Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Production of Recombinant Anti-Cancer Vaccines in Plants

  • Lee, Jeong Hwan (Department of Medicine, Therapeutic Protein Engineering Lab, College of Medicine, Chung-Ang University) ;
  • Ko, Kisung (Department of Medicine, Therapeutic Protein Engineering Lab, College of Medicine, Chung-Ang University)
  • Received : 2016.06.13
  • Accepted : 2017.02.06
  • Published : 2017.07.01
Download PDF
⟨ Previous Next ⟩

Abstract

Plant expression systems have been developed to produce anti-cancer vaccines. Plants have several advantages as bioreactors for the production of subunit vaccines: they are considered safe, and may be used to produce recombinant proteins at low production cost. However, several technical issues hinder large-scale production of anti-cancer vaccines in plants. The present review covers design strategies to enhance the immunogenicity and therapeutic potency of anti-cancer vaccines, methods to increase vaccine-expressing plant biomass, and challenges facing the production of anti-cancer vaccines in plants. Specifically, the issues such as low expression levels and plant-specific glycosylation are described, along with their potential solutions.

Keywords

References

  1. Andrianov, V., Brodzik, R., Spitsin, S., Bandurska, K., McManus, H., Koprowski, H. and Golovkin, M. (2010) Production of recombinant anthrax toxin receptor (ATR/CMG2) fused with human Fc in planta. Protein Expr. Purif. 70, 158-162. https://doi.org/10.1016/j.pep.2009.09.016
  2. Bachmann, M. F. and Jennings, G. T. (2010) Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 10, 787-796. https://doi.org/10.1038/nri2868
  3. Bendandi, M., Marillonnet, S., Kandzia, R., Thieme, F., Nickstadt, A., Herz, S., Frode, R., Inoges, S., Lopez-Dìaz de Cerio, A., Soria, E., Villanueva, H., Vancanneyt, G., McCormick, A., Tuse, D., Lenz, J., Butler-Ransohoff, J. E., Klimyuk, V. and Gleba, Y. (2010) Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin's lymphoma. Ann. Oncol. 21, 2420-2427. https://doi.org/10.1093/annonc/mdq256
  4. Bhoo, S. H., Lai, H., Ma, J., Arntzen, C. J., Chen, Q. and Mason H. S. (2006) Expression of an immunogenic Ebola immune complex in Nicotiana benthamiana. Plant Biotechnol. J. 9, 807-816.
  5. Brodzik, R., Glogowska, M., Bandurska, K., Okulicz, M., Deka, D., Ko, K., van der Linden, J., Leusen, J. H., Pogrebnyak, N., Golovkin, M., Steplewski, Z. and Koprowski, H. (2006) Plant-derived anti-Lewis Y mAb exhibits biological activities for efficient immunotherapy against human cancer cells. Proc. Nati. Acad. Sci. U.S.A. 103, 8804-8809. https://doi.org/10.1073/pnas.0603043103
  6. Brodzik, R., Spitsin, S., Golovkin, M., Bandurska, K., Portocarrero, C., Okulicz, M., Steplewski, Z. and Koprowski, H. (2008) Plant-derived EpCAM antigen induces protective anti-cancer response. Cancer Immunol. Immunother. 57, 317-323. https://doi.org/10.1007/s00262-007-0366-4
  7. Chargelegue, D., Drake, P. M., Obregon, P., Prada, A., Fairweather, N. and Ma, J. K. (2005) Highly immunogenic and protective recombinant vaccine candidate expressed in transgenic plants. Infect. Immun. 73, 5915-5922. https://doi.org/10.1128/IAI.73.9.5915-5922.2005
  8. Chotprakaikiat, W., Allen, A., Bui-Minh, D., Harden, E., Jobsri, J., Cavallo, F., Gleba, Y., Stevenson, F. K., Ottensmeier, C., Klimyuk, V. and Savelyeva, N. (2016) A plant-expressed conjugate vaccine breaks $CD4^+$ tolerance and induces potent immunity against metastatic $Her2^+$ breast cancer. Oncoimmunology 22, e1166323.
  9. Conley, A. J., Zhu, H., Le, L. C., Jevnikar, A. M., Lee, B. H., Brandle, J. E. and Menassa, R. (2011) Recombinant protein production in a variety of Nicotiana hosts: a comparative analysis. Plant Biotechnol. J. 9, 434-444. https://doi.org/10.1111/j.1467-7652.2010.00563.x
  10. Cripps, A. W., Kyd, J. M. and Foxwell, A. R. (2001) Vaccines and mucosal immunisation. Vaccine 19, 2513-2515. https://doi.org/10.1016/S0264-410X(00)00481-3
  11. Curtiss, III, R. and Cardineau, G. A., inventors; Washington University, assignee. Oral immunization by transgenic plants. United States patent US 5,679,880. 1997 Oct 21.
  12. Daniell, H., Datta, R., Varma, S., Gray, S. and Lee, S. B. (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat. Biotechnol. 16, 345-348. https://doi.org/10.1038/nbt0498-345
  13. Dicker, M., Tschofen, M., Maresch, D., Konig, J., Juarez, P., Orzaez, D., Altmann, F., Steinkellner, H. and Strasser, R. (2016) Transient glyco-engineering to produce recombinant IgA1 with defined Nand O-glycans in plants. Front. Plant Sci. 7, 18.
  14. Donaldson, M., Wood, H. A., Kulakosky, P. C. and Shuler, M. L. (1999) Glycosylation of a recombinant protein in the Tn5B1-4 insect cell line: influence of ammonia, time of harvest, temperature, and dissolved oxygen. Biotechnol. Bioeng. 63, 255-262. https://doi.org/10.1002/(SICI)1097-0290(19990505)63:3<255::AID-BIT1>3.0.CO;2-R
  15. Evans, D. E., Coleman, J. O. D. and Kearns, A. (2003) Plant Cell Culture. Tayler & Francis Group, London.
  16. Fazlalipour, M., Keyvani, H., Monavari, S. H. and Mollaie, H. R. (2015) Expression, purification and immunogenic description of a hepatitis C virus recombinant coreE1E2 protein expressed by yeast pichiapastoris. Jundishapur J. Microbiol. 8, e17157.
  17. Frazer, I. H., Lowy, D. R. and Schiller, J. T. (2007) Prevention of cancer through immunization: Prospects and challenges for the 21st century. Eur. J. Immunol. 37, S148-S155. https://doi.org/10.1002/eji.200737820
  18. Gaume, A., Komarnytsky, S., Borisjuk, N. and Raskin, I. (2003) Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Rep. 21, 1188-1193. https://doi.org/10.1007/s00299-003-0660-3
  19. Gomord, V., Chamberlain, P., Jefferis, R. and Faye, L. (2005) Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol. 23, 559-565. https://doi.org/10.1016/j.tibtech.2005.09.003
  20. Goodin, M. M., Zaitlin, D., Naidu, R. A. and Lommel, S. A. (2008) Nicotianabenthamiana: its history and future as a model for plantpathogen interactions. Mol. Plant Microbe Interact. 21, 1015-1026. https://doi.org/10.1094/MPMI-21-8-1015
  21. Hong, S. Y., Kwon, T. H., Jang, Y. S., Kim, S. H. and Yang, M. S. (2006) Production of bioactive human granulocyte-colony stimulating factor in transgenic rice cell suspension cultures. Protein Expr. Purif. 47, 68-73. https://doi.org/10.1016/j.pep.2005.09.028
  22. Huang, T. K. and McDonald, K. A. (2012) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol. Adv. 30, 398-409. https://doi.org/10.1016/j.biotechadv.2011.07.016
  23. Hussain, M. S., Fareed, S., Ansari, S., Rahman, M. A., Ahmad, I. Z. and Saeed, M. (2012) Current approaches toward production of secondary plant metabolites. J. Pharm. Bioallied Sci. 4, 10-20.
  24. Hwang, S. J., Kim, K. S., Byo, B. K. and Hwang, B. (1999) Saponin production by hairy root cultures of Panax ginseng CA Meyer: Influence of PGR and Polyamines. Biotechnol. Bioprecess Eng. 4, 309-312. https://doi.org/10.1007/BF02933759
  25. Jamal, A., Ko, K., Kim, H. S., Choo, Y. K., Joung, H. and Ko, K. (2009) Role of genetic factors and environmental conditions in recombinant protein production for molecular farming. Biotechnol. Adv. 27, 914-923. https://doi.org/10.1016/j.biotechadv.2009.07.004
  26. Jamal, A., Lee, J. H., Lee, K. J., Oh, D. B., Kim, D. S., Lee, K. K., Choo, Y. K., Hwang, K. A. and Ko, K. (2012) Chimerism of Multiple Monoclonal Antibodies Expressed in a Single Plant. Hortic. Environ. Biotechnol. 53, 544-551. https://doi.org/10.1007/s13580-012-0153-9
  27. Jensen, C. S., Salchert, K., Gao, C., Andersen, C., Didion, T. and Nielsen, K. K. (2004) Floral inhibition in red fescue (Festucarubra L.) through expression of a heterologous flowering repressor from Lolium. Mol. Breed. 13, 37-48. https://doi.org/10.1023/B:MOLB.0000012327.47625.23
  28. Jobsri, J., Allen, A., Rajagopal, D., Shipton, M., Kanyuka, K., Lomonossoff, G. P., Ottensmeier, C., Diebold, S. S., Stevenson, F. K. and Savelyeva, N. (2015) Plant virus particles carrying tumour antigen activate TLR7 and Induce high levels of protective antibody. PLoS ONE 10, e0118096. https://doi.org/10.1371/journal.pone.0118096
  29. Kang, Y., Shin, Y. K., Park, S. W. and Ko, K. (2016) Effect of Nitrogen Deficiency on Recombinant Protein Production and Dimerization and Growth in Transgenic Plants. Hortic. Environ. Biotechnol. 57, 299-307. https://doi.org/10.1007/s13580-016-0045-5
  30. Kim, D. S., Song, I., Kim, J., Kim, D. S. and Ko, K. (2016) Plant recycling for molecular biofarming to produce recombinant anti-cancer mAb. Front. Plant Sci. 7, 1037.
  31. Klimyuk, V., Pogue, G., Herz, S., Butler, J. and Haydon, H. (2014) Production of recombinant antigens and antibodies in Nicotiana benthamiana using 'magnifection' technology: GMP-compliant facilities for small-and large-scale manufacturing. Curr. Top. Microbiol. Immunol. 375, 127-154.
  32. Ko, K., Wei, X., Crooks, P. A. and Koprowski, H. (2004) Elimination of alkaloids from plant-derived human monoclonal antibody. J. Immunol. Methods 286, 79-85. https://doi.org/10.1016/j.jim.2003.11.015
  33. Kuo, Y. C., Tan, C. C., Ku, J. T., Hsu, W. C., Su, S. C., Lu, C. A. and Huang, L. F. (2013) Improving pharmaceutical protein production in Oryza sativa. Int. J. Mol. Sci. 14, 8719-8739. https://doi.org/10.3390/ijms14058719
  34. Kurokawa, S., Nakamura, R., Mejima, M., Kozuka-Hata, H., Kuroda, M., Takeyama, N., Oyama, M., Satoh, S., Kiyono, H., Masumura, T., Teshima, R. and Yuki, Y. (2013) MucoRice-cholera toxin B-subunit, a rice-based oral cholera vaccine, down-regulates the expression of ${\alpha}$-amylase/trypsin inhibitor-like protein family as major rice allergens. J. Proteome Res. 12, 3372-3382. https://doi.org/10.1021/pr4002146
  35. Lee, J. H., Park, D. Y., Lee, K. J., Kim, Y. K., So, Y. K., Ryu, J. S., Oh, S. H., Han, Y. S., Ko, K., Choo, Y. K., Park, S. J., Brodzik, R., Lee, K. K., Oh, D. B., Hwang, K. A., Koprowski, H., Lee, Y. S. and Ko, K. (2013) Intracellular reprogramming of expression, glycosylation, and function of a plant-derived antiviral therapeutic monoclonal antibody. PLoS ONE 8, e68772. https://doi.org/10.1371/journal.pone.0068772
  36. Lee, S. Y., Kim, Y. H., Roh, Y. S., Myoung, H. J., Lee, K. Y. and Kim, D. I. (2004) Bioreactor operation for transgenic Nicotiana tabacum cell cultures and continuous production of recombinant human granulocyte-macrophage colony-stimulating factor by perfusion culture. Enzyme Microb. Technol. 35, 663-671. https://doi.org/10.1016/j.enzmictec.2004.08.019
  37. Li, W., Asada, Y. and Yoshikawa, T. (1998) Antimicrobial flavonoids from Glycyrrhizaglabra hairy root cultures. Planta Med. 64, 746-747. https://doi.org/10.1055/s-2006-957571
  38. Lico, C., Chen, Q. and Santi, L. (2008) Viral vectors for production of recombinant proteins in plants. J. Cell. Physiol. 216, 366-377. https://doi.org/10.1002/jcp.21423
  39. Lim, C. Y., Lee, K. J., Oh, D. B. and Ko, K. (2015) Effect of the developmental stage and tissue position on the expression and glycosylation of recombinant glycoprotein GA733-FcK in transgenic plants. Front. Plant Sci. 5, 778.
  40. Liu, L., Davies, J. W. and Stanley, J. (1998) Mutational analysis of bean yellow dwarf virus, a geminivirus of the genus Mastrevirus that is adapted to dicotyledonous plants. J. Gen. Virol. 79, 2265-2274. https://doi.org/10.1099/0022-1317-79-9-2265
  41. Liu, Y. K., Huang, L. F., Ho, S. L., Liao, C. Y., Liu, H. Y., Lai, Y. H., Yu, S. M. and Lu, C. A. (2012) Production of mouse granulocytemacrophage colony-stimulating factor by gateway technology and transgenic rice cell culture. Biotechnol. Bioeng. 109, 1239-1247. https://doi.org/10.1002/bit.24394
  42. Loos, A. and Steinkellner, H. (2014) Plant glyco-biotechnology on the way to synthetic biology. Front. Plant Sci. 5, 523.
  43. Lu, Z., Lee, K. J., Shao, Y., Lee, J. H., So, Y., Choo, Y. K., Oh, D. B., Hwang, K. A., Oh, S. H., Han, Y. S. and Ko, K. (2012) Expression of GA733-Fc fusion protein as a vaccine candidate for colorectal cancer in transgenic plants. J. Biomed. Biotechnol. 2012, 364240.
  44. Ma, J. K., Chikwamba, R., Sparrow, P., Fischer, R., Mahoney, R. and Twyman, R. M. (2005) Plant-derived pharmaceuticals-the road forward. Trends Plant Sci. 10, 580-585. https://doi.org/10.1016/j.tplants.2005.10.009
  45. Magnuson, N. S., Linzmaier, P. M., Reeves, R., An, G., HayGlass, K. and Lee, J. M. (1998) Secretion of biologically active human interleukin-2 and interleukin-4 from genetically modified tobacco cells in suspension culture. Protein Expr. Purif. 13, 45-52. https://doi.org/10.1006/prep.1998.0872
  46. Marillonnet, S., Giritch, A., Gils, M., Kandzia, R., Klimyuk, V. and Gleba, Y. (2004) In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium. Proc. Natl. Acad. Sci. U.S.A. 101, 6852-6857. https://doi.org/10.1073/pnas.0400149101
  47. Maruyama, D., Sugiyama, T., Endo, T. and Nishikawa, S. (2014) Multiple BiP genes of Arabidopsis thaliana are required for male gametogenesis and pollen competitiveness. Plant Cell Physiol. 55, 801-810. https://doi.org/10.1093/pcp/pcu018
  48. Massa, S., Franconi, R., Brandi, R., Muller, A., Mett, V., Yusibov, V. and Venuti, A. (2007) Anti-cancer activity of plant-produced HPV16 E7 vaccine. Vaccine 25, 3018-3021. https://doi.org/10.1016/j.vaccine.2007.01.018
  49. Matzeit, V., Schaefer, S., Kammann, M., Schalk, H. J., Schell, J. and Gronenborn, B. (1991) Wheat dwarf virus vectors replicate and express foreign genes in cells of monocotyledonous plants. Plant Cell 3, 247-258. https://doi.org/10.1105/tpc.3.3.247
  50. Mayo, K. J., Gonzales, B. J. and Mason, H. S. (2006) Genetic transformation of tobacco NT1 cells with Agrobacterium tumefaciens. Nat. Protoc. 1, 1105-1111. https://doi.org/10.1038/nprot.2006.176
  51. 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., Tuse, D. and Levy, R. (2008) Plantproduced 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. 105, 10131-10136. https://doi.org/10.1073/pnas.0803636105
  52. McCormick, A. A. (2011) Tobacco derived cancer vaccines for non-Hodgkin's lymphoma: perspectives and progress. Hum. Vaccin. 7, 305-312. https://doi.org/10.4161/hv.7.3.14163
  53. Medina-Bolivar, F., Wright, R., Funk, V., Sentz, D., Barroso, L., Wilkins, T. D., Petri, W., Jr. and Cramer, C. L. (2003) A non-toxic lectin for antigen delivery of plant-based mucosal vaccines. Vaccine. 21, 997-1005. https://doi.org/10.1016/S0264-410X(02)00551-0
  54. Meyers, B., Zaltsman, A., Lacroix, B., Kozlovsky, S. V. and Krichevsky, A. (2010) Nuclear and plastid genetic engineering of plants: comparison of opportunities and challenges. Biotechnol. Adv. 28, 747-756. https://doi.org/10.1016/j.biotechadv.2010.05.022
  55. Monsurro, V., Nagorsen, D., Wang, E., Provenzano, M., Dudley, M. E., Rosenberg, S. A. and Marincola, F. M. (2002) Functional heterogeneity of vaccine-induced CD8+ T cells. J. Immunol. 168, 5933-5942. https://doi.org/10.4049/jimmunol.168.11.5933
  56. Nishi, A. and Sugano, N. (1970) Growth and division of carrot cells in suspension culture. Plant Cell Phsiol. 11, 757-765.
  57. Park, S. R., Lim, C. Y., Kim, D. S. and Ko, K. (2015) Optimization of ammonium sulfate concentration for purification of colorectal cancer vaccine candidate recombinant protein GA733-FcK isolated from plants. Front. Plant Sci. 6, 1040.
  58. Paz-Maldonado, L. M. and Gonzalez-Ramirez, J. E. (2014) Bioreactors for plant biomass production and bioprocessing. In Genetically Engineered Plants as a Source of Vaccines against Wide Spread Diseases, pp. 129-140. Springer, New York.
  59. Peruzzi, P. P. and Chiocca, E. A. (2016) Cancer immunotherapy: A vaccine from plant virus proteins. Nat. Nanotechnol. 11, 214-215. https://doi.org/10.1038/nnano.2015.306
  60. Pineo, C. B., Hitzeroth, I. I. and Rybicki, E. P. (2013) Immunogenic assessment of plant-produced human papillomavirus type 16 L1/L2 chimaeras. Plant Biotechnol. J. 11, 964-975. https://doi.org/10.1111/pbi.12089
  61. Pinkhasov, J., Alvarez, M. L., Rigano, M. M., Piensook, K., Larios, D., Pabst, M., Grass, J., Mukherjee, P., Gendler, S. J., Walmsley, A. M. and Mason, H. S. (2011) Recombinant plant-expressed tumourassociated MUC1 peptide is immunogenic and capable of breaking tolerance in MUC1.Tg mice. Plant Biotechnol J. 9, 991-1001 https://doi.org/10.1111/j.1467-7652.2011.00614.x
  62. Plchova, H., Moravec, T., Hoffmeisterova, H., Folwarczna, J. and Cerovska, N. (2011) Expression of human papillomavirus 16 E7ggg oncoprotein on N-and C-terminus of potato virus X coat protein in bacterial and plant cells. Protein Expr. Purif. 77, 146-152. https://doi.org/10.1016/j.pep.2011.01.008
  63. Pleass, R. J. (2009) Fc-receptors and immunity to malaria: from models to vaccines. Parasite Immunol. 31, 529-538. https://doi.org/10.1111/j.1365-3024.2009.01101.x
  64. Qiao, L., Lee, K. J. and Ko, K. (2015) Characterization of the glycan structures of glycoprotein GA733-Fc expressed in a baculovirusinsect cell system. Bull. Korean Chem. Soc. 36, 139-149. https://doi.org/10.1002/bkcs.10035
  65. Radford, K. J., Higgins, D. E., Pasquini, S., Cheadle, E. J., Carta, L., Jackson, A. M., Lemoine, N. R. and Vassaux, G. (2002) A recombinant E. coli vaccine to promote MHC class I-dependent antigen presentation: application to cancer immunotherapy. Gene Ther. 9, 1455-1463. https://doi.org/10.1038/sj.gt.3301812
  66. Rao, S. R. and Ravishankar, G. A. (2002) Plant cell cultures: Chemical factories of secondary metabolites. Biotechnol. Adv. 20, 101-153. https://doi.org/10.1016/S0734-9750(02)00007-1
  67. Rappuoli, R. (2007) Bridging the knowledge gaps in vaccine design. Nat. Biotechnol. 25, 1361-1366. https://doi.org/10.1038/nbt1207-1361
  68. Raskin, I., Ribnicky, D. M., Komarnytsky, S., Ilic, N., Poulev, A., Borisjuk, N., Brinker, A., Moreno, D. A., Ripoll, C., Yakoby, N., O'Neal, J. M., Cornwell, T., Pastor, I. and Fridlender, B. (2002) Plants and human health in the twenty-first century. Trends Biotechnol. 20, 522-531. https://doi.org/10.1016/S0167-7799(02)02080-2
  69. Rigano, M. M. and Walmsley, A. M. (2005) Expression systems and developments in plant-made vaccines. Immunol. Cell Biol. 83, 271-277. https://doi.org/10.1111/j.1440-1711.2005.01336.x
  70. Ruf, S., Hermann, M., Berger, I. J., Carrer, H. and Bock, R. (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat. Biotechnol. 19, 870-875. https://doi.org/10.1038/nbt0901-870
  71. Rymerson, R. T., Babiuk, L., Menassa, R., Vanderbeld, B. and Brandle, J. E. (2003) Immunogenicity of the capsid protein VP2 from porcine parvovirus expressed in low alkaloid transgenic tobacco. Mol. Breed. 11, 267-276. https://doi.org/10.1023/A:1023426906756
  72. Shaaltiel, Y., Bartfeld, D., Hashmueli, S., Baum, G., Brill-Almon, E., Galili, G., Dym, O., Boldin-Adamsky, S. A., Silman, I., Sussman, J. L., Futerman, A. H. and Aviezer, D. (2007) Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol. J. 5, 579-590. https://doi.org/10.1111/j.1467-7652.2007.00263.x
  73. Sharp, J. M. and Doran, P. M. (2001) Characterization of monoclonal antibody fragments produced by plant cells. Biotechnol. Bioeng. 73, 338-346. https://doi.org/10.1002/bit.1067
  74. Sheludko, Y. V., Sindarovska, Y. R., Gerasymenko, I. M., Bannikova, M. A. and Kuchuk, N. V. (2007) Comparison of several Nicotiana species as hosts for high-scale Agrobacterium-mediated transient expression. Biotechnol. Bioeng. 96, 608-614. https://doi.org/10.1002/bit.21075
  75. Shivprasad, S., Pogue, G. P., Lewandowski, D. J., Hidalgo, J., Donson, J., Grill, L. K. and Dawson, W. O. (1999) Heterologous sequences greatly affect foreign gene expression in tobacco mosaic virus-based vectors. Virology 255, 312-323. https://doi.org/10.1006/viro.1998.9579
  76. Singh, D., Basu, C., Meinhardt-Wollweber, M. and Roth, B. (2015) LEDs for energy efficient greenhouse lighting. Renew. Sustainable Energy Rev. 49, 139-147. https://doi.org/10.1016/j.rser.2015.04.117
  77. Smith, M. L., Mason, H. S. and Shuler, M. L. (2002) Hepatitis B surface antigen (HBsAg) expression in plant cell culture: Kinetics of antigen accumulation in batch culture and its intracellular form. Biotechnol. Bioeng. 80, 812-822. https://doi.org/10.1002/bit.10444
  78. Song, I., Kim, D. S., Kim, M. K., Jamal, A., Hwang, K. A. and Ko, K. (2015) Comparison of total soluble protein in various horticultural crops and evaluation of its quantification methods. Hortic Environ. Biotechnol. 56, 123-129. https://doi.org/10.1007/s13580-015-0097-y
  79. Spangenberg, G., Wang, Z. Y. and Potrykus, I. (2012) Biotechnology in forage and turf grass improvement (Vol. 23), Springer Science & Business Media, New York.
  80. Staib, L., Birebent, B., Somasundaram, R., Purev, E., Braumuller, H., Leeser, C., Kuttner, N., Li, W., Zhu, D., Diao, J., Wunner, W., Speicher, D., Beger, H. G., Song, H. and Herlyn, D. (2001) Immunogenicity of recombinant GA733-2E antigen (CO17-1A, EGP, KS1-4, KSA, Ep-CAM) in gastro-intestinal carcinoma patients. Int. J. Cancer 92, 79-87. https://doi.org/10.1002/1097-0215(200102)9999:9999<::AID-IJC1164>3.0.CO;2-J
  81. Strasser, R., Bondili, J. S., Vavra, U., Schoberer, J., Svoboda, B., Glossl, J., Leonard, R., Stadlmann, J., Altmann, F., Steinkellner, H. and Mach, L. (2007) A unique beta1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19, 2278-2292. https://doi.org/10.1105/tpc.107.052985
  82. Tacket, C. O. (2009) Plant-based oral vaccines: results of human trials. Curr. Top. Microbiol. Immunol. 332, 103-117.
  83. Takaiwa, F. (2007) A rice-based edible vaccine expressing multiple Tcell epitopes to induce oral tolerance and inhibit allergy. Immunol. Allergy Clin. North Am. 27, 129-139. https://doi.org/10.1016/j.iac.2006.11.001
  84. Tepfer, M. and Casse-Delbart, F. (1987) Agrobacterium rhizogenes as a vector for transforming higher plants. Microbiol. Sci. 4, 24-28.
  85. Vasilev, N., Gromping, U., Lipperts, A., Raven, N., Fischer, R. and Schillberg, S. (2013) Optimization of BY-2 cell suspension culture medium for the production of a human antibody using a combination of fractional factorial designs and the response surface method. Plant Biotechnol. J. 11, 867-874. https://doi.org/10.1111/pbi.12079
  86. Verch, T., Hooper, D. C., Kiyatkin, A., Steplewski, Z. and Koprowski, H. (2004) Immunization with a plant-produced colorectal cancer antigen. Cancer Immunol. Immunother. 53, 92-99. https://doi.org/10.1007/s00262-003-0428-1
  87. Wang, Z. Y. and Ge, Y. (2006) Recent advances in genetic transformation of forage and turf grasses. In vitro Cell. Dev. Biol., Plant 42, 1-18.
  88. Zhang, S., Zhang, H. and Zhao, J. (2009) The role of CD4 T cell help for CD8 CTL activation. Biochem. Biophys. Res. Commun. 384, 405-408. https://doi.org/10.1016/j.bbrc.2009.04.134
  89. Zhang, X. and Mason, H. (2006) Bean Yellow Dwarf Virus replicons for high-level transgene expression in transgenic plants and cell cultures. Biotechnol. Bioeng. 93, 271-279. https://doi.org/10.1002/bit.20695
  90. Zhang, Y., Li, J., Pu, H., Jin, J., Zhang, X., Chen, M., Wang, B., Han, C., Yu, J. and Li, D. (2010) Development of Tobacco necrosis virus A as a vector for efficient and stable expression of FMDV VP1 peptides. Plant Biotechnol. J. 8, 506-523. https://doi.org/10.1111/j.1467-7652.2010.00500.x

Cited by

  1. Agroinfiltration of leaves for deconstructed viral vector-based transient gene expression: infiltrated leaf area affects recombinant hemagglutinin yield vol.59, pp.4, 2018, https://doi.org/10.1007/s13580-018-0047-6
  2. Expression, glycosylation, and function of an anti-rabies virus monoclonal antibody in tobacco and Arabidopsis plants vol.59, pp.2, 2018, https://doi.org/10.1007/s13580-018-0031-1
  3. Evaluation of the oral immunogenicity of M cell-targeted tetravalent EDIII antigen for development of plant-based edible vaccine against dengue infection pp.1573-5044, 2019, https://doi.org/10.1007/s11240-018-01544-9
  4. Immune response of heterologous recombinant antigenic protein of viral hemorrhagic septicemia virus (VHSV) in mice pp.2151-2485, 2019, https://doi.org/10.1080/19768354.2019.1575904
  5. Virus-based pharmaceutical production in plants: an opportunity to reduce health problems in Africa vol.16, pp.1, 2017, https://doi.org/10.1186/s12985-019-1263-0
  6. Expression and in vitro function of anti-cancer mAbs in transgenic Arabidopsis thaliana vol.53, pp.4, 2017, https://doi.org/10.5483/bmbrep.2020.53.4.106
  7. Expression, function, and glycosylation of anti-colorectal cancer large single-chain antibody (LSC) in plant vol.14, pp.3, 2017, https://doi.org/10.1007/s11816-020-00610-z
  8. Expression of a Large Single-Chain 13F6 Antibody with Binding Activity against Ebola Virus-Like Particles in a Plant System vol.21, pp.19, 2017, https://doi.org/10.3390/ijms21197007
  9. Optimization of the human colorectal carcinoma antigen GA733-2 production in tobacco plants vol.15, pp.1, 2017, https://doi.org/10.1007/s11816-020-00657-y
  10. Plant-based vaccines and cancer therapy: Where are we now and where are we going? vol.169, pp.None, 2017, https://doi.org/10.1016/j.phrs.2021.105655