Accumulation of secreted antibodies in plant cell cultures varies according to the isotype, host species and culture conditions

Plant Biotechnology Journal

Volumn 12, Issue 4, 2014, Pages 457-467

  Magy, Bertrand ^a   Tollet, Jérémie ^a   Laterre, Raphaëlle ^a   Boutry, Marc ^a   Navarre, Catherine ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Antibody; Arabidopsis; Isotype; Nicotiana; Protease; Suspension cells

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM;

CULTURE MEDIUM; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G; SUSPENSION;

ANIMAL; ARABIDOPSIS; CELL LINE; CHEMISTRY; CULTURE MEDIUM; CULTURE TECHNIQUE; EXTRACELLULAR SPACE; HUMAN; METABOLISM; MOUSE; PLANT CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES; PROTEIN DEGRADATION; SPECIES DIFFERENCE; SUSPENSION; TIME; TOBACCO; TRANSGENIC PLANT;

ANIMALS; ARABIDOPSIS; CELL CULTURE TECHNIQUES; CELL LINE; CULTURE MEDIA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXTRACELLULAR SPACE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN ISOTYPES; MICE; PLANT CELLS; PLANTS, GENETICALLY MODIFIED; PROTEOLYSIS; SPECIES SPECIFICITY; SUSPENSIONS; TIME FACTORS; TOBACCO;

EID: 84899129295     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12152     Document Type: Article

References (42)

1. Axelos, M., Curie, C., Mazzolini, L. and Bardet, C. (1992) A protocol for transient gene expression in Arabidopsis thaliana protoplasts isolated from cell suspension cultures. Plant Physiol. Biochem. 30, 123-128.
2. Baici, A., Knopfel, M. and Fehr, K. (1982) Cleavage of the four human IgG subclasses with cathepsin G. Scand. J. Immunol. 16, 487-498.
3. Benchabane, M., Goulet, C., Rivard, D., Faye, L., Gomord, V. and Michaud, D. (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol. J. 6, 633-648.
4. Berasain, P., Carmona, C., Frangione, B., Cazzulo, J.J. and Goni, F. (2003) Specific cleavage sites on human IgG subclasses by cruzipain, the major cysteine proteinase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 130, 23-29.
5. Borderies, G., Jamet, E., Lafitte, C., Rossignol, M., Jauneau, A., Boudart, G., Monsarrat, B., Esquerre-Tugaye, M.T., Boudet, A. and Pont-Lezica, R. (2003) Proteomics of loosely bound cell wall proteins of Arabidopsis thaliana cell suspension cultures: a critical analysis. Electrophoresis, 24, 3421-3432.
6. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Brezski, R.J. and Jordan, R.E. (2010) Cleavage of IgGs by proteases associated with invasive diseases: an evasion tactic against host immunity? mAbs, 2, 212-220.
8. Calinski, A., Classen, B., Zoglauer, K. and Boehm, R. (2009) IgG stability in fresh and conditioned medium of tobacco (Nicotiana tabacum) and larch (Larix decidua) embryogenic suspension cultures. Biotechnol. Lett. 31, 771-778.
9. Correia, I.R. (2010) Stability of IgG isotypes in serum. mAbs, 2, 221-232.
10. De Muynck, B., Navarre, C., Nizet, Y., Stadlmann, J. and Boutry, M. (2009) Different subcellular localization and glycosylation for a functional antibody expressed in Nicotiana tabacum plants and suspension cells. Transgenic Res. 18, 467-482.
11. De Muynck, B., Navarre, C. and Boutry, M. (2010) Production of antibodies in plants: status after twenty years. Plant Biotechnol. J. 8, 529-563.
12. Doran, P.M. (2006a) Foreign protein degradation and instability in plants and plant tissue cultures. Trends Biotechnol. 24, 426-432.
13. Doran, P.M. (2006b) Loss of secreted antibody from transgenic plant tissue cultures due to surface adsorption. J. Biotechnol. 122, 39-54.
14. Doran, P.M. (2013) Therapeutically important proteins from in vitro plant tissue culture systems. Curr. Med. Chem. 20, 1047-1055.
15. Fischer, R., Liao, Y.C. and Drossard, J. (1999) Affinity-purification of a TMV-specific recombinant full-size antibody from a transgenic tobacco suspension culture. J. Immunol. Methods, 226, 1-10.
16. van der Fits, L., Deakin, E.A., Hoge, J.H.C. and Memelink, J. (2000) The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation. Plant Mol. Biol. 43, 495-502.
17. Goderis, I., De Bolle, M.F.C., Francois, I., Wouters, P.F.J., Broekaert, W.F. and Cammue, B.P.A. (2002) A set of modular plant transformation vectors allowing flexible insertion of up to six expression units. Plant Mol. Biol. 50, 17-27.
18. Gomord, V., Fitchette, A.C., Menu-Bouaouiche, L., Saint-Jore-Dupas, C., Plasson, C., Michaud, D. and Faye, L. (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol. J. 8, 564-587.
19. Hellwig, S., Drossard, J., Twyman, R.M. and Fischer, R. (2004) Plant cell cultures for the production of recombinant proteins. Nat. Biotechnol. 22, 1415-1422.
20. Holland, T., Sack, M., Rademacher, T., Schmale, K., Altmann, F., Stadlmann, J., Fischer, R. and Hellwig, S. (2010) Optimal nitrogen supply as a key to increased and sustained production of a monoclonal full-size antibody in BY-2 suspension culture. Biotechnol. Bioeng. 107, 278-289.
21. Huang, T.K. and McDonald, K.A. (2012) Molecular farming using bioreactor-based plant cell suspension cultures for recombinant protein production. In: Molecular Farming in Plants: Recent Advances and Future Prospects (Wang, A. and Ma, S., eds), pp. 37-67. the Netherlands: Springer Netherlands.
22. Kirchhoff, J., Raven, N., Boes, A., Roberts, J.L., Russell, S., Treffenfeldt, W., Fischer, R., Schinkel, H., Schiermeyer, A. and Schillberg, S. (2012) Monoclonal tobacco cell lines with enhanced recombinant protein yields can be generated from heterogeneous cell suspension cultures by flow sorting. Plant Biotechnol. J. 10, 936-944.
23. Kwon, J.-Y., Lee, K.-H., Cheon, S.-H., Ryu, H.-N., Kim, S. and Kim, D.-I. (2012) Adsorptive loss of secreted recombinant proteins in transgenic rice cell suspension cultures. Plant Cell Rep. 31, 551-560.
24. Loos, A. and Steinkellner, H. (2012) IgG-Fc glycoengineering in non-mammalian expression hosts. Arch. Biochem. Biophys. 526, 167-173.
25. López, J., Lencina, F., Petruccelli, S., Marconi, P. and Alvarez, M. (2010) Influence of the KDEL signal, DMSO and mannitol on the production of the recombinant antibody 14D9 by long-term Nicotiana tabacum cell suspension culture. Plant Cell, Tissue Organ Cult. 103, 307-314.
26. McDonald, K.A. and Huang, T.K. (2009) Bioreactor engineering for recombinant protein production in plant cell suspension cultures. Biochem. Eng. J. 45, 168-184.
27. Nagata, T., Nemoto, Y. and Hasezawa, S. (1992) Tobacco by-2 cell-line as the HeLa-cell in the cell biology of higher-plants. Int. Rev. Cytol. 132, 1-30.
28. Navarre, C., De Muynck, B., Alves, G., Vertommen, D., Magy, B. and Boutry, M. (2012) Identification, gene cloning and expression of serine proteases in the extracellular medium of Nicotiana tabacum cells. Plant Cell Rep. 10, 1959-1968.
29. Paul, M. and Ma, J.K.C. (2011) Plant-made pharmaceuticals: leading products and production platforms. Biotechnol. Appl. Biochem. 58, 58-67.
30. Salfeld, J.G. (2007) Isotype selection in antibody engineering. Nat. Biotech. 25, 1369-1372.
31. Schuurman, J., Perdok, G.J., Gorter, A.D. and Aalberse, R.C. (2001) The inter-heavy chain disulfide bonds of IgG4 are in equilibrium with intra-chain disulfide bonds. Mol. Immunol. 38, 1-8.
32. Sharp, J.M. and Doran, P.M. (2001a) Characterization of monoclonal antibody fragments produced by plant cells. Biotechnol. Bioeng. 73, 338-346.
33. Sharp, J.M. and Doran, P.M. (2001b) Strategies for enhancing monoclonal antibody accumulation in plant cell and organ cultures. Biotechnol. Prog. 17, 979-992.
34. Sheridan, C. (2010) Fresh from the biologic pipeline-2009. Nat. Biotech. 28, 307-310.
35. Tsoi, B.M. and Doran, P.M. (2002) Effect of medium properties and additives on antibody stability and accumulation in suspended plant cell cultures. Biotechnol. Appl. Biochem. 35, 171-180.
36. Twyman, R.M., Schillberg, S. and Fischer, R. (2012) The production of vaccines and therapeutic antibodies in plants. In Molecular Farming in Plants: Recent Advances and Future Prospects (Wang, A. and Ma, S., eds), pp. 145-159. the Netherlands: Springer Netherlands.
37. Ullisch, D.A., Muller, C.A., Maibaum, S., Kirchhoff, J., Schiermeyer, A., Schillberg, S., Roberts, J.L., Treffenfeldt, W. and Buchs, J. (2012) Comprehensive characterization of two different Nicotiana tabacum cell lines leads to doubled GFP and HA protein production by media optimization. J. Biosci. Bioeng. 113, 242-248.
38. Vasilev, N., Gromping, U., Lipperts, A., Raven, N., Fischer, R. and Schillberg, S. (2013) Optimization of BY-2 cell suspension culture medium for the production of a human antibody using a combination of fractional factorial designs and the response surface method. Plant Biotechnol. J. 11, 867-874.
39. Whaley, K.J., Hiatt, A. and Zeitlin, L. (2011) Emerging antibody products and Nicotiana manufacturing. Hum. Vaccin. 7, 349-356.
40. Xu, J., Ge, X. and Dolan, M.C. (2011) Towards high-yield production of pharmaceutical proteins with plant cell suspension cultures. Biotechnol. Adv. 29, 278-299.
41. Xu, J., Dolan, M.C., Medrano, G., Cramer, C.L. and Weathers, P.J. (2012) Green factory: plants as bioproduction platforms for recombinant proteins. Biotechnol. Adv. 30, 1171-1184.
42. Yusibov, V., Streatfield, S.J. and Kushnir, N. (2011) Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond. Hum. Vaccin. 7, 313-321.