Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Multiple Alternating Immunizations with DNA Vaccine and Replication-incompetent Adenovirus Expressing gB of Pseudorabies Virus Protect Animals Against Lethal Virus Challenge

  • Kim, Seon-Ju (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • Kim, Hye-Kyung (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • Han, Young-Woo (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • Aleyas, Abi G. (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • George, Junu A. (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • Yoon, Hyun-A (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University) ;
  • Yoo, Dong-Jin (Department of Chemistry, Seonam University) ;
  • Kim, Koan-Hoi (Department of Pharmacology, School of Medicine, Pusan National University) ;
  • Eo, Seong-Kug (Laboratory of Microbiology, College of Veterinary Medicine and Bio-Safety Research Institute, Chonbuk National University)
  • Published : 2008.07.31
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Abstract

The prime-boost vaccination with DNA vaccine and recombinant viral vector has emerged as an effective prophylactic strategy to control infectious diseases. Here, we compared the protective immunities induced by multiple alternating immunizations with DNA vaccine (pCIgB) and replication-incompetent adenovirus (Ad-gB) expressing glycoprotein gB of pseudorabies virus (PrV). The platform of pCIgB-prime and Ad-gB-boost induced the most effective immune responses and provided protection against virulent PrV infection. However, priming with pCIgB prior to vaccinating animals by the DNA vaccine-prime and Ad-boost protocol provided neither effective immune responses nor protection against PrV. Similarly, boosting with Ad-gB following immunization with DNA vaccine-prime and Ad-boost showed no significant responses. Moreover, whereas the administration of Ad-gB for primary immunization induced Th2-type-biased immunity, priming with pCIgB induced Th1-type-biased immunity, as judged by the production of PrV-specific IgG isotypes and cytokine IFN-$\gamma$. These results indicate that the order and injection frequency of vaccine vehicles used for heterologous prime-boost vaccination affect the magnitude and nature of the immunity. Therefore, our demonstration implies that the prime-boost protocol should be carefully considered and selected to induce the desired immune responses.

Keywords

References

  1. Amara, R. R., F. Villinger, J. D. Altman, S. L. Lydy, S. P. O'Neil, S. I. Staprans, et al. 2002. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Vaccine 20: 1949-1955 https://doi.org/10.1016/S0264-410X(02)00076-2
  2. Barouch, D. H. and G. J. Nabel. 2005. Adenovirus vector-based vaccines for human immunodeficiency virus type 1. Hum. Gene Ther. 16: 149-156 https://doi.org/10.1089/hum.2005.16.149
  3. Bianchi, A. T., H. W. Moonen-Leusen, F. J. van Milligen, H. F. Savelkoul, R. J. Zwart, and T. G. Kimman. 1998. A mouse model to study immunity against Pseudorabies virus infection: Significance of CD4+ and CD8+ cells in protective immunity. Vaccine 16: 1550-1558 https://doi.org/10.1016/S0264-410X(98)00044-9
  4. Casimiro, D. R., A. J. Bett, T. M. Fu, M. E. Davies, A. Tang, K. A. Wilson, et al. 2004. Heterologous human immunodeficiency virus type 1 priming-boosting immunization strategies involving replication-defective adenovirus and poxvirus vaccine vectors. J. Virol. 78: 11434-11438 https://doi.org/10.1128/JVI.78.20.11434-11438.2004
  5. Dory, D., T. Fischer, V. Beven, R. Cariolet, H. J. Rziha, and A. Jestin. 2006. Prime-boost immunization using DNA vaccine and recombinant Orf virus protects pigs against Pseudorabies virus (Herpes suid 1). Vaccine 24: 6256-6263 https://doi.org/10.1016/j.vaccine.2006.05.078
  6. Dory, D., A. M. Torche, V. Beven, P. Blanchard, C. Loizel, R. Cariolet, and A. Jestin. 2005. Effective protection of pigs against lethal Pseudorabies virus infection after a single injection of low-dose Sindbis-derived plasmids encoding PrV gB, gC, and gD glycoproteins. Vaccine 23: 3483-3491 https://doi.org/10.1016/j.vaccine.2004.10.050
  7. Dufour, V. and C. De Boisseson. 2003. Use of a Sindbis virus DNA-based expression vector for induction of protective immunity against Pseudorabies virus in pigs. Vet. Immunol. Immunopathol. 93: 125-134 https://doi.org/10.1016/S0165-2427(03)00066-7
  8. Eo, S. K., S. Lee, S. Chun, and B. T. Rouse. 2001. Modulation of immunity against herpes simplex virus infection via mucosal genetic transfer of plasmid DNA encoding chemokines. J. Virol. 75: 569-578 https://doi.org/10.1128/JVI.75.2.569-578.2001
  9. Fischer, L., S. Barzu, C. Andreoni, N. Buisson, A. Brun, and J. C. Audonnet. 2003. DNA vaccination of neonate piglets in the face of maternal immunity induces humoral memory and protection against a virulent Pseudorabies virus challenge. Vaccine 21: 1732-1741 https://doi.org/10.1016/S0264-410X(02)00736-3
  10. Fitzgerald, J. C., G. P. Gao, A. Reyes-Sandoval, G. N. Pavlakis, Z. Q. Xiang, A. P. Wlazlo, W. Giles-Davis, J. M. Wilson, and H. C. Ertl. 2003. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J. Immunol. 170: 1416-1422 https://doi.org/10.4049/jimmunol.170.3.1416
  11. Gonin, P., W. Oualikene, A. Fournier, and M. Eloit. 1996. Comparison of the efficacy of replication-defective adenovirus and Nyvac poxvirus as vaccine vectors in mice. Vaccine 14: 1083-1087 https://doi.org/10.1016/0264-410X(95)00226-Q
  12. Griot, C., C. Moser, P. Cherpillod, L. Bruckner, R. Wittek, A. Zurbriggen, and R. Zurbriggen. 2004. Early DNA vaccination of puppies against canine distemper in the presence of maternally derived immunity. Vaccine 22: 650-654 https://doi.org/10.1016/j.vaccine.2003.08.022
  13. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, et al. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745 https://doi.org/10.1038/35047123
  14. Hong, W., S. Xiao, R. Zhou, L. Fang, Q. He, B. Wu, F. Zhou, and H. Chen. 2002. Protection induced by intramuscular immunization with DNA vaccines of Pseudorabies in mice, rabbits and piglets. Vaccine 20: 1205-1214 https://doi.org/10.1016/S0264-410X(01)00416-9
  15. Huh, S., K. Lee, H.-S. Yun, D.-J. Paik, J. M. Kim, and J. Youn. 2007. Functions of metallothionein generating interleukin-10-producing regulatory CD4+ T cells potentiate suppression of collagen-induced arthritis. J. Microbiol. Biotechnol. 17: 348-358
  16. Kent, S. J., A. Zhao, S. J. Best, J. D. Chandler, D. B. Boyle, and I. A. Ramshaw. 1998. Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant Fowlpox virus. J. Virol. 72: 10180-10188
  17. Kit, S. 1990. Genetically engineered vaccines for control of Aujeszky's disease (Pseudorabies). Vaccine 8: 420-424 https://doi.org/10.1016/0264-410X(90)90240-M
  18. Kluge, J. P., G. W. Beren, H. T. Hill, and K. B. Platt, Pseudorabies (Aujeszky's disease), 1999. pp. 233-246. In B. E. Straw, S. D'Aillaire, W. L. Mengeling, and D. J. Taylor (eds.), Disease of Swine, 8th Ed. Iowa State University Press, Ames, Iowa
  19. Letvin, N. L., Y. Huang, B. K. Chakrabarti, L. Xu, M. S. Seaman, K. Beaudry, et al. 2004. Heterologous envelope immunogens contribute to AIDS vaccine protection in Rhesus monkeys. J. Virol. 78: 7490-7497 https://doi.org/10.1128/JVI.78.14.7490-7497.2004
  20. Ludewig, B., K. J. Maloy, C. Lopez-Macias, B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 2000. Induction of optimal anti-viral neutralizing B cell responses by dendritic cells requires transport and release of virus particles in secondary lymphoid organs. Eur. J. Immunol. 30: 185-196 https://doi.org/10.1002/1521-4141(200001)30:1<185::AID-IMMU185>3.0.CO;2-L
  21. McConkey, S. J., W. H. Reece, V. S. Moorthy, D. Webster, S. Dunachie, G. Butcher, et al. 2003. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med. 9: 729-735 https://doi.org/10.1038/nm881
  22. Mettenleiter, T. C. 1996. Immunobiology of Pseudorabies (Aujeszky's disease). Vet. Immunol. Immunopathol. 54: 221-229 https://doi.org/10.1016/S0165-2427(96)05695-4
  23. Monteil, M., M. F. Le Pottier, A. A. Ristov, R. Cariolet, R. L'Hospitalier, B. Klonjkowski, and M. Eloit. 2000. Single inoculation of replication-defective adenovirus-vectored vaccines at birth in piglets with maternal antibodies induces high level of antibodies and protection against Pseudorabies. Vaccine 18: 1738-1742 https://doi.org/10.1016/S0264-410X(99)00545-9
  24. Passarinha, L. A., M. M. Diogo, J. A. Queiroz, G. A. Monteiro, and L. P. Fonseca. 2006. Production of ColE1 type plasmid by Escherichia coli DH5$\alpha$ cultured under nonselective conditions. J. Microbiol. Biotechnol. 16: 1026-1031
  25. Perkins, S. D., L. M. O'Brien, and R. J. Phillpotts. 2006. Boosting with an adenovirus-based vaccine improves protective efficacy against Venezuelan equine encephalitis virus following DNA vaccination. Vaccine 24: 3440-3445 https://doi.org/10.1016/j.vaccine.2006.02.020
  26. Randrianarison-Jewtoukoff, V. and M. Perricaudet. 1995. Recombinant adenoviruses as vaccines. Biologicals 23: 145-157 https://doi.org/10.1006/biol.1995.0025
  27. Rocha, C. D., B. C. Caetano, A. V. Machado, and O. Bruna-Romero. 2004. Recombinant viruses as tools to induce protective cellular immunity against infectious diseases. Int. Microbiol. 7: 83-94
  28. Rollier, C., E. J. Verschoor, G. Paranhos-Baccala, J. A. Drexhage, B. E. Verstrepen, J. L. Berland, 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 https://doi.org/10.1086/432517
  29. Schijns, V. E., B. L. Haagmans, E. O. Rijke, S. Huang, M. Aguet, and M. C. Horzinek. 1994. IFN-gamma receptor-deficient mice generate antiviral Th1-characteristic cytokine profiles but altered antibody responses. J. Immunol. 153: 2029-2037
  30. Schneider, J., S. C. Gilbert, T. J. Blanchard, T. Hanke, K. J. Robson, C. M. Hannan, et al. 1998. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat. Med. 4: 397-402 https://doi.org/10.1038/nm0498-397
  31. Sedegah, M., M. Belmonte, J. E. Epstein, C. A. Siegrist, W. R. Weiss, T. R. Jones, M. Lu, D. J. Carucci, and S. L. Hoffman. 2003. Successful induction of CD8 T cell-dependent protection against malaria by sequential immunization with DNA and recombinant poxvirus of neonatal mice born to immune mothers. J. Immunol. 171: 3148-3153 https://doi.org/10.4049/jimmunol.171.6.3148
  32. Shiver, J. W., T. M. Fu, L. Chen, D. R. Casimiro, M. E. Davies, R. K. Evans, et al. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415: 331-335 https://doi.org/10.1038/415331a
  33. Sullivan, N. J., A. Sanchez, P. E. Rollin, Z. Y. Yang, and G. J. Nabel. 2000. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408: 605-609 https://doi.org/10.1038/35046108
  34. Tritel, M., A. M. Stoddard, B. J. Flynn, P. A. Darrah, C. Y. Wu, U. Wille, et al. 2003. Prime-boost vaccination with HIV-1 Gag protein and cytosine phosphate guanosine oligodeoxynucleotide, followed by adenovirus, induces sustained and robust humoral and cellular immune responses. J. Immunol. 171: 2538-2547 https://doi.org/10.4049/jimmunol.171.5.2538
  35. van Rooij, E. M., M. G. de Bruin, Y. E. de Visser, W. G. Middel, W. J. Boersma, and A. T. Bianchi. 2004. Vaccineinduced T cell-mediated immunity plays a critical role in early protection against Pseudorabies virus (suid herpes virus type 1) infection in pigs. Vet. Immunol. Immunopathol. 99: 113-125 https://doi.org/10.1016/j.vetimm.2004.01.004
  36. Walhout, A. J., G. F. Temple, M. A. Brasch, J. L. Hartley, M. A. Lorson, S. van den Heuvel, and M. Vidal. 2000. GATEWAY recombinational cloning: Application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328: 575-592 https://doi.org/10.1016/S0076-6879(00)28419-X
  37. Wesley, R. D., M. Tang, and K. M. Lager. 2004. Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine 22: 3427-3434 https://doi.org/10.1016/j.vaccine.2004.02.040
  38. Woo, G. J., E. Y. Chun, K. H. Kim, and W. Kim. 2005. Analysis of immune responses against nucleocapsid protein of the Hantaan virus elicited by virus infection or DNA vaccination. J. Microbiol. 43: 537-545
  39. Woodland, D. L. 2004. Jump-starting the immune system: Prime-boosting comes of age. Trends Immunol. 25: 98-104 https://doi.org/10.1016/j.it.2003.11.009
  40. Wu, L., W. P. Kong, and G. J. Nabel. 2005. Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immunodeficiency virus Env and Gag immunogens. J. Virol. 79: 8024-8031 https://doi.org/10.1128/JVI.79.13.8024-8031.2005
  41. Yoon, H. A., A. G. Aleyas, J. A. George, S. O. Park, Y. W. Han, S. H. Kang, J. G. Cho, and S. K. Eo. 2006. Differential segregation of protective immunity by encoded antigen in DNA vaccine against Pseudorabies virus. Immunol. Cell Biol. 84: 502-511 https://doi.org/10.1111/j.1440-1711.2006.01463.x
  42. Yoon, H. A. and S. K. Eo. 2007. Differential polarization of immune responses by genetic cotransfer of chemokines changes the protective immunity of DNA vaccine against Pseudorabies virus. Immunology 120: 182-191 https://doi.org/10.1111/j.1365-2567.2006.02490.x
  43. Yoon, H. A., S. K. Eo, A. G. Aleyas, S. O. Park, J. H. Lee, J. S. Chae, J. G. Cho, and H. J. Song. 2005. Molecular survey of latent Pseudorabies virus infection in nervous tissues of slaughtered pigs by nested and real-time PCR. J. Microbiol. 43: 430-436
  44. Zhang, X., S. Sun, I. Hwang, D. F. Tough, and J. Sprent. 1998. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 8: 591-599 https://doi.org/10.1016/S1074-7613(00)80564-6