Plant-derived human vaccines; an overview

International Journal of Pharmacology

Volumn 2, Issue 3, 2006, Pages 268-279

  Aliahmadi, Atousa ^a   Rahmani, Nasim ^a   Abdollahi, Mohammad ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Bacteria; Human pathogens; Plant; Vaccine; Viruses

Indexed keywords

ANTHRAX VACCINE; BACTERIAL VACCINE; BCG VACCINE; CHOLERA VACCINE; CYTOMEGALOVIRUS VACCINE; DNA VACCINE; ESCHERICHIA COLI VACCINE; HELICOBACTER PYLORI VACCINE; HEPATITIS B VACCINE; HEPATITIS C VACCINE; HEPATITIS VACCINE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; MEASLES VACCINE; PLANT EXTRACT; PSEUDOMONAS VACCINE; RABIES VACCINE; RECOMBINANT ANTIGEN; RECOMBINANT PROTEIN; RESPIRATORY SYNCYTIAL VIRUS VACCINE; ROTAVIRUS VACCINE; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; SUBUNIT VACCINE; TETANUS TOXOID; VIRUS VACCINE; WART VIRUS VACCINE;

ANTHRAX; BACTERIAL INFECTION; BIOTECHNOLOGY; CHOLERA; CLINICAL TRIAL; CYTOMEGALOVIRUS INFECTION; DISEASE MODEL; DRUG FORMULATION; ENTEROBACTER INFECTION; GENOME; GRAM NEGATIVE INFECTION; HEPATITIS B; HEPATITIS C; HEPATITIS E; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; MEASLES; MEDICINAL PLANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PLANT GENETICS; REVIEW; SEVERE ACUTE RESPIRATORY SYNDROME; TETANUS; TUBERCULOSIS; VERRUCA VULGARIS; VIRUS INFECTION;

EID: 33745738463     PISSN: 18117775     EISSN: 18125700     Source Type: Journal    
DOI: 10.3923/ijp.2006.268.279     Document Type: Review

References (112)

1. Arakawa, T., D.K.X. Chong, J. Lawrence Merritt and W.H.R. Langridge, 1997. Expression of cholera toxin B subunit oligomers in transgenic potato plants. Transgenic Res., 6: 403-413.
2. Arakawa, T., W.H.R. Langridge and D.K.X. Chong, 1998. Efficacy of a food plant-based oral cholera toxin B subunit vaccine. Nat. Biotechnol., 16: 292-297.
3. Ashraf, S., P.K. Singh, D.K. Yadav, Md. Shahnawaz, S. Mishra, S.V. Sawant and R. Tuli, 2005. High level expression of surface glycoprotein of rabies virus in tobacco leaves and its immunoprotective activity in mice. J. Biotechnol., 199: 1-14.
4. Aziz, M.A., S. Singh, P. Annand Kumar and R. Bhatnagar, 2002. Expression of protective antigen in transgenic plants: A step towards edible vaccine against anthrax. Biochem. Biophys. Res. Commun., 299: 345-451.
5. Barta, A., K. Sommergruber and D. Thompson, 1986. Expression of a nopaline synthase-human growth hormone chimeric gene in transformed tobacco and sunflower callus tissue. Plant Mol. Biol., 6: 347-57.
6. Belanger, H., N. Fleysh, C. Cox, G. Bartman, D. Deka, M. Trudel, H. Koprowski and V. Yusibov, 2000. Human respiratory syncytial virus vaccine antigen produced in plants. FASEB J., 14: 2323-2328.
7. Biemelt, S., U. Sonnewald, P. Galmbacher, M. Müller and L. Willmitzer, 2003. Production of human papillomavirus type 16 virus-like particles in transgenic plants. J. Virol., 77:9211-9220.
8. Birch-Machint, I., C.A. Newell, J.M. Hibberd and J.C. Gray, 2004. Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability. Plant Biotechnol. J., 2: 261-270.
9. Bouche, F.B., C.P. Muller, E. Marquet-Blouin, A. Steinmetz and Y. Yanagi, 2003. Neutralising immunogenicity of a polyepitope antigen expressed in a transgenic food plant: A novel antigen to protect against measles. Vaccine, 21:2074-2081.
10. Bouche, F.B., A. Steinmetz, Y. Yanagi and C.P. Muller, 2005. Induction of broadly neutralizing antibodies against measles virus mutants using a polyepitope vaccine strategy. Vaccine, 23: 2074-2077.
11. Brennan, F.R., T.D. Jones, T. Bellaby, F. Xu, P.C. North, A. Thompson, W.D.O. Hamilton, L.B. Gilleland, J. Staczek, H.E. Gilleland Jr., T. Lin and J.E. Johnson, 1999. Pseudomonas aeruginosa outer-membrane protein F epitopes are highly immunogenic in mice when expressed on a plant virus. Microbiology, 145:211-220.
12. Carter, J.E. and W.H.R. Langridge, 2002. Plant-based vaccines for protection against infectious and autoimmune diseases. Crit. Rev. Plant Sci., 21: 93-109.
13. Chikwamba, R.K., J. Cunnick, D. Hathaway, J. McMurray, H. Mason and K.Wang, 2002. A functional antigen in a practical crop: LT-B producing maize protects mice against Escherichia coli heat Labile Enterotoxin (LT) and Cholera Toxin (CT). Transgenic Res., 11: 479-493.
14. Chikwamba, R.K., L.B. Mejia, K. Wang, M.P. Scott and H.S. Mason, 2003. Localization of a bacterial protein in starch granules of transgenic maize kernels. Proc. Natl. Acad. Sci. US., 100: 11127-11132.
15. Chong, D.K.X. and W.H.R. Langridge, 2000. Expression of full-length bioactive antimicrobial human lactoferrin in potato plants. Transgenic Res., 9: 71-78.
16. Daniell, H., S.B. Lee, T. Panchal and P.O. Wiebe, 2001. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J. Mol. Biol., 311:1001-1009.
17. Daniell, H., M.S. Khan and L. Allison, 2002. Milestones in chloroplast genetiengineering: An environmentally friendly era in biotechnology. Trends Plant Sci., 7: 84-91.
18. Datar, R.V., T. Cartwright and C.G. Rosen, 1993. Process economics of animal cell and bacterial fermentations: a case study analysis of tissue plasminogen activator. Biotechnology, 11: 349-357.
19. DeZoeten, G.A., J.R. Penswick, M.A. Horisberger, P. Ahl, M. Schultze and T. Hohn, 1989. The expression, localization and effect of a human interferon in plants. Virology, 172: 213-222.
20. Dong, J.L., B.G. Liang, Y.S. Jin, W.J. Zhang and T. Wang, 2005. Oral immunization with pBsVP6-transgenic alfalfa protects mice against rotavirus infection. Virology, 339: 153-163.
21. Durrani, Z., T.L. McInerney, L. McLain, N.J. Dimmock, T. Jones, T. Bellaby and F.R. Brennan, 1998. Intranasal immunization with a plant virus expressing a peptide from HIV-1 gp41 stimulates better mucosal and systemic HIV-1-specific IgA and IgG than oral immunization. J. Immunol. Methods, 220: 93-103.
22. Dus Santos, M.J., C. Carrillo, F. Ardila, R.D. Rios, P. Franzone, M.E., Piccone A. Wigdorovitz and M.V. Borca, 2005. Development of transgenic alfalfa plants containing the foot and mouth disease virus structural polyprotein gene P1 and its utilization as an experimental immunogen. Vaccine, 23:1838-1843.
23. El Attar, A.K., A.A. Shalaby, H.M. Mazyad, J.M. Keith, A.M. Shamloul, B.Y. Riad and A. Saad, 2004. Expression of chimeric HCV peptide in transgenic plants infected with recombinant alfalfa mosaic virus for development of a plant-derived vaccine against HCV. Afr. J. Biotechnol., 3: 588-594.
24. Faye, L., A. Boulaflous, M. Benchabane, V. Gomord and D. Michaud, 2005. Protein modifications in the plant secretory pathway: Current status and practical implications in molecular pharming. Vaccine, 23: 1770-1778.
25. Fischer, R., E. Stoger, S. Schillberg, P. Christou, R.M. Twyman, 2004. Plant-based production of biopharmaceuticals. Curr. Opin. Plant Biol., 7: 152-158.
26. Koprowski, H. and V. Yusibov, 2001. The green revolution: Plants as heterologous expression vectors. Vaccine, 19: 2735-2741.
27. 19), a potential malaria vaccine candidate, in tobacco. Plant Sci., 162: 335-343.
28. Goldschmidt-Clermont, M., 1991. Transgenic expression of aminoglycoside adenine transferase in the chloroplast: A selectable marker for site-directed transformation of Chlamydomonas. Nucleic Acids Res., 19: 4083-4089.
29. Goldstein, D.A. and J.A. Thomas, 2004. Biopharmaceuticals derived from genetically modified plants. Q. J. Med., 97: 705-716.
30. Gomez, N., J.M. Escribano, C. Carrillo, M.V. Borca, J. Salinas and F. Parra, 1998. Expression of immunogenic glycoprotein S polypeptides from transmissible gastroenteritis coronavirus in transgenic plants. Virology, 249: 352-358.
31. Gomez, N., A. Wigdorovitz, S. Castanon, F. Gil, R. Ordas, M.V. Borca and J.M. Escribano, 2000. Oral immunogenicity of the plant derived spike protein from swine-transmissible gastroenteritis coronavirus. Arch. Virol., 145: 1725-1732.
32. Gu, Q., N. Han, J. Liu and M. Zhu, 2005. Cloning of Helicobacter pylori urease subunit B gene and its expression in tobacco (Nicotiana tabacum L.). Plant Cell Rep., 24: 532-539.
33. Hadjibabaie, M., N. Rastkari, A. Rezaie and M. Abdollahi, 2005. The Adverse Drug Reaction in the Gastrointestinal Tract: An overview. Intl. J. Pharmacol., 1: 1-8.
34. Haq, T.A., H.S. Mason, J.D. Clements and C.J. Arntzen 1995. Oral immunization with recombinant bacterial antigen produced in transgenic plants. Science, 268: 714-716.
35. Holmgren, J., C. Czerkinsky, K. Eriksson and A. Mharandi, 2003. Mucosal immunisation and adjuvants: A brief overview of recent advances and challenges. Vaccine, 21. Suppl 2: S 89-95.
36. Huang, Z., I. Dry, D. Webster, R. Strugnell and S. Wesselingh, 2001. Plant-derived measles virus hemagglutinin protein induces neutralizing antibodies in mice. Vaccine, 19: 2163-2171.
37. Huang, Z., C.J. Arntzen, H.S. Mason, G. Elkin, Y. Thanavala, B.J. Maloney and N. Beuhner, 2005. Virus-like particle expression and assembly in plants: Hepatitis Band Norwalk viruses. Vaccine, 23: 1851-1858.
38. Jani, D., N.K. Singh, S. Bhattacharya, A.K. Sharma, A.K. Tyagi, S. Bhattacharya, S.N. Upadhyay, L.S. Meena and Y. Singh, 2004. Studies on the immunogenic potential of plant-expressed cholera toxin B subunit. Plant Cell Rep., 22: 471-477.
39. Jani, D., L.S. Meena and Rizwan-ul-Haq, 2002. Expression of cholera toxin B subunit in transgenic tomato plants. Transgenic Res., 11: 447-454.
40. Joelson, T., L. Akerblom, P. Oxelfelt, B. Strandberg, K. Tomenius and T.J. Morris, 1997. Presentation of a foreign peptide on the surface of tomato bushy stunt virus. J. Gen. Virol., 78: 1213-1217.
41. Joensuu, J.J., M. Kotiaho, T. Riipi, T.H. Teeri, V. Niklander-Teeri, V. Snoeck, E. Cox, B.M. Goddeeris, E.T. Palva and H. Lng, 2004. Fimbrial subunit protein FaeG expressed in transgenic tobacco inhibits the binding of F4ac enterotoxigenic Escherichia coli to porcine enterocytes. Transgenic Res., 13: 295-298.
42. Joung, Y.H., J.W. Youm, J.H. Jeon, B.C. Lee, C.J. Ryu, H.J. Hong, H.C. Kim, H. Joung and H.S. Kim, 2004. Expression of the hepatitis B surface S and preS2 antigens in mbers of Solanum tuberosum. Plant Cell Rep., 22: 925-930.
43. Kapusta, J., T. Pniewski, M. Letellier, O. Lisowa, A.B. Legocki, A. Modelska, M. Figlerowicz, A. Plucienniczak, V. Yusibov and H. Koprowski, 1999. A plant-derived edible vaccine against hepatitis B virus. FASEB J., 13: 1796-1799.
44. Kapusta, J., A. Modelska, T. Pniewski, M. Figlerowicz, K. Jankowski, O. Lisowa, A. Plucienniczak, H. Koprowski and A.B. Legocki, 2001. Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Adv. Exp. Med. Biol., 495: 299-303.
45. Kang, T.J., N.H. Loc, M.O. Jang, Y.S. Jang, M.S. Yang, Y.S. Kim and J.E. Seo, 2003. Expression of the B subunit of E. coli heat-labile enterotoxin in the chloroplasts of plants and its characterization. Transgenic Res., 12:683-691.
46. Karasev, A., S. Foulke, C. Wellens, A. Rich, K.J. Shon, I. Zwierzynski, D. Hone, H. Koprowski and M. Reitz, 2005. Plant based HIV-1 vaccine canditate: Tat protein produced in spinach. Vaccine, 23:1875-1880.
47. mac Gag p27 capsid protein cholera toxin B subunit fusion protein in transgenic potato. Applied Biochem. Biotechnol. -Part B Mol. Biotechnol., 28: 33-40.
48. mac Gag p27 capsid protein gene expression in potato. Protein Exp. Pufif., 36: 312-317.
49. Kim, T.G. and W.H. Langridge, 2004. Synthesis of an HIV-1 Tat transduction domain-rotavirus enterotoxin fusion protein in transgenic potato. Plant Cell. Rep., 22: 382-387.
50. Kim, T.G., W.H. Langridge and A. Gruber, 2004. HIV-I gpl20, V3 cholera toxin B subunit fusion gene expression in transgenic potato. Protein Exp. Purif., 37: 196-202.
51. Kirk, D.D. and S.R. Webb, 2005. The next 15 years: Taking plant-made vaccines beyond proof of concept. Immunol Cell Biol., 83: 248-256.
52. Kong, Q., L. Richter, Yu Fang Yang, C.J. Arntzen, H.S. Mason and Y. Thanavala, 2001. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc. Natl. Acad. Sci. USA., 98: 11539-11544.
53. Koya, V., M. Moayeri, S.H. Leppla and H. Daniell, 2005. Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect Immun., 73: 8266-8274.
54. Kuroda, H. and P. Maliga, 2001. Sequence downstream of the translation initiation codon is important determinants of translation efficiency in chloroplasts. Plant Physiol., 125: 430-436.
55. Lauterslager, T.G., D.E. Florack, T.J. Van der Wal, J.W. Molthoff, J.P.M. Langeveld, D. Bosch, W.J.A. Boersma and L.A.Th. Hilgers, 2001. Oral immunisation of naive and primed animals with transgenic potato tubers expressing LT-B. Vaccine, 19: 2749-2755,
56. Liu, H.L., W.S. Li, T. Lei, J. Zheng, X.F. Yan, Y.L. Wang, L.S. Si, Z. Zhang and Z.Z. Wang, 2005. Expression of human papillomavirus type 16 L1 protein in transgenic tobacco plants, Acta Biochim, Biophys. Sin. (Shanghai), 37:153-158.
57. Lycke, N., 1997. The mechanism of cholera toxin adjuvaticity. Res. Immunol., 148: 504-520.
58. Ma, S. and A.M. Jevnikar, 1999. Autoantigens Produced in Plants for Oral Tolerance Therapy of Autoimmune Diseases. In: Shahidi et al. (Eds.). Chemicals Via Higher Plant Biotechnology. New York: Kluwer Academic Publishers/Plenum Publishers, pp: 179-194.
59. Ma, Y., Y. Gao, W.X. Luo, J. Zhang, N.S. Xia, S.Q. Lin and M. Li, 2003. Expression of ORF2 partial gene of hepatitis E virus in tomatoes and immunoactivity of expression products. World J. Gastroenterol., 9: 2211-2215.
60. Macrides, S.C., 1996. Strategies for achieving high-level expression of genes in Escherichia cola. Microbiol. Rev., 60: 512-538.
61. Maloney, B.J., N. Takeda, Y. Suzaki, Y. Ami, T. C. Li, T. Miyamura, C.J. Arntzen and H.S. Mason, 2005. Challenges in creating a vaccine to prevent hepatitis E. Vaccine, 23:1870-1874.
62. Mason, H.S., D.M.K. Lam and C.J. Arntzen, 1992. Expression of hepatitis B surface antigen in transgenic plants. Proc. Natl. Acad. Sci. USA., 89: 11745-11749.
63. Mason, H.S., J.J. Shi, C.J. Arntzen, J.M. Ball, X. Jiang and M.K. Estes, 1996. Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc. Natl. Acad Sci. USA., 93: 5335-5340.
64. Mason, H.S., T.A. Haq, J.D. Clements and C.J. Arntzen, 1998. Edible vaccine protects mice against Escherichia coli heat-labile enterotoxin (LT): Potatoes expressing a synthetic LT-B gene. Vaccine, 16: 1336-1343.
65. Marquet-Blouin, E., A. Steinmetz, F.B. Bouche and C.P. Muller, 2003. Neutralizing immunogenicity of transgenic carrot (Daucus carota L.)- derived measles virus hemagglutinin. Plant Mol. Biol., Mar., 51: 459-469,
66. Marusic, C., P. Rizza, L. Lattanzi, C. Mancini, M. Spada, F. Belardelli, E. Benvenuto and I. Capone, 2001. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. J. Virol., 75: 8434-8439.
67. McCluskie M.J., R.D. Weeratna, A.M. Krieg and H.L. Davis, 2000. CpG DNA is an effective oral adjuvant to protein antigen in mice. Vaccine, 19: 950-957.
68. McGarvey, P.B., J. Hammond, M.M. Dienelt, D.C. Hooper, Zhen Fang Fu, B. Dietzschold, H. Koprowski and F.H. Michaels, 1995. Expression of the rabies virus glycoprotein in transgenic tomatoes. Biotechnology, 13: 1484-1487.
69. McLain, L., N. Porta, G. Lomonossoff, Z. Durrani and N.J. Dimmock, 1995. Human immunodeficiency virus type 1 neutralising antibodies raised to a gp41 peptide expressed on the surface of a plant virus. AIDS Res. Hum. Retroviruses., 11: 327-34.
70. McLain, L., Z. Durrani, L. Wisniewski, C. Porta, G.P. Lomonossoff and N.J. Dimmock, 1996. Stimulation of neutralizing antibodies to human immunodeficiency virus type 1 in three strains of mice immunized with a 22 amino acid peptide of gp41 expressed on the surface of a plant virus. Vaccine, 14: 799-810.
71. Nemchinov, L.G., T.J. Liang, M.M. Rifaat, H. M. Mazyad, A. Hadidi and J. M. Keith, 2000. Development of a plant-derived subunit vaccine candidate against hepatitis C virus. Arch. Virol., 145: 2557-2573.
72. PhRMA., 2002 survey-new medicines in development biotechnology, www.pharma.org/newmedicines/resources/2002-10-21.93.pdf
73. Piazzolla, G., C. Tortorella, E. Panella, S. Antonaci, M. Nuzzaci, A. Natilla, P. Piazzolla, D. Boscia and A. De Stradis, 2005. A chimeric plant virus as a potential candidate for hepatitis C vaccine. J Hepatol., 40: 122-122.
74. Pizza, M., M. Giuliani, M. Fontana, E. Monaci, G. Douce, G. Dougan, K.H. Mills, R. Rappuoli and G. Del Giudice, 2001. Mucosal vaccines: Non-toxic derivatives of LT and CT as mucosal adjuvants. Vaccine, 19: 2534-2541.
75. Pogrebnyak, N., M. Golovkin, V. Andrianov, S. Spitsin, Y. Smimov, R. Egolfand H. Koprowski, 2005. Sever Acute Respiratory Syndrome (SARS) S protein production in plants: Development of recombinant vaccine. Proc. Natl. Acad. Sci. USA., 102: 9062-9067.
76. Porta, C., V. Spall, J. Loveland, J.E. Johnson, P.J. Barker and G.P. Lomonossoff, 1994. Development of cowpea mosaic virus as a high-yielding system for the presentation of foreign peptides. Virology, 202: 949-955.
77. Rezaie, A., B. Taghavi-Bayat and M. Abdollahi, 2005. Biologic Management of Fistulizing Crohn's Disease. Intl. J. Pharmacol., 1: 17-24.
78. Richter, L.J. and P.B. Kipp, 1999. Transgenic plants as edible vaccines. Curr. Topics Microbiol. Immunol., 240:159-176.
79. Richter, L.J., Y. Thanavala, C.J. Arntzen and H.S. Mason, 2000. Production of hepatitis B surface antigen in transgenic plants for oral immunization. Natl. Biotechnol., 18:1167-1171.
80. Rigano, M.M. and A.M. Walmsley, 2005. Expression system and developments in plant-made vaccines. Immunol. Cell. Biol., 83:271-277.
81. Rigano, M.M., S. Dreitz, A.P. Kipnis, A.A. Izzo and A.M. Walmsley, 2006. Oral immunogenicity of a plant-made, subunit, tuberculosis vaccine. Vaccine. 24: 691-695.
82. Sala, F., M. Manuela Rigano, A. Barbante, B. Basso, A.M. Walmsley and S. Castiglione, 2003. Vaccine antigen production in transgenic plants: Strategies, gene constructs and perspectives. Vaccine, 21: 803-808.
83. Sandhu, J.S., S.F. Krasnyanski, L.L. Domier, S.S. Korban, M.D. Osadjan and D.E. Buetow. 2000. Oral immunization of mice with transgenic tomato fruit expressing respiratory syncytial virus-F protein induces a systemic immune response. Transgenic Res., 9: 127-135.
84. Schillberg, S., R.M. Twyman and R.M. Fischer, 2005. Opportunities for recombinant antigen and antibody expression in transgenic plants-biotechnology assessment. Vaccine. 23 (15 SPEC. ISS): 1764-1769.
85. Shchelkunov, S.N., R.K. Saliaev, T.S. Ryzhoya, S.G. Pozdniakov, A.E. Nesterov, N.I. Rekoslavskaia, V.M. Sumtsova, N.V. Pakova, U.O. Mishutina, T.V. Kopytina and R.V. Hammond, 2004. Designing of a candidate edible vaccine against hepatitis B and HIV on the basis of a transgenic tomato. Vestn Ross Akad Med. Nauk., Russian, 11: 50-55.
86. Shin, E.A, J.Y. Lee, T.G. Kim, Y.K. Park and W.H. Langridge. 2005. Synthesis and assembly of an adjuvanted Porphyromonas gingivalis fimbrial antigen fusion protein in plants. Protein Expr Purif. In Press, Corrected Proof, Available online 5 October 2005.
87. Sijmons, O.C., B.M.N. Dekker, B. Schrammeijer, R.C. Vorwoerd, P.J.M. Van den Elzen, A. Hoekema, 1990. Production of correctly processed human serum albumin in transgenic plants. Biotechnology, 8: 217-221.
88. Smith, M.L., M.L. Shuler, L. Richter, C.J. Arntzen and H.S. Mason, 2003. Structural characterization of plant-derived hepatitis B surface antigen employed in oral immunization studies. Vaccine, 21:4011-4021.
89. Stoger, E., M. Sack and Y. Perrin, 2002. Practical considerations for pharmaceutical antibody production in different crop systems. Mol. Breed., 9: 149-158.
90. Streatfield, S.J., J.M. Mayor, D.K. Barker, C. Brooks, B.J. Lamphear, S.L. Woodard, K.K. Beifuss, D.V. Vicuna, L.A. Massey, M.E. Horn, D.E. Delaney, Z.L. Nikolov, E.E. Hood, J.M. Jilka and J.A. Howard, 2002. Development of an edible subunit vaccine in com against enterotoxigenic strains of Escherichia coli. In vitro Cell. Dev. Biol. Plant., 38:11-17
91. Sun, M., K. Qian and N. Su, 2003. Foot and moot disease virus VP1 protein fused with cholera toxin B subunit expressed in Chlamydomonas reinhardtii chloroplast. Biotechnol. Lett., 25: 1087-1092.
92. Tacket, C.O., G. Losonsky, M.M. Levine, H.S. Mason, C.J. Arntzen and J.D. Clements, 1998. Immunogenicity in humans of a recombinant bacterial antigen delivered in a transgenic potato. Natl. Med., 4: 607-609.
93. Tacket, C.O., H.S. Mason, G. Losonsky, M.K. Estes, M.M. Levine and C. J. Arntzen, 2000. Human immune responses to a novel Norwalk virus vaccine delivered in transgenic potatoes. J. Infect. Dis., 182:302-365.
94. Tacket, C.O., M.F. Pasetti, R. Edelman, J.A. Howard, S. Streatfield, 2004. Immunogenicity of recombinant LT-B delivered orally to humans in transgenic com. Vaccine, 2: 4385-4389.
95. Thanavala, Y., S. Pal, A. Scott, M. Mahoney, N. Natarajan, P. Goodwin, L. Richter, C.J. Arntzen and H.S. Mason, 2005. Immunogenicity in humans of an edible vaccine for hepatitis B. Proc. Natl. Acad. Sei. USA., 102: 3378-3382.
96. Tregoning, J.S., H. Kuroda, Z. Svab, P. Maliga, P. Nixon, S. Clare, F. Bowe, N. Fairweather, G. Dougan, J. Ytterberg and K.J. Van Wijk, 2003. Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Res., 31: 1174-1179.
97. Tregoning, J.S., S. Clare, F. Bowe, L. Edwards, N. Fairweather, O. Qazi, P.J. Nixon, P. Maliga, G. Dougan and T. Hussell, 2005. Protection against tetanus toxin using a plant-based vaccine. Eur. J. Immunol., 35: 1320-1326.
98. Verch, T., V. Yusibov and H. Koprowski, 1998. Expression and assembly of a full-length monoclonal antibody in plants using a plant virus vector. J. Immunol. Methods, 220: 69-75.
99. Wagner, B., K. Hufnagl, C. Radauer, S. Wagner, K. Baier, O. Scheiner, U. Wiedermann and H. Breiteneder, 2004. Expression of the B subunit of the heat-labile enterotoxin of Escherichia coli in tobacco mosaic virus-infected Nicitiana benthamiana plants and its characterization as mocusal immunogen and adjuant. J. Immunol. Methods, 287:203-215.
100. Walmsley, A.M. and C.J. Arntzen, 2003. Plant cell factories and mucosal vaccines. Curr. Opin. Biotechnol., 14: 145-150.
101. Walmsley, A.M., D.D. Kirk, H.S. Mason, M.L. Alvarez, Y. Jin, J. Pinkhasov, M.M. Rigano, C.J. Arntzen and S.M. Lee, 2003. Expression of the B subunit of Escherichia coli heat-labile enterotoxin as a fusion protein in transgenic tomato. Plant Cell Rep., 21: 1020-1026.
102. Warzecha, H., H.S. Mason, A. Tryggvesson, C. Lane, R.C. Rose, E. Rybicki, A.L. Williamson and J.D. Clements, 2003. Oral immunogenicity of human papillomavirus-like particles expressed in potato. J. Virol., 77:8702-8711.
103. Watson, J., V. Koya, H. Daniell and S.H. Leppla, 2004. Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a non-food/feed crop. Vaccine, 22: 4374-4384.
104. Webster, D.E., M.L. Cooney, Z. Huang, D. R. Drew, I.A. Ramshaw, I. B. Dry, R. A. Strugnell, J. L. Martin and S. L. Wesselingh, 2002. Successful boosting of a DNA measles immunization with an oral plant-derived measles virus vaccine. J. Virol., 76:7910-7912.
105. Wright, K.E., F. Prior, R. Sardana, I. Altosaar, A.K. Dudani, P.R. Ganz and E.S. Tackaberry, 2001. Sorting of glycoprotein B from human cytomegalovirus to protein storage vesicles in seeds of transgenic tobacco. Transgenic Res., 10:177-181.
106. Wu, Y.Z., J.T. Li, Z.R. Mou, L. Fei, B. Ni, M. Geng, Z.C. Jia, W. Zhou, L.Y. Zou and Y. Tang, 2003. Oral immunization with rotavirus VP7 expressed in transgenic potatoes induced high titers of mucosal neutralizing IgA. Virology, 313: 337-242.
107. Yu, J. and W.H. Langridge, 2001. A plant-based multicomponent vaccine protects mice from enteric diseases. Nat Biotechnol., 19: 548-552.
108. Yu, J. and W.H. Langride, 2003. Expression of rotavirus capsid protein VP6 in transgenic potato and its oral immunogenicity in mice. Transgenic Res., 12:163-169.
109. Yusibov, V., A. Modelska, K. Steplewski, D.C. Hooper, H. Koprowski, M. Agadjanyan and D. Weiner, 1997. Antigens produced in plants by infection with chimeric plant viruses immunize against rabies virus and HIV-1. Proc. Natl Acad. Sci. USA., 94: 5784-5788.
110. Yusibov, V., D.C. Hooper, S.V. Spitsin, N. Fleysh, R.B. Kean, T. Mikheeva, D. Deka, A. Karasev, S. Cox, J. Randall and H. Koprowski, 2002. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine, 20: 3155-3164.
111. Zhang, G.G., C. Leung and L. Murdin, 2000. In planta expression of HIV-1 p24 protein using RNA plant virus-based expression vector. Mol. Biotechnol., 14: 99-107.
112. Zhang, G.G., L. Rodrigues, B. Rovinski and K.A. White, 2002. Production of HIV-1 p24 protein in transgenic tobacco plants. Mol. Biotechnol., 20: 131-136.