Characterization of humoral responses induced by an H7N9 influenza virus-like particle vaccine in BALB/C mice

Viruses

Volumn 7, Issue 8, 2015, Pages 4369-4384

  Zhang, Li ^a   Lu, Jing ^a   Chen, Yin ^a   Shi, Fengjuan ^a   Yu, Huiyan ^a   Huang, Chao ^a   Cui, Lunbiao ^a   Shi, Zhiyang ^a   Jiao, Yongjun ^a   Hu, Yuemei ^a  

^a JIANGSU PROVINCIAL CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Cross reactivity; H7N9 avian influenza; Neutralizing antibodies; Vaccine; Virus like particles

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; IMMUNOGLOBULIN G; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; MATRIX 1 PROTEIN; MATRIX PROTEIN; SIALIDASE; UNCLASSIFIED DRUG; VIRUS LIKE PARTICLE VACCINE; VIRUS RNA; HEMAGGLUTININ, AVIAN INFLUENZA A VIRUS; M1 PROTEIN, INFLUENZA A VIRUS; NA PROTEIN, INFLUENZA A VIRUS; NEUTRALIZING ANTIBODY; VIRAL PROTEIN; VIRUS ANTIBODY;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; BIOSAFETY; CELLULAR IMMUNITY; CHINA; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENE AMPLIFICATION; GENETIC TRANSFECTION; HEMAGGLUTINATION; HEMAGGLUTINATION INHIBITION; HUMORAL IMMUNITY; IMMUNIZATION; INFLUENZA A VIRUS (H7N9); MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; VIRUS NEUTRALIZATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELL LINE; GENETICS; HEMAGGLUTINATION INHIBITION TEST; HUMAN; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; ISOLATION AND PURIFICATION; SECRETION (PROCESS); SERODIAGNOSIS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRAMUSCULAR; INTERFERON-GAMMA; MICE, INBRED BALB C; NEURAMINIDASE; NEUTRALIZATION TESTS; T-LYMPHOCYTES, CYTOTOXIC; VACCINES, VIRUS-LIKE PARTICLE; VIRAL MATRIX PROTEINS; VIRAL PROTEINS;

EID: 84941100783     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7082821     Document Type: Article

References (39)

1. Dai, J.; Zhou, X.; Dong, D.; Liu, Y.; Gu, Q.; Zhu, B.; Wu, C.; Cai, H. Human infection with a novel avian-origin influenza A (H7N9) virus: Serial chest radiographic and ct findings. Chin. Med. J. 2014, 127, 2206-2211. [PubMed]
2. World Health Organization. Human infection with avian influenza A (H7N9) virus in China. World Health Organization 2013 April. Available online: http://www.who.int/csr/don/2013_04_18/en/ (accessed on 18 April 2013).
3. Gao, R.; Cao, B.; Hu, Y.; Feng, Z.; Wang, D.; Hu, W.; Chen, J.; Jie, Z.; Qiu, H.; Xu, K.; et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 2013, 368, 1888-1897. [CrossRef] [PubMed]
4. Wikipedia. Influenza A virus subtype H7N9. Wikipedia 2014 July. Available online: http://en.wikipedia.org/wiki/Influenza_A_virus_subtype_H7N9 (accessed on 15 July 2014).
5. Liao, Q.; Ip, D.K.; Tsang, T.K.; Cao, B.; Jiang, H.; Liu, F.; Zheng, J.; Peng, Z.; Wu, P.; Huai, Y.; et al. A clinical prediction rule for diagnosing human infections with avian influenza A (H7N9) in a hospital emergency department setting. BMC Med. 2014, 12, e127. [CrossRef] [PubMed]
6. Li, Q.; Zhou, L.; Zhou, M.; Chen, Z.; Li, F.; Wu, H.; Xiang, N.; Chen, E.; Tang, F.; Wang, D.; et al. Epidemiology of human infections with avian influenza A (H7N9) virus in china. N. Engl. J. Med. 2014, 370, 520-532. [CrossRef] [PubMed]
7. Roos, R. Experts offer dim view of potential vaccine response to H7N9. Regents of the University of Minnesota 2013 May. Available online: http://www.cidrap.umn.edu/news-perspective/2013/05/ experts-offer-dim-view-potential-vaccine-response-h7n9 (accessed on 5 May 2013).
8. Kalthoff, D.; Bogs, J.; Grund, C.; Tauscher, K.; Teifke, J.P.; Starick, E.; Harder, T.; Beer, M. Avian influenza h7n9/13 and h7n7/13: A comparative virulence study in chickens, pigeons, and ferrets. J. Virol. 2014, 88, 9153-9165. [CrossRef] [PubMed]
9. De Groot, A.S.; Ardito, M.; Terry, F.; Levitz, L.; Ross, T.; Moise, L.; Martin, W. Low immunogenicity predicted for emerging avian-origin H7N9: Implication for influenza vaccine design. Hum. Vaccines Immunother. 2013, 9, 950-956.
10. Behzadian, F.; Goodarzi, Z.; Fotouhi, F.; Saberfar, E. Baculoviral co-expression of HA, NA and M1 proteins of highly pathogenic H5N1 influenza virus in insect cells. Jundishapur J. Microbiol. 2013, 6, e7665. [CrossRef]
11. He, F.; Madhan, S.; Kwang, J. Baculovirus vector as a delivery vehicle for influenza vaccines. Expert Rev. Vaccines 2009, 8, 455-467. [CrossRef] [PubMed]
12. Lopez-Macias, C. Virus-like particle (vlp)-based vaccines for pandemic influenza: Performance of a vlp vaccine during the 2009 influenza pandemic. Hum.Vaccines Immunother. 2012, 8, 411-414. [CrossRef] [PubMed]
13. Lee, D.H.; Bae, S.W.; Park, J.K.; Kwon, J.H.; Yuk, S.S.; Song, J.M.; Kang, S.M.; Kwon, Y.K.; Kim, H.Y.; Song, C.S. Virus-like particle vaccine protects against H3N2 canine influenza virus in dog. Vaccine 2013, 31, 3268-3273. [CrossRef] [PubMed]
14. Lin, S.C.; Lin, Y.F.; Chong, P.; Wu, S.C. Broader neutralizing antibodies against H5N1 viruses using prime-boost immunization of hyperglycosylated hemagglutinin DNA and virus-like particles. PLoS ONE 2012, 7, e39075. [CrossRef] [PubMed]
15. Lin, S.C.; Liu, W.C.; Lin, Y.F.; Huang, Y.H.; Liu, J.H.; Wu, S.C. Heterologous prime-boost immunization regimens using adenovirus vector and virus-like particles induce broadly neutralizing antibodies against H5N1 avian influenza viruses. Biotechnol. J. 2013, 8, 1315-1322. [CrossRef] [PubMed]
16. Park, J.K.; Lee, D.H.; Youn, H.N.; Kim, M.S.; Lee, Y.N.; Yuk, S.S.; Lim, T.H.; Jang, J.H.; Kwon, J.H.; Kim, B.Y.; et al. Protective efficacy of crude virus-like particle vaccine against hpai H5N1 in chickens and its application on diva strategy. Influenza Other Respir. Viruses 2013, 7, 340-348. [CrossRef] [PubMed]
17. Lee, D.H.; Park, J.K.; Lee, Y.N.; Song, J.M.; Kang, S.M.; Lee, J.B.; Park, S.Y.; Choi, I.S.; Song, C.S. H9N2 avian influenza virus-like particle vaccine provides protective immunity and a strategy for the differentiation of infected from vaccinated animals. Vaccine 2011, 29, 4003-4007. [CrossRef] [PubMed]
18. Smith, G.E.; Flyer, D.C.; Raghunandan, R.; Liu, Y.; Wei, Z.; Wu, Y.; Kpamegan, E.; Courbron, D.; Fries, L.F., 3rd; Glenn, G.M. Development of influenza H7N9 virus like particle (vlp) vaccine: Homologous a/anhui/1/2013 (h7n9) protection and heterologous a/chicken/jalisco/cpa1/2012 (H7N3) cross-protection in vaccinated mice challenged with H7N9 virus. Vaccine 2013, 31, 4305-4313. [CrossRef] [PubMed]
19. Klausberger, M.; Wilde, M.; Palmberger, D.; Hai, R.; Albrecht, R.A.; Margine, I.; Hirsh, A.; Garcia-Sastre, A.; Grabherr, R.; Krammer, F. One-shot vaccination with an insect cell-derived low-dose influenza a h7 virus-like particle preparation protects mice against H7N9 challenge. Vaccine 2014, 32, 355-362. [CrossRef] [PubMed]
20. Bellone, S.; El-Sahwi, K.; Cocco, E.; Casagrande, F.; Cargnelutti, M.; Palmieri, M.; Bignotti, E.; Romani, C.; Silasi, D.A.; Azodi, M.; et al. Human papillomavirus type 16 (HPV-16) virus-like particle l1-specific cd8+ cytotoxic T lymphocytes (ctls) are equally effective as e7-specific cd8+ ctls in killing autologous HPV-16-positive tumor cells in cervical cancer patients: Implications for l1 dendritic cell-based therapeutic vaccines. J. Virol. 2009, 83, 6779-6789. [PubMed]
21. Huret, C.; Desjardins, D.; Miyalou, M.; Levacher, B.; Amadoudji Zin, M.; Bonduelle, O.; Combadiere, B.; Dalba, C.; Klatzmann, D.; Bellier, B. Recombinant retrovirus-derived virus-like particle-based vaccines induce hepatitis C virus-specific cellular and neutralizing immune responses in mice. Vaccine 2013, 31, 1540-1547. [CrossRef] [PubMed]
22. Quan, F.S.; Kim, Y.C.; Song, J.M.; Hwang, H.S.; Compans, R.W.; Prausnitz, M.R.; Kang, S.M. Long-term protective immunity from an influenza virus-like particle vaccine administered with a microneedle patch. Clin. Vaccine Immunol. 2013, 20, 1433-1439. [CrossRef] [PubMed]
23. Sistigu, A.; Bracci, L.; Valentini, M.; Proietti, E.; Bona, R.; Negri, D.R.; Ciccaglione, A.R.; Tritarelli, E.; Nisini, R.; Equestre, M.; et al. Strong cd8+ T cell antigenicity and immunogenicity of large foreign proteins incorporated in HIV-1 vlps able to induce a nef-dependent activation/maturation of dendritic cells. Vaccine 2011, 29, 3465-3475. [CrossRef] [PubMed]
24. Xu, J.; Guo, H.C.; Wei, Y.Q.; Dong, H.; Han, S.C.; Ao, D.; Sun, D.H.; Wang, H.M.; Cao, S.Z.; Sun, S.Q. Self-assembly of virus-like particles of canine parvovirus capsid protein expressed from Escherichia coli and application as virus-like particle vaccine. Appl. Microbiol. Biotechnol. 2014, 98, 3529-3538. [CrossRef] [PubMed]
25. Rodriguez-Limas, W.A.; Pastor, A.R.; Esquivel-Soto, E.; Esquivel-Guadarrama, F.; Ramirez, O.T.; Palomares, L.A. Immunogenicity and protective efficacy of yeast extracts containing rotavirus-like particles: A potential veterinary vaccine. Vaccine 2014, 32, 2794-2798. [CrossRef] [PubMed]
26. Cervera, L.; Gutierrez-Granados, S.; Martinez, M.; Blanco, J.; Godia, F.; Segura, M.M. Generation of HIV-1 gag vlps by transient transfection of hek 293 suspension cell cultures using an optimized animal-derived component free medium. J. Biotechnol. 2013, 166, 152-165. [CrossRef] [PubMed]
27. Wang, W.; Peng, H.; Tao, Q.; Zhao, X.; Tang, H.; Tang, Z.; Wang, Y.; Wang, Y.; Zhao, P.; Qi, Z. Serologic assay for avian-origin influenza A (H7N9) virus in adults of Shanghai, Guangzhou and Yunnan, china. J. Clin. Virol.: Off. Publ. Pan Am. Soc. Clin. Virol. 2014, 60, 305-308. [CrossRef] [PubMed]
28. Steinhauer, D.A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 1999, 258, 1-20. [CrossRef] [PubMed]
29. Air, G.M. Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc. Natl. Acad. Sci. USA 1981, 78, 7639-7643. [CrossRef] [PubMed]
30. Bright, R.A.; Carter, D.M.; Daniluk, S.; Toapanta, F.R.; Ahmad, A.; Gavrilov, V.; Massare, M.; Pushko, P.; Mytle, N.; Rowe, T.; et al. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007, 25, 3871-3878. [CrossRef] [PubMed]
31. Haredy, A.M.; Yamada, H.; Sakoda, Y.; Okamatsu, M.; Yamamoto, N.; Omasa, T.; Mori, Y.; Kida, H.; Okamoto, S.; Okuno, Y.; et al. Neuraminidase gene homology contributes to the protective activity of influenza vaccines prepared from the influenza virus library. J. Gen. Virol. 2014, 95, 2365-2371.
32. Kovacsovics-Bankowski, M.; Rock, K.L. Presentation of exogenous antigens by macrophages: Analysis of major histocompatibility complex class i and ii presentation and regulation by cytokines. Eur. J. Immunol. 1994, 24, 2421-2428. [PubMed]
33. Garcia-Sastre, A. Inhibition of interferon-mediated antiviral responses by influenza a viruses and other negative-strand RNA viruses. Virology 2001, 279, 375-384. [CrossRef] [PubMed]
34. Buonaguro, L.; Tornesello, M.L.; Tagliamonte, M.; Gallo, R.C.; Wang, L.X.; Kamin-Lewis, R.; Abdelwahab, S.; Lewis, G.K.; Buonaguro, F.M. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol. 2006, 80, 9134-9143. [CrossRef] [PubMed]
35. Ali, A.; Avalos, R.T.; Ponimaskin, E.; Nayak, D.P. Influenza virus assembly: Effect of influenza virus glycoproteins on the membrane association of M1 protein. J. Virol. 2000, 74, 8709-8719. [CrossRef] [PubMed]
36. Wu, C.Y.; Chang, C.Y.; Ma, H.H.; Wang, C.W.; Chen, Y.T.; Hsiao, P.W.; Chang, C.C.; Chan, C.H.; Liu, C.C.; Chen, J.R. Squalene-adjuvanted H7N9 virus vaccine induces robust humoral immune response against H7N9 and H7N7 viruses. Vaccine 2014, 32, 4485-4494. [CrossRef] [PubMed]
37. Quan, F.S.; Compans, R.W.; Cho, Y.K.; Kang, S.M. Ginseng and salviae herbs play a role as immune activators and modulate immune responses during influenza virus infection. Vaccine 2007, 25, 272-282. [CrossRef] [PubMed]
38. World Health Organization. Serological detection of avian influenza A (H7N9) virus infections by turkey haemagglutination-inhibition assay. World Health Organization 2013 May. Available online: http://www.who.int/influenza/gisrs_laboratory/cnic_serological_diagnosis_hai_ a_h7n9. pdf (accessed on 15 May 2013).
39. World Health Organization. Serological detection of avian influenza A (H7N9) infections by microneutralization assay. World Health Organization 2013 May. Available online: http:// www.who.int/influenza/gisrs_laboratory/cnic_serological_diagnosis_microneutralization_a_ h7n9. pdf (accessed on 1 December 2013).