Intranasal vaccination with a plant-derived H5 HA vaccine protects mice and ferrets against highly pathogenic avian influenza virus challenge

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 5, 2015, Pages 1235-1243

  Major, Diane ^a   Chichester, Jessica A ^b   Pathirana, Rishi D ^c,d   Guilfoyle, Kate ^a   Shoji, Yoko ^b   Guzman, Carlos A ^e   Yusibov, Vidadi ^b   Cox, Rebecca J ^c,d  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^b Fraunhofer USA Inc   (United States)

^c UNIVERSITY OF BERGEN   (Norway)

^d HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^e HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Adjuvant; C di GMP; Ferret infection model; Influenza H5N1; Intranasal vaccination; Mice; Plant vaccine

Indexed keywords

CYCLIC GMP; HEPATITIS A VACCINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; VIRUS HEMAGGLUTININ; BIS(3',5')-CYCLIC DIGUANYLIC ACID; HEMAGGLUTININ, AVIAN INFLUENZA A VIRUS; IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; RECOMBINANT VACCINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA VIRUS; BODY TEMPERATURE; BODY WEIGHT; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FERRET; IMMUNOGENICITY; LIMIT OF DETECTION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SURVIVAL RATE; VIRUS LOAD; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H5N1); INTRANASAL DRUG ADMINISTRATION; ISOLATION AND PURIFICATION; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; TRANSGENIC PLANT; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; CYCLIC GMP; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MALE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; PLANTS, GENETICALLY MODIFIED; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VACCINES, SYNTHETIC;

EID: 84942427613     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/21645515.2014.988554     Document Type: Article

References (36)

1. World Health Organization. Summary of assessment as of January 2015. Available from: http://www.who.int/ influenza/human_animal_interface/Influenza_Summary_ IRA_HA_interface_26January2015.pdf.pdf?ua=1
2. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012; 486:420-8; PMID:22722205
3. Zhang Y, Zhang Q, Kong H, Jiang Y, Gao Y, Deng G, Shi J, Tian G, Liu L, Liu J, et al. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 2013; 340:1459-63; PMID:23641061; http://dx.doi.org/10.1126/ science.1229455
4. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012; 336:1534-41; PMID:22723413; http://dx.doi.org/ 10.1126/science.1213362
5. Chichester JA, Haaheim LR, Yusibov V. Using plant cells as influenza vaccine substrates. Expert Rev Vaccin 2009; 8:493-8; PMID:19348564; http://dx.doi.org/ 10.1586/erv.09.3
6. Mutsch M, Zhou W, Rhodes P, Bopp M, Chen RT, Linder T, Spyr C, Steffen R. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 2004; 350:896-903; PMID:14985487; http://dx.doi.org/10.1056/ NEJMoa030595
7. Lewis DJ, Huo Z, Barnett S, Kromann I, Giemza R, Galiza E, Woodrow M, Thierry-Carstensen B, Andersen P, Novicki D, et al. Transient facial nerve paralysis (Bell's palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PloS One 2009; 4:e6999; PMID:19756141; http://dx.doi.org/10.1371/journal.pone.0006999
8. Chen W, Kuolee R, Yan H. The potential of 30, 50-cyclic diguanylic acid (c-di-GMP) as an effective vaccine adjuvant. Vaccine 2010; 28:3080-5; PMID:20197136; http://dx.doi.org/10.1016/j. vaccine.2010.02.081
9. Ebensen T, Schulze K, Riese P, Morr M, Guzman CA. The bacterial second messenger cdiGMP exhibits promising activity as a mucosal adjuvant. Clin Vaccine Immunol 2007; 14:952-8; PMID:17567766; http:// dx.doi.org/10.1128/CVI.00119-07
10. Karaolis DK, Means TK, Yang D, Takahashi M, Yoshimura T, Muraille E, Philpott D, Schroeder JT, Hyodo M, Hayakawa Y, et al. Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 2007; 178:2171-81; http://dx.doi.org/10.4049/ jimmunol.178.4.2171
11. Madhun AS, Haaheim LR, Nostbakken JK, Ebensen T, Chichester J, Yusibov V, Guzman CA, Cox RJ. Intranasal c-di-GMP-adjuvanted plant-derived H5 influenza vaccine induces multifunctional Th1 CD4C cells and strong mucosal and systemic antibody responses in mice. Vaccine 2011; 29:4973-82; PMID:21600260; http://dx.doi.org/10.1016/j.vaccine.2011.04.094
12. Pedersen GK, Ebensen T, Gjeraker IH, Svindland S, Bredholt G, Guzman CA, Cox RJ. Evaluation of the sublingual route for administration of influenza H5N1 virosomes in combination with the bacterial second messenger c-di-GMP. PloS One 2011; 6:e26973; PMID:22069479; http://dx.doi.org/10.1371/journal. pone.0026973
13. Hobson D, Curry RL, Beare AS, Ward-Gardner A. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg 1972; 70:767-77; PMID:4509641; http://dx.doi.org/10.1017/ S0022172400022610
14. Banner D, Kelvin AA. The current state of H5N1 vaccines and the use of the ferret model for influenza therapeutic and prophylactic development. J Infect Dev Ctries 2012; 6:465-9; PMID:22706187
15. Wood JM, Robertson JS. From lethal virus to life-saving vaccine: developing inactivated vaccines for pandemic influenza. Nat Rev Microbiol 2004; 2:842-7; PMID:15378048; http://dx.doi.org/10.1038/ nrmicro979
16. Clegg CH, Rininger JA, Baldwin SL. Clinical vaccine development for H5N1 influenza. Expert Rev Vaccin 2013; 12:767-77; PMID:23885822; http://dx.doi.org/ 10.1586/14760584.2013.811178
17. Shoji Y, Chichester JA, Jones M, Manceva SD, Damon E, Mett V, Musiychuk K, Bi H, Farrance C, Shamloul M, et al. Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccin 2011; 7 Suppl:41-50; PMID:21266846; http://dx.doi.org/10.4161/hv.7.0. 14561
18. Chichester JA, Yusibov V. Plants as alternative systems for production of vaccines. Hum Vaccin 2007; 3:146-8; PMID:17643065; http://dx.doi.org/10.4161/hv.3. 4.4148
19. Shoji Y, Bi H, Musiychuk K, Rhee A, Horsey A, Roy G, Green B, Shamloul M, Farrance CE, Taggart B, et al. Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine 2009; 27:1087-92; PMID:19100806; http://dx.doi.org/10.1016/j.vaccine. 2008.11.108
20. Brandtzaeg P. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 2007; 25:5467-84; PMID:17227687; http://dx.doi.org/10.1016/j. vaccine.2006.12.001
21. Cox RJ, Major D, Hauge S, Madhun AS, Brokstad KA, Kuhne M, Smith J, Vogel FR, Zambon M, Haaheim LR, et al. A cell-based H7N1 split influenza virion vaccine confers protection in mouse and ferret challenge models. Influenza Other Respir Viruses 2009; 3:107-17; PMID:19453487; http://dx.doi.org/10.1111/ j.1750-2659.2009.00082.x
22. Lipatov AS, Hoffmann E, Salomon R, Yen HL, Webster RG. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J Infect Dis 2006; 194:1040-3; PMID:16991078; http://dx.doi.org/10.1086/507709
23. Baz M, Luke CJ, Cheng X, Jin H, Subbarao K. H5N1 vaccines in humans. Virus Res 2013; 178(1):78-98; PMID:23726847
24. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, Hyodo M, Hayakawa Y, Vance RE. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011; 478:515-8; PMID:21947006; http://dx. doi.org/10.1038/nature10429
25. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461:788-92; PMID:19776740; http://dx.doi.org/10.1038/nature 08476
26. Parvatiyar K, Zhang Z, Teles RM, Ouyang S, Jiang Y, Iyer SS, Zaver SA, Schenk M, Zeng S, Zhong W, et al. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 2012; 13:1155-61; PMID:23142775; http:// dx.doi.org/10.1038/ni.2460
27. Blaauboer SM, Gabrielle VD, Jin L. MPYS/STINGmediated TNF-alpha, not type I IFN, is essential for the mucosal adjuvant activity of (3'-5')-cyclic-di-guanosinemonophosphate in vivo. J Immunol 2014; 192:492-502; http://dx.doi.org/10.4049/jimmunol.1301812
28. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. H5N1 Virus Attachment to Lower Respiratory Tract. Science 2006; 312:399; PMID:16556800; http://dx.doi.org/ 10.1126/science.1125548
29. Schrauwen EJ, Herfst S, Leijten LM, van Run P, Bestebroer TM, Linster M, Bodewes R, Kreijtz JH, Rimmelzwaan GF, Osterhaus AD, et al. The multibasic cleavage site in H5N1 virus is critical for systemic spread along the olfactory and hematogenous routes in ferrets. J Virol 2012; 86:3975-84; PMID:22278228; http://dx.doi.org/10.1128/JVI.06828-11
30. Shoji Y, Chichester JA, Bi H, Musiychuk K, de la Rosa P, Goldschmidt L, Horsey A, Ugulava N, Palmer GA, Mett V, et al. Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 2008; 26:2930-4; PMID:18440103; http://dx.doi.org/10.1016/j.vaccine. 2008.03.045
31. Ebensen T, Schulze K, Riese P, Link C, Morr M, Guzman CA. The bacterial second messenger cyclic diGMP exhibits potent adjuvant properties. Vaccine 2007; 25:1464-9; PMID:17187906; http://dx.doi.org/ 10.1016/j.vaccine.2006.10.033
32. Mahy BWJ, Kangro HO. Virology methods manual. New York: Academic Press Limited, 1996; page 37. ISBN 0-12-465330-8
33. Hauge S, Madhun A, Cox RJ, Haaheim LR. Quality and kinetics of the antibody response inmice after three different low-dose influenza virus vaccination strategies. Clin Vaccine Immunol 2007; 14:978-83; PMID:17596426; http://dx.doi.org/10.1128/CVI.00033-07
34. Hovden AO, Cox RJ, Haaheim LR. Whole influenza virus vaccine is more immunogenic than split influenza virus vaccine and induces primarily an IgG2a response in BALB/c mice. Scand J Immunol 2005; 62:36-44; PMID:16092921; http://dx.doi.org/10.1111/j.1365-3083.2005.01633.x
35. Stephenson I, Wood JM, Nicholson KG, Charlett A, Zambon MC. Detection of anti-H5 responses in human sera by HI using horse erythrocytes following MF59-adjuvanted influenza A/Duck/Singapore/97 vaccine. Virus Res 2004; 103:91-5; PMID:15163495; http://dx.doi.org/10.1016/j.virusres.2004.02.019
36. Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, Wood J, Hoschler K, Zambon MC. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 2006; 367:1657-64; PMID:16714186; http://dx.doi.org/10.1016/S0140-6736(06)68656-X