Platelet activation and prothrombotic properties in a mouse model of peritoneal sepsis

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Vardon Bounes, Fanny ^a,b   Mémier, Vincent ^a,b   Marcaud, Marina ^a   Jacquemin, Aemilia ^a,b   Hamzeh Cognasse, Hind ^c   Garcia, Cédric ^b   Series, Jennifer ^b   Sié, Pierre ^a,b   Minville, Vincent ^a,b   Gratacap, Marie Pierre ^a   Payrastre, Bernard ^a,b  

^a Université de Toulouse   (France)

^b TOULOUSE UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1-PHOSPHATIDYLINOSITOL 3-KINASE P110 SUBUNIT, MOUSE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; THROMBOCYTE FACTOR 4;

ANIMAL; ARTERIOLE; BLOOD; C57BL MOUSE; DISEASE MODEL; GENE KNOCKDOWN; GENETICS; HUMAN; MALE; MICROBIOLOGY; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PERITONITIS; SEPSIS; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTOPENIA; THROMBOSIS; TRANSGENIC MOUSE;

ANIMALS; ARTERIOLES; BLOOD PLATELETS; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; DISEASE MODELS, ANIMAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PERITONITIS; PLATELET ACTIVATION; PLATELET FACTOR 4; SEPSIS; THROMBOCYTOPENIA; THROMBOSIS;

EID: 85053203216     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-31910-8     Document Type: Article

References (56)

1. Fleischmann, C. et al. Assessment of Global Incidence and Mortality of Hospital-treated Sepsis. Current Estimates and Limitations. Am J Respir Crit Care Med 193, 259–272 (2016).
2. Vincent, J.-L. et al. Assessment of the worldwide burden of critical illness: the Intensive Care Over Nations (ICON) audit. Lancet Respir Med 2, 380–386 (2014).
3. Gaieski, D. F., Edwards, J. M., Kallan, M. J. & Carr, B. G. Benchmarking the incidence and mortality of severe sepsis in the United States. Critical Care Medicine 41, 1167–1174 (2013).
4. Singer, M. et al. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA 315, 801–10 (2016).
5. Jenne, C. N. & Kubes, P. Platelets in inflammation and infection. Platelets 26, 286–292 (2015).
6. Yeaman, M. R. Platelets: at the nexus of antimicrobial defence. Nat Rev Micro 12, 426–437 (2014).
7. Venkata, C., Kashyap, R., Farmer, J. C. & Afessa, B. Thrombocytopenia in adult patients with sepsis: incidence, risk factors, and its association with clinical outcome. Journal of Intensive Care 1, 9 (2013).
8. Furie, B. & Furie, B. C. Mechanisms of Thrombus Formation. N Engl Med 359, 938–949 (2008).
9. Nieswandt, B., Varga-szabo, D. & Elvers, M. Integrins in platelet activation. J Thromb Haemost 7, 206–209 (2009).
10. Cognasse, F. The inflammatory role of platelets via their TLRs and Siglec receptors. Frontiers in Immunology 6 (2015).
11. Kilic, Y. A., Kilic, I. & Tez, M. Sepsis and multiple organ failure represent a chaotic adaptation to severe stress which must be controlled at nanoscale. Crit Care 2009 13, 424 (2009).
12. O’Brien, J. M., Ali, N. A. & Abraham, E. Year in review 2007: Critical Care – multiple organ failure and sepsis. Crit Care 2009 12, 228 (2008).
13. McDonald, B. et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood 129, 1357–1367 (2017).
14. Xiang, B. et al. Platelets protect from septic shock by inhibiting macrophage-dependent inflammation via the cyclooxygenase 1 signalling pathway. Nat Commun 4, 264 (2013).
15. Rayes, J. et al. The podoplanin-CLEC-2 axis inhibits inflammation in sepsis. Nat Commun 8, 840 (2017).
16. Arman, M. et al. Amplification of bacteria-induced platelet activation is triggered by Fc RIIA, integrin IIb 3, and platelet factor 4. Blood 123, 3166–3174 (2014).
17. Cox, D., Kerrigan, S. W. & Watson, S. P. Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J Thromb Haemost 9, 1097–1107 (2011).
18. Moriarty, R. D., Cox, A., McCall, M., Smith, S. G. J. & Cox, D. Escherichia coliinduces platelet aggregation in an FcγRIIa-dependent manner. J Thromb Haemost 14, 797–806 (2016).
19. Watson, C. N. et al. Human platelet activation by Escherichia coli: roles for FcγRIIA and integrin αIIbβ3. Platelets 27, 535–540 (2016).
20. Muhlestein, J. B. Effect of antiplatelet therapy on inflammatory markers in atherothrombotic patients. Thromb Haemost 103, 71–82 (2010).
21. Jackson, S. P. et al. PI 3-kinase p110β: a new target for antithrombotic therapy. Nat Med 11, 507–514 (2005).
22. Nylander, S. et al. Human target validation of phosphoinositide 3-kinase (PI3K)β: effects on platelets and insulin sensitivity, using AZD6482 a novel PI3Kβ inhibitor. J Thromb Haemost 10, 2127–2136 (2012).
23. Layios, N. et al. Sepsis prediction in critically ill patients by platelet activation markers on ICU admission: a prospective pilot study. Intensive Care Med Exp. 5, 32 (2017).
24. Gawaz, M., Dickfeld, T., Bogner, C., Fateh-Moghadam, S. & Neumann, F. J. Platelet function in septic multiple organ dysfunction syndrome. Intensive Care Med 23, 379–385 (1997).
25. Faraday, N. et al. Leukocytes Can Enhance Platelet-mediated Aggregation and Thromboxane Release via Interaction of P-selectin Glycoprotein Ligand 1 with P-selectin. Anesthesiology 94, 145–151 (2001).
26. Fitzgerald, J. R. et al. Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgammaRIIa receptor. Mol Microbiol 59, 212–230 (2006).
27. Tóth, J. et al. Characteristics of thrombin generation in a fulminant porcine sepsis model. Thromb Res 158, 25–34 (2017).
28. Akinosoglou, K. et al. Platelet reactivity in sepsis syndrome: results from the PRESS study. Eur J Clin Microbiol Infect Dis 36, 2503–2512 (2017).
29. Hurley, S. M., Lutay, N., Holmqvist, B. & Shannon, O. The Dynamics of Platelet Activation during the Progression of Streptococcal Sepsis. PLoS ONE 11, e0163531 (2016).
30. Zarbock, A., Polanowska-Grabowska, R. K. & Ley, K. Platelet-neutrophil-interactions: Linking hemostasis and inflammation. Blood Rev 21, 99–111 (2007).
31. Rutten, B. et al. Platelet density per monocyte predicts adverse events in patients after percutaneous coronary intervention. Thromb Haemost 115, 353–360 (2016).
32. Henn, V. et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 391, 591–594 (1998).
33. Dennis, E. A. & Norris, P. C. Eicosanoid storm in infection and inflammation. Nat Rev Immunol 15, 511–523 (2015).
34. Nylander, S., Wågberg, F., Andersson, M., Skärby, T. & Gustafsson, D. Exploration of efficacy and bleeding with combined phosphoinositide 3-kinase β inhibition and aspirin in man. J Thromb Haemost 13, 1494–1502 (2015).
35. Laurent, P.-A. et al. Platelet PI3K and GSK3 regulate thrombus stability at a high shear rate. Blood 125, 881–888 (2015).
36. Barrera, G. et al. Model of Polymicrobial Peritonitis That Induces the Proinflammatory and Immunosuppressive Phases of Sepsis. Infect. Immun. 79, 1280–1288 (2011).
37. Rittirsch, D., Huber-Lang, M. S., Flierl, M. A. & Ward, P. A. Immunodesign of experimental sepsis by cecal ligation and puncture. Nature Protocols 4, 31–36 (2009).
38. Ruiz, S. et al. Sepsis modeling in mice: ligation length is a major severity factor in cecal ligation and puncture. Intensive Care Medicine Experimental 4, 138 (2016).
39. Ferreira, F. L. Serial Evaluation of the SOFA Score to Predict Outcome in Critically Ill Patients. JAMA 286, 1754 (2001).
40. Moreau, D. et al. Platelet count decline: an early prognostic marker in critically ill patients with prolonged ICU stays. Chest 131, 1735–1741 (2007).
41. Akca, S. et al. Time course of platelet counts in critically ill patients. Critical Care Med 30, 753–756 (2002).
42. Strauss, R. et al. Thrombocytopenia in patients in the medical intensive care unit: Bleeding prevalence, transfusion requirements, and outcome. Critical Care Med 30, 1765–1771 (2002).
43. Russwurm, S. et al. Platelet and Leukocyte Activation Correlate with the Severity of Septic Organ Dysfunction. Shock 17, 263–268 (2002).
44. Michelson, A. D., Barnard, M. R., Krueger, L. A., Valeri, C. R. & Furman, M. I. Circulating Monocyte-Platelet Aggregates Are a More Sensitive Marker of In Vivo Platelet Activation Than Platelet Surface P-Selectin: Studies in Baboons, Human Coronary Intervention, and Human Acute Myocardial Infarction. Circulation 104, 1533–1537 (2001).
45. Finsterbusch, M., Schrottmaier, W. C., Kral-Pointner, J. B., Salzmann, M. & Assinger, A. Measuring and interpreting platelet-leukocyte aggregates. Platelets 88, 1–9 (2018).
46. Heffner, J. E. Platelet-neutrophil interactions in sepsis - platelet guilt by association? Intensive Care Med 23, 366–368 (1997).
47. Rahman, M. et al. Platelet shedding of CD40L is regulated by matrix metalloproteinase-9 in abdominal sepsis. J Thromb Haemost 11, 1385–1398 (2013).
48. Inwald, D. P., Peters, M. J., Faust, S. N., Levin, M. & Klein, N. The Role of Platelet CD40L in Inflammation. J Intensive Care Society 6, 28–29 (2005).
49. Damås, J. K. et al. Increased levels of soluble CD40L in African tick bite fever: possible involvement of TLRs in the pathogenic interaction between Rickettsia africae, endothelial cells, and platelets. Journal Immunol 177, 2699–2706 (2006).
50. Lorente, L. et al. Association between serum soluble CD40 ligand levels and mortality in patients with severe sepsis. Crit Care 2009 13:6 15, R97 (2011).
51. Lerolle, N. et al. von Willebrand factor is a major determinant of ADAMTS-13 decrease during mouse sepsis induced by cecum ligation and puncture. J Thromb Haemost 7, 843–850 (2009).
52. Peigne, V. et al. The prognostic value of ADAMTS13 (a disintegrin and metalloprotease with thrombospondin type 1 repeats, member 13) deficiency in septic shock patients involves interleukin-6 and is not dependent on disseminated intravascular coagulation. Crit Care 17, R273 (2013).
53. Yin, H. et al. Role for platelet glycoprotein Ib-IX and effects of its inhibition in endotoxemia-induced thrombosis, thrombocytopenia, and mortality. Arterioscler Thromb Vasc Biol. 33, 2529–2537 (2013).
54. Martin, V. et al. Deletion of the p110 isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitro and in vivo. Blood 115, 2008–2013 (2010).
55. Rahman, M., Gustafsson, D., Wang, Y., Thorlacius, H. & Braun, O. Ö. Ticagrelor reduces neutrophil recruitment and lung damage in abdominal sepsis. Platelets 25, 257–263 (2014).
56. Le Faouder, P. et al. LC–MS/MS method for rapid and concomitant quantification of pro-inflammatory and pro-resolving polyunsaturated fatty acid metabolites. Journal of Chromatography B 932, 123–133 (2013).