Vaccine-induced protection of rhesus macaques against plasma viremia after intradermal infection with a European lineage 1 strain of west nile virus

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Verstrepen, Babs E ^a   Oostermeijer, Herman ^a   Fagrouch, Zahra ^a   Van Heteren, Melanie ^a   Niphuis, Henk ^a   Haaksma, Tom ^b   Kondova, Ivanela ^b   Bogers, Willy M ^a   De Filette, Marina ^c   Sanders, Niek ^c   Stertman, Linda ^d   Magnusson, Sofia ^d   Lörincz, Orsolya ^e   Lisziewicz, Julianna ^e   Barzon, Luisa ^f   Palù, Giorgio ^f   Diamond, Michael S ^g   Chabierski, Stefan ^h   Ulbert, Sebastian ^h   Verschoor, Ernst J ^a  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b Animal Science Department Division of Pathology and Microbiology BPRC Rijswijk   (Netherlands)

^c GHENT UNIVERSITY   (Belgium)

^d NOVAVAX INC   (United States)

^e EMMUNITY Inc   (Hungary)

^f UNIVERSITY OF PADOVA   (Italy)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; NANOPARTICLE; WEST NILE VACCINE; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DNA IMMUNIZATION; HIGH RISK POPULATION; INFECTION PREVENTION; INFECTION RISK; NONHUMAN; RHESUS MONKEY; TISSUE DISTRIBUTION; VACCINATION; VIREMIA; VIRUS ENVELOPE; VIRUS GENOME; VIRUS STRAIN; WEST NILE FLAVIVIRUS; ANIMAL; BLOOD; CLASSIFICATION; EUROPE; HUMORAL IMMUNITY; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; MOSQUITO; PROTEIN TERTIARY STRUCTURE; VIRUS LOAD; WEST NILE FEVER; WEST NILE VIRUS;

MACACA MULATTA; WEST NILE VIRUS;

ANIMALS; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CULICIDAE; EUROPE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; INJECTIONS, INTRADERMAL; INTERFERON-GAMMA; MACACA MULATTA; PROTEIN STRUCTURE, TERTIARY; VIRAL ENVELOPE PROTEINS; VIRAL LOAD; VIREMIA; WEST NILE FEVER; WEST NILE VIRUS; WEST NILE VIRUS VACCINES;

EID: 84911871549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112568     Document Type: Article

References (60)

1. Petersen LR, Brault AC, Nasci RS (2013) West Nile virus: Review of the literature. JAMA 310: 308-315.
2. Murray K, Walker C, Herrington E, Lewis JA, McCormick J, et al. (2010) Persistent infection with West Nile virus years after initial infection. J Infect Dis 201: 2-4.
3. Danis K, Papa A, Theocharopoulos G, Dougas G, Athanasiou M, et al. (2011) Outbreak of West Nile virus infection in Greece, 2010. Emerg Infect Dis 17: 1868-1872.
4. Barzon L, Pacenti M, Franchin E, Lavezzo E, Martello T, et al. (2012) New endemic West Nile virus lineage 1a in northern Italy, July 2012. Euro Surveill 17.
5. Barzon L, Pacenti M, Franchin E, Lavezzo E, Masi G, et al. (2013) Whole genome sequencing and phylogenetic analysis of West Nile virus lineage 1 and lineage 2 from human cases of infection, Italy, August 2013. Euro Surveill 18.
6. Popovic N, Milosevic B, Urosevic A, Poluga J, Lavadinovic L, et al. (2013) Outbreak of West Nile virus infection among humans in Serbia, August to October 2012. Euro Surveill 18.
7. Pervanidou D, Detsis M, Danis K, Mellou K, Papanikolaou E, et al. (2014) West Nile virus outbreak in humans, Greece, 2012: Third consecutive year of local transmission. Euro Surveill 19.
8. Chung WM, Buseman CM, Joyner SN, Hughes SM, Fomby TB, et al. (2013) The 2012 West Nile encephalitis epidemic in Dallas, Texas. JAMA 310: 297-307.
9. Vazquez A, Sanchez-Seco MP, Ruiz S, Molero F, Hernandez L, et al. (2010) Putative new lineage of west nile virus, Spain. Emerg Infect Dis 16: 549-552.
10. Pesko KN, Ebel GD (2012) West Nile virus population genetics and evolution. Infect Genet Evol 12: 181-190.
11. Lanciotti RS, Ebel GD, Deubel V, Kerst AJ, Murri S, et al. (2002) Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 298: 96-105.
12. Bakonyi T, Ferenczi E, Erdelyi K, Kutasi O, Csorgo T, et al. (2013) Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/ 2009. Vet Microbiol 165: 61-70.
13. Murray KO, Mertens E, Despres P (2010) West Nile virus and its emergence in the United States of America. Vet Res 41: 67.
14. ECDC (2012) Epidemiological situation of West Nile virus infection in the European Union.
15. Papa A (2012) West Nile virus infections in Greece: An update. Expert Rev Anti Infect Ther 10: 743-750.
16. De Filette M, Ulbert S, Diamond M, Sanders NN (2012) Recent progress in West Nile virus diagnosis and vaccination. Vet Res 43: 16.
17. Brandler S, Tangy F (2013) Vaccines in development against West Nile virus. Viruses 5: 2384-2409.
18. Wang T, Anderson JF, Magnarelli LA, Wong SJ, Koski RA, et al. (2001) Immunization of mice against West Nile virus with recombinant envelope protein. J Immunol 167: 5273-5277.
19. Pinto AK, Richner JM, Poore EA, Patil, Amanna IJ, et al. (2013) A Hydrogen Peroxide-Inactivated Virus Vaccine Elicits Humoral and Cellular Immunity and Protects against Lethal West Nile Virus Infection in Aged Mice. J Virol 87: 1926-1936.
20. Widman DG, Ishikawa T, Winkelmann ER, Infante E, Bourne N, et al. (2009) RepliVAX WN, a single-cycle flavivirus vaccine to prevent West Nile disease, elicits durable protective immunity in hamsters. Vaccine 27: 5550-5553.
21. Spohn G, Jennings GT, Martina BE, Keller I, Beck M, et al. (2010) A VLPbased vaccine targeting domain III of the West Nile virus E protein protects from lethal infection in mice. Virol J 7: 146.
22. Arroyo J, Miller C, Catalan J, Myers GA, Ratterree MS, et al. (2004) ChimeriVax-West Nile virus live-attenuated vaccine: Preclinical evaluation of safety, immunogenicity, and efficacy. J Virol 78: 12497-12507.
23. Monath TP, Liu J, Kanesa-Thasan N, Myers GA, Nichols R, et al. (2006) A live, attenuated recombinant West Nile virus vaccine. Proc Natl Acad Sci U S A 103: 6694-6699.
24. Lieberman MM, Nerurkar VR, Luo H, Cropp B, Carrion R Jr, et al. (2009) Immunogenicity and protective efficacy of a recombinant subunit West Nile virus vaccine in rhesus monkeys. Clin Vaccine Immunol 16: 1332-1337.
25. Pletnev AG, Swayne DE, Speicher J, Rumyantsev AA, Murphy BR (2006) Chimeric West Nile/dengue virus vaccine candidate: Preclinical evaluation in mice, geese and monkeys for safety and immunogenicity. Vaccine 24: 6392-6404.
26. Widman DG, Ishikawa T, Giavedoni LD, Hodara VL, Garza Mde L, et al. (2010) Evaluation of RepliVAX WN, a single-cycle flavivirus vaccine, in a nonhuman primate model of West Nile virus infection. Am J Trop Med Hyg 82: 1160-1167.
27. Whiteman MC, Li L, Wicker JA, Kinney RM, Huang C, et al. (2010) Development and characterization of non-glycosylated E and NS1 mutant viruses as a potential candidate vaccine for West Nile virus. Vaccine 28: 1075-1083.
28. Verstrepen BE, Fagrouch Z, van Heteren M, Buitendijk H, Haaksma T, et al. (2014) Experimental infection of rhesus macaques and common marmosets with a European strain of West Nile virus. PLoS Negl Trop Dis 8: E2797.
29. Busch MP, Kleinman SH, Tobler LH, Kamel HT, Norris PJ, et al. (2008) Virus and antibody dynamics in acute west nile virus infection. J Infect Dis 198: 984-993.
30. Diamond MS, Shrestha B, Mehlhop E, Sitati E, Engle M (2003) Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus. Viral Immunol 16: 259-278.
31. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M (2003) B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol 77: 2578-2586.
32. Shrestha B, Diamond MS (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78: 8312-8321.
33. Brien JD, Uhrlaub JL, Nikolich-Zugich J (2007) Protective capacity and epitope specificity of CD8(+) T cells responding to lethal West Nile virus infection. Eur J Immunol 37: 1855-1863.
34. Purtha WE, Myers N, Mitaksov V, Sitati E, Connolly J, et al. (2007) Antigenspecific cytotoxic T lymphocytes protect against lethal West Nile virus encephalitis. Eur J Immunol 37: 1845-1854.
35. Throsby M, Ter Meulen J, Geuijen C, Goudsmit J, de Kruif J (2007) Mapping and analysis of West Nile virus-specific monoclonal antibodies: Prospects for vaccine development. Expert Rev Vaccines 6: 183-191.
36. Oliphant T, Nybakken GE, Austin SK, Xu Q, Bramson J, et al. (2007) Induction of epitope-specific neutralizing antibodies against West Nile virus. J Virol 81: 11828-11839.
37. Schneeweiss A, Chabierski S, Salomo M, Delaroque N, Al-Robaiy S, et al. (2011) A DNA vaccine encoding the E protein of West Nile virus is protective and can be boosted by recombinant domain DIII. Vaccine 29: 6352-6357.
38. Bengtsson KL, Karlsson KH, Magnusson SE, Reimer JM, Stertman L (2013) Matrix-M adjuvant: Enhancing immune responses by 'setting the stage' for the antigen. Expert Rev Vaccines 12: 821-823.
39. Magnusson SE, Reimer JM, Karlsson KH, Lilja L, Bengtsson KL, et al. (2013) Immune enhancing properties of the novel Matrix-M adjuvant leads to potentiated immune responses to an influenza vaccine in mice. Vaccine 31: 1725-1733.
40. Koup RA, Graham BS, Douek DC (2011) The quest for a T cell-based immune correlate of protection against HIV: A story of trials and errors. Nat Rev Immunol 11: 65-70.
41. Lorincz O, Toke ER, Somogyi E, Horkay F, Chandran PL, et al. (2012) Structure and biological activity of pathogen-like synthetic nanomedicines. Nanomedicine 8: 497-506.
42. De Filette M, Soehle S, Ulbert S, Richner J, Diamond MS, et al. (2014) Vaccination of mice using the West Nile virus E-protein in a DNA prime-protein boost strategy stimulates cell-mediated immunity and protects mice against a lethal challenge. PLoS One 9: E87837.
43. Diebold SS, Kursa M, Wagner E, Cotten M, Zenke M (1999) Mannose polyethylenimine conjugates for targeted DNA delivery into dendritic cells. J Biol Chem 274: 19087-19094.
44. Magnusson SE, Karlsson KH, Reimer JM, Corbach-Sohle S, Patel S, et al. (2014) Matrix-M adjuvanted envelope protein vaccine protects against lethal lineage 1 and 2 West Nile virus infection in mice. Vaccine 32: 800-808.
45. Toke ER, Lorincz O, Somogyi E, Lisziewicz J (2010) Rational development of a stable liquid formulation for nanomedicine products. Int J Pharm 392: 261-267.
46. Barzon L, Franchin E, Squarzon L, Lavezzo E, Toppo S, et al. (2009) Genome sequence analysis of the first human West Nile virus isolated in Italy in 2009. Euro Surveill 14.
47. Amanna IJ, Raue HP, Slifka MK (2012) Development of a new hydrogen peroxide-based vaccine platform. Nat Med 18: 974-979.
48. Karber G (1931) 50% end-point calculation Arch Exp Pathol Pharmakol 162: 480-483.
49. Donaldson MM, Kao SF, Eslamizar L, Gee C, Koopman G, et al. (2012) Optimization and qualification of an 8-color intracellular cytokine staining assay for quantifying T cell responses in rhesus macaques for pre-clinical vaccine studies. J Immunol Methods 386: 10-21.
50. Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, et al. (2000) Rapid detection of west nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol 38: 4066-4071.
51. Nolan MS, Podoll AS, Hause AM, Akers KM, Finkel KW, et al. (2012) Prevalence of chronic kidney disease and progression of disease over time among patients enrolled in the Houston West Nile virus cohort. PLoS One 7: E40374.
52. Hughes HR, Crill WD, Davis BS, Chang GJ (2012) A West Nile virus CD4 T cell epitope improves the immunogenicity of dengue virus serotype 2 vaccines. Virology 424: 129-137.
53. Netland J, Bevan MJ (2013) CD8 and CD4 T cells in west nile virus immunity and pathogenesis. Viruses 5: 2573-2584.
54. Larsen MV, Lelic A, Parsons R, Nielsen M, Hoof I, et al. (2010) Identification of CD8+ T cell epitopes in the West Nile virus polyprotein by reverse-immunology using NetCTL. PLoS One 5: E12697.
55. Mooij P, Nieuwenhuis IG, Knoop CJ, Doms RW, Bogers WM, et al. (2004) Qualitative T-helper responses to multiple viral antigens correlate with vaccineinduced immunity to simian/human immunodeficiency virus infection. J Virol 78: 3333-3342.
56. Rollier C, Verschoor EJ, Paranhos-Baccala G, Drexhage JA, Verstrepen BE, et al. (2005) Modulation of vaccine-induced immune responses to hepatitis C virus in rhesus macaques by altering priming before adenovirus boosting. J Infect Dis 192: 920-929.
57. Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S, et al. (2005) Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11: 522-530.
58. Styer LM, Kent KA, Albright RG, Bennett CJ, Kramer LD, et al. (2007) Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog 3: 1262-1270.
59. Ishikawa T, Yamanaka A, Konishi E (2014) A review of successful flavivirus vaccines and the problems with those flaviviruses for which vaccines are not yet available. Vaccine 32: 1326-1337.
60. Sambri V, Capobianchi M, Charrel R, Fyodorova M, Gaibani P, et al. (2013) West Nile virus in Europe: Emergence, epidemiology, diagnosis, treatment, and prevention. Clin Microbiol Infect 19: 699-704.