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Archives of Virology

, Volume 164, Issue 2, pp 359–370 | Cite as

Evaluation of an African swine fever (ASF) vaccine strategy incorporating priming with an alphavirus-expressed antigen followed by boosting with attenuated ASF virus

  • Maria V. Murgia
  • Mark Mogler
  • Andrea Certoma
  • Diane Green
  • Paul Monaghan
  • David T. Williams
  • Raymond R. R. Rowland
  • Natasha N. GaudreaultEmail author
Original Article

Abstract

In this study, an alphavirus vector platform was used to deliver replicon particles (RPs) expressing African swine fever virus (ASFV) antigens to swine. Alphavirus RPs expressing ASFV p30 (RP-30), p54 (RP-54) or pHA-72 (RP-sHA-p72) antigens were constructed and tested for expression in Vero cells and for immunogenicity in pigs. RP-30 showed the highest expression in Vero cells and was the most immunogenic in pigs, followed by RP-54 and RP-sHA-p72. Pigs primed with two doses of the RP-30 construct were then boosted with a naturally attenuated ASFV isolate, OURT88/3. Mapping of p30 identified an immunodominant region within the amino acid residues 111–130. However, the principal effect of the prime-boost was enhanced recognition of an epitope covered by the peptide sequence 61–110. The results suggest that a strategy incorporating priming with a vector-expressed antigen followed by boosting with an attenuated live virus may broaden the recognition of ASFV epitopes.

Notes

Acknowledgements

We would like to acknowledge Dr. Baker for the contribution of the pHUE expression vector. We also thank Luca Popescu, Vlad Petrovan, Ana Stoian, and the personnel at the Biosecurity Research Institute for technical assistance.

Funding

This work was funded by the Kansas National Bio and Agro-Defense Facility (NBAF) Transition Fund. Partial support was from the Department of Homeland Security Center of Excellence for Emerging and Zoonotic Animal Diseases (CEEZAD) (Grant no. 2010-ST061-AG0001), and Kansas Biosciences Authority/CEEZAD matching funds (Award no. BG2428).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

Experiments involving animals and viruses were performed in accordance with the Federation of Animal Science Societies Guide for the Care and Use of Agricultural Animals in Research and Teaching, the USDA Animal Welfare Act and Animal Welfare Regulations, and were approved by the Kansas State University animal care and use committees and institutional biosafety committees. This article does not contain any studies with human participants performed by any of the authors.

References

  1. 1.
    Alonso C, Borca M, Dixon L, Revilla Y, Rodriguez F, Escribano JM, ICTV Report Consortium (2018) ICTV virus taxonomy profile: Asfarviridae. J Gen Virol 99(5):613–614CrossRefGoogle Scholar
  2. 2.
    Tabares E, Martínez J, Martín E, Escribano JM (1983) Proteins specified by African Swine Fever virus. IV. Glycoproteins and phosphoproteins. Arch Virol 77:167–180CrossRefGoogle Scholar
  3. 3.
    Escribano JM, Tabares E (1987) Proteins specified by African swine fever virus: V. Identification of immediate early, early and late proteins. Arch Virol 92:221–232CrossRefGoogle Scholar
  4. 4.
    Kollnberger SD, Gutierrez-Castañeda B, Foster-Cuevas M, Corteyn A, Parkhouse RM (2002) Identification of the principal serological immunodeterminants of African swine fever virus by screening a virus cDNA library with antibody. J Gen Virol 83:1331–1342CrossRefGoogle Scholar
  5. 5.
    Gomez-Puertas P, Rodríguez F, Oviedo JM, Brun A, Alonso C, Escribano JM (1998) The African swine fever virus proteins p54 and p30 are involved in two distinct steps of virus attachment and both contribute to the antibody-mediated protective immune response. Virology 243:461–471CrossRefGoogle Scholar
  6. 6.
    Neilan JG, Zsak L, Lu Z, Burrage TG, Kutish GF, Rock DL (2004) Neutralizing antibodies to African swine fever virus proteins p30, p54, and p72 are not sufficient for antibody-mediated protection. Virology 319:337–342CrossRefGoogle Scholar
  7. 7.
    Barderas MG, Rodríguez F, Gómez-Puertas P, Avilés M, Beitia F, Alonso C et al (2001) Antigenic and immunogenic properties of a chimera of two immunodominant African swine fever virus proteins. Arch Virol 146:1681–1691CrossRefGoogle Scholar
  8. 8.
    Argilaguet JM, Pérez-Martín E, Nofrarías M, Gallardo C, Accensi F, Lacasta A et al (2012) DNA vaccination partially protects against African swine fever virus lethal challenge in the absence of antibodies. PLoS One 7:e40942CrossRefGoogle Scholar
  9. 9.
    Argilaguet JM, Pérez-Martín E, López S, Goethe M, Escribano JM, Giesow K et al (2013) BacMam immunization partially protects pigs against sublethal challenge with African swine fever virus. Antiviral Res 98:61–65CrossRefGoogle Scholar
  10. 10.
    Mogler M, Erdman M,Vander Veen R, Harris DLH, Owens G, Kamrud K et al (2009) Replicon particle PRRSV vaccine provides partial protection from challenge. In: Proceedings of the American Association of Swine Veterinarians, 40th annual meeting, pp 367–368Google Scholar
  11. 11.
    Mogler M, Vander Veen R, McVicker J, Russel B, Harris DLH (2010) Vaccination of pigs with PRRVENT or PrrSV-RP recombinant vaccines reduces viremia following heterologous challenge. In: Proceedings of the American Association of Swine Veterinarians, 41st annual meeting, pp 403–404Google Scholar
  12. 12.
    Vander Veen RL, Loynachan AT, Mogler MA, Russell BJ, Harris DLH, Kamrud KI (2012) Safety, immunogenicity, and efficacy of an alphavirus replicon-based swine influenza virus hemagglutinin vaccine. Vaccine 30:1944–1950CrossRefGoogle Scholar
  13. 13.
    Vander Veen RL, Mogler MA, Russell BJ, Loynachan AT, Harris DLH, Kamrud KI (2013) Haemagglutinin and nucleoprotein replicon particle vaccination of swine protects against the pandemic H1N1 2009 virus. Vet Rec 173:344CrossRefGoogle Scholar
  14. 14.
    Mogler MA, Gander J, Harris DLH (2014) Development of an alphavirus RNA particle vaccine against portice epidemic diarrhea virus. In: Proceedings of the American Association of Swine Veterinarians, 45th annual meeting, pp 63–64Google Scholar
  15. 15.
    Boinas FS, Hutchings GH, Dixon LK, Wilkinson PJ (2004) Characterization of pathogenic and non-pathogenic African swine fever virus isolates from Ornithodoros erraticus inhabiting pig premises in Portugal. J Gen Virol 85:2177–2187CrossRefGoogle Scholar
  16. 16.
    King K, Chapman D, Argilaguet JM, Fishbourne E, Hutet E, Cariolet R, Hutchings G, Oura CA, Netherton CL, Moffat K, Taylor G, Le Potier MF, Dixon LK, Takamatsu HH (2011) Protection of European domestic pigs from virulent African isolates of African swine fever virus by experimental immunisation. Vaccine 29:4593–4600CrossRefGoogle Scholar
  17. 17.
    Mulumba-Mfumu LK, Goatley LC, Saegerman C, Takamatsu HH, Dixon LK (2016) Immunization of African indigenous pigs with attenuated genotype I African swine fever virus OURT88/3 induces protection against challenge with virulent strains of genotype I. Transbound Emerg Dis 63:e323–e327CrossRefGoogle Scholar
  18. 18.
    Abrams CC, Goatley L, Fishbourne E, Chapman D, Cooke L, Oura CA, Netherton CL, Takamatsu HH, Dixon LK (2013) Deletion of virulence associated genes from attenuated African swine fever virus isolate OUR T88/3 decreases its ability to protect against challenge with virulent virus. Virology 443:99–105CrossRefGoogle Scholar
  19. 19.
    Kamrud KI, Custer M, Dudek JM, Owens G, Alterson KD, Lee JS et al (2007) Alphavirus replicon approach to promoterless analysis of IRES elements. Virology 360:376–387CrossRefGoogle Scholar
  20. 20.
    Hierholzer JC, Killington RA (1996) 2—Virus isolation and quantitation A2—Mahy, Brian WJ. In: Kangro HO (ed) Virology methods manual. Academic Press, London, pp 25–46.  https://doi.org/10.1016/B978-012465330-6/50003-8 (Prickett J, Simer R) CrossRefGoogle Scholar
  21. 21.
    Christopher-Hennings J, Yoon K-J, Evans RB, Zimmerman JJ (2008) Detection of Porcine reproductive and respiratory syndrome virus infection in porcine oral fluid samples: a longitudinal study under experimental conditions. J Vet Diagn Investig 20:156–163CrossRefGoogle Scholar
  22. 22.
    King DP, Reid SM, Hutchings GH, Grierson SS, Wilkinson PJ, Dixon LK, Bastos AD, Drew TW (2003) Development of a TaqMan PCR assay with internal amplification control for the detection of African swine fever virus. J Virol Methods 107:53–61CrossRefGoogle Scholar
  23. 23.
    Catanzariti A-M, Soboleva TA, Jans DA, Board PG, Baker RT (2004) An efficient system for high-level expression an easy purification of authentic recombinant proteins. Protein Sci 13:1331–1339CrossRefGoogle Scholar
  24. 24.
    Hernaez B, Escribano JM, Alonso C (2008) African swine fever virus protein p30 interaction with heterogeneous nuclear ribonucleoprotein K (hnRNP-K) during infection. FEBS Lett 582:3275–3280CrossRefGoogle Scholar
  25. 25.
    Oviedo JM, Rodriguez F, Gomez-Puertas P, Brun A, Gomez N, Alonso Cand Escribano JM (1997) High level expression of the major antigenic African swine fever virus proteins p54 and p30 in baculovirus and their potential use as diagnostic reagents. J Virol Methods 64:27–35CrossRefGoogle Scholar
  26. 26.
    Prados FJ, Vinuela E, Alcami A (1993) Sequence and characterization of the major early phosphoprotein p32 of African swine fever virus. J Virol 67(5):2475–2485Google Scholar
  27. 27.
    Gomez-Puertas P, Rodríguez F, Oviedo JM, Ramiro-Ibáñez F, Ruiz-Gonzalvo F, Alonso C et al (1996) Neutralizing antibodies to different proteins of African swine fever virus inhibit both virus attachment and internalization. J Virol 70:5689–5694Google Scholar
  28. 28.
    Takamatsu HH, Denyer MS, Lacasta A, Stirling CM, Argilaguet JM, Netherton CL, Oura CA, Martins C, Rodriguez F (2013) Cellular immunity in ASFV responses. Virus Res 173:110–121CrossRefGoogle Scholar
  29. 29.
    Oura CA, Denyer MS, Takamatsu H, Parkhouse RM (2005) In vivo depletion of CD8+ T lymphocytes abrogates protective immunity to African swine fever virus. J Gen Virol 86:2445–2450CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Diagnostic Medicine and Pathobiology, College of Veterinary MedicineKansas State UniversityManhattanUSA
  2. 2.Merck Animal HealthAmesUSA
  3. 3.CSIRO Australian Animal Health LaboratoryGeelongAustralia

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