Neuraminidase gene homology contributes to the protective activity of influenza vaccines prepared from the influenza virus library

Journal of General Virology

Volumn 95, Issue , 2014, Pages 2365-2371

  Haredy, Ahmad M ^a,b,c   Yamada, Hiroshi ^a   Sakoda, Yoshihiro ^d   Okamatsu, Masatoshi ^d   Yamamoto, Naoki ^d   Omasa, Takeshi ^b,e   Mori, Yasuko ^a,f   Kida, Hiroshi ^d,g   Okamoto, Shigefumi ^a,h   Okuno, Yoshinobu ^c   Yamanishi, Koichi ^a,c  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c Osaka University   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKUSHIMA   (Japan)

^f KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g HOKKAIDO UNIVERSITY   (Japan)

^h KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS SIALIDASE; SIALIDASE; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC HETEROGENEITY; GENETIC REASSORTMENT; INFLUENZA A (H3N2); INFLUENZA VACCINATION; INFLUENZA VIRUS A; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H3N4; INFLUENZA VIRUS A H3N5; INFLUENZA VIRUS A H3N7; LIMIT OF DETECTION; MOLECULAR LIBRARY; MOUSE; NONHUMAN; SEQUENCE HOMOLOGY; SURVIVAL RATE; VIRAL CLEARANCE; VIRUS STRAIN; ANIMAL; BAGG ALBINO MOUSE; BLOOD; ENZYMOLOGY; GENE LIBRARY; GENETICS; IMMUNOLOGY; ORTHOMYXOVIRIDAE INFECTIONS; VIROLOGY; VIRUS GENE;

ANIMALS; ANTIBODIES, VIRAL; FEMALE; GENE LIBRARY; GENES, VIRAL; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; REASSORTANT VIRUSES; VIRAL ENVELOPE PROTEINS;

EID: 84908277930     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.067488-0     Document Type: Article

References (40)

1. Avellaneda, G., Sylte, M. J., Lee, C. W. & Suarez, D. L. (2010). A heterologous neuraminidase subtype strategy for the differentiation of infected and vaccinated animals (DIVA) for avian influenza virus using an alternative neuraminidase inhibition test. Avian Dis 54 (Suppl), 272–277.
2. Beato, M. S., Rigoni, M., Milani, A. & Capua, I. (2007). Generation of avian influenza reassortant viruses of the H7N5 subtype as potential vaccine candidates to be used in the framework of a ‘‘DIVA’’ vaccination strategy. Avian Dis 51 (Suppl), 479–480.
3. Black, S., Nicolay U, Vesikari, T., Knuf, M, DelGiudice, G., DellaCioppa, G., Tsai, T., Clemens, R. & Rappuoli, R. (2011). Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children. Pediatr Infect Dis J 30, 1081–1085.
4. Capua, I., Terregino, C., Cattoli, G., Mutinelli, F. & Rodriguez, J. F. (2003). Development of a DIVA (Differentiating Infected from Vaccinated Animals) strategy using a vaccine containing a heterologous neuraminidase for the control of avian influenza. Avian Pathol 32, 47–55.
5. Cottey, R., Rowe, C. A. & Bender, B. S. (2001). Influenza virus. Curr Protoc Immunol 42, 19.11.1–19.11.32.
6. Couch, R. B., Atmar, R. L., Franco, L. M., Quarles, J. M., Wells, J., Arden, N., Niño, D. & Belmont, J. W. (2013). Antibody correlates and predictors of immunity to naturally occurring influenza in humans and the importance of antibody to the neuraminidase. J Infect Dis 207, 974–981.
7. Coudeville, L., Bailleux, F., Riche, B., Megas, F., Andre, P. & Ecochard, R. (2010). Relationship between haemagglutinationinhibiting antibody titres and clinical protection against influenza: development and application of a bayesian random-effects model. BMC Med Res Methodol 10, 18.
8. Cox, N. J. & Subbarao, K. (1999). Influenza. Lancet 354, 1277–1282.
9. Cox, M. M., Patriarca, P. A. & Treanor, J. (2008). FluBlok, a recombinant hemagglutinin influenza vaccine. Influenza Other Respi Viruses 2, 211–219.
10. FDA CBER (2007). Guidance for Industry: Clinical Data Needed to Support the Licensure of Seasonal Inactivated Influenza Vaccines. Rockville, MD: US DHHS.
11. Fritz, R., Sabarth, N., Kiermayr, S., Hohenadl, C., Howard, M. K., Ilk, R., Kistner, O., Ehrlich, H. J., Barrett, P. N. & Kreil, T. R. (2012). A Vero cell-derived whole-virus H5N1 vaccine effectively induces neuraminidase- inhibiting antibodies. J Infect Dis 205, 28–34.
12. Gamblin, S. J. & Skehel, J. J. (2010). Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem285, 28403–28409.
13. Haredy, A. M., Takenaka, N., Yamada, H., Sakoda, Y., Okamatsu, M., Yamamoto, N., Omasa, T., Ohtake, H., Mori, Y. & other authors (2013). An MDCK cell culture-derived formalin-inactivated influenza virus whole-virion vaccine from an influenza virus library confers cross-protective immunity by intranasal administration in mice. Clin Vaccine Immunol 20, 998–1007.
14. Isoda, N., Sakoda, Y., Kishida, N., Soda, K., Sakabe, S., Sakamoto, R., Imamura, T., Sakaguchi, M., Sasaki, T. & other authors (2008). Potency of an inactivated avian influenza vaccine prepared from a non-pathogenic H5N1 reassortant virus generated between isolates from migratory ducks in Asia. Arch Virol 153, 1685–1692.
15. Itoh, Y., Ozaki, H., Tsuchiya, H., Okamoto, K., Torii, R., Sakoda, Y., Kawaoka, Y., Ogasawara, K. & Kida, H. (2008). A vaccine prepared from a non-pathogenic H5N1 avian influenza virus strain confers protective immunity against highly pathogenic avian influenza virus infection in cynomolgus macaques. Vaccine 26, 562–572.
16. Johansson, B. E. & Cox, M. M. (2011). Influenza viral neuraminidase: the forgotten antigen. Expert Rev Vaccines 10, 1683–1695.
17. Johansson, B. E., Moran, T. M., Bona, C. A. & Kilbourne, E. D. (1987). Immunologic response to influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. III. Reduced generation of neuraminidase-specific helper T cells in hemagglutinin-primed mice. J Immunol 139, 2015–2019.
18. Kendal, A. P., Bozeman, F. M. & Ennis, F. A. (1980). Further studies of the neuraminidase content of inactivated influenza vaccines and the neuraminidase antibody responses after vaccination of immunologically primed and unprimed populations. Infect Immun 29, 966–971.
19. Kida, H. & Sakoda, Y. (2006). Library of influenza virus strains for vaccine and diagnostic use against highly pathogenic avian influenza and human pandemics. Dev Biol (Basel) 124, 69–72.
20. Kida, H., Webster, R. G. & Yanagawa, R. (1983). Inhibition of virusinduced hemolysis with monoclonal antibodies to different antigenic areas on the hemagglutinin molecule of A/seal/Massachusetts/1/80 (H7N7) influenza virus. Arch Virol 76, 91–99.
21. Kilbourne, E. D. (2006a). Influenza immunity: new insights from old studies. J Infect Dis 193, 7–8.
22. Kilbourne, E. D. (2006b). Influenza pandemics of the 20th century. Emerg Infect Dis 12, 9–14.
23. Kilbourne, E. D., Cerini, C. P., Khan, M. W., Mitchell, J. W., Jr & Ogra, P. L. (1987). Immunologic response to the influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. I. Studies in human vaccinees. J Immunol 138, 3010–3013.
24. Kilbourne, E. D., Couch, R. B., Kasel, J. A., Keitel, W. A., Cate, T. R., Quarles, J. H., Grajower, B., Pokorny, B. A. & Johansson, B. E. (1995). Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans. Vaccine 13, 1799–1803.
25. Luytjes, W., Enouf, V., Schipper, M., Gijzen, K., Liu, W. M., van der Lubben, M., Meijer, A., van der Werf, S. & Soethout, E. C. (2012). HI responses induced by seasonal influenza vaccination are associated with clinical protection and with seroprotection against nonhomologous strains. Vaccine 30, 5262–5269.
26. Peeters, B., de Boer, S. M., Tjeerdsma, G., Moormann, R. & Koch, G. (2012). New DIVA vaccine for the protection of poultry against H5 highly pathogenic avian influenza viruses irrespective of the Nsubtype. Vaccine 30, 7078–7083.
27. Rockman, S., Brown, L. E., Barr, I. G., Gilbertson, B., Lowther, S., Kachurin, A., Kachurina, O., Klippel, J., Bodle, J. & other authors (2013). Neuraminidase-inhibiting antibody is a correlate of crossprotection against lethal H5N1 influenza virus in ferrets immunized with seasonal influenza vaccine. J Virol 87, 3053–3061.
28. Samad, R. A., Nomura, N., Tsuda, Y., Manzoor, R., Kajihara, M., Tomabechi, D., Sasaki, T., Kokumai, N., Ohgitani, T. & other authors (2011). A vaccine prepared from a non-pathogenic H5N1 influenza virus strain from the influenza virus library conferred protective immunity to chickens against the challenge with antigenically drifted highly pathogenic avian influenza virus. Jpn J Vet Res 59, 23–29.
29. Sandbulte, M. R., Jimenez, G. S., Boon, A. C., Smith, L. R., Treanor, J. J. & Webby, R. J. (2007). Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med 4, e59.
30. Seto, J. T. & Rott, R. (1966). Functional significance of sialidose during influenza virus multiplication. Virology 30, 731–737.
31. Soda, K., Ozaki, H., Sakoda, Y., Isoda, N., Haraguchi, Y., Sakabe, S., Kuboki, N., Kishida, N., Takada, A. & Kida, H. (2008a). Antigenic and genetic analysis of H5 influenza viruses isolated from water birds for the purpose of vaccine use. Arch Virol 153, 2041–2048.
32. Soda, K., Sakoda, Y., Isoda, N., Kajihara, M., Haraguchi, Y., Shibuya, H., Yoshida, H., Sasaki, T., Sakamoto, R. & other authors (2008b). Development of vaccine strains of H5 and H7 influenza viruses. Jpn J Vet Res 55, 93–98.
33. Tamura, S., Hasegawa, H. & Kurata, T. (2010). Estimation of the effective doses of nasal-inactivated influenza vaccine in humans from mouse-model experiments. Jpn J Infect Dis 63, 8–15.
34. The European Agency for the Evaluation of Medicinal Products Committee for Proprietary Medicinal Products (1997). Note for Guidance on Harmonization of Requirements for Influenza Vaccines. CPMP/BWP/214/96. London: European Medicines Agency.
35. Valette, M. & Aymard, M. (2002). Quality control assessment of influenza and RSV testing in Europe: 2000–01 season. Euro Surveill 7, 161–165.
36. Wang, L., Qin, Z., Pantin-Jackwood, M., Faulkner, O., Suarez, D. L., Garcia, M., Lupiani, B., Reddy, S. M., Saif, Y. M. & Lee, C. W. (2011). Development of DIVA (differentiation of infected from vaccinated animals) vaccines utilizing heterologous NA and NS1 protein strategies for the control of triple reassortant H3N2 influenza in turkeys. Vaccine 29, 7966–7974.
37. Webster, R. G. & Laver, W. G. (1967). Preparation and properties of antibody directed specifically against the neuraminidase of influenza virus. J Immunol 99, 49–55.
38. Wood, J. M. & Levandowski, R. A. (2003). The influenza vaccine licensing process. Vaccine 21, 1786–1788.
39. Yamada, H., Moriishi, E., Haredy, A. M., Takenaka, N., Mori, Y., Yamanishi, K. & Okamoto, S. (2012). Influenza virus neuraminidase contributes to the dextran sulfate-dependent suppressive replication of some influenza A virus strains. Antiviral Res 96, 344–352.
40. Yoden, S., Kida, H., Kuwabara, M., Yanagawa, R. & Webster, R. G. (1986). Spin-labeling of influenza virus hemagglutinin permits analysis of the conformational change at low pH and its inhibition by antibody. Virus Res 4, 251–261.