Autoimmunity in dengue pathogenesis

Journal of the Formosan Medical Association

Volumn 112, Issue 1, 2013, Pages 3-11

  Wan, Shu Wen ^a,b   Lin, Chiou Feng ^a,b   Yeh, Trai Ming ^a,b   Liu, Ching Chuan ^b,c   Liu, Hsiao Sheng ^a,b   Wang, Shuying ^a,b   Ling, Pin ^a,b   Anderson, Robert ^a,b,d   Lei, Huan Yao ^a,b   Lin, Yee Shin ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^d DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Autoimmunity; Dengue; Immunopathogenesis

Indexed keywords

AUTOANTIBODY; DENGUE VACCINE; INTERFERON; VIRUS PROTEIN;

AUTOIMMUNITY; BLEEDING; CELLULAR IMMUNITY; CROSS REACTION; DENGUE; DENGUE VIRUS; DISEASE SEVERITY; ENDOTHELIUM CELL; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; NONHUMAN; REVIEW; THROMBOCYTE; THROMBOCYTOPENIA; TROPISM; VASCULAR DISEASE; VASCULAR LEAKAGE;

ANTIBODY-DEPENDENT ENHANCEMENT; AUTOIMMUNITY; CYTOKINES; DENGUE; DENGUE VIRUS; HUMANS; IMMUNITY, CELLULAR; VIRAL VACCINES;

EID: 84872372074     PISSN: None     EISSN: 09296646     Source Type: Journal    
DOI: 10.1016/j.jfma.2012.11.006     Document Type: Review

References (100)

1. Monath T.P. Dengue: the risk to developed and developing countries. Proc Natl Acad Sci U S A 1994, 91:2395-2400.
2. Guzman M.G., Halstead S.B., Artsob H., Buchy P., Farrar J., Gubler D.J., et al. Dengue: a continuing global threat. Nat Rev Microbiol 2010, 8:S7-16.
3. Guzman A., Isturiz R.E. Update on the global spread of dengue. Int J Antimicrob Agents 2010, 36(Suppl. 1):S40-S42.
4. Lin C.C., Huang Y.H., Shu P.Y., Wu H.S., Lin Y.S., Yeh T.M., et al. Characteristic of dengue disease in Taiwan: 2002-2007. Am J Trop Med Hyg 2010, 82:731-739.
5. Chang S.F., Huang J.H., Shu P.Y. Characteristics of dengue epidemics in Taiwan. J Formos Med Assoc 2012, 111:297-299.
6. Henchal E.A., Putnak J.R. The dengue viruses. Clin Microbiol Rev 1990, 3:376-396.
7. Clyde K., Kyle J.L., Harris E. Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J Virol 2006, 80:11418-11431.
8. Rodenhuis-Zybert I.A., Wilschut J., Smit J.M. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci 2010, 67:2773-2786.
9. Gubler D.J. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 1998, 11:480-496.
10. Kittigul L., Pitakarnjanakul P., Sujirarat D., Siripanichgon K. The differences of clinical manifestations and laboratory findings in children and adults with dengue virus infection. J Clin Virol 2007, 39:76-81.
11. Martina B.E., Koraka P., Osterhaus A.D. Dengue virus pathogenesis: an integrated view. Clin Microbiol Rev 2009, 22:564-581.
12. Murphy B.R., Whitehead S.S. Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 2011, 29:587-619.
13. Bandyopadhyay S., Lum L.C.S., Kroeger A. Classifying dengue: a review of the difficulties in using the WHO case classification for dengue haemorrhagic fever. Trop Med Int Health 2006, 11:1238-1255.
14. Barniol J., Gaczkowski R., Barbato E.V., da Cunha R.V., Salgado D., Martinez E., et al. Usefulness and applicability of the revised dengue case classification by disease: multi-centre study in 18 countries. BMC Infect Dis 2011, 11:106-117.
15. Whitehorn J., Simmons C.P. The pathogenesis of dengue. Vaccine 2011, 29:7221-7228.
16. Lin C.F., Wan S.W., Cheng H.J., Lei H.Y., Lin Y.S. Autoimmune pathogenesis in dengue virus infection. Viral Immunol 2006, 19:127-132.
17. 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.
18. Pandey B.D., Morita K., Hasebe F., Parquet M.C., Igarashi A. Molecular evolution, distribution and genetic relationship among the dengue 2 viruses isolated from different clinical severity. Southeast Asian J Trop Med Public Health 2000, 31:266-272.
19. Vaughn D.W., Green S., Kalayanarooj S., Innis B.L., Nimmannitya S., Suntayakorn S., et al. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 2000, 181:2-9.
20. Cologna R., Rico-Hesse R. American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J Virol 2003, 77:3929-3938.
21. Leitmeyer K.C., Vaughn D.W., Watts D.M., Salas R., Villalobos I., de C., et al. Dengue virus structural differences that correlate with pathogenesis. J Virol 1999, 73:4738-4747.
22. Prestwood T.R., Prigozhin D.M., Sharar K.L., Zellweger R.M., Shresta S. A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 2008, 82:8411-8421.
23. Wu S.J., Grouard-Vogel G., Sun W., Mascola J.R., Brachtel E., Putvatana R., et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med 2000, 6:816-820.
24. Kou Z., Quinn M., Chen H., Rodrigo W.W., Rose R.C., Schlesinger J.J., et al. Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells. J Med Virol 2008, 80:134-146.
25. Paes M.V., Lenzi H.L., Nogueira A.C., Nuovo G.J., Pinhao A.T., Mota E.M., et al. Hepatic damage associated with dengue-2 virus replication in liver cells of BALB/c mice. Lab Invest 2009, 89:1140-1151.
26. Chen H.C., Hofman F.M., Kung J.T., Lin Y.D., Wu-Hsieh B.A. Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 2007, 81:5518-5526.
27. 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.
28. Despres P., Frenkiel M.P., Ceccaldi P.E., Duarte Dos Santos C., Deubel V. Apoptosis in the mouse central nervous system in response to infection with mouse-neurovirulent dengue viruses. J Virol 1998, 72:823-829.
29. Lee E., Lobigs M. Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry. J Virol 2000, 74:8867-8875.
30. Halstead S.B. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 2003, 60:421-467.
31. Huang K.J., Yang Y.C., Lin Y.S., Huang J.H., Liu H.S., Yeh T.M., et al. The dual-specific binding of dengue virus and target cells for the antibody-dependent enhancement of dengue virus infection. J Immunol 2006, 176:2825-2832.
32. Wang S., He R.T., Patarapotikul J., Innis B.L., Anderson R. Antibody-enhanced binding of dengue virus to human platelets. Virology 1995, 213:254-257.
33. Ubol S., Phuklia W., Kalayanarooj S., Modhiran N. Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 2010, 201:923-935.
34. Ubol S., Halstead S.B. How innate immune mechanisms contribute to antibody-enhanced viral infections. Clin Vaccine Immunol 2010, 17:1829-1835.
35. Halstead S.B., Mahalingam S., Marovich M.A., Ubol S., Mosser D.M. Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 2010, 10:712-722.
36. Anderson R., Wang S., Osiowy C., Issekutz A.C. Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes. J Virol 1997, 71:4226-4232.
37. King C., Anderson R., Marshall J.S. Dengue virus selectively induces human mast cell chemokine production. J Virol 2002, 76:8408-8419.
38. Brown M.G., King C.A., Sherren C., Marshall J.S., Anderson R. A dominant role for FcγRII in antibody-enhanced dengue virus infection of human mast cells and associated CCL5 release. J Leuk Biol 2006, 80:1242-1250.
39. Brown M.G., McAlpine S.M., Huang Y.Y., Haidl I., Al-Afif A., Marshall J.S., et al. RNA sensors enable human mast cell anti-viral chemokine production and IFN-mediated protection in response to antibody-enhanced dengue virus infection. PLoS One 2012, 7:e34055.
40. Brown M.G., Huang Y.Y., Marshall J.S., King C.A., Hoskin D.W., Anderson R. Dramatic caspase-dependent apoptosis in antibody-enhanced dengue virus infection of human mast cells. J Leukoc Biol 2009, 85:71-80.
41. Brown M.G., Hermann L.L., Issekutz A.C., Marshall J.S., Rowter D., Al-Afif A., et al. Dengue virus infection of mast cells triggers endothelial cell activation. J Virol 2011, 85:1145-1150.
42. Selin L.K., Varga S.M., Wong I.C., Welsh R.M. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J Exp Med 1998, 188:1705-1715.
43. Kurane I., Innis B.L., Nimmannitya S., Nisalak A., Meager A., Janus J., et al. Activation of T lymphocytes in dengue virus infections. High levels of soluble interleukin 2 receptor, soluble CD4, soluble CD8, interleukin 2, and interferon-gamma in sera of children with dengue. J Clin Invest 1991, 88:1473-1480.
44. + T cells to heterologous serotypes. J Immunol 2005, 175:2676-2683.
45. Hatch S., Endy T.P., Thomas S., Mathew A., Potts J., Pazoles P., et al. Intracellular cytokine production by dengue virus-specific T cells correlates with subclinical secondary infection. J Infect Dis 2011, 203:1282-1291.
46. Gagnon S.J., Ennis F.A., Rothman A.L. Bystander target cell lysis and cytokine production by dengue virus-specific human CD4(+) cytotoxic T-lymphocyte clones. J Virol 1999, 73:3623-3629.
47. Chen H.C., Lai S.Y., Sung J.M., Lee S.H., Lin Y.C., Wang W.K., et al. Lymphocyte activation and hepatic cellular infiltration in immunocompetent mice infected by dengue virus. J Med Virol 2004, 73:419-431.
48. high regulatory T cells in acute dengue infection. J Exp Med 2007, 204:979-985.
49. Hober D., Poli L., Roblin B., Gestas P., Chungue E., Granic G., et al. Serum levels of tumor necrosis factor-alpha (TNF-alpha), interleukin-6 (IL-6), and interleukin-1 beta (IL-1 beta) in dengue-infected patients. Am J Trop Med Hyg 1993, 48:324-331.
50. Chaturvedi U.C. Shift to Th2 cytokine response in dengue haemorrhagic fever. Indian J Med Res 2009, 129:1-3.
51. Raghupathy R., Chaturvedi U.C., Al-Sayer H., Elbishbishi E.A., Agarwal R., Nagar R., et al. Elevated levels of IL-8 in dengue hemorrhagic fever. J Med Virol 1998, 56:280-285.
52. Green S., Vaughn D.W., Kalayanarooj S., Nimmannitya S., Suntayakorn S., Nisalak A., et al. Elevated plasma interleukin-10 levels in acute dengue correlate with disease severity. J Med Virol 1999, 59:329-334.
53. Mustafa A.S., Elbishbishi E.A., Agarwal R., Chaturvedi U.C. Elevated levels of interleukin-13 and IL-18 in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol 2001, 30:229-233.
54. Agarwal R., Elbishbishi E.A., Chaturvedi U.C., Nagar R., Mustafa A.S. Profile of transforming growth factor-beta 1 in patients with dengue haemorrhagic fever. Int J Exp Pathol 1999, 80:143-149.
55. Hober D., Nguyen T.L., Shen L., Ha D.Q., Huong V.T., Benyoucef S., et al. Tumor necrosis factor alpha levels in plasma and whole-blood culture in dengue-infected patients: relationship between virus detection and pre-existing specific antibodies. J Med Virol 1998, 54:210-218.
56. Chaturvedi U.C., Agarwal R., Elbishbishi E.A., Mustafa A.S. Cytokine cascade in dengue hemorrhagic fever: implications for pathogenesis. FEMS Immunol Med Microbiol 2000, 28:183-188.
57. Lee Y.R., Liu M.T., Lei H.Y., Liu C.C., Wu J.M., Tung Y.C., et al. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 2006, 87:3623-3630.
58. 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.
59. Shresta S., Sharar K.L., Prigozhin D.M., Beatty P.R., Harris E. Murine model for dengue virus-induced lethal disease with increased vascular permeability. J Virol 2006, 80:10208-10217.
60. Carr J.M., Hocking H., Bunting K., Wright P.J., Davidson A., Gamble J., et al. Supernatants from dengue virus type-2 infected macrophages induce permeability changes in endothelial cell monolayers. J Med Virol 2003, 69:521-528.
61. Talavera D., Castillo A.M., Dominguez M.C., Gutierrez A.E., Meza I. IL8 release, tight junction and cytoskeleton dynamic reorganization conducive to permeability increase are induced by dengue virus infection of microvascular endothelial monolayers. J Gen Virol 2004, 85:1801-1813.
62. 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.
63. Luplertlop N., Misse D., Bray D., Deleuze V., Gonzalez J.P., Leardkamolkarn V., et al. Dengue-virus-infected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 2006, 7:1176-1181.
64. Luplertlop N., Misse D. MMP cellular responses to dengue virus infection-induced vascular leakage. Jpn J Infect Dis 2008, 61:298-301.
65. Suharti C., van Gorp E.C., Setiati T.E., Dolmans W.M., Djokomoeljanto R.J., Hack C.E., et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost 2002, 87:42-46.
66. Rachman A., Rinaldi I. Coagulopathy in dengue infection and the role of interleukin-6. Acta Med Indones 2006, 38:105-108.
67. Huerta-Zepeda A., Cabello-Gutierrez C., Cime-Castillo J., Monroy-Martinez V., Manjarrez-Zavala M.E., Gutierrez-Rodriguez M., et al. Crosstalk between coagulation and inflammation during dengue virus infection. Thromb Haemost 2008, 99:936-943.
68. Juffrie M., van Der Meer G.M., Hack C.E., Haasnoot K., Sutaryo, Veerman A.J., et al. Inflammatory mediators in dengue virus infection in children: interleukin-8 and its relationship to neutrophil degranulation. Infect Immun 2000, 68:702-707.
69. Azeredo E.L., Zagne S.M., Santiago M.A., Gouvea A.S., Santana A.A., Neves-Souza P.C., et al. Characterisation of lymphocyte response and cytokine patterns in patients with dengue fever. Immunobiology 2001, 204:494-507.
70. Avirutnan P., Punyadee N., Noisakran S., Komoltri C., Thiemmeca S., Auethavornanan K., et al. Vascular leakage in severe dengue virus infections: a potential role for the nonstructural viral protein NS1 and complement. J Infect Dis 2006, 193:1078-1088.
71. Nascimento E.J., Silva A.M., Cordeiro M.T., Brito C.A., Gil L.H., Braga-Neto U., et al. Alternative complement pathway deregulation is correlated with dengue severity. PLoS One 2009, 4:e6782. 10.1371/journal.pone.0006782.
72. Avirutnan P., Malasit P., Seliger B., Bhakdi S., Husmann M. Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 1998, 161:6338-6346.
73. 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 2011, 236:515-523.
74. 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.
75. Oishi K., Inoue S., Cinco M.T., Dimaano E.M., Alera M.T., Alfon J.A., et al. Correlation between increased platelet-associated IgG and thrombocytopenia in secondary dengue virus infections. J Med Virol 2003, 71:259-264.
76. Saito M., Oishi K., Inoue S., Dimaano E.M., Alera M.T., Alfon J.A., et al. Association of increased platelet-associated immunoglobulins with thrombocytopenia and the severity of disease in secondary dengue virus infections. Clin Exp Immunol 2004, 138:299-303.
77. Falconar A.K. The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol 1997, 142:897-916.
78. Lin C.F., Lei H.Y., Shiau A.L., Liu C.C., Liu H.S., Yeh T.M., et al. Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J Med Virol 2003, 69:82-90.
79. 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.
80. 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.
81. Falconar A.K. Antibody responses are generated to immunodominant ELK/KLE-type motifs on the nonstructural-1 glycoprotein during live dengue virus infections in mice and humans: implications for diagnosis, pathogenesis, and vaccine design. Clin Vaccine Immunol 2007, 14:493-504.
82. Liu I.J., Chiu C.Y., Chen Y.C., Wu H.C. Molecular mimicry of human endothelial cell antigen by autoantibodies to nonstructural protein 1 of dengue virus. J Biol Chem 2011, 286:9726-9736.
83. Lin C.F., Lei H.Y., Lin Y.S., Liu C.C., Anderson R. Patient and mouse antibodies against Dengue virus nonstructural protein 1 cross-react with platelets and cause their dysfunction or depletion. Am J Infect Dis 2008, 4:69-75.
84. 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.
85. Lin C.F., Chiu S.C., Hsiao Y.L., Wan S.W., Lei H.Y., Shiau A.L., et al. Expression of cytokine, chemokine, and adhesion molecules during endothelial cell activation induced by antibodies against dengue virus nonstructural protein 1. J Immunol 2005, 174:395-403.
86. 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.
87. 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 2009, 234:63-73.
88. Cheng H.J., Lei H.Y., Lin C.F., Luo Y.H., Wan S.W., Liu H.S., et al. Anti-dengue virus nonstructural protein 1 antibodies recognize protein disulfide isomerase on platelets and inhibit platelet aggregation. Mol Immunol 2009, 47:398-406.
89. Chen M.C., Lin C.F., Lei H.Y., Lin S.C., Liu H.S., Yeh T.M., et al. Deletion of the C-terminal region of dengue virus nonstructural protein 1 (NS1) abolishes anti-NS1-mediated platelet dysfunction and bleeding tendency. J Immunol 2009, 183:1797-1803.
90. Wan S.W., Lin C.F., Chen M.C., Lei H.Y., Liu H.S., Yeh T.M., et al. C-terminal region of dengue virus nonstructural protein 1 is involved in endothelial cell cross-reactivity via molecular mimicry. Am J Infect Dis 2008, 4:85-91.
91. Chang H.H., Shyu H.F., Wang Y.M., Sun D.S., Shyu R.H., Tang S.S., et al. 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 2002, 186:743-751.
92. 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.
93. 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.
94. 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.
95. Jardim D.L., Tsukumo D.M., Angerami R.N., Carvalho Filho M.A., Saad M.J. Autoimmune features caused by dengue fever: a case report. Braz J Infect Dis 2012, 16:92-95.
96. Rajadhyaksha A., Mehra S. Dengue fever evolving into systemic lupus erythematosus and lupus nephritis: a case report. Lupus 2012, 21:999-1002.
97. Garcia G., Gonzalez N., Perez A.B., Sierra B., Aguirre E., Rizo D., et al. Long-term persistence of clinical symptoms in dengue-infected persons and its association with immunological disorders. Int J Infect Dis 2010, 15:e38-e43.
98. Thomas S.J., Endy T.P. Critical issues in dengue vaccine development. Curr Opin Infect Dis 2011, 24:442-450.
99. Schlesinger J.J., Brandriss M.W., Walsh E.E. Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus non-structural glycoprotein NS1. J Gen Virol 1987, 68(Pt 3):853-857.
100. Henchal E.A., Henchal L.S., Schlesinger J.J. Synergistic interactions of anti-NS1 monoclonal antibodies protect passively immunized mice from lethal challenge with dengue 2 virus. J Gen Virol 1988, 69(Pt 8):2101-2107.