Molecular farming in tobacco hairy roots by triggering the secretion of a pharmaceutical antibody

Biotechnology and Bioengineering

Volumn 111, Issue 2, 2014, Pages 336-346

  Häkkinen, Suvi T ^a   Raven, Nicole ^b   Henquet, Maurice ^c   Laukkanen, Marja Leena ^a   Anderlei, Tibor ^d   Pitkänen, Juha Pekka ^a   Twyman, Richard M ^e   Bosch, Dirk ^c   Oksman Caldentey, Kirsi Marja ^a   Schillberg, Stefan ^b   Ritala, Anneli ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d Kühner   (Switzerland)

^e TRM Ltd   (United Kingdom)

Author keywords

Antibody; Hairy roots; Molecular farming; Secretion; Tobacco

Indexed keywords

COMPLEX-TYPE GLYCANS; HAIRY ROOTS; LATERAL ROOT FORMATION; MOLECULAR FARMING; MORPHOLOGICAL CHANGES; PHARMACEUTICAL PROTEIN; POLY VINYL PYRROLIDONE; SECRETION;

AFFINITY CHROMATOGRAPHY; ANTIBODIES; DESIGN OF EXPERIMENTS; ENZYME ACTIVITY; MONOCLONAL ANTIBODIES; OPTIMIZATION; PHYSIOLOGY; POLYSACCHARIDES; RECOMBINANT PROTEINS;

TOBACCO;

1 NAPHTHYLACETIC ACID; GLYCAN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY M12; POVIDONE; PROTEIN A; SEPHAROSE; UNCLASSIFIED DRUG; ANTIBODY; CULTURE MEDIUM; POLYSACCHARIDE; RECOMBINANT PROTEIN;

ANTIBODY PRODUCTION; ARTICLE; BINDING ASSAY; CHROMATOGRAPHY; CONTROLLED STUDY; CULTURE MEDIUM; HAIRY ROOT CULTURE; MICROSCOPY; MOLECULAR CLONING; MOLECULAR FARMING; PLANT ROOT; PROTEIN ISOLATION; PROTEIN PURIFICATION; ROOT MORPHOLOGY; TOBACCO; CHEMISTRY; GENETICS; GLYCOSYLATION; ISOLATION AND PURIFICATION; METABOLISM; PHARMACEUTICS; PROCEDURES;

NICOTIANA TABACUM;

ANTIBODIES; CULTURE MEDIA; GLYCOSYLATION; MOLECULAR FARMING; PLANT ROOTS; POLYSACCHARIDES; RECOMBINANT PROTEINS; TECHNOLOGY, PHARMACEUTICAL; TOBACCO;

EID: 84890798095     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25113     Document Type: Article

References (55)

1. Anderlei T, Mrotzek C, Bartsch S, Amoabediny G, Peter CP, Büchs J. 2007. New method to determine the mass transfer resistance of sterile closures for shaken bioreactors. Biotechnol Bioeng 98:999-1007.
2. Bakker H, Rouwendal GJ, Karnoup AS, Florack DE, Stoopen GM, Helsper JP, van Ree R, van Die I, Bosch D. 2006. An antibody produced in tobacco expressing a hybrid beta-1, 4-galactosyltransferase is essentially devoid of plant carbohydrate epitopes. Proc Natl Acad Sci USA 103:7577-7582.
3. Bloemendal HJ, de Boer HC, Koop EA, van Dongen AJ, Goldschmeding R, Landman WJM, Logtenberg T, Gebbink MFBG, Voest EE. 2004. Activated vitronectin as a target for anticancer therapy with human antibodies. Cancer Immunol Immunother 53:799-808.
4. Bourdeau N, Bissell MJ. 1998. Extracellular matrix signalling: Integration of form and function in normal and malignant cells. Curr Opin Cell Biol 10:640-646.
5. 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.
6. De Smet I. 2012. Lateral root initiation: One step at a time. New Phytol 193(4):867-873.
7. Drake PMW, Chargelegue DM, Vine ND, Dolleweerd CJ, Obrecon P, Ma JKC. 2003. Rhizosecretion of a monoclonal antibody protein complex from transgenic tobacco roots. Plant Mol Biol 52:233-241.
8. Drake PMW, Barbi T, Sexton A, McGowan E, Stadlmann J, Navarre C, Paul MJ, Ma JKC. 2009. Development of rhizosecretion as a production system for recombinant proteins from hydroponic cultivated tobacco. FASEB J 23:3581-3589.
9. Elbers IJ, Stoopen GM, Bakker H, Stevens LH, Bardor M, Molthoff JW, Jordi WJ, Bosch D, Lommen A. 2001. Influence of growth conditions and developmental stage on N-glycan heterogeneity of transgenic immunoglobulin G and endogenous proteins in tobacco leaves. Plant Physiol 126:1314-1322.
10. Faye L, Gomord V. 2010. Success stories in molecular farming-A brief overview. Plant Biotechnol J 8:525-528.
11. Fischer R, Schillberg S, Hellwig S, Twyman RM, Drossard J. 2012. GMP issues for recombinant plant-derived pharmaceutical proteins. Biotechnol Adv 30:434-439.
12. Fujiyama K, Misaki R, Sakai Y, Omasa T, Seki T. 2009. Change in glycosylation pattern with extension of endoplasmic reticulum retention signal sequence of mouse antibody produced by suspension-cultured tobacco BY2 cells. J Biosci Bioeng 107:165-172.
13. Gaume A, Komarnytsky S, Borisjuk N, Raskin I. 2003. Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Rep 21:1188-1193.
14. Geldner N. 2013. The endodermis. Ann Rev Plant Biol 64:531-558.
15. Go EP, Rebecchi KR, Dalpathado DS, Bandu ML, Zhang Y, Desaire H. 2007. GlycoPep DB: A tool for glycopeptide analysis using a "Smart Search". Anal Chem 79:1708-1713.
16. Guillon S, Trémouillaux-Guiller J, Kumar Pati P, Rideau M, Gantet P. 2006. Hairy root research: Recent scenario and exciting prospects. Curr Opin Plant Biol 9:341-346.
17. Häkkinen ST, Ritala A. 2010. Medicinal compounds produced in plant cell factories. In: Arora R, editor. Medicinal plant biotechnology. United Kingdom: CAB International Oxfordshire. p 13-35.
18. Häkkinen ST, Tilleman S, Šwia{ogonek}tek A, De Sutter V, Rischer H, Vanhoutte I, Van Onckelen H, Hilson P, Inzé D, Oksman-Caldentey K-M, Goossens A. 2007. Functional characterisation of genes involved in pyridine alkaloid biosynthesis in tobacco. Phytochemistry 68:2773-2785.
19. Hashimoto T, Yukimune Y, Yamada Y. 1986. Tropane alkaloid production in Hyoscyamus root cultures. J Plant Physiol 124:61-75.
20. Hellwig S, Drossard J, Twyman RM, Fischer R. 2004. Plant cell cultures for the production of recombinant proteins. Nature Biotechnol 22:1415-1422.
21. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T. 2002. Auxin-mediated cell cycle activation during early lateral root induction. Plant Cell 14:2339-2351.
22. Holland T, Sack M, Rademacher T, Schmale K, Altmann F, Stadlmann J, Fischer R, 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.
23. Kirchhoff J, Raven N, Boes A, Roberts JL, Russell S, Treffenfeldt W, Fischer R, Schinkel H, Schiermeyer A, 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.
24. Kwon TH, Seo JE, Lee JH, Yang MS. 2003. Expression and secretion of the heterodimeric protein interleukin-12 in plant cell suspension culture. Biotechnol Bioeng 81:870-875.
25. LaCount W, An G, Lee JM. 1997. The effect of polyvinylpyrrolidine (PVP) on the heavy chain monoclonal antibody production from plant suspension cultures. Biotechnol Lett 19:93-96.
26. Ma JKC, Lehner T, Stabila P, Fux CI, Hiatt A. 1994. Assembly of monoclonal antibodies with IgG1 and IgA heavy chain domains in transgenic tobacco plant. Eur J Immunol 24:131-138.
27. Ma JKC, Barros E, Bock R, Christou P, Dale PJ, Dix PJ, Fischer R, Irwin J, Mahoney R, Pezzotti M, Schillberg S, Sparrow P, Stoger E, Twyman RM. 2005. Molecular farming for new drugs and vaccines-Current perspectives on the production of pharmaceuticals in transgenic plants. EMBO Rep 6:593-599.
28. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473-497.
29. Nagata T, Kumagai F. 1999. Plant cell biology through the window of the highly synchronized tobacco BY-2 cell line. Methods Cell Sci 21:123-127.
30. Nagata T, Hasezawa S, Inzé D. 2004. Tobacco BY-2 cells, biotechnology in agriculture and forestry, Vol. 53. Heidelberg, Germany: Springer Verlag. 347p.
31. Oksman-Caldentey K-M, Kivelä O, Hiltunen R. 1991. Spontaneous shoot organogenesis and plant regeneration from hairy root cultures of Hyoscyamus muticus. Plant Sci 78:129-136.
32. Oksman-Caldentey K-M, Sevón N, Vanhala L, Hiltunen R. 1994. Effect of nitrogen and sucrose on the primary and secondary metabolism of transformed root cultures of Hyoscyamus muticus. Plant Cell Tissue Org Cult 38:263-272.
33. Paul MJ, Teh AY, Twyman RM, Ma JKC. 2013. Target product selection-Where can Molecular Pharming make the difference? Curr Pharm Des 19:5478-5485.
34. Payne GF, Payne NN, Shuler ML. 1988. Bioreactor considerations for secondary metabolite production from plant cell tissue culture: Indole alkaloids from Catharanthus roseus. Biotechnol Bioeng 31:905-912.
35. Peng M, Bi Y-M, Zhu T, Rothstein SJ. 2007. Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65:775-797.
36. Pitkänen J-P, Vuolanto A. 2004. Reactor device. Finnish Patent, FI118192.
37. Raven N, Schillberg S, Kirchhoff J, Brändli J, Imseng N, Eibl R. 2011. Growth of BY-2 suspension cells and plantibody production in single-use bioreactors. In: Eibl R, Eibl D, editors. Single-use technology in biopharmaceutical manufacture. Hoboken, NJ, USA: John Wiley & Sons. p 251-261.
38. Roshchina VV, Roshchina VD. 1993. The excretory function of higher plants. Berlin Heidelberg New York: Springer.
39. Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M. 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2486-2499.
40. Schillberg S, Raven N, Fischer R, Twyman RM, Schiermeyer A. 2013. Molecular farming of pharmaceutical proteins using plant suspension cell and tissue cultures. Curr Pharm Design 19:5531-5542.
41. Shaaltiel Y, Bartfeld D, Hashmueli S, Baum G, Brill-Almon E, Galili G, Dym O, Boldin-Adamsky S-A, Silman I, Sussman JL, Futermanand AH, Aviezer D. 2007. Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol J 5:579-590.
42. Sijmons PC, Dekker BMM, Schrammeijer B, Verwoerd TC, van den Elzen BMJ, Hoekema A. 1990. Production of correctly processed human serum albumin in transgenic plants. Nature Biotechnol 8:217-221.
43. Strasser R, Bondili JS, Schoberer J, Svoboda B, Liebminger E, Glossl J, Altmann F, Steinkellner H, Mach L. 2007. Enzymatic properties and subcellular localization of Arabidopsis beta-N-acetylhexosaminidases. Plant Physiol 145:5-16.
44. Strasser R, Stadlmann J, Schahs M, Stiegler G, Quendler H, Mach L, Glossl J, Weterings K, Pabst M, Steinkellner H. 2008. 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.
45. Twyman RM, Schillberg S, Fischer R. 2005. Transgenic plants in the biopharmaceutical market. Expert Opin Emerg Drugs 10:185-218.
46. Ullisch DA, Müller CA, Maibaum S, Kirchhoff J, Schiermeyer A, Schillberg S, Roberts JL, Treffenfeldt W, Büchs 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(2):242-248.
47. Van Craeyveld V, Holopainen U, Selinheimo E, Poutanen K, Delcour JA, Courtin CM. 2009. Extensive dry ball milling of wheat and rye bran leads to in situ production of arabinoxylan oligosaccharides through nanoscale fragmentation. J Agric Food Chem 57:8467-8473.
48. Vasilev N, Grömping U, Lipperts A, Raven N, Fischer R, Schillberg S. 2013. Optimization of BY2 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.
49. Wahl MF, An G, Lee JM. 1995. Effects of dimethyl sulfoxide on heavy chain monoclonal antibody production from plant cell culture. Biotechnol Lett 17:463-468.
50. Wang YH, Garvin DF, Kochian LV. 2001. Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol 127:345-359.
51. Widholm J. 1972. The use of fluorescein diacetate and phenosaphranine for determining viability of cultured plant cells. Stain Technol 47:189-194.
52. Wongsamuth R, Doran PM. 1996. Production of monoclonal antibodies by tobacco hairy roots. Biotechnol Bioeng 54:401-415.
53. Wu A, Senter PD. 2005. Arming antibodies: Prospects and challenges for immunoconjugates. Nature Biotechnol 23:1137-1146.
54. Xu J, Dolan MC, Medrano G, Cramer CL, Weathers PJ. 2012. Green factory: Plants as bioproduction platforms for recombinant proteins. Bitechnol Adv 30:1171-1184.
55. Zimran A, Brill-Almon E, Chertkoff R, Petakov M, Blanco-Favela F, Terreros Munoz E, Solorio-Meza SE, Amato D, Duran G, Giona F, Heitner R, Rosenbaum H, Giraldo P, Mehta A, Park G, Phillips M, Elstein D, Altarescu G, Szleifer M, Hashmueli S, Aviezer D. 2011. Pivotal trial with plant cell-expressed recombinant glucocerebrosidase, taliglucerase alfa, a novel enzyme replacement therapy for Gaucher disease. Blood 118:5767-5773.