitt, K ^a   Gould, T J ^c   Liaw, P C ^d   James, P D ^a   Swystun, L L ^a   Lillicrap, D ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

Author keywords

endothelial cells; histones; inflammation; von Willebrand factor; Weibel Palade bodies

Indexed keywords

DNA; HISTONE; PATHOGEN ASSOCIATED MOLECULAR PATTERN; ARGININE; CASPASE; LYSINE;

ADOLESCENT; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; C57BL 6 MOUSE; CHILD; CONTROLLED STUDY; ENDOTHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTOPENIA; THROMBOSIS; VERY ELDERLY; WEIBEL PALADE BODY; ANIMAL; C57BL MOUSE; CHEMISTRY; METABOLISM; PATHOLOGY; THROMBOCYTE ADHESION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ARGININE; CASPASES; DNA; ENDOTHELIAL CELLS; EXOCYTOSIS; HISTONES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; LYSINE; MICE; MICE, INBRED C57BL; PLATELET ADHESIVENESS; THROMBOSIS; WEIBEL-PALADE BODIES;

EID: 84995812295     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13493     Document Type: Article

References (50)

1. Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev 2013; 13: 34–45.
2. Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 2012; 189: 2689–95.
3. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880–5.
4. Pisetsky DS. The effectors of innate immunity: DAMPs, DAMEs, or DIMEs? Arthritis Res Ther 2013; 15: 123–5.
5. Mitchell JA, Ryffel B, Quesniaux VF, Cartwright N, Paul-Clark M. Role of pattern-recognition receptors in cardiovascular health and disease. Biochem Soc Trans 2007; 35: 1449–52.
6. Oehmcke S, Morgelin M, Herwald H. Activation of the human contact system on neutrophil extracellular traps. J Innate Immun 2009; 1: 225–30.
7. Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost 2011; 9: 1795–803.
8. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, Esmon CT. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 2011; 118: 1952–61.
9. Gould TJ, Vu TT, Swystun LL, Dwivedi DJ, Mai SH, Weitz JI, Liaw PC. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms. Arterioscler Thromb Vasc Biol 2014; 34: 1977–84.
10. Longstaff C, Varju I, Sotonyi P, Szabo L, Krumrey M, Hoell A, Bota A, Varga Z, Komorowicz E, Kolev K. Mechanical stability and fibrinolytic resistance of clots containing fibrin, DNA, and histones. J Biol Chem 2013; 288: 6946–56.
11. Yang X, Li L, Liu J, Lv B, Chen F. Extracellular histones induce tissue factor expression in vascular endothelial cells via TLR and activation of NF-κB and AP-1. Thromb Res 2016; 137: 211–18.
12. Mayadas T, Wagner DD, Simpson PJ. von Willebrand factor biosynthesis and partitioning between constitutive and regulated pathways of secretion after thrombin stimulation. Blood 1989; 73: 706–11.
13. Pinsky DJ, Naka Y, Liao H, Oz MC, Wagner DD, Mayadas TN, Johnson RC, Hynes RO, Heath M, Lawson CA, Stern DM. Hypoxia-induced exocytosis of endothelial cell Weibel–Palade bodies: a mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest 1996; 97: 493–500.
14. Ruggeri ZM. von Willebrand factor. J Clin Invest 1997; 100: S41–6.
15. Petri B, Broermann A, Li H, Khandoga AG, Zarbock A, Krombach F, Goerge T, Schneider SW, Jones C, Nieswandt B, Wild MK, Vestweber D. von Willebrand factor promotes leukocyte extravasation. Blood 2010; 116: 4712–19.
16. Koster T, Blann AD, Briet E, Vandenbroucke JP, Rosendaal FR. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet 1995; 345: 152–5.
17. Morange PE, Simon C, Alessi MC, Luc G, Arveiler D, Ferrieres J, Amouyel P, Evans A, Ducimetiere P, Juhan-Vague I; PRIME Study Group. Endothelial cell markers and the risk of coronary heart disease: the Prospective Epidemiological Study of Myocardial Infarction (PRIME) study. Circulation 2004; 109: 1343–8.
18. Ward CM, Tetaz TJ, Andrews RK, Berndt MC. Binding of the von Willebrand factor A1 domain to histone. Thromb Res 1997; 86: 469–77.
19. Carestia A, Rivadeneyra L, Romaniuk MA, Fondevila C, Negrotto S, Schattner M. Functional responses and molecular mechanisms involved in histone-mediated platelet activation. Thromb Haemost 2013; 110: 1035–45.
20. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood 2011; 118: 3708–14.
21. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012; 10: 136–44.
22. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, Taylor FB, Esmon NL, Lupu F, Esmon CT. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318–21.
23. Nishimura S, Manabe I, Nagasaki M, Kakuta S, Iwakura Y, Takayama N, Ooehara J, Otsu M, Kamiya A, Petrich BG, Urano T, Kadono T, Sato S, Aiba A, Yamashita H, Sugiura S, Kadowaki T, Nakauchi H, Eto K, Nagai R. In vivo imaging visualizes discoid platelet aggregations without endothelium disruption and implicates contribution of inflammatory cytokine and integrin signaling. Blood 2012; 119: e45–56.
24. Darbousset R, Delierneux C, Mezouar S, Hego A, Lecut C, Guillaumat I, Riederer MA, Evans RJ, Dignat-George F, Panicot-Dubois L, Oury C, Dubois C. P2X1 expressed on polymorphonuclear neutrophils and platelets is required for thrombosis in mice. Blood 2014; 124: 2575–85.
25. Starke RD, Ferraro F, Paschalaki KE, Dryden NH, McKinnon TA, Sutton RE, Payne EM, Haskard DO, Hughes AD, Cutler DF, Laffan MA, Randi AM. Endothelial von Willebrand factor regulates angiogenesis. Blood 2011; 117: 1071–80.
26. Martin-Ramirez J, Hofman M, van den Biggelaar M, Hebbel RP, Voorberg J. Establishment of outgrowth endothelial cells from peripheral blood. Nat Protoc 2012; 7: 1709–15.
27. Bernardo A, Ball C, Nolasco L, Choi H, Moake JL, Dong JF. Platelets adhered to endothelial cell-bound ultra-large von Willebrand factor strings support leukocyte tethering and rolling under high shear stress. J Thromb Haemost 2005; 3: 562–70.
28. Albánez S, Ogiwara K, Michels A, Grabell J, James PD, Lillicrap D. Aging and ABO blood type influence VWF and FVIII levels through interrelated mechanisms. J Thromb Haemost 2016; 14: 953–63.
29. Dwivedi DJ, Toltl LJ, Swystun LL, Pogue J, Liaw KL, Weitz JI, Cook DJ, Fox-Robichaud AE, Liaw PC; Canadian Critical Care Translational Biology Group. Prognostic utility and characterization of cell-free DNA in patients with severe sepsis. Crit Care 2012; 16: R151.
30. Pruss CM, Golder M, Bryant A, Hegadorn C, Haberichter S, Lillicrap D. Use of a mouse model to elucidate the phenotypic effects of the von Willebrand factor cleavage mutants, Y1605A/M1606A and R1597W. J Thromb Haemost 2012; 10: 940–50.
31. Demers M, Krause DS, Schatzberg D, Martinod K, Voorhees JR, Fuchs TA, Scadden DT, Wagner DD. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci USA 2012; 109: 13076–81.
32. Cleator JH, Zhu WQ, Vaughan DE, Hamm HE. Differential regulation of endothelial exocytosis of P-selectin and von Willebrand factor by protease-activated receptors and cAMP. Blood 2006; 107: 2736–44.
33. Wang JW, Valentijn JA, Valentijn KM, Dragt BS, Voorberg J, Reitsma PH, Eikenboom J. Formation of platelet-binding von Willebrand factor strings on non-endothelial cells. J Thromb Haemost 2012; 10: 2168–78.
34. Abrams ST, Zhang N, Manson J, Liu T, Dart C, Baluwa F, Wang SS, Brohi K, Kipar A, Yu W, Wang G, Toh CH. Circulating histones are mediators of trauma-associated lung injury. Am J Respir Crit Care Med 2013; 187: 160–9.
35. Fish RJ, Yang H, Viglino C, Schorer R, Dunoyer-Geindre S, Kruithof EK. Fluvastatin inhibits regulated secretion of endothelial cell von Willebrand factor in response to diverse secretagogues. Biochem J 2007; 405: 597–604.
36. De Meyer SF, Savchenko AS, Haas MS, Schatzberg D, Carroll MC, Schiviz A, Dietrich B, Rottensteiner H, Scheiflinger F, Wagner DD. Protective anti-inflammatory effect of ADAMTS13 on myocardial ischemia/reperfusion injury in mice. Blood 2012; 120: 5217–23.
37. Mayadas TN, Johnson RC, Rayburn H, Hynes RO, Wagner DD. Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell 1993; 74: 541–54.
38. Ziegler T, Horstkotte J, Schwab C, Pfetsch V, Weinmann K, Dietzel S, Rohwedder I, Hinkel R, Gross L, Lee S, Hu J, Soehnlein O, Franz WM, Sperandio M, Pohl U, Thomas M, Weber C, Augustin HG, Fässler R, Deutsch U, et al. Angiopoietin 2 mediates microvascular and hemodynamic alterations in sepsis. J Clin Invest 2013; 123: 3436–45.
39. Chaaban H, Keshari RS, Silasi-Mansat R, Popescu NI, Mehta-D'Souza P, Lim YP, Lupu F. Inter-alpha inhibitor protein and its associated glycosaminoglycans protect against histone-induced injury. Blood 2015; 125: 2286–96.
40. De Ceunynck K, De Meyer SF, Vanhoorelbeke K. Unwinding the von Willebrand factor strings puzzle. Blood 2013; 121: 270–7.
41. Fuchs TA, Kremer Hovinga JA, Schatzberg D, Wagner DD, Lammle B. Circulating DNA and myeloperoxidase indicate disease activity in patients with thrombotic microangiopathies. Blood 2012; 120: 1157–64.
42. Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, Carter C, Yu BP, Leeuwenburgh C. Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 2009; 8: 18–30.
43. Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev 2007; 65: S173–6.
44. Jylhava J, Kotipelto T, Raitala A, Jylha M, Hervonen A, Hurme M. Aging is associated with quantitative and qualitative changes in circulating cell-free DNA: the Vitality 90+ study. Mech Ageing Dev 2011; 132: 20–6.
45. Kraft P, Drechsler C, Gunreben I, Nieswandt B, Stoll G, Heuschmann PU, Kleinschnitz C. Von Willebrand factor regulation in patients with acute and chronic cerebrovascular disease: a pilot, case-control study. PLoS ONE 2014; 9: e99851.
46. Smith NL, Rice KM, Bovill EG, Cushman M, Bis JC, McKnight B, Lumley T, Glazer NL, van Hylckama Vlieg A, Tang W, Dehghan A, Strachan DP, O'Donnell CJ, Rotter JI, Heckbert SR, Psaty BM, Rosendaal FR. Genetic variation associated with plasma von Willebrand factor levels and the risk of incident venous thrombosis. Blood 2011; 117: 6007–11.
47. Ward PA. Acute and chronic inflammation. In: Serhan CN, Ward PA, eds.Fundamentals of Inflammation. 1st edn; New York, NY: Cambridge University Press, 2010: 1–16.
48. Kayal S, Jaïs JP, Aguini N, Chaudière J, Labrousse J. Elevated circulating E-selectin, intercellular adhesion molecule 1, and von Willebrand factor in patients with severe infection. Am J Respir Crit Care Med 1998; 157: 776–84.
49. de Kruif MD, Lemaire LC, Giebelen IA, van Zoelen MA, Pater JM, van den Pangaart PS, Groot AP, de Vos AF, Elliott PJ, Meijers JC, Levi M, van der Poll T. Prednisolone dose-dependently influences inflammation and coagulation during human endotoxemia. J Immunol 2007; 178: 1845–51.
50. Schoergenhofer C, Schwameis M, Hobl E, Ay C, Key NS, Derhaschnig U, Jilma B, Spiel AO. Potent irreversible P2Y 12 inhibition does not reduce LPS-induced coagulation activation in a randomized, double-blind, placebo-controlled trial. Clin Sci (Lond) 2016; 130: 433–40.