Role of plant expression systems in antibody production for passive immunization

International Journal of Developmental Biology

Volumn 57, Issue 6-8, 2013, Pages 587-593

  Virdi, Vikram ^a   Depicker, Ann ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Disruptive technology; In leaf production; In seed production; Molecular farming; Plantibodies

Indexed keywords

2G12 ANTIBODY; ADALIMUMAB; BAPINEUZUMAB; BEVACIZUMAB; CETUXIMAB; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MONOCLONAL ANTIBODY; SOLANEZUMAB; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANTIBODY PRODUCTION; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; COLON CANCER; DRUG ISOLATION; FRUIT; GENE EXPRESSION SYSTEM; GOOD MANUFACTURING PRACTICE; HUMAN; MAIZE; NONHUMAN; PASSIVE IMMUNIZATION; PEA; PLANT EXPRESSION SYSTEM; PLANT LEAF; PLANT ROOT; PLANT SEED; PLANT TISSUE; PLANT TUBER; POTATO; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; RICE; STOMACH MUCOSA; TOBACCO; TOMATO; TRANSGENIC PLANT;

ANIMALS; ANTIBODY FORMATION; BIOMASS; BIOTECHNOLOGY; GENE EXPRESSION REGULATION, PLANT; HUMANS; IMMUNIZATION, PASSIVE; PLANT LEAVES; PLANTIBODIES; PLANTS; PLANTS, GENETICALLY MODIFIED; SEEDS; TOBACCO;

EID: 84886897589     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.130266ad     Document Type: Article

References (80)

1. ANDRABI R, KUMAR R, BALA M, NAIR A, BISWAS A, WIG N, KUMAR P, PAL R, SINHA S, LUTHRA K. (2012). Production and characterization of human anti-V3 monoclonal antibodies from the cells of HIV-1 infected Indian donors. Virol J 9: 196.
2. BERENDS E, SCHOLTMEIJER K, WÖSTEN HAB, BOSCH D, LUGONES LG. (2009). The use of mushroom-forming fungi for the production of N-glycosylated therapeutic proteins. Trends Microbiol 17: 439-443.
3. BERGHMAN LR, ABI-GHANEM D, WAGHELA SD, RICKE SC. (2005). Antibodies: An alternative for antibiotics? Poult Sci 84: 660-666.
4. BOTH L, BANYARD AC, VAN DOLLEWEERD C, HORTON DL, MA JK-C, FOOKS AR. (2012). Passive immunity in the prevention of rabies. Lancet Infect Dis 12: 397-407.
5. BRÜGGEMANN M, CASKEY HM, TEALE C, WALDMANN H, WILLIAMS GT, SURANI MA, NEUBERGER MS. (1989). A repertoire of monoclonal antibodies with human heavy chains from transgenic mice. Proc Natl Acad Sci USA 86: 6709-6713.
6. CASADEVALL A, DADACHOVA E, PIROFSKI L-A. (2004). Passive antibody therapy for infectious diseases. Nat Rev Microbiol 2: 695-703.
7. CASTILHO A, BOHOROVA N, GRASS J, BOHOROV O, ZEITLIN L, WHALEY K, ALTMANN F, STEINKELLNER H. (2011). Rapid high yield production of different glycoforms of Ebola virus monoclonal antibody. PLoS ONE 6: e26040.
8. CHEN M, LIU X, WANG Z, SONG J, QI Q, WANG PG. (2005). Modification of plant N-glycans processing: The future of producing therapeutic protein by transgenic plants. Med Res Rev 25: 343-360.
9. CHEN ZL, SCHULER MA, BEACHY RN. (1986). Functional analysis of regulatory elements in a plant embryo-specific gene. Proc Natl Acad Sci USA 83: 8560-8564.
10. CHENG M, LOWE BA, SPENCER TM, YE X, ARMSTRONG CL. (2004). Factors influencing Agrobacterium-mediated transformation of monocotyledonous species. In vitro Cell Dev Biol-Plant 40: 31-45.
11. CHRISTENSEN AH, QUAIL PH. (1996). Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5: 213-218.
12. CORTHÉSY B. (2003). Recombinant secretory immunoglobulin A in passive immunotherapy: linking immunology and biotechnology. Curr Pharm Biotechnol 4: 51-67.
13. CORTHÉSY B, SPERTINI F. (1999). Secretory immunoglobulin A: from mucosal protection to vaccine development. Biol Chem 380: 1251-1262.
14. COX KM, STERLING JD, REGAN JT, GASDASKA JR, FRANTZ KK, PEELE CG, BLACK A, PASSMORE D, MOLDOVAN-LOOMIS C, SRINIVASAN M, CUISON S, CARDARELLI PM, DICKEY LF. (2006). Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat Biotechnol 24: 1591-1597.
15. DE JAEGER G, SCHEFFER S, JACOBS A, ZAMBRE M, ZOBELL O, GOOSSENS A, DEPICKER A, ANGENON G. (2002). Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat Biotechnol 20: 1265-1268.
16. DE MUYNCK B, NAVARRE C, BOUTRY M. (2010). Production of antibodies in plants: status after twenty years. Plant Biotechnol J 8: 529-563.
17. DE WILDE K, DE BUCK S, VANNESTE K, DEPICKER A. (2013). Recombinant antibody production in Arabidopsis seeds triggers an unfolded protein response. Plant Physiol 161: 1021-1033.
18. DECKER EL, RESKI R. (2008). Current achievements in the production of complex biopharmaceuticals with moss bioreactors. Bioprocess Biosyst Eng 31: 3-9.
19. DRAKAKAKI G, MARCEL S, ARCALIS E, ALTMANN F, GONZALEZ-MELENDI P, FISCHER R, CHRISTOU P, STOGER E. (2006). The intracellular fate of a recombinant protein is tissue dependent. Plant Physiol 141: 578-586.
20. DURANDY A, KAVERI SV, KUIJPERS TW, BASTA M, MIESCHER S, RAVETCH JV, RIEBEN R. (2009). Intravenous immunoglobulins-understanding properties and mechanisms. Clin Exp Immunol 158: 2-13.
21. EIBL MM. (2008). History of immunoglobulin replacement. Immunol Allergy Clin North Am 28: 737-764.
22. FLOSS DM, FALKENBURG D, CONRAD U. (2007). Production of vaccines and therapeutic antibodies for veterinary applications in transgenic plants: an overview. Transgenic Res 16: 315-332.
23. FRANKLIN SE, MAYFIELD SP. (2005). Recent developments in the production of human therapeutic proteins in eukaryotic algae. Expert Opin Biol Ther 5: 225-235.
24. GLEBA Y, KLIMYUK V, MARILLONNET S. (2005). Magnifection-a new platform for expressing recombinant vaccines in plants. Vaccine 23: 2042-2048.
25. GONIK B. (2011). Passive immunization: the forgotten arm of immunologically based strategies for disease containment. Am J Obstet Gynecol 205: 444. e441-444. e446.
26. HARA-NISHIMURA I, SHIMADA T, HATANO K, TAKEUCHI Y, NISHIMURA M. (1998). Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10: 825-836.
27. HELLWIG S, DROSSARD J, TWYMAN RM, FISCHER R. (2004). Plant cell cultures for the production of recombinant proteins. Nat Biotechnol 22: 1415-1422.
28. HIATT A, CAFFERKEY R, BOWDISH K. (1989). Production of antibodies in transgenic plants. Nature 342: 76-78.
29. HOHL I, ROBINSON DG, CHRISPEELS MJ, HINZ G. (1996). Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J Cell Sci 109: 2539-2550.
30. HOLLIGER P, HUDSON PJ. (2005). Engineered antibody fragments and the rise of single domains. Nat Biotechnol 23: 1126-1136.
31. HSU JL, SAFDAR N. (2011). Polyclonal immunoglobulins and hyperimmune globulins in prevention and management of infectious diseases. Infect Dis Clin North Am 25: 773-788.
32. HUANG Z, PHOOLCHAROEN W, LAI H, PIENSOOK K, CARDINEAU G, ZEITLIN L, WHALEY KJ, ARNTZEN CJ, MASON HS, CHEN Q. (2010). High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol Bioeng 106: 9-17.
33. KAPILA J, DE RYCKE R, VAN MONTAGU M, ANGENON G. (1997). An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122: 101-108.
34. KHAN I, TWYMAN RM, ARCALIS E, STOGER E. (2012). Using storage organelles for the accumulation and encapsulation of recombinant proteins. Biotechnol J 7: 1099-1108.
35. KO K, KOPROWSKI H. (2005). Plant biopharming of monoclonal antibodies. Virus Res 111: 93-100.
36. KÖHLER G, MILSTEIN C. (1975). Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495-497.
37. KOSTEN T, OWENS SM. (2005). Immunotherapy for the treatment of drug abuse. Pharmacol Ther 108: 76-85.
38. LOOS A, VAN DROOGENBROECK B, HILLMER S, GRASS J, KUNERT R, CAO J, ROBINSON DG, DEPICKER A, STEINKELLNER H. (2011a). Production of monoclonal antibodies with a controlled N-glycosylation pattern in seeds of Arabidopsis Thaliana. Plant Biotechnol J 9: 179-192.
39. LOOS A, VAN DROOGENBROECK B, HILLMER S, GRASS J, PABST M, CASTILHO A, KUNERT R, LIANG M, ARCALIS E, ROBINSON DG, DEPICKER A, STEINKELLNER H. (2011b). Expression of antibody fragments with a controlled N-glycosylation pattern and induction of endoplasmic reticulum-derived vesicles in seeds of Arabidopsis. Plant Physiol 155: 2036-2048.
40. MA JK-C, HIATT A, HEIN M, VINE ND, WANG F, STABILA P, VAN DOLLEWEERD C, MOSTOV K, LEHNER T. (1995). Generation and assembly of secretory antibodies in plants. Science 268: 716-719.
41. MAYFIELD SP, FRANKLIN SE. (2005). Expression of human antibodies in eukaryotic micro-algae. Vaccine 23: 1828-1832.
42. MOR TS, MOON Y-S, PALMER KE, MASON HS. (2003). Geminivirus vectors for high-level expression of foreign proteins in plant cells. Biotechnol Bioeng 81: 430-437.
43. NAZ RK, RAJESH C. (2004). Passive immunization for immunocontraception: lessons learned from infectious diseases. Front Biosci 9: 2457-2465.
44. OBEMBE OO, POPOOLA JO, LEELAVATHI S, REDDY SV. (2011). Advances in plant molecular farming. Biotechnol Adv 29: 210-222.
45. OLEKSIEWICZ MB, NAGY G, NAGY E. (2012). Anti-bacterial monoclonal antibodies: Back to the future? Arch Biochem Biophys 526: 124-131.
46. OLINGER GG, JR., PETTITT J, KIM D, WORKING C, BOHOROV O, BRATCHER B, HIATT E, HUME SD, JOHNSON AK, MORTON J, PAULY M, WHALEY KJ, LEAR CM, BIGGINS JE, SCULLY C, HENSLEY L, ZEITLIN L. (2012). Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques. Proc Natl Acad Sci USA 109: 18030-18035.
47. PAUL M, MA JK-C. (2011). Plant-made pharmaceuticals: Leading products and production platforms. Biotechnol Appl Biochem 58: 58-67.
48. PAUL M, VAN DOLLEWEERD C, DRAKE PMW, RELJIC R, THANGARAJ H, BARBI T, STYLIANOU E, PEPPONI I, BOTH L, HEHLE V, MADEIRA L, INCHAKALODY V, HO S, GUERRA T, MA JK-C. (2011). Molecular pharming: future targets and aspirations. Hum Vaccin 7: 375-382.
49. PERRIN Y, VAQUERO C, GERRARD I, SACK M, DROSSARD J, STÖGER E, CHRISTOU P, FISCHER R. (2000). Transgenic pea seeds as bioreactors for the production of a single-chain Fv fragment (scFV) antibody used in cancer diagnosis and therapy. Mol Breeding 6: 345-352.
50. PETERS J, STOGER E. (2011). Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum Vaccin 7: 367-374.
51. PETRUCCELLI S, OTEGUI MS, LAREU F, DINH OT, FITCHETTE A-C, CIRCOSTA A, RUMBO M, BARDOR M, CARCAMO R, GOMORD V, BEACHY RN. (2006). A KDEL-tagged monoclonal antibody is efficiently retained in the endoplasmic reticulum in leaves, but is both partially secreted and sorted to protein storage vacuoles in seeds. Plant Biotechnol J 4: 511-527.
52. POGUE GP, VOJDANI F, PALMER KE, HIATT E, HUME S, PHELPS J, LONG L, BOHOROVA N, KIM D, PAULY M, VELASCO J, WHALEY K, ZEITLIN L, GARGER SJ, WHITE E, BAI Y, HAYDON H, BRATCHER B. (2010). Production of pharmaceutical-grade recombinant aprotinin and a monoclonal antibody product using plant-based transient expression systems. Plant Biotechnol J 8: 638-654.
53. RAAB CP. (2011). Passive immunization. Prim Care: Clinics in Office Practice 38: 681-691.
54. RADEMACHER T, SACK M, ARCALIS E, STADLMANN J, BALZER S, ALTMANN F, QUENDLER H, STIEGLER G, KUNERT R, FISCHER R, STOGER E. (2008). Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol J 6: 189-201.
55. RAMESSAR K, RADEMACHER T, SACK M, STADLMANN J, PLATIS D, STIEGLER G, LABROU N, ALTMANN F, MA J, STÖGER E, CAPELL T, CHRISTOU P. (2008). Cost-effective production of a vaginal protein microbicide to prevent HIV transmission. Proc Natl Acad Sci USA 105: 3727-3732.
56. RYBICKI EP. (2010). Plant-made vaccines for humans and animals. Plant Biotechnol J 8: 620-637.
57. SAINSBURY F, SACK M, STADLMANN J, QUENDLER H, FISCHER R, LOMONOSSOFF GP. (2010). Rapid transient production in plants by replicating and non-replicating vectors yields high quality functional anti-HIV antibody. PLoS ONE 5: e13976.
58. SAINSBURY F, THUENEMANN EC, LOMONOSSOFF GP. (2009). pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7: 682-693.
59. SCHIRRMANN T, AL-HALABI L, DÜBEL S, HUST M. (2008). Production systems for recombinant antibodies. Front Biosci 13: 4576-4594.
60. SHARP JM, DORAN PM. (2001). Strategies for enhancing monoclonal antibody accumulation in plant cell and organ cultures. Biotechnol Prog 17: 979-992.
61. SMITH GP. (1985). Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228: 1315-1317.
62. STÖGER E, VAQUERO C, TORRES E, SACK M, NICHOLSON L, DROSSARD J, WILLIAMS S, KEEN D, PERRIN Y, CHRISTOU P, FISCHER R. (2000). Cereal crops as viable production and storage systems for pharmaceutical scFv antibodies. Plant Mol Biol 42: 583-590.
63. STREATFIELD SJ. (2007). Approaches to achieve high-level heterologous protein production in plants. Plant Biotechnol J 5: 2-15.
64. TILLER T, MEFFRE E, YURASOV S, TSUIJI M, NUSSENZWEIG MC, WARDEMANN H. (2008). Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329: 112-124.
65. TRKOLA A, PURTSCHER M, MUSTER T, BALLAUN C, BUCHACHER A, SULLIVAN N, SRINIVASAN K, SODROSKI J, MOORE JP, KATINGER H. (1996). Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70: 1100-1108.
66. VAN DROOGENBROECK B, CAO J, STADLMANN J, ALTMANN F, COLANESI S, HILLMER S, ROBINSON DG, VAN LERBERGE E, TERRYN N, VAN MONTAGU M, LIANG M, DEPICKER A, DE JAEGER G. (2007). Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds. Proc Natl Acad Sci USA 104: 1430-1435.
67. VAN DROOGENBROECK B, DE WILDE K, DEPICKER A. (2009). Production of antibody fragments in Arabidopsis seeds. In Recombinant Proteins From Plants (Methods in Molecular Biology, Vol 483) Eds. FAYE L and GOMORD V). Humana Press, New York, pp.89-101.
68. VIRDI V, CODDENS A, DE BUCK S, MILLET S, GODDEERIS BM, COX E, DE GREVE H, DEPICKER A. (2013). Orally fed seeds producing designer IgAs protect weaned piglets against enterotoxigenic Escherichia coli infection. Proc Natl Acad Sci USA 110: 11809-11814.
69. VOINNET O, RIVAS S, MESTRE P, BAULCOMBE D. (2003). 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: 949-956.
70. WEBSTER DE, THOMAS MC. (2012). Post-translational modification of plant-made foreign proteins; glycosylation and beyond. Biotechnol Adv 30: 410-418.
71. WERNER S, MARILLONNET S, HAUSE G, KLIMYUK V, GLEBA Y. (2006). Immunoabsorbent nanoparticles based on a tobamovirus displaying protein A. Proc Natl Acad Sci USA 103: 17678-17683.
72. WHALEY KJ, HIATT A, ZEITLIN L. (2011). Emerging antibody products and Nicotiana manufacturing. Hum Vaccin 7: 349-356.
73. WURM FM. (2004). Production of recombinant protein therapeutics in cultivated mammalian cells. Nat Biotechnol 22: 1393-1398.
74. WYCOFF KL. (2005). Secretory IgA antibodies from plants. Curr Pharm Design 11: 2429-2437.
75. XU J, DOLAN MC, MEDRANO G, CRAMER CL, WEATHERS PJ. (2012). Green factory: Plants as bioproduction platforms for recombinant proteins. Biotechnol Adv 30: 1171-1184.
76. XU J, GE X, DOLAN MC. (2011). Towards high-yield production of pharmaceutical proteins with plant cell suspension cultures. Biotechnol Adv 29: 278-299.
77. ZEITLIN L, CONE RA, MOENCH TR, WHALEY KJ. (2000). Preventing infectious disease with passive immunization. Microbes Infect 2: 701-708.
78. ZEITLIN L, CONE RA, WHALEY KJ. (1999). Using monoclonal antibodies to prevent mucosal transmission of epidemic infectious diseases. Emerging Infect Dis 5: 54-64.
79. ZEITLIN L, PETTITT J, SCULLY C, BOHOROVA N, KIM D, PAULY M, HIATT A, NGO L, STEINKELLNER H, WHALEY KJ, OLINGER GG. (2011). Enhanced potency of a fucose-free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc Natl Acad Sci USA 108: 20690-20694.
80. ZIMMERMANN J, SAALBACH I, JAHN D, GIERSBERG M, HAEHNEL S, WEDEL J, MACEK J, ZOUFAL K, GLÜNDER G, FALKENBURG D, KIPRIYANOV SM. (2009). Antibody expressing pea seeds as fodder for prevention of gastrointestinal parasitic infections in chickens. BMC Biotechnol 9: 79.