A universal influenza virus vaccine candidate confers protection against pandemic H1N1 infection in preclinical ferret studies

npj Vaccines

Volumn 2, Issue 1, 2017, Pages

  Nachbagauer, Raffael ^a   Liu, Wen Chun ^a   Choi, Angela ^a   Wohlbold, Teddy John ^a   Atlas, Talia ^a   Rajendran, Madhusudan ^a   Solórzano, Alicia ^a   Berlanda Scorza, Francesco ^b   Garciá Sastre, Adolfo ^a   Palese, Peter ^a   Albrecht, Randy A ^a   Krammer, Florian ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b PATH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85041487503     PISSN: None     EISSN: 20590105     Source Type: Journal    
DOI: 10.1038/s41541-017-0026-4     Document Type: Article

References (49)

1. WHO. Influenza (Seasonal) Fact sheet 211. http://www.who.int/mediacentre/factsheets/fs211/en/.
2. Gerdil, C. The annual production cycle for influenza vaccine. Vaccine 21, 1776-1779 (2003).
3. Tricco, A. C., et al. Comparing influenza vaccine efficacy against mismatched and matched strains: A systematic review and meta-analysis. BMC Med. 11, 153 (2013).
4. Krammer, F., Palese, P. Advances in the development of influenza virus vaccines. Nat. Rev. Drug Discov. 14, 167-182 (2015).
5. Ekiert, D. C., Wilson, I. A. Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr. Opin. Virol. 2, 134-141 (2012).
6. Krammer, F., Palese, P. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr. Opin. Virol. 3, 521-530 (2013).
7. Wrammert, J., et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453, 667-671 (2008).
8. Moody, M. A., et al. H3N2 influenza infection elicits more cross-reactive and less clonally expanded anti-hemagglutinin antibodies than influenza vaccination. PLoS One 6, e25797 (2011).
9. Margine, I., et al. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J. Virol. 87, 4728-4737 (2013).
10. Ellebedy, A. H., et al. Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc. Natl. Acad. Sci. USA 111, 13133-13138 (2014).
11. Gerhard, W., Yewdell, J., Frankel, M. E., Webster, R. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290, 713-717 (1981).
12. Chen, C. J., et al. Influenza A viruses expressing intra-or intergroup chimeric hemagglutinins. J. Virol. 90, 3789-3793 (2016).
13. Krammer, F., Pica, N., Hai, R., Margine, I., Palese, P. Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. J. Virol. 87, 6542-6550 (2013).
14. Margine, I., et al. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza a viruses. J. Virol. 87, 10435-10446 (2013).
15. Nachbagauer, R., et al. Hemagglutinin stalk immunity reduces influenza virus replication and transmission in ferrets. J. Virol. 90, 3268-3273 (2015).
16. Krammer, F., et al. Assessment of influenza virus hemagglutinin stalk-based immunity in ferrets. J. Virol. 88, 3432-3442 (2014).
17. Nachbagauer, R., et al. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans. J. Virol. 88, 13260-13268 (2014).
18. Nachbagauer, R., et al. Age dependence and isotype specificity of influenza virus hemagglutinin stalk-reactive antibodies in humans. MBio, doi:10.1128/mBio.01996-15 (2016).
19. Babu, T. M., et al. Live attenuated H7N7 influenza vaccine primes for a vigorous antibody response to inactivated H7N7 influenza vaccine. Vaccine 32, 6798-6804 (2014).
20. Halliley, J. L., et al. High-affinity h7 head and stalk domain-specific antibody responses to an inactivated influenza H7N7 vaccine after priming with live attenuated influenza vaccine. J. Infect. Dis. 212, 1270-1278 (2015).
21. Talaat, K. R., et al. A live attenuated influenza A(H5N1) vaccine induces long-term immunity in the absence of a primary antibody response. J. Infect. Dis. 209, 1860-1869 (2014).
22. Ledgerwood, J. E., et al. DNA priming and influenza vaccine immunogenicity: Two phase 1 open label randomized clinical trials. Lancet Infect. Dis. 11, 916-924 (2011).
23. Ledgerwood, J. E., et al. Prime-boost interval matters: A randomized phase 1 study to identify the minimum interval necessary to observe the H5 DNA influenza vaccine priming effect. J. Infect. Dis. 208, 418-422 (2013).
24. Jin, H., et al. Multiple amino acid residues confer temperature sensitivity to human influenza virus vaccine strains (FluMist) derived from cold-adapted A/Ann Arbor/6/60. Virology 306, 18-24 (2003).
25. Chen, Z., et al. Evaluation of live attenuated influenza a virus h6 vaccines in mice and ferrets. J. Virol. 83, 65-72 (2009).
26. Sui, J., et al. Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza a antibodies. Clin. Infect. Dis. 52, 1003-1009 (2011).
27. Wohlbold, T. J., et al. Vaccination with soluble headless hemagglutinin protects mice from challenge with divergent influenza viruses. Vaccine 33, 3314-3321 (2015).
28. Dreyfus, C., et al. Highly conserved protective epitopes on influenza B viruses. Science 337, 1343-1348 (2012).
29. Luke, C. J., Subbarao, K. Improving pandemic H5N1 influenza vaccines by combining different vaccine platforms. Expert. Rev. Vaccin. 13, 873-883 (2014).
30. Rudenko, L., et al. Assessment of immune responses to H5N1 inactivated influenza vaccine among individuals previously primed with H5N2 live attenuated influenza vaccine. Hum. Vaccin Immunother. 11, 2839-2848 (2015).
31. Wei, C. J., et al. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 329, 1060-1064 (2010).
32. Nachbagauer, R., et al. A chimeric haemagglutinin-based influenza split virion vaccine adjuvanted with AS03 induces protective stalk-reactive antibodies in mice. npj Vaccines 1, 16015 (2016).
33. Easterbrook, J. D. Protection against a lethal H5N1 influenza challenge by intranasal immunization with virus-like particles containing 2009 pandemic H1N1 neuraminidase in mice. Virology 432, 39-44 (2012).
34. Wohlbold, T. J., et al. Vaccination with adjuvanted recombinant neuraminidase induces broad heterologous, but not heterosubtypic, cross-protection against influenza virus infection in mice. MBio, doi:10.1128/mBio.02556-14 (2015).
35. Liu, W. C., Lin, C. Y., Tsou, Y. T., Jan, J. T., Wu, S. C. Cross-reactive neuraminidase-inhibiting antibodies elicited by immunization with recombinant neuraminidase proteins of H5N1 and pandemic H1N1 influenza a viruses. J. Virol. 89, 7224-7234 (2015).
36. Hamilton, J. R., et al. Club cells surviving influenza A virus infection induce temporary nonspecific antiviral immunity. Proc Natl Acad Sci USA, doi:10.1073/pnas.1522376113 (2016).
37. Isakova-Sivak, I., Rudenko, L. Safety, immunogenicity and infectivity of new live attenuated influenza vaccines. Expert. Rev. Vaccin. 14, 1313-1329 (2015).
38. Schuind, A., Segall, N., Drame, M., Innis, B. L. Immunogenicity and safety of an EB66 cell-culture-derived influenza a/indonesia/5/2005(H5N1) AS03-adjuvanted vaccine: A phase 1 randomized trial. J. Infect. Dis. 212, 531-541 (2015).
39. Weir, J. P., Gruber, M. F. An overview of the regulation of influenza vaccines in the United States. Influenza Other Respir. Virus. 10, 354-360 (2016).
40. Margine, I., Palese, P., Krammer, F. Expression of functional recombinant hemagglutinin and neuraminidase proteins from the novel H7N9 influenza virus using the baculovirus expression system. J Vis Exp, doi:10.3791/5111 (2013).
41. Krammer, F., et al. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7, e43603 (2012).
42. Hai, R., et al. Influenza viruses expressing chimeric hemagglutinins: Globular head and stalk domains derived from different subtypes. J. Virol. 86, 5774-5781 (2012).
43. Garçon, N., Vaughn, D. W., Didierlaurent, A. M. Development and evaluation of AS03, an Adjuvant System containing α-tocopherol and squalene in an oil-in-water emulsion. Expert. Rev. Vaccin. 11, 349-366 (2012).
44. Morel, S., et al. Adjuvant System AS03 containing α-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine 29, 2461-2473 (2011).
45. Isakova-Sivak, I., et al. Genetic bases of the temperature-sensitive phenotype of a master donor virus used in live attenuated influenza vaccines: A/leningrad/134/17/57 (H2N2). Virology 412, 297-305 (2011).
46. Ridenour, C., et al. Development of influenza A(H7N9) candidate vaccine viruses with improved hemagglutinin antigen yield in eggs. Influenza Other Respir. Virus. 9, 263-270 (2015).
47. Hai, R., Garciá-Sastre, A., Swayne, D. E., Palese, P. A reassortment-incompetent live attenuated influenza virus vaccine for protection against pandemic virus strains. J. Virol. 85, 6832-6843 (2011).
48. Hierholzer, J. C., Killington, R. A. in Virology Methods Manual (eds Mahy, B.W.J., Kangro, H.O.) 24-32 (Academic, 1996).
49. Wang, S., et al. Hemagglutinin (HA) proteins from H1 and H3 serotypes of influenza A viruses require different antigen designs for the induction of optimal protective antibody responses as studied by codon-optimized HA DNA vaccines. J. Virol. 80, 11628-11637 (2006).