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Plant-Produced Avian Influenza Antigens

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Prospects of Plant-Based Vaccines in Veterinary Medicine

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Abstract

Avian influenza (AI) is a highly contagious respiratory disease that can also affect the enteric and nervous systems, causing a high degree of morbidity and mortality in animals and even in humans. Although current vaccines are effective against virus infection, new strategies need to be developed to satisfy the global demand for an AI vaccine. Plant-based expression systems can function as inexpensive platforms for the large scale production of recombinant pharmaceuticals or subunit vaccines. During the last decade, successful cases of influenza antigens production have been reported in plants, using both transient and stable expression systems. Full-length hemagglutinin (HA), as well as subunits thereof, has been produced in different compartments of the cell fused or not to other polypeptides. Immunizations of animals (mice, ferrets, rabbit, chickens and human) were performed with some of these plant-derived HA variants. These results demonstrate that plant-produced HA protein is antigenic and can induce immune response that correlate with protection against lethal AI virus. This paper reviews studies developed by several groups of researchers to improve the production of plant-based AI vaccines.

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References

  • Acha PN, Szyfres B (2003) Zoonoses and communicable diseases common to man and animals: parasitic zoonoses: Pan American Health Org

    Google Scholar 

  • Arcalis E, Ibl V, Peters J, Melnik S, Stoger E (2015) The dynamic behavior of storage organelles in developing cereal seeds and its impact on the production of recombinant proteins. Adv Seed Biol 118

    Google Scholar 

  • Azhakanandam K, Weissinger SM, Nicholson JS, Qu R, Weissinger AK (2007) Amplicon-plus targeting technology (APTT) for rapid production of a highly unstable vaccine protein in tobacco plants. Plant Mol Biol 63(3):393–404

    Article  CAS  PubMed  Google Scholar 

  • Barbazan P, Thitithanyanont A, Misse D, Dubot A, Bosc P, Luangsri N et al (2008) Detection of H5N1 avian influenza virus from mosquitoes collected in an infected poultry farm in Thailand. Vector-Borne Zoonotic Dis 8(1):105–110

    Article  PubMed  Google Scholar 

  • Ben Embarek P, Briand S, Brown I, Bruscke C, Domenech J, Formenty P et al (2009) FAO-OIE-WHO joint technical consultation on avian influenza at the human-animal interface. Influenza Other Respir Viruses 4:1–29

    Google Scholar 

  • Buyel JF (2015) Process development strategies in plant molecular farming. Curr Pharm Biotechnol 16(11):966–982

    Article  CAS  PubMed  Google Scholar 

  • Ceballo Y, Tiel K, López A, Cabrera G, Pérez M, Ramos O et al (2017) High accumulation in tobacco seeds of hemagglutinin antigen from avian (H5N1) influenza. Transgenic Res 26(6):775–789

    Article  CAS  PubMed  Google Scholar 

  • Chan HT, Daniell H (2015) Plant-made oral vaccines against human infectious diseases-are we there yet? Plant Biotechnol J 13(8):1056–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chichester JA, Jones RM, Green BJ, Stow M, Miao F, Moonsammy G et al (2012) Safety and immunogenicity of a plant-produced recombinant hemagglutinin-based influenza vaccine (HAI-05) derived from A/Indonesia/05/2005 (H5N1) influenza virus: a phase 1 randomized, double-blind, placebo-controlled, dose-escalation study in healthy adults. Viruses 4(11):3227–3244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke JL, Daniell H, Nugent JM (2011) Chloroplast biotechnology, genomics and evolution: current status, challenges and future directions. Plant Mol Biol 76(3):207–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cummings JF, Guerrero ML, Moon JE, Waterman P, Nielsen RK, Jefferson S et al (2014) Safety and immunogenicity of a plant-produced recombinant monomer hemagglutinin-based influenza vaccine derived from influenza A (H1N1) pdm09 virus: a Phase 1 dose-escalation study in healthy adults. Vaccine 32(19):2251–2259

    Article  CAS  PubMed  Google Scholar 

  • D’Aoust MA, Lavoie PO, Couture MMJ, Trépanier S, Guay JM, Dargis M et al (2008) Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol J 6(9):930–940

    Article  CAS  PubMed  Google Scholar 

  • D’Aoust MA, Couture MM, Charland N, Trepanier S, Landry N, Ors F et al (2010) The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J 8(5):607–619

    Article  CAS  PubMed  Google Scholar 

  • De Jaeger G, Scheffer S, Jacobs A, Zambre M, Zobell O, Goossens A et al (2002) Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat Biotechnol 20(12):1265–1268

    Article  CAS  PubMed  Google Scholar 

  • De Wilde K, De Buck S, Vanneste K, Depicker A (2013) Recombinant antibody production in Arabidopsis seeds triggers an unfolded protein response. Plant Physiol 161(2):1021–1033

    Article  CAS  PubMed  Google Scholar 

  • Du Y, Lou B, Wu Z, Zhao P, Cui Z (2012) Influence of antibody-mediated immune pressure on neuraminidase gene mutations of avian influenza virus H9N2. Bing du xue bao = Chin J Virol 28(1):1–6

    Google Scholar 

  • Fahad S, Khan FA, Pandupuspitasari NS, Ahmed MM, Liao YC, Waheed MT et al (2015) Recent developments in therapeutic protein expression technologies in plants. Biotechnol Lett 37(2):265–279

    Article  CAS  PubMed  Google Scholar 

  • FAO U (2016) Rational use of vaccination for prevention and control of H5 highly pathogenic avian influenza

    Google Scholar 

  • Farsad A, Malekzadeh-Shafaroudi S, Moshtaghi N, Fotouhi F, Zibaee S (2017) Transient Expression of HA1 Antigen of H5N1 Influenza Virus in Tobacco (Nicotiana tabacum L.) via Agro-infiltration. J Agric Sci Technol 19(2):439–451

    Google Scholar 

  • Ferguson NM, Cummings DA, Fraser C, Cajka JC, Cooley PC, Burke DS (2006) Strategies for mitigating an influenza pandemic. Nature 442(7101):448–452

    Article  CAS  PubMed  Google Scholar 

  • Firsov A, Tarasenko I, Mitiouchkina T, Ismailova N, Shaloiko L, Vainstein A et al (2015) High-yield expression of M2e peptide of avian influenza virus H5N1 in transgenic duckweed plants. Mol Biotechnol 57(7):653–661

    Article  CAS  PubMed  Google Scholar 

  • Floyd DL, Ragains JR, Skehel JJ, Harrison SC, van Oijen AM (2008) Single-particle kinetics of influenza virus membrane fusion. Proc National Acad Sci 105(40):15382–15387

    Article  Google Scholar 

  • Fujiuchi N, Matoba N, Matsuda R (2016) Environment control to improve recombinant protein yields in plants based on agrobacterium-mediated transient gene expression. Front Bioeng Biotechnol 4:23

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant–pathogen interactions. Mol Plant-Microbe Interact 21(8):1015–1026

    Article  CAS  PubMed  Google Scholar 

  • Hannoun C, Megas F, Piercy J (2004) Immunogenicity and protective efficacy of influenza vaccination. Virus Res 103(1):133–138

    Article  CAS  PubMed  Google Scholar 

  • Harfoot R, Webby RJ (2017) H5 influenza, a global update. J Microbiol 55(3):196–203

    Article  PubMed  Google Scholar 

  • Hernández A, López A, Ceballo Y, Rosabal L, Rosabal Y, Tiel K et al (2013) High-level production and aggregation of hepatitis B surface antigen in transgenic tobacco seeds. Biotecnol Apl 30:97–100

    Google Scholar 

  • Hernández-Velázquez A, López-Quesada A, Ceballo-Cámara Y, Cabrera-Herrera G, Tiel-González K, Mirabal-Ortega L et al (2015) Tobacco seeds as efficient production platform for a biologically active anti-HBsAg monoclonal antibody. Transgenic Res 24(5):897–909

    Article  CAS  PubMed  Google Scholar 

  • Hickling J, D’Hondt E (2006) A review of production technologies for influenza virus vaccines, and their suitability for deployment in developing countries for influenza pandemic preparedness. World Health Organization Initiative for Vaccine Research 1–34

    Google Scholar 

  • Hofbauer A, Melnik S, Tschofen M, Arcalis E, Phan HT, Gresch U et al (2016) The encapsulation of hemagglutinin in protein bodies achieves a stronger immune response in mice than the soluble antigen. Front Plant Sci 7:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu CJ, Chien CY, Liu MT, Fang ZS, Chang SY, Juang RH et al (2017) Multi-antigen avian influenza a (H7N9) virus-like particles: particulate characterizations and immunogenicity evaluation in murine and avian models. BMC Biotechnol 17(1):2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson LC, Garg R, Bost KL, Piller KJ (2014) Soybean seeds: a practical host for the production of functional subunit vaccines. Biomed Res Int 2014:340804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iowa State University Center for Food Security and Public Health, “Avian Influenza” (2016) Center for Food Security and Public Health. Technical Factsheets. 10. http://lib.dr.iastate.edu/cfsph_factsheets/10

  • Iyer V, Liyanage MR, Shoji Y, Chichester JA, Jones RM, Yusibov V et al (2012) Formulation development of a plant-derived h1n1 influenza vaccine containing purified recombinant hemagglutinin antigen. Human Vaccines Immunotherapeutics 8(4):453–464

    Article  CAS  PubMed  Google Scholar 

  • Joseph T, McAuliffe J, Lu B, Vogel L, Swayne D, Jin H et al (2008) A live attenuated cold-adapted influenza A H7N3 virus vaccine provides protection against homologous and heterologous H7 viruses in mice and ferrets. Virology 378(1):123–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jul-Larsen Å, Madhun AS, Brokstad KA, Montomoli E, Yusibov V, Cox RJ (2012) The human potential of a recombinant pandemic influenza vaccine produced in tobacco plants. Human Vaccines immunotherapeutics 8(5):653–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalthoff D, Giritch A, Geisler K, Bettmann U, Klimyuk V, Hehnen H-R et al (2010a) Immunization with plant-expressed hemagglutinin protects chickens from lethal highly pathogenic avian influenza virus H5N1 challenge infection. J Virol 84(22):12002–12010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalthoff D, Globig A, Beer M (2010b) (Highly pathogenic) avian influenza as a zoonotic agent. Vet Microbiol 140(3):237–245

    Article  PubMed  Google Scholar 

  • Kanagarajan S, Tolf C, Lundgren A, Waldenstrom J, Brodelius PE (2012) Transient expression of hemagglutinin antigen from low pathogenic avian influenza A (H7N7) in Nicotiana benthamiana. PLoS ONE 7(3):e33010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolpe A, Schepens B, Fiers W, Saelens X (2017) M2-based influenza vaccines: recent advances and clinical potential. Expert Rev Vaccines 16(2):123–136

    Article  CAS  PubMed  Google Scholar 

  • Landry N, Ward BJ, Trepanier S, Montomoli E, Dargis M, Lapini G et al (2010) Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS ONE 5(12):e15559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landry N, Pillet S, Favre D, Poulin J-F, Trépanier S, Yassine-Diab B et al (2014) Influenza virus-like particle vaccines made in Nicotiana benthamiana elicit durable, poly-functional and cross-reactive T cell responses to influenza HA antigens. Clin Immunol 154(2):164–177

    Article  CAS  PubMed  Google Scholar 

  • Le Mauff F, Mercier G, Chan P, Burel C, Vaudry D, Bardor M et al (2015) Biochemical composition of haemagglutinin-based influenza virus-like particle vaccine produced by transient expression in tobacco plants. Plant Biotechnol J 13(5):717–725

    Article  CAS  PubMed  Google Scholar 

  • Lee G, Na YJ, Yang BG, Choi JP, Seo YB, Hong CP et al (2015) Oral immunization of haemaggulutinin H5 expressed in plant endoplasmic reticulum with adjuvant saponin protects mice against highly pathogenic avian influenza A virus infection. Plant Biotechnol J 13(1):62–72

    Article  CAS  PubMed  Google Scholar 

  • Ling H-Y, Edwards AM, Gantier MP, DeBoer KD, Neale AD, Hamill JD et al (2012) An interspecific Nicotiana hybrid as a useful and cost-effective platform for production of animal vaccines. PLoS ONE 7(4):e35688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Major D, Chichester JA, Pathirana RD, Guilfoyle K, Shoji Y, Guzman CA et al (2015) Intranasal vaccination with a plant-derived H5 HA vaccine protects mice and ferrets against highly pathogenic avian influenza virus challenge. Hum Vaccin Immunother 11(5):1235–1243

    PubMed  PubMed Central  Google Scholar 

  • Mao H, Liu Y, Sia SF, Peiris JM, Lau Y-L, Tu W (2017) Avian influenza virus directly infects human natural killer cells and inhibits cell activity. Virologica Sinica 1–8

    Google Scholar 

  • Marangon S, Capua I (eds) (2005) Control of AI in Italy: from “Stamping-out”-strategy to emergency and prophylactic vaccination. Proc Internat Conf on Avian Influenza, Paris

    Google Scholar 

  • Mardanova ES, Kotlyarov RY, Kuprianov VV, Stepanova LA, Tsybalova LM, Lomonosoff GP et al (2015) 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 Biotechnol 15(1):42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mardanova ES, Blokhina EA, Tsybalova LM, Peyret H, Lomonossoff GP, Ravin NV (2017) Efficient transient expression of recombinant proteins in plants by the novel pEff vector based on the genome of potato virus X. Front Plant Sci 8:247

    Article  PubMed  PubMed Central  Google Scholar 

  • Marsian J, Lomonossoff GP (2016) Molecular pharming—VLPs made in plants. Curr Opin Biotechnol 37:201–206

    Article  CAS  PubMed  Google Scholar 

  • Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk H-D (2004) Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 78(22):12665–12667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina RA, García-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9(8):590–603

    Article  CAS  PubMed  Google Scholar 

  • Mett V, Musiychuk K, Bi H, Farrance CE, Horsey A, Ugulava N (2008) A plant-produced influenza subunit vaccine protects ferrets against virus challenge. Viruses 2

    Google Scholar 

  • Mortimer E, Maclean JM, Mbewana S, Buys A, Williamson A-L, Hitzeroth II et al (2012) Setting up a platform for plant-based influenza virus vaccine production in South Africa. BMC Biotechnol 12(1):14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nahampun HN, Bosworth B, Cunnick J, Mogler M, Wang K (2015) Expression of H3N2 nucleoprotein in maize seeds and immunogenicity in mice. Plant Cell Rep 34(6):969–980

    Article  CAS  PubMed  Google Scholar 

  • Nemchinov LG, Natilla A (2007) Transient expression of the ectodomain of matrix protein 2 (M2e) of avian influenza A virus in plants. Protein Expr Purif 56(2):153–159

    Article  CAS  PubMed  Google Scholar 

  • Neuhaus V, Chichester JA, Ebensen T, Schwarz K, Hartman CE, Shoji Y et al (2014) A new adjuvanted nanoparticle-based H1N1 influenza vaccine induced antigen-specific local mucosal and systemic immune responses after administration into the lung. Vaccine 32(26):3216–3222

    Article  CAS  PubMed  Google Scholar 

  • Nidom CA, Takano R, Yamada S, Sakai-Tagawa Y, Daulay S, Aswadi D et al (2010) Influenza A (H5N1) viruses from pigs, Indonesia. Emerg Infect Dis 16(10):1515

    Article  PubMed  PubMed Central  Google Scholar 

  • Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA (2006) Global patterns of influenza A virus in wild birds. Science 312(5772):384–388

    Article  CAS  PubMed  Google Scholar 

  • Peyret H, Lomonossoff GP (2015) When plant virology met Agrobacterium: the rise of the deconstructed clones. Plant Biotechnol J 13(8):1121–1135

    Article  PubMed  PubMed Central  Google Scholar 

  • Phan HT, Pohl J, Floss DM, Rabenstein F, Veits J, Le BT et al (2013) ELPylated haemagglutinins produced in tobacco plants induce potentially neutralizing antibodies against H5N1 viruses in mice. Plant Biotechnol J 11(5):582–593

    Article  CAS  PubMed  Google Scholar 

  • Phan HT, Hause B, Hause G, Arcalis E, Stoger E, Maresch D et al (2014) Influence of elastin-like polypeptide and hydrophobin on recombinant hemagglutinin accumulations in transgenic tobacco plants. PLoS ONE 9(6):e99347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pietrzak M, Macioła A, Zdanowski K, Protas-Klukowska AM, Olszewska M, Śmietanka K et al (2016) An avian influenza H5N1 virus vaccine candidate based on the extracellular domain produced in yeast system as subviral particles protects chickens from lethal challenge. Antiviral Res 133:242–249

    Article  CAS  PubMed  Google Scholar 

  • Pillet S, Racine T, Nfon C, Di Lenardo TZ, Babiuk S, Ward BJ et al (2015) Plant-derived H7 VLP vaccine elicits protective immune response against H7N9 influenza virus in mice and ferrets. Vaccine. 33(46):6282–6289

    Article  CAS  PubMed  Google Scholar 

  • Pillet S, Aubin E, Trepanier S, Bussiere D, Dargis M, Poulin JF et al (2016) A plant-derived quadrivalent virus like particle influenza vaccine induces cross-reactive antibody and T cell response in healthy adults. Clin Immunol 168:72–87

    Article  CAS  PubMed  Google Scholar 

  • Pose AG, Gomez JN, Sanchez AV, Redondo AV, Rodriguez ER, Segui RM et al (2011) Subunit influenza vaccine candidate based on CD154 fused to HAH5 increases the antibody titers and cellular immune response in chickens. Vet Microbiol 152(3–4):328–337

    Article  CAS  PubMed  Google Scholar 

  • Pua T-L, Chan XY, Loh H-S, Omar AR, Yusibov V, Musiychuk K et al (2017) Purification and immunogenicity of hemagglutinin from highly pathogenic avian influenza virus H5N1 expressed in Nicotiana benthamiana. Human Vaccines Immunotherapeutics 13:306–313

    Article  PubMed  Google Scholar 

  • Pushko P, Tretyakova I, Hidajat R, Zsak A, Chrzastek K, Tumpey TM et al (2017) Virus-like particles displaying H5, H7, H9 hemagglutinins and N1 neuraminidase elicit protective immunity to heterologous avian influenza viruses in chickens. Virology 501:176–182

    Article  CAS  PubMed  Google Scholar 

  • Ravin NV, Kotlyarov RY, Mardanova ES, Kuprianov VV, Migunov AI, Stepanova LA (2012) Plant-produced recombinant influenza vaccine based on virus-like HBc particles carrying an extracellular domain of M2 protein. Biochem (Mosc) 77(1):33–44

    Article  CAS  Google Scholar 

  • Redkiewicz P, Sirko A, Kamel KA, Góra-Sochacka A (2014) Plant expression systems for production of hemagglutinin as a vaccine against influenza virus. Acta Biochim Pol 61(3):551–560

    PubMed  Google Scholar 

  • Rossi L, Pinotti L, Agazzi A, Dell’Orto V, Baldi A (2014) Plant bioreactors for the antigenic hook-associated flgK protein expression. Ital J Anim Sci 13(1)

    Article  CAS  Google Scholar 

  • Sack M, Hofbauer A, Fischer R, Stoger E (2015) The increasing value of plant-made proteins. Curr Opin Biotechnol 32:163–170

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682–693

    Article  CAS  PubMed  Google Scholar 

  • Shoji Y, Chichester JA, Bi H, Musiychuk K, de la Rosa P, Goldschmidt L et al (2008) Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 26(23):2930–2934

    Article  CAS  PubMed  Google Scholar 

  • Shoji Y, Farrance CE, Bi H, Shamloul M, Green B, Manceva S et al (2009a) Immunogenicity of hemagglutinin from A/Bar-headed Goose/Qinghai/1A/05 and A/Anhui/1/05 strains of H5N1 influenza viruses produced in Nicotiana benthamiana plants. Vaccine 27(25–26):3467–3470

    Article  CAS  PubMed  Google Scholar 

  • Shoji Y, Bi H, Musiychuk K, Rhee A, Horsey A, Roy G et al (2009b) Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine 27(7):1087–1092

    Article  CAS  PubMed  Google Scholar 

  • Shoji Y, Chichester JA, Jones M, Manceva SD, Damon E, Mett V (2011) Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccines 7:41–50

    Article  CAS  Google Scholar 

  • Shoji Y, Jones RM, Mett V, Chichester JA, Musiychuk K, Sun X et al (2013) A plant-produced H1N1 trimeric hemagglutinin protects mice from a lethal influenza virus challenge. Human Vaccines Immunotherapeutics 9(3):553–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoji Y, Prokhnevsky A, Leffet B, Vetter N, Tottey S, Satinover S et al (2015) Immunogenicity of H1N1 influenza virus-like particles produced in Nicotiana benthamiana. Hum Vaccin Immunother 11(1):118–123

    Article  PubMed  Google Scholar 

  • Sievert K, Avarez R, Cortada R, Valks M (2006) House flies carrying avian influenza virus (AIV). Int Pest Control 48(3):114–116

    Google Scholar 

  • Sims L, Domenech J, Benigno C, Kahn S, Kamata A, Lubroth J et al (2005) Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet Rec 157(6):159

    Article  CAS  PubMed  Google Scholar 

  • Spackman E (2008) A brief introduction to the avian influenza virus. Avian Influenza Virus 1–6

    Google Scholar 

  • Spitsin S, Andrianov V, Pogrebnyak N, Smirnov Y, Borisjuk N, Portocarrero C et al (2009) Immunological assessment of plant-derived avian flu H5/HA1 variants. Vaccine 27(9):1289–1292

    Article  CAS  PubMed  Google Scholar 

  • Stachyra A, Pietrzak M, Maciola A, Protasiuk A, Olszewska M, Smietanka K et al (2017) A prime/boost vaccination with HA DNA and Pichia-produced HA protein elicits a strong humoral response in chickens against H5N1. Virus Res 232:41–47

    Article  CAS  PubMed  Google Scholar 

  • Stephenson I, Wood J, Nicholson K, Zambon M (2003) Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol 70(3):391–398

    Article  CAS  PubMed  Google Scholar 

  • Suguitan AL Jr, McAuliffe J, Mills KL, Jin H, Duke G, Lu B et al (2006) Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 3(9):e360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Topp E, Irwin R, McAllister T, Lessard M, Joensuu JJ, Kolotilin I et al (2016) The case for plant-made veterinary immunotherapeutics. Biotechnol Adv 34:597–604

    Article  PubMed  Google Scholar 

  • Treanor JJ, Chu L, Essink B, Muse D, El Sahly HM, Izikson R et al (2017) Stable emulsion (SE) alone is an effective adjuvant for a recombinant, baculovirus-expressed H5 influenza vaccine in healthy adults: a Phase 2 trial. Vaccine 35(6):923–928

    Article  CAS  PubMed  Google Scholar 

  • Vamvaka E, Twyman RM, Murad AM, Melnik S, Teh AYH, Arcalis E et al (2016) Rice endosperm produces an underglycosylated and potent form of the HIV-neutralizing monoclonal antibody 2G12. Plant Biotechnol J 14(1):97–108

    Article  CAS  PubMed  Google Scholar 

  • Van Droogenbroeck B, Cao J, Stadlmann J, Altmann F, Colanesi S, Hillmer S et al (2007) Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc National Acad Sci 104(4):1430–1435

    Article  CAS  Google Scholar 

  • Veits J, Wiesner D, Fuchs W, Hoffmann B, Granzow H, Starick E et al (2006) Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc National Acad Sci 103(21):8197–8202

    Article  CAS  Google Scholar 

  • Velkers FC, Blokhuis SJ, Veldhuis Kroeze EJ, Burt SA (2017) The role of rodents in Avian Influenza outbreaks in poultry farms: a review. Vet Q 37(1):182–194

    Article  PubMed  Google Scholar 

  • Vittecoq M, Gauduin H, Oudart T, Bertrand O, Roche B, Guillemain M et al (2017) Modeling the spread of avian influenza viruses in aquatic reservoirs: a novel hydrodynamic approach applied to the Rhône delta (southern France). Sci Total Environ 595:787–800

    Article  CAS  PubMed  Google Scholar 

  • Wanaratana S, Panyim S, Pakpinyo S (2011) The potential of house flies to act as a vector of avian influenza subtype H5N1 under experimental conditions. Med Vet Entomol 25(1):58–63

    Article  CAS  PubMed  Google Scholar 

  • Ward BJ, Landry N, Trépanier S, Mercier G, Dargis M, Couture M et al (2014) Human antibody response to N-glycans present on plant-made influenza virus-like particle (VLP) vaccines. Vaccine 32(46):6098–6106

    Article  CAS  PubMed  Google Scholar 

  • Yang W-T, Yang G-L, Wang Q, Huang H-B, Jiang Y-L, Shi C-W et al (2017) Protective efficacy of Fc targeting conserved influenza virus M2e antigen expressed by Lactobacillus plantarum. Antiviral Res 138:9–21

    Article  CAS  PubMed  Google Scholar 

  • Zheng M, Luo J, Chen Z (2014) Development of universal influenza vaccines based on influenza virus M and NP genes. Infection 42(2):251–262

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Plant Biotechnology Department, Center for Genetic Engineering and Biotechnology (CIGB), PO Box 6162, 10600, Havana, Cuba

    Yanaysi Ceballo, Alina Lopez, Kenia Tiel & Abel Hernandez

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  1. Yanaysi Ceballo
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  2. Alina Lopez
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  3. Kenia Tiel
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  4. Abel Hernandez
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Correspondence to Yanaysi Ceballo .

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  1. Western University, London, Ontario, Canada

    Jacqueline MacDonald

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Ceballo, Y., Lopez, A., Tiel, K., Hernandez, A. (2018). Plant-Produced Avian Influenza Antigens. In: MacDonald, J. (eds) Prospects of Plant-Based Vaccines in Veterinary Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-90137-4_8

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