Advertisement

Virus Genes

, Volume 53, Issue 4, pp 555–564 | Cite as

Newcastle disease virus-like particles induce dendritic cell maturation and enhance viral-specific immune response

  • Jing Qian
  • Jiaxin Ding
  • Renfu Yin
  • Yixue Sun
  • Cong Xue
  • Xiaohong Xu
  • Jianzhong Wang
  • Chan Ding
  • Shengqing Yu
  • Xiufan Liu
  • Shunlin Hu
  • Yanlong CongEmail author
  • Zhuang DingEmail author
Article

Abstract

Circulating of genotype VII Newcastle disease virus (NDV) is a great threat to the poultry industry worldwide. Virus-like particles (VLPs) are increasingly being considered as potential viral vaccines due to their safety and efficacy. In this study, we analyzed in vitro the stimulatory effects of VLPs containing the matrix and hemagglutinin-neuraminidase of genotype VII NDV on dendritic cells (DCs) and evaluated their immunogenicity in mice. The results showed that immature bone marrow-derived dendritic cells (BMDCs) responded to stimulation with VLPs by up-regulating expressions of MHC II, CD40, CD80, and CD86 molecules and by increasing the cytokine secretions of TNF-α, IFN-γ, IL-6, and IL-12p70. Besides, VLPs enhanced the immunostimulatory capacity of DCs to stimulate autologous T cell proliferation. Furthermore, VLPs can induce efficient humoral and cellular immune responses, and recruit mature DCs to the spleen in C57BL/6 mice, as shown by an obvious increase in double-positive proliferation of splenic CD11c+CD86+ cells. These data indicate that NDV VLPs can be a valuable candidate for NDV vaccine development.

Keywords

Newcastle disease virus Virus-like particle Dendritic cell Immune response 

Notes

Acknowledgements

This work was supported by the Special Fund for Agro-scientific Research in the Public Interest (201303033) and the National Natural Science Foundation of China (31272561, 31472195, 31402195).

Author’s contribution

JQ, JD, YC, RY, YS, CX, XX, and ZD conceived and designed the experiments; JQ, JD, YS, and XX performed the experiments; JQ, YC, JW, RY analyzed the data; YS, CX, JW, CD, SY, XL, SH, and ZD contributed reagents/materials/analysis tools; JQ, XX, and YC wrote the paper. RY, XL, YC, and ZD requested financial support. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing interests exist.

Ethical approval

This study was conducted in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the Ministry of Science and Technology of the People’s Republic of China. The protocols for animal studies were approved by the Committee on the Ethics of Animal Experiments of Jilin University (approval numbers 2015047815-1 for mice).

Supplementary material

11262_2017_1451_MOESM1_ESM.docx (50 kb)
Supplementary material 1 (DOCX 50 kb)

References

  1. 1.
    D.J. Alexander, Rev. Sci. Tech. 19, 443–462 (2000)CrossRefPubMedGoogle Scholar
  2. 2.
    M.A. Mayo, Adv. Virol. 147, 1655–1663 (2002)Google Scholar
  3. 3.
    V. Zaitsev, I.M. Von, D. Groves, M. Kiefel, T. Takimoto, A. Portner, G. Taylor, J. Virol. 78, 3733–3741 (2004)CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    P.J. Miller, D.J. King, C.L. Afonso, D.L. Suarez, Vaccine 25, 7238–7246 (2007)CrossRefPubMedGoogle Scholar
  5. 5.
    H. Liu, Z. Wang, Y. Wu, D. Zheng, C. Sun, D. Bi, Y. Zuo, T. Xu, J. Virol. Methods 140, 206–211 (2007)CrossRefPubMedGoogle Scholar
  6. 6.
    A. Lu, Y. Diao, H. Chen, J. Wang, P. Ge, X. Sun, D. Hao, Avian Pathology 43, 325 (2014)CrossRefPubMedGoogle Scholar
  7. 7.
    I. Cornax, P.J. Miller, C.L. Afonso, Avian Dis. 56, 464 (2012)CrossRefPubMedGoogle Scholar
  8. 8.
    A. Roldão, M.C.M. Mellado, L.R. Castilho, M.J. Carrondo, P.M. Alves, Expert Review of Vaccines 9, 1149–1176 (2014)CrossRefGoogle Scholar
  9. 9.
    R. Noad, P. Roy, Trends Microbiol. 11, 438–444 (2003)CrossRefPubMedGoogle Scholar
  10. 10.
    Group F.I.S., N. Engl. J. Med. 356, 1915–1927 (2007)CrossRefGoogle Scholar
  11. 11.
    S. Yin, S. Sun, S. Yang, Y. Shang, X. Cai, X. Liu, Virology Journal 7, 1–5 (2010)CrossRefGoogle Scholar
  12. 12.
    G.T. Jennings, M.F. Bachmann, Biol. Chem. 389, 521–536 (2008)CrossRefPubMedGoogle Scholar
  13. 13.
    N. Kushnir, S.J. Streatfield, V. Yusibov, Vaccine 31, 58–83 (2012)CrossRefPubMedGoogle Scholar
  14. 14.
    L.W. Mcginnes, H. Pantua, J.P. Laliberte, K.A. Gravel, S. Jain, T.G. Morrison, J. Virol. 84, 4513–4523 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    H.D. Pantua, L.W. Mcginnes, M.E. Peeples, T.G. Morrison, J. Virol. 80, 11062–11073 (2006)CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    X.R. Wang, G.M. Yan, R. Zhang, X.L. Lang, Y.L. Yang, X.Y. Li, S. Chen, J. Qian, X.L. Wang, Mol. Med. Rep. 9, 653–658 (2014)PubMedGoogle Scholar
  17. 17.
    T.G. Morrison, Future Virol. 5, 545–554 (2011)CrossRefGoogle Scholar
  18. 18.
    M.J. Robinson, D. Sancho, E.C. Slack, S. LeibundGut-Landmann, C. Reis e Sousa, Nat. Immunol. 7, 1258–1265 (2006)CrossRefPubMedGoogle Scholar
  19. 19.
    M. Cella, F. Sallusto, A. Lanzavecchia, Curr. Opin. Immunol. 9, 10–16 (1997)CrossRefPubMedGoogle Scholar
  20. 20.
    C. Ardavín, S. Amigorena, E.S.C. Reis, Immunity 20, 17–23 (2004)CrossRefPubMedGoogle Scholar
  21. 21.
    J.Y. Noh, J.K. Park, D.H. Lee, S.S. Yuk, J.H. Kwon, S.W. Lee, J.B. Lee, S.Y. Park, I.S. Choi, C.S. Song, PLoS ONE 11, e0162946 (2016)CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    M. Xu, Z. Ding, J.Y. Wan, L. Liu, J. Xu, J. Arch. Virol. 153, 1797 (2008)CrossRefGoogle Scholar
  23. 23.
    L.W. Mcginnes, T.G. Morrison, Curr. Protoc. Microbiol. 30, 18.12.11–18.12.21 (2013)Google Scholar
  24. 24.
    Oie A.H.S., in Bulletin. Office international des épizooties, Paris, pp. 1092–1106 (2008)Google Scholar
  25. 25.
    M.B. Lutz, N. Kukutsch, A.L.J. Ogilvie, S. Rößner, F. Koch, N. Romani, G. Schuler, J. Immunol. Methods 223, 77–92 (1999)CrossRefPubMedGoogle Scholar
  26. 26.
    D. Gray, P. Dullforce, S. Jainandunsing, J. Exp. Med. 180, 141–155 (1994)CrossRefPubMedGoogle Scholar
  27. 27.
    Z.J. Li, L. Yang, C. Shuang, D. Zhuang, L.Z. Mu, Y.L. Cong, Adv. Virol. 155, 499–505 (2010)Google Scholar
  28. 28.
    H. Shen, C. Xue, L. Lv, W. Wang, Q. Liu, K. Liu, X. Chen, J. Zheng, X. Li, Y. Cao, Virus Res. 178, 430–436 (2013)CrossRefPubMedGoogle Scholar
  29. 29.
    J.M. Trevejo, M.W. Marino, N. Philpott, R. Josien, E.C. Richards, K.B. Elkon, E. Falck-Pedersen, Proc. Natl. Acad. Sci. 98, 12162–12167 (2001)CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    M.Z. Ladjemi, M. Lecocq, B. Weynand, H. Bowen, H.J. Gould, S.J. Van, B. Detry, C. Pilette, Eur. Respir. J. 45, 980–993 (2015)CrossRefPubMedGoogle Scholar
  31. 31.
    P.L. Vieira, E.C. de Jong, E.A. Wierenga, M.L. Kapsenberg, P. Kaliński, J. Immunol. 164, 4507–4512 (2000)CrossRefPubMedGoogle Scholar
  32. 32.
    S.B. Boscardin, J.C. Hafalla, R.F. Masilamani, A.O. Kamphorst, H.A. Zebroski, U. Rai, A. Morrot, F. Zavala, R.M. Steinman, R.S. Nussenzweig, J. Exp. Med. 203, 599–606 (2006)CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    M. Inobe, N. Aoki, P.S. Linsley, J.A. Ledbetter, R. Abe, M. Murakami, T. Uede, J. Immunol. 157, 582–588 (1996)PubMedGoogle Scholar
  34. 34.
    M.A. Mir, Costimulation Immunotherapy in Allergies and Asthma (ACP Press, Sydney, 2015)CrossRefGoogle Scholar
  35. 35.
    Z. Wu, L. Rothwell, J.R. Young, J. Kaufman, C. Butter, P. Kaiser, Immunology 129, 133–145 (2009)CrossRefPubMedGoogle Scholar
  36. 36.
    W.G.J. Degen, N.V. Daal, L. Rothwell, P. Kaiser, V.E.J.C. Schijns, Vet. Microbiol. 105, 163–167 (2005)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Jing Qian
    • 1
    • 2
  • Jiaxin Ding
    • 1
    • 2
  • Renfu Yin
    • 1
    • 2
  • Yixue Sun
    • 3
  • Cong Xue
    • 1
    • 2
  • Xiaohong Xu
    • 1
    • 2
  • Jianzhong Wang
    • 3
  • Chan Ding
    • 4
  • Shengqing Yu
    • 4
  • Xiufan Liu
    • 5
  • Shunlin Hu
    • 5
  • Yanlong Cong
    • 1
    • 2
    Email author
  • Zhuang Ding
    • 1
    • 2
    Email author
  1. 1.Laboratory of Infectious Diseases, College of Veterinary MedicineJilin UniversityChangchunChina
  2. 2.Key Laboratory of Zoonosis Research, Ministry of EducationJilin UniversityChangchunChina
  3. 3.Engineering Research Center of Jilin Province for Animals Probiotics, College of Animal Science and TechnologyJilin Agricultural UniversityChangchunChina
  4. 4.Shanghai Veterinary Research InstituteChinese Academy of Agricultural SciencesShanghaiChina
  5. 5.Animal Infectious Disease Laboratory, College of Veterinary MedicineYangzhou UniversityYangzhouChina

Personalised recommendations