Sequential immunization with consensus influenza hemagglutinins raises cross-reactive neutralizing antibodies against various heterologous HA strains

Vaccine

Volumn 35, Issue 2, 2017, Pages 305-312

  Zhou, Hui ^a,b   Huang, Yang ^c   Yuan, Songhua ^d   Li, Yuanyuan ^a   Wu, Shuyan ^a   Xu, Jianqing ^d   Huang, Rui ^a  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^c VacDiagn Biotechnology ^*  (China)

^d FUDAN UNIVERSITY   (China)

Author keywords

Influenza virus; Neutralizing antibody; Sequential immunization; Vaccine

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA A VIRUS (H1N1); MDCK CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS NEUTRALIZATION; VIRUS STRAIN; ANIMAL; BAGG ALBINO MOUSE; BLOOD; HETEROLOGOUS IMMUNITY; IMMUNOLOGY; INFLUENZA A VIRUS; PROCEDURES; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNITY, HETEROLOGOUS; IMMUNIZATION; INFLUENZA A VIRUS; MICE, INBRED BALB C; TREATMENT OUTCOME;

EID: 85007018617     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.11.051     Document Type: Article

References (33)

1. [1] Thompson, W.W., Comanor, L., Shay, D.K., Epidemiology of seasonal influenza: use of surveillance data and statistical models to estimate the burden of disease. J Infect Dis 194:Suppl 2 (2006), S82–S91.
2. [2] Pica, N., Hai, R., Krammer, F., Wang, T.T., Maamary, J., Eggink, D., et al. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc Natl Acad Sci USA 109 (2012), 2573–2578.
3. [3] Subbarao, K., Klimov, A., Katz, J., Regnery, H., Lim, W., Hall, H., et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279 (1998), 393–396.
4. [4] Garten, R.J., Davis, C.T., Russell, C.A., Shu, B., Lindstrom, S., Balish, A., et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325 (2009), 197–201.
5. [5] Smith, G.J., Vijaykrishna, D., Bahl, J., Lycett, S.J., Worobey, M., Pybus, O.G., et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459 (2009), 1122–1125.
6. [6] 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 368 (2013), 1888–1897.
7. + memory B cells. PLoS ONE, 3, 2008, e3942.
8. [8] Corti, D., Voss, J., Gamblin, S.J., Codoni, G., Macagno, A., Jarrossay, D., et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333 (2011), 850–856.
9. [9] Wang, T.T., Tan, G.S., Hai, R., Pica, N., Petersen, E., Moran, T.M., et al. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog, 6, 2010, e1000796.
10. [10] Tan, G.S., Lee, P.S., Hoffman, R.M., Mazel-Sanchez, B., Krammer, F., Leon, P.E., et al. Characterization of a broadly neutralizing monoclonal antibody that targets the fusion domain of group 2 influenza A virus hemagglutinin. J Virol 88 (2014), 13580–13592.
11. [11] Tan, G.S., Krammer, F., Eggink, D., Kongchanagul, A., Moran, T.M., Palese, P., A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J Virol 86 (2012), 6179–6188.
12. [12] Qiu, C., Huang, Y., Wang, Q., Tian, D., Zhang, W., Hu, Y., et al. Boosting heterosubtypic neutralization antibodies in recipients of 2009 pandemic H1N1 influenza vaccine. Clin Infect Dis 54 (2012), 17–24.
13. [13] Craigo, J.K., Ezzelarab, C., Cook, S.J., Liu, C., Horohov, D., Issel, C.J., et al. Protective efficacy of centralized and polyvalent envelope immunogens in an attenuated equine lentivirus vaccine. PLoS Pathog, 11, 2015, e1004610.
14. [14] Yang, O.O., Ali, A., Kasahara, N., Faure-Kumar, E., Bae, J.Y., Picker, L.J., et al. Short conserved sequences of HIV-1 are highly immunogenic and shift immunodominance. J Virol 89 (2015), 1195–1204.
15. [15] Laddy, D.J., Yan, J., Corbitt, N., Kobasa, D., Kobinger, G.P., Weiner, D.B., Immunogenicity of novel consensus-based DNA vaccines against avian influenza. Vaccine 25 (2007), 2984–2989.
16. [16] Jones, F.R., Gabitzsch, E.S., Xu, Y., Balint, J.P., Borisevich, V., Smith, J., et al. Prevention of influenza virus shedding and protection from lethal H1N1 challenge using a consensus 2009 H1N1 HA and NA adenovirus vector vaccine. Vaccine 29 (2011), 7020–7026.
17. [17] Yan, J., Villarreal, D.O., Racine, T., Chu, J.S., Walters, J.N., Morrow, M.P., et al. Protective immunity to H7N9 influenza viruses elicited by synthetic DNA vaccine. Vaccine 32 (2014), 2833–2842.
18. [18] Qiu, C., Huang, Y., Zhang, A., Tian, D., Wan, Y., Zhang, X., et al. Safe pseudovirus-based assay for neutralization antibodies against influenza A(H7N9) virus. Emerg Infect Dis 19 (2013), 1685–1687.
19. [19] Deng, Y., Yewdell, J.W., Eisenlohr, L.C., Bennink, J.R., MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J Immunol 158 (1997), 1507–1515.
20. [20] Tamura, M., Kuwano, K., Kurane, I., Ennis, F.A., Definition of amino acid residues on the epitope responsible for recognition by influenza A virus H1-specific, H2-specific, and H1- and H2-cross-reactive murine cytotoxic T-lymphocyte clones. J Virol 72 (1998), 9404–9406.
21. + T cells for heterosubtypic protection. Proc Natl Acad Sci USA 111 (2014), 5676–5681.
22. [22] Manicassamy, B., Medina, R.A., Hai, R., Tsibane, T., Stertz, S., Nistal-Villan, E., et al. Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog, 6, 2010, e1000745.
23. [23] Li, G.M., Chiu, C., Wrammert, J., McCausland, M., Andrews, S.F., Zheng, N.Y., et al. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci USA 109 (2012), 9047–9052.
24. [24] Miller, M.S., Tsibane, T., Krammer, F., Hai, R., Rahmat, S., Basler, C.F., et al. 1976 and 2009 H1N1 influenza virus vaccines boost anti-hemagglutinin stalk antibodies in humans. J Infect Dis 207 (2013), 98–105.
25. [25] Thomson, C.A., Wang, Y., Jackson, L.M., Olson, M., Wang, W., Liavonchanka, A., et al. Pandemic H1N1 influenza infection and vaccination in humans induces cross-protective antibodies that target the hemagglutinin stem. Front Immunol, 3, 2012, 87.
26. [26] Xu, J., Ren, L., Huang, X., Qiu, C., Liu, Y., Liu, Y., et al. Sequential priming and boosting with heterologous HIV immunogens predominantly stimulated T cell immunity against conserved epitopes. AIDS 20 (2006), 2293–2303.
27. [27] Wei, C.J., Boyington, J.C., McTamney, P.M., Kong, W.P., Pearce, M.B., Xu, L., et al. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 329 (2010), 1060–1064.
28. [28] Kanekiyo, M., Wei, C.J., Yassine, H.M., McTamney, P.M., Boyington, J.C., Whittle, J.R., et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499 (2013), 102–106.
29. [29] Sagawa, H., Ohshima, A., Kato, I., Okuno, Y., Isegawa, Y., The immunological activity of a deletion mutant of influenza virus haemagglutinin lacking the globular region. J Gen Virol 77:Pt 7 (1996), 1483–1487.
30. [30] Steel, J., Lowen, A.C., Wang, T.T., Yondola, M., Gao, Q., Haye, K., et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio, 2010, 1.
31. [31] Krammer, F., Palese, P., Steel, J., Advances in universal influenza virus vaccine design and antibody mediated therapies based on conserved regions of the hemagglutinin. Curr Top Microbiol Immunol 386 (2015), 301–321.
32. [32] Wohlbold, T.J., Nachbagauer, R., Margine, I., Tan, G.S., Hirsh, A., Krammer, F., Vaccination with soluble headless hemagglutinin protects mice from challenge with divergent influenza viruses. Vaccine 33 (2015), 3314–3321.
33. [33] Crevar, C.J., Carter, D.M., Lee, K.Y., Ross, T.M., Cocktail of H5N1 COBRA HA vaccines elicit protective antibodies against H5N1 viruses from multiple clades. Hum Vaccin Immunother 11 (2015), 572–583.