Factors contributing to the disturbance of coagulation and fibrinolysis in dengue virus infection

Journal of the Formosan Medical Association

Volumn 112, Issue 1, 2013, Pages 12-17

  Chuang, Yung Chun ^a   Lin, Yee Shin ^a   Liu, Ching Chuan ^a,b   Liu, Hsiao Sheng ^a   Liao, Shu Hsing ^c   Shi, Ming Der ^c   Lei, Huan Yao ^a   Yeh, Trai Ming ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^c KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Autoantibody; Coagulation; Cytokine; Dengue virus; Fibrinolysis; Hemorrhage

Indexed keywords

AUTOANTIBODY; CYTOKINE; HOST FACTOR; NONSTRUCTURAL PROTEIN 1; PROTHROMBIN; VIRUS PROTEIN;

BLEEDING; BLOOD CLOTTING; CELL STIMULATION; DENGUE; DENGUE VIRUS; FIBRINOLYSIS; HEMOSTASIS; HUMAN; MOLECULAR MIMICRY; NONHUMAN; PROTEIN EXPRESSION; REVIEW;

AUTOANTIBODIES; BLOOD COAGULATION DISORDERS; CYTOKINES; DENGUE VIRUS; FIBRINOLYSIS; HUMANS; MOLECULAR MIMICRY; PROTHROMBIN; SEVERE DENGUE; THROMBOMODULIN; TISSUE PLASMINOGEN ACTIVATOR; VIRAL PROTEINS;

EID: 84872413363     PISSN: None     EISSN: 09296646     Source Type: Journal    
DOI: 10.1016/j.jfma.2012.10.013     Document Type: Review

References (57)

1. Davie E.W., Fujikawa K., Kisiel W. The coagulation cascade: initiation, maintenance, and regulation. Biochemistry 1991, 30:10363-10370.
2. Esmon C.T. The protein C pathway. Chest 2003, 124:26S-32S.
3. Schoenmakers S.H., Reitsma P.H., Spek C.A. Blood coagulation factors as inflammatory mediators. Blood Cells Mol Dis 2005, 34:30-37.
4. Esmon C.T. Crosstalk between inflammation and thrombosis. Maturitas 2004, 47:305-314.
5. Esmon C.T. Inflammation and thrombosis. J Thromb Haemost 2003, 1:1343-1348.
6. Cosgriff T.M. Viruses and hemostasis. Rev Infect Dis 1989, 11(Suppl. 4):S672-S688.
7. Chen J.P., Cosgriff T.M. Hemorrhagic fever virus-induced changes in hemostasis and vascular biology. Blood Coagul Fibrinolysis 2000, 11:461-483.
8. Henchal E.A., Putnak J.R. The dengue viruses. Clin Microbiol Rev 1990, 3:376-396.
9. Chang S.F., Huang J.H., Shu P.Y. Characteristics of dengue epidemics in Taiwan. J Formos Med Assoc 2012, 111:297-299.
10. Halstead S.B. Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. Rev Infect Dis 1989, 11(Suppl. 4):S830-S839.
11. Lei H.Y. Transient hemophagocytic activity in dengue immunopathogenesis. J Formos Med Assoc 2009, 108:595-598.
12. Rothman A.L. Dengue: defining protective versus pathologic immunity. J Clin Invest 2004, 113:946-951.
13. Lei H.Y., Yeh T.M., Liu H.S., Lin Y.S., Chen S.H., Liu C.C. Immunopathogenesis of dengue virus infection. J Biomed Sci 2001, 8:377-388.
14. Marchi R., Nagaswami C., Weisel J.W. Fibrin formation and lysis studies in dengue virus infection. Blood Coagul Fibrinolysis 2009, 20:575-582.
15. Huang Y.H., Liu C.C., Wang S.T., Lei H.Y., Liu H.L., Lin Y.S., et al. Activation of coagulation and fibrinolysis during dengue virus infection. J Med Virol 2001, 63:247-251.
16. Sosothikul D., Seksarn P., Pongsewalak S., Thisyakorn U., Lusher J. Activation of endothelial cells, coagulation and fibrinolysis in children with Dengue virus infection. Thromb Haemost 2007, 97:627-634.
17. Lin Y.S., Yeh T.M., Lin C.F., Wan S.W., Chuang Y.C., Hsu T.K., et al. Molecular mimicry between virus and host and its implications for dengue disease pathogenesis. Exp Biol Med (Maywood) 2011, 236:515-523.
18. Markoff L.J., Innis B.L., Houghten R., Henchal L.S. Development of cross-reactive antibodies to plasminogen during the immune response to dengue virus infection. J Infect Dis 1991, 164:294-301.
19. Chungue E., Poli L., Roche C., Gestas P., Glaziou P., Markoff L.J. Correlation between detection of plasminogen cross-reactive antibodies and hemorrhage in dengue virus infection. J Infect Dis 1994, 170:1304-1307.
20. Huang Y.H., Chang B.I., Lei H.Y., Liu H.S., Liu C.C., Wu H.L., et al. Antibodies against dengue virus E protein peptide bind to human plasminogen and inhibit plasmin activity. Clin Exp Immunol 1997, 110:35-40.
21. Chuang Y.C., Lei H.Y., Lin Y.S., Liu H.S., Wu H.L., Yeh T.M. Dengue virus-induced autoantibodies bind to plasminogen and enhance its activation. J Immunol 2011, 187:6483-6490.
22. Ames P.R., Iannaccone L., Alves J.D., Margarita A., Lopez L.R., Brancaccio V. Factor XIII in primary antiphospholipid syndrome. J Rheumatol 2005, 32:1058-1062.
23. Yang Y.H., Chien D., Wu M., FitzGerald J., Grossman J.M., Hahn B.H., et al. Novel autoantibodies against the activated coagulation factor IX (FIXa) in the antiphospholipid syndrome that interpose the FIXa regulation by antithrombin. J Immunol 2009, 182:1674-1680.
24. Zhao Y., Rumold R., Zhu M., Zhou D., Ahmed A.E., Le D.T., et al. An IgG antiprothrombin antibody enhances prothrombin binding to damaged endothelial cells and shortens plasma coagulation times. Arthritis Rheum 1999, 42:2132-2138.
25. Yang C.D., Hwang K.K., Yan W., Gallagher K., FitzGerald J., Grossman J.M., et al. Identification of anti-plasmin antibodies in the antiphospholipid syndrome that inhibit degradation of fibrin. J Immunol 2004, 172:5765-5773.
26. Bidot C.J., Jy W., Horstman L.L., Huisheng H., Jimenez J.J., Yaniz M., et al. Factor VII/VIIa: a new antigen in the anti-phospholipid antibody syndrome. Br J Haematol 2003, 120:618-626.
27. Cheng H.J., Lin C.F., Lei H.Y., Liu H.S., Yeh T.M., Luo Y.H., et al. Proteomic analysis of endothelial cell autoantigens recognized by anti-dengue virus nonstructural protein 1 antibodies. Exp Biol Med (Maywood) 2009, 234:63-73.
28. Lin C.F., Lei H.Y., Shiau A.L., Liu H.S., Yeh T.M., Chen S.H., et al. Endothelial cell apoptosis induced by antibodies against dengue virus nonstructural protein 1 via production of nitric oxide. J Immunol 2002, 169:657-664.
29. Lin C.F., Lei H.Y., Liu C.C., Liu H.S., Yeh T.M., Wang S.T., et al. Generation of IgM anti-platelet autoantibody in dengue patients. J Med Virol 2001, 63:143-149.
30. Lin C.F., Wan S.W., Chen M.C., Lin S.C., Cheng C.C., Chiu S.C., et al. Liver injury caused by antibodies against dengue virus nonstructural protein 1 in a murine model. Lab Invest 2008, 88:1079-1089.
31. Yen Y.T., Chen H.C., Lin Y.D., Shieh C.C., Wu-Hsieh B.A. Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 2008, 82:12312-12324.
32. Bethell D.B., Flobbe K., Cao X.T., Day N.P., Pham T.P., Buurman W.A., et al. Pathophysiologic and prognostic role of cytokines in dengue hemorrhagic fever. J Infect Dis 1998, 177:778-782.
33. Chen L.C., Lei H.Y., Liu C.C., Shiesh S.C., Chen S.H., Liu H.S., et al. Correlation of serum levels of macrophage migration inhibitory factor with disease severity and clinical outcome in dengue patients. Am J Trop Med Hyg 2006, 74:142-147.
34. Assunção-Miranda I., Amaral F.A., Bozza F.A., Fagundes C.T., Sousa L.P., Souza D.G., et al. Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. FASEB J 2010, 24:218-228.
35. Chuang Y.C., Lei H.Y., Liu H.S., Lin Y.S., Fu T.F., Yeh T.M. Macrophage migration inhibitory factor induced by dengue virus infection increases vascular permeability. Cytokine 2011, 54:222-231.
36. Calandra T., Bernhagen J., Mitchell R.A., Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 1994, 179:1895-1902.
37. Calandra T., Bernhagen J., Metz C.N., Spiegel L.A., Bacher M., Donnelly T., et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995, 377:68-71.
38. Makita H., Nishimura M., Miyamoto K., Nakano T., Tanino Y., Hirokawa J., et al. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am J Respir Crit Care Med 1998, 158:573-579.
39. Souza D.G., Fagundes C.T., Sousa L.P., Amaral F.A., Souza R.S., Souza A.L., et al. Essential role of platelet-activating factor receptor in the pathogenesis of Dengue virus infection. Proc Natl Acad Sci U S A 2009, 106:14138-14143.
40. Shyu L.Y., Yeh T.M., Chang H.H., Lin D.P., Teng Y.H., Chen L.C., et al. Macrophage migration inhibitory factor induces ICAM-1and thrombomobulin expression in vitro. Thromb Res 2012, 129:43-49.
41. Chuang Y.C., Su W.H., Lei H.Y., Lin Y.S., Liu H.S., Chang C.P., et al. Macrophage migration inhibitory factor induces autophagy via reactive oxygen species generation. PLoS One 2012, 7:e37613.
42. Lee Y.R., Lei H.Y., Liu M.T., Wang J.R., Chen S.H., Jiang-Shieh Y.F., et al. Autophagic machinery activated by dengue virus enhances virus replication. Virology 2008, 374:240-248.
43. Mairuhu A., Setiati T., Koraka P., Hack C., Leyte A., Faradz S., et al. Increased PAI-1 plasma levels and risk of death from dengue: no association with the 4G/5G promoter polymorphism. Thromb J 2005, 3:17.
44. Huang Y.H., Lei H.Y., Liu H.S., Lin Y.S., Chen S.H., Liu C.C., et al. Tissue plasminogen activator induced by dengue virus infection of human endothelial cells. J Med Virol 2003, 70:610-616.
45. Jiang Z., Tang X., Xiao R., Jiang L., Chen X. Dengue virus regulates the expression of hemostasis-related molecules in human vein endothelial cells. J Infect 2007, 55:e23-e28.
46. Shyu H.W., Lin Y.Y., Chen L.C., Wang Y.F., Yeh T.M., Su S.J., et al. The dengue virus envelope protein induced PAI-1 gene expression via MEK/ERK pathways. Thromb Haemost 2010, 104:1219-1227.
47. Chen L.C., Yeh T.M., Lin Y.Y., Wang Y.F., Su S.J., Chen C.Y., et al. The envelope glycoprotein domain III of dengue virus type 2 induced the expression of anticoagulant molecules in endothelial cells. Mol Cell Biochem 2010, 342:215-221.
48. Chen L.C., Shyu H.W., Lin H.M., Lei H.Y., Lin Y.S., Liu H.S., et al. Dengue virus induces thrombomodulin expression in human endothelial cells and monocytes in vitro. J Infect 2009, 58:368-374.
49. Stearns-Kurosawa D.J., Kurosawa S., Mollica J.S., Ferrell G.L., Esmon C.T. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci U S A 1996, 93:10212-10216.
50. Butthep P., Chunhakan S., Tangnararatchakit K., Yoksan S., Pattanapanyasat K., Chuansumrit A. Elevated soluble thrombomodulin in the febrile stage related to patients at risk for dengue shock syndrome. Pediatr Infect Dis J 2006, 25:894-897.
51. Gutsche I., Coulibaly F., Voss J.E., Salmon J., d'Alayer J., Ermonval M., et al. Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein. Proc Natl Acad Sci U S A 2011, 108:8003-8008.
52. Libraty D.H., Young P.R., Pickering D., Endy T.P., Kalayanarooj S., Green S., et al. High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J Infect Dis 2002, 186:1165-1168.
53. Avirutnan P., Zhang L., Punyadee N., Manuyakorn A., Puttikhunt C., Kasinrerk W., et al. Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog 2007, 3:e183.
54. Avirutnan P., Fuchs A., Hauhart R.E., Somnuke P., Youn S., Diamond M.S., et al. Antagonism of the complement component C4 by flavivirus nonstructural protein NS1. J Exp Med 2010, 207:793-806.
55. Somnuke P., Hauhart R.E., Atkinson J.P., Diamond M.S., Avirutnan P. N-linked glycosylation of dengue virus NS1 protein modulates secretion, cell-surface expression, hexamer stability, and interactions with human complement. Virology 2011, 413:253-264.
56. Lin S.W., Chuang Y.C., Lin Y.S., Lei H.Y., Liu H.S., Yeh T.M. Dengue virus nonstructural protein NS1 binds to prothrombin/thrombin and inhibits prothrombin activation. J Infect 2012, 64:325-334.
57. Wills B., Tran V.N., Nguyen T.H., Truong T.T., Tran T.N., Nguyen M.D., et al. Hemostatic changes in Vietnamese children with mild dengue correlate with the severity of vascular leakage rather than bleeding. Am J Trop Med Hyg 2009, 81:638-644.