Extracellular histone H3 levels are inversely correlated with antithrombin levels and platelet counts and are associated with mortality in sepsis patients

Thrombosis Research

Volumn 136, Issue 3, 2015, Pages 542-547

  Wildhagen, Karin C A A ^a   Wiewel, Maryse A ^b   Schultz, Marcus J ^b   Horn, Janneke ^b   Schrijver, Roy ^a   Reutelingsperger, Chris P M ^a   Van Der Poll, Tom ^b   Nicolaes, Gerry A F ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Antithrombin; Histones; Mortality; NETosis; Sepsis; Thrombin generation

Indexed keywords

ANTITHROMBIN; HISTONE H3; LACTATE DEHYDROGENASE; LACTIC ACID; PROTHROMBIN; BIOLOGICAL MARKER; HISTONE; HYDROLYASE; LACTATE DEHYDRATASE;

ADULT; ANTICOAGULATION; ARTICLE; BLOOD SAMPLING; CAUSE OF DEATH; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; EXTRACELLULAR MATRIX; FEMALE; HOSPITAL ADMISSION; HUMAN; INTENSIVE CARE UNIT; MALE; METABOLIC PARAMETERS; MORTALITY; MULTIPLE ORGAN FAILURE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; SEPSIS; SEPTIC SHOCK; SURVIVOR; THROMBOCYTE COUNT; TISSUE METABOLISM; BLOOD; EPIDEMIOLOGY; INCIDENCE; MIDDLE AGED; NETHERLANDS; PROGNOSIS; REPRODUCIBILITY; RISK FACTOR; SENSITIVITY AND SPECIFICITY; STATISTICS AND NUMERICAL DATA; SURVIVAL RATE;

ANTITHROMBINS; BIOMARKERS; FEMALE; HISTONES; HUMANS; HYDRO-LYASES; INCIDENCE; MALE; MIDDLE AGED; NETHERLANDS; PLATELET COUNT; PROGNOSIS; REPRODUCIBILITY OF RESULTS; RISK FACTORS; SENSITIVITY AND SPECIFICITY; SEPSIS; SURVIVAL RATE;

EID: 84940438616     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2015.06.035     Document Type: Article

References (45)

1. N. Adhikari, R. Fowler, S. Bhagwanjee, and G. Rubenfeld Critical care and the global burden of critical illness in adults Lancet 376 2010 1339 1346
2. D. Angus, and T. van der Poll Severe sepsis and septic shockvere sepsis and septic shock N. Engl. J. Med. 369 2013 840 851
3. J. Xu, X. Zhang, R. Pelayo, M. Monestier, C. Ammollo, and et al. Extracellular histones are major mediators of death in sepsis Nat. Med. 15 2009 1318 1321
4. K. Luger, A. Mäder, R. Richmond, D. Sargent, and T. Richmond Crystal structure of the nucleosome core particle at 2.8 A resolution Nature 389 1997 251 260
5. S. Zeerleder, B. Zwart, W. Wuillemin, L. Aarden, A. Groeneveld, and et al. Elevated nucleosome levels in systemic inflammation and sepsis Crit. Care Med. 31 2003 1947 1951
6. T. Fuchs, A. Brill, D. Duerschmied, D. Schatzberg, M. Monestier, and et al. Extracellular DNA traps promote thrombosis PNAS 107 2010 15880 15885
7. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, and et al. Neutrophil extracellular traps kill bacteria Science 303 2004 1532 1535
8. C. Chaput, and A. Zychlinsky Sepsis: the dark side of histones Nat. Med. 15 2009 1245 1246
9. T. Kleine, P. Lewis, and S. Lewis Histone-induced damage of a mammalian epithelium: the role of protein and membrane structure Am. J. Physiol. 273 1997 C1925 C1936
10. E. Hariton-Gazal, J. Rosenbluh, A. Graessmann, C. Gilon, and A. Loyter Direct translocation of histone molecules across cell membranes J. Cell Sci. 116 2003 4577 4586
11. J. Rosenbluh, E. Hariton-Gazal, A. Dagan, S. Rottem, A. Graessmann, and et al. Translocation of histone proteins across lipid bilayers and Mycoplasma membranes J. Mol. Biol. 345 2005 387 400
12. J. Xu, X. Zhang, M. Monestier, N. Esmon, and C. Esmon Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury J. Immunol. 187 2011 2626 2631
13. R. Allam, C. Scherbaum, M. Darisipudi, S. Mulay, H. Hagele, and et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4 J. Am. Soc. Nephrol. 23 2012 1375 1388
14. F. Semeraro, C. Ammollo, J. Morrissey, G. Dale, P. Friese, and et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4 Blood 118 2011 1952 1961
15. S. Zeerleder, F. Stephan, M. Emonts, E. de Kleijn, C. Esmon, and et al. Circulating nucleosomes and severity of illness in children suffering from meningococcal sepsis treated with protein C Crit. Care Med. 40 2012 3224 3229
16. Q. Chen, L. Ye, Y. Jin, N. Zhang, T. Lou, and et al. Circulating nucleosomes as a predictor of sepsis and organ dysfunction in critically ill patients Int. J. Infect. Dis. 16 2012 e558 e564
17. M. Kutcher, J. Xu, R. Vilardi, C. Ho, C. Esmon, and et al. Extracellular histone release in response to traumatic injury: implications for a compensatory role of activated protein C J. Trauma. Acute Care Surg. 73 2012 1389 1394
18. R. Allam, S. Kumar, M. Darisipudi, and H. Anders Extracellular histones in tissue injury and inflammation J. Mol. Med. (Berl) 92 2014 465 472
19. R. Bone, R. Balk, F. Cerra, R. Dellinger, A. Fein, and et al. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine Chest 101 1992 1644 1655
20. J.E. Zimmerman, A.A. Kramer, D.S. McNair, and F.M. Malila Acute Physiology and Chronic Health Evaluation (APACHE) IV: hospital mortality assessment for today's critically ill patients Crit. Care Med. 34 2006 1297 1310
21. J.L. Vincent, R. Moreno, J. Takala, S. Willatts, A. De Mendonca, and et al. The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the Working Group on Sepsis-Related Problems of the European Society of Intensive Care Medicine Intensive Care Med. 22 1996 707 710
22. R. Bellomo, C. Ronco, J.A. Kellum, R.L. Mehta, P. Palevsky, and et al. Acute renal failure - definition, outcome measures, animal models, fluid therapy and information technology needs: the Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group Crit. Care 8 2004 R204 R212
23. H. Hemker, P. Giesen, R.A. Dieri, V. Regnault, and Smedt Ed The calibrated automated thrombogram (CAT): a universal routine test for hyper- and hypocoagulability Pathophysiol. Haemost. Thromb. 32 2002 249 253
24. O. Odegard, M. Lie, and U. Abildgaard Heparin cofactor activity measured with an amidolytic method Thromb. Res. 6 1975 287 294
25. J. Zein, G. Lee, M. Tawk, M. Dabaja, and G. Kinasewitz Prognostic Significance of Elevated Serum Lactate Dehydrogenase (LDH) in Patients with Severe Sepsis Chest 126 2004 873S
26. P. Van Dreden, B. Woodhams, A. Rousseau, J. Dreyfus, and M. Vasse Contribution of procoagulant phospholipids, thrombomodulin activity and thrombin generation assays as prognostic factors in intensive care patients with septic and non-septic organ failure Clin. Chem. Lab. Med. 51 2013 387 396
27. P. Collins, L. Macchiavello, S. Lewis, N. Macartney, A. Saayman, and et al. Global tests of haemostasis in critically ill patients with severe sepsis syndrome compared to controls Br. J. Haematol. 135 2006 220 227
28. S. Petros, P. Kliem, T. Siegemund, and R. Siegemund Thrombin generation in severe sepsis Thromb. Res. 129 2012 797 800
29. P. Massion, P. Peters, D. Ledoux, V. Zimermann, J. Canivet, and et al. Persistent hypocoagulability in patients with septic shock predicts greater hospital mortality: impact of impaired thrombin generation Intensive Care Med. 38 2012 1326 1335
30. P. Marty, A. Roquilly, F. Vallée, A. Luzi, F. Ferré, and et al. Lactate clearance for death prediction in severe sepsis or septic shock patients during the first 24 hours in Intensive Care Unit: an observational study Ann. Intensive Care 3 2013
31. J. Londoño, A. León, F. Rodríguez, L. Barrera, G. de la Rosa, and et al. Serum lactate in the emergency department as a prognostic factor in patients with sepsis without hypotension Med. Clin. (Barc.) 141 2013 246 251
32. R. Al Dieri, B. de Laat, and H.C. Hemker Thrombin generation: What have we learned? Blood Rev. 26 2012 197 203
33. M. Levi, E. de Jonge, and T. van der Poll Sepsis and disseminated intravascular coagulation J. Thromb. Thrombolysis 16 2003 43 47
34. M. Levi, and T. Van der Poll Two-way interactions between inflammation and coagulation Trends Cardiovasc. Med. 15 2005 254 259
35. B. Phypers, and J. Pierce Lactate physiology in health and disease Anaesthesia, Critical Care & Pain 6 2006 128 132
36. S. Gibot On the origins of lactate during sepsis Crit. Care 16 2012 151
37. A. Carestia, L. Rivadeneyra, M. Romaniuk, C. Fondevila, S. Negrotto, and et al. Functional responses and molecular mechanisms involved in histone-mediated platelet activation Thromb. Haemost. 110 2013 1035 1045
38. T. Fuchs, A. Bhandari, and D. Wagner Histones induce rapid and profound thrombocytopenia in mice Blood 118 2011 3708 3714
39. K. Wildhagen, P. García de Frutos, C. Reutelingsperger, R. Schrijver, C. Aresté, and et al. Nonanticoagulant heparin prevents histone-mediated cytotoxicity in vitro and improves survival in sepsis Blood 123 2014 1098 1101
40. R. Allam, M. Darisipudi, J. Tschopp, and H. Anders Histones trigger sterile inflammation by activating the NLRP3 inflammasome Eur. J. Immunol. 43 2013 3336 3342
41. K. Schroder, and J. Tschopp The inflammasomes Cell 140 2010 821 832
42. M. Nakahara, T. Ito, K. Kawahara, M. Yamamoto, T. Nagasato, and et al. Recombinant thrombomodulin protects mice against histone-induced lethal thromboembolism PLoS ONE 8 2013 e75961
43. M. Ekaney, G. Otto, M. Sossdorf, C. Sponholz, M. Boehringer, and et al. Impact of plasma histones in human sepsis and their contribution to cellular injury and inflammation Crit. Care 18 2014 543
44. M. Saffarzadeh, C. Juenemann, M. Queisser, G. Lochnit, G. Barreto, and et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones PLoS ONE 7 2012 e32366
45. C. Ammollo, F. Semeraro, J. Xu, N. Esmon, and C. Esmon Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation J. Thromb. Haemost. 9 2011 1795 1803