One-shot vaccination with an insect cell-derived low-dose influenza A H7 virus-like particle preparation protects mice against H7N9 challenge

Vaccine

Volumn 32, Issue 3, 2014, Pages 355-362

  Klausberger, Miriam ^a   Wilde, Monika ^a   Palmberger, Dieter ^a   Hai, Rong ^b   Albrecht, Randy A ^b   Margine, Irina ^b   Hirsh, Ariana ^b   García Sastre, Adolfo ^b   Grabherr, Reingard ^a   Krammer, Florian ^b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Baculovirus; Cross reactivity; H7N9; Influenza; Pandemic; Virus like particle

Indexed keywords

H7 VIRUS LIKE PARTICLE VACCINE; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; MATRIX PROTEIN; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS LIKE PARTICLE VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DRUG EFFICACY; FEMALE; HEMAGGLUTINATION INHIBITION; INFECTION PREVENTION; INFLUENZA A; INFLUENZA A (H7N9); INFLUENZA VACCINATION; INFLUENZA VIRUS A H7N9; INSECT CELL; LD 50; LOW DRUG DOSE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; VIRUS STRAIN;

BACULOVIRUS; CROSS-REACTIVITY; H7N9; INFLUENZA; PANDEMIC; VIRUS-LIKE PARTICLE;

ANIMALS; ANTIBODIES, VIRAL; CROSS REACTIONS; DISEASE MODELS, ANIMAL; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; SF9 CELLS; SPODOPTERA; SURVIVAL ANALYSIS; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE; VIRAL MATRIX PROTEINS;

EID: 84891014819     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.11.036     Document Type: Article

References (47)

1. WHO. Human infection with influenza A (H7N9) virus in China. WHO; n.d.
2. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 2013, 368:1888-1897.
3. WHO. Human infection with avian influenza A (H7N9) virus - update. WHO; n.d.
4. Liu D., Shi W., Shi Y., Wang D., Xiao H., Li W., et al. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 2013, 381:1926-1932.
5. National Health and Family Planning Commission. Diagnosis and treatment guideline for human infection with influenza A (H7N9) virus, 2nd ed. Beijing NPFPC, 2013; n.d. Available from http://www.moh.gov.cn/mohgjhzs/s7952/201304/98ceede1daf74a45b1105f18c4e23ece.shtm.
6. Liu X., Li T., Zheng Y., Wong K.-W., Lu S., Lu H. Poor responses to oseltamivir treatment in a patient with influenza A (H7N9) virus infection. Emerg Microbes Infect 2013, 2:e27.
7. Hu Y., Lu S., Song Z., Wang W., Hao P., Li J., et al. Association between adverse clinical outcome in human disease caused by novel influenza A H7N9 virus and sustained viral shedding and emergence of antiviral resistance. Lancet 2013, 381:2273-2279.
8. De Wit E., Munster V.J., Spronken M.I.J., Bestebroer T.M., Baas C., Beyer W.E.P., et al. Protection of mice against lethal infection with highly pathogenic H7N7 influenza A virus by using a recombinant low-pathogenicity vaccine strain. J Virol 2005, 79:12401-12407.
9. Whiteley A., Major D., Legastelois I., Campitelli L., Donatelli I., Thompson C.I., et al. Generation of candidate human influenza vaccine strains in cell culture - rehearsing the European response to an H7N1 pandemic threat. Influenza Other Respir Viruses 2007, 1:157-166.
10. Pappas C., Matsuoka Y., Swayne D.E., Donis R.O. Development and evaluation of an influenza virus subtype H7N2 vaccine candidate for pandemic preparedness. Clin Vaccine Immunol 2007, 14:1425-1432.
11. Jadhao S.J., Achenbach J., Swayne D.E., Donis R., Cox N., Matsuoka Y. Development of Eurasian H7N7/PR8 high growth reassortant virus for clinical evaluation as an inactivated pandemic influenza vaccine. Vaccine 2008, 26:1742-1750.
12. Talaat K.R., Karron R.A., Callahan K.A., Luke C.J., DiLorenzo S.C., Chen G.L., et al. A live attenuated H7N3 influenza virus vaccine is well tolerated and immunogenic in a Phase I trial in healthy adults. Vaccine 2009, 27:3744-3753.
13. Goff P.H., Krammer F., Hai R., Seibert C.W., Margine I., García-Sastre A., et al. Induction of cross-reactive antibodies to novel H7N9 influenza virus by recombinant Newcastle disease virus expressing a North American lineage H7 subtype hemagglutinin. J Virol 2013, 87:8235-8240.
14. Smith G.E., Flyer D.C., Raghunandan R., Liu Y., Wei Z., Wu Y. 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(40):4305-4313. Epub 2013 Jul 26. 10.1016/j.vaccine.2013.07.043.
15. Abe T., Takahashi H., Hamazaki H., Miyano-Kurosaki N., Matsuura Y., Takaku H. Baculovirus induces an innate immune response and confers protection from lethal influenza virus infection in mice. J Immunol (Baltim., MD) 2003, 171:1133-1139. 1950.
16. Margine I., Martinez-Gil L., Chou Y.-Y., Krammer F. Residual baculovirus in insect cell-derived influenza virus-like particle preparations enhances immunogenicity. PLoS ONE 2012, 7:e51559.
17. Krammer F., Schinko T., Palmberger D., Tauer C., Messner P., Grabherr R. Trichoplusia ni cells (High Five) are highly efficient for the production of influenza A virus-like particles: a comparison of two insect cell lines as production platforms for influenza vaccines. Mol Biotechnol 2010, 45:226-234.
18. Palmberger D., Wilson I.B.H., Berger I., Grabherr R., Rendic D. SweetBac:. A new approach for the production of mammalianised glycoproteins in insect cells. PLoS One 2012, 7(4):e34226. Epub 2012 Apr 2. 10.1371/journal.pone.0034226.
19. Fodor E., Devenish L., Engelhardt O.G., Palese P., Brownlee G.G., García-Sastre A. Rescue of influenza A virus from recombinant DNA. J Virol 1999, 73:9679-9682.
20. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Gao P., et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci USA 1999, 96:9345-9350.
21. Hai R., Krammer F., Tan G.S., Pica N., Eggink D., Maamary J., et al. Influenza viruses expressing chimeric hemagglutinins: globular head and stalk domains derived from different subtypes. J Virol 2012, 86:5774-5781.
22. Krammer F., Pica N., Hai R., Margine I., Palese P. Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. J Virol 2013, 87:6542-6550.
23. Krammer F., Margine I., Tan G.S., Pica N., Krause J.C., Palese P. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS ONE 2012, 7:e43603.
24. Bac-to-Bac Baculovirus Expression System, User Manual, Version F as of 04 September 2010; n.d. Available from http://tools.lifetechnologies.com/content/sfs/manuals/bactobac_man.pdf.
25. Salem M.L., Hossain M.S. In vivo acute depletion of CD8(+) T cells before murine cytomegalovirus infection upregulated innate antiviral activity of natural killer cells. Int J Immunopharmacol 2000, 22:707-718.
26. Hemann E.A., Kang S.-M., Legge K.L. Protective CD8T cell-mediated immunityagainst influenza A virus infection following influenza virus-like particle vac-cination. J Immunol 2013, 191(5):2486-2494. Epub 2013 Jul 24. 10.4049/jimmunol.1300954.
27. Hillaire M.L.B., Osterhaus A.D.M.E., Rimmelzwaan G.F. Induction of virus-specific cytotoxic T lymphocytes as a basis for the development of broadly protective influenza vaccines. J Biomed Biotechnol 2011, 2011:939860.
28. Joseph T., McAuliffe J., Lu B., Jin H., Kemble G., Subbarao K. Evaluation of replication and pathogenicity of avian influenza A H7 subtype viruses in a mouse model. J Virol 2007, 81:10558-10566.
29. Osterholm M.T., Ballering K.S., Kelley N.S. Major challenges in providing an effective and timely pandemic vaccine for influenza A (H7N9). J Am Med Assoc 2013, 309:2557-2558.
30. Cowling B.J., Jin L., Lau E.H., Liao Q., Wu P., Jiang H., et al. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet 2013, 382:129-137.
31. Chang G.R.-L., Lai S.-Y., Chang P.-C., Wang M.-Y. Production of immunogenic one-component avian H7-subtype influenza virus-like particles. Process Biochem 2011, 46:1292-1298.
32. Joseph T., McAuliffe J., Lu B., Vogel L., Swayne D., Jin H., et al. A live attenuated cold-adapted influenza A H7N3 virus vaccine provides protection against homologous and heterologous H7 viruses in mice and ferrets. Virology 2008, 378:123-132.
33. WHO. Clinical evaluation of influenza vaccines. WHO; n.d.
34. Cox R.J., Madhun A.S., Hauge S., Sjursen H., Major D., Kuhne M., et al. A phase I clinical trial of a PER.C6 cell grown influenza H7 virus vaccine. Vaccine 2009, 27:1889-1897.
35. Couch R.B., Patel S.M., Wade-Bowers C.L., Niño D. A randomized clinical trial of an inactivated avian influenza A (H7N7) vaccine. PLoS ONE 2012, 7:e49704.
36. Partridge J., Kieny M.P. Global production capacity of seasonal influenza vaccine in 2011. Vaccine 2013, 31:728-731.
37. Report of the second WHO Consultation on the Global Action Plan for Influenza Vaccines (GAP), Geneva, Switzerland, 12-14 July 2011; n.d. Availble from http://whqlibdoc.who.int/publications/2012/9789241564410_eng.pdf.
38. Sun J., Braciale T.J. Role of T cell immunity in recovery from influenza virusinfection. Curr Opin Virol 2013, 3(4):425-429. Epub 2013 May 27. 10.1016/j.coviro.2013.05.001.
39. Bender B.S., Croghan T., Zhang L., Small P.A. Transgenic mice lacking class I major histocompatibility complex-restricted T cells have delayed viral clearance and increased mortality after influenza virus challenge. J Exp Med 1992, 175:1143-1145.
40. Gerhard W. The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 2001, 260:171-190.
41. Cubas R., Zhang S., Kwon S., Sevick-Muraca E.M., Li M., Chen C., et al. Virus-like particle (VLP) lymphatic trafficking and immune response generation after immunization by different routes. J Immunother (Hagerstown, MD) 2009, 32:118-128.
42. Muramatsu M., Yoshida R., Miyamoto H., Tomabechi D., Kajihara M., Maruyama J., et al. Heterosubtypic antiviral activity of hemagglutinin-specific antibodies induced by intranasal immunization with inactivated influenza viruses in mice. PLoS ONE 2013, 8:e71534.
43. Margine I., Krammer F., Hai R., Heaton N.S., Tan G.S., Andrews S.A., et al. Hemagglu-tinin stalk-based universal vaccine constructs protect against group 2 influenzaA viruses. J Virol 2013, 87(19):10435-10446. Epub 2013 Jul 31. 10.1128/JVI.01715-13.
44. Abbas M.A., Spackman E., Fouchier R., Smith D., Ahmed Z., Siddique N., et al. H7 avian influenza virus vaccines protect chickens against challenge with antigenically diverse isolates. Vaccine 2011, 29:7424-7429.
45. He F., Madhan S., Kwang J. Baculovirus vector as a delivery vehicle for influenza vaccines. Expert Rev Vaccines 2009, 8:455-467.
46. Song J.-M., Choi C.-W., Kwon S.-O., Compans R.W., Kang S.-M., Kim S.I. Proteomic characterization of influenza H5N1 virus-like particles and their protective immunogenicity. J Proteome Res 2011, 10:3450-3459.
47. Thompson C.M., Petiot E., Lennaertz A., Henry O., Kamen A.A. Analytical technologies for influenza virus-like particle candidate vaccines: challenges and emerging approaches. Virol J 2013, 10:141.