Molecular and immunological characterization of a DNA-launched yellow fever virus 17D infectious clone

Journal of General Virology

Volumn 96, Issue 4, 2015, Pages 804-814

  Jiang, Xiaohong ^a   Dalebout, Tim J ^a   Lukashevich, Igor S ^b   Bredenbeek, Peter J ^a   Franco, David ^c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b University of Louisville School of Medicine   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; LIVE VACCINE; NEUTRALIZING ANTIBODY; YELLOW FEVER VACCINE; DNA; VIRUS ANTIBODY; VIRUS VACCINE;

ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA IMMUNIZATION; DNA TRANSFECTION; DRUG ANALYSIS; ELECTROPORATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS NEUTRALIZATION; YELLOW FEVER; YELLOW FEVER FLAVIVIRUS; ANIMAL; C57BL MOUSE; CELL LINE; GENE VECTOR; GENETICS; HAMSTER; IMMUNOLOGY; TRANSGENIC MOUSE; VIROLOGY; VIRUS REPLICATION; YELLOW FEVER VIRUS;

MIRIDAE; MUS; YELLOW FEVER VIRUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELL LINE; CRICETINAE; DNA; FEMALE; GENETIC VECTORS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; VACCINES, ATTENUATED; VACCINES, DNA; VIRAL VACCINES; VIRUS REPLICATION; YELLOW FEVER; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS;

EID: 84925003791     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000026     Document Type: Article

References (65)

1. Appaiahgari, M. B. & Vrati, S. (2010). IMOJEV(1): a yellow fever virus-based novel Japanese encephalitis vaccine. Expert Rev Vaccines 9, 1371–1384.
2. Arroyo, J., Miller, C., Catalan, J., Myers, G. A., Ratterree, M. S., Trent, D. W. & Monath, T. P. (2004). ChimeriVax-West Nile virus liveattenuated vaccine: preclinical evaluation of safety, immunogenicity, and efficacy. J Virol 78, 12497–12507.
3. Barrett, A. D. & Gould, E. A. (1986). Comparison of neurovirulence of different strains of yellow fever virus in mice. J Gen Virol 67, 631–637.
4. Barrett, A. D. & Teuwen, D. E. (2009). Yellow fever vaccine - how does it work and why do rare cases of serious adverse events take place? Curr Opin Immunol 21, 308–313.
5. Barrett, A. D., Monath, T. P., Barban, V., Niedrig, M. & Teuwen, D. E. (2007). 17D Yellow fever vaccines: new insights: a report of a workshop held during theWorld Congress on Medicine and Health in the Tropics, Marseille, France, Monday 12 September 2005 Vaccine 25, 2758–2765.
6. Bonaldo, M. C., Garratt, R. C., Caufour, P. S., Freire, M. S., Rodrigues, M. M., Nussenzweig, R. S. & Galler, R. (2002). Surface expression of an immunodominant malaria protein B cell epitope by yellow fever virus. J Mol Biol 315, 873–885.
7. Bonaldo, M. C., Mello, S. M., Trindade, G. F., Rangel, A. A., Duarte, A. S., Oliveira, P. J., Freire, M. S., Kubelka, C. F. & Galler, R. (2007). Construction and characterization of recombinant flaviviruses bearing insertions between E and NS1 genes. Virol J 4, 115.
8. Bråve, A., Gudmundsdotter, L., Sandström, E., Haller, B. K., Hallengärd, D., Maltais, A. K., King, A. D., Stout, R. R., Blomberg, P. & other authors (2010). Biodistribution, persistence and lack of integration of a multigene HIV vaccine delivered by needle-free intradermal injection and electroporation. Vaccine 28, 8203–8209.
9. Bråve, A., Nyström, S., Roos, A. K. & Applequist, S. E. (2011). Plasmid DNA vaccination using skin electroporation promotes polyfunctional CD4 T-cell responses. Immunol Cell Biol 89, 492–496.
10. Bredenbeek, P. J., Kooi, E. A., Lindenbach, B., Huijkman, N., Rice, C. M. & Spaan, W. J. (2003). A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication. J Gen Virol 84, 1261–1268.
11. Bredenbeek, P. J., Molenkamp, R., Spaan, W. J., Deubel, V., Marianneau, P., Salvato, M. S., Moshkoff, D., Zapata, J., Tikhonov, I. & other authors (2006). A recombinant yellow fever 17D vaccine expressing Lassa virus glycoproteins. Virology 345, 299–304.
12. Chambers, T. J., Nestorowicz, A., Mason, P. W. & Rice, C. M. (1999). Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol 73, 3095–3101.
13. Charlier, N., Molenkamp, R., Leyssen, P., Vandamme, A.-M., De Clercq, E., Bredenbeek, P. & Neyts, J. (2003). A rapid and convenient variant of fusion-PCR to construct chimeric flaviviruses. J Virol Methods 108, 67–74.
14. Franco, D., Li, W., Qing, F., Stoyanov, C. T., Moran, T., Rice, C. M. & Ho, D. D. (2010). Evaluation of yellow fever virus 17D strain as a new vector for HIV-1 vaccine development. Vaccine 28, 5676–5685.
15. Galler, R., Marchevsky, R. S., Caride, E., Almeida, L. F., Yamamura, A. M., Jabor, A. V., Motta, M. C., Bonaldo, M. C., Coutinho, E. S. & Freire, M. S. (2005). Attenuation and immunogenicity of recombinant yellow fever 17D-dengue type 2 virus for rhesus monkeys. Braz J Med Biol Res 38, 1835–1846.
16. Gardiner, D. F., Rosenberg, T., Zaharatos, J., Franco, D. & Ho, D. D. (2009). A DNA vaccine targeting the receptor-binding domain of Clostridium difficile toxin A. Vaccine 27, 3598–3604.
17. Gaucher, D., Therrien, R., Kettaf, N., Angermann, B. R., Boucher, G., Filali-Mouhim, A., Moser, J. M., Mehta, R. S., Drake, D. R., III & other authors (2008). Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J Exp Med 205, 3119–3131.
18. Guirakhoo, F., Zhang, Z. X., Chambers, T. J., Delagrave, S., Arroyo, J., Barrett, A. D. & Monath, T. P. (1999). Immunogenicity, genetic stability, and protective efficacy of a recombinant, chimeric yellow fever-Japanese encephalitis virus (ChimeriVax-JE) as a live, attenuated vaccine candidate against Japanese encephalitis. Virology 257, 363–372.
19. Guirakhoo, F., Arroyo, J., Pugachev, K. V., Miller, C., Zhang, Z. X., Weltzin, R., Georgakopoulos, K., Catalan, J., Ocran, S. & other authors (2001). Construction, safety, and immunogenicity in nonhuman primates of a chimeric yellow fever-dengue virus tetravalent vaccine. J Virol 75, 7290–7304.
20. Guy, B., Saville, M. & Lang, J. (2010). Development of Sanofi Pasteur tetravalent dengue vaccine. Hum Vaccin 6, 695–705.
21. Hall, R. A., Nisbet, D. J., Pham, K. B., Pyke, A. T., Smith, G. A. & Khromykh, A. A. (2003). DNA vaccine coding for the full-length infectious Kunjin virus RNA protects mice against the New York strain of West Nile virus. Proc Natl Acad Sci U S A 100, 10460–10464.
22. Halstead, S. B. & Thomas, S. J. (2011). New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10, 355–364.
23. Hsieh, C. S., Macatonia, S. E., O’Garra, A. & Murphy, K. M. (1995). T cell genetic background determines default T helper phenotype development in vitro. J Exp Med 181, 713–721.
24. Inoue, H., Nojima, H. & Okayama, H. (1990). High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23–28.
25. Jiang, X., Dalebout, T. J., Bredenbeek, P. J., Carrion, R., Jr, Brasky, K., Patterson, J., Goicochea, M., Bryant, J., Salvato, M. S. & Lukashevich, I. S. (2011). Yellow fever 17D-vectored vaccines expressing Lassa virus GP1 and GP2 glycoproteins provide protection against fatal disease in guinea pigs. Vaccine 29, 1248–1257.
26. Khan, A. S., Pope, M. A. & Draghia-Akli, R. (2005). Highly efficient constant-current electroporation increases in vivo plasmid expression. DNA Cell Biol 24, 810–818.
27. Khromykh, A. A. & Westaway, E. G. (1997). Subgenomic replicons of the flavivirus Kunjin: construction and applications. J Virol 71, 1497–1505.
28. Khromykh, A. A., Varnavski, A. N., Sedlak, P. L. & Westaway, E. G. (2001). Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cDNA clones of Kunjin virus. J Virol 75, 4633–4640.
29. Kopycinski, J., Cheeseman, H., Ashraf, A., Gill, D., Hayes, P., Hannaman, D., Gilmour, J., Cox, J. H. & Vasan, S. (2012). A DNAbased candidate HIV vaccine delivered via in vivo electroporation induces CD4 responses toward the a4b7-binding V2 loop of HIV gp120 in healthy volunteers. Clin Vaccine Immunol 19, 1557–1559.
30. Kutzler, M. A. & Weiner, D. B. (2008). DNA vaccines: ready for prime time? Nat Rev Genet 9, 776–788.
31. Lin, F., Shen, X., Kichaev, G., Mendoza, J. M., Yang, M., Armendi, P., Yan, J., Kobinger, G. P., Bello, A. & other authors (2012). Optimization of electroporation-enhanced intradermal delivery of DNA vaccine using a minimally invasive surface device. Hum Gene Ther Methods 23, 157–168.
32. Lindenbach, B. & Rice, C. M. (2007). Flaviviridae: the viruses and their replication. In Fields Virology, 5th edn, pp. 991–1042.Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams and Wilkins.
33. Luxembourg, A., Hannaman, D., Ellefsen, B., Nakamura, G. & Bernard, R. (2006). Enhancement of immune responses to an HBV DNA vaccine by electroporation. Vaccine 24, 4490–4493.
34. Maciel, M., Jr, Kellathur, S. N., Chikhlikar, P., Dhalia, R., Sidney, J., Sette, A., August, T. J. & Marques, E. T., Jr (2008). Comprehensive analysis of T cell epitope discovery strategies using 17DD yellow fever virus structural proteins and BALB/c (H2d) mice model. Virology 378, 105–117.
35. McAllister, A., Arbetman, A. E., Mandl, S., Peña-Rossi C. & Andino, R. (2000). Recombinant yellow fever viruses are effective therapeutic vaccines for treatment of murine experimental solid tumors and pulmonary metastases. J Virol 74, 9197–9205.
36. Medi, B. M., Hoselton, S., Marepalli, R. B. & Singh, J. (2005). Skin targeted DNA vaccine delivery using electroporation in rabbits: I: efficacy. Int J Pharm 294, 53–63.
37. Meier, K. C., Gardner, C. L., Khoretonenko, M. V., Klimstra, W. B. & Ryman, K. D. (2009). A mouse model for studying viscerotropic disease caused by yellow fever virus infection. PLoS Pathog 5, e1000614.
38. Monath, T. P. (2005). Yellow fever vaccine. Expert Rev Vaccines 4, 553–574.
39. Monath, T. P., Soike, K., Levenbook, I., Zhang, Z. X., Arroyo, J., Delagrave, S., Myers, G., Barrett, A. D., Shope, R. E. & other authors (1999). Recombinant, chimaeric live, attenuated vaccine (ChimeriVax) incorporating the envelope genes of Japanese encephalitis (SA14-14-2) virus and the capsid and nonstructural genes of yellow fever (17D) virus is safe, immunogenic and protective in non-human primates. Vaccine 17, 1869–1882.
40. Monath, T. P., Liu, J., Kanesa-Thasan, N., Myers, G. A., Nichols, R., Deary, A., McCarthy, K., Johnson, C., Ermak, T. & other authors (2006). A live, attenuated recombinant West Nile virus vaccine. Proc Natl Acad Sci U S A 103, 6694–6699.
41. Otten, G., Schaefer, M., Doe, B., Liu, H., Srivastava, I., zur Megede, J., O’Hagan, D., Donnelly, J., Widera, G. & other authors (2004). Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine 22, 2489–2493.
42. Otten, G. R., Schaefer, M., Doe, B., Liu, H., Megede, J. Z., Donnelly, J., Rabussay, D., Barnett, S. & Ulmer, J. B. (2006). Potent immunogenicity of an HIV-1 gag–pol fusion DNA vaccine delivered by in vivo electroporation. Vaccine 24, 4503–4509.
43. Pulendran, B. (2009). Learning immunology from the yellow fever vaccine: innate immunity to systems vaccinology. Nat Rev Immunol 9, 741–747.
44. Querec, T. D., Akondy, R. S., Lee, E. K., Cao, W., Nakaya, H. I., Teuwen, D., Pirani, A., Gernert, K., Deng, J. & other authors (2009). Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 10, 116–125.
45. Rice, C. M., Lenches, E. M., Eddy, S. R., Shin, S. J., Sheets, R. L. & Strauss, J. H. (1985). Nucleotide sequence of yellow fever virus: implications for flavivirus gene expression and evolution. Science 229, 726–733.
46. Sambrook, J., Fritsch, T. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Sangster, M. Y., Mackenzie, J. S. & Shellam, G. R. (1998). Genetically determined resistance to flavivirus infection in wild Mus musculus domesticus and other taxonomic groups in the genus Mus. Arch Virol 143, 697–715.
48. Seregin, A., Nistler, R., Borisevich, V., Yamshchikov, G., Chaporgina, E., Kwok, C. W. & Yamshchikov, V. (2006). Immunogenicity of West Nile virus infectious DNA and its noninfectious derivatives. Virology 356, 115–125.
49. Silva, P. A., Pereira, C. F., Dalebout, T. J., Spaan, W. J. & Bredenbeek, P. J. (2010). An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J Virol 84, 11395–11406.
50. Stoyanov, C. T., Boscardin, S. B., Deroubaix, S., Barba-Spaeth, G., Franco, D., Nussenzweig, R. S., Nussenzweig, M. & Rice, C. M. (2010). Immunogenicity and protective efficacy of a recombinant yellow fever vaccine against the murine malarial parasite Plasmodium yoelii. Vaccine 28, 4644–4652.
51. Tao, D., Barba-Spaeth, G., Rai, U., Nussenzweig, V., Rice, C. M. & Nussenzweig, R. S. (2005). Yellow fever 17D as a vaccine vector for microbial CTL epitopes: protection in a rodent malaria model. J Exp Med 201, 201–209.
52. Theiler, M. & Smith, H. H. (1937). The use of yellow fever virus modified by in vitro cultivation for human immunization. J Exp Med 65, 787–800.
53. Theiler, M., Smith, H. H. & Mortimer, P. (2000). The use of yellow fever virus modified by in vitro cultivation for human immunization. Rev Med Virol 10, 3–16.
54. Tilgner, M. & Shi, P. Y. (2004). Structure and function of the 39 terminal six nucleotides of the West Nile virus genome in viral replication. J Virol 78, 8159–8171.
55. Tollefsen, S., Vordermeier, M., Olsen, I., Storset, A. K., Reitan, L. J., Clifford, D., Lowrie, D. B., Wiker, H. G., Huygen, K. & other authors (2003). DNA injection in combination with electroporation: a novel method for vaccination of farmed ruminants. Scand J Immunol 57, 229–238.
56. Tretyakova, I., Nickols, B., Hidajat, R., Jokinen, J., Lukashevich, I. S. & Pushko, P. (2014). Plasmid DNA initiates replication of yellow fever vaccine in vitro and elicits virus-specific immune response in mice. Virology 468-470, 28–35.
57. van Dinten, L. C., den Boon, J. A., Wassenaar, A. L., Spaan, W. J. & Snijder, E. J. (1997). An infectious arterivirus cDNA clone: identification of a replicase point mutation that abolishes discontinuous mRNA transcription. Proc Natl Acad Sci U S A 94, 991–996.
58. Van Epps, H. L. (2005). Broadening the horizons for yellow fever: new uses for an old vaccine. J Exp Med 201, 165–168.
59. Vasan, S., Hurley, A., Schlesinger, S. J., Hannaman, D., Gardiner, D. F., Dugin, D. P., Boente-Carrera, M., Vittorino, R., Caskey, M. & other authors (2011). In vivo electroporation enhances the immunogenicity of an HIV- 1 DNA vaccine candidate in healthy volunteers. PLoS ONE 6, e19252.
60. Webster, R. G. & Robinson, H. L. (1997). DNA vaccines. BioDrugs 8, 273–292.
61. Weiner, D. B., Sardesai, N. Y. & Schmaljohn, C. (2010). Introduction to DNA vaccines – Las Vegas. Vaccine 28, 1893–1896.
62. WHO (2009). Yellow Fever Fact Sheet no.100. Geneva, Switzerland: World Health Organization. http://www.who.int/mediacentre/factsheets/fs100/en/.
63. WHO (2013). Yellow Fever Vaccine Information. Geneva, Switzerland: WorldHealth Organization. http://www.who.int/vaccines/en/yellowfever.shtml.
64. Widera, G., Austin, M., Rabussay, D., Goldbeck, C., Barnett, S. W., Chen, M., Leung, L., Otten, G. R., Thudium, K. & other authors (2000). Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 164, 4635–4640.
65. Widman, D. G., Frolov, I. & Mason, P. W. (2008). Third-generation flavivirus vaccines based on single-cycle, encapsidation-defective viruses. Adv Virus Res 72, 77–126.