1,588
Views
128
CrossRef citations to date
0
Altmetric
Review

Transient expression systems for plant-derived biopharmaceuticals

, , , , &
Pages 859-876 | Published online: 09 Jan 2014

References

  • Hammond RW, Nemchinov LG. Plant production of veterinary vaccines and therapeutics. Curr. Top. Microbiol. Immunol.332, 79–102 (2009).
  • Daniell H, Singh ND, Mason H, Streatfield SJ. Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci.14, 669–679 (2009).
  • Chebolu S, Daniell H. Chloroplast-derived vaccine antigens and biopharmaceuticals: expression, folding, assembly and functionality. Curr. Top. Microbiol. Immunol.332, 33–54 (2009).
  • Aviezer D, Brill-Almon E, Shaaltiel Y et al. A plant-derived recombinant human glucocerebrosidase enzyme – a preclinical and Phase I investigation. PLoS One4, e4792 (2009).
  • McCormick AA, Reddy S, Reinl SJ et al. Plant-produced idiotype vaccines for the treatment of non-Hodgkin’s lymphoma: safety and immunogenicity in a Phase I clinical study. Proc. Natl Acad. Sci. USA105, 10131–10136 (2008).
  • D’Aoust MA, Couture MM, Charland N et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J.8, 607–619 (2010).
  • Chichester JA, Haaheim LR, Yusibov V. Using plant cells as influenza vaccine substrates. Expert Rev. Vaccines8, 493–498 (2009).
  • Gleba Y, Klimyuk V, Marillonnet S. Magnifection – a new platform for expressing recombinant vaccines in plants. Vaccine23, 2042–2048 (2005).
  • Jones HD, Doherty A, Sparks CA. Transient transformation of plants. Methods Mol. Biol.513, 131–152 (2009).
  • Lico C, Chen Q, Santi L. Viral vectors for production of recombinant proteins in plants. J. Cell Physiol.216, 366–377 (2008).
  • Marusic C, Vitale A, Pedrazzini E et al. Plant-based strategies aimed at expressing HIV antigens and neutralizing antibodies at high levels. Nef as a case study. Transgenic Res.18, 499–512 (2009).
  • McCormick AA, Palmer KE. Genetically engineered tobacco mosaic virus as nanoparticle vaccines. Expert Rev. Vaccines7, 33–41 (2008).
  • Rybicki EP. Plant-produced vaccines: promise and reality. Drug Discov. Today14, 16–24 (2009).
  • Smith ML, Fitzmaurice WP, Turpen TH, Palmer KE. Display of peptides on the surface of tobacco mosaic virus particles.Curr. Top. Microbiol. Immunol.332, 13–31 (2009).
  • Yusibov V, Rabindran S. Recent progress in the development of plant derived vaccines. Expert Rev. Vaccines7, 1173–1183 (2008).
  • Vancanneyt G, Dubald M, Schröder W, Peters J, Botterman J. A case study for plant-made pharmaceuticals comparing different plant expression and production systems. Methods Mol. Biol.483, 209–221 (2009).
  • Komori T, Imayama T, Kato N et al. Current status of binary vectors and superbinary vectors. Plant Physiol.145, 1155–1160 (2007).
  • Lee LY, Gelvin SB. T-DNA binary vectors and systems. Plant Physiol.146, 325–332 (2008).
  • Goodin MM, Zaitlin D, Naidu RA, Lommel SA. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions.Mol. Plant Microbe Interact.21, 1015–1026 (2008).
  • Kim MJ, Baek K, Park CM. Optimization of conditions for transient Agrobacterium-mediated gene expression assays in Arabidopsis. Plant Cell Rep.28, 1159–1167 (2009).
  • Lee MW, Yang Y. Transient expression assay by agroinfiltration of leaves. Methods Mol. Biol.323, 225–229 (2006).
  • Negrouk V, Eisner G, Lee H et al. Highly efficient transient expression of functional recombinant antibodies in lettuce. Plant Sci.169, 433–438 (2005).
  • Medrano G, Reidy MJ, Liu J et al. Rapid system for evaluating bioproduction capacity complex pharmaceutical proteins in plants. Methods Mol. Biol.483, 51–67 (2009).
  • Simmons CW, VanderGheynst JS, Upadhyaya SK et al. A model of Agrobacterium tumefaciens vacuum infiltration into harvested leaf tissue and subsequent in planta transgene transient expression. Biotechnol. Bioeng.102, 965–970 (2009).
  • Tague BW, Mantis J. In planta Agrobacterium-mediated transformation by vacuum infiltration. Methods Mol. Biol.323, 215–223 (2006).
  • Azhakanandam K, Weissinger SM, Nicholson JS, Qu R, Weissinger AK. Amplicon-plus targeting technology (APTT) for rapid production of a highly unstable vaccine protein in tobacco plants. Plant Mol. Biol.63, 393–404 (2007).
  • 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.23, 718–723 (2005).
  • Lombardi R, Circelli P, Villani ME et al. High-level HIV-1 Nef transient expression in Nicotiana benthamiana using the P19 gene silencing suppressor protein of Artichoke mottled crinckle virus. BMC Biotechnol.96, 1–11 (2009).
  • Zheng N, Xia R, Yang C et al. Boosted expression of the SARS-CoV nucleocapsid protein in tobacco and its immunogenicity in mice. Vaccine27, 5001–5007 (2009).
  • Yang L, Wang H, Liu J et al. A simple and effective system for foreign gene expression in plants via root absorption of agrobacterial suspension. J. Biotechnol.134, 320–324 (2008).
  • Huang Z, Mason HS. Conformational analysis of hepatitis B surface antigen fusions in an Agrobacterium-mediated transient expression system. Plant Biotechnol. J.2, 241–249 (2004).
  • Lacorte C, Lohuis H, Goldbach R, Prins M. Assessing the expression of chicken anemia virus proteins in plants. Virus Res.129, 80–86 (2007).
  • Joensuu JJ, Conley AJ, Lienemann M et al. Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol.152, 622–633 (2009).
  • Gómez E, Zoth SC, Asurmendi S et al. Expression of hemagglutinin–neuraminidase glycoprotein of newcastle disease virus in agroinfiltrated Nicotiana benthamiana plants. J. Biotechnol.337–340 (2009).
  • Escribano JM, Perez-Filgueira DM. Strategies for improving vaccine antigens expression in transgenic plants: fusion to carrier sequences. Methods Mol. Biol.483, 275–287 (2009).
  • Obregon P, Chargelegue D, Drake et al. HIV-1 p24–immunoglobulin fusion molecule: a new strategy for plant-based protein production. Plant Biotechnol. J.4, 195–207 (2006).
  • Shadwick FS, Doran PM. Infection, propagation, distribution and stability of plant virus in hairy root cultures. J. Biotechnol.131, 318–329 (2007).
  • Shadwick FS, Doran PM. Propagation of plant viruses in hairy root cultures: a potential method for in vitro production of epitope vaccines and foreign proteins. Biotechnol. Bioeng.96, 570–583 (2007).
  • Skarjinskaia M, Karl J, Araujo A et al. Production of recombinant proteins in clonal root cultures using episomal expression vectors. Biotechnol. Bioeng.100, 814–819 (2008).
  • Ahlquist P, French R, Janda M, Loesch-Fries S. Multicomponent RNA plant virus infection derived from cloned viral cDNA. Proc. Natl Acad. Sci. USA81, 7066–7070 (1984).
  • Goelet P, Lomonossoff GP, Butler PJ, Akam ME, Gait MJ, Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proc. Natl Acad. Sci. USA79, 5818–5822 (1982).
  • Palukaitis P, Zaitlin M. The rod-shaped plant viruses. In: The Plant Viruses (Volume 2). Van Regenmortel M, Fraenkel-Conrat H (Eds). Plenum Press, NY, USA, 105–131 (1986).
  • Chapman SN. Construction of infectious clones for RNA viruses: TMV. Methods Mol. Biol.451, 477–490 (2008).
  • Marillonnet S, Giritch A, Gils M, Kandzia R, Klimyuk V, Gleba Y. In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium. Proc. Natl Acad. Sci. USA101, 6852–6857 (2004).
  • Dohi K, Tamai A, Mori M. Insertion in the coding region of the movement protein improves stability of the plasmid encoding a tomato mosaic virus-based expression vector. Arch. Virol.153, 1667–1675 (2008).
  • Dorokhov YL, Ivanov PA, Komarova TV et al. An internal ribosome entry site located upstream of the crTMV coat protein (CP) gene can be used for CP synthesis in vivo.J. Gen. Virol.87, 2693–2697 (2006).
  • Verchot-Lubicz J. A new cell-to-cell transport model for Potexviruses. Mol. Plant Microbe Interact.18, 283–290 (2005).
  • Verchot-Lubicz J, Ye CM, Bamunusinghe D. Molecular biology of potexviruses: recent advances. J. Gen. Virol.88, 1643–1655 (2007).
  • Baulcombe DC, Chapman S, Santa Cruz S. Jellyfish green fluorescent protein as a reporter for virus infections. Plant J.7, 1045–1053 (1995).
  • Mechtcheriakova IA, Eldarov MA, Nicholson L et al. The use of viral vectors to produce hepatitis B virus core particles in plants. J. Virol. Methods131, 10–15 (2006).
  • Avesani L, Marconi G, Morandini F et al. Stability of potato virus X expression vectors is related to insert size: implications for replication models and risk assessment. Transgenic Res.16, 587–597 (2007).
  • Giritch A, Marillonnet S, Engler C et al. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc. Natl Acad. Sci. USA103, 14701–14706 (2006).
  • Komarova TV, Skulachev MV, Zvereva AS, Schwartz AM, Dorokhov YL, Atabekov JG. New viral vector for efficient production of target proteins in plants. Biochemistry (Mosc.)71, 846–850 (2006).
  • Uhde K, Fischer R, Commandeur U. Expression of multiple foreign epitopes presented as synthetic antigens on the surface of potato virus X particles. Arch. Virol.150, 327–340 (2005).
  • Santa Cruz S, Chapman S, Roberts AG, Roberts IM, Prior DA, Oparka KJ. Assembly and movement of a plant virus carrying a green fluorescent protein overcoat. Proc. Natl Acad. Sci. USA93, 6286–6290 (1996).
  • Dolja VV, McBride HJ, Carrington JC. Tagging of plant potyvirus replication and movement by insertion of β-glucuronidase into the viralpolyprotein. Proc. Natl Acad. Sci. USA89, 10208–10212 (1992).
  • Varrelmann M, Maiss E. Mutations in the coat protein gene of plum pox virus suppress particle assembly, heterologous encapsidation and complementation in transgenic plants of Nicotiana benthamiana. J. Gen. Virol.81, 567–576 (2000).
  • Beauchemin C, Bougie V, Laliberté JF. Simultaneous production of two foreign proteins from a potyvirus-based vector. Virus Res.112, 1–8 (2005).
  • Kelloniemi J, Mäkinen K, Valkonen JP. Three heterologous proteins simultaneously expressed from a chimeric potyvirus: infectivity, stability and the correlation of genome and virion lengths.Virus Res.135, 282–291 (2008).
  • Zhao Y, Hammond J, Tousignant ME, Hammond RW. Development and evaluation of a complementation-dependent gene delivery system based on cucumber mosaic virus. Arch. Virol.145, 2285–2295 (2000).
  • Sudarshana MR, Plesha MA, Uratsu SL et al. A chemically inducible cucumber mosaic virus amplicon system for expression of heterologous proteins in plant tissues. Plant Biotechnol. J.4, 551–559 (2006).
  • Kim SH, Kalinina NO, Andreev I et al. The C-terminal 33 amino acids of the cucumber mosaic virus 3a protein affect virus movement, RNA binding and inhibition of infection and translation. J. Gen. Virol.85, 221–230 (2004).
  • Fujiki M, Kaczmarczyk JF, Yusibov V, Rabindran S. Development of a new cucumber mosaic virus-based plant expression vector with truncated 3a movement protein. Virology381, 136–142 (2008).
  • Green BJ, Fujiki M, Mett V et al. Transient protein expression in three Pisum sativum (green pea) varieties. Biotechnol. J.4, 230–237 (2009).
  • Sainsbury F, Liu L, Lomonossoff GP. Cowpea mosaic virus-based systems for the expression of antigens and antibodies in plants. Methods Mol. Biol.483, 25–39 (2009).
  • Gopinath K, Wellink J, Porta C, Taylor KM, Lomonossoff GP, van Kammen A. Engineering cowpea mosaic virus RNA-2 into a vector to express heterologous proteins in plants. Virology267, 159–173 (2000).
  • Liu L, Grainger J, Canizares MC, Angell SM, Lomonossoff GP. Cowpea mosaic virus RNA-1 acts as an amplicon whose effects can be counteracted by a RNA-2-encoded suppressor of silencing. Virology323, 37–48 (2004).
  • Sainsbury F, Lavoie PO, D’Aoust MA, Vézina LP, Lomonossoff GP. Expression of multiple proteins using full-length and deleted versions of cowpea mosaic virus RNA-2. Plant Biotechnol. J.6, 82–92 (2008).
  • Jeske H. Geminiviruses. Curr. Top. Microbiol. Immunol.331, 185–226 (2009).
  • Kim K, Sunter G, Bisaro DM, Chung IS. Improved expression of recombinant GFP using a replicating vector based on beet curly top virus in leaf-disks and infiltrated Nicotiana benthamiana leaves. Plant Mol. Biol.64, 103–112 (2007).
  • Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol. Bioeng.103, 706–714 (2009).
  • Dorokhov YL, Sheveleva AA, Frolova OY et al. Superexpression of tuberculosis antigens in plant leaves. Tuberculosis (Edinb.)87, 218–224 (2007).
  • Dorokhov YL, Frolova OY, Skurat EV et al. A novel function for a ubiquitous plant enzyme pectin methylesterase: the enhancer of RNA silencing. FEBS Lett.580, 3872–3878 (2006).
  • Gleba Y, Klimyuk V, Marillonnet S. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol.18, 134–141 (2007).
  • Engler C, Gruetzner R, Kandzia R, Marillonnet S. Golden gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS One4, e5553 (2009).
  • Santi L, Giritch A, Roy CJ et al. Protection conferred by recombinant Yersinia pestis antigens produced by a rapid and highly scalable plant expression system. Proc. Natl Acad. Sci. USA103, 861–866 (2006).
  • Wigdorovitz A, Pérez Fuilgueira DM, Robertson N et al. Protection of mice against challenge with Foot and mouth disease virus (FMDV) by immunization with foliar extracts from plants infected with recombinant Tobacco mosaic virus expressing the FMDV structural protein. Virology264, 85–91 (1999).
  • Mishra S, Yadav DK, Tuli R. Ubiquitin fusion enhances cholera toxin B subunit expression in transgenic plants and the plant-expressed protein binds GM1 receptors more efficiently. J. Biotechnol.127, 95–108 (2006).
  • Patel J, Zhu H, Menassa R, Gyenis L, Richman A, Brandle JE. Elastin-like polypeptide fusions enhance the accumulation of recombinant proteins in tobacco leaves. Transgenic Res.16, 239–249 (2007).
  • Goldman M, Lambert P-H. Immunological safety of vaccines: facts hypothesis and allegations. In: Novel Vaccination Strategies. Kaufmann SHE (Ed.). Wiley-VCH, Weinheim, Germany, 595–611 (2004).
  • Huang Z, Santi L, LePore K, Kilbourne J, Arntzen CJ, Mason HS. Rapid, high-level production of hepatitis B core antigen in plant leaf and its immunogenicity in mice. Vaccine24, 2506–2513 (2006).
  • Santi L, Batchelora L, Huanga Z et al. An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine26, 1846–1854 (2008).
  • D’Aoust MA, Lavoie PO, Couture MM et al. 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, 930–940 (2008).
  • Natilla A, Hammond RW, Nemchinov LG. Epitope presentation system based on cucumber mosaic virus coat protein expressed from a potato virus X-based vector. Arch. Virol.151, 1373–1386 (2006).
  • Saunders K, Sainsbury F, Lomonossoff GP. Efficient generation of cowpea mosaic virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology393, 329–337 (2009).
  • Cañizares MC, Nicholson L, Lomonossoff GP. Use of viral vectors for vaccine production in plants. Immunol. Cell. Biol.83, 263–270 (2005).
  • Molnár E, Dopfer EP, Deswal S, Schamel WW. Models of antigen receptor activation in the design of vaccines. Curr. Pharm. Des.15, 3237–3248 (2009).
  • Azizi A, Diaz-Mitoma F. Viral peptide immunogens: current challenges and opportunities. J. Pept. Sci.13, 776–786 (2007).
  • Knittelfelder R, Riemer AB, Jensen-Jarolim E. Mimotope vaccination-from allergy to cancer. Expert Opin. Biol. Ther.9, 493–506 (2009).
  • Sette A, Sidney J. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics50, 201–212 (1999).
  • Johnson J, Lin T, Lomonossoff G. Presentation of heterologous peptides on plant viruses: genetics, structure and function. Annu. Rev. Phytopathol.35, 67–86 (1997).
  • Bendahmane M, Koo M, Karrer E, Beachy RN. Display of epitopes on the surface of Tobacco mosaic virus: impact of charge and isoelectric point of the epitope on virus–host interaction. J. Mol. Biol.290, 9–20 (1999).
  • McCormick AA, Corbo TA, Wykoff-Clary S et al. TMV-peptide fusion vaccines induce cell-mediated immune responses and tumor protection in two murine models. Vaccine24, 6414–6423 (2006).
  • Li G, Jiang L, Li M et al. Morphology and stability changes of recombinant TMV particles caused by a cysteine residue in the foreign peptide fused to the coat protein. J. Virol. Methods140, 212–217 (2007).
  • Werner S, Marillonnet S, Hause G, Klimyuk V, Gleba Y. Immunoabsorbent nanoparticles based on a tobamovirus displaying protein A. Proc. Natl Acad. Sci. USA103, 17678–17683 (2006).
  • Lico C, Capuano F, Renzone G et al. Peptide display on potato virus X: molecular features of the coat protein-fused peptide affecting cell-to-cell and phloem movement of chimeric virus particles. J. Gen. Virol.87, 3103–3112 (2006).
  • Lico C, Mancini C, Italiani P et al. Plant-produced potato virus X chimeric particles displaying an influenza virus-derived peptide activate specific CD8+ T cells in mice. Vaccine27, 5069–5076 (2009).
  • De Muynck B, Navarre C, Boutry M. Production of antibodies in plants: status after twenty years. Plant Biotechnol. J.8, 529–563 (2010).
  • Ma JK, Drake PM, Chargelegue D, Obregon P, Prada A. Antibody processing and engineering in plants, and new strategies for vaccine production. Vaccine23, 1814–1818 (2005).
  • Ko K, Koprowski H. Plant biopharming of monoclonal antibodies. Virus Res.111, 93–100 (2005).
  • Brodzik R, Glogowska M, Bandurska K et al. Plant-derived anti-Lewis Y mAb exhibits biological activities for efficient immunotherapy against human cancer cells. Proc. Natl Acad. Sci. USA103, 8804–8809 (2006).
  • Hull AK, Criscuolo CJ, Mett V et al. Human-derived, plant-produced monoclonal antibody for the treatment of anthrax. Vaccine23, 2082–2086 (2005).
  • Orzaez, D, Mirabel S, Wieland WH, Granell A. Agroinjection of tomato fruits. A tool for rapid functional analysis of transgenes directly in fruit. Plant Physiol.140, 3–11 (2006).
  • Vaquero C, Sack M, Chandler J et al. Transient expression of a tumor-specific single-chain fragment and a chimeric antibody in tobacco leaves. Proc. Natl Acad. Sci USA96, 11128–11133 (1999).
  • Vézina LP, Faye L, Lerouge P et al. Transient co-expression for fast and high-yield production of antibodies with human-like N-glycans in plants. Plant Biotechnol. J.7, 442–455 (2009).
  • Villani MA, Morgun B, Brunetti P et al. Plant pharming of a full-sized, tumour-targeting antibody using different expression strategies. Plant Biotech. J.7, 59–72 (2009).
  • Lombardi R, Villani ME, Di Carli M, Brunetti P, Benvenuto E, Donini M. Optimisation of the purification process of a tumour-targeting antibody produced in N. benthamiana using vacuum-agroinfiltration. Transgenic Res. DOI: 10.1007/s11248–010–9382–9389 (2010) (Epub ahead of print)
  • Lai H, Engle M, Fuchs A et al. Monoclonal antibody produced in plants efficiently treats West Nile virus infection in mice. Proc. Natl Acad. Sci. USA107, 2419–2424 (2010).
  • Sainsbury F, Lomonossoff GP. Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol.148, 1212–1218 (2008).
  • Huang Z, Phoolcharoen W, Lai H et al. High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol. Bioeng.106, 9–17 (2010).
  • Yusibov V, Hooper DC, Spitsin SV et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine20, 3155–3164 (2002).
  • Tacket CC. Plant-based oral vaccines: results of human trials. Curr. Top. Microbiol. Immunol.332, 103–117 (2009).
  • Takagi H, Hiroi T, Yang L et al.A rice-based edible vaccine expressing multiple T cell epitopes induces oral tolerance for inhibition of Th2-mediated IgE responses. Proc. Natl Acad. Sci. USA102, 17525–17530 (2005).
  • Smart V, Foster PS, Rothenberg ME, Higgins TJ, Hogan SP. A plant-based allergy vaccine suppresses experimental asthma via an IFN-g and CD4+CD45RBlowT cell-dependent mechanism. J. Immunol.171, 2116–2126 (2003).
  • Tzfira T, Citovsky V. Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr. Opin. Biotechnol.17, 1–8 (2006).
  • Petrunia IV, Frolova OY, Komarova TV et al. Agrobacterium tumefaciens caused bacteraemia does not lead to GFP gene expression in mouse organs. PLoS One3, e2352 (2008).
  • Gomord V, Fitchette AC, Menu-Bouaouiche L et al. Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol. J.8, 564–587 (2010).
  • Meyers A, Chakauya E, Shephard E et al. Expression of HIV-1 antigens in plants as potential subunit vaccines. BMC Biotechnol.8, 53 (2008).
  • Maclean J, Koekemoer M, Olivier AJ et al. Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J. Gen. Virol.88, 1460–1469 (2007).
  • Karasev AV, Foulke S, Wellens C et al. Plant based HIV-1 vaccine candidate: Tat protein produced in spinach. Vaccine23, 1875–1880 (2005).
  • Varsani A, Williamson AL, Stewart D, Rybicki EP. Transient expression of human papillomavirus type 16 L1 protein in Nicotiana benthamiana using an infectious tobamovirus vector. Virus Res.120, 91–96 (2006).
  • Saejung W, Fujiyama K, Takasaki T et al. Production of dengue 2 envelope domain III in plant using TMV-based vector system. Vaccine25, 6646–6654. (2007).
  • Rabindran S, Stevenson N, Roy G et al. Plant-produced human growth hormone shows biological activity in a rat model. Biotechnol. Prog.25, 530–534 (2009).
  • Golovkin M, Spitsin S, Andrianov V et al. Smallpox subunit vaccine produced in planta confers protection in mice. Proc. Natl Acad. Sci. USA104, 6864–6869 (2007).
  • Webster DE, Wang L, Mulcair M et al. Production and characterization of an orally immunogenic Plasmodium antigen in plants using a virus-based expression system. Plant Biotechnol. J.7, 1–10 (2009).
  • Zelada AM, Calamante G, de la Paz Santangelo M et al. Expression of tuberculosis antigen ESAT-6 in Nicotiana tabacum using a potato virus X-based vector. Tuberculosis (Edinb.)86, 263–267 (2006).
  • Nemchinov LG, Liang TJ, Rifaat MM, Mazyad HM, Hadidi A, Keith JM. Development of a plant-derived subunit vaccine candidate against hepatitis C virus. Arch. Virol.145, 2557–2573 (2000).
  • Férnandez-Férnandez MR, Mourino M, Rivera J, Rodriguez F, Plana-Duran J, Garcia JA. Protection of rabbits against Rabbit hemorrhagic disease virus by immunization with the VP60 protein expressed in plants with a Potyvirus-based vector. Virology280, 283–291, (2001).
  • Franconi R, Di Bonito P, Dibello F et al. Plant-derived Human papillomavirus 16 E7 oncoprotein induces immune response and specific tumor protection. Cancer Res.62, 3654–3658 (2002).
  • Perez Filgueira DM, Zamorano PI, Dominguez MG et al. Bovine herpes virus gD protein produced in plants using a recombinant tobacco mosaic virus (TMV) vector possesses authentic antigenicity. Vaccine21, 4201–4209 (2003).
  • Verch T, Hooper DC, Kiyatkin A, Steplewski Z, Koprowski H. Immunization with a plant-produced colorectal cancer antigen. Cancer Immunol. Immunother.53, 92–99 (2004).
  • Clemente M, Curilovic R, Sassone A, Zelada A, Angel SO, Mentaberry AN. Production of the main surface antigen of Toxoplasma gondii in tobacco leaves and analysis of its antigenicity and immunogenicity. Mol. Biotechnol.30, 41–50 (2005).
  • Chichester JA, Musiychuk K, de la Rosa P et al. Immunogenicity of a subunit vaccine against Bacillus anthracis. Vaccine25, 3111–3114 (2007).
  • Massa S, Franconi R, Brandi R et al. Anti-cancer activity of plant-produced HPV16 E7 vaccine. Vaccine25, 3018–3021 (2007).
  • Mett V, Lyons J, Musiychuk K et al. A plant-produced plague vaccine candidate confers protection to monkeys. Vaccine25, 3014–3017 (2007).
  • Shoji Y, Bi H, Musiychuk K et al. Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine27, 1087–1092 (2009).
  • Shoji Y, Farrance CE, Bi H et al. 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. Vaccine27, 3467–3470 (2009).
  • Spitsin S, Andrianov V, Pogrebnyak N et al. Immunological assessment of plant-derived avian flu H5/HA1 variants. Vaccine27, 1289–1292 (2009).
  • Porta C, Spall VE, Loveleand J, Johnson JE, Barker PJ, Lomonossoff GP. Development of cowpea mosaic virus as a high-yielding system for the presentation of foreign peptides. Virology202, 949–955 (1994).
  • Dalsgaard K, Uttenthal A, Jones GB et al. Plant-derived vaccine protects target animals against a viral disease. Nat. Biotechnol.15, 248–252 (1997).
  • Joelson T, Akerblom L, Oxelfelt P, Strandberg B, Tomenius K, Morris TJ. Presentation of a foreign peptide on the surface of tomato bushy stunt virus. J. Gen. Virol.78, 1213–1217 (1997).
  • Yusibov V, Modelska A, Steplewski K et al. Antigens produced in plants by infection with chimeric plant viruses immunize against rabies virus and HIV-1. Proc. Natl Acad. Sci. USA94, 5784–5788 (1997).
  • Férnandez-Férnandez MR, Martinez-Torrecuadrada JL, Casal JI, Garcia JA. Development of an antigen presentation system based on plum pox potyvirus. FEBS Lett.427, 229–235 (1998).
  • Brennan FR, Jones TD, Longstaff M et al. Immunogenicity of peptides derived from a fibronectin-binding protein of S. aureus expressed on two different plant viruses. Vaccine17, 1846–1857 (1999).
  • Staczek J, Bendahmane M, Gilleland LB, Beachy RN, Gilleland HE Jr. Immunization with a chimeric tobacco mosaic virus containing an epitope of outer membrane protein F of Pseudomonas aeruginosa provides protection against challenge with P. aeruginosa. Vaccine18, 2266–2274 (2000).
  • Langeveld JPM, Brennan FR, Martinez-Torrecuadrada JL et al. Inactivated recombinant plant virus protects dogs from a lethal challenge with canine parvovirus. Vaccine19, 3661–3670 (2001).
  • Marusic C, Rizza P, Lattanzi L et al. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1.J. Virol.75, 8434–8439 (2001).
  • Natilla A, Piazzolla G, Nuzzaci M et al. Cucumber mosaic virus as carrier of a hepatitis C virus-derived epitope. Arch. Virol.149, 137–154 (2004).
  • Yusibov V, Mett V, Mett V et al. Peptide-based candidate vaccine against respiratory syncytial virus. Vaccine23, 2261–2265 (2005).
  • Marconi G, Albertini E, Barone P et al. In planta production of two peptides of the Classical swine fever virus (CSFV) E2 glycoprotein fused to the coat protein of potato virus X. BMC Biotechnol.6, 29 (2006).
  • Smith ML, Lindbo JA, Dillard-Telm S et al. Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology348, 475–488 (2006).
  • Meshcheryakova YA, Eldarov MA, Migunov AI et al. Cowpea mosaic virus chimeric particles bearing the ectodomain of matrix protein 2 (M2E) of the influenza A virus: production and characterization. Mol. Biol.43, 685–694 (2009).
  • Nuzzaci M, Vitti A, Condelli V et al. In vitro stability of cucumber mosaic virus nanoparticles carrying a hepatitis C virus-derived epitope under simulated gastrointestinal conditions and in vivo efficacy of an edible vaccine. J. Virol. Meth.165, 211–215 (2010).
  • Uhde-Holzem K, Schlössera V, Viazov S, Fischer R, Commandeur U. Immunogenic properties of chimeric potato virus X particles displaying the hepatitis C virus hypervariable region I peptide R9. J. Virol. Meth.166, 12–20 (2010).

Patents

  • Dorokhov YL, Komarova TV, Atabekov JG. Method of hyperproduction of target protein in a plant. WO2008063093 (2008).
  • Dorokhov YL, Komarova TV. Method for overproducing anti-HER2/Neu oncogene antibodies in plant. WO2009048354 (2009).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.