Clinical development of plant-produced recombinant pharmaceuticals: Vaccines, antibodies and beyond

Human Vaccines

Volumn 7, Issue 3, 2011, Pages 313-321

  Yusibov, Vidadi ^a   Streatfield, Stephen J ^a   Kushnir, Natasha ^a  

^a Fraunhofer USA Inc   (United States)

Author keywords

Influenza; Monoclonal antibody; Plant produced; Recombinant protein; Subunit vaccine; Transgenic plant; Transient expression; Virus like particle

Indexed keywords

BLX 301; CANCER VACCINE; CARORX; CHEMOKINE RECEPTOR CCR5 ALPHA ANTIBODY; ESCHERICHIA COLI VACCINE; GLYCOPROTEIN GP 120 ANTIBODY; HEPATITIS B VACCINE; HUMAN INSULIN; INFLUENZA VACCINE; INTRINSIC FACTOR; ISOPHANE INSULIN; LACROMIN; LACTOFERRIN; MERISPASE; MONENSIN; MONOCLONAL ANTIBODY; NEWCASTLE DISEASE VACCINE; NOROVAXX; NOROVIRUS VACCINE; PLACEBO; RABIES VACCINE; RECOMBINANT VACCINE; STREPTOCOCCUS SURFACE ANTIGEN ANTIBODY; SUBUNIT VACCINE; TALIGLUCERASE ALFA; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTINEOPLASTIC ACTIVITY; CANCER IMMUNIZATION; CYANOCOBALAMIN DEFICIENCY; CYSTIC FIBROSIS; DENTAL CARIES; DIABETES MELLITUS; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG INDICATION; DRUG RESEARCH; DRUG SAFETY; DRUG SYNTHESIS; DRUG TOLERABILITY; GASTROINTESTINAL INFECTION; GAUCHER DISEASE; GENE EXPRESSION SYSTEM; GOOD MANUFACTURING PRACTICE; HEPATITIS B; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; INFECTIOUS DIARRHEA; INFLUENZA A (H1N1); INFLUENZA A (H5N1); NEWCASTLE DISEASE; NONHODGKIN LYMPHOMA; NONHUMAN; NOROVIRUS; PANCREATITIS; PLANT BIOTECHNOLOGY; PLANT CELL CULTURE; RABIES; REPEATED DRUG DOSE; REVIEW; RHEUMATOID ARTHRITIS; SINGLE DRUG DOSE; VACCINATION; VACCINE PRODUCTION;

ANTIBODIES; ANTIBODIES, MONOCLONAL; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI VACCINES; GAUCHER DISEASE; GLUCOSYLCERAMIDASE; HEPATITIS B VACCINES; HUMANS; INFANT; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; LYMPHOMA, NON-HODGKIN; NEWCASTLE DISEASE VIRUS; NORWALK VIRUS; PLANTS; PLANTS, GENETICALLY MODIFIED; RABIES VACCINES; VACCINES; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 79953697416     PISSN: 15548600     EISSN: 15548619     Source Type: Journal    
DOI: 10.4161/hv.7.3.14207     Document Type: Review

References (61)

1. Hilleman MR. Vaccines in historic evolution and perspective: A narrative of vaccine discoveries. Vaccine 2000; 18:1436-47. (Pubitemid 30017824)
2. st century. Intervirology 2002; 45:199-211.
3. Mäkelä PH. Vaccines, coming of age after 200 years. FEMS Microbiol Rev 2000; 24:9-20.
4. Yusibov V, Rabindran S. Recent progress in the development of plant derived vaccines. Expert Rev Vaccines 2008; 7:1173-83.
5. Streatfield SJ. Mucosal immunization using recombinant plant-based oral vaccines. Methods 2006; 38:150-7. (Pubitemid 43163476)
6. Savarino SJ, Hall ER, Bassily S, Wierzba TF, Youssef FG, Peruski LF Jr, et al. Pride Study Group. Introductory evaluation of an oral, killed whole cell enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine in Egyptian infants. Pediatr Infect Dis J 2002; 21:322-30.
7. Haq TA, Mason HS, Clements JD, Arntzen CJ. Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 1995; 268:714-6.
8. Mason HS, Haq TA, Clements JD, Arntzen CJ. Edible vaccine protects mice against Escherichia coli heat-labile enterotoxin (LT): potatoes expressing a synthetic LT-B gene. Vaccine 1998; 16:1336-43.
9. Tacket CO, Mason HS, Losonsky G, Clements JD, Levine MM, Arntzen CJ. Immunogenicity in humans of a recombinant bacterial antigen delivered in a transgenic potato. Nat Med 1998; 4:607-9. (Pubitemid 28237361)
10. Tacket CO, Pasetti MF, Edelman R, Howard JA, Streatfield S. Immunogenicity of recombinant LT-B delivered orally to humans in transgenic corn. Vaccine 2004; 22:4385-9. (Pubitemid 39334819)
11. Lamphear BJ, Streatfield SJ, Jilka JM, Brooks CA, Barker DK, Turner DD, et al. Delivery of subunit vaccines in maize seed. J Control Release 2002; 85:169-80. (Pubitemid 35449463)
12. Streatfield SJ, Lane JR, Brooks CA, Barker DK, Poage ML, Mayor JM, et al. Corn as a production system for human and animal vaccines. Vaccine 2003; 21:812-5. (Pubitemid 36092004)
13. Streatfield SJ, Jilka JM, Hood EE, Turner DD, Bailey MR, Mayor JM, et al. Plant-based vaccines: Unique advantages. Vaccine 2001; 19:2742-8. (Pubitemid 32234298)
14. Tacket CO. Plant-based vaccines against diarrheal diseases. Trans Am Clin Climatol Assoc 2007; 118:79-87.
15. Mason HS, Ball JM, Shi JJ, Jiang X, Estes MK, Arntzen CJ. Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc Natl Acad Sci USA 1996; 93:5335-40. (Pubitemid 26159450)
16. 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 2000; 182:302-5. (Pubitemid 30497819)
17. Mason HS, Lam DM, Arntzen CJ. Expression of hepatitis B surface antigen in transgenic plants. Proc Natl Acad Sci USA 1992; 89:11745-9. (Pubitemid 23004720)
18. Thanavala Y, Yang YF, Lyons P, Mason HS, Arntzen C. Immunogenicity of transgenic plant-derived hepatitis B surface antigen. Proc Natl Acad Sci USA 1995; 92:3358-61.
19. Kong Q, Richter L, Yang YF, Arntzen CJ, Mason HS, Thanavala Y. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci USA 2001; 98:11539-44. (Pubitemid 32928764)
20. Richter LJ, Thanavala Y, Arntzen CJ, Mason HS. Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol 2000; 18:1167-71.
21. Thanavala Y, Mahoney M, Pal S, Scott A, Richter L, Natarajan N, et al. Immunogenicity in humans of an edible vaccine for hepatitis B. Proc Natl Acad Sci USA 2005; 102:3378-82. (Pubitemid 40328053)
22. Kapusta J, Modelska A, Figlerowicz M, Pniewski T, Letellier M, Lisowa O, et al. A plant-derived edible vaccine against hepatitis B virus. FASEB J 1999; 13:1796-9. (Pubitemid 29473341)
23. Kapusta J, Modelska A, Pniewski T, Figlerowicz M, Jankowski K, Lisowa O, et al. Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Adv Exp Med Biol 2001; 495:299-303. (Pubitemid 34106950)
24. Modelska A, Dietzschold B, Sleysh N, Fu ZF, Steplewski K, Hooper DC, et al. Immunization against rabies with plant-derived antigen. Proc Natl Acad Sci USA 1998; 95:2481-5. (Pubitemid 28145967)
25. Yusibov V, Hooper DC, Spitsin SV, Fleysh N, Kean RB, Mikheeva T, et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 2002;20:3155-64.
26. Sharma AK, Sharma MK. Plants as bioreactors: Recent developments and emerging opportunities. Biotechnol Adv 2009; 27:811-32.
27. Roussel A, Miled N, Berti-Dupuis L, Rivière M, Spinelli S, Berna P, et al. Crystal structure of the open form of dog gastric lipase in complex with a phosphonate inhibitor. J Biol Chem 2002; 277:2266-74. (Pubitemid 34968814)
28. Samyn-Petit B, Gruber V, Flahaut C, Wajda-Dubos JP, Farrer S, Pons A, et al. N-glycosylation potential of maize: The human lactoferrin used as a model. Glycoconj J 2001; 18:519-27.
29. Fedosov SN, Laursen NB, Nexø E, Moestrup SK, Petersen TE, Jensen EØ, et al. Human intrinsic factor expressed in the plant Arabidopsis thaliana. Eur J Biochem 2003; 270:3362-7. (Pubitemid 37020922)
30. Mihaliak CA, Webb S, Miller T, Fanton M, Kirk D, Cardineau G, et al. Development of plant cell produced vaccines for animal health applications. Proceedings of the 108th Annual Meeting of the United States Animal Health Association. Greensboro NC 2005; 158-63.
31. McCormick AA, Kumagai MH, Hanley K, Turpen TH, Hakim I, Grill LK, et al. Rapid production of specific vaccines for lymphoma by expression of the tumor-derived single-chain Fv epitopes in tobacco plants. Proc Natl Acad Sci USA 1999; 96:703-8. (Pubitemid 29061272)
32. McCormick AA, Reinl SJ, Cameron TI, Vojdani F, Fronefield M, Levy R, et al. Individualized human scFv vaccines produced in plants: Humoral anti-idiotype responses in vaccinated mice confirm relevance to the tumor Ig. J Immunol Methods 2003; 278:95-104. (Pubitemid 37287600)
33. McCormick AA, Reddy S, Reinl SJ, Cameron TI, Czerwinkski DK, Vojdani F, et al. Plant-produced idiotype vaccines for the treatment of non-Hodgkin's lymphoma: Safety and immunogenicity in a phase I clinical study. Proc Natl Acad Sci USA 2008; 105:10131-6.
34. 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 2004; 101:6852-7.
35. Giritch A, Marillonnet S, Engler C, van Eldik G, Botterman J, Klimyuk V, et al. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci USA 2006; 103:14701-6. (Pubitemid 44527793)
36. Bendandi M, Marillonnet S, Kandzia R, Thieme F, Nickstadt A, Herz S, et al. Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin's lymphoma. Ann Oncol 2010; 21;2420-7.
37. Cox KM, Sterling JD, Regan JT, Gasdaska JR, Frantz KK, Peele CG, et al. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat Biotechnol 2006; 24:1591-7. (Pubitemid 44967485)
38. D'Aoust MA, Lavoie PO, Couture MM, Trépanier S, Guay JM, Dargis M, 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 2008; 6:930-40.
39. D'Aoust MA, Couture MM, Charland N, Trépanier S, Landry N, Ors F, et al. The production of hemagglutinin-based virus-like particles in plants: A rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J 2010; 8:607-19.
40. Shoji Y, Bi H, Musiychuk K, Rhee A, Horsey A, Roy G, et al. Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine 2009; 27:1087-92.
41. Shoji Y, Chichester JA, Jones M, Manceva SD, Damon E, Mett M, et al. Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccin 2011; 7 (Jan/Feb Suppl): 41-50.
42. Musiychuk K, Stephenson N, Bi H, Farrance CE, Orozovic G, Brodelius M, et al. A launch vector for the production of vaccine antigens in plants. Influenza Other Respi Viruses 2007; 1:19-25.
43. Shaaltiel Y, Bartfeld D, Hashmueli S, Baum G, Brill-Almon E, Galili G, 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 2007; 5:579-90. (Pubitemid 47196361)
44. Wycoff KL. Secretory IgA antibodies from plants. Curr Pharm Des 2005; 11:2429-37. (Pubitemid 40872688)
45. Ma JK, Lehner T. Prevention of colonization of Streptococcus mutans by topical application of monoclonal antibodies in human subjects. Arch Oral Biol 1990; 35:115-22.
46. Ma JK, Hunjan M, Smith R, Lehner T. Specificity of monoclonal antibodies in local passive immunization against Streptococcus mutans. Clin Exp Immunol 1989; 77:331-7. (Pubitemid 19234378)
47. Ma JK, Hikmat BY, Wycoff K, Vine ND, Chargelegue D, Yu L, et al. Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. Nat Med 1998; 4:601-6. (Pubitemid 28237360)
48. De Muynck B, Navarre C, Boutry M. Production of antibodies in plants: Status after twenty years. Plant Biotechnol J 2010; 8:529-63.
49. Pogue GP, Vojdani F, Palmer KE, Hiatt E, Hume S, Phelps J, et al. Production of pharmaceutical-grade recombinant aprotinin and a monoclonal antibody product using plant-based transient expression systems. Plant Biotechnol J 2010; 8:638-54.
50. Trkola A, Kuster H, Rusert P, Joos B, Fischer M, Leemann C, et al. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 2005; 11:615-22.
51. Rademacher T, Sack M, Arcalis E, Stadlmann J, Balzer S, Altmann F, et al. Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol J 2008; 6:189-201.
52. Ramessar K, Rademacher T, Sack M, Stadlmann J, Platis D, Stiegler G, et al. Cost-effective production of a vaginal protein microbicide to prevent HIV transmission. Proc Natl Acad Sci USA 2008; 105:3727-32. (Pubitemid 351723466)
53. Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H. Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J 2007; 5:657-63. (Pubitemid 47196370)
54. Strasser R, Stadlmann J, Schähs M, Stiegler G, Quendler H, Mach L, et al. Generation of glycoengineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous humanlike N-glycan structure. Plant Biotechnol J 2008; 6:392-402.
55. Pujol M, Ramírez NI, Ayala M, Gavilondo JV, Valdés R, Rodríguez M, et al. An integral approach towards a practical application for a plant-made monoclonal antibody in vaccine purification. Vaccine 2005; 23:1833-7. (Pubitemid 40331854)
56. WHO Expert Committee on Biological Standardization. WHO Technical Report Series 1992; 822.
57. van der Laan JW, Minor P, Mahoney R, Arntzen C, Shin J, Wood D. WHO Informal Consultation Group. WHO informal consultation on scientific basis for regulatory evaluation of candidate human vaccines from plants, Geneva, Switzerland 24-25 January 2005. Vaccine 2006; 24:4271-8.
58. FDA. Guidance for Industry: Drugs, biologics and medical devices derived from bioengineered plants for use in humans and animals. Draft Guidance, September 2002. Rockville, MD USA: United States Food and Drug Administration.
59. EMEA. Guideline on the quality of biological active substances produced by stable transgene expression in higher plants. Draft 2, July 2006. London, UK: European Agency for the Evaluation of Medicinal Products.
60. Rybicki EP. Third International Conference on Plant-Based Vaccines and Antibodies. Expert Rev Vaccines 2009; 8:1151-5.
61. Gilbert N. Europe prepares for drugs from GM plants. Nature 2009; 460:791.