Next generation dengue vaccines: A review of the preclinical development pipeline

Vaccine

Volumn 33, Issue 50, 2015, Pages 7091-7099

  Vannice, Kirsten S ^a   Roehrig, John T ^b   Hombach, Joachim ^a  

^a WORLD HEALTH ORGANIZATION   (Switzerland)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Dengue vaccine; Vaccine development

Indexed keywords

DENGUE VACCINE; DNA VACCINE; INACTIVATED VIRUS VACCINE; LIVE VACCINE; RECOMBINANT VACCINE; SUBUNIT VACCINE; VIRUS VECTOR;

ARTICLE; DENGUE; DRUG EFFICACY; HIGH RISK POPULATION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIMATE; PRIORITY JOURNAL; TECHNOLOGY; ANIMAL; CLINICAL TRIAL (TOPIC); DRUG DEVELOPMENT; IMMUNOLOGY; ISOLATION AND PURIFICATION; PRECLINICAL STUDY;

ANIMALS; CLINICAL TRIALS AS TOPIC; DENGUE; DENGUE VACCINES; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; HUMANS; PRIMATES;

EID: 84952637751     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.09.053     Document Type: Article

References (123)

1. World Health Organization Global strategy for dengue prevention and control, 2012-2020 2012, Geneva, Switzerland.
2. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., et al. The global distribution and burden of dengue. Nature 2013, 496(7446):504-507.
3. Achee N.L., Gould F., Perkins T.A., Reiner R.C., Morrison A.C., Ritchie S.A., et al. A critical assessment of vector control for dengue prevention. PLoS Negl Trop Dis 2015, 9(5):e0003655.
4. Capeding M.R., Tran N.H., Hadinegoro S.R., Ismail H.I., Chotpitayasunondh T., Chua M.N., et al. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 2014, 384(9951):1358-1365.
5. Villar L., Dayan G.H., Arredondo-Garcia J.L., Rivera D.M., Cunha R., Deseda C., et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 2015, 372(2):113-123.
6. Hadinegoro S.R., Arredondo-Garcia J.L., Capeding M.R., Deseda C., Chotpitayasunondh T., Dietze R., et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med 2015, 373(13):1195-1206.
7. Simmons C.P. A candidate dengue vaccine walks a tightrope. N Engl J Med 2015, 373(13):1263-1264.
8. Pasteur S. New England Journal of Medicine publishes new analyses confirming that Sanofi Pasteur's vaccine candidate safely protects pre-adolescents to adults against dengue 2015, Lyon, France.
9. Schmitz J., Roehrig J., Barrett A., Hombach J. Next generation dengue vaccines: a review of candidates in preclinical development. Vaccine 2011, 29(42):7276-7284.
10. Messina J.P., Brady O.J., Scott T.W., Zou C., Pigott D.M., Duda K.A., et al. Global spread of dengue virus types: mapping the 70 year history. Trends Microbiol 2014, 22(3):138-146.
11. Murphy B.R., Whitehead S.S. Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 2011, 29:587-619.
12. Sabchareon A., Wallace D., Sirivichayakul C., Limkittikul K., Chanthavanich P., Suvannadabba S., et al. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 2012, 380(9853):1559-1567.
13. Sirivichayakul C., Sabchareon A., Limkittikul K., Yoksan S. Plaque reduction neutralization antibody test does not accurately predict protection against dengue infection in Ratchaburi cohort, Thailand. Virol J 2014, 11:48.
14. Mukherjee S., Dowd K.A., Manhart C.J., Ledgerwood J.E., Durbin A.P., Whitehead S.S., et al. Mechanism and significance of cell type-dependent neutralization of flaviviruses. J Virol 2014, 88(13):7210-7220.
15. Hombach J., Cardosa M.J., Sabchareon A., Vaughn D.W., Barrett A.D. Scientific consultation on immunological correlates of protection induced by dengue vaccines report from a meeting held at the World Health Organization 17-18 November 2005. Vaccine 2007, 25(21):4130-4139.
16. Halstead S.B. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 2003, 60:421-467.
17. Halstead S.B. Antibodies determine virulence in dengue. Ann N Y Acad Sci 2009, 1171(Suppl. 1):E48-E56.
18. Guzman M.G., Harris E. Dengue. Lancet 2015, 385(9966):453-465.
19. Pierson T.C., Fremont D.H., Kuhn R.J., Diamond M.S. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 2008, 4(3):229-238.
20. Dowd K.A., Pierson T.C. Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 2011, 411(2):306-315.
21. Junjhon J., Edwards T.J., Utaipat U., Bowman V.D., Holdaway H.A., Zhang W., et al. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J Virol 2010, 84(16):8353-8358.
22. Perera R., Kuhn R.J. Structural proteomics of dengue virus. Curr Opin Microbiol 2008, 11(4):369-377.
23. Beltramello M., Williams K.L., Simmons C.P., Macagno A., Simonelli L., Quyen N.T., 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 2010, 8(3):271-283.
24. Crill W.D., Roehrig J.T. 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 2001, 75(16):7769-7773.
25. Roehrig J.T. Antigenic structure of flavivirus proteins. Adv Virus Res 2003, 59:141-175.
26. Brien J.D., Austin S.K., Sukupolvi-Petty S., O'Brien K.M., Johnson S., Fremont D.H., et al. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 2010, 84(20):10630-10643.
27. Dejnirattisai W., Jumnainsong A., Onsirisakul N., Fitton P., Vasanawathana S., Limpitikul W., et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010, 328(5979):745-748.
28. Rodenhuis-Zybert I.A., van der Schaar H.M., da Silva Voorham J.M., van der Ende-Metselaar H., Lei H.Y., Wilschut J., et al. Immature dengue virus: a veiled pathogen?. PLoS Pathog 2010, 6(1):e1000718.
29. Shrestha B., Brien J.D., Sukupolvi-Petty S., Austin S.K., Edeling M.A., Kim T., et al. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 2010, 6(4):e1000823.
30. Sukupolvi-Petty S., Austin S.K., Engle M., Brien J.D., Dowd K.A., Williams K.L., et al. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 2010, 84(18):9227-9239.
31. Wahala W.M., Donaldson E.F., de Alwis R., Accavitti-Loper M.A., Baric R.S., de Silva A.M. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 2010, 6(3):e1000821.
32. Widman D.G., Baric R.S. Dengue virus envelope protein domain I/II hinge: a key target for dengue virus vaccine design?. Expert Rev Vaccines 2015, 14(1):5-8.
33. de Alwis R., Smith S.A., Olivarez N.P., Messer W.B., Huynh J.P., Wahala W.M., et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci U S A 2012, 109(19):7439-7444.
34. Smith S.A., de Alwis A.R., Kose N., Jadi R.S., de Silva A.M., Crowe J.E. Isolation of dengue virus-specific memory B cells with live virus antigen from human subjects following natural infection reveals the presence of diverse novel functional groups of antibody clones. J Virol 2014, 88(21):12233-12241.
35. Rouvinski A., Guardado-Calvo P., Barba-Spaeth G., Duquerroy S., Vaney M.C., Kikuti C.M., et al. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 2015, 520(7545):109-113.
36. Fibriansah G., Tan J.L., Smith S.A., de Alwis R., Ng T.S., Kostyuchenko V.A., et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat Commun 2015, 6:6341.
37. Dejnirattisai W., Wongwiwat W., Supasa S., Zhang X., Dai X., Rouvinski A., et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 2015, 16(2):170-177.
38. Cassetti M.C., Durbin A., Harris E., Rico-Hesse R., Roehrig J., Rothman A., et al. Report of an NIAID workshop on dengue animal models. Vaccine 2010, 28(26):4229-4234.
39. Williams K.L., Zompi S., Beatty P.R., Harris E. A mouse model for studying dengue virus pathogenesis and immune response. Ann N Y Acad Sci 2009, 1171(Suppl 1):E12-E23.
40. Balsitis S.J., Williams K.L., Lachica R., Flores D., Kyle J.L., Mehlhop E., et al. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 2010, 6(2):e1000790.
41. Zellweger R.M., Prestwood T.R., Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 2010, 7(2):128-139.
42. Kuruvilla J.G., Troyer R.M., Devi S., Akkina R. Dengue virus infection and immune response in humanized RAG2(-/-)gamma(c)(-/-) (RAG-hu) mice. Virology 2007, 369(1):143-152.
43. Mota J., Rico-Hesse R. Humanized mice show clinical signs of dengue fever according to infecting virus genotype. J Virol 2009, 83(17):8638-8645.
44. Bhamarapravati N., Sutee Y. Live attenuated tetravalent dengue vaccine. Vaccine 2000, 18(Suppl. 2):44-47.
45. Edelman R., Wasserman S.S., Bodison S.A., Putnak R.J., Eckels K.H., Tang D., et al. Phase I trial of 16 formulations of a tetravalent live-attenuated dengue vaccine. Am J Trop Med Hyg 2003, 69(Suppl. 6):48-60.
46. Guy B., Barban V., Mantel N., Aguirre M., Gulia S., Pontvianne J., et al. Evaluation of interferences between dengue vaccine serotypes in a monkey model. Am J Trop Med Hyg 2009, 80(2):302-311.
47. Watanaveeradej V., Gibbons R.V., Simasathien S., Nisalak A., Jarman R.G., Kerdpanich A., et al. Safety and immunogenicity of a rederived, live-attenuated dengue virus vaccine in healthy adults living in Thailand: a randomized trial. Am J Trop Med Hyg 2014, 91(1):119-128.
48. Lin L., Thomas S.J. Current dengue vaccine status. Curr Trop Med Rep 2014, 1:6-12.
49. Keelapang P., Nitatpattana N., Suphatrakul A., Punyahathaikul S., Sriburi R., Pulmanausahakul R., et al. Generation and preclinical evaluation of a DENV-1/2 prM+E chimeric live attenuated vaccine candidate with enhanced prM cleavage. Vaccine 2013, 31(44):5134-5140.
50. Zust R., Dong H., Li X.F., Chang D.C., Zhang B., Balakrishnan T., et al. Rational design of a live attenuated dengue vaccine: 2'-o-methyltransferase mutants are highly attenuated and immunogenic in mice and macaques. PLoS Pathog 2013, 9(8):e1003521.
51. Dayan G.H., Garbes P., Noriega F., Izoton de Sadovsky A.D., Rodrigues P.M., Giuberti C., et al. Immunogenicity and safety of a recombinant tetravalent dengue vaccine in children and adolescents ages 9-16 years in Brazil. Am J Trop Med Hyg 2013, 89(6):1058-1065.
52. Khanam S., Pilankatta R., Khanna N., Swaminathan S. An adenovirus type 5 (AdV5) vector encoding an envelope domain III-based tetravalent antigen elicits immune responses against all four dengue viruses in the presence of prior AdV5 immunity. Vaccine 2009, 27(43):6011-6021.
53. Khalil S.M., Tonkin D.R., Mattocks M.D., Snead A.T., Johnston R.E., White L.J. A tetravalent alphavirus-vector based dengue vaccine provides effective immunity in an early life mouse model. Vaccine 2014, 32(32):4068-4074.
54. Brandler S., Ruffie C., Combredet C., Brault J.B., Najburg V., Prevost M.C., et al. A recombinant measles vaccine expressing chikungunya virus-like particles is strongly immunogenic and protects mice from lethal challenge with chikungunya virus. Vaccine 2013, 31(36):3718-3725.
55. Liu M.A. Immunologic basis of vaccine vectors. Immunity 2010, 33(4):504-515.
56. Fernandez S., Thomas S.J., De La Barrera R., Im-Erbsin R., Jarman R.G., Baras B., et al. An adjuvanted, tetravalent dengue virus purified inactivated vaccine candidate induces long-lasting and protective antibody responses against dengue challenge in rhesus macaques. Am J Trop Med Hyg 2015, 92(4):698-708.
57. Coller B.A., Clements D.E., Bett A.J., Sagar S.L., Ter Meulen J.H. The development of recombinant subunit envelope-based vaccines to protect against dengue virus induced disease. Vaccine 2011, 29(42):7267-7275.
58. Ulmer J.B., Mason P.W., Geall A., Mandl C.W. RNA-based vaccines. Vaccine 2012, 30(30):4414-4418.
59. Valdes I., Hermida L., Martin J., Menendez T., Gil L., Lazo L., et al. Immunological evaluation in nonhuman primates of formulations based on the chimeric protein P64k-domain III of dengue 2 and two components of Neisseria meningitidis. Vaccine 2009, 27(7):995-1001.
60. Hermida L., Bernardo L., Martin J., Alvarez M., Prado I., Lopez C., et al. A recombinant fusion protein containing the domain III of the dengue-2 envelope protein is immunogenic and protective in nonhuman primates. Vaccine 2006, 24(16):3165-3171.
61. Bernardo L., Izquierdo A., Alvarez M., Rosario D., Prado I., Lopez C., et al. Immunogenicity and protective efficacy of a recombinant fusion protein containing the domain III of the dengue 1 envelope protein in non-human primates. Antivir Res 2008, 80(2):194-199.
62. Suzarte E., Marcos E., Gil L., Valdes I., Lazo L., Ramos Y., et al. Generation and characterization of potential dengue vaccine candidates based on domain III of the envelope protein and the capsid protein of the four serotypes of dengue virus. Arch Virol 2014, 159(7):1629-1640.
63. Gil L., Marcos E., Izquierdo A., Lazo L., Valdes I., Ambala P., et al. The protein DIIIC-2, aggregated with a specific oligodeoxynucleotide and adjuvanted in alum, protects mice and monkeys against DENV-2. Immunol Cell Biol 2015, 93(1):57-66.
64. Izquierdo A., Garcia A., Lazo L., Gil L., Marcos E., Alvarez M., et al. A tetravalent dengue vaccine containing a mix of domain III-P64k and domain III-capsid proteins induces a protective response in mice. Arch Virol 2014, 159(10):2597-2604.
65. Valdes I., Hermida L., Gil L., Lazo L., Castro J., Martin J., et al. Heterologous prime-boost strategy in non-human primates combining the infective dengue virus and a recombinant protein in a formulation suitable for human use. Int J Infect Dis 2010, 14(5):e377-e383.
66. Valdes I., Gil L., Romero Y., Castro J., Puente P., Lazo L., et al. The chimeric protein domain III-capsid of dengue virus serotype 2 (DEN-2) successfully boosts neutralizing antibodies generated in monkeys upon infection with DEN-2. Clin Vaccine Immunol 2011, 18(3):455-459.
67. McDonald W.F., Huleatt J.W., Foellmer H.G., Hewitt D., Tang J., Desai P., et al. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 2007, 195(11):1607-1617.
68. Liu G., Song L., Beasley D.W., Putnak R., Parent J., Misczak J., et al. Immunogenicity and efficacy of flagellin-envelope fusion dengue vaccines in mice and monkeys. Clin Vaccine Immunol 2015, 22(5):516-525.
69. Treanor J.J., Taylor D.N., Tussey L., Hay C., Nolan C., Fitzgerald T., et al. Safety and immunogenicity of a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125) in healthy young adults. Vaccine 2010, 28(52):8268-8274.
70. Taylor D.N., Treanor J.J., Strout C., Johnson C., Fitzgerald T., Kavita U., et al. Induction of a potent immune response in the elderly using the TLR-5 agonist, flagellin, with a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125, STF2.HA1 SI). Vaccine 2011, 29(31):4897-4902.
71. Leng C.H., Liu S.J., Tsai J.P., Li Y.S., Chen M.Y., Liu H.H., et al. A novel dengue vaccine candidate that induces cross-neutralizing antibodies and memory immunity. Microbes Infect 2009, 11(2):288-295.
72. Chen H.W., Liu S.J., Li Y.S., Liu H.H., Tsai J.P., Chiang C.Y., et al. A consensus envelope protein domain III can induce neutralizing antibody responses against serotype 2 of dengue virus in non-human primates. Arch Virol 2013, 158(7):1523-1531.
73. Chiang C.Y., Huang M.H., Pan C.H., Hsieh C.H., Chen M.Y., Liu H.H., et al. Induction of robust immunity by the emulsification of recombinant lipidated dengue-1 envelope protein domain III. Microbes Infect 2013, 15(10-11):719-728.
74. Chiang C.Y., Liu S.J., Tsai J.P., Li Y.S., Chen M.Y., Liu H.H., et al. A novel single-dose dengue subunit vaccine induces memory immune responses. PLoS ONE 2011, 6(8):e23319.
75. Chiang C.Y., Hsieh C.H., Chen M.Y., Tsai J.P., Liu H.H., Liu S.J., et al. Recombinant lipidated dengue-4 envelope protein domain III elicits protective immunity. Vaccine 2014, 32(12):1346-1353.
76. Chang G.J., Hunt A.R., Holmes D.A., Springfield T., Chiueh T.S., Roehrig J.T., et al. Enhancing biosynthesis and secretion of premembrane and envelope proteins by the chimeric plasmid of dengue virus type 2 and Japanese encephalitis virus. Virology 2003, 306(1):170-180.
77. Purdy D.E., Chang G.J. Secretion of noninfectious dengue virus-like particles and identification of amino acids in the stem region involved in intracellular retention of envelope protein. Virology 2005, 333(2):239-250.
78. Beckett C.G., Tjaden J., Burgess T., Danko J.R., Tamminga C., Simmons M., et al. Evaluation of a prototype dengue-1 DNA vaccine in a Phase 1 clinical trial. Vaccine 2011, 29(5):960-968.
79. Raviprakash K., Porter K.R., Kochel T.J., Ewing D., Simmons M., Phillips I., et al. Dengue virus type 1 DNA vaccine induces protective immune responses in rhesus macaques. J Gen Virol 2000, 81(Pt 7):1659-1667.
80. Raviprakash K., Marques E., Ewing D., Lu Y., Phillips I., Porter K.R., et al. Synergistic neutralizing antibody response to a dengue virus type 2 DNA vaccine by incorporation of lysosome-associated membrane protein sequences and use of plasmid expressing GM-CSF. Virology 2001, 290(1):74-82.
81. Blair P.J., Kochel T.J., Raviprakash K., Guevara C., Salazar M., Wu S.J., et al. Evaluation of immunity and protective efficacy of a dengue-3 pre-membrane and envelope DNA vaccine in Aotus nancymae monkeys. Vaccine 2006, 24(9):1427-1432.
82. Lu Y., Raviprakash K., Leao I.C., Chikhlikar P.R., Ewing D., Anwar A., et al. Dengue 2 PreM-E/LAMP chimera targeted to the MHC class II compartment elicits long-lasting neutralizing antibodies. Vaccine 2003, 21(17-18):2178-2189.
83. Sullivan S.M., Doukas J., Hartikka J., Smith L., Rolland A. Vaxfectin: a versatile adjuvant for plasmid DNA- and protein-based vaccines. Expert Opin Drug Deliv 2010, 7(12):1433-1446.
84. Porter K.R., Ewing D., Chen L., Wu S.J., Hayes C.G., Ferrari M., et al. Immunogenicity and protective efficacy of a vaxfectin-adjuvanted tetravalent dengue DNA vaccine. Vaccine 2012, 30(2):336-341.
85. Ramanathan M.P., Kuo Y.C., Selling B.H., Li Q., Sardesai N.Y., Kim J.J., et al. Development of a novel DNA SynCon tetravalent dengue vaccine that elicits immune responses against four serotypes. Vaccine 2009, 27(46):6444-6453.
86. Konishi E., Kosugi S., Imoto J. Dengue tetravalent DNA vaccine inducing neutralizing antibody and anamnestic responses to four serotypes in mice. Vaccine 2006, 24(12):2200-2207.
87. Azevedo A.S., Yamamura A.M., Freire M.S., Trindade G.F., Bonaldo M., Galler R., et al. DNA vaccines against dengue virus type 2 based on truncate envelope protein or its domain III. PLoS ONE 2011, 6(7):e20528.
88. Costa S.M., Azevedo A.S., Paes M.V., Sarges F.S., Freire M.S., Alves A.M. DNA vaccines against dengue virus based on the ns1 gene: the influence of different signal sequences on the protein expression and its correlation to the immune response elicited in mice. Virology 2007, 358(2):413-423.
89. Costa S.M., Yorio A.P., Goncalves A.J., Vidale M.M., Costa E.C., Mohana-Borges R., et al. Induction of a protective response in mice by the dengue virus NS3 protein using DNA vaccines. PLoS ONE 2011, 6(10):e25685.
90. Bisht H., Chugh D.A., Raje M., Swaminathan S.S., Khanna N. Recombinant dengue virus type 2 envelope/hepatitis B surface antigen hybrid protein expressed in Pichia pastoris can function as a bivalent immunogen. J Biotechnol 2002, 99(2):97-110.
91. Gurramkonda C., Adnan A., Gabel T., Lunsdorf H., Ross A., Nemani S.K., et al. Simple high-cell density fed-batch technique for high-level recombinant protein production with Pichia pastoris: application to intracellular production of Hepatitis B surface antigen. Microb Cell Fact 2009, 8:13.
92. Khetarpal N., Poddar A., Nemani S.K., Dhar N., Patil A., Negi P., et al. Dengue-specific subviral nanoparticles: design, creation and characterization. J Nanobiotechnol. 2013, 11:15.
93. Mani S., Tripathi L., Raut R., Tyagi P., Arora U., Barman T., et al. Pichia pastoris-expressed dengue 2 envelope forms virus-like particles without pre-membrane protein and induces high titer neutralizing antibodies. PLoS ONE 2013, 8(5):e64595.
94. Spohn G., Jennings G.T., Martina B.E., Keller I., Beck M., Pumpens P., et al. A VLP-based vaccine targeting domain III of the West Nile virus E protein protects from lethal infection in mice. Virol J 2010, 7:146.
95. Kuwahara M., Konishi E. Evaluation of extracellular subviral particles of dengue virus type 2 and Japanese encephalitis virus produced by Spodoptera frugiperda cells for use as vaccine and diagnostic antigens. Clin Vaccine Immunol 2010, 17(10):1560-1566.
96. White L.J., Parsons M.M., Whitmore A.C., Williams B.M., de Silva A., Johnston R.E. An immunogenic and protective alphavirus replicon particle-based dengue vaccine overcomes maternal antibody interference in weanling mice. J Virol 2007, 81(19):10329-10339.
97. White L.J., Sariol C.A., Mattocks M.D., Wahala M.P.B.W., Yingsiwaphat V., Collier M.L., et al. An alphavirus vector-based tetravalent dengue vaccine induces a rapid and protective immune response in macaques that differs qualitatively from immunity induced by live virus infection. J Virol 2013, 87(6):3409-3424.
98. Brandler S., Ruffie C., Najburg V., Frenkiel M.P., Bedouelle H., Despres P., et al. Pediatric measles vaccine expressing a dengue tetravalent antigen elicits neutralizing antibodies against all four dengue viruses. Vaccine 2010, 28(41):6730-6739.
99. Brandler S., Lucas-Hourani M., Moris A., Frenkiel M.P., Combredet C., Fevrier M., et al. Pediatric measles vaccine expressing a dengue antigen induces durable serotype-specific neutralizing antibodies to dengue virus. PLoS Negl Trop Dis 2007, 1(3):e96.
100. Ramsauer K., Schwameis M., Firbas C., Mullner M., Putnak R.J., Thomas S.J., et al. Immunogenicity, safety, and tolerability of a recombinant measles-virus-based chikungunya vaccine: a randomised, double-blind, placebo-controlled, active-comparator, first-in-man trial. Lancet Infect Dis 2015, 15(5):519-527.
101. Raviprakash K., Wang D., Ewing D., Holman D.H., Block K., Woraratanadharm J., et al. A tetravalent dengue vaccine based on a complex adenovirus vector provides significant protection in rhesus monkeys against all four serotypes of dengue virus. J Virol 2008, 82(14):6927-6934.
102. Widman D.G., Frolov I., Mason P.W. Third-generation flavivirus vaccines based on single-cycle, encapsidation-defective viruses. Adv Virus Res 2008, 72:77-126.
103. Suzuki R., Winkelmann E.R., Mason P.W. Construction and characterization of a single-cycle chimeric flavivirus vaccine candidate that protects mice against lethal challenge with dengue virus type 2. J Virol 2009, 83(4):1870-1880.
104. Maves R.C., Ore R.M., Porter K.R., Kochel T.J. Immunogenicity and protective efficacy of a psoralen-inactivated dengue-1 virus vaccine candidate in Aotus nancymaae monkeys. Vaccine 2011, 29(15):2691-2696.
105. Raviprakash K., Sun P., Raviv Y., Luke T., Martin N., Kochel T. Dengue virus photo-inactivated in presence of 1,5-iodonaphthylazide (INA) or AMT, a psoralen compound (4'-aminomethyl-trioxsalen) is highly immunogenic in mice. Hum Vaccines Immunother 2013, 9(11):2336-2341.
106. Robert Putnak J., Coller B.A., Voss G., Vaughn D.W., Clements D., Peters I., et al. An evaluation of dengue type-2 inactivated, recombinant subunit, and live-attenuated vaccine candidates in the rhesus macaque model. Vaccine 2005, 23(35):4442-4452.
107. Briggs C.M., Smith K.M., Piper A., Huitt E., Spears C.J., Quiles M., et al. Live attenuated tetravalent dengue virus host range vaccine is immunogenic in African green monkeys following a single vaccination. J Virol 2014, 88(12):6729-6742.
108. Li Z., Yang H., Yang J., Lin H., Wang W., Liu L., et al. Construction and preliminary investigation of a novel dengue serotype 4 chimeric virus using Japanese encephalitis vaccine strain SA14-14-2 as the backbone. Virus Res 2014, 191:10-20.
109. Li X.F., Deng Y.Q., Yang H.Q., Zhao H., Jiang T., Yu X.D., et al. A chimeric dengue virus vaccine using Japanese encephalitis virus vaccine strain SA14-14-2 as backbone is immunogenic and protective against either parental virus in mice and nonhuman primates. J Virol 2013, 87(24):13694-13705.
110. Chen L., Ewing D., Subramanian H., Block K., Rayner J., Alterson K.D., et al. A heterologous DNA prime-Venezuelan equine encephalitis virus replicon particle boost dengue vaccine regimen affords complete protection from virus challenge in cynomolgus macaques. J Virol 2007, 81(21):11634-11639.
111. Simmons M., Burgess T., Lynch J., Putnak R. Protection against dengue virus by non-replicating and live attenuated vaccines used together in a prime boost vaccination strategy. Virology 2010, 396(2):280-288.
112. Sun W., Cunningham D., Wasserman S.S., Perry J., Putnak J.R., Eckels K.H., et al. Phase 2 clinical trial of three formulations of tetravalent live-attenuated dengue vaccine in flavivirus-naive adults. Hum Vaccin 2009, 5(1):33-40.
113. Caufour P.S., Motta M.C., Yamamura A.M., Vazquez S., Ferreira, Jabor A.V., et al. Construction, characterization and immunogenicity of recombinant yellow fever 17D-dengue type 2 viruses. Virus Res 2001, 79(1-2):1-14.
114. Galler R., Marchevsky R.S., Caride E., Almeida L.F., Yamamura A.M., Jabor A.V., et al. Attenuation and immunogenicity of recombinant yellow fever 17D-dengue type 2 virus for rhesus monkeys. Braz J Med Biol Res 2005, 38(12):1835-1846.
115. Mateu G.P., Marchevsky R.S., Liprandi F., Bonaldo M.C., Coutinho E.S., Dieudonne M., et al. Construction and biological properties of yellow fever 17D/dengue type 1 recombinant virus. Trans R Soc Trop Med Hyg 2007, 101(3):289-298.
116. Trindade G.F., Marchevsky R.S., Fillipis A.M., Nogueira R.M., Bonaldo M.C., Acero P.C., et al. Limited replication of yellow fever 17DD and 17D-Dengue recombinant viruses in rhesus monkeys. An Acad Bras Cienc 2008, 80(2):311-321.
117. Azevedo A.S., Goncalves A.J., Archer M., Freire M.S., Galler R., Alves A.M. The synergistic effect of combined immunization with a DNA vaccine and chimeric yellow fever/dengue virus leads to strong protection against dengue. PLoS ONE 2013, 8(3):e58357.
118. Zlatkovic J., Stiasny K., Heinz F.X. Immunodominance and functional activities of antibody responses to inactivated West Nile virus and recombinant subunit vaccines in mice. J Virol 2011, 85(5):1994-2003.
119. World Health Organization NIAID/WHO workshop on heterologous prime-boost strategies for HIV, malaria and tuberculosis vaccines 2012, http://www.who.int/immunization/research/meetings_workshops/niaid_workshop_hiv_malaria_tb_2012/en/.
120. World Health Organization Heterologous prime-boost immunization in Ebola vaccine development, testing and licensure 2014, http://www.who.int/immunization/research/meetings_workshops/ebola_primeboost_21nov14/en/.
121. Cassetti M.C., Thomas S.J. Dengue human infection model: introduction. J Infect Dis 2014, 209(Suppl. 2):S37-S39.
122. Halstead S.B. Identifying protective dengue vaccines: guide to mastering an empirical process. Vaccine 2013, 31(41):4501-4507.
123. Sariol C.A., White L.J. Utility, limitations, and future of non-human primates for dengue research and vaccine development. Front Immunol 2014, 5:452.