Skip to main content
SpringerLink
Log in

125 years of virology and ascent of biotechnologies based on viral expressio

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

The study of viruses lasts for more than a century since their discovery in 1892. In recent decades, viruses are also being actively exploited as a biotechnological tool. Plant-virus-driven transient expression of heterologous proteins is an actively developing production platform; it is the basis of several industrial processes that are currently being used for the production of multiple recombinant proteins. Viral vectors have also become useful tools for research. Viral vectors delivered by Agrobacterium (magnifection) provide for high protein yield, rapid scale up and fast manufacturing. In this review, we explore modern approaches for biotechnological production of recombinant proteins in plants using viral vectors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Iwanowski, D., Über die Mosaikkrankheit der Tabakpflanze, Bull. Acad. Imp. Sci. St. Petersbourg, Nouv. Ser. III, 1892, vol. 35, pp. 67–70.

    Google Scholar 

  2. Lechevalier, H., Dmitri Iosifovich Ivanovski, Bacteriol. Rev., 1972, vol. 36, no. 2, pp. 135–145.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Stanley, W.M., Soviet studies on viruses, Science, 1944, vol. 99, pp. 136–138.

    Article  CAS  PubMed  Google Scholar 

  4. Lustig, A. and Levine, A.J., One hundred years of virology, J. Virol., 1992, vol. 6, pp. 4629–4631.

    Google Scholar 

  5. Gallie, D.R., Sleat, D.E., Watts, J.W., Turner, P.C., and Wilson, T.M.A., The 59-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo, Nucleic Acids Res., 1987, vol. 15, pp. 3257–3273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Creager, A.N.H., Scholthof, K.-B.G., Citovsky, V., and Scholthof, H.B., Tobacco mosaic virus: pioneering research for a century, Plant Cell, 1999, vol. 11, pp. 301–308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gleba, Y., Klimyuk, V., and Marillonnet, S., Viral vectors for the expression of proteins in plants, Curr. Opin. Biotechnol., 2007, vol. 18, pp. 134–141.

    Article  CAS  PubMed  Google Scholar 

  8. Gleba, Y., Marillonnet, S., and Klimyuk, V., Plant virus vectors (gene expression systems), in Encyclopedia of Virology, 3rd ed., van Regenmortel, M.H.V. and Mahy, B.W.J., Eds., San Diego, CA: Elsevier Academic Press, 2008, vol. 4, pp. 155–192.

    Google Scholar 

  9. Gleba, Y.Y., Tusé, D., and Giritch, A., Plant viral vectors for delivery by Agrobacterium, Curr. Top. Microbiol. Immunol., 2014, vol. 375, pp. 155–192.

    CAS  PubMed  Google Scholar 

  10. Canizares, M.C., Lomonossoff, G.P., and Nicholson, L., Development of cowpea mosaic virus-based vectors for the production of vaccines in plants, Expert Rev. Vaccines, 2005, vol. 4, pp. 687–697.

    Article  CAS  PubMed  Google Scholar 

  11. Canizares, M.C., Nicholson, L., and Lomonossoff, G.P., Use of viral vectors for vaccine production in plants, Immunol. Cell. Biol., 2005, vol. 83, pp. 263–270.

    Article  CAS  PubMed  Google Scholar 

  12. McCormick, A.A. and Palmer, K.E., Genetically engineered tobacco mosaic virus as nanoparticle vaccines, Expert. Rev. Vaccines, 2008, vol. 7, pp. 33–41.

    Article  CAS  PubMed  Google Scholar 

  13. Lico, C., Chen, Q., and Santi, L., Viral vectors for production of recombinant proteins in plants, J. Cell Physiol., 2008, vol. 216, pp. 366–377.

    Article  CAS  PubMed  Google Scholar 

  14. Yusibov, V. and Rabindran, S., Recent progress in the development of plant derived vaccines, Expert Rev. Vaccines, 2008, vol. 7, pp. 1173–1183.

    Article  PubMed  Google Scholar 

  15. Mett, V., Farrance, C.E., Green, B.J., and Yusibov, V., Plants as biofactories, Biologicals, 2008, vol. 36, pp. 354–358.

    Article  PubMed  Google Scholar 

  16. Rybicki, E.P., Plant-produced vaccines: promise and reality, Drug. Discov. Today, 2009, vol. 14, pp. 16–24.

    Article  CAS  PubMed  Google Scholar 

  17. Daniell, H., Singh, N.D., Mason, H., and Streatfield, S.J., Plant-made vaccine antigens and biopharmaceuticals, Trends Plant Sci., 2009, vol. 14, pp. 669–679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Smith, M.L., Fitzmaurice, W.P., Turpen, T.H., and Palmer, K.E., Display of peptides on the surface of tobacco mosaic virus particles, Curr. Top. Microbiol. Immunol., 2009, vol. 332, pp. 13–31.

    CAS  PubMed  Google Scholar 

  19. Karg, S.R. and Kallio, P.T., The production of biopharmaceuticals in plant systems, Biotechnol. Adv., 2009, vol. 27, pp. 879–894.

    Article  CAS  PubMed  Google Scholar 

  20. Sainsbury, F., Liu, L., and Lomonossoff, G.P., Cowpea mosaic virus-based systems for the expression of antigens and antibodies in plants, Methods Mol. Biol., 2009, vol. 483, pp. 25–39.

    Article  CAS  PubMed  Google Scholar 

  21. Lomonossoff, G.P. and D’Aoust, M.-A., Plant-produced biopharmaceuticals: a case of technical developments driving clinical deployment, Science, 2016, vol. 353, pp. 1237–1240.

    Article  CAS  PubMed  Google Scholar 

  22. Tschofen, M., Knopp, D., Hood, E., and Stoger, E., Plant molecular farming: much more than medicines, Annu. Rev. Anal. Chem., 2016, vol. 9, pp. 271–294.

    Article  Google Scholar 

  23. Gleba, Y., Marillonnet, S., and Klimyuk, V., Engineering viral expression vectors for plants: the ‘full virus’ and the ‘deconstructed virus’ strategies, Curr. Opin. Plant Biol., 2004, vol. 7, pp. 182–188.

    Article  CAS  PubMed  Google Scholar 

  24. Donson, J., Kearney, C.M., Hilf, M.E., and Dawson, W.O., Systemic expression of a bacterial gene by a tobacco mosaic virus-based vector, Proc. Natl. Acad. Sci. U. S. A., 1991, vol. 88, pp. 7204–7208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Turpen, T.H., Reinl, S.J., Charoenvit, Y., Hoffman, S.L., Fallarme, V., and Grill, L.K., Malarial epitopes expressed on the surface of recombinant tobacco mosaic virus, Biotechnology (New York), 1995, vol. 13, pp. 53–57.

    Article  CAS  Google Scholar 

  26. Shivprasad, S., Pogue, G.P., Lewandowski, D.J., Hidalgo, J., Donson, J., Grill, L.K., and Dawson, W.O., Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors, Virology, 1999, vol. 255, pp. 312–323.

    Article  CAS  PubMed  Google Scholar 

  27. Turpen, T.H., Tobacco mosaic virus and the virescence of biotechnology, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 1999, vol. 354, pp. 665–673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. McCormick, A.A., Kumagai, M.H., Hanley, K., Turpen, T.H., Hakim, I., Grill, L.K., Tusé, D., Levy, S., and Levy, R., Rapid production of specific vaccines for lymphoma by expression of the tumor-derived singlechain Fv epitopes in tobacco plants, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 703–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. McCormick, A.A., Reinl, S.J., Cameron, T.I., Vojdani, F., Fronefield, M., Levy, R., and Tusé, D., Individualized human scFv vaccines produced in plants: humoral anti-idiotype responses in vaccinated mice confirm relevance to the tumor Ig, J. Immunol. Methods, 2003, vol. 278, pp. 95–104.

    Article  CAS  PubMed  Google Scholar 

  30. McCormick, A.A., Reddy, S., Reinl, S.J., Cameron, T.I., Czerwinkski, D.K., Vojdani, F., Hanley, K.M., Garger, S.J., White, E.L., Novak, J., Barrett, J., Holtz, R.B., Tusé, D., and Levy, R., 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. U. S. A., 2008, vol. 105, pp. 10131–10136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kumagai, M.H., Turpen, T.H., Weinzettl, N., Cioppa, G., Turpen, A.M., Donson, J., Hilf, M.E., Grantham, G.L., Dawson, W.O., Chow, T.P., Piatak, M., Jr., and Grill, L.K., Rapid, high-level expression of biologically active alpha-trichosanthin in transfected plants by an RNA viral vector, Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, pp. 427–430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kumagai, M.H., Donson, J., Cioppa, G., Harvey, D., Hanley, K., and Grill, L.K., Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA, Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, pp. 1679–1683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kumagai, M.H., Donson, J., Cioppa, G., and Grill, L.K., Rapid, high-level expression of glycosylated rice alpha-amylase in transfected plants by an RNA viral vector, Gene, 2000, vol. 245, pp. 169–174.

    Article  CAS  PubMed  Google Scholar 

  34. Rabindran, S. and Dawson, W.O., Assessment of recombinants that arise from the use of a TMV-based transient expression vector, Virology, 2001, vol. 284, pp. 182–189.

    Article  CAS  PubMed  Google Scholar 

  35. Lindbo, J.A., High-efficiency protein expression in plants from agroinfection-compatible tobacco mosaic virus expression vectors, BMC Biotechnol., 2007, vol. 7, article52.

  36. O’Keefe, B.R., Vojdani, F., Buffa, V., Shattock, R.J., Montefiori, D.C., Bakke, J., Mirsalis, J., d’Andrea, A.L., Hume, S.D., Bratcher, B., Saucedo, C.J., McMahon, J.B., Pogue, G.P., and Palmer, K.E., Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 6099–6104.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Marillonnet, S., Giritch, A., Gils, M., Kandzia, R., Klimyuk, V., and Gleba, Y., In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, pp. 6852–6857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Marillonnet, S., Thoeringer, C., Kandzia, R., Klimyuk, V., and Gleba, Y., Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants, Nat. Biotechnol., 2005, vol. 23, pp. 718–723.

    Article  CAS  PubMed  Google Scholar 

  39. Gleba, Y., Klimyuk, V., and Marillonnet, S., Magnifection— a new platform for expressing recombinant vaccines in plants, Vaccine, 2005, vol. 23, pp. 2042–2048.

    Article  CAS  PubMed  Google Scholar 

  40. Gils, M., Kandzia, R., Marillonnet, S., Klimyuk, V., and Gleba, Y., High-yield production of authentic human growth hormone using a plant virus-based expression system, Plant Biotechnol. J., 2005, vol. 3, pp. 613–620.

    Article  CAS  PubMed  Google Scholar 

  41. Giritch, A., Marillonnet, S., Engler, C., van Eldik, G., Botterman, J., Klimyuk, V., and Gleba, Y., Rapid highyield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 14701–14706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Huang, Z., Santi, L., LePore, K., Kilbourne, J., Arntzen, C.J., and Mason, H.S., Rapid, high-level production of hepatitis B core antigen in plant leaf and its immunogenicity in mice, Vaccine, 2006, vol. 24, pp. 2506–2513.

    Article  CAS  PubMed  Google Scholar 

  43. Santi, L., Giritch, A., Roy, C.J., Marillonnet, S., Klimyuk, V., Gleba, Y., Webb, R., Arntzen, C.J., and Mason, H.S., Protection conferred by recombinant Yersinia pestis antigens produced by a rapid and highly scalable plant expression system, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 861–866.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Santi, L., Batchelor, L., Huang, Z., Hjelm, B., Kilbourne, J., Arntzen, C.J., Chen, Q., and Mason, H.S., An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles, Vaccine, 2008, vol. 26, pp. 1846–1854.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Webster, D.E., Wang, L., Mulcair, M., Ma, C., Santi, L., Mason, H.S., Wesselingh, S.L., and Coppel, R.L., Production and characterization of an orally immunogenic Plasmodium antigen in plants using a virus-based expression system, Plant Biotechnol. J., 2009, vol. 7, pp. 846–855.

    Article  CAS  PubMed  Google Scholar 

  46. Vancanneyt, G., Dubald, M., Schroder, W., Peters, J., and Botterman, J., A case study for plant-made pharmaceuticals comparing different plant expression and production systems, Methods Mol. Biol., 2009, vol. 483, pp. 209–221.

    Article  CAS  PubMed  Google Scholar 

  47. Bendandi, M., Marillonnet, S., Kandzia, R., Thieme, F., Nickstadt, A., Herz, S., Frode, R., Inoges, S., Lopez-Diaz de Cerio, A., Soria, E., Villanueva, H., Vancanneyt, G., McCormick, A., Tusé, D., Lenz, J., Butler-Ransohoff, J.E., Klimyuk, V., and Gleba, Y., Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin’s lymphoma, Ann. Oncol., 2010, vol. 21, pp. 2420–2427.

    Article  CAS  PubMed  Google Scholar 

  48. Werner, S., Marillonnet, S., Hause, G., Klimyuk, V., and Gleba, Y., Immunoabsorbent nanoparticles based on a tobamovirus displaying protein A, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 17678–17683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lindbo, J.A., TRBO: a high-efficiency tobacco mosaic virus RNA-based overexpression vector, Plant Physiol., 2007, vol. 145, pp. 1232–1240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Dorokhov, Y.L., Sheveleva, A.A., Frolova, O.Y., Komarova, T.V., Zvereva, A.S., Ivanov, P.A., and Atabekov, J.G., Superexpression of tuberculosis antigens in plant leaves, Tuberculosis (Edinb.), 2007, vol. 87, pp. 218–224.

    Article  CAS  Google Scholar 

  51. Maclean, J., Koekemoer, M., Olivier, A.J., and Stewart, D., Hitzeroth, I.I., Rademacher, T., Fischer, R., Williamson, A.L., and Rybicki, E.P., 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., 2007, vol. 88, pp. 1460–1469.

    Article  CAS  PubMed  Google Scholar 

  52. Sainsbury, F. and Lomonossoff, G.P., Extremely high-level and rapid transient protein production in plants without the use of viral replication, Plant Physiol., 2008, vol. 148, pp. 1212–1218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Fujiki, M., Kaczmarczyk, J.F., Yusibov, V., and Rabindran, S., Development of a new cucumber mosaic virus-based plant expression vector with truncated 3a movement protein, Virology, 2008, vol. 381, pp. 136–142.

    Article  CAS  PubMed  Google Scholar 

  54. Green, B.J., Fujiki, M., Mett, V., Kaczmarczyk, J., Shamloul, M., Musiychuk, K., Underkoffler, S., Yusibov, V., and Mett, V., Transient protein expression in three Pisum sativum (green pea) varieties, Biotechnol. J., 2009, vol. 4, pp. 230–237.

    Article  CAS  PubMed  Google Scholar 

  55. Huang, Z., Chen, Q., Hjelm, B., Arntzen, C., and Mason, H., A DNA replicon system for rapid highlevel production of virus-like particles in plants, Biotechnol. Bioeng., 2009, vol. 103, pp. 706–714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Vezina, L.P., Faye, L., Lerouge, P., D’Aoust, M.A., Marquet-Blouin, E., Burel, C., Lavoie, P.O., Bardor, M., and Gomord, V., Transient co-expression for fast and high-yield production of antibodies with humanlike nglycans in plants, Plant Biotechnol. J., 2009, vol. 7, pp. 442–455.

    Article  CAS  PubMed  Google Scholar 

  57. Huang, Z., Phoolcharoen, W., Lai, H., Piensook, K., Cardineau, G., Zeitlin, L., Whaley, K.J., Arntzen, C.J., Mason, H.S., and Chen, Q., High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system, Biotechnol. Bioeng., 2009, vol. 106, pp. 9–17.

    Google Scholar 

  58. Zvereva, A.S., Petrovskaya, L.E., Rodina, A.V., Frolova, O.Y., Ivanov, P.A., Shingarova, L.N., Komarova, T.V., Dorokhov, Y.L., Dolgikh, D.A., Kirpichnikov, M.P., and Atabekov, J.G., Production of biologically active human myelocytokines in plants, Biochemistry (Mosc.), 2009, vol. 74, pp. 1187–1194.

    Article  CAS  Google Scholar 

  59. Kalthoff, D., Giritch, A., Geisler, K., Bettmann, U., Klimyuk, V., Hehnen, H.R., Gleba, Y., and Beer, M., Immunization with plant-expressed hemagglutinin protects chickens from lethal highly pathogenic avian influenza virus H5N1 challenge infection, J. Virol., 2010, vol. 84, pp. 12002–12010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Joensuu, J.J., Conley, A.J., Lienemann, M., Brandle, J.E., Linder, M.B., and Menassa, R., Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana, Plant Physiol., 2010, vol. 152, no. 2, pp. 622–633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Noris, E., Poli, A., Cojoca, R., Rittè, M., Cavallo, F., Vaglio, S., Matic, S., and Landolfo, S., A human papillomavirus 8 E7 protein produced in plants is able to trigger the mouse immune system and delay the development of skin lesions, Arch. Virol., 2011, vol. 156, no. 4, pp. 587–595.

    Article  CAS  PubMed  Google Scholar 

  62. Kanagarajan, S., Tolf, C., Lundgren, A., Waldenström, J., and Brodelius, P.E., Transient expression of hemagglutinin antigen from low pathogenic avian influenza A (H7N7) in Nicotiana benthamiana, PLoS One, 2012, vol. 7, p. e33010.

    Google Scholar 

  63. Hamorsky, K.T., Grooms-Williams, T.W., Husk, A.S., Bennett, L.J., Palmer, K.E., and Matoba, N., Efficient single tobamoviral vector-based bioproduction of broadly neutralizing anti-HIV-1 monoclonal antibody VRC01 in Nicotiana benthamiana plants and utility of VRC01 in combination microbicides, Antimicrob. Agents Chemother., 2013, vol. 57, no. 5, pp. 2076–2086.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hahn, S., Giritch, A., Bartels, D., Bortesi, L., and Gleba, Y., A novel and fully scalable Agrobacterium spray-based process for manufacturing cellulases and other cost-sensitive proteins in plants, Plant Biotechnol. J., 2015, vol. 13, no. 5, pp. 708–716.

    Article  CAS  PubMed  Google Scholar 

  65. Schulz, S., Stephan, A., Hahn, S., Bortesi, L., Jarczowski, F., Bettmann, U., Paschke, A.-K., Tusé, D., Stahl, C.H., Giritch, A., and Gleba, Y., Broad and efficient control of major food-borne pathogenic strains of Escherichia coli by mixtures of plant-produced colicins, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, no. 40, pp. E5454–E5460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Moore, L., Hamorsky, K., and Matoba, N., Production of recombinant cholera toxin b subunit in Nicotiana benthamiana using GENEWARE® tobacco mosaic virus vector, Methods Mol. Biol., 2016, vol. 1385, pp. 129–137.

    Article  PubMed  Google Scholar 

  67. Sainsbury, F., Jutras, P.V., Vorster, J., Goulet, M.C., and Michaud, D.A., Chimeric affinity tag for efficient expression and chromatographic purification of heterologous proteins from plants, Front. Plant Sci., 2016, no. 7, article141.

  68. Yadav, N.S., Postle, K., Saiki, R.K., Thomashow, M.F., and Chilton, M.-D., T-DNA of a crown gall teratoma is covalently joined to host plant DNA, Nature, 1980, vol. 287, pp. 458–461.

    Article  CAS  PubMed  Google Scholar 

  69. Willmitzer, L., De Beuckeleer, M., Lemmers, M., Van Montagu, M., and Schell, J., DNA from Ti plasmid present in nucleus and absent from plastids of crown gall plant cells, Nature, 1980, vol. 287, pp. 359–361.

    Article  CAS  Google Scholar 

  70. Gelvin, S.B., Agrobacterium virulence gene induction, Methods Mol. Biol., 2006, vol. 343, pp. 77–84.

    CAS  PubMed  Google Scholar 

  71. Gelvin, S.B., Agrobacterium-mediated DNA transfer, and then some, Nat. Biotechnol., 2008, vol. 26, pp. 998–1000.

    Article  CAS  Google Scholar 

  72. Gelvin, S.B., Agrobacterium in the genomics age, Plant Physiol., 2009, vol. 150, pp. 1665–1676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gelvin, S.B., Plant proteins involved in Agrobacteriummediated genetic transformation, Annu. Rev. Phytopathol., 2010, vol. 48, pp. 45–68.

    Article  CAS  PubMed  Google Scholar 

  74. Gelvin, S.B., Traversing the cell: Agrobacterium T-DNA’s journey to the host genome, Front. Plant Sci., 2012, vol. 3, article52.

  75. Citovsky, V., Kozlovsky, S.V., Lacroix, B., Zaltsman, A., Dafny-Yelin, M., Vyas, S., Tovkach, A., and Tzfira, T., Biological systems of the host cell involved in Agrobacterium infection, Cell Microbiol., 2007, vol. 9, pp. 9–20.

    Article  CAS  PubMed  Google Scholar 

  76. Dafny-Yelin, M., Levy, A., and Tzfira, T., The ongoing saga of Agrobacterium-host interactions, Trends Plant Sci., 2008, vol. 13, pp. 102–105.

    Article  CAS  PubMed  Google Scholar 

  77. Christie, P.J. and Gordon, J.E., The Agrobacterium Ti plasmids, Microbiol. Spectrum, 2014, vol. 2, no. 6. doi 10.1128/microbiolspec.PLAS-0010-2013

    Google Scholar 

  78. Bourras, S., Rouxel, T., and Meyer, M., Agrobacterium tumefaciens gene transfer: how a plant pathogen hacks the nuclei of plant and nonplant organisms, Phytopathology, 2015, vol. 105, no. 10, pp. 1288–1301.

    Article  CAS  PubMed  Google Scholar 

  79. Lacroix, B. and Citovsky, V., Transfer of DNA from bacteria to eukaryotes, MBio, 2016, vol. 12, no. 4, p. e00863-16.

    Google Scholar 

  80. Fraley, R.T., Rogers, S.G., Horsch, R.B., Sanders, P.R., Flick, J.S., Adams, S.P., Bittner, M.L., Brand, L.A., Fink, C.L., Fry, J.S., Galluppi, G.R., Goldberg, S.B., Hoffmann, N.L., and Woo, S.C., Expression of bacterial genes in plant cells, Proc. Natl. Acad. Sci. U. S. A., 1983, vol. 80, pp. 4803–4807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Barton, K.A., Binns, A.N., Matzke, A.J., and Chilton, M.D., Regeneration of intact tobacco plants containing full length copies of genetically engineered TDNA, and transmission of T-DNA to R1 progeny, Cell, 1983, vol. 32, pp. 1033–1043.

    Article  CAS  PubMed  Google Scholar 

  82. Koo, M., Bendahmane, M., Lettieri, G.A., Paoletti, A.D., Lane, T.E., Fitchen, J.H., Buchmeier, M.J., and Beachy, R.N., Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carries an MHV epitope, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 7774–7779.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Wu, L., Jiang, L., Zhou, Z., Fan, J., Zhang, Q., Zhu, H., Han, Q., and Xu, Z., Expression of foot-and-mouth disease virus epitopes in tobacco by a tobacco mosaic virus-based vector, Vaccine, 2003, vol. 21, pp. 4390–4398.

    Article  CAS  PubMed  Google Scholar 

  84. McCormick, A.A., Corbo, T.A., Wykoff-Clary, S., Nguyen, L.V., Smith, M.L., Palmer, K.E., and Pogue, G.P., TMV-peptide fusion vaccines induce cellmediated immune responses and tumor protection in two murine models, Vaccine, 2006, vol. 24, pp. 6414–6423.

    Article  CAS  PubMed  Google Scholar 

  85. Kohl, T., Hitzeroth, II, Stewart, D., Varsani, A., Govan, V.A., Christensen, N.D., Williamson, A.L., and Rybicki, E.P., Plant-produced cottontail rabbit papillomavirus L1 protein protects against tumor challenge: a proof-of-concept study, Clin. Vaccine Immunol., 2006, vol. 13, pp. 845–853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Chichester, J.A., Musiychuk, K., de la Rosa, P., Horsey, A., Stevenson, N., Ugulava, N., Rabindran, S., Palmer, G.A., Mett, V., and Yusibov, V., Immunogenicity of a subunit vaccine against Bacillus anthracis, Vaccine, 2007, vol. 25, pp. 3111–3114.

    Article  CAS  PubMed  Google Scholar 

  87. Mett, V., Lyons, J., Musiychuk, K., Chichester, J.A., Brasil, T., Couch, R., Sherwood, R., Palmer, G.A., Streatfield, S.J., and Yusibov, V., A plant-produced plague vaccine candidate confers protection to monkeys, Vaccine, 2007, vol. 25, pp. 3014–3017.

    Article  CAS  PubMed  Google Scholar 

  88. Golovkin, M., Spitsin, S., Andrianov, V., Smirnov, Y., Xiao, Y., Pogrebnyak, N., Markley, K., Brodzik, R., Gleba, Y., Isaacs, S.N., and Koprowski, H., Smallpox subunit vaccine produced in planta confers protection in mice, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, pp. 6864–6869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Massa, S., Franconi, R., Brandi, R., Muller, A., Mett, V., Yusibov, V., and Venuti, A., Anti-cancer activity of plant-produced HPV16 E7 vaccine, Vaccine, 2007, vol. 25, pp. 3018–3021.

    Article  CAS  PubMed  Google Scholar 

  90. Yang, C.D., Liao, J.T., Lai, C.Y., Jong, M.H., Liang, C.M., Lin, Y.L., Lin, N.S., Hsu, Y.H., and Liang, S.M., Induction of protective immunity in swine by recombinant bamboo mosaic virus expressing foot-and-mouth disease virus epitopes, BMC Biotechnol., 2007, vol. 7, article62.

  91. Meyers, A., Chakauya, E., Shephard, E., Tanzer, F.L., Maclean, J., Lynch, A., Williamson, A.L., and Rybicki, E.P., Expression of HIV-1 antigens in plants as potential subunit vaccines, BMC Biotechnol., 2008, vol. 8, article53.

  92. Shoji, Y., Chichester, J.A., Bi, H., Musiychuk, K., de la Rosa, P., Goldschmidt, L., Horsey, A., Ugulava, N., Palmer, G.A., Mett, V., and Yusibov, V., Plant-expressed HAas a seasonal influenza vaccine candidate, Vaccine, 2008, vol. 26, pp. 2930–2934.

    Article  CAS  PubMed  Google Scholar 

  93. Shoji, Y., Farrance, C.E., Bi, H., Shamloul, M., Green, B., Manceva, S., Rhee, A., Ugulava, N., Roy, G., Musiychuk, K., Chichester, J.A., Mett, V., and Yusibov, V., Immunogenicity of hemagglutinin from A/Barheaded Goose/Qinghai/1A/05 and A/Anhui/1/05 strains of H5N1 influenza viruses produced in Nicotiana benthamiana plants, Vaccine, 2009, vol. 27, pp. 3467–3470.

    Article  CAS  PubMed  Google Scholar 

  94. D’Aoust, M.A., Lavoie, P.O., Couture, M.M., Trepanier, S., Guay, J.M., Dargis, M., Mongrand, S., Landry, N., Ward, B.J., and Vezina, L.P., 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., 2008, vol. 6, no. 9, pp. 930–940.

    Article  PubMed  CAS  Google Scholar 

  95. Hamorsky, K.T., Kouokam, J.C., Bennett, L.J., Baldauf, K.J., Kajiura, H., Fujiyama, K., and Matoba, N., Rapid and scalable plant-based production of a cholera toxin B subunit variant to aid in mass vaccination against cholera outbreaks, PLoS Negl. Trop. Dis., 2013, vol. 7, p. e2046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Chichester, J.A., Manceva, S.D., Rhee, A., Coffin, M.V., Musiychuk, K., Mett, V., Shamloul, M., Norikane, J., Streatfield, S.J., and Yusibov, V., A plant-produced protective antigen vaccine confers protection in rabbits against a lethal aerosolized challenge with Bacillus anthracis Ames spores, Hum. Vaccin. Immunother., 2013, vol. 9, pp. 544–552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Thuenemann, E.C., Meyers, A.E., Verwey, J., Rybicki, E.P., and Lomonossoff, G.P., A method for rapid production of heteromultimeric protein complexes in plants: assembly of protective bluetongue virus-like particles, Plant Biotechnol. J., 2013, vol. 11, no. 7, pp. 839–846.

    Article  CAS  PubMed  Google Scholar 

  98. Pillet, S., Racine, T., Nfon, C., Di Lenardo, T.Z., Babiuk, S., Ward, B.J., Kobinger, G.P., and Landry, N., Plant-derived H7 VLP vaccine elicits protective immune response against H7N9 influenza virus in mice and ferrets, Vaccine, 2015, vol. 33, no. 46, pp. 6282–6289.

    Article  CAS  PubMed  Google Scholar 

  99. Hiatt, A., Cafferkey, R., and Bowdish, K., Production of antibodies in transgenic plants, Nature, 1989, vol. 342, pp. 76–78.

    Article  CAS  PubMed  Google Scholar 

  100. Ma, J.K., Hiatt, A., Hein, M., Vine, N.D., Wang, F., Stabila, P., van Dolleweerd, C., Mostov, K., and Lehner, T., Generation and assembly of secretory antibodies in plants, Science, 1995, vol. 268, pp. 716–719.

    Article  CAS  PubMed  Google Scholar 

  101. Hiatt, A. and Pauly, M., Monoclonal antibodies from plants: a new speed record, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 14645–14646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Mori, M., Fujihara, N., Mise, K., and Furusawa, I., Inducible high-level mRNA amplification system by viral replicase in transgenic plants, Plant J., 2001, vol. 27, no. 1, pp. 79–86.

    Article  CAS  PubMed  Google Scholar 

  103. Mallory, A.C., Parks, G., Endres, M.W., Baulcombe, D., Bowman, L.H., Pruss, G.J., and Vance, V.B., The amplicon-plus system for high-level expression of transgenes in plants, Nat. Biotechnol., 2002, vol. 20, pp. 622–625.

    Article  CAS  PubMed  Google Scholar 

  104. Padidam, M., Chemically regulated gene expression in plants, Curr. Opin. Plant Biol., 2003, vol. 6, pp. 169–177.

    Article  CAS  PubMed  Google Scholar 

  105. Padidam, M., Gore, M., Lu, D.L., and Smirnova, O., Chemical-inducible, ecdysone receptor-based gene expression system for plants, Transgenic Res., 2003, vol. 12, pp. 101–109.

    Article  CAS  PubMed  Google Scholar 

  106. Dohi, K., Nishikiori, M., Tamai, A., Ishikawa, M., Meshi, T., and Mori, M., Inducible virus-mediated expression of a foreign protein in suspension-cultured plant cells, Arch. Virol., 2006, vol. 151, pp. 1075–1084.

    Article  CAS  PubMed  Google Scholar 

  107. Sudarshana, M.R., Plesha, M.A., Uratsu, S.L., Falk, B.W., Dandekar, A.M., Huang, T.K., and McDonald, K.A., A chemically inducible cucumber mosaic virus amplicon system for expression of heterologous proteins in plant tissues, Plant Biotechnol. J., 2006, vol. 4, pp. 551–559.

    CAS  PubMed  Google Scholar 

  108. Zhang, X. and Mason, H., Bean yellow dwarf virus replicons for high-level transgene expression in transgenic plants and cell cultures, Biotechnol. Bioeng., 2006, vol. 93, no. 2, pp. 271–279.

    Article  CAS  PubMed  Google Scholar 

  109. Tremblay, A., Beauchemin, C., Seguin, A., and Laliberte, J.F., Reactivation of an integrated disabled viral vector using a Cre–loxP recombination system in Arabidopsis thaliana, Transgenic Res, 2007, vol. 16, pp. 213–222.

    Article  CAS  PubMed  Google Scholar 

  110. Plesha, M.A., Huang, T.K., Dandekar, A.M., Falk, B.W., and McDonald, K.A., High-level transient production of a heterologous protein in plants by optimizing induction of a chemically inducible viral amplicon expression system, Biotechnol. Prog, 2007, vol. 23, pp. 1277–1285.

    Article  CAS  PubMed  Google Scholar 

  111. Plesha, M.A., Huang, T.K., Dandekar, A.M., Falk, B.W., and McDonald, K.A., Optimization of the bioprocessing conditions for scale-up of transient production of a heterologous protein in plants using a chemically inducible viral amplicon expression system, Biotechnol. Prog., 2009, vol. 25, pp. 722–734.

    Article  CAS  PubMed  Google Scholar 

  112. Dujovny, G., Valli, A., Calvo, M., and Garcia, J.A., A temperature-controlled amplicon system derived from plum pox potyvirus, Plant Biotechnol. J., 2009, vol. 7, no. 1, pp. 49–58.

    Article  CAS  PubMed  Google Scholar 

  113. Werner, S., Breus, O., Symonenko, Y., Marillonnet, S., and Gleba, Y., High-level recombinant protein expression in transgenic plants by using a double-inducible viral vector, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 34, pp. 14061–14066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Palacpac, N.Q., Yoshida, S., Sakai, H., Kimura, Y., Fujiyama, K., Yoshida, T., and Seki, T., Stable expression of human beta1,4-galactosyltransferase in plant cells modifies N-linked glycosylation patterns, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 4692–4697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Bakker, H., Bardor, M., Molthoff, J.W., Gomord, V., Elbers, I., Stevens, L.H., Jordi, W., Lommen, A., Faye, L., Lerouge, P., and Bosch, D., Galactose-extended glycans of antibodies produced by transgenic plants, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, pp. 2899–2904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Cox, K.M., Sterling, J.D., Regan, J.T., Gasdaska, J.R., Frantz, K.K., Peele, C.G., Black, A., Passmore, D., Moldovan-Loomis, C., Srinivasan, M., Cuison, S., Cardarelli, P.M., and Dickey, L.F., Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor, Nat. Biotechnol., 2006, vol. 24, pp. 1591–1597.

    Article  CAS  PubMed  Google Scholar 

  117. Schaehs, M., Strasser, R., Stadlmann, J., Kunert, R., Rademacher, T., and Steinkellner, H., Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern, Plant Biotechnol. J., 2007, vol. 5, pp. 657–663.

    Article  CAS  Google Scholar 

  118. Strasser, R., Stadlmann, J., Schahs, M., Stiegler, G., Quendler, H., Mach, L., Glossl, J., Weterings, K., Pabst, M., and Steinkellner, H., Generation of glycoengineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure, Plant Biotechnol. J., 2008, vol. 6, pp. 392–402.

    Article  CAS  PubMed  Google Scholar 

  119. Decker, E.L. and Reski, R., Current achievements in the production of complex biopharmaceuticals with moss bioreactors, Bioprocess Biosyst. Eng., 2008, vol. 31, pp. 3–9.

    Article  CAS  PubMed  Google Scholar 

  120. Kallolimath, S., Castilho, A., Strasser, R., Grunwald-Gruber, C., Altmann, F., Strubl, S., Galuska, C.E., Zlatina, K., Galuska, S.P., Werner, S., Thiesler, H., Werneburg, S., Hildebrandt, H., Gerardy-Schahn, R., and Steinkellner, H., Engineering of complex protein sialylation in plants, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 34, pp. 9498–9503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Roque, A.C., Lowe, C.R., and Taipa, M.A., Antibodies and genetically engineered related molecules: production and purification, Biotechnol. Prog., 2004, vol. 20, pp. 639–654.

    Article  CAS  PubMed  Google Scholar 

  122. Vollenkle, C., Weigert, S., Ilk, N., Egelseer, E., Weber, V., Loth, F., Falkenhagen, D., Sleytr, U.B., and Sara, M., Construction of a functional S-layer fusion protein comprising an immunoglobulin G-binding domain for development of specific adsorbents for extracorporeal blood purification, Appl. Environ. Microbiol., 2004, vol. 70, pp. 1514–1521.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Nomellini, J.F., Duncan, G., Dorocicz, I.R., and Smit, J., S-layer-mediated display of the immunoglobulin g-binding domain of streptococcal protein G on the surface of Caulobacter crescentus: development of an immunoactive reagent, Appl. Environ. Microbiol., 2007, vol. 73, pp. 3245–3253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Kushwaha, A., Chowdhury, P.S., Arora, K., Abrol., S., and Chaudhary, V.K., Construction and characterization of M13 bacteriophages displaying functional IgGbinding domains of staphylococcal protein A, Gene, 1994, vol. 151, pp. 45–51.

    Article  CAS  PubMed  Google Scholar 

  125. Cao, Y., Zhang, Q., Wang, C., Zhu, Y., and Bai, G., Preparation of novel immunomagnetic cellulose microspheres via cellulose binding domain-protein A linkage and its use for the isolation of interferon alpha-2b, J. Chromatogr., A, 2007, vol. 1149, pp. 228–235.

    Article  CAS  Google Scholar 

  126. Qiu, X., Wong, G., Audet, J., Bello, A., FeRNAndo, L., Alimonti, J.B., Fausther-Bovendo, H., Wei, H., Aviles, J., Hiatt, E., Johnson, A., Morton, J., Swope, K., Bohorov, O., Bohorova, N., Goodman, C., Kim, D., Pauly, M.H., Velasco, J., Pettitt, J., Olinger, G.G., Whaley, K., Xu, B., Strong, J.E., Zeitlin, L., and Kobinger, G.P., Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp, Nature, 2014, vol. 514, pp. 47–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Zeitlin, L., Whaley, K.J., Olinger, G.G., Jacobs, M., Gopal, R., Qiu, X., and Kobinger, G.P., Antibody therapeutics for Ebola virus disease, Curr. Opin. Virol., 2016, vol. 17, pp. 45–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Tusé, D., Ku, N., Bendandi, M., Becerra, C., Collins, R.J., Langford, N., Sancho, S.I., López-Díaz de Cerio, A., Pastor, F., Kandzia, R., Thieme, F., Jarczowski, F., Krause, D., Ma, J.K., Pandya, S., Klimyuk, V., Gleba, Y., and Butler-Ransohoff, J.E., Clinical safety and immunogenicity of tumor-targeted, plant-made Id-KLH conjugate vaccines for follicular lymphoma, Biomed. Res. Int., 2015, article ID648143.

    Google Scholar 

  129. American Cancer Society, ACS Cancer Facts and Figures 2011, American Cancer Society, 2014.

  130. Kwak, L.W., Campbell, M.J., Czerwinski, D.K., Hart, S., Miller, R.A., and Levy, R., Induction of immune responses in patients with B-cell lymphoma against the surface-immunoglobulin idiotype expressed by their tumors, New Engl. J. Med., 1992, vol. 327, no. 17, pp. 1209–1215.

    Article  CAS  PubMed  Google Scholar 

  131. Gould, L.H., Bopp, C., Strockbine, N., Atkinson, R., Baselski, V., Body, B., Carey, R., Crandall, C., Hurd, S., Kaplan, R., Neill, M., Shea, S., Somsel, P., Tobin-D’Angelo, M., Griffin, P.M., and Gerner-Smidt, P., Centers for Disease Control and Prevention (CDC). Recommendations for diagnosis of Shiga toxin-producing Escherichia coli infections by clinical laboratories, MMWR Recomm. Rep., 2009, vol. 58, no. RR-12, pp. 1–14.

    PubMed  Google Scholar 

  132. Cascales, E., Buchanan, S.K., Duche, D., Kleanthous, C., Lloubès, R., Postle, K., Riley, M., Slatin, S., and Cavard, D., Colicin biology, Microbiol. Mol. Biol. Rev., 2007, vol. 71, no. 1, pp. 158–229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Nomad Bioscience GmbH, Weinbergweg 22, 06120, Halle, Germany

    A. Giritch & Y. Gleba

  2. Icon Genetics GmbH, Weinbergweg 22, 06120, Halle, Germany

    V. Klimyuk

Authors
  1. A. Giritch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Klimyuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Gleba
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. Gleba.

Additional information

Published in Ukrainian in Tsitologiya i Genetika, 2017, Vol. 51, No. 2, pp. 13–34.

The article was translated by the authors.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giritch, A., Klimyuk, V. & Gleba, Y. 125 years of virology and ascent of biotechnologies based on viral expressio. Cytol. Genet. 51, 87–102 (2017). https://doi.org/10.3103/S0095452717020037

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452717020037

Keywords

Search

Navigation