Matrix-M adjuvated seasonal virosomal influenza vaccine induces partial protection in mice and ferrets against avian H5 and H7 challenge

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Cox, Freek ^a   Roos, Anna ^a   Hafkemeijer, Nicole ^a   Baart, Matthijs ^a   Tolboom, Jeroen ^a   Dekking, Liesbeth ^a   Stittelaar, Koert ^b   Goudsmit, Jaap ^a   Radošević, Katarina ^a,c   Saeland, Eirikur ^a  

^a Janssen Research and Development   (Netherlands)

^b ViroClinics Biosciences   (Netherlands)

^c SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; MATRIX M; SEASONAL TRIVALENT VIROSOMAL INFLUENZA VACCINE; UNCLASSIFIED DRUG; MATRIX PROTEIN; VIROSOME VACCINE; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; AVIAN INFLUENZA; CLINICAL FEATURE; CONTROLLED STUDY; CROSS REACTION; DISEASE SEVERITY; FEMALE; FERRET; IMMUNOPOTENTIATION; INFLUENZA A (H5N1); INFLUENZA A (H7N7); INFLUENZA A (H7N9); INFLUENZA A VIRUS (H7N7); INFLUENZA A VIRUS (H7N9); INFLUENZA VACCINATION; LOWER RESPIRATORY TRACT INFECTION; MOUSE; MOUSE MODEL; NONHUMAN; VIRAL UPPER RESPIRATORY TRACT INFECTION; VIRUS LOAD; VIRUS STRAIN; ANIMAL; BLOOD; CLASSIFICATION; DISEASE MODEL; IMMUNIZATION; IMMUNOLOGY; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE INFECTIONS; VIROLOGY; VIRUS REPLICATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, VIRAL; CROSS REACTIONS; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; IMMUNIZATION; INFLUENZA A VIRUS; INFLUENZA VACCINES; MICE; ORTHOMYXOVIRIDAE INFECTIONS; VACCINES, VIROSOME; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

EID: 84946935133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135723     Document Type: Article

References (47)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiological reviews. 1992 Mar; 56(1):152-79. PMID: 1579108. Pubmed Central PMCID: 372859.
2. Pica N, Palese P. Toward a universal influenza virus vaccine: prospects and challenges. Annual review of medicine. 2013; 64:189-202. PMID: 23327522. doi: 10.1146/annurev-med-120611-145115
3. Medina RA, Garcia-Sastre A. Influenza A viruses: new research developments. Nat Rev Microbiol. 2011 Aug; 9(8):590-603. PMID: 21747392. doi: 10.1038/nrmicro2613
4. Belser JA, Szretter KJ, Katz JM, Tumpey TM. Use of Animal Models to Understand the Pandemic Potential of Highly Pathogenic Avian Influenza Viruses. Advances in Virus Research. 2009; 73:55-97. doi: 10.1016/S0065-3527(09)73002-7 PMID: 19695381
5. Hannoun C. The evolving history of influenza viruses and influenza vaccines. Expert Rev Vaccines. 2013 Sep; 12(9):1085-94. PMID: 24024871. doi: 10.1586/14760584.2013.824709
6. WHO. Influenza at the human-animal interface; Summary and assessment as of 4 July 2013. Available: http://wwwwhoint/influenza/human-animal-interface/Influenza-Summary-IRA-HA-interface- 03July13pdf.
7. WHO. Report 9-data in WHO/HQ as of 12 August 2013. Available: http://wwwwhoint/influenza/ human-animal-interface/influenza-h7n9/09-ReportWebH7N9Numberpdf.
8. Richard M, Schrauwen EJ, de Graaf M, Bestebroer TM, Spronken MI, van Boheemen S, et al. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature. 2013 Sep 26; 501 (7468):560-3. PMID: 23925116. Pubmed Central PMCID: 3819191. doi: 10.1038/nature12476
9. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science. 2012 Jun 22; 336(6088):1534-41. PMID: 22723413. doi: 10.1126/science.1213362
10. Schulman JL, Kilbourne ED. Airborne transmission of influenza virus infection in mice. Nature. 1962 Sep 15; 195:1129-30. PMID: 13909471.
11. Knossow M, Skehel JJ. Variation and infectivity neutralization in influenza. Immunology. 2006 Sep; 119 (1):1-7. PMID: 16925526. Pubmed Central PMCID: 1782343.
12. Gerhard W, Yewdell J, Frankel ME, Webster R. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature. 1981 Apr 23; 290(5808):713-7. PMID: 6163993.
13. Treanor JJ, Campbell JD, Zangwill KM, Rowe T, Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. The New England journal of medicine. 2006 Mar 30; 354 (13):1343-51. PMID: 16571878.
14. Couch RB, Patel SM, Wade-Bowers CL, Nino D. A randomized clinical trial of an inactivated avian influenza A (H7N7) vaccine. PLoS One. 2012; 7(12):e49704. PMID: 23239968. Pubmed Central PMCID: 3519847. doi: 10.1371/journal.pone.0049704
15. Cox RJ, Madhun AS, Hauge S, Sjursen H, Major D, Kuhne M, et al. A phase I clinical trial of a PER.C6 cell grown influenza H7 virus vaccine. Vaccine. 2009 Mar 18; 27(13):1889-97. PMID: 19368768. doi: 10.1016/j.vaccine.2009.01.116
16. Leroux-Roels I, Borkowski A, Vanwolleghem T, Drame M, Clement F, Hons E, et al. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet. 2007 Aug 18; 370(9587):580-9. PMID: 17707753.
17. Baras B, de Waal L, Stittelaar KJ, Jacob V, Giannini S, Kroeze EJ, et al. Pandemic H1N1 vaccine requires the use of an adjuvant to protect against challenge in naive ferrets. Vaccine. 2011 Mar 3; 29 (11):2120-6. PMID: 21238573. doi: 10.1016/j.vaccine.2010.12.125
18. van den Brand JM, Kreijtz JH, Bodewes R, Stittelaar KJ, van Amerongen G, Kuiken T, et al. Efficacy of vaccination with different combinations of MF59-adjuvanted and nonadjuvanted seasonal and pandemic influenza vaccines against pandemic H1N1 (2009) influenza virus infection in ferrets. J Virol. 2011 Mar; 85(6):2851-8. PMID: 21209108. Pubmed Central PMCID: 3067945. doi: 10.1128/JVI. 01939-10
19. Cox RJ, Pedersen G, Madhun AS, Svindland S, Saevik M, Breakwell L, et al. Evaluation of a virosomal H5N1 vaccine formulated with Matrix M adjuvant in a phase I clinical trial. Vaccine. 2011 Oct 19; 29 (45):8049-59. PMID: 21864624. doi: 10.1016/j.vaccine.2011.08.042
20. Sambhara S, Woods S, Arpino R, Kurichh A, Tamane A, Underdown B, et al. Heterotypic protection against influenza by immunostimulating complexes is associated with the induction of cross-reactive cytotoxic T lymphocytes. J Infect Dis. 1998 May; 177(5):1266-74. PMID: 9593011.
21. Sambhara S, Kurichh A, Miranda R, Tumpey T, Rowe T, Renshaw M, et al. Heterosubtypic immunity against human influenza A viruses, including recently emerged avian H5 and H9 viruses, induced by FLU-ISCOM vaccine in mice requires both cytotoxic T-lymphocyte and macrophage function. Cell Immunol. 2001 Aug 1; 211(2):143-53. PMID: 11591118.
22. Rockman S, Brown LE, Barr IG, Gilbertson B, Lowther S, Kachurin A, et al. Neuraminidase-inhibiting antibody is a correlate of cross-protection against lethal H5N1 influenza virus in ferrets immunized with seasonal influenza vaccine. J Virol. 2013 Mar; 87(6):3053-61. PMID: 23283953. doi: 10.1128/JVI. 02434-12
23. Lovgren Bengtsson K, Morein B, Osterhaus AD. ISCOM technology-based Matrix M adjuvant: success in future vaccines relies on formulation. Expert Rev Vaccines. 2011 Apr; 10(4):401-3. PMID: 21506635. doi: 10.1586/erv.11.25
24. Morein B, Sundquist B, Hoglund S, Dalsgaard K, Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature. 1984 Mar 29-Apr 4; 308 (5958):457-60. PMID: 6709052.
25. Radosevic K, Rodriguez A, Mintardjo R, Tax D, Bengtsson KL, Thompson C, et al. Antibody and T-cell responses to a virosomal adjuvanted H9N2 avian influenza vaccine: impact of distinct additional adjuvants. Vaccine. 2008 Jul 4; 26(29-30):3640-6. PMID: 18514980. doi: 10.1016/j.vaccine.2008.04.071
26. Pedersen G, Major D, Roseby S, Wood J, Madhun AS, Cox RJ. Matrix-M adjuvanted virosomal H5N1 vaccine confers protection against lethal viral challenge in a murine model. Influenza Other Respi Viruses. 2011 Nov; 5(6):426-37. PMID: 21668670.
27. Pedersen GK, Madhun AS, Breakwell L, Hoschler K, Sjursen H, Pathirana RD, et al. T-helper 1 cells elicited by H5N1 vaccination predict seroprotection. J Infect Dis. 2012 Jul 15; 206(2):158-66. PMID: 22551811. doi: 10.1093/infdis/jis330
28. Leigh MW, Connor RJ, Kelm S, Baum LG, Paulson JC. Receptor specificity of influenza virus influences severity of illness in ferrets. Vaccine. 1995; 13(15):1468-73. PMID: 8578828.
29. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. The American journal of pathology. 2007 Oct; 171(4):1215-23. PMID: 17717141. Pubmed Central PMCID: 1988871.
30. Smith H, Sweet C. Lessons for human influenza from pathogenicity studies with ferrets. Reviews of infectious diseases. 1988 Jan-Feb; 10(1):56-75. PMID: 3281223.
31. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, et al. Antibody recognition of a highly conserved influenza virus epitope. Science. 2009 Apr 10; 324(5924):246-51. PMID: 19251591. doi: 10.1126/science.1171491
32. Throsby M, van den Brink E, Jongeneelen M, Poon LL, Alard P, Cornelissen L, et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One. 2008; 3(12):e3942. PMID: 19079604. doi: 10.1371/journal.pone. 0003942
33. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science. 2011 Aug 12; 333(6044):843-50. PMID: 21737702. Pubmed Central PMCID: 3210727. doi: 10.1126/science.1204839
34. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, et al. Highly conserved protective epitopes on influenza B viruses. Science. 2012 Sep 14; 337(6100):1343-8. PMID: 22878502. Pubmed Central PMCID: 3538841. doi: 10.1126/science.1222908
35. Ekiert DC, Wilson IA. Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr Opin Virol. 2012 Apr; 2(2):134-41. PMID: 22482710. doi: 10.1016/j.coviro.2012.02.005
36. Friesen RH, Koudstaal W, Koldijk MH, Weverling GJ, Brakenhoff JP, Lenting PJ, et al. New class of monoclonal antibodies against severe influenza: prophylactic and therapeutic efficacy in ferrets. PLoS One. 2010; 5(2):e9106. PMID: 20161706. Pubmed Central PMCID: 2817000. doi: 10.1371/journal. pone.0009106
37. Doyle TM, Hashem AM, Li C, Domselaar GV, Larocque L, Wang J, et al. Universal Anti-Neuraminidase Antibody Inhibiting all Influenza A Subtypes. Antiviral Res. Sep 30. PMID: 24091204.
38. Johansson BE, Cox MM. Influenza viral neuraminidase: the forgotten antigen. Expert Rev Vaccines. 2011 Dec; 10(12):1683-95. PMID: 22085172. doi: 10.1586/erv.11.130
39. Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, Webby RJ. Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med. 2007 Feb; 4(2):e59. PMID: 17298168.
40. Wohlbold TJ, Krammer F. In the shadow of hemagglutinin: a growing interest in influenza viral neuraminidase and its role as a vaccine antigen. Viruses. 2014 Jun; 6(6):2465-94. PMID: 24960271. Pubmed Central PMCID: 4074938. doi: 10.3390/v6062465
41. Jegaskanda S, Vandenberg K, Laurie KL, Loh L, Kramski M, Winnall WR, et al. Cross-reactive influenza- specific antibody-dependent cellular cytotoxicity in intravenous immunoglobulin as a potential therapeutic against emerging influenza viruses. J Infect Dis. 2014 Jun 10. PMID: 24916185.
42. Jegaskanda S, Weinfurter JT, Friedrich TC, Kent SJ. Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques. J Virol. 2013 May; 87 (10):5512-22. PMID: 23468501. Pubmed Central PMCID: 3648138. doi: 10.1128/JVI.03030-12
43. Mischler R, Metcalfe IC. Inflexal V a trivalent virosome subunit influenza vaccine: production. Vaccine. 2002 Dec 20; 20 Suppl 5:B17-23. PMID: 12477413.
44. Kreijtz JH, Wiersma LC, De Gruyter HL, Vogelzang-van Trierum SE, van Amerongen G, Stittelaar KJ, et al. A Single Immunization With Modified Vaccinia Virus Ankara-Based Influenza Virus H7 Vaccine Affords Protection in the Influenza A(H7N9) Pneumonia Ferret Model. The Journal of infectious diseases. 2014 Sep 22. PMID: 25246535.
45. van den Brand JM, Stittelaar KJ, van Amerongen G, Rimmelzwaan GF, Simon J, de Wit E, et al. Severity of pneumonia due to new H1N1 influenza virus in ferrets is intermediate between that due to seasonal H1N1 virus and highly pathogenic avian influenza H5N1 virus. J Infect Dis. 2010 Apr 1; 201 (7):993-9. PMID: 20187747. doi: 10.1086/651132
46. Kreijtz JH, Kroeze EJ, Stittelaar KJ, de Waal L, van Amerongen G, van Trierum S, et al. Low pathogenic avian influenza A(H7N9) virus causes high mortality in ferrets upon intratracheal challenge: a model to study intervention strategies. Vaccine. 2013 Oct 9; 31(43):4995-9. PMID: 23816392. doi: 10.1016/j. vaccine.2013.06.071
47. Rimmelzwaan GF, Baars M, Claas EC, Osterhaus AD. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. Journal of virological methods. 1998 Sep; 74(1):57-66. PMID: 9763129.