Recent progress in the development of plant-derived vaccines

Expert Review of Vaccines

Volumn 7, Issue 8, 2008, Pages 1173-1183

  Yusibov, Vidadi ^a   Rabindran, Shailaja ^b  

^a Fraunhofer USA Inc   (United States)

^b NONE

Author keywords

Oral delivery; Plant virus; Production platform; Recombinant protein; Subunit vaccine; Transgenic plant; Vaccine

Indexed keywords

PLANT EXTRACT; RECOMBINANT PROTEIN; VACCINE;

DRUG INDUSTRY; DRUG MANUFACTURE; DRUG SAFETY; EXPRESSION VECTOR; HUMAN; IMMUNOGENICITY; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; REVIEW; TRANSGENIC PLANT;

HUMANS; PLANTS; UNITED STATES; VACCINES, SUBUNIT; VACCINES, SYNTHETIC;

EID: 53849112341     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.7.8.1173     Document Type: Review

References (79)

1. Hilleman MR. Vaccines in historic evolution and perspective: a narrative of vaccine discoveries. Vaccine 18, 1436-1447 (2000).
2. Mäkelä PK. Vaccines, coming of age after 200 years. FEMS Microbiol. Rev. 24, 9-20 (2000).
3. Choi JH, Lee SY. Secretory and extracellular production of recombinant proteins using Escherichia coli. Appl. Microbiol. Biotechnol. 64, 625-635 (2004).
4. Baneyx F, Mujacic M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol. 22, 1399-1408 (2004).
5. Romanos MA, Scorer CA, Clare JJ. Foreign gene expression in yeast: a review. Yeast 8, 423-488 (1992).
6. Valenzuela P, Medina A, Rutter WJ, Ammerer G, Hall BD. Synthesis and assembly of hepatits B virus surface antigen particles in yeast. Nature 298, 347-350 (1982).
7. Wurm FM. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat. Biotechnol. 22, 1393-1398 (2004).
8. Ikonomou L, Schneider YJ, Agathos SN. Insect cell culture for industrial production of recombinant proteins. Appl. Microbiol. Biotechnol. 62, 1-20 (2003).
9. Twyman RM, Schillberg S, Fischer R. Transgenic plants in the biopharmaceutical market. Expert Opin. Emerg. Drugs 10, 185-218 (2005).
10. Ma JKC, Drake P, Christou P. The production of recombinant pharmaceutical proteins in plants. Nat. Rev. Genet. 4, 794-805 (2003).
11. Streatfield SJ. Mucosal immunization using recombinant plant-based oral vaccines. Methods 38, 150-157 (2006).
12. Stoger E, Sack M, Perrin Y, Vaquero C et al. Practical considerations for pharmaceutical antibody production in different crop systems. Mol. Breeding 9, 149-158 (2002).
13. Arlen PA, Signelton M, Adamovicz JJ, Ding Y, Davoodi-Semiromi A, Daniell H. Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect. Immun. 76 (8), 3640-3650 (2008).
14. Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R. Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 21, 570-578 (2003).
15. Daniell H, Chebolu S, Kumar S, Singleton M, Falconer R. Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine 23, 1779-1783 (2005).
16. Vema D, Daniell H. Chloroplast vector systems for biotechnology applications. Plant Physiol. 145, 1129-1143 (2007).
17. Daniell H, Lee SB, Panchal T, Wiebe PO. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J. Mol. Biol. 311, 1001-1009 (2001).
18. Tregoning JS, Nixon P, Kuroda H et al. Expression of tetanus toxin fragment C in tobacco chloroplasts. Nucleic Acids Res. 31, 1174-1179 (2003).
19. Watson J, Koya V, Leppla SH, Daniell H. Expression of Bacillus anthracis protective antigen in transgenic chloroplasts of tobacco, a nonfood/feed crop. Vaccine 22, 4374-4384 (2004).
20. Koya V, Moayeri M, Leppla SH, Daniell H. Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect. Immun. 73, 8266-8274 (2005).
21. Daniell H, Chebolu S, Kumar S, Singleton M, Falconer R. Chloroplast-derived vaccine antigens and other therapeutic proteins. Vaccine 23, 1779-1783 (2005).
22. Chebolu S, Daniell H. Stable expression of Gal/GalNAc lectin of Entamoeba histolytica in transgenic chloroplasts and immunogenicity in mice towards vaccine development for amoebiasis. Plant Biotechnol. J. 5, 230-239 (2007).
23. Yusibov V, Rabindran S, Commandeur U, Twyman RM, Fischer R. The potential of plant virus vectors for vaccine production. Drugs RD 7, 203-217 (2006).
24. Porta C, Lomonossoff GP. Viruses as vectors for the expression of foreign sequences in plants. Biotechnol. Genet. Eng. Rev. 19, 245-91 (2002).
25. Porta C, Lomonossoff GP. Scope for using plant viruses to present epitopes from animal pathogens. Rev. Med. Virol. 8, 25-41 (1998).
26. Lomonossoff GP, Johnson JE. Use of macromolecular assemblies as expression systems for peptides and synthetic vaccines. Curr. Opin. Struct. Biol. 6, 176-182 (1996).
27. Smith ML, Lindbo JA, Dillard-Telm S et al. Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology 348, 475-488 (2006).
28. Rae CS, Khor IW, Wang Q et al. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 343, 224-235 (2005).
29. Musiychuk K, Stephenson N, Bi H et al. A launch vector the the production of vaccine antigens in plants. Influenza Other Respir. Viruses 1, 19-25 (2007).
30. Marillonnet S, Thoeringer C, Kandzia R et al. Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat. Biotechnol. 23, 718-723 (2005).
31. Santi L, Giritch A, Roy CJ et al. Protection conferred by recombinant Yersinia pestis antigens produced by a rapid and highly scalable plant expression system. Proc. Natl Acad. Sci. USA 103, 861-866 (2006).
32. Chichester JA, Musiychuk K, de la Rosa P et al. Immunogenicity of a subunit vaccine against Bacillus anthracis. Vaccine 25, 3111-3114 (2007).
33. Mett V, Lyons J, Musiychuk K et al. A plant-produced plague vaccine candidate confers protection to monkeys. Vaccine 25, 3014-3017 (2007).
34. Shoji Y, Chichester JA, Bi H et al. Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 26, 2930-2934 (2008).
35. Hellwig S, Drossard J, Twyman RM, Fischer R. Plant cell cultures for the production of recombinant proteins. Nat. Biotechnol. 22, 1415-1422 (2004).
36. 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, 62-72 (2007).
37. Streatfield SJ. Engineered chloroplasts as vaccine factories to combat bioterrorism. Trends Biotechnol. 24, 339-342 (2006).
38. Mett, V, Musiychuk, K, Bi, H et al. A plant-produced influenza subunit vaccine protescts ferrets against virus challenge. Influenza Other Respir. Viruses 2, 33-40 (2008).
39. Tacket CO. Plant-based vaccines against diarrheal diseases. Trans. Amer. Clin. Climatol. Assn. 118, 79-87 (2007).
40. Faye L, Boulaflous A, Benchabane M, Gomord V, Michaud D. Protein modifications in the plant secretory pathway: current status and practical im-plications in molecular pharming. Vaccine 23, 1770-1778 (2005).
41. Sparrow PAC, Irwin JA, Dale PJ, Twyman RM, Ma JKC. Pharma-Planta: road testing the developing regulatory guidelines for plant-made pharmaceuticals. Transgenic Res. 16, 147-161 (2007).
42. Blixt O, Allin K, Pereira L, Datta A, Paulson JC. Efficient chemoenzymatic synthesis of O-linked sialyl oligosaccharides. J. Am. Chem. Soc. 124, 5739-5746 (2002).
43. Bakker H, Bardor M, Molthoff JW et al. Galactose-extended glycans of antibodies produced by transgenic plants. Proc. Natl Acad. Sci. USA 98, 2899-2904 (2001).
44. Strasser R, Altmann F, Mach L, Glossl J, Steinkellner H. Generation of Arabidopsis thaliana plants with complex N-glycans lacking β1,2-linked xylose and core α1,3-linked fucose. FEBS Lett. 561, 132-136 (2004).
45. Strasser R, Stadlmann J, Schähs M et al. Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol. J. 6, 392-402 (2008).
46. Rademacher T, Sack M, Arcalis E et al. Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol. J. 6, 189-201 (2008).
47. Jin C, Altmann F, Strasser R et al. A plant-derived human monoclonal antibody induces an anti-carbohydrate immune response in rabbits. Glycobiology 18, 235-241 (2008).
48. Jin C, Hantusch G, Hemmer W, Stadlmann J, Altmann F. Affinity of IgE and IgG against cross-reactive carbohydrate determinants on plant and insect glycoproteins. J. Allergy Clin. Immunol. 121, 185-190 (2008).
49. Menkhaus TJ, Bai Y, Zhang C, Nikolov ZL, Glatz CE. Considerations for the recovery of recombinant proteins from plants. Biotechnol. Prog. 20, 1001-1014 (2004).
50. Spök A, Twyman RM, Fischer R, Ma JKC, Sparrow PAC. Evolution of a regulatory framework for plant-made pharmaceuticals. Trends Biotechnol. 26(9), 516-517 (2008).
51. Lee KY, Kim DH, Kang TJ et al. Induction of protective immune responses against the challenge of Actinobacillus pleuropneumoniae by the oral administration of transgenic tobacco plant expressing ApxIIA toxin from the bacteria. FEMS Immunol. Med. Microbiol. 48, 381-389 (2006).
52. Perez Filgueira DM, Zamorano PI, Dominguez MG et al. Bovine herpes virus gD protein produced in plants using a recombinant tobacco mosaic virus (TMV) vector possesses authentic antigenicity. Vaccine 21, 4201-4209 (2003).
53. Nicholas BL, Brennan FR, Martinez-Torrecuadrada JL, Casal JI, Hamilton WDO, Wakelin D. Characterization of the immune response to canine parvovirus induced by vaccination with chimaeric plant viruses. Vaccine 20, 2727-2734 (2002).
54. Joensuu JJ, 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, 295-298 (2004).
55. Dus Santos MJ, Wigdorovitz A, Trono K et al. A novel methodology to develop a foot and mouth disease virus (FMDV) peptide-based vaccine in transgenic plants. Vaccine 20, 1141-1147 (2002).
56. Verch T, Yusibov V, Koprowski H. Expression and assembly of a full-length monoclonal antibody in plants using a plant virus vector. J. Immunol. Methods 220, 69-75 (1998).
57. 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, 49-57 (2001).
58. Pan L, Zhang YG, Wang YL 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, 83-90 (2008).
59. Zhou JY, Wu JX, Cheng LQ et al. Expression of immunogenic S1 glycoprotein of infectious bronchitis virus in transgenic potatoes. J. Virol. 77, 9090-9093 (2003).
60. Wu JX, Yu L, Li L et al. Oral immunization with transgenic rice seeds expressing VP2 protein of infectious bursal disease virus induces protective immune responses in chickens. Plant Biotechnol. J. 5, 570-578 (2007).
61. Dalsgaard K, Uttenthal A, Jones TD et al. Plant-derived vaccine protects target animals against a viral disease. Nat. Biotechnol. 15, 248-252 (1997).
62. Koo M, Bendahmane M, Lettieri GA et al. Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carries an MHV epitope. Proc. Natl Acad. Sci. USA 96, 7774-7779 (1999).
63. Fernandez-Fernandez MR, Mourino M, Rivera J, Rodriguez R, Plana-Duran J, Garcia JA. Protection of rabbits against rabbit hemorrhagic disease virus by immunization with the VP60 protein expressed in plants with a potyvirus-based vector. Virology 280, 283-291 (2001).
64. Castanon S, Marin MS, Martin-Alonso JM et al. Immunization with potato plants expressing VP60 protein protects against rabbit hemorrhagic disease virus. J. Virol. 73, 4452-4455 (1999).
65. Lamphear BJ, Streatfield SJ, Jilka JM et al. Delivery of subunit vaccines in maize seed. J. Control. Release 85, 169-180 (2002).
66. Hernandez M, Cabrera-Ponce JL, Fragoso G et al. A new highly effective anticysticercosis vaccine expressed in transgenic papaya. Vaccine 25, 4252-4260 (2007).
67. Chikwamba R, Cunnick J, Hathaway D, McMurray J, Mason H, Wang K. 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 (2002).
68. Haq TA, Mason HS, Clements JD, Arntzen CJ. Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 268, 714-716 (1995).
69. Yu J, Langridge WH. A plant-based multicomponent vaccine protects mice from enteric diseases. Nat. Biotechnol. 19, 548-552 (2001).
70. Rosales-Mendoza S, Soria-Guerra RE, Lopez-Revilla R et al. Ingestion of transgenic carrots expressing the Escherichia coli heat-labile enterotoxin B subunit protects mice against cholera toxin challenge. Plant Cell Rep. 27, 79-84 (2008).
71. Judge NA, Mason HS, O'Brien AD. Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect. Immunol. 72, 168-175 (2004).
72. Kapusta J, Modelska A, Figlerowicz M et al. A plant-derived edible vaccine against hepatitis B virus. FASEB J. 13, 1796-1799 (1999).
73. Tacket CO, Mason HS, Losonsky G, Estes MK, Levine MM, Arntzen CJ. Human immune responses to a novel Norwalk virus vaccine delivered in transgenic potatoes. J. Infect. Dis. 182, 302-305 (2000).
74. Brennan FR, Jones TD, Gilleland LB et al. Psuedemonas aeruginosa outer-membrane protein F epitopes are highly immunogenic in mice when expressed on a plant virus. Microbiology 145, 211-220 (1999).
75. Staczek J, Bendahmane M, Gilleland LB, Beachy RN, Gilleland HE Jr. Immunization with a chimeric tobacco mosaic virus containing an epitope of outer membrane protein F of Pseudomonas aeruginosa provides protection against challenge with P. aeruginosa. Vaccine 18, 2266-2274 (2000).
76. Yusibov V, Hooper DC, Spitsin S et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 20, 3155-3164 (2002).
77. Belanger H, Fleysh N, Cox S et al. Human respiratory syncytial virus vaccine antigen produced in plants. FASEB J. 14, 2323-2328 (2000).
78. Golovkin M, Spitsin S, Andrianov V et al. Smallpox subunit vaccine produced in planta confers protection in mice. Proc. Natl Acad. Sci. USA 104, 6864-6869 (2007).
79. Arakawa T, Chong DK, Langridge WH. Efficacy of food plant-based oral cholera toxin B subunit vaccine. Nat. Biotechnol. 16(3), 292-297 (1998).