Protective efficacy of in vitro synthesized, specific mRNA vaccines against influenza A virus infection

Nature Biotechnology

Volumn 30, Issue 12, 2012, Pages 1210-1216

  Petsch, Benjamin ^a,b   Schnee, Margit ^b   Vogel, Annette B ^a   Lange, Elke ^a   Hoffmann, Bernd ^a   Voss, Daniel ^b   Schlake, Thomas ^b   Thess, Andreas ^b   Kallen, Karl Josef ^b   Stitz, Lothar ^a   Kramps, Thomas ^b  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b CureVac GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IN-VITRO; INFLUENZA A VIRUS; INFLUENZA VACCINES; MEDICAL NEEDS; PANDEMIC STRAINS; PROTECTIVE EFFECTS; PROTECTIVE EFFICACY; QUICK RESPONSE; VACCINOLOGY;

NUCLEIC ACIDS; VIRUSES;

VACCINES;

INFLUENZA VACCINE; VIRUS NUCLEOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; FERRET; IMMUNOGENICITY; IN VITRO STUDY; INFLUENZA A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; MALE; NONHUMAN; PRIORITY JOURNAL; SWINE; T LYMPHOCYTE; TEMPERATURE STRESS;

AGING; ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTES; BIOTECHNOLOGY; CROSS PROTECTION; FEMALE; FERRETS; HUMANS; INFLUENZA A VIRUS; INFLUENZA VACCINES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED DBA; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; RATS; RATS, INBRED LEW; RNA, MESSENGER; RNA, VIRAL; SUS SCROFA; T-LYMPHOCYTES; VACCINES, SYNTHETIC;

INFLUENZA A VIRUS; MUS; MUSTELA; SUIDAE;

EID: 84870869040     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2436     Document Type: Article

References (47)

1. Plotkin, S.A., Orenstein, W.A. & Offit, P.A. Vaccines: Expert Consult (Saunders, 2008).
2. Fiore, A.E. et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm. Rep. 59, 1-62 (2010).
3. Doherty, P.C., Turner, S.J., Webby, R.G. & Thomas, P.G. Influenza and the challenge for immunology. Nat. Immunol. 7, 449-455 (2006).
4. Salomon, R. & Webster, R.G. The influenza virus enigma. Cell 136, 402-410 (2009).
5. Knipe, D.M., Howley, P.M., Griffin, D.E., Lamb, R.A. & Martin, M.A. Fields Virology (Lippincott Williams & Wilkins, 2006).
6. Tong, S. et al. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 109, 4269-4274 (2012).
7. de Jong, J.C., Beyer, W.E., Palache, A.M., Rimmelzwaan, G.F. & Osterhaus, A.D. Mismatch between the 1997/1998 influenza vaccine and the major epidemic A(H3N2) virus strain as the cause of an inadequate vaccine-induced antibody response to this strain in the elderly. J. Med. Virol. 61, 94-99 (2000).
8. Ulmer, J.B., Valley, U. & Rappuoli, R. Vaccine manufacturing: challenges and solutions. Nat. Biotechnol. 24, 1377-1383 (2006).
9. Lambert, L.C. & Fauci, A.S. Influenza vaccines for the future. N. Engl. J. Med. 363, 2036-2044 (2010).
10. Nabel, G.J. & Fauci, A.S. Induction of unnatural immunity: prospects for a broadly protective universal influenza vaccine. Nat. Med. 16, 1389-1391 (2010).
11. Forde, G.M. Rapid-response vaccines - does DNA offer a solution? Nat. Biotechnol. 23, 1059-1062 (2005).
12. Liu, M.A. Immunologic basis of vaccine vectors. Immunity 33, 504-515 (2010).
13. Thalhamer, J., Weiss, R. & Scheiblhofer, S. Gene Vaccines (Springer, Wien and New York; 2011).
14. Hoerr, I., Obst, R., Rammensee, H.G. & Jung, G. In vivo application of RNA leads to induction of specific cytotoxic T lymphocytes and antibodies. Eur. J. Immunol. 30, 1-7 (2000).
15. Fotin-Mleczek, M. et al. Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity. J. Immunother. 34, 1-15 (2011).
16. Sebastian, M. et al. Messenger RNA vaccination in NSCLC: findings from a phase I/ IIa clinical trial. J. Clin. Oncol. 29 (suppl; abstr 2584) (2011).
17. Kübler, H. et al. Final analysis of a phase I/IIa study with CV9103, an intradermally administered prostate cancer immunotherapy based on self-adjuvanted mRNA. J. Clin. Oncol. 29 (suppl; abstr 4535) (2011).
18. Potter, C.W. & Oxford, J.S. Determinants of immunity to influenza infection in man. Br. Med. Bull. 35, 69-75 (1979).
19. Plotkin, S.A. Vaccines: correlates of vaccine-induced immunity. Clin. Infect. Dis. 47, 401-409 (2008).
20. Brown, D.M., Dilzer, A.M., Meents, D.L. & Swain, S.L. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J. Immunol. 177, 2888-2898 (2006).
21. + T cell response that predicts long-term persistence of protective antibody levels. Proc. Natl. Acad. Sci. USA 106, 3877-3882 (2009).
22. Hamada, H. et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J. Immunol. 182, 3469-3481 (2009).
23. + T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 18, 274-280 (2012).
24. 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, 1507-1515 (1997).
25. Boon, A.C.M. et al. 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 (2010).
26. McMichael, A.J., Gotch, F.M., Noble, G.R. & Beare, P.A. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309, 13-17 (1983).
27. Ulmer, J.B. et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259, 1745-1749 (1993).
28. Rimmelzwaan, G.F., Fouchier, R.A.M. & Osterhaus, A.D.M.E. Influenza virus-specific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr. Opin. Biotechnol. 18, 529-536 (2007).
29. Kistner, O. et al. A whole virus pandemic influenza H1N1 vaccine is highly immunogenic and protective in active immunization and passive protection mouse models. PLoS ONE 5, e9349 (2010).
30. Chaloupka, I., Schuler, A., Marschall, M. & Meier-Ewert, H. Comparative analysis of six European influenza vaccines. Eur. J. Clin. Microbiol. Infect. Dis. 15, 121-127 (1996).
31. Belshe, R.B. Translational research on vaccines: influenza as an example. Clin. Pharmacol. Ther. 82, 745-749 (2007).
32. van der Laan, J.W. et al. Animal models in influenza vaccine testing. Expert Rev. Vaccines 7, 783-793 (2008).
33. Van Reeth, K., Labarque, G., De Clercq, S. & Pensaert, M. Efficacy of vaccination of pigs with different H1N1 swine influenza viruses using a recent challenge strain and different parameters of protection. Vaccine 19, 4479-4486 (2001).
34. Pyo, H.-M. et al. Pandemic H1N1 influenza virus-like particles are immunogenic and provide protective immunity to pigs. Vaccine 30, 1297-1304 (2012).
35. Lefevre, E.A. et al. Immune responses in pigs vaccinated with adjuvanted and non-adjuvanted A(H1N1)pdm/09 influenza vaccines used in human immunization programmes. PLoS ONE 7, e32400 (2012).
36. Laurent, P.E. et al. Evaluation of the clinical performance of a new intradermal vaccine administration technique and associated delivery system. Vaccine 25, 8833-8842 (2007).
37. Dormitzer, P.R., Ulmer, J.B. & Rappuoli, R. Structure-based antigen design: a strategy for next generation vaccines. Trends Biotechnol. 26, 659-667 (2008).
38. Johansson, D.X., Ljungberg, K., Kakoulidou, M. & Liljeström, P. Intradermal electroporation of naked replicon RNA elicits strong immune responses. PLoS ONE 7, e29732 (2012).
39. Fotin-Mleczek, M. et al. Highly potent mRNA based cancer vaccines represent an attractive platform for combination therapies supporting an improved therapeutic effect. J. Gene Med. 14, 428-439 (2012).
40. Schlake, T. et al. Developing mRNA-vaccine technologies. RNA Biol. (in the press) (2012).
41. Pascolo, S. Vaccination with messenger RNA. Methods Mol. Med. 127, 23-40 (2006).
42. Pascolo, S. Vaccination with messenger RNA (mRNA). Handb. Exp. Pharmacol. 221-235 (2008) doi:10.1007/978-3-540-72167-3-11.
43. Reed, L.J. & Muench, H. A simple method of estimation of fifty percent end points. Am. J. Hyg. 27, 493-497 (1938).
44. Hai, R. et al. PB1-F2 expression by the 2009 pandemic H1N1 influenza virus has minimal impact on virulence in animal models. J. Virol. 84, 4442-4450 (2010).
45. Cobbold, S.P., Jayasuriya, A., Nash, A., Prospero, T.D. & Waldmann, H. Therapy with monoclonal antibodies by elimination of T-cell subsets in vivo. Nature 312, 548-551 (1984).
46. Lange, E. et al. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J. Gen. Virol. 90, 2119-2123 (2009).
47. Hoffmann, B. et al. New real-time reverse transcriptase polymerase chain reactions facilitate detection and differentiation of novel A/H1N1 influenza virus in porcine and human samples. Berl. Munch. Tierarztl. Wochenschr. 123, 286-292 (2010).