Therapeutic antibodies as a treatment option for dengue fever

Expert Review of Anti-Infective Therapy

Volumn 11, Issue 11, 2013, Pages 1147-1157

  Chan, Kuan Rong ^a   Ong, Eugenia Z ^a   Ooi, Eng Eong ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

antibody; antibody dependent enhancement; dengue; neutralization; therapeutics

Indexed keywords

ANTIVIRUS AGENT; DENGUE VACCINE; EPITOPE; FC RECEPTOR; IMMUNOGLOBULIN; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

ANTIBODY SPECIFICITY; ANTIVIRAL ACTIVITY; CROSS REACTION; DENGUE; DENGUE VIRUS; DRUG HALF LIFE; DRUG TARGETING; EPIDEMIC; HUMAN; INFECTION RISK; MACROPHAGE; MONOCYTE; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; REVIEW; RISK REDUCTION; SEROTYPE; VIRUS INHIBITION; VIRUS NEUTRALIZATION;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS REACTIONS; DENGUE; DENGUE VIRUS; HUMANS; IMMUNIZATION, PASSIVE; MODELS, IMMUNOLOGICAL;

EID: 84888384594     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/14787210.2013.839941     Document Type: Review

References (106)

1. Bhatt S, Gething PW, Brady OJ et al. The global distribution and burden of dengue. Nature 496(7446), 504-507 (2013
2. Simmons CP, Farrar JJ, Nguyen v V, Wills B. Dengue. N. Engl. J. Med. 366(15), 1423-1432 (2012
3. Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 10(2), 100-103 (2002
4. Gubler DJ. The changing epidemiology of yellow fever and dengue, 1900 to 2003: Full circle? Comp. Immunol. Microbiol. Infect. Dis. 27(5), 319-330 (2004
5. Gubler DJ, Meltzer M. Impact of dengue/dengue hemorrhagic fever on the developing world. Adv. Virus Res. 53, 35-70 (1999
6. Rigau-Perez JG, Clark GG, Gubler DJ, Reiter P, Sanders EJ, Vorndam AV. Dengue and dengue haemorrhagic fever. Lancet 352(9132), 971-977 (1998
7. Sabin AB. Research on dengue during World War II. Am. J. Trop. Med. Hyg. 1(1), 30-50 (1952
8. Imrie A, Meeks J, Gurary A et al. Antibody to dengue 1 detected more than 60 years after infection. Viral. Immunol. 20(4), 672-675 (2007
9. Murphy BR, Whitehead SS. Immune response to dengue virus and prospects for a vaccine. Ann. Rev. Immunol. 29, 587-619 (2011
10. Simmons CP, Chau TN, Thuy TT et al. Maternal antibody and viral factors in the pathogenesis of dengue virus in infants. J. Infect. Dis. 196(3), 416-424 (2007
11. Halstead SB. Pathogenesis of dengue: Challenges to molecular biology. Science 239(4839), 476-481 (1988
12. Kliks SC, Nimmanitya S, Nisalak A, Burke DS. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am. J. Trop. Med. Hyg. 38(2), 411-419 (1988
13. Gubler DJ, Clark GG. Community-based integrated control of Aedes aegypti: A brief overview of current programs. Am. J. Trop. Med. Hyg. 50(6 Suppl.), 50-60 (1994
14. Gubler DJ. Aedes aegypti and Aedes aegypti-borne disease control in the 1990s: Top down or bottom up. Charles Franklin Craig Lecture. Am. J. Trop. Med. Hyg. 40(6), 571-578 (1989
15. Goh KT. Changing epidemiology of dengue in Singapore. Lancet 346(8982), 1098 (1995
16. Ooi EE, Hart TJ, Tan HC, Chan SH. Dengue seroepidemiology in Singapore. Lancet 357(9257), 685-686 (2001
17. Ooi EE, Goh KT, Gubler DJ. Dengue prevention and 35 years of vector control in Singapore. Emerg. Infect. Dis. 12(6), 887-893 (2006
18. Halstead SB, ÓRourke EJ. Antibodyenhanced dengue virus infection in primate leukocytes. Nature 265(5596), 739-741 (1977
19. Halstead SB, ÓRourke EJ. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J. Exp. Med. 146(1), 201-217 (1977
20. Monath TP. Prospects for development of a vaccine against the West Nile virus. Ann. NY Acad. Sci. 951, 1-12 (2001
21. Guirakhoo F, Weltzin R, Chambers TJ et al. Recombinant chimeric yellow fever-dengue type 2 virus is immunogenic and protective in nonhuman primates. J. Virol. 74(12), 5477-5485 (2000
22. Guy B, Guirakhoo F, Barban V, Higgs S, Monath TP, Lang J. Preclinical and clinical development of YFV 17D-based chimeric vaccines against dengue, West Nile and Japanese encephalitis viruses. Vaccine 28(3), 632-649 (2010
23. Guy B. Immunogenicity of sanofi pasteur tetravalent dengue vaccine. J. Clin. Virol. 46 (Suppl. 2), S16-19 (2009
24. Sabchareon A, Wallace D, Sirivichayakul C et al. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: A randomised, controlled phase 2b trial. Lancet 380(9853), 1559-1567 (2012
25. Srikiatkhachorn A, Wichit S, Gibbons RV et al. Dengue viral RNA levels in peripheral blood mononuclear cells are associated with disease severity and preexisting dengue immune status. PloS ONE 7(12), e51335 (2012
26. Carter PJ. Potent antibody therapeutics by design. Nat. Rev. Immunol. 6(5), 343-357 (2006
27. Carter P. Improving the efficacy of antibody-based cancer therapies. Nat. Rev. Cancer 1(2), 118-129 (2001
28. Presta LG. Engineering antibodies for therapy. Curr. Pharma. Biotechnol. 3(3), 237-256 (2002
29. Marasco WA, Sui J. The growth and potential of human antiviral monoclonal antibody therapeutics. Nat. Biotechnol. 25(12), 1421-1434 (2007
30. Keller MA, Stiehm ER. Passive immunity in prevention and treatment of infectious diseases. Clin. Microbiol. Rev. 13(4), 602-614 (2000
31. Lai CY, Tsai WY, Lin SR et al. Antibodies to envelope glycoprotein of dengue virus during the natural course of infection are predominantly cross-reactive and recognize epitopes containing highly conserved residues at the fusion loop of domain II. J. virol. 82(13), 6631-6643 (2008
32. Beltramello M, Williams KL, Simmons CP et al. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe. 8(3), 271-283 (2010
33. Dejnirattisai W, Jumnainsong A, Onsirisakul N et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328(5979), 745-748 (2010
34. Kashmiri SV, De Pascalis R, Gonzales NR, Schlom J. SDR grafting-a new approach to antibody humanization. Methods 36(1), 25-34 (2005
35. Sloan SE, Hanlon C, Weldon W et al. Identification and characterization of a human monoclonal antibody that potently neutralizes a broad panel of rabies virus isolates. Vaccine 25(15), 2800-2810 (2007
36. Hoogenboom HR. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23(9), 1105-1116 (2005
37. Lanzavecchia A, Corti D, Sallusto F. Human monoclonal antibodies by immortalization of memory B cells. Curr. Opin. Biotechnol. 18(6), 523-528 (2007
38. Huang K, Incognito L, Cheng X, Ulbrandt ND, Wu H. Respiratory syncytial virus-neutralizing monoclonal antibodies motavizumab and palivizumab inhibit fusion. J. virol. 84(16), 8132-8140 (2010
39. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. The IMpact-RSV Study Group. Pediatrics 102(3 Pt 1), 531-537 (1998
40. Parnes C, Guillermin J, Habersang R et al. Palivizumab prophylaxis of respiratory syncytial virus disease in 2000-2001: Results from The Palivizumab Outcomes Registry. Pediatr. Pulmonol. 35(6), 484-489 (2003
41. Zhu Z, Bossart KN, Bishop KA et al. Exceptionally potent cross-reactive neutralization of Nipah and Hendra viruses by a human monoclonal antibody. J. Infect. Dis. 197(6), 846-853 (2008
42. Kuhn RJ, Zhang W, Rossmann MG et al. Structure of dengue virus: Implications for flavivirus organization, maturation, and fusion. Cell 108(5), 717-725 (2002
43. Rey FA. Dengue virus envelope glycoprotein structure: New insight into its interactions during viral entry. Proc. Natl Acad. Sci. USA 100(12), 6899-6901 (2003
44. Brien JD, Austin SK, Sukupolvi-Petty S et al. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J. Virol. 84(20), 10630-10643 (2010
45. Sukupolvi-Petty S, Austin SK, Engle M et al. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 84(18), 9227-9239 (2010
46. Sinclair R, Moult BJ, Mumford JA. Characterization of an antigenic site on glycoprotein 13 (gC) of equid herpesvirus type-1. Arch. Virol. 129(1-4), 327-336 (1993
47. Crill WD, Roehrig JT. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J. Virol. 75(16), 7769-7773 (2001
48. Shrestha B, Brien JD, Sukupolvi-Petty S et al. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virustype 1. PLoS pathog. 6(4), e1000823 (2010
49. de Alwis R, Beltramello M, Messer WB et al. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl. Trop. Dis. 5(6), e1188 (2011
50. Wahala WM, Huang C, Butrapet S, White LJ, de Silva AM. Recombinant dengue type 2 viruses with altered e protein domain III epitopes are efficiently neutralized by human immune sera. J. Virol. 86(7), 4019-4023 (2012
51. Williams KL, Wahala WM, Orozco S, de Silva AM, Harris E. Antibodies targeting dengue virus envelope domain III are not required for serotype-specific protection or prevention of enhancement in vivo. Virology 429(1), 12-20 (2012
52. de Alwis R, Smith SA, Olivarez NP et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl Acad. Sci. USA 109(19), 7439-7444 (2012
53. Teoh EP, Kukkaro P, Teo EW et al. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 4(139), 139ra183 (2012
54. Vogt MR, Moesker B, Goudsmit J et al. Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J. Virol. 83(13), 6494-6507 (2009
55. Kaufmann B, Vogt MR, Goudsmit J et al. Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Proc. Natl Acad. Sci. USA 107(44), 18950-18955 (2010
56. Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS pathog. 6(3), e1000821 (2010
57. Zou G, Kukkaro P, Lok SM et al. Resistance analysis of an antibody that selectively inhibits dengue virus serotype-1. Antivir. Res. 95(3), 216-223 (2012
58. Brien JD, Sukupolvi-Petty S, Williams KL et al. Protection by Immunoglobulin Dual-Affinity Retargeting Antibodies against Dengue Virus. J. Virol. 87(13), 7747-7753 (2013
59. Della-Porta AJ, Westaway EG. A multi-hit model for the neutralization of animal viruses. J. Gen. Virol. 38(1), 1-19 (1978
60. Dowd KA, Pierson TC. Antibody-mediated neutralization of flaviviruses: A reductionist view. Virology 411(2), 306-315 (2011
61. Pierson TC, Diamond MS. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert Rev. Mol. Med. 10, e12 (2008
62. Pierson TC, Xu Q, Nelson S et al. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe. 1(2), 135-145 (2007
63. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: Implications for vaccine development. Cell Host Microbe. 4(3), 229-238 (2008
64. Lok SM, Kostyuchenko V, Nybakken GE et al. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Bio. 15(3), 312-317 (2008
65. Gollins SW, Porterfield JS. A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature 321(6067), 244-246 (1986
66. Chen Y, Maguire T, Hileman RE et al. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3(8), 866-871 (1997
67. Reyes-Del Valle J, Chavez-Salinas S, Medina F, Del Angel RM. Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J. Virol. 79(8), 4557-4567 (2005
68. Chen YC, Wang SY, King CC. Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/ macrophages by blockade of virus entry via a CD14-dependent mechanism. J. Virol. 73(4), 2650-2657 (1999
69. Chen ST, Lin YL, Huang MT et al. CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453(7195), 672-676 (2008
70. Tassaneetrithep B, Burgess TH, Granelli-Piperno A et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197(7), 823-829 (2003
71. Miller JL, de Wet BJ, Martinez-Pomares L et al. The mannose receptor mediates dengue virus infection of macrophages. PLoS pathog. 4(2), e17 (2008
72. Chan KR, Zhang SL, Tan HC et al. Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection. Proc. Natl Acad. Sci. USA 108(30), 12479-12484 (2011
73. van der Schaar HM, Rust MJ, Chen C et al. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4(12), e1000244 (2008
74. Haas A. The phagosome: Compartment with a license to kill. Traffic 8(4), 311-330 (2007
75. Thompson BS, Moesker B, Smit JM, Wilschut J, Diamond MS, Fremont DH. A therapeutic antibody against west nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog. 5(5), e1000453 (2009
76. Kurane I, Hebblewaite D, Brandt WE, Ennis FA. Lysis of dengue virus-infected cells by natural cell-mediated cytotoxicity and antibody-dependent cell-mediated cytotoxicity. J. Virol. 52(1), 223-230 (1984
77. Nakamura M, Sasaki H, Terada M, Ohno T. Complement-dependent virolysis of HIV-1 with monoclonal antibody NM-01. AIDS Res. Hum Retroviruses 9(7), 619-626 (1993
78. Yamanaka A, Kosugi S, Konishi E. Infection-enhancing and -neutralizing activities of mouse monoclonal antibodies against dengue type 2 and 4 viruses are controlled by complement levels. J. Virol. 82(2), 927-937 (2008
79. Mehlhop E, Ansarah-Sobrinho C, Johnson S et al. Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host Microbe. 2(6), 417-426 (2007
80. Russell PK, Nisalak A. Dengue virus identification by the plaque reduction neutralization test. J. Immunol. 99(2), 291-296 (1967
81. Russell PK, Nisalak A, Sukhavachana P, Vivona S. A plaque reduction test for dengue virus neutralizing antibodies. J. Immunol. 99(2), 285-290 (1967
82. Endy TP, Nisalak A, Chunsuttitwat S et al. Relationship of preexisting dengue virus (DV) neutralizing antibody levels to viremia and severity of disease in a prospective cohort study of DV infection in Thailand. J. Infect. Dis. 189(6), 990-1000 (2004
83. Kou Z, Quinn M, Chen H et al. Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral bloodmononuclear cells. J. Med. Virol. 80(1), 134-146 (2008
84. Wu RS, Chan KR, Tan HC, Chow A, Allen JC Jr, Ooi EE. Neutralization of dengue virus in the presence of Fc receptor-mediated phagocytosis distinguishes serotype-specific from cross-neutralizing antibodies. Antivir. Res. 96(3), 340-343 (2012
85. Tharakaraman K, Robinson LN, Hatas A et al. Redesign of a cross-reactive antibody to dengue virus with broad-spectrum activity and increased in vivo potency. Proc. Natl Acad. Sci. USA 110(17), E1555-1564 (2013
86. Williams KL, Sukupolvi-Petty S, Beltramello M et al. Therapeutic efficacy of antibodies lacking FcgammaR against lethal dengue virus infection is due to neutralizing potency and blocking of enhancing antibodies. PLoS Pathog. 9(2), e1003157 (2013
87. Sapir T, Shoenfeld Y. Facing the enigma of immunomodulatory effects of intravenous immunoglobulin. Clin. Rev. Allergy Immunol. 29(3), 185-199 (2005
88. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313(5787), 670-673 (2006
89. Tackenberg B, Jelcic I, Baerenwaldt A et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc. Natl Acad. Sci. USA 106(12), 4788-4792 (2009
90. Jaiyen Y, Masrinoul P, Kalayanarooj S, Pulmanausahakul R, Ubol S. Characteristics of dengue virus-infected peripheral blood mononuclear cell death that correlates with the severity of illness. Microbiol. Immunol. 53(8), 442-450 (2009
91. Smith KG, Clatworthy MR. FcgammaRIIB in autoimmunity and infection: Evolutionary and therapeutic implications. Nat. Rev. Immunol. 10(5), 328-343 (2010
92. Zellweger RM, Prestwood TR, Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe. 7(2), 128-139 (2010
93. Balsitis SJ,Williams KL, Lachica R et al. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 6(2), e1000790 (2010
94. Wu AM, Yazaki PJ. Designer genes: Recombinant antibody fragments for biological imaging. Q. J. Nucl. Med. 44(3), 268-283 (2000
95. Bruhns P, Iannascoli B, England P et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113(16), 3716-3725 (2009
96. Jacobson JM, Kuritzkes DR, Godofsky E et al. Safety, pharmacokinetics, and antiretroviral activity of multiple doses of ibalizumab (formerly TNX-355), an anti-CD4 monoclonal antibody, in human immunodeficiency virus type 1-infected adults. Antimicrob. Agents Chemother. 53(2), 450-457 (2009
97. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc. Natl Acad. Sci. USA 104(22), 9422-9427 (2007
98. Burmeister WP, Huber AH, Bjorkman PJ. Crystal structure of the complex of rat neonatal Fc receptor with Fc. Nature 372(6504), 379-383 (1994
99. Hinton PR, Xiong JM, Johlfs MG, Tang MT, Keller S, Tsurushita N. An engineered human IgG1 antibody with longer serum half-life. J. Immunol. 176(1), 346-356 (2006
100. Datta-Mannan A, Witcher DR, Tang Y, Watkins J, Wroblewski VJ. Monoclonal antibody clearance. Impact of modulating the interaction of IgG with the neonatal Fc receptor. J. Biol. Chem. 282(3), 1709-1717 (2007
101. Liu XY, Pop LM, Vitetta ES. Engineering therapeutic monoclonal antibodies. Immunol. Rev. 222, 9-27 (2008). Discusses potential antibody modifications that can improve effector functions and pharmacokinetic properties of antibodies
102. Schieffelin JS, Costin JM, Nicholson CO et al. Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol. J. 7, 28 (2010
103. Smith SA, Zhou Y, Olivarez NP, Broadwater AH, de Silva AM, Crowe JE Jr. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J. Virol. 86(5), 2665-2675 (2012
104. Costin JM, Zaitseva E, Kahle KM et al. Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. J. Virol. 87(1), 52-66 (2013
105. Setthapramote C, Sasaki T, Puiprom O et al. Human monoclonal antibodies to neutralize all dengue virus serotypes using lymphocytes from patients at acute phase of the secondary infection. Biochem. Biophys. Res. Commun. 423(4), 867-872 (2012
106. Sasaki T, Setthapramote C, Kurosu T et al. Dengue virus neutralization and antibody-dependent enhancement activities of human monoclonal antibodies derived from dengue patients at acute phase of secondary infection. Antiviral Res. 98(3), 423-431 (2013