Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-19T14:44:51.491Z Has data issue: false hasContentIssue false
  • English
  • Français

Plant-made vaccines: biotechnology and immunology in animal health

Published online by Cambridge University Press:  08 March 2007

J. Rice ,
W. M. Ainley  and
P. Shewen
J. Rice*
Affiliation:
Dow AgroSciences, 9330 Zionsville Road, Indianapolis, IN 46268, USA
W. M. Ainley
Affiliation:
Dow AgroSciences, 9330 Zionsville Road, Indianapolis, IN 46268, USA
P. Shewen
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada, N1G 2W1
*
*Corresponding author: Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The use of plants as production systems for vaccine antigens has been actively investigated over the last 15 years. The original research focused on the value of this expression system for oral delivery based on the hypothesis that plant-expressed antigens would be more stable within the digestive tract and would allow for the use of the oral route of administration to stimulate a mucosal immune response. However, while first conceived for utility via the oral route, plant-made antigens have also been studied as classical immunogens delivered via a needle to model animal systems. Antigens have been expressed in a number of whole plant and cell culture systems. Several alternative expression platforms have been developed to increase expression of antigens or to elicit preferred immunological responses. The biotechnological advances in plant expression and the immunological testing of these antigens will be reviewed in this paper focusing primarily on diseases of livestock and companion animals.

Keywords

plant-madevaccineimmunogenicityanimal health
Type
Research Article
Information
Animal Health Research Reviews , Volume 6 , Issue 2 , December 2005 , pp. 199 - 209
Copyright
Copyright © CAB International 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abler, ML and Green, PJ (1996). Control of mRNA stability in higher plants. Plant Molecular Biology 32: 63–78.CrossRefGoogle ScholarPubMed
Arakawa, T, Yu, J, Chong, DKX, Hough, J, Engen, PC and Langridge, WHR (1998). A plant-based cholera toxin B subunit-insulin fusion protein protects against the development of autoimmune diabetes. Nature Biotechnology 16: 934–938.CrossRefGoogle ScholarPubMed
Arntzen, C, Plotkin, S and Dodet, B (2005). Plant-derived vaccines and antibodies: potential and limitations. Vaccine 23: 1753–1756.CrossRefGoogle ScholarPubMed
Bakker, HAC, Florack, DEA, Bosch, HJ and Rouwendal, GJA (2003). Optimizing protein glycosylation in transgenic plants using plant/mammalian or mammalian/mammalian (human) chimeric glycosyltransferases for antibody production. World Patent Application; WO 2003/078637.Google Scholar
Brendel, V, Kleffe, J, Carle-Urioste, JC and Walbot, V (1998). Prediction of splice sites in plant pre-mRNA from sequence properties. Journal of Molecular Biology 276: 85–104.CrossRefGoogle ScholarPubMed
Cardineau, G, Mason, H, Van Eck, J, Kirk, D and Walmsley, A (2004). Vectors and cells for preparing immunoprotective compositions derived from transgenic plants. World Patent Application; WO 2004/098533.Google Scholar
Carter, JE IIILangridge, WHR (2002). Plant-based vaccines for protection against infectious and autoimmune diseases. Critical Reviews in Plant Sciences 21: 93–109.CrossRefGoogle Scholar
Castañón, M, Marín, J, Martín-Alonso, J, Boga, J, Casais, R, Humara, J, Ordás, R and Parra, F (1999). Immunization with potato plants expressing VP60 protein protects against rabbit hemorrhagic disease virus. Journal of Virology 73: 4452–4455.CrossRefGoogle ScholarPubMed
Castanon, S, Martin-Alonso, JM, Marin, MS, Boga, JA, Alonso, P, Parra, F and Ordas, RJ (2002). The effect of the promoter on expression of VP60 gene from rabbit hemorrhagic disease virus in potato plants. Plant Science (Shannon, Irel) 162: 87–95.CrossRefGoogle Scholar
Chargelegue, D, Obregon, P and Drake, PM (2001). Transgenic plants for vaccine production: expectations and limitations. Trends in Plant Science 6: 495–496.CrossRefGoogle ScholarPubMed
Chikwamba, R, Cunnick, J, Hathaway, D, McMurray, J, Mason, H and Wang, K (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 Research 11: 479–493.CrossRefGoogle Scholar
Curtiss, R and Cardineau, C (1990). Oral immunization by transgenic plants. World Patent Application; 5,679,880.Google Scholar
D'Aoust, MA, Busse, U, Martel, M, Faye, L and Levesque, LP (2002). Alfalfa: an efficient bioreactor for continuous recombinant protein production. In: Erickson, L (ed.) Molecular Farming of Plants and Animals for Human and Veterinary Medicine. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 33–47.CrossRefGoogle Scholar
Dalsgaard, K, Uttenthal, A, Jones, TD, Xu, F, Merryweather, A, Hamilton, WD, Langeveld, JP, Boshuizen, RS, Kamstrup, S, Lomonossoff, GP, Porta, C, Vela, C, Casal, JI, Meloen, RH and Rodgers, PB (1997). Plant-derived vaccine protects target animals against a viral disease. Nature Biotechnology 15: 248–252.CrossRefGoogle ScholarPubMed
Daniell, H, Lee, S, Tanvi, P and Wiebe, P (2001). Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. Journal of Molecular Biology 311: 1001–1009.CrossRefGoogle ScholarPubMed
Daniell, H, Chebolu, S, Kumar, S, Singleton, M and Falconer, R (2005). Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine 23: 1779–1783.CrossRefGoogle ScholarPubMed
Denecke, J, Botterman, J and Deblaere, R (1990). Protein secretion in plant cells can occur via a default pathway. Plant Cell 2: 51–59.Google Scholar
Dertzbaugh, MT and Elson, CO (1993). Comparative effectiveness of the cholera toxin B subunits and alkaline phosphatase as carrier for oral vaccines. Infection and Immunity 61: 48–55.CrossRefGoogle ScholarPubMed
Dus Santos, MJ and Wigdorovitz, A (2005). Transgenic plants for the production of veterinary vaccines. Immunology and Cell Biology 83: 229–238.CrossRefGoogle ScholarPubMed
Dus Santos, MJ, Carrillo, C, Ardila, F, Rios, RD, Franzone, P, Piccone, ME, Wigdorovitz, A and Borca, MV (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.CrossRefGoogle ScholarPubMed
Erickson, L, Yu, WJ, Tuboly, T, Nagy, E, Bailey, A, Zhang, J, Yoo, D and Du, S (2002). Edible vaccines in plants for livestock pathogens. In: Erickson, L (ed.) Molecular Farming of Plants and Animals for Human and Veterinary Medicine. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 339–367.CrossRefGoogle Scholar
Gallie, DR (2002). The 5'-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Research 30: 3401–3411.CrossRefGoogle ScholarPubMed
Gallie, DR, Sleat, DE, Watts, JW, Turner, PC and Wilson, TM (1987). The 5'-leader sequence of tobacco mosiac virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Research 15: 3257–3273.CrossRefGoogle Scholar
Gomez, N, Wigdorovitz, A, Castanon, A, Gil, F, Ordas, R, Borca, MV and Escribano, JM (2000). Oral immunogenicity of the plant derived spike protein from swine-transmissible gastroenteritis coronavirus. Archives of Virology 145: 1725–1732.CrossRefGoogle ScholarPubMed
Gomord, V and Faye, L (2004). Posttranslational modification of therapeutic proteins in plants. Current Opinion in Plant Biology 7: 171–181.CrossRefGoogle ScholarPubMed
Haq, T, Mason, H, Clements, J and Arntzen, C (1995). Oral immunization with recombinant bacterial antigen produced in transgenic plants. Science 268: 714–716.CrossRefGoogle ScholarPubMed
Hellwig, S, Drossard, J, Twyman, RM and Fischer, R (2004). Plant cell cultures for the production of recombinant proteins. Nature Biotechnology 22: 1415–1422.CrossRefGoogle ScholarPubMed
Horn, ME, Pappu, KM, Bailey, MR, Clough, RC, Barker, M, Jilka, JM, Howard, JA and Streatfield, SJ (2003). Advantageous features of plant-based systems for the development of HIV vaccines. Journal of Drug Targeting 11: 539–545.CrossRefGoogle ScholarPubMed
Hunt, AG (1994). Messenger RNA 3' end formation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 45: 47–60.CrossRefGoogle Scholar
Kang, TJ, Loc, NH, Jang, MO and Yang, MS (2004). Modification of the cholera toxin B subunit coding sequence to enhance expression in plants. Molecular Breeding 13: 143–153.CrossRefGoogle Scholar
Kapusta, J, Modelska, A, Figlerowicz, M, Pniewski, T, Letellier, M, Lisowa, O, Yusibov, V, Koprowski, H, Plucienniczak, A and Legocki, AB (1999). A plant-derived edible vaccine against hepatitis B virus. The FASEB Journal 13: 1796–1799.CrossRefGoogle ScholarPubMed
Kapusta, J, Modelska, A, Pniewski, T, Figlerowicz, M, Jankowski, K, Lisowa, O, Plucienniczak, A, Koprowski, H and Legocki, AB (2001). Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Advances in Experimental Medicine and Biology 495: 299–303.CrossRefGoogle ScholarPubMed
Kim, TG, Gruber, A and Langridge, WHR (2004a). HIV-1 gp120 V3 cholera toxin B subunit fusion gene expression in transgenic potato. Protein Expression and Purification 37: 196–202.CrossRefGoogle ScholarPubMed
Kim, TG, Gruber, A, Ruprecht, RM and Langridge, WHR (2004b). Synthesis and assembly of SIVmac Gag p27 capsid protein cholera toxin B subunit fusion protein in transgenic potato. Molecular Biotechnology 28: 33–40.CrossRefGoogle ScholarPubMed
Kim, TG, Ruprecht, R and Langridge, WHR (2004c). Synthesis and assembly of a cholera toxin B subunit SHIV 89.6p Tat fusion protein in transgenic potato. Protein Expression and Purification 35: 313–319.CrossRefGoogle ScholarPubMed
Kirk, D and Webb, S (2005). The next 15 years: taking plant-made vaccines beyond proof of concept. Immunology and Cell Biology 83: 248–256.CrossRefGoogle ScholarPubMed
Korban, SS (2002). Invited review: targeting and expression of antigenic proteins in transgenic plants for production of edible oral vaccines. In Vitro Cellular & Developmental Biology: Plant 38: 231–236.CrossRefGoogle Scholar
Lamphear, B, Streatfield, S, Jilka, J, Brooks, C, Barker, D, Turner, D, Delaney, D, Garcia, M, Wiggins, B, Woodard, S, Hood, E, Tizard, I, Lawhorn, B and Howard, J (2002). Delivery of subunit vaccines in maize seed. Journal of Controlled Release 85: 169–180.CrossRefGoogle ScholarPubMed
Lamphear, BJ, Jilka, JM, Kesl, L, Welter, M, Howard, JA and Streatfield, SJ (2004). A corn-based delivery system for animal vaccines: an oral transmissible gastroenteritis virus vaccine boosts lactogenic immunity in swine. Vaccine 22: 2420–2424.CrossRefGoogle ScholarPubMed
Langeveld, JP, Brennan, FR, Martinez-Torrecuadrada, JL, Jones, TD, Boshuizen, RS, Vela, C, Casal, JI, Kamstrup, S, Dalsgaard, K, Meloen, RH, Bendig, MM and Hamilton, WD (2001). Inactivated recombinant plant virus protects dogs from a lethal challenge with canine parvovirus. Vaccine 19: 3661–3670.CrossRefGoogle ScholarPubMed
Lee, RWH, Strommer, J, Hodgins, D, Shewen, PE, Niu, Y and Lo, RYC (2001). Towards development of an edible vaccine against bovine pneumonic pasteurellosis using transgenic white clover expressing a Mannheimia haemolytica A1 lkt50 fusion protein. Infection and Immunity 69: 5786–5793.CrossRefGoogle ScholarPubMed
Lee, RWH, Pool, AN, Ziauddin, A, Lo, RYC, Shewen, PE and Strommer, JN (2003). Edible vaccine development: stability of Mannheimia haemolytica A1 leukotoxin 50 in field-grown transgenic white clover. Molecular Breeding 11: 259–266.CrossRefGoogle Scholar
Legocki, AB, Miedzinska, K, Czaplinska, M, Plucieniczak, A and Wedrychowicz, H (2005). Immunoprotective properties of transgenic plants expressing E2 glycoprotein from CSFV and cysteine protease from Fasciola hepatica. Vaccine 23: 1844–1846.CrossRefGoogle ScholarPubMed
Ma, S, Huang, Y, Yin, Z, Menassa, R, Brandle, JE and Jevnikar, AM (2004). Induction of oral tolerance to prevent diabetes with transgenic plants requires glutamic acid decarboxylase (GAD) and IL-4. Proceedings of the National Academy of Sciences 101: 5680–5685.CrossRefGoogle ScholarPubMed
Ma, Y, Lin, SQ, Gao, Y, Li, M, Luo, WX, Zhang, J and Xia, NS (2003). Expression of ORF2 partial gene of hepatitis E virus in tomatoes and immunoactivity of expression products. World Journal of Gastroenterology 9: 2211–2215.CrossRefGoogle ScholarPubMed
Maloney, BJ, Takeda, N, Suzaki, Y, Ami, Y, Li, TC, Miyamura, T, Arntzen, CJ and Mason, HS (2005). Challenges in creating a vaccine to prevent hepatitis E. Vaccine 23: 1870–1874.CrossRefGoogle ScholarPubMed
Mason, HS, Lam, DM and Arntzen, CJ (1992). Expression of hepatitis B surface antigen in transgenic plants. Proceedings of the National Academy of Sciences 89: 11745–11749.CrossRefGoogle ScholarPubMed
Mason, HS, Ball, J, Shi, J, Jiang, X, Estes, M and Arntzen, C (1996). Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogeniciy in mice. Proceedings of the National Academy of Sciences 93: 5335–5340.CrossRefGoogle Scholar
Mason, HS, Haq, TA, Clements, JD and Arntzen, CJ (1998). Edible vaccine protects mice against Escherichia coli heat-labile enterotoxin (LT): potatoes expressing synthetic LT-B gene. Vaccine 16: 1336–1343.CrossRefGoogle ScholarPubMed
Miller, T, Fanton, M and Webb, S (2004). Stable immuno-prophylactic and therapeutic compositions derived from transgenic plant cells and methods for production. World Patent Application; WO 2004/098530.Google Scholar
Modelska, A, Dietzschold, B, Sleysh, N, Fu, ZF, Steplewski, K, Hooper, DC, Koprowski, H and Yusibov, V (1998). Immunization against rabies with plant-derived antigen. Proceedings of the National Academy of Sciences 95: 2481–2485.CrossRefGoogle ScholarPubMed
Molina, A, Hervas-Stubbs, S, Daniell, H, Mngo-Castel, AM and Veramendi, J (2004). High yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnology 2: 141–153.CrossRefGoogle ScholarPubMed
Molina, A, Veramendi, J and Hervas-Stubbs, S (2005). Induction of neutralizing antibodies by a tobacco chloroplast-derived vaccine based on a B cell epitope form canine parvovirus. Virology 342: 266–275.CrossRefGoogle Scholar
Moloney, MM (2002). Plant molecular farming: using oleosin partitioning technology in oilseeds. In: Hood, EE and Howard, JA (eds) Plants as Factories for Protein Production. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 55–75.CrossRefGoogle Scholar
Mor, TS and Mason, HS (2004). Plants as a source for subunit vaccines. In: Christou, P and Klee, H (eds) Handbook of Plant Biotechnology. Chichester, UK: John Wiley & Sons, pp. 769–780.Google Scholar
Mor, TS, Mason, HS, Arntzen, CJ, Cardineau, GA and Kirk, DD (2003). Plants as a production and delivery vehicle for orally delivered subunit vaccines. In: Levine, MM (ed.) New Generation Vaccines. New York, NY: Marcel Dekker, pp. 305–311.Google Scholar
Muller, CP, Fack, F, Damien, B and Bouche, FB (2003). Immunogenic measles antigens expressed in plants: role as an edible vaccine for adults. Vaccine 21: 816–819.CrossRefGoogle ScholarPubMed
Nagata, T, Nemoto, Y and Hasezawi, S (1992). Tobacco BY-2 cell line as the 'HeLa' cell in the cell biology of higher plants. International Review of Cytology 132: 1–29.CrossRefGoogle Scholar
Napier, JA, Richard, G and Shewry, R (2005). Trafficking and stability of heterologous proteins in transgenic plants. In: Cunningham, LC and Porter, AJR (eds) Methods in Biotechnology: Vol. 3: Recombinant Proteins from Plants: Production and Isolation of Clinically Useful Compounds. Totowa, NJ: Humana Press, pp. 189–202.Google Scholar
Ni, M, Cui, D, Einstein, J, Narasimhulu, S, Vergara, CE and Gelvin, SB (1995). Strength and tissue specificity of chimeric promoters derived from the octopine and mannopine synthase genes. Plant Journal 7: 661–676.CrossRefGoogle Scholar
O'Dowd, AM, Botting, CH, Precious, B, Shawcross, R and Randall, RE (1999). Novel modifications to the C-terminus of LTB that facilitate site-directed chemical coupling of antigens and the development of LTB as a carrier for mucosal vaccines. Vaccine 17: 1442–1453.CrossRefGoogle Scholar
Prasad, V, Satyavathi, VV, Sanjaya, KM, Valli, KM, Khandelwal, A, Shaila, MS and Lakshmi Sita, G (2004). Expression of biologically active hemagglutinin–neuraminidase protein of Peste des petits ruminants virus in transgenic pigeonpea [Cajanus cajan (L) Millsp.]. Plant Science (Amsterdam) 166: 199–205.CrossRefGoogle Scholar
Rigano, MM, Sala, F, Arntzen, CJ and Walmsley, AM (2003). Targeting of plant-derived vaccine antigens to immunoresponsive mucosal sites. Vaccine 21: 809–811.CrossRefGoogle ScholarPubMed
Rigano, M, Alvarez, M, Pinkhasov, J, Jin, Y, Sala, F, Arntzen, C and Walmsley, A (2004). Production of a fusion protein consisting of the enterotoxigenic Escherichia coli heat-labiletoxin B subunit and a tuberculosis antigen in Arabidopsis thaliana. Plant Cell Reports 22: 502–508.CrossRefGoogle Scholar
Sala, F, Rigano, MM, Barbante, A, Basso, B, Walmsley, AM and Castiglione, S (2005). Vaccine antigen production in transgenic plants: strategies, gene constructs and perspectives. Vaccine 21: 803–808.CrossRefGoogle Scholar
Sandhu, JS, Krasnyanski, SF, Domier, LL, Korban, SS, Osadjan, MD and Buetow, DE (2000). Oral immunization of mice with transgenic tomato fruit expressing respiratory syncytial virus-F protein induces a systemic immune response. Transgenic Research 9: 127–135.CrossRefGoogle ScholarPubMed
Satyavathi, VV, Prasad, V, Khandelwhal, A, Shala, MS and Sita, G (2003). Expression of the hemagglutinin protein of Rinderpest virus in transgenic pigeon pea [Cajanus cajan (L.) Millsp.] plants. Plant Cell Reproduction 21: 651–658.CrossRefGoogle Scholar
Savelyeva, N, Zhu, D and Stevenson, FK (2003). Engineering DNA vaccines that include plant virus coat proteins. Biotechnology and Genetic Engineering Reviews 20: 101–114.CrossRefGoogle ScholarPubMed
Scholthof, KB, Mirkov, TE and Scholthof, HB (2002). Plant virus gene vectors: biotechnology applications in agriculture and medicine. Genetic Engineering 24: 67–85.Google ScholarPubMed
Seki, T, Fujiyama, K and Yoshida, T (2000). Manufacturing glycoproteins having human-type glycosylation using plants expressing human glycosyltransferases. World Patent Application; WO 2000/34490.Google Scholar
Shchelkunov, SN, Salyaev, RK, Rekoslavskaya, NI, Ryzhova, TS, Pozdnyakov, SG, Sumtsova, VM, Pakova, NV, Mishutina, UO, Kopytina, TV and Hammond, R (2004). The obtaining of transgenic tomato plant producing chimerical proteins TBI-HBsAg. Doklady Biochemistry and Biophysics 396: 139–142.CrossRefGoogle ScholarPubMed
Snowden, SL and Langridge, WHR (2003). Plant-based mucosal immunization. Biotechnology & Genetic Engineering Reviews 20: 165–182.CrossRefGoogle ScholarPubMed
Sonnewald, U, Hajirezaei, MR, Biemelt, S and Mueller, M (2003). Designer tubers for production of novel compounds. In: Congress Proceedings, BCPC International Congress: Crop Science and Technology. Bracknell, UK (ed.) Glasgow, UK, BCPC, pp. 123–132.Google Scholar
Streatfield, S (2005). Oral hepatitis B vaccine candidates produced and delivered in plant material. Immunology and Cell Biology 83: 257–262.CrossRefGoogle ScholarPubMed
Streatfield, SJ and Howard, JA (2003). Plant-based vaccines. International Journal for Parasitology 33: 479–493.CrossRefGoogle ScholarPubMed
Streatfield, SJ, Jilka, JM, Hood, EE, Turner, DD, Bailey, MR, Mayor, JM, Woodard, SL, Beifuss, KK, Horn, ME, Delaney, DE, Tizard, IR and Howard, JA (2001). Plant-based vaccines: unique advantages. Vaccine 19: 2742–2748.CrossRefGoogle ScholarPubMed
Streatfield, SJ, Lane, JR, Brooks, CA, Barker, DK, Poage, ML, Mayor, JM, Lamphear, BJ, Drees, CF, Jilka, JM, Hood, EE and Howard, JA (2003). Corn as a production system for human and animal vaccines. Vaccine 21: 812–815.CrossRefGoogle Scholar
Tacket, CO (2005). Plant-derived vaccines against diarrheal diseases. Vaccine 23: 1866–1869.CrossRefGoogle ScholarPubMed
Tacket, CO, Mason, HS, Losonsky, G, Clements, JD, Levine, MM and Arntzen, CJ (1998). Immunogenicity in humans of a recombinant bacterial antigen delivered in transgenic potato. Nature Medicine 4: 607–609.CrossRefGoogle ScholarPubMed
Tacket, CO, Mason, HS, Losonsky, G, Estes, MK, Levine, MM and Arntzen, CJ (2000). Human immune responses to a novel norwalk virus vaccine delivered in transgenic potatoes. Journal of Infectious Diseases 182: 302–305.CrossRefGoogle ScholarPubMed
Tacket, CO, Pasetti, MF, Edelman, R, Howard, JA and Streatfield, S (2004). Immunogenicity of recombinant LT-B delivered orally to humans in transgenic corn. Vaccine 22: 4385–4389.CrossRefGoogle ScholarPubMed
Thanavala, Y, Mahoney, M, Pal, S, Scott, A, Richter, L, Natarajan, N, Goodwin, P, Arntzen, CJ and Mason, H (2005). Immunogenicity in humans of an edible vaccine for hepatitis B. Proceedings of the National Academy of Sciences 102: 3378–3382.CrossRefGoogle ScholarPubMed
Tizard, I (2004). Veterinary Immunology, An Introduction. 7th edn. Philadelphia, PA: W.B. Saunders.Google Scholar
Tregoning, JS, Nixon, P, Kuroda, H, Svab, Z, Clare, S, Bowe, F, Fairweather, N, Ytterberg, J, van Wijk, KJ, Dougan, G and Maliga, P (2003). Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Research 31: 1174–1179.CrossRefGoogle ScholarPubMed
Tuboly, T, Yu, W, Bailey, A, Degrandis, S, Du, S, Erickson, L and Nagy, E (2000). Immunogenicity of porcine transmissible gastroenterititis virus spike protein expressed in plants. Vaccine 18: 2023–2028.CrossRefGoogle Scholar
Walmsley, AM and Arntzen, CJ (2003). Plant cell factories and mucosal vaccines. Current Opinion in Biotechnology 14: 145–150.CrossRefGoogle ScholarPubMed
Walmsley, AM, Alvarez, ML, Jin, Y, Kirk, DD, Lee, SM, Pinkhasov, J, Rigano, MM, Arntzen, CJ and Mason, HS (2003). Expression of the B subunit of Escherichia coli heat-labile enterotoxin as a fusion protein in transgenic tomato. Plant Cell Reports 21: 1020–1026.CrossRefGoogle Scholar
Wigdorovitz, A, Carillo, C, Dus Santos, M, Trono, K, Peralta, A, Gómez, M, Rios, R, Franzone, F, Sadir, A, Escribano, J and Borca, M (1999). Induction of a protective antibody response to foot and mouth disease virus in mice following oral or parenteral immunization with alfalfa transgenic plants expressing the viral structural protein VP1. Virology 255: 347–353.CrossRefGoogle ScholarPubMed
Wigdorovitz, A, Mozgovoj, M, Dus Santos, MJ, Parreno, V, Gomez, C, Perez-Filgueira, DM, Trono, KG, Rios, RD, Franzone, PM, Fernandez, F, Carrillo, C, Babiuk, LA, Escribano, JM and Borca, MV (2004). Protective lactogenic immunity conferred by an edible peptide vaccine to bovine rotavirus produced in transgenic plants. Journal of General Virology 85: 1825–1832.CrossRefGoogle ScholarPubMed
Wu, H, Singh, NK, Locy, RD, Scissum-Gunn, K and Giambrone, JJ (2004a). Expression of immunogenic VP2 protein of infectious bursal disease virus in Arabidopsis thaliana. Biotechnology Letters 26: 787–792.CrossRefGoogle ScholarPubMed
Wu, H, Singh, NK, Locy, RD, Scissum-Gunn, K and Giambrone, JJ (2004b). Immunization of chickens with VP2 protein of infectious bursal disease virus expressed in Arabidopsis thaliana. Avian Diseases 48: 663–668.CrossRefGoogle ScholarPubMed
Yu, J and Langridge, W (2001). A plant-based multicomponent vaccine protects mice from enteric diseases. Nature Biotechnology 19: 548–552.CrossRefGoogle ScholarPubMed
Zhang, GG (2002). Use of plant virus-based expression systems for the production of HIV vaccines. In: Erickson, L (ed.) Molecular Farming of Plants and Animals for Human and Veterinary Medicine. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 155–177.CrossRefGoogle Scholar
Ziauddin, A, Lee, RWH, Lo, R, Shewen, P and Strommer, J (2004). Transformation of alfalfa with a bacterial fusion gene, Mannheimia haemolytica A1 leukotoxin50-gfp: response with Agrobacterium tumefaciens strains LBA4404 and C58. Plant Cell, Tissue and Organ Culture 79: 271–278.CrossRefGoogle Scholar