Rapid high-yield expression of a candidate influenza vaccine based on the ectodomain of M2 protein linked to flagellin in plants using viral vectors

BMC Biotechnology

Volumn 15, Issue 1, 2015, Pages

  Mardanova, Eugenia S ^a   Kotlyarov, Roman Y ^a   Kuprianov, Victor V ^a   Stepanova, Liudmila A ^b   Tsybalova, Liudmila M ^b   Lomonosoff, George P ^c   Ravin, Nikolai V ^a  

^a INSTITUTE OF BIOENGINEERING   (Russian Federation)

^b N N BLOKHIN NATIONAL MEDICAL RESEARCH CENTER OF ONCOLOGY   (Russian Federation)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

Flagellin; Influenza; M2 protein; Potato virus X; Vaccine; Viral vector

Indexed keywords

PLANTS (BOTANY); PROTEINS; SALMONELLA; VACCINES; VECTORS; VIRUSES;

EXTRACELLULAR DOMAINS; FLAGELLIN; INFLUENZA; INTRANASAL IMMUNIZATIONS; POTATO VIRUS X; POTATO VIRUS X-BASED VECTORS; SALMONELLA TYPHIMURIUM; VIRAL VECTORS;

RECOMBINANT PROTEINS;

FLAGELLIN; FLG 4M PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; INFLUENZA VACCINE; PROTEIN M2; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS VECTOR; M2 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIGENICITY; ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; COWPEA MOSAIC VIRUS; FEMALE; GENE EXPRESSION SYSTEM; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA; INFLUENZA VACCINATION; MOUSE; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT LEAF; PLANT TISSUE; POTATO VIRUS X; PROTEIN EXPRESSION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; BIOSYNTHESIS; CHEMISTRY; COMOVIRUS; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; METABOLISM; ORTHOMYXOVIRIDAE INFECTIONS; PHYSIOLOGY; PLANT VIRUS; POTEXVIRUS; TOBACCO; VIROLOGY;

BACTERIA (MICROORGANISMS); COWPEA MOSAIC VIRUS; INFLUENZA A VIRUS; MUS; NICOTIANA BENTHAMIANA; ORTHOMYXOVIRIDAE; POTATO VIRUS X; SALMONELLA TYPHIMURIUM;

ADMINISTRATION, INTRANASAL; ANIMALS; COMOVIRUS; FLAGELLIN; GENETIC VECTORS; HUMANS; INFLUENZA VACCINES; MICE; ORTHOMYXOVIRIDAE INFECTIONS; PLANT VIRUSES; POTEXVIRUS; RECOMBINANT PROTEINS; SALMONELLA TYPHIMURIUM; TOBACCO; VIRAL MATRIX PROTEINS;

EID: 84930506399     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/s12896-015-0164-6     Document Type: Article

References (42)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992;56:152-79.
2. Fiers W, De Filette M, El Bakkouri K, Schepens B, Roose K, Schotsaert M, et al. M2e-based universal influenza A vaccine. Vaccine. 2009;27:6280-3.
3. Fiers W, De Filette M, Birkett A, Neirynck S, Min Jou W. A "universal" human influenza A vaccine. Virus Res. 2004;103:173-6.
4. Ito T, Gorman OT, Kawaoka Y, Bean WJ, Webster RG. Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol. 1991;65:5491-8.
5. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med. 1999;5:1157-63.
6. Feng J, Zhang M, Mozdzanowska K, Zharikova D, Hoff H, Wunner W, et al. Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2. Virol J. 2006;3:102.
7. Liu W, Peng Z, Liu Z, Lu Y, Ding J, Chen YH. High-epitope density in a single recombinant protein molecule of the extracellular domain of influenza A virus M2 protein significantly enhances protective immunity. Vaccine. 2004;2:366-71.
8. Mozdzanowska K, Feng J, Eid M, Kragol G, Cudic M, Otvos L, et al. Induction of influenza type A virus-specific resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2. Vaccine. 2003;21(19-20):2616-26.
9. Ravin NV, Kotlyarov RY, Mardanova ES, Kuprianov VV, Migunov AI, Stepanova LA, et al. Plant-produced recombinant influenza vaccine based on virus-like HBc particles carrying an extracellular domain of M2 protein. Biochemistry (Mosc). 2012;77:33-40.
10. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004;5:987-95.
11. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335-76.
12. McDonald WF, Huleatt JW, Foellmer HG, Hewitt D, Tang J, Desai P, et al. A West Nile virus recombinant protein vaccine that co-activates innate and adaptive immunity. J Infect Dis. 2007;195:1607-17.
13. Huleatt JW, Nakaar V, Desai P, Huang Y, Hewitt D, Jacobs A, et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine. 2008;26:201-14.
14. Jeon SH, Ben-Yedidia T, Arnon R. Intranasal immunization with synthetic recombinant vaccine containing multiple epitopes of influenza virus. Vaccine. 2002;20:2772-80.
15. Hong SH, Byun Y-H, Nguyen CT, Kim SY, Seong BL, Park S, et al. Intranasal administration of flagellin-adjuvanted inactivated influenza vaccine enhances mucosal immune responses to protect mice against lethal infection. Vaccine. 2012;30:466-74.
16. Liu G, Tarbet B, Song L, Reiserova L, Weaver B, Chen Y, et al. Immunogenicity and efficacy of flagellin-fused vaccine candidates targeting 2009 pandemic H1N1 influenza in mice. PLoS One. 2011;6:e20928.
17. Liu G, Song L, Reiserova L, Trivedi U, Li H, Liu X, et al. Flagellin-HA vaccines protect ferrets and mice against H5N1 highly pathogenic avian influenza virus (HPAIV) infections. Vaccine. 2012;30:6833-8.
18. Song L, Zhang Y, Yun NE, Poussard AL, Smith JN, Smith JK, et al. Superior efficacy of a recombinant flagellin: H5N1 HA globular head vaccine is determined by the placement of the globular head within flagellin. Vaccine. 2009;27:5875-84.
19. Wang B-Z, Xu R, Quan F-S, Kang SM, Wang L, Compans RW. Intranasal immunization with influenza VLPs incorporating membrane-anchored flagellin induces strong heterosubtypic protection. PLoS One. 2010;5:e13972.
20. Gleba Y, Klimyuk V, Marillonnet S. Viral vectors for the expression of proteins in plants. Curr Opin Biotechnol. 2007;18:134-41.
21. Lico C, Chen Q, Santi L. Vectors for production of recombinant proteins in plants. J Cell Physiol. 2008;216:366-77.
22. Thuenemann EC, Lenzi P, Love AJ, Taliansky M, Becares M, Zuniga S, et al. The use of transient expression systems for the rapid production of virus-like particles in plants. Curr Pharm Des. 2013;19:5564-73.
23. Edelbaum O, Stein D, Holland N, Gafni Y, Livneh O, Novick D, et al. Expression of active human interferon-β in transgenic plants. J Interferon Res. 1992;12:449-53.
24. Kusnadi AR, Nikolov ZL, Howard JA. Production of recombinant proteins in transgenic plants: practical considerations. Biotechnol Bioeng. 1997;56:473-84.
25. Kapila J, De Rycke R, van Montagu M, Angenon G. An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci. 1997;122:101-8.
26. Marillonnet S, Thoeringer C, Kandzia R, Klimyuk V, Gleba Y. Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat Biotechnol. 2005;23:718-23.
27. Cañizares MC, Nicholson L, Lomonossoff GP. Use of viral vectors for vaccine production in plants. Immunol Cell Biol. 2005;83:263-70.
28. Chichester JA, Yusibov V. Plants as alternative systems for production of vaccines. Hum Vaccines. 2007;3:146-9.
29. D'Aoust MA, Couture MM, Charland N, Trepanier S, Landry N, Ors F, et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J. 2010;8:607-19.
30. Mett V, Musiychuk K, Bi H, Farrance CE, Horsey A, Ugulava N, et al. A plant-produced influenza subunit vaccine protects ferrets against virus challenge. Viruses. 2008;2:33-40.
31. Shoji Y, Chichester JA, Jones M, Manceva SD, Damon E, Mett V. Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccines. 2011;7:41-50.
32. Mardanova ES, Kotliarov RIu, Ravin NV. Increased efficiency of recombinant proteins production in plants due to optimized translation of RNA of viral vector. Mol Biol (Mosk). 2009;43(3):568-71.
33. Sainsbury F, Lomonossoff GP. Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol. 2008;148:1212-8.
34. Sainsbury F, Thuenemann EC, Lomonossoff GP. pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J. 2009;7:682-93.
35. De Filette M, Fiers W, Martens W, Birkett A, Ramne A, Löwenadler B, et al. Improved design and intranasal delivery of an M2e-based human influenza A vaccine. Vaccine. 2006;24:6597-601.
36. Blokhina EA, Kuprianov VV, Stepanova LA, Tsybalova LM, Kiselev OI, Ravin NV, et al. A molecular assembly system for presentation of antigens on the surface of HBc virus-like particles. Virology. 2013;435:293-300.
37. Matić S, Masenga V, Poli A, Rinaldi R, Milne RG, Vecchiati M, et al. Comparative analysis of recombinant Human Papillomavirus 8L1 production in plants by a variety of expression systems and purification methods. Plant Biotechnol J. 2012;10:410-21.
38. Girard A, Saron W, Bergeron-Sandoval LP, Sarhan F, Archambault D. Flagellin produced in plants is a potent adjuvant for oral immunization. Vaccine. 2011;29:6695-703.
39. Stepanova L, Kotlyarov R, Kovaleva A, Potapchuk M, Korotkov A, Sergeeva M, et al. Protection against multiple influenza A virus strains induced by candidate recombinant vaccine based on heterologous M2e peptides linked to flagellin. PLoS One. 2015;10(3):e0119520.
40. Matić S, Rinaldi R, Masenga V, Noris E. Efficient production of chimeric human papillomavirus 16L1 protein bearing the M2e influenza epitope in Nicotiana benthamiana plants. BMC Biotechnol. 2011;11:106.
41. Petukhova NV, Gasanova TV, Stepanova LA, Rusova OA, Potapchuk MV, Korotkov AV, et al. Immunogenicity and protective efficacy of candidate universal influenza A nanovaccines produced in plants by tobacco mosaic virus-based vectors. Curr Pharm Des. 2013;19:5587-600.
42. Chiba M, Reed JC, Prokhnevsky AI, Chapman EJ, Mawassi M, Koonin EV, et al. Diverse suppressors of RNA silencing enhance agroinfection by a viral replicon. Virology. 2006;346:7-14.