Intranasal vaccination with H5, H7 and H9 hemagglutinins co-localized in a virus-like particle protects ferrets from multiple avian influenza viruses

Virology

Volumn 442, Issue 1, 2013, Pages 67-73

  Tretyakova, Irina ^a   Pearce, Melissa B ^b   Florese, Ruth ^a   Tumpey, Terrence M ^b   Pushko, Peter ^a  

^a Medigen Inc   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

Avian influenza; Influenza; Trivalent; Vaccine; Virus like particle; VLP

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; MATRIX PROTEIN; VIRUS LIKE PARTICLE VACCINE; VIRUS SIALIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; AVIAN INFLUENZA; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H7N2; INFLUENZA VIRUS A H9N2; MALE; MATRIX GENE; NONHUMAN; PRIORITY JOURNAL; VIRUS GENE; VIRUS HEMAGGLUTINATION; VIRUS SIALIDASE GENE; VIRUS STRAIN;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, VIRAL; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H7N2 SUBTYPE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA VACCINES; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINANT PROTEINS; VACCINATION; VIRION;

AVES; AVIAN INFLUENZA VIRUS; MUSTELA; ORTHOMYXOVIRIDAE;

EID: 84878933189     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.03.027     Document Type: Article

References (51)

1. Belser J.A., Blixt O., Chen L.M., Pappas C., Maines T.R., Van Hoeven N., Donis R., Busch J., McBride R., Paulson J.C., Katz J.M., Tumpey T.M. Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:7558-7563.
2. Blanco J.C., Pletneva L.M., Wan H., Araya Y., Angel M., Oue R.O., Sutton T.C., Perez D.R. Receptor characterization and susceptibility of cotton rats to avian and 2009 pandemic influenza virus strains. J. Virol. 2013, 87:2036-2045.
3. Boulay F., Doms R.W., Webster R.G., Helenius A. Posttranslational oligomerization and cooperative acid activation of mixed influenza hemagglutinin trimers. J. Cell Biol. 1988, 106:629-639.
4. Chao C.C. A single amino acid deletion at the amino terminus of influenza virus hemagglutinin causes malfolding and blocks exocytosis of the molecule in mammalian cells. J. Biol. Chem. 1992, 267:2142-2148.
5. Cheng, P.K.C.a.L., W.L. 2010. Molecular characterization of H9N2 isolated in Hong Kong from 2008 to 2009, Unpublished, Hong Kong, GenBank Acc. No. CY055137.
6. Cheng X., Eisenbraun M., Xu Q., Zhou H., Kulkarni D., Subbarao K., Kemble G., Jin H. H5N1 vaccine-specific B cell responses in ferrets primed with live attenuated seasonal influenza vaccines. PLoS One 2009, 4:e4436.
7. Couch R.B., Decker W.K., Utama B., Atmar R.L., Nino D., Feng J.Q., Halpert M.M., Air G.M. Evaluations for in vitro correlates of immunogenicity of inactivated influenza a h5, h7 and h9 vaccines in humans. PLoS One 2012, 7:e50830.
8. Denis J., Acosta-Ramirez E., Zhao Y., Hamelin M.E., Koukavica I., Baz M., Abed Y., Savard C., Pare C., Lopez Macias C., Boivin G., Leclerc D. Development of a universal influenza A vaccine based on the M2e peptide fused to the papaya mosaic virus (PapMV) vaccine platform. Vaccine 2008, 26:3395-3403.
9. Ebrahimi, S.M., Tebianian, M., Aghaiypour, K., Nili, H., Mirjalili, A., Prokaryotic expression and characterization of avian influenza A virus M2 gene as a candidate for universal recombinant vaccine against influenza A subtypes; specially H5N1 and H9N2. Mol. Biol. Rep. 37, 2909-2914.
10. Galarza J.M., Latham T., Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 2005, 18:244-251.
11. Huang S.S., Banner D., Fang Y., Ng D.C., Kanagasabai T., Kelvin D.J., Kelvin A.A. Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS One 2011, 6:e27512.
12. Hussain A.I., Cordeiro M., Sevilla E., Liu J. Comparison of egg and high yielding MDCK cell-derived live attenuated influenza virus for commercial production of trivalent influenza vaccine: in vitro cell susceptibility and influenza virus replication kinetics in permissive and semi-permissive cells. Vaccine 2010, 28:3848-3855.
13. Kang S.M., Pushko P., Bright R.A., Smith G., Compans R.W. Influenza virus-like particles as pandemic vaccines. Curr. Top. Microbiol. Immunol. 2009, 333:269-289.
14. Maines T.R., Lu X.H., Erb S.M., Edwards L., Guarner J., Greer P.W., Nguyen D.C., Szretter K.J., Chen L.M., Thawatsupha P., Chittaganpitch M., Waicharoen S., Nguyen D.T., Nguyen T., Nguyen H.H., Kim J.H., Hoang L.T., Kang C., Phuong L.S., Lim W., Zaki S., Donis R.O., Cox N.J., Katz J.M., Tumpey T.M. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 2005, 79:11788-11800.
15. Morens D.M., Fauci A.S. Emerging infectious diseases in 2012: 20 years after the institute of medicine report. mBio 2012, 3.
16. Mozdzanowska K., Furchner M., Washko G., Mozdzanowski J., Gerhard W. A pulmonary influenza virus infection in SCID mice can be cured by treatment with hemagglutinin-specific antibodies that display very low virus-neutralizing activity in vitro. J. Virol. 1997, 71:4347-4355.
17. Nguyen H.H., Moldoveanu Z., Novak M.J., van Ginkel F.W., Ban E., Kiyono H., McGhee J.R., Mestecky J. Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8(+) cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology 1999, 254:50-60.
18. O'Neill E., Donis R.O. Generation and characterization of candidate vaccine viruses for prepandemic influenza vaccines. Curr. Top. Microbiol. Immunol. 2009, 333:83-108.
19. Ostrowsky B., Huang A., Terry W., Anton D., Brunagel B., Traynor L., Abid S., Johnson G., Kacica M., Katz J., Edwards L., Lindstrom S., Klimov A., Uyeki T.M. Low pathogenic avian influenza A (H7N2) virus infection in immunocompromised adult, New York, USA, 2003. Emerg. Infect. Dis. 18 2012, 1128-1131.
20. Oxford J.S., Lambkin R., Elliot A., Daniels R., Sefton A., Gill D. Scientific lessons from the first influenza pandemic of the 20th century. Vaccine 2006, 24:6742-6746.
21. Palese P. Influenza: old and new threats. Nat. Med. 2004, 10:S82-87.
22. Palese P. Making better influenza virus vaccines?. Emerg. Infect. Dis. 12 2006, 61-65.
23. 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.
24. Perrone L.A., Ahmad A., Veguilla V., Lu X., Smith G., Katz J.M., Pushko P., Tumpey T.M. Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J. Virol. 2009, 83:5726-5734.
25. Pica N., Palese P. Toward a universal influenza virus vaccine: prospects and challenges. Annu. Rev. Med. 2013, 64:189-202.
26. Pillet S., Kobasa D., Meunier I., Gray M., Laddy D., Weiner D.B., von Messling V., Kobinger G.P. Cellular immune response in the presence of protective antibody levels correlates with protection against 1918 influenza in ferrets. Vaccine 2011, 29:6793-6801.
27. Plosker G.L. A/H5N1 prepandemic influenza vaccine (whole virion, vero cell-derived, inactivated) [Vepacel(R)]. Drugs 2012, 72:1543-1557.
28. Pushko P., Geisbert J., Parker M., Jahrling P., Smith J. Individual and bivalent vaccines based on alphavirus replicons protect guinea pigs against infection with Lassa and Ebola viruses. J. Virol. 2001, 75:11677-11685.
29. Pushko, P., Kort, T., Nathan, M., Pearce, M.B., Smith, G., Tumpey, T.M., Recombinant H1N1 virus-like particle vaccine elicits protective immunity in ferrets against the 2009 pandemic H1N1 influenza virus. Vaccine 28, 4771-4776.
30. Pushko P., Pearce M.B., Ahmad A., Tretyakova I., Smith G., Belser J.A., Tumpey T.M. Influenza virus-like particle can accommodate multiple subtypes of hemagglutinin and protect from multiple influenza types and subtypes. Vaccine 2011, 29:5911-5918.
31. Pushko P,R.B, Tumpey T., Smith G. Engineering better influenza vaccines: traditional and new approaches. Medicinal Protein Engineering 2009, 2009:169-204. CRC Press, Boca Raton.
32. Pushko P., Tumpey T.M., Bu F., Knell J., Robinson R., Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 2005, 23:5751-5759.
33. Quan, F.S., Vunnava, A., Compans, R.W., Kang, S.M., Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice. PLoS One 5, e9161.
34. Rao S.S., Kong W.P., Wei C.J., Van Hoeven N., Gorres J.P., Nason M., Andersen H., Tumpey T.M., Nabel G.J. Comparative efficacy of hemagglutinin, nucleoprotein, and matrix 2 protein gene-based vaccination against H5N1 influenza in mouse and ferret. PLoS One 2010, 5:e9812.
35. Rebmann T., Zelicoff A. Vaccination against influenza: role and limitations in pandemic intervention plans. Expert Rev. Vaccines 2012, 11:1009-1019.
36. Ross T.M., Mahmood K., Crevar C.J., Schneider-Ohrum K., Heaton P.M., Bright R.A. A trivalent virus-like particle vaccine elicits protective immune responses against seasonal influenza strains in mice and ferrets. PLoS One 2009, 4:e6032.
37. Schotsaert M., De Filette M., Fiers W., Saelens X. Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments. Expert Rev. Vaccines 2009, 8:499-508.
38. Stephenson I., Zambon M.C., Rudin A., Colegate A., Podda A., Bugarini R., Del Giudice G., Minutello A., Bonnington S., Holmgren J., Mills K.H., Nicholson K.G. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J. Virol. 2006, 80:4962-4970.
39. Taubenberger J.K., Baltimore D., Doherty P.C., Markel H., Morens D.M., Webster R.G., Wilson I.A. Reconstruction of the 1918 influenza virus: unexpected rewards from the past. mBio 2012, 3.
40. Treanor J.J., Campbell J.D., Zangwill K.M., Rowe T., Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N. Engl. J. Med. 2006, 354:1343-1351.
41. Treanor J.J., El Sahly H., King J., Graham I., Izikson R., Kohberger R., Patriarca P., Cox M. Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine (FluBlok(R)) against influenza in healthy adults: a randomized, placebo-controlled trial. Vaccine 2011, 29:7733-7739.
42. Tumpey T.M., Renshaw M., Clements J.D., Katz J.M. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J. Virol. 2001, 75:5141-5150.
43. Wan H., Sorrell E.M., Song H., Hossain M.J., Ramirez-Nieto G., Monne I., Stevens J., Cattoli G., Capua I., Chen L.M., Donis R.O., Busch J., Paulson J.C., Brockwell C., Webby R., Blanco J., Al-Natour M.Q., Perez D.R. Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 2008, 3:e2923.
44. Wang B.Z., Liu W., Kang S.M., Alam M., Huang C., Ye L., Sun Y., Li Y., Kothe D.L., Pushko P., Dokland T., Haynes B.F., Smith G., Hahn B.H., Compans R.W. Incorporation of high levels of chimeric human immunodeficiency virus envelope glycoproteins into virus-like particles. J. Virol. 2007, 81:10869-10878.
45. Wang T.T., Palese P. Universal epitopes of influenza virus hemagglutinins?. Nat. Struct. Mol. Biol. 2009, 16:233-234.
46. Wei C.J., Boyington J.C., McTamney P.M., Kong W.P., Pearce M.B., Xu L., Andersen H., Rao S., Tumpey T.M., Yang Z.Y., Nabel G.J. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science (New York, N.Y) 2010, 329:1060-1064.
47. WHO, 2012a. Antigenic and genetic characteristics of influenza A(H5N1) and influenza A(H9N2) viruses and candidate vaccine viruses developed for potential use in human vaccines.
48. WHO, 2012b. WHO Manual on Animal Influenza Diagnosis and Surveillance, WHO/CDS/CSR/NCS/2002.5 Rev. 1.
49. WHO, 2013. Antigenic and genetic characteristics of A(H5N1), A(H7N3), A(H9N2) and variant influenza viruses and candidate vaccine viruses developed for potential use in human vaccines.
50. Yen H.L., Webster R.G. Pandemic influenza as a current threat. Curr. Top. Microbiol. Immunol. 2009, 333:3-24.
51. Zeng H., Goldsmith C., Thawatsupha P., Chittaganpitch M., Waicharoen S., Zaki S., Tumpey T.M., Katz J.M. Highly pathogenic avian influenza H5N1 viruses elicit an attenuated type i interferon response in polarized human bronchial epithelial cells. J. Virol. 2007, 81:12439-12449.