Endothelial cell sensitization by death receptor fractions of an anti-dengue nonstructural protein 1 antibody induced plasma leakage, coagulopathy, and mortality in mice

Journal of Immunology

Volumn 195, Issue 6, 2015, Pages 2743-2753

  Sun, Der Shan ^a   Chang, Ying Chen ^a,e   Lien, Te Sheng ^a   King, Chwan Chuen ^b   Shih, Yung Luen ^c,d   Huang, Hsuan Shun ^a,e   Wang, Teng Yi ^a   Li, Chen Ru ^a   Lee, Chin Cheng ^c   Hsu, Ping Ning ^b   Chang, Hsin Hou ^a  

^a TZU CHI UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; DEATH RECEPTOR 4; IMMUNOGLOBULIN G; NONSTRUCTURAL PROTEIN 1 ANTIBODY; PROTEIN ANTIBODY; THROMBOMODULIN; UNCLASSIFIED DRUG; ANTIBODY; ANTICOAGULANT AGENT; NS1 PROTEIN, DENGUE VIRUS TYPE 2; SMALL INTERFERING RNA; TNFRSF10A PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; VIRUS PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD CLOTTING DISORDER; CLINICAL ARTICLE; CROSS REACTION; CYTOTOXICITY; DENGUE; EMBRYO; ENDOTHELIUM CELL; HEMATOLOGIC DISEASE; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PLASMA LEAKAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; ANIMAL; BIOSYNTHESIS; BLOOD CLOTTING; CELL LINE; CELL SURVIVAL; CHICK EMBRYO; DENGUE VIRUS; GENETICS; IMMUNOLOGY; MOSQUITO; PATHOLOGY; RABBIT; RNA INTERFERENCE;

ANIMALS; ANTIBODIES; ANTICOAGULANTS; APOPTOSIS; AUTOANTIBODIES; BLOOD COAGULATION; CELL LINE; CELL SURVIVAL; CHICK EMBRYO; CULICIDAE; DENGUE VIRUS; ENDOTHELIAL CELLS; HUMANS; IMMUNOGLOBULIN G; MICE; RABBITS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA INTERFERENCE; RNA, SMALL INTERFERING; SEVERE DENGUE; THROMBOMODULIN; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84941773519     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500136     Document Type: Article

References (68)

1. Bhatt, S., P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, et al. 2013. The global distribution and burden of dengue. Nature 496: 504-507.
2. Tomashek, K. M., T. M. Sharp, and H. S. Margolis. 2015. Chapter 3. Infectious diseases related to travel-dengue. In Travelers' Health (Yellow Book 2016). U.S. Centers for Disease Control and Prevention, Atlanta, GA. Available at: http:// wwwnc.cdc.gov/travel/yellowbook/2016/infectious-diseases-related-to-travel/ dengue. Accessed: July 28, 2015.
3. Guzman, M. G., and E. Harris. 2015. Dengue. Lancet 385: 453-465.
4. Halstead, S. B. 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239: 476-481.
5. Halstead, S. B. 2007. Dengue. Lancet 370: 1644-1652.
6. Suhrbier, A., and M. La Linn. 2003. Suppression of antiviral responses by antibodydependent enhancement of macrophage infection. Trends Immunol. 24: 165-168.
7. Sun, D. S., C. C. King, H. S. Huang, Y. L. Shih, C. C. Lee, W. J. Tsai, C. C. Yu, and H. H. Chang. 2007. Antiplatelet autoantibodies elicited by dengue virus nonstructural protein 1 cause thrombocytopenia and mortality in mice. J. Thromb. Haemost. 5: 2291-2299.
8. Chang, H. H., H. F. Shyu, Y. M. Wang, D. S. Sun, R. H. Shyu, S. S. Tang, and Y. S. Huang. 2002. Facilitation of cell adhesion by immobilized dengue viral nonstructural protein 1 (NS1): arginine-glycine-aspartic acid structural mimicry within the dengue viral NS1 antigen. J. Infect. Dis. 186: 743-751.
9. Lin, C. F., S. W. Wan, M. C. Chen, S. C. Lin, C. C. Cheng, S. C. Chiu, Y. L. Hsiao, H. Y. Lei, H. S. Liu, T. M. Yeh, and Y. S. Lin. 2008. Liver injury caused by antibodies against dengue virus nonstructural protein 1 in a murine model. Lab. Invest. 88: 1079-1089.
10. Chuang, Y. C., S. Y. Wang, Y. S. Lin, H. R. Chen, and T. M. Yeh. 2013. Reevaluation of the pathogenic roles of nonstructural protein 1 and its antibodies during dengue virus infection. J. Biomed. Sci. 20: 42.
11. Oishi, K., S. Inoue, M. T. Cinco, E. M. Dimaano, M. T. Alera, J. A. Alfon, F. Abanes, D. J. Cruz, R. R. Matias, H. Matsuura, et al. 2003. Correlation between increased platelet-associated IgG and thrombocytopenia in secondary dengue virus infections. J. Med. Virol. 71: 259-264.
12. Saito, M., K. Oishi, S. Inoue, E. M. Dimaano, M. T. Alera, A. M. Robles, B. D. Estrella, Jr., A. Kumatori, K. Moji, M. T. Alonzo, et al. 2004. Association of increased platelet-associated immunoglobulins with thrombocytopenia and the severity of disease in secondary dengue virus infections. Clin. Exp. Immunol. 138: 299-303.
13. Honda, S., M. Saito, E. M. Dimaano, P. A. Morales, M. T. Alonzo, L. A. Suarez, N. Koike, S. Inoue, A. Kumatori, R. R. Matias, et al. 2009. Increased phagocytosis of platelets from patients with secondary dengue virus infection by human macrophages. Am. J. Trop. Med. Hyg. 80: 841-845.
14. Chen, C. L., C. F. Lin, S. W. Wan, L. S. Wei, M. C. Chen, T. M. Yeh, H. S. Liu, R. Anderson, and Y. S. Lin. 2013. Anti-dengue virus nonstructural protein 1 antibodies cause NO-mediated endothelial cell apoptosis via ceramide-regulated glycogen synthase kinase-3b and NF-kB activation. J. Immunol. 191: 1744-1752.
15. Chuang, Y. C., Y. S. Lin, H. S. Liu, J. R. Wang, and T. M. Yeh. 2013. Antibodies against thrombin in dengue patients contain both anti-thrombotic and profibrinolytic activities. Thromb. Haemost. 110: 358-365.
16. Wang, S., and W. S. El-Deiry. 2003. TRAIL and apoptosis induction by TNFfamily death receptors. Oncogene 22: 8628-8633.
17. Wilson, N. S., V. Dixit, and A. Ashkenazi. 2009. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat. Immunol. 10: 348-355.
18. Silke, J. 2011. The regulation of TNF signalling: what a tangled web we weave. Curr. Opin. Immunol. 23: 620-626.
19. Georgakis, G. V., Y. Li, R. Humphreys, M. Andreeff, S. O'Brien, M. Younes, A. Carbone, V. Albert, and A. Younes. 2005. Activity of selective fully human agonistic antibodies to the TRAIL death receptors TRAIL-R1 and TRAIL-R2 in primary and cultured lymphoma cells: induction of apoptosis and enhancement of doxorubicin- and bortezomib-induced cell death. Br. J. Haematol. 130: 501-510.
20. Pukac, L., P. Kanakaraj, R. Humphreys, R. Alderson, M. Bloom, C. Sung, T. Riccobene, R. Johnson, M. Fiscella, A. Mahoney, et al. 2005. HGS-ETR1, a fully human TRAIL-receptor 1 monoclonal antibody, induces cell death in multiple tumour types in vitro and in vivo. Br. J. Cancer 92: 1430-1441.
21. Srikiatkhachorn, A. 2009. Plasma leakage in dengue haemorrhagic fever. Thromb. Haemost. 102: 1042-1049.
22. Wills, B. A., E. E. Oragui, A. C. Stephens, O. A. Daramola, N. M. Dung, H. T. Loan, N. V. Chau, M. Chambers, K. Stepniewska, J. J. Farrar, and M. Levin. 2002. Coagulation abnormalities in dengue hemorrhagic fever: serial investigations in 167 Vietnamese children with Dengue shock syndrome. Clin. Infect. Dis. 35: 277-285.
23. Nguyen, T. H., H. Y. Lei, T. L. Nguyen, Y. S. Lin, K. J. Huang, B. L. Le, C. F. Lin, T. M. Yeh, Q. H. Do, T. Q. Vu, et al. 2004. Dengue hemorrhagic fever in infants: a study of clinical and cytokine profiles. J. Infect. Dis. 189: 221-232.
24. World Health Organization. 1997. Dengue Haemorrhagic Fever: Diagnosis, Treatment, Prevention and Control, 2nd Ed. World Health Organization, Geneva, p. 12-23.
25. World Health Organization. 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. World Health Organization, Geneva.
26. Inglis, J. 2014. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Lien, T. S., D. S. Sun, C. M. Chang, C. Y. Wu, M. S. Dai, H. Chan, W. S. Wu, S. H. Su, Y. Y. Lin, and H. H. Chang. 2015. Dengue virus and antiplatelet autoantibodies synergistically induce haemorrhage through Nlrp3-inflammasome and FcgRIII. Thromb. Haemost. 113: 1060-1070.
28. Huang, H. S., D. S. Sun, T. S. Lien, and H. H. Chang. 2010. Dendritic cells modulate platelet activity in IVIg-mediated amelioration of ITP in mice. Blood 116: 5002-5009.
29. Chang, H. H., Y. W. Chiang, T. K. Lin, G. L. Lin, Y. Y. Lin, J. H. Kau, H. H. Huang, H. L. Hsu, J. H. Wang, and D. S. Sun. 2014. Erythrocytic mobilization enhanced by the granulocyte colony-stimulating factor is associated with reduced anthrax-lethal-toxin-induced mortality in mice. PLoS One 9: e111149.
30. Chang, H. H., T. P. Wang, P. K. Chen, Y. Y. Lin, C. H. Liao, T. K. Lin, Y. W. Chiang, W. B. Lin, C. Y. Chiang, J. H. Kau, et al. 2013. Erythropoiesis suppression is associated with anthrax lethal toxin-mediated pathogenic progression. PLoS One 8: e71718.
31. Chen, P. K., H. H. Chang, G. L. Lin, T. P. Wang, Y. L. Lai, T. K. Lin, M. C. Hsieh, J. H. Kau, H. H. Huang, H. L. Hsu, et al. 2013. Suppressive effects of anthrax lethal toxin on megakaryopoiesis. PLoS One 8: e59512.
32. Wu, M. S., D. S. Sun, Y. C. Lin, C. L. Cheng, S. C. Hung, P. K. Chen, J. H. Yang, and H. H. Chang. 2015. Nanodiamonds protect skin from ultraviolet B-induced damage in mice. J. Nanobiotechnology 13: 35.
33. Bonner, S. M., and M. A. O'Sullivan. 1998. Endothelial cell monolayers as a model system to investigate dengue shock syndrome. J. Virol. Methods 71: 159-167.
34. Gudgeon, J. R., and W. Martin. 1989. Modulation of arterial endothelial permeability: studies on an in vitro model. Br. J. Pharmacol. 98: 1267-1274.
35. Arora, N., R. Masood, T. Zheng, J. Cai, D. L. Smith, and P. S. Gill. 1999. Vascular endothelial growth factor chimeric toxin is highly active against endothelial cells. Cancer Res. 59: 183-188.
36. Kau, J. H., D. S. Sun, W. J. Tsai, H. F. Shyu, H. H. Huang, H. C. Lin, and H. H. Chang. 2005. Antiplatelet activities of anthrax lethal toxin are associated with suppressed p42/44 and p38 mitogen-activated protein kinase pathways in the platelets. J. Infect. Dis. 192: 1465-1474.
37. Kau, J. H., Y. L. Shih, T. S. Lien, C. C. Lee, H. H. Huang, H. C. Lin, D. S. Sun, and H. H. Chang. 2012. Activated protein C ameliorates Bacillus anthracis lethal toxin-induced lethal pathogenesis in rats. J. Biomed. Sci. 19: 98.
38. Martin, F. A., R. P. Murphy, and P. M. Cummins. 2013. Thrombomodulin and the vascular endothelium: insights into functional, regulatory, and therapeutic aspects. Am. J. Physiol. Heart Circ. Physiol. 304: H1585-H1597.
39. Maroney, S. A., B. C. Cooley, R. Sood, H. Weiler, and A. E. Mast. 2008. Combined tissue factor pathway inhibitor and thrombomodulin deficiency produces an augmented hypercoagulable state with tissue-specific fibrin deposition. J. Thromb. Haemost. 6: 111-117.
40. Su, H. L., Y. L. Lin, H. P. Yu, C. H. Tsao, L. K. Chen, Y. T. Liu, and C. L. Liao. 2001. The effect of human bcl-2 and bcl-X genes on dengue virus-induced apoptosis in cultured cells. Virology 282: 141-153.
41. Lee, C. J., C. L. Liao, and Y. L. Lin. 2005. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 79: 8388-8399.
42. Lu, M. Y., and F. Liao. 2011. Interferon-stimulated gene ISG12b2 is localized to the inner mitochondrial membrane and mediates virus-induced cell death. Cell Death Differ. 18: 925-936.
43. Liu, Y., H. Liu, J. Zou, B. Zhang, and Z. Yuan. 2014. Dengue virus subgenomic RNA induces apoptosis through the Bcl-2-mediated PI3k/Akt signaling pathway. Virology 448: 15-25.
44. O'Reilly, R. A. 1998. Drugs used in disorders of coagulation. In Basic and Clinical Pharmacology, 7th Ed. B. G. Katzung, ed. Prentice Hall, San Francisco, p. 547-562.
45. Hermans, C., S. Eeckhoudt, and C. Lambert. 2012. Dabigatran etexilate (Pradaxa) for preventing warfarin-induced skin necrosis in a patient with severe protein C deficiency. Thromb. Haemost. 107: 1189-1191.
46. Sosothikul, D., P. Seksarn, S. Pongsewalak, U. Thisyakorn, and J. Lusher. 2007. Activation of endothelial cells, coagulation and fibrinolysis in children with Dengue virus infection. Thromb. Haemost. 97: 627-634.
47. Horan, J. T., and C. W. Francis. 2001. Fibrin degradation products, fibrin monomer and soluble fibrin in disseminated intravascular coagulation. Semin. Thromb. Hemost. 27: 657-666.
48. Inoue, H., H. Aizawa, K. Matsumoto, M. Shigyo, S. Takata, M. Hara, and N. Hara. 1997. Effect of b2-agonists on histamine-induced airway microvascular leakage in ozone-exposed guinea pigs. Am. J. Respir. Crit. Care Med. 156: 723-727.
49. Setrkraising, K., C. Bongsebandhu-phubhakdi, N. Voraphani, C. Pancharoen, U. Thisyakorn, and C. Thisyakorn. 2007. D-dimer as an indicator of dengue severity. Asian Biomed. 1: 53-57.
50. Esmon, C. T. 1999. Possible involvement of cytokines in diffuse intravascular coagulation and thrombosis. Best Pract. Res. Clin. Haematol. 12: 343-359.
51. Norman, K. E., M. J. Cotter, J. B. Stewart, K. B. Abbitt, M. Ali, B. E. Wagner, W. A. Wallace, S. B. Forlow, and P. G. Hellewell. 2003. Combined anticoagulant and antiselectin treatments prevent lethal intravascular coagulation. Blood 101: 921-928.
52. Gandini, M., C. Gras, E. L. Azeredo, L. M. d. O. Pinto, N. Smith, P. Despres, R. V. da Cunha, L. J. de Souza, C. F. Kubelka, and J.-P. Herbeuval. 2013. Dengue virus activates membrane TRAIL relocalization and IFN-a production by human plasmacytoid dendritic cells in vitro and in vivo. PLoS Negl. Trop. Dis. 7: e2257. Available at: http://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.00.02257.
53. Thongtan, T., S. Panyim, and D. R. Smith. 2004. Apoptosis in dengue virus infected liver cell lines HepG2 and Hep3B. J. Med. Virol. 72: 436-444.
54. Espina, L. M., N. J. Valero, J. M. Hernández, and J. A. Mosquera. 2003. Increased apoptosis and expression of tumor necrosis factor-alpha caused by infection of cultured human monocytes with dengue virus. Am. J. Trop. Med. Hyg. 68: 48-53.
55. Liew, K. J., and V. T. Chow. 2006. Microarray and real-time RT-PCR analyses of a novel set of differentially expressed human genes in ECV304 endothelial-like cells infected with dengue virus type 2. J. Virol. Methods 131: 47-57.
56. Tamatani, M., Y. H. Che, H. Matsuzaki, S. Ogawa, H. Okado, S. Miyake, T. Mizuno, and M. Tohyama. 1999. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkB activation in primary hippocampal neurons. J. Biol. Chem. 274: 8531-8538.
57. Levina, V., A. M. Marrangoni, R. DeMarco, E. Gorelik, and A. E. Lokshin. 2008. Multiple effects of TRAIL in human carcinoma cells: induction of apoptosis, senescence, proliferation, and cytokine production. Exp. Cell Res. 314: 1605-1616.
58. Bai, J., J. Sui, A. Demirjian, C. M. Vollmer, Jr., W. Marasco, and M. P. Callery. 2005. Predominant Bcl-XL knockdown disables antiapoptotic mechanisms: tumor necrosis factor-related apoptosis-inducing ligand-based triple chemotherapy overcomes chemoresistance in pancreatic cancer cells in vitro. Cancer Res. 65: 2344-2352.
59. Jung, K. J., K. J. Min, J. H. Bae, and T. K. Kwon. 2015. Carnosic acid sensitized TRAIL-mediated apoptosis through down-regulation of c-FLIP and Bcl-2 expression at the post translational levels and CHOP-dependent up-regulation of DR5, Bim, and PUMA expression in human carcinoma caki cells. Oncotarget 6: 1556-1568.
60. Kim, K., H. Nakagawa, P. Fei, A. K. Rustgi, and W. S. El-Deiry. 2004. Targeting Bcl-xL in esophageal squamous cancer to sensitize to chemotherapy plus TRAIL-induced apoptosis while normal epithelial cells are protected by blockade of caspase 9. Cell Death Differ. 11: 583-587.
61. Jang, J. Y., S. J. Kim, E. K. Cho, S. W. Jeong, E. J. Park, W. C. Lee, S. H. Lee, S. G. Kim, Y. S. Kim, H. S. Kim, et al. 2014. TRAIL enhances apoptosis of human hepatocellular carcinoma cells sensitized by hepatitis C virus infection: therapeutic implications. PLoS One 9: e98171.
62. Laforge, M., L. Campillo-Gimenez, V. Monceaux, M. C. Cumont, B. Hurtrel, J. Corbeil, J. Zaunders, C. Elbim, and J. Estaquier. 2011. HIV/SIV infection primes monocytes and dendritic cells for apoptosis. PLoS Pathog. 7: e1002087.
63. Lan, L., S. Gorke, S. J. Rau, M. B. Zeisel, E. Hildt, K. Himmelsbach, M. Carvajal-Yepes, R. Huber, T.Wakita, A. Schmitt-Graeff, et al. 2008. Hepatitis C virus infection sensitizes human hepatocytes to TRAIL-induced apoptosis in a caspase 9-dependent manner. J. Immunol. 181: 4926-4935.
64. Liang, X., Y. Liu, Q. Zhang, L. Gao, L. Han, C. Ma, L. Zhang, Y. H. Chen, and W. Sun. 2007. Hepatitis B virus sensitizes hepatocytes to TRAIL-induced apoptosis through Bax. J. Immunol. 178: 503-510.
65. Kotelkin, A., E. A. Prikhod'ko, J. I. Cohen, P. L. Collins, and A. Bukreyev. 2003. Respiratory syncytial virus infection sensitizes cells to apoptosis mediated by tumor necrosis factor-related apoptosis-inducing ligand. J. Virol. 77: 9156-9172.
66. Wynne, J. W., B. J. Shiell, G. A. Marsh, V. Boyd, J. A. Harper, K. Heesom, P. Monaghan, P. Zhou, J. Payne, R. Klein, et al. 2014. Proteomics informed by transcriptomics reveals Hendra virus sensitizes bat cells to TRAIL-mediated apoptosis. Genome Biol. 15: 532.
67. Janssen, H. L., H. Higuchi, A. Abdulkarim, and G. J. Gores. 2003. Hepatitis B virus enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) cytotoxicity by increasing TRAIL-R1/death receptor 4 expression. J. Hepatol. 39: 414-420.
68. Deng, Z., H. Yan, J. Hu, S. Zhang, P. Peng, Q. Liu, and D. Guo. 2012. Hepatitis C virus sensitizes host cells to TRAIL-induced apoptosis by up-regulating DR4 and DR5 via a MEK1-dependent pathway. PLoS One 7: e37700.