The coagulation system in melioidosis: from pathogenesis to new treatment strategies

Reference

• Cheng AC, Currie BJ. Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 2005;18(2):383-416
   PubMed Web of Science ®Google Scholar
• Currie BJ, Ward L, Cheng AC. The epidemiology and clinical spectrum of melioidosis: 540 cases from the 20 year darwin prospective study. PLoS Negl Trop Dis 2010;4(11):e900
   PubMed Web of Science ®Google Scholar
• Wiersinga WJ, Currie BJ, Peacock SJ. Melioidosis. N Engl J Med 2012;367(11):1035-44
   PubMed Web of Science ®Google Scholar
• Wiersinga WJ, van der Poll T, White NJ, et al. Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 2006;4(4):272-82
   PubMed Web of Science ®Google Scholar
• Limmathurotsakul D, Wongratanacheewin S, Teerawattanasook N, et al. Increasing incidence of human melioidosis in Northeast Thailand. Am J Trop Med Hyg 2010;82(6):1113-17
   PubMed Web of Science ®Google Scholar
• Meumann EM, Cheng AC, Ward L, Currie BJ. Clinical features and epidemiology of melioidosis pneumonia: results from a 21-year study and review of the literature. Clin Infect Dis 2012;54(3):362-9
   PubMed Web of Science ®Google Scholar
• Butler D. Viral research faces clampdown. Nature 2012;490(7421):456
   PubMedGoogle Scholar
• Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 2008;83(3):536-45
   PubMed Web of Science ®Google Scholar
• Bast A, Krause K, Schmidt IH, et al. Caspase-1-Dependent and -Independent Cell Death Pathways in Burkholderia pseudomallei Infection of Macrophages. PLoS Pathog 2014;10(3):e1003986
   PubMed Web of Science ®Google Scholar
• Wiersinga WJ, Wieland CW, Roelofs JJ, van der Poll T. MyD88 dependent signaling contributes to protective host defense against Burkholderia pseudomallei. PLoS One 2008;3(10):e3494
   Google Scholar
• Lauw FN, Simpson AJ, Prins JM, et al. Elevated plasma concentrations of interferon (IFN)-gamma and the IFN-gamma-inducing cytokines interleukin (IL)-18, IL-12, and IL-15 in severe melioidosis. J Infect Dis 1999;180(6):1878-85
   PubMedGoogle Scholar
• Santanirand P, Harley VS, Dance DA, et al. Obligatory role of gamma interferon for host survival in a murine model of infection with Burkholderia pseudomallei. Infect Immun 1999;67(7):3593-600
   PubMedGoogle Scholar
• Easton A, Haque A, Chu K, et al. A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J Infect Dis 2007;195(1):99-107
   PubMed Web of Science ®Google Scholar
• Dahlback B. Blood coagulation. Lancet 2000;355(9215):1627-32
   PubMed Web of Science ®Google Scholar
• van der Poll T, Opal SM. Host-pathogen interactions in sepsis. Lancet Infect Dis 2008;8(1):32-43
   PubMedGoogle Scholar
• Esmon CT. The interactions between inflammation and coagulation. Br J Haematol 2005;131(4):417-30
   PubMed Web of Science ®Google Scholar
• LaRosa SP, Opal SM, Utterback B, et al. Decreased protein C, protein S, and antithrombin levels are predictive of poor outcome in Gram-negative sepsis caused by Burkholderia pseudomallei. Int J Infect Dis 2006;10(1):25-31
   PubMedGoogle Scholar
• Wiersinga WJ, Meijers JC, Levi M, et al. Activation of coagulation with concurrent impairment of anticoagulant mechanisms correlates with a poor outcome in severe melioidosis. J Thromb Haemost 2008;6(1):32-9
   PubMedGoogle Scholar
• Koh GC, Meijers JC, Maude RR, et al. Diabetes does not influence activation of coagulation, fibrinolysis or anticoagulant pathways in Gram-negative sepsis (melioidosis). Thromb Haemost 2011;106(6):1139-48
   PubMedGoogle Scholar
• Atisook K, Panyathanya R. Acute systemic melioidosis: an autopsy study of six cases. Southeast Asian J Trop Med Public Health 1988;19(4):637-42
   PubMedGoogle Scholar
• Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007;109(8):3161-72
   PubMedGoogle Scholar
• Stenflo J. A new vitamin K-dependent protein. Purification from bovine plasma and preliminary characterization. J Biol Chem 1976;251(2):355-63
   PubMed Web of Science ®Google Scholar
• Conway EM. Thrombomodulin and its role in inflammation. Semin Immunopathol 2012;34(1):107-25
   PubMed Web of Science ®Google Scholar
• Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, et al. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci U S A 1996;93(19):10212-16
   PubMedGoogle Scholar
• Spiegel S, Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat Rev Immunol 2011;11(6):403-15
   PubMed Web of Science ®Google Scholar
• Finigan JH, Dudek SM, Singleton PA, et al. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 2005;280(17):17286-93
   PubMed Web of Science ®Google Scholar
• Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood 2005;105(8):3178-84
   PubMed Web of Science ®Google Scholar
• Xu J, Zhang X, Pelayo R, et al. Extracellular histones are major mediators of death in sepsis. Nat Med 2009;15(11):1318-21
   PubMed Web of Science ®Google Scholar
• Weiler-Guettler H, Christie PD, Beeler DL, et al. A targeted point mutation in thrombomodulin generates viable mice with a prethrombotic state. J Clin Invest 1998;101(9):1983-91
   PubMedGoogle Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. A thrombomodulin mutation that impairs active protein C generation is detrimental in severe pneumonia-derived Gram-negative sepsis (melioidosis). PLoS Negl Trop Dis 2014;8(4):e2819
   Google Scholar
• Xu J, Ji Y, Zhang X, et al. Endogenous activated protein C signaling is critical to protection of mice from lipopolysaccaride-induced septic shock. J Thromb Haemost 2009;7(5):851-6
   PubMedGoogle Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. Endogenous protein C has a protective role during Gram-negative pneumosepsis (melioidosis). J Thromb Haemost 2013;11(2):282-92
   PubMedGoogle Scholar
• Awad AS, Ye H, Huang L, et al. Selective sphingosine 1-phosphate 1 receptor activation reduces ischemia-reperfusion injury in mouse kidney. Am J Physiol Renal Physiol 2006;290(6):F1516-24
   PubMed Web of Science ®Google Scholar
• van Sluis GL, Niers TM, Esmon CT, et al. Endogenous activated protein C limits cancer cell extravasation through sphingosine-1-phosphate receptor 1-mediated vascular endothelial barrier enhancement. Blood 2009;114(9):1968-73
   PubMedGoogle Scholar
• Bernard GR, Vincent JL, Laterre PF, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001;344(10):699-709
   PubMed Web of Science ®Google Scholar
• Ranieri VM, Thompson BT, Barie PS, et al. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med 2012;366(22):2055-64
   PubMed Web of Science ®Google Scholar
• Mitka M. Drug for severe sepsis is withdrawn from market, fails to reduce mortality. JAMA 2011;306(22):2439-40
   PubMedGoogle Scholar
• Schouten M, van ’t Veer C, Van Den Boogaard FE, et al. Therapeutic recombinant murine activated protein C attenuates pulmonary coagulopathy and improves survival in murine pneumococcal pneumonia. J Infect Dis 2010;202(10):1600-7
   PubMedGoogle Scholar
• Schouten M, van ’t Veer C, Roelofs JJ, et al. Recombinant activated protein C attenuates coagulopathy and inflammation when administered early in murine pneumococcal pneumonia. Thromb Haemost 2011;106(6):1189-96
   PubMedGoogle Scholar
• Isermann B, Vinnikov IA, Madhusudhan T, et al. Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 2007;13(11):1349-58
   PubMedGoogle Scholar
• Macias WL, Dhainaut JF, Yan SC, et al. Pharmacokinetic-pharmacodynamic analysis of drotrecogin alfa (activated) in patients with severe sepsis. Clin Pharmacol Ther 2002;72(4):391-402
   PubMedGoogle Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. Overexpression of activated protein C is detrimental during severe experimental gram-negative sepsis (Melioidosis)*. Crit Care Med 2013;41(10):e266-74
   Google Scholar
• Esmon CT. The endothelial protein C receptor. Curr Opin Hematol 2006;13(5):382-5
   PubMedGoogle Scholar
• Liaw PC, Esmon CT, Kahnamoui K, et al. Patients with severe sepsis vary markedly in their ability to generate activated protein C. Blood 2004;104(13):3958-64
   PubMedGoogle Scholar
• Kurosawa S, Stearns-Kurosawa DJ, Carson CW, et al. Plasma levels of endothelial cell protein C receptor are elevated in patients with sepsis and systemic lupus erythematosus: lack of correlation with thrombomodulin suggests involvement of different pathological processes. Blood 1998;91(2):725-7
   PubMedGoogle Scholar
• Guitton C, Gerard N, Sebille V, et al. Early rise in circulating endothelial protein C receptor correlates with poor outcome in severe sepsis. Intensive Care Med 2011;37(6):950-6
   PubMedGoogle Scholar
• Faust SN, Levin M, Harrison OB, et al. Dysfunction of endothelial protein C activation in severe meningococcal sepsis. N Engl J Med 2001;345(6):408-16
   PubMed Web of Science ®Google Scholar
• Borgel D, Bornstain C, Reitsma PH, et al. A comparative study of the protein C pathway in septic and nonseptic patients with organ failure. Am J Respir Crit Care Med 2007;176(9):878-85
   PubMedGoogle Scholar
• Kager LM, Schouten M, Wiersinga WJ, et al. Overexpression of the endothelial protein C receptor is detrimental during pneumonia-derived gram-negative sepsis (Melioidosis). PLoS Negl Trop Dis 2013;7(7):e2306
   Google Scholar
• Li W, Zheng X, Gu J, et al. Overexpressing endothelial cell protein C receptor alters the hemostatic balance and protects mice from endotoxin. J Thromb Haemost 2005;3(7):1351-9
   PubMedGoogle Scholar
• Conway EM, Van de Wouwer M, Pollefeyt S, et al. The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappaB and mitogen-activated protein kinase pathways. J Exp Med 2002;196(5):565-77
   PubMedGoogle Scholar
• Van de Wouwer M, Plaisance S, de Vriese A, et al. The lectin-like domain of thrombomodulin interferes with complement activation and protects against arthritis. J Thromb Haemost 2006;4(8):1813-24
   PubMedGoogle Scholar
• Huang HC, Shi GY, Jiang SJ, et al. Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J Biol Chem 2003;278(47):46750-9
   PubMedGoogle Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. Mice lacking the lectin-like domain of thrombomodulin are protected against melioidosis. Crit Care Med 2014;42(3):e221-30
   PubMedGoogle Scholar
• Abeyama K, Stern DM, Ito Y, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 2005;115(5):1267-74
   PubMed Web of Science ®Google Scholar
• Walport MJ. Complement. First of two parts. N Engl J Med 2001;344(14):1058-66
   PubMed Web of Science ®Google Scholar
• Delvaeye M, Noris M, de Vriese A, et al. Thrombomodulin mutations in atypical hemolytic-uremic syndrome. N Engl J Med 2009;361(4):345-57
   PubMed Web of Science ®Google Scholar
• Yamakawa K, Fujimi S, Mohri T, et al. Treatment effects of recombinant human soluble thrombomodulin in patients with severe sepsis: a historical control study. Crit Care 2011;15(3):R123
   PubMed Web of Science ®Google Scholar
• Ogawa Y, Yamakawa K, Ogura H, et al. Recombinant human soluble thrombomodulin improves mortality and respiratory dysfunction in patients with severe sepsis. J Trauma Acute Care Surg 2012;72(5):1150-7
   PubMedGoogle Scholar
• Vincent JL, Ramesh MK, Ernest D, et al. A randomized, double-blind, placebo-controlled, Phase 2b study to evaluate the safety and efficacy of recombinant human soluble thrombomodulin, ART-123, in patients with sepsis and suspected disseminated intravascular coagulation. Crit Care Med 2013;41(9):2069-79
   PubMed Web of Science ®Google Scholar
• Carpenter SL, Mathew P. Alpha2-antiplasmin and its deficiency: fibrinolysis out of balance. Haemophilia 2008;14(6):1250-4
   PubMed Web of Science ®Google Scholar
• Lijnen HR. Pleiotropic functions of plasminogen activator inhibitor-1. J Thromb Haemost 2005;3(1):35-45
   PubMed Web of Science ®Google Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. Endogenous tissue-type plasminogen activator impairs host defense during severe experimental Gram-negative sepsis (melioidosis). Crit Care Med 2012;40(7):2168-75
   PubMedGoogle Scholar
• Kager LM, Wiersinga WJ, Roelofs JJ, et al. Plasminogen activator inhibitor type I contributes to protective immunity during experimental Gram-negative sepsis (melioidosis). J Thromb Haemost 2011;9(10):2020-8
   PubMedGoogle Scholar
• Kager LM, Weehuizen TA, Wiersinga WJ, et al. Endogenous Alpha-2-Antiplasmin is Protective during Severe Gram-Negative Sepsis (Melioidosis). Am J Respir Crit Care Med 2013;188(8):967-75
   PubMedGoogle Scholar
• Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002;3(12):932-43
   PubMed Web of Science ®Google Scholar
• Gyetko MR, Sud S, Kendall T, et al. Urokinase receptor-deficient mice have impaired neutrophil recruitment in response to pulmonary Pseudomonas aeruginosa infection. J Immunol 2000;165(3):1513-19
   PubMedGoogle Scholar
• Rijneveld AW, Levi M, Florquin S, et al. Urokinase receptor is necessary for adequate host defense against pneumococcal pneumonia. J Immunol 2002;168(7):3507-11
   PubMedGoogle Scholar
• Wiersinga WJ, Kager LM, Hovius JW, et al. Urokinase receptor is necessary for bacterial defense against pneumonia-derived septic melioidosis by facilitating phagocytosis. J Immunol 2010;184(6):3079-86
   PubMedGoogle Scholar
• Ely EW, Laterre PF, Angus DC, et al. Drotrecogin alfa (activated) administration across clinically important subgroups of patients with severe sepsis. Crit Care Med 2003;31(1):12-19
   PubMed Web of Science ®Google Scholar
• Wiersinga WJ, Leopold SJ, Cranendonk DR, van der Poll T. Host innate immune responses to sepsis. Virulence 2014;5(1):36-44
   PubMed Web of Science ®Google Scholar
• Angus DC. The search for effective therapy for sepsis: back to the drawing board? JAMA 2011;306(23):2614-15
   PubMed Web of Science ®Google Scholar