Current status of plant-made vaccines for veterinary purposes

Expert Review of Vaccines

Volumn 9, Issue 8, 2010, Pages 971-982

  Ling, Huai Yian ^a   Pelosi, Assunta ^a   Walmsley, Amanda M ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

mucosal delivery; plant vaccines; regulations; veterinary

Indexed keywords

CARROT EXTRACT; HEAT LABILE TOXIN B SUBUNIT; MAIZE SEED EXTRACT; PEANUT LEAF EXTRACT; PLANT EXTRACT; RECOMBINANT VACCINE; RICE EXTRACT; SUBUNIT VACCINE; TOMATO LEAF EXTRACT; UNCLASSIFIED DRUG; VACCINE; VIGNA UNGUICULATA EXTRACT; VP1 HEPATITIS B CORE FUSION PROTEIN; ESCHERICHIA COLI VACCINE; VIRUS VACCINE;

ALFALFA; ANTIGEN SPECIFICITY; AVIAN INFLUENZA; BIRD DISEASE; DIARRHEA; DRUG EFFICACY; ENTEROTOXIGENIC ESCHERICHIA COLI; FOOT AND MOUTH DISEASE; IMMUNE RESPONSE; IMMUNOGENICITY; MEDICINAL PLANT; MUCOSAL IMMUNITY; NONHUMAN; POULTRY; PRIORITY JOURNAL; REVIEW; STABLE EXPRESSION; TRANSGENIC PLANT; TRANSIENT EXPRESSION; VACCINATION; VACCINE PRODUCTION; VETERINARY MEDICINE; ANIMAL; BIOSYNTHESIS; BIOTECHNOLOGY; BIRD; ESCHERICHIA COLI INFECTIONS; FOOT-AND-MOUTH DISEASE; GENETICS; INFLUENZA IN BIRDS; METABOLISM; NEWCASTLE DISEASE; PHARMACEUTICS; PROCEDURES; VETERINARY;

ANIMALS; BIOTECHNOLOGY; BIRDS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI VACCINES; FOOT-AND-MOUTH DISEASE; INFLUENZA IN BIRDS; NEWCASTLE DISEASE; PLANTS, GENETICALLY MODIFIED; TECHNOLOGY, PHARMACEUTICAL; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 77955240271     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.10.87     Document Type: Review

References (97)

1. Joensuu JJ, Niklander-Teeri V, Brandle JE. Transgenic plants for animal health: plant-made vaccine infectious disease control. Phytochem. Rev. 7, 553-577 (2008).
2. Fouchier RAM, Munster V, Wallensten A et al. Characterization of a novel influenza-a virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79(5), 2814-2822 (2005).
3. Treanor J. Influenza vaccine - outmaneuvering antigenic shift and drift. N. Engl. J. Med. 350(3), 218-220 (2004).
4. Macken CA, Webby RJ, Bruno WJ. Genotype turnover by reassortment of replication complex genes from avian influenza A virus. J. General Virol. 87(10), 2803-2815 (2006).
5. D'Aoust MA, Lavoie PO, Couture MM et al. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J. 6(9), 930-940 (2008).
6. Shoji Y, Chichester JA, Bi H et al. Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 26(23), 2930-2934 (2008).
7. Shoji Y, Bi H, Musiychuk K et al. Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/ 05/05 strain of avian influenza. Vaccine 27(7), 1087-1092 (2009).
8. Spitsin S, Andrianov V, Pogrebnyak N et al. Immunological assessment of plant-derived avian flu H5/HA1 variants. Vaccine 27(9), 1289-1292 (2009).
9. Meshcheryakova YA, Eldarov MA, Migunov AI et al. Cowpea mosaic virus chimeric particles bearing the ectodomain of matrix protein 2 (M2E) of the influenza A virus: production and characterization. Appl. Mol. Biology 43(4), 751-760 (2009).
10. Lamb RA, Collins PL, Kolakofsky D et al. Paramyxoviridae. In: Virus Taxonomy. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (Eds). Elsevier, Amsterdam, The Netherlands, 655-668
11. Phillips RJ, Samson ACR, Emmerson PT. Nucleotide sequence of the 5-terminus of Newcastle disease virus and assembly of the complete genomic sequence: agreement with the "rule of six". Arch. Virol. 143(10), 1993-2002 (1998).
12. Alexander DJ. Preface. In: Newcastle Disease. Alexander DJ (Ed.) Kluwer Academic Publishers, MA, USA, XI (1988).
13. Mihaliak CA, Webb SR, Miller T et al. Development of plant cell produced vaccines for animal health applications. In: Proceedings of US Animal Health Association. Greensboro, NC, USA, 158-163 (2005)
14. Berinstein A, Vazquez-Rovere C, Asurmendi S et al. Mucosal and systemic immunization elicited by Newcastle disease virus (NDV) transgenic plants as antigens. Vaccine 23(48-49), 5583-5589 (2005).
15. Gomez E, Chimeno Zoth S, Carrillo E, Estela Roux M, Berinstein A. Mucosal immunity induced by orally administered transgenic plants. Immunobiology 213(8), 671-675 (2008).
16. Guerrero-Andrade O, Loza-Rubio E, Olivera-Flores T, Fehervari-Bone T, Gomez-Lim MA. Expression of the Newcastle disease virus fusion protein in transgenic maize and immunological studies. Transg. Res. 15(4), 455-463.
17. Yang CD, Liao JT, Lai CY et al. Induction of protective immunity in swine by recombinant bamboo mosaic virus expressing foot-and-mouth disease virus epitopes. BMC Biotechnol. 7(1), 62 (2007).
18. Hahn B-S, Jeon I-S, Jung Y-J et al. Expression of hemagglutinin- neuraminidase protein of Newcastle disease virus in transgenic tobacco. Plant Biotechnol. Reports 1(2), 85-92 (2007).
19. Gomez E, Zoth SC, Asurmendi S, Vazquez Rovere C, Berinstein A. Expression of hemagglutinin- neuraminidase glycoprotein of Newcastle disease virus in agroinfiltrated Nicotiana benthamiana plants. J. Biotechnol. 144(4), 337-340 (2009).
20. Doel TR. FMD vaccines. Virus Res. 91(1), 81-99 (2003).
21. Alexandersen S, Zhang Z, Donaldson AI, Garland AJM. The pathogenesis and diagnosis of foot-and-mouth disease. J. Comparative Pathol. 129(1), 1-36 (2003).
22. Thompson D, Muriel P, Russell D et al. Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. Rev. Off. Int. Epizoot. 21(3), 675-687 (2002).
23. Blake A, Sinclair MT, Sugiyarto G. Quantifying the impact of foot and mouth disease on tourism and the UK economy. Tourism Economics 19(4), 449-465 (2003).
24. Mackay DKJ, Forsyth MA, Davies PR et al. Differentiating infection from vaccination in foot-and-mouth disease using a panel of recombinant, non- structural proteins in ELISA. Vaccine 16(5), 446-459 (1998).
25. Francis MJ, Hastings GZ, Brown F, McDermed J, Lu YA, Tam JP. Immunological evaluation of the multiple antigen peptide (MAP) system using the major immunogenic site of foot-and- mouth disease virus. Immunology 73(3), 249-254 (1991).
26. Berinstein A, Tami C, Taboga O, Smitsaart E, Carrillo E. Protective immunity against foot-and-mouth disease virus induced by a recombinant vaccinia virus. Vaccine 18(21), 2231-2238 (2000).
27. Hammond RW, Nemchinov LG. Plant production of veterinary vaccines and therapeutics. Plant-Produced Microb. Vaccines 332, 79-102 (2009).
28. Usha R, Rohll JB, Spall VE et al. Expression of an animal virus antigenic site on the surface of a plant virus particle. Virology 197, 366-374 (1993).
29. Wigdorovitz A, Perez Filgueira DM, Robertson N et al. Protection of mice against challenge with foot and mouth disease virus (FMDV) by immunization with foliar extracts from plants infected with recombinant tobacco mosaic virus expressing the FMDV structural protein VP1. Virology 264(1), 85-91 (1999).
30. Carrillo C, Wigdorovitz A, Oliveros JC et al. Protective immune response to foot-and-mouth disease virus with VP1 expressed in transgenic plants. J. Virol. 72(2), 1688-1690 (1998).
31. Wigdorovitz A, Carrillo C, Dus Santos MJ et al. Induction of a protective antibody response to foot and mouth disease virus in mice following oral or parenteral immunization with alfalfa rransgenic plants expressing the viral structural protein VP1. Virology 255(2), 347-353 (1999).
32. Carrillo C, Wigdorovitz A, Trono K et al. Induction of a virus-specific antibody response to foot and mouth disease virus using the structural protein VP1 expressed in transgenic potato plants. Viral Immunol. 14(1), 49-57 (2001).
33. Huang Y, Liang W, Wang Y et al. Immunogenicity of the epitope of the foot-and-mouth disease virus fused with a hepatitis B core protein as expressed in transgenic tobacco. Viral Immunol. 18, 668-677 (2005).
34. Pan L, Zhang Y, Wang Y et al. Foliar extracts from transgenic tomato plants expressing the structural polyprotein, P1-2A, and protease, 3C, from foot-and- mouth disease virus elicit a protective response in guinea pigs. Vet. Immunol. Immunopathol 121(1-2), 83-90 (2008).
35. Li Y, Sun M, Liu J, Yang Z, Zhang Z, Shen G. High expression of foot-and- mouth disease virus structural protein VP1 in tobacco chloroplasts. Plant Cell Reports 25(4), 329-333 (2006).
36. Lentz EM, Segretin ME, Morgenfeld MM et al. High expression level of a foot and mouth disease virus epitope in tobacco transplastomic plants. Planta 231(2), 387-395 (2010).
37. Dus Santos MJ, Carrillo C, Ardila F et al. 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(15), 1838-1843 (2005).
38. Nagy B, Fekete PZ. Enterotoxigenic Escherichia coli in veterinary medicine. Int. J. Med. Microbiol. 295(6-7), 443-454 (2005).
39. de Haan L, Verweij WR, Feil IK et al. Role of GM1 binding in the mucosal immunogenicity and adjuvant activity of the Escherichia coli heat-labile enterotoxin and its B subunit. Immunology 94(3), 424-430 (1998).
40. Clements JD, Hartzog NM, Lyon FL. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 6(3), 269-277 (1988).
41. Lebens M, Shahabi V, Backstrom M, Houze T, Lindblad N, Holmgren J. Synthesis of hybrid molecules between heat-labile enterotoxin and cholera toxin B subunits: potential for use in a broad-spectrum vaccine. Infect. Immun. 64(6), 2144-2150 (1996).
42. Rigano MM, Sala F, Arntzen CJ, Walmsley AM. Targeting of plant-derived vaccine antigens to immunoresponsive mucosal sites. Vaccine 21(7-8), 809-811 (2003).
43. Haq TA, Mason HS, Clements JD, Arntzen CJ. Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 268(5211), 714-716 (1995).
44. Mason HS, Haq TA, Clements JD, Arntzen CJ. Edible vaccine protects mice against Escherichia coll heat-labile enterotoxin (LT): potatoes expressing a synthetic LT-B gene. Vaccine 16(13), 1336-1343 (1998).
45. Lauterslager TGM, Florack DEA, van der Wal TJ et al. Oral immunisation of naive and primed animals with transgenic potato tubers expressing LT-B. Vaccine 19(17-19), 2749-2755 (2001).
46. Lamphear BJ, Streatfield SJ, Jilka JM et al. Delivery of subunit vaccines in maize seed. J. Control. Release 85(1-3), 169-180 (2002).
47. Streatfield S, Mayor J, Barker D et al. Development of an edible subunit vaccine in corn against enterotoxigenic strains of Escherichia coli. In Vitro Cell. Dev. Biol. Plant 38(1), 11-17 (2002).
48. Streatfield SJ, Lane JR, Brooks CA et al. Corn as a production system for human and animal vaccines. Vaccine 21, 812-815 (2003).
49. Chikwamba R, McMurray J, Shou H et al. Expression of a synthetic E. coli heat-labile enterotoxin B sub-unit (LT-B) in maize. Mol. Breeding 10(4), 253-265 (2002).
50. Karaman S, Cunnick J, Wang K. Analysis of immune response in young and aged mice vaccinated with corn-derived antigen against Escherichia coli heat-labile enterotoxin. Mol. Biotechnol. 32(1), 31-42 (2006).
51. Moravec T, Schmidt MA, Herman EM, Woodford-Thomas T. Production of Escherichia coli heat labile toxin (LT) B subunit in soybean seed and analysis of its immunogenicity as an oral vaccine. Vaccine 25(9), 1647-1657 (2007).
52. Stoger E, Ma JKC, Fischer R, Christou P. Sowing the seeds of success: pharmaceutical proteins from plants. Curr. Opin. Biotechnol. 16(2), 167-173 (2005).
53. Kang T-J, Loc N-H, Jang M-O et al. Expression of the B subunit of E. coli heat-labile enterotoxin in the chloroplasts of plants and its characterization. Transgenic Res. 12(6), 683-691 (2003).
54. Kang T-J, Lee W-S, Choi E-G, Kim J-W, Kim B-G, Yang M-S. Mass production of somatic embryos expressing Escherichia coli heat-labile enterotoxin B subunit in Siberian ginseng. J. Biotechnol. 121(2), 124-133 (2006).
55. Kim T-G, Kim M-Y, Kim B-G et al. Synthesis and assembly of Escherichia coli heat-labile enterotoxin B subunit in transgenic lettuce (Lactuca sativa). Protein Expr. Purif. 51(1), 22-27 (2007).
56. Oszvald M, Kang T-J, Tomoskozi S et al. Expression of a synthetic neutralizing epitope of porcine epidemic diarrhea virus fused with synthetic B subunit of Escherichia coli heat labile enterotoxin in rice endosperm. Mol. Biotechnol. 35(3), 215-224 (2007).
57. Rosales-Mendoza S, Soria-Guerra R, de Jesus Olivera-Flores M et al. Expression of Escherichia coli heat-labile enterotoxin B subunit (LTB) in carrot (Daucus carota L.). Plant Cell Reports 26(7), 969-976 (2007).
58. Rosales-Mendoza S, Soria-Guerra RE, Lopez-Revilla R, Moreno-Fierros L, Alpuche-Solis AG. Ingestion of transgenic carrots expressing the Escherichia coli heat-labile enterotoxin B subunit protects mice against cholera toxin challenge. Plant Cell Reports 27(1), 79-84 (2008).
59. Ravin NV, Kuprianov VV, Zamchuk LA et al. Highly efficient expression of Escherichia coli heat-labile enterotoxin B subunit in plants using potato virus X-based vector. Biochemistry (Moscow) 73(10), 1108-1113 (2008).
60. Walmsley AM, Alvarez ML, Jin Y et al. Expression of the B subunit of Escherichia coli heat-labile enterotoxin as a fusion protein in transgenic tomato. Plant Cell Reports 21(10), 1020-1026 (2003).
61. Rigano MM, Alvarez ML, Pinkhasov J et al. Production of a fusion protein consisting of the enterotoxigenic Escherichia coli heat-labile toxin B subunit and a tuberculosis antigen in Arabidopsis thaliana. Plant Cell Reports 22(7), 502-508 (2004).
62. Rigano MM, Dreitz S, Kipnis A-P, Izzo AA, Walmsley AM. Oral immunogenicity of a plant-made, subunit, tuberculosis vaccine. Vaccine 24(5), 691-695 (2006).
63. Zhang X, Yuan Z, Guo X, Li J, Li Z, Wang Q. Expression of Chlamydophila psittaci MOMP heat-labile toxin B subunit fusion gene in transgenic rice. Biologicals 36, 296-302 (2008).
64. Zhang X, Yuan Z, Duan Q, Zhu H, Yu H, Wang Q. Mucosal immunity in mice induced by orally administered transgenic rice. Vaccine 27(10), 1596-1600 (2009).
65. Sim J-S, Pak H-K, Kim D-S, Lee S-B, Kim Y-H, Hahn B-S. Expression and characterization of synthetic heat-labile enterotoxin B subunit and hemagglutinin- neuraminidase-neutralizing epitope fusion protein in Escherichia coli and tobacco chloroplasts. Plant Mol. Biol. Report. 27(3), 388-399 (2009).
66. Van den Broeck W, Cox E, Oudega B, Goddeeris BM. The F4 fimbrial antigen of Escherichia coli and its receptors. Vet. Microbiol. 71(3-4), 223-244 (2000).
67. Joensuu J, Kotiaho M, Riipi T et al. Fimbrial subunit protein FaeG expressed in transgenic tobacco inhibits the binding of F4ac enterotoxigenic Escherichia coli to porcine enterocytes. Transgenic Res. 13(3), 295-298 (2004).
68. Joensuu J, Kotiaho M, Teeri T et al. Glycosylated F4 (K88) fimbrial adhesin FaeG expressed in barley endosperm induces ETEC-neutralizing antibodies in mice. Transgenic Res. 15(3), 359-373 (2006).
69. Joensuu JJ, Verdonck F, Ehrstrom A et al. F4 (K88) fimbrial adhesin FaeG expressed in alfalfa reduces F4+ enterotoxigenic Escherichia coli excretion in weaned piglets. Vaccine 24(13), 2387-2394 (2006).
70. Piller K, Clemente T, Jun S et al. Expression and immunogenicity of an Escherichia coli K99 fimbriae subunit antigen in soybean. Planta 222(1), 6-18 (2005).
71. Drake PMW, Barbi T, Sexton A et al. Development of rhizosecretion as a production system for recombinant proteins from hydroponic cultivated tobacco. FASEB J. 23, 1-9 (2009).
72. Floss DM, Falkenburg D, Conrad U. Production of vaccines and therapeutic antibodies for veterinary applications in transgenic plants: an overview. Transgenic Res. 16, 315-332 (2007).
73. Streatfield SJ, Howard JA. Plant-based vaccines. Int. J. Parasitol. 33, 479-493 (2003).
74. Kirk DD, McIntosh K, Walmsley AM, Peterson RKD. Risk analysis for plant- made vaccines. Transgenic Res. 14(4), 449-462 (2005).
75. Alvarez ML, Pinyerd HL, Topal E, Cardineau GA. P19-dependent and P19 independent reversion of F1-V gene silencing in tomato. Plant Mol. Biol. 68, 61-79 (2008).
76. Daniell H, Singh ND, Mason H, Streatfield SJ. Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci. 14(12), 669-679 (2009).
77. Molina A, Hervas-Stubbs S, Daniell H, Mingo-Castel AM, Veramendi J. High- yield expression of a viral peptide animal vaccine in transgenic tobacco chloroplasts. Plant Biotechnol. J. 2, 141-153 (2004).
78. Daniell H, Lee S-B, Panchal T, Wiebe PO. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic chloroplasts. J. Mol. Biol. 311, 1001-1009 (2001).
79. Davoodi-Semiromi A, Schreiber M, Nalapalli S et al. Chloroplast-derived vaccine antigens confer dual immunity against cholera and malaria by oral or injectable delivery. Plant Biotechnol. J. 8(2), 223-242 (2009).
80. Rosales-Mendoza S, Alpuche-Solis AG, Soria-Guerra RE et al. Expression of an Escherichia coli antigenic fusion protein comprising the heat labile toxin B subunit and the heat stable toxin, and its assembly as a functional oligomer in transplastomic tobacco plants. Plant J. 57(1), 45-54 (2009).
81. Rybicki EP. Plant-produced vaccines: promise and reality. Drug Discov. Today 14(1-2), 16-24 (2009).
82. Rybicki EP. Plant-made vaccines for humans and animals. Plant Biotechnol. J. 8, 620-637 (2010).
83. D'Aoust MA, Couture MM, Charland N et al. The production of hemagglutinin- based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J. 8, 607-619 (2010).
84. Gleba Y, Klimyuk V, Marillonnet S. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol. 18(2), 134-141 (2007).
85. Voinnet O, Rivas S, Mestre P, Baulcombe D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33(5), 949-956 (2003).
86. Johansen LK, Carrington JC. Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium- mediated transient expression system. Plant Physiol. 126(3), 930-938 (2001).
87. Joensuu JJ, Conley AJ, Lienemann M, Brandle JE, Linder MB, Menassa R. Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol. 152(2), 622-633 (2009).
88. Marillonnet S, Giritch A, Gils M, Kandzia R, Klimyuk V, Gleba Y. In planta engineering of viral RNA replicons: efficient assembly by recombination of DNA modules delivered by Agrobacterium. Proc. Natl Acad. Sci. USA 101(18), 6852-6857 (2004).
89. Gleba Y, Klimyuk V, Marillonnet S. Magnifection - a new platform for expressing recombinant vaccines in plants. Vaccine 23(17-18), 2042-2048 (2005).
90. Kostrzak A, Cervantes Gonzalez M, Guetard D et al. Oral administration of low doses of plant-based HBsAg induced antigen-specific IgAs and IgGs in mice, without increasing levels of regulatory T cells. Vaccine 27(35), 4798-4807 (2009).
91. Shaaltiel Y, Bartfeld D, Hashmueli S et al. Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol. J. 5(5), 579-590 (2007).
92. Rybicki EP. Third International Conference on plant-based vaccines and antibodies. Expert Rev. Vaccines 8(9), 1151-1155 (2009).
93. Shepherd RP. Plant-based vaccines and antibodies - third international conference 15-17 June 2009, Verona Italy. IDrugs 12(8), 485-488 (2009).
94. Khandelwal A, Sita GL, Shaila MS. Oral immunization of cattle with hemagglutinin protein of rinderpest virus expressed in transgenic peanut induces specific immune responses. Vaccine 21, 3282-3289 (2003).
95. Shewen PE, Carrasco-Medina L, McBey BA, Hodgins DC. Challenges in mucosal vaccination of cattle. Vet. Immunol. Immunopathol. 128, 192-198 (2009).
96. AgroSciences D. Dow AgroScience: media Coverage www.dowagro.com/ animalhealth/ resources/firstlic.htm
97. The Syndney Morning Herald. Foot-and- mouth spreads in Japan www.smh.com.au/world/footandmouth- spreads-in-japan-20100522-w2ys.html