Immunogenicity and protective efficacy of a vero cell culture-derived whole-virus H7N9 vaccine in mice and guinea pigs

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Wodal, Walter ^a   Schwendinger, Michael G ^a   Savidis Dacho, Helga ^a   Crowe, Brian A ^a   Hohenadl, Christine ^a   Fritz, Richard ^a   Brühl, Peter ^a   Portsmouth, Daniel ^a   Karner Pichl, Anita ^a   Balta, Dalida ^a   Grillberger, Leopold ^a   Kistner, Otfried ^a   Barrett, P Noel ^a   KeithHoward, M ^a  

^a BAXTER BIOSCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; INFLUENZA VACCINE; UNCLASSIFIED DRUG; VIRUS SIALIDASE; VIRUS VACCINE; WHOLE VIRUS INFLUENZA A H7N9 VACCINE; GAMMA INTERFERON; INFLUENZA VIRUS HEMAGGLUTININ; INTERLEUKIN 4; SIALIDASE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CELL CULTURE; CELLULAR IMMUNITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GUINEA PIG; HELPER CELL; HEMAGGLUTINATION INHIBITION TEST; IMMUNIZATION; IMMUNOGENICITY; IMMUNOPROPHYLAXIS; INFLUENZA; MOUSE; NONHUMAN; VERO CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIBODY PRODUCTION; CHLOROCEBUS AETHIOPS; DBA MOUSE; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H7N9); METABOLISM; MORTALITY; ORTHOMYXOVIRIDAE INFECTIONS; PHYSIOLOGY; TH1 CELL; TH2 CELL;

ANIMALIA; AVES; CAVIA; MUS;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY FORMATION; CERCOPITHECUS AETHIOPS; FEMALE; GUINEA PIGS; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; INTERFERON-GAMMA; INTERLEUKIN-4; MICE; MICE, INBRED DBA; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; TH1 CELLS; TH2 CELLS; VERO CELLS;

EID: 84923810027     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113963     Document Type: Article

References (54)

1. Gao R, Cao B, Hu Y, Feng Z, Wang D, et al. (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368: 1888-1897. doi: 10.1056/NEJMoa1304459 PMID: 23577628
2. Liu D, Shi W, Shi Y, Wang D, Xiao H, et al. (2013) Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381: 1926-1932. doi: 10.1016/S0140-6736(13)60938-1 PMID: 23643111
3. Lam TT, Wang J, Shen Y, Zhou B, Duan L, et al. (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502: 241-244. doi: 10.1038/nature12515 PMID: 23965623
4. Gao HN, Lu HZ, Cao B, Du B, Shang H, et al. (2013) Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med 368: 2277-2285. doi: 10.1056/NEJMoa1305584 PMID: 23697469
5. Li Q, Zhou L, Zhou M, Chen Z, Li F, et al. (2014) Epidemiology of human infections with Avian Influenza A (H7N9) Virus in China. N Engl J Med 370: 520-532. doi: 10.1056/NEJMoa1304617 PMID: 23614499
6. Qi X, Qian YH, Bao CJ, Guo XL, Cui LB, et al. (2013) Probable person to person transmission of novel avian influenza A (H7N9) virus in Eastern China, 2013: epidemiological investigation. BMJ 347: f4752.doi: 10.1136/bmj.f4752 PMID: 23920350
7. Shi Y, Zhang W, Wang F, Qi J, Wu Y, et al. (2013) Structures and receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses. Science 342: 243-247. doi: 10.1126/science.1242917 PMID: 24009358
8. Tharakaraman K, Jayaraman A, Raman R, Viswanathan K, Stebbins NW, et al. (2013) Glycan receptor binding of the influenza A virus H7N9 hemagglutinin. Cell 153: 1486-1493. doi: 10.1016/j.cell.2013.05. 034 PMID: 23746830
9. Zhou J, Wang D, Gao R, Zhao B, Song J, et al. (2013) Biological features of novel avian influenza A (H7N9) virus. Nature 499: 500-503. doi: 10.1038/nature12379 PMID: 23823727
10. Chan MC, Chan RW, Chan LL, Mok CK, Hui KP, et al. (2013) Tropism and innate host responses of a novel avian influenza A H7N9 virus: an analysis of ex-vivo and in-vitro cultures of the human respiratory tract. Lancet Respir Med 1: 534-542. doi: 10.1016/S2213-2600(13)70138-3 PMID: 24461614
11. Knepper J, Schierhorn KL, Becher A, Budt M, Tonnies M, et al. (2013) The Novel Human Influenza A (H7N9) Virus Is Naturally Adapted to Efficient Growth in Human Lung Tissue. MBio 4: 601-613.
12. van Riel D, Leijten LM, de Graaf M, Siegers JY, Short KR, et al. (2013) Novel avian-origin influenza A (H7N9) virus attaches to epithelium in both upper and lower respiratory tract of humans. Am J Pathol 183: 1137-1143. doi: 10.1016/j.ajpath.2013.06.011 PMID: 24029490
13. Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, et al. (2013) Characterization of H7N9 influenza A viruses isolated from humans. Nature 501: 551-555. doi: 10.1038/nature12392 PMID: 23842494
14. Zhang Q, Shi J, Deng G, Guo J, Zeng X, et al. (2013) H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341: 410-414. doi: 10.1126/science.1240532 PMID: 23868922
15. De Groot AS, Ardito M, Terry F, Levitz L, Ross T, et al. (2013) Low immunogenicity predicted for emerging avian-origin H7N9: Implication for influenza vaccine design. Hum Vaccin Immunother 9: 950-956. doi: 10.4161/hv.24939 PMID: 23807079
16. Ehrlich HJ, Muller M, Kollaritsch H, Pinl F, Schmitt B, et al. (2012) Pre-vaccination immunity and immune responses to a cell culture-derived whole-virus H1N1 vaccine are similar to a seasonal influenza vaccine. Vaccine 30: 4543-4551. doi: 10.1016/j.vaccine.2012.03.061 PMID: 22475864
17. Kistner O, Crowe BA, Wodal W, Kerschbaum A, Savidis-Dacho H, et al. (2010) A whole virus pandemic influenza H1N1 vaccine is highly immunogenic and protective in active immunization and passive protection mouse models. PLoS One 5: e9349. doi: 10.1371/journal.pone.0009349 PMID: 20186321
18. Loew-Baselli A, Pavlova BG, Fritsch S, Poellabauer EM, Draxler W, et al. (2012) A non-adjuvanted whole-virus H1N1 pandemic vaccine is well tolerated and highly immunogenic in children and adolescents and induces substantial immunological memory. Vaccine 30: 5956-5966. doi: 10.1016/j. vaccine.2012.07.039 PMID: 22846396
19. Twenty-second pandemic pharmacovigilance update (2010) EMA/527985/2010. PMID: 25506974
20. Kistner O, Howard MK, Spruth M, Wodal W, Brühl P, et al. (2007) Cell culture (Vero) derived whole virus (H5N1) vaccine based on wild-type virus strain induces cross-protective immune responses. Vaccine 25: 6028-6036. PMID: 17614165
21. Fritz R, Sabarth N, Kiermayr S, Hohenadl C, Howard MK, et al. (2012) A vero cell-derived whole-virus H5N1 vaccine effectively induces neuraminidase-inhibiting antibodies. J Infect Dis 205: 28-34. doi: 10. 1093/infdis/jir711 PMID: 22090447
22. Kundi M (1999) One-hit models for virus inactivation studies. Antiviral Res 41: 145-152. PMID: 10320047
23. Jia N, Wang SX, Liu YX, Zhang PH, Zuo SQ, et al. (2008) Increased sensitivity for detecting avian influ-enza-specific antibodies by a modified hemagglutination inhibition assay using horse erythrocytes. J Virol Methods 153: 43-48. doi: 10.1016/j.jviromet.2008.06.016 PMID: 18634828
24. Meijer A, Bosman A, van de Kamp EE, Wilbrink B, Du Ry van Beest Holle, et al. (2006) Measurement of antibodies to avian influenza virus A(H7N7) in humans by hemagglutination inhibition test. J Virol Methods 132: 113-120. PMID: 16271401
25. Smith GE, Flyer DC, Raghunandan R, Liu Y, Wei Z, et al. (2013) Development of influenza H7N9 virus like particle (VLP) vaccine: homologous A/Anhui/1/2013 (H7N9) protection and heterologous A/chicken/ Jalisco/CPA1/2012 (H7N3) cross-protection in vaccinated mice challenged with H7N9 virus. Vaccine 31: 4305-4313. doi: 10.1016/j.vaccine.2013.07.043 PMID: 23891795
26. Srivastava B, Blazejewska P, Hemann M, Bruder D, Geffers R, et al. (2009) Host genetic background strongly influences the response to influenza A virus infections. PLoS One 4: e4857. doi: 10.1371/ journal.pone.0004857 PMID: 19293935
27. Boon ACM, deBeauchamp J, Hollmann A, Luke J, Kotb M, et al. (2009) Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J Virol 83: 10417-10426. doi: 10.1128/JVI.00514-09 PMID: 19706712
28. Solórzano A, Ye J, Pérez DR (2010) Alternative live-attenuated influenza vaccines based on modifications in the polymerase genes protect against epidemic and pandemic flu. J Virol 84: 4587-4596. doi: 10.1128/JVI.00101-10 PMID: 20181702
29. Pica N, Iyer A, Ramos I, Bouvier NM, Fernandez-Sesma A, García-Sastre A, et al (2011) The DBA.2 mouse is susceptible to disease following infection with a broad, but limited, range of influenza A and B viruses. J Virol 85: 12825-12829 doi: 10.1128/JVI.05930-11 PMID: 21917963
30. Dengler L, May M, Wilk E, Bahgat MM, Schughart K (2012) Immunization with live virus vaccine protects highly susceptible DBA/2J mice from lethal influenza A H1N1 infection. Virol J 9: 212 doi: 10. 1186/1743-422X-9-212 PMID: 22992381
31. de Jong JC, Palache AM, Beyer WE, Rimmelzwaan GF, Boon AC, et al. (2003) Haemagglutination-inhibiting antibody to influenza virus. Dev Biol (Basel) 115: 63-73. PMID: 15088777
32. Hobson D, Curry RL, Beare AS, Ward-Gardner A (1972) The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg (Lond) 70: 767-777. PMID: 4509641
33. Howard MK, Sabarth N, Savidis-Dacho H, Portsmouth D, Kistner O, et al. (2011) H5N1 whole-virus vaccine induces neutralizing antibodies in humans which are protective in a mouse passive transfer model. PLoS One 6: e23791. doi: 10.1371/journal.pone.0023791 PMID: 21876771
34. Pandemic Influenza Vaccine H5N1 Baxter AG (2012) EPAR summary for the public. Available: http:// www.ema.europa.eu/docs/en-GB/document-library/EPAR-Summary-for-the-public/human/ 001200/WC500049617.pdf. Accessed 26 October 2014.
35. Vepacel (2012) EPAR summary for the public. Available: http://www.ema.europa.eu/docs/en-GB/ document-library/EPAR-Summary-for-the-public/human/002089/WC500124226.pdf. Accessed26 October 2014.
36. Couch RB, Atmar RL, Franco LM, Quarles JM, Wells J, et al. (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. doi: 10.1093/infdis/jis935 PMID: 23307936
37. Rockman S, Brown LE, Barr IG, Gilbertson B, Lowther S, et al. (2013) Neuraminidase-Inhibiting Antibody Is a Correlate of Cross-Protection against Lethal H5N1 Influenza Virus in Ferrets Immunized with Seasonal Influenza Vaccine. J Virol 87: 3053-3061. doi: 10.1128/JVI.02434-12 PMID: 23283953
38. Boon ACM, deBeauchamp J, Krauss S, Rubrum A, Webb AD, et al. (2010) Cross-reactive neutralizing antibodies directed against pandemic H1N1 2009 virus are protective in a highly sensitive DBA/2 mouse influenza model. J Virol 84: 7662-7667 doi: 10.1128/JVI.02444-09 PMID: 20484500
39. Geeraedts F, Goutagny N, Hornung V, Severa M, de Haan A, et al. (2008) Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog 4: e1000138. doi: 10.1371/journal.ppat.1000138 PMID: 18769719
40. Hagenaars N, Mastrobattista E, Glansbeek H, Heldens J, van den Bosch H, et al. (2008) Head-to-head comparison of four nonadjuvanted inactivated cell culture-derived influenza vaccines: effect of composition, spatial organization and immunization route on the immunogenicity in a murine challenge model. Vaccine 26: 6555-6563. doi: 10.1016/j.vaccine.2008.09.057 PMID: 18848856
41. Geeraedts F, Bungener L, Pool J, Ter Veer W, Wilschut J, et al. (2008) Whole inactivated virus influenza vaccine is superior to subunit vaccine in inducing immune responses and secretion of proinflammatory cytokines by DCs. Influenza Other Respir Viruses 2: 41-51. doi: 10.1111/j.1750-2659.2008.00038.x PMID: 19453471
42. Doherty PC, Turner SJ, Webby RG, Thomas PG (2006) Influenza and the challenge for immunology. Nat Immunol 7: 449-455. PMID: 16622432
43. McKinstry KK, Strutt TM, Swain SL (2011) Hallmarks of CD4 T cell immunity against influenza. J Intern Med 269: 507-518. doi: 10.1111/j.1365-2796.2011.02367.x PMID: 21362069
44. Fries LF, Smith GE, Glenn GM (2013) A Recombinant Viruslike Particle Influenza A (H7N9) Vaccine. N Engl J Med 369: 2564-2566. doi: 10.1056/NEJMc1313728 PMID: 24369087
45. Bart SA, Hohenboken M, Della Cioppa G, Narasimhan V, Dormitzer PR, et al (2014) A cell culture-derived MF59-adjuvanted pandemic A/H7N9 vaccine is immunogenic in adults. Sci Transl Med 6: 234ra55. doi: 10.1126/scitranslmed.3008761 PMID: 24786323
46. Chu D-C, Sakoda Y, Nishi T, Hiono T, Shichinohe S, et al. (2014) Potency of an inactivated influenza vaccine prepared from A/duck/Mongolia/119/2008 (H7N9) against the challenge with A/Anhui/1/2013 (H7N9). Vaccine 32: 3473-3479. doi: 10.1016/j.vaccine.2014.04.060 PMID: 24793949
47. Wu C-Y, Chang C-Y, Ma H-H, Wang C-W, Chen Y-T, et al. (2014) Squalene-adjuvanted H7N9 virus vaccine induces robust humoral immune response against H7N9 and H7N7 viruses. Vaccine 32: 4485-449446. doi: 10.1016/j.vaccine.2014.06.043 PMID: 24962757
48. Tang LH, Lim JH, Kuah LF, Lau YF (2014) Complete protection against lethal challenge of novel H7N9 virus with heterologous inactivated H7 vaccine in mice. Vaccine 32: 5375-5378. doi: 10.1016/j. vaccine.2014.07.087 PMID: 25130540
49. Wong S-S, Jeevan T, Kercher L, Yoon S-W, Petkova A-M, et al. (2014) A single dose of whole inactivated H7N9 influenza vaccine confers protection from severe disease but not infection in ferrets. Vaccine 32: 4571-4577. doi: 10.1016/j.vaccine.2014.06.016 PMID: 24950355
50. Celvapan (2012) EPAR summary for the public Available: http://www.ema.europa.eu/docs/en-GB/ document-library/EPAR-Summary-for-the-public/human/000982/WC500022671.pdf. Accessed 26 October 2014.
51. Ehrlich HJ, Müller M, Oh HM, Tambyah PA, Joukhadar C, et al. (2008) A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N Engl J Med 358: 2573-2584. doi: 10.1056/NEJMoa073121 PMID: 18550874
52. Ehrlich HJ, Müller M, Fritsch S, Zeitlinger M, Berezuk G, et al. (2009) A cell culture (Vero)-derived H5N1 whole-virus vaccine induces cross-reactive memory responses. J Infect Dis 200: 1113-1118. doi: 10. 1086/605608 PMID: 19712040
53. van der Velden MV, Aichinger G, Pöllabauer EM, Löw-Baselli A, Fritsch S, et al. (2012) Cell culture (Vero cell) derived whole-virus non-adjuvanted H5N1 influenza vaccine induces long-lasting cross-reactive memory immune response: homologous or heterologous booster response following two dose or single dose priming. Vaccine 30: 6127-6135. doi: 10.1016/j.vaccine.2012.07.077 PMID: 22884662
54. van der Velden MV, Fritz R, Pöllabauer EM, Portsmouth D, Howard MK, et al. (2014) Safety and Immunogenicity of a Vero Cell Culture-Derived Whole-Virus Influenza A(H5N1) Vaccine in a Pediatric Population. J Infect Dis 209: 12-23. doi: 10.1093/infdis/jit498 PMID: 24041789