Abstract
Plant seeds are potentially one of the most economical systems for large-scale production of recombinant proteins for industrial and pharmaceutical uses. Plant-based systems in general have several advantages over the current production systems for biopharmaceuticals, such as yeasts, fungi, insect cells, mammalian cell cultures and transgenic animals. These advantages include the ability to post-translationally modify recombinant proteins, cost-effective production of recombinant proteins, due to the ease of scale-up and the availability of established protocols for harvesting, transport, storage and processing, and a minimal possibility of product contamination by animal/human pathogens. Plant seeds have a further significant advantage, that of providing a stable repository for recombinant proteins. Despite significant progress in the use of transgenic plants and seeds for therapeutic protein production, there are still technical challenges that must be surmounted before these systems can be fully embraced as suitable, viable alternatives for large-scale production of biopharmaceuticals and other products. These challenges include: (1) Enhancing the yields of recombinant proteins to maximize economic feasibility; (2) Manipulating the post-translational machinery of the plant or seed so that the recombinant protein is structurally and functionally similar to the native protein; (3) Developing efficient methods for downstream processing of recombinant proteins, including the removal of any foreign amino acid motifs, in vitro post-translational processing and protein purification, and (4) Addressing regulatory issues, such as suitable mechanisms for containment of the transgenic materials to prevent inadvertent transgene flow. Considerable strides have been made toward addressing these challenges particularly in the past 5 years. This has culminated in some plant-derived pharmaceutical proteins including antibodies, vaccines, human blood products and growth regulators reaching the stage of preclinical studies or commercial development, and the promise of the first plant-made pharmaceutical glycoprotein intended for human parenteral administration. Below this progress is reviewed, with an emphasis on enhancing protein yields in seeds and controlling the N-glycan status of seed-produced recombinant proteins.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ali S, Taylor WC (2001) The 3′ non-coding region of a C4 photosynthesis gene increases transgene expression when combined with heterologous promoters. Plant Mol Biol 46:325–333
Allison M (2010) As Genzyme flounders, competitors and activist investors swoop in. Nat Biotechnol 28:3–4
Arcalis E, Marcel S, Altmann F, Kolarich D, Drakakaki G, Fischer R, Christou P, Stoger E (2004) Unexpected deposition patterns of recombinant proteins in post-endoplasmic reticulum compartments of wheat endosperm. Plant Physiol 136:3457–3466
Arcalis E, Stadlmann J, Marcel S, Drakakaki G, Winter V, Rodriguez J, Fischer R, Altmann F, Stoger E (2010) The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol 153:693–702
Bakker H, Bardor M, Molthoff JW, Gomord V, Elbers I, Stevens LH, Jordi W, Lommen A, Faye L, Lerouge P, Bosch D (2001) Galactose-extended glycans of antibodies produced by transgenic plants. Proc Natl Acad Sci USA 98:2899–2904
Bakker H, Rouwendal GA, Karnoup AS, Florack DEA, Stoopen GM, Helsper JPF, 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
Banki MR, Feng L, Wood DW (2005) Simple bioseparations using self-cleaving elastin-like polypeptide tags. Nat Methods 2:659–661
Barbante A, Irons S, Hawes C, Frigerio L, Vitale A, Pedrazzini E (2008) Anchorage to the cytosolic face of the endoplasmic reticulum membrane: a new strategy to stabilize a cytosolic recombinant antigen in plants. Plant Biotechnol J 6:560–575
Beck A, Wagner-Rousset E, Bussat MC, Lokteff M, Klinguer-Hamour C, Haeuw JF, Goetsch L, Van Dorsselaer A, Corvaïa N (2008) Trends in glycosylation, glycoanalysis and glycoengineering of therapeutic antibodies and Fc-fusion proteins. Curr Pharm Biotechnol 9:482–501
Benchabane M, Goulet C, Rivard D, Faye L, Gomord V, Michaud D (2008) Preventing unintended proteolysis in plant protein biofactories. Plant Biotechnol J 6:633–648
Boothe J, Nykiforuk C, Shen Y, Zaplachinski S, Szarka S, Kuhlman P, Murray E, Morck D, Moloney MM (2010) Seed-based expression systems for plant molecular farming. Plant Biotechnol J 8:588–606
Castilho A, Strasser R, Stadlmann J, Grass J, Jez J, Gattinger P, Kunert R, Quendler H, Pabst M, Leonard R, Altmann F, Steinkellner H (2010) In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 285:15923–15930
Cheung SC, Sun SS, Chan JC, Tong PC (2009) Expression and subcellular targeting of human insulin-like growth factor binding protein-3 in transgenic tobacco. Transgenic Res 18:943–951
Chikwamba R, McMurray J, Shou H, Frame B, Pegg SE, Scott P, Mason H, Wang K (2002) Expression of a synthetic E. coli heat-labile enterotoxin B sub-unit (LT-B) in maize. Mol Breed 10:253–265
Clarke LA (2008) The mucopolysaccharidoses: a success of molecular medicine. Expert Rev Mol Med 10:e 1
Conley AJ, Joensuu JJ, Menassa R, Brandle JE (2009) Induction of protein body formation in plant leaves by elastin-like polypeptide fusions. BMC Biol 7:48
Conley AJ, Joensuu JJ, Richman A, Menassa R (2011) Protein body-inducing fusions for high-level production and purification of recombinant proteins in plants. Plant Biotechnol J 9:419–433
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
Cunha NB, Araújo ACG, Leite A, Murad AM, Vianna GR, Rech EL (2010) Correct targeting of proinsulin in protein storage vacuoles of transgenic soybean seeds. Genet Mol Res 9:1163–1170
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
De Muynck B, Navarre C, Boutry M (2010) Production of antibodies in plants: status after twenty years. Plant Biotechnol J 8:529–563
de Virgilio M, De Marchis F, Bellucci M, Mainieri D, Rossi M, Benvenuto E, Arcioni S, Vitale A (2008) The human immunodeficiency virus antigen Nef forms protein bodies in leaves of transgenic tobacco when fused to zeolin. J Exp Bot 59:2815–2829
de Vries JM, van der Beek NAME, Kroos MA, Özkan L, van Doorn PA, Richards SM, Sung CCC, Brugma J-D C, Zandbergen AAM, van der Ploeg AT, Reuser AJJ (2010) High antibody titer in an adult with Pompe disease affects treatment with alglucosidase alfa. Mol Genet Metab 101:338–345
Desnick RJ, Schuchman EH (2002) Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat Rev Genet 3:954–966
Downing WL, Galpin JD, Clemens S, Lauzon SM, Samuels AL, Pidkowich MS, Clarke A, Kermode AR (2006) Synthesis of enzymatically active human alpha-L-iduronidase in Arabidopsis cgl (complex glycan-deficient) seeds. Plant Biotechnol J 4:169–181
Downing WL, Hu X, Kermode AR (2007) Post-transcriptional factors are important for high-level expression of the human α-L-iduronidase gene in Arabidopsis cgl (complex-glycan-deficient) seeds. Plant Sci 172:327–334
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
Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila and Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487
Faye L, Gomord V (2010) Success stories in molecular farming – a brief overview. Plant Biotechnol J 8:525–528
Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM (2004) Plant-based production of biopharmaceuticals. Curr Opin Plant Biol 7:152–158
Floss DM, Sack M, Arcalis E, Stadlmann J, Quendler H, Rademacher T, Stoger E, Scheller J, Fischer R, Conrad U (2009) Influence of elastin-like peptide fusions on the quantity and quality of a tobacco-derived human immunodeficiency virus-neutralizing antibody. Plant Biotechnol J 7:899–913
Floss DM, Schallau K, Rose-John S, Conrad U, Scheller J (2010) Elastin-like polypeptides revolutionize recombinant protein expression and their biomedical application. Trends Biotechnol 28:37–45
Fong BA, Wu W-Y, Wood DW (2009) Optimization of ELP-intein mediated protein purification by salt substitution. Protein Expr Purif 66:198–202
Fox JL (2006) Turning plants into protein factories. Nat Biotechnol 24:1191–1193
Frank J, Kaulfürst-Soboll H, Rips S, Koiwa H, von Schaewen A (2008) Comparative analyses of Arabidopsis complex glycan1 mutants and genetic interaction with staurosporin and temperature sensitive3a. Plant Physiol 148:1354–1367
Frey AD, Karg SR, Kallio PT (2009) Expression of rat beta(1,4)-N-acetylglucosaminyltransferase III in Nicotiana tabacum remodels the plant-specific N-glycosylation. Plant Biotechnol J 6:33–48
Fu LH, Miao Y, Lo SW, Seto TC, Sun SSM, Xu Z-F, Clemens S, Clarke LA, Kermode AR, Jiang L (2009) Production and characterization of soluble human lysosomal enzyme α-iduronidase with high activity from culture media of transgenic tobacco BY-2 cells. Plant Sci 177:668–675
Gallie DR (2002) The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res 30:3401–3411
Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TM (1987) A comparison of eukaryotic viral 5′-leader sequences as enhancers of mRNA expression in vivo. Nucleic Acids Res 15:8693–8711
Galpin JD, Clemens S, Kermode AR (2010) The carboxy-terminal ER-retention motif, SEKDEL, influences the N-linked glycosylation of recombinant human α-L-iduronidase but has little effect on enzyme activity in seeds of Brassica napus and Nicotiana tabacum. Plant Sci 178:440–447
Geli MI, Torrent M, Ludevid D (1994) Two structural domains mediate two sequential events in [Gamma]-zein targeting: protein endoplasmic reticulum retention and protein body formation. Plant Cell 6:1911–1922
Giddings G, Allison G, Brooks D, Carter A (2000) Transgenic plants as factories for biopharmaceuticals. Nat Biotechnol 18:1151–1155
Gomord V, Faye L (2004) Post-translational modification of therapeutic proteins in plants. Curr Opin Plant Biol 7:171–181
Gomord V, Fischette A-C, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C, Michaud D, Faye L (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8:564–587
Goossens A, Dillen W, De Clercq J, Van Montagu M, Angenon G (1999a) The arcelin-5 gene of Phaseolus vulgaris directs high seed-specific expression in transgenic Phaseolus acutifolius and Arabidopsis plants. Plant Physiol 20:1095–1104
Goossens A, Van Montagu M, Angenon G (1999b) Co-introduction of an antisense gene for an endogenous seed storage protein can increase expression of a transgene in Arabidopsis thaliana seeds. FEBS Lett 456:160–164
Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22:346–353
Hakanpää J, Paananen A, Askolin S, Nakari-Setälä T, Parkkinen T, Penttilä M, Linder MB, Rouvinen J (2004) Atomic resolution structure of the hfbii hydrophobin, a self-assembling amphiphile. J Biol Chem 279:534–539
Henquet M, Lehle L, Schreuder M, Rouwendal G, Molthoff J, Helsper J, Van Der Krol S, Bosch D (2008) Identification of the gene encoding the alpha1,3-mannosyltransferase (ALG3) in Arabidopsis and characterization of downstream N-glycan processing. Plant Cell 20:1652–1664
Henquet M, Eigenhuijsen J, Hesselink T, Spiegel H, Schreuder M, van Duijn E, Cordewener J, Depicker A, van der Krol A, Bosch D (2010) Characterization of the single-chain Fv-Fc antibody MBP10 produced in Arabidopsis alg3 mutant seeds. Transgenic Res. doi:10.1007/s11248-010-9475-5
Hossler P, Khattak SF, Li ZJ (2009) Optimal and consistent protein glycosylation in mammalian cell culture. Glycobiology 19:936–949
Huang J, Wu L, Yalda D, Adkins Y, Kelleher SL, Crane M, Lonnerdal B, Rodriguez RL, Huang N (2002) Expression of functional recombinant human lysozyme in transgenic rice culture. Transgenic Res 11:229–239
Jiang L, Sun SS (2002) Membrane anchors for vacuolar targeting: application in plant bioreactors. Trends Biotechnol 20:99–102
Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–770
Joensuu JJ, Conley AJ, Lienemann M, Brandle JE, Linder MB, Menassa R (2010) Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana Benthamiana. Plant Physiol 152:622–633
Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993–1001
Kajiura H, Seki T, Fujiyama K (2010) Arabidopsis thaliana ALG3 mutant synthesizes immature oligosaccharides in the ER and accumulates unique N-glycans. Glycobiology 20:736–751
Karg SR, Kallio PT (2009) The production of biopharmaceuticals in plant systems. Biotechnol Adv 27:879–894
Karg SR, Frey AD, Ferrara C, Streich DK, Umaña P, Kallio PT (2009) A small-scale method for the preparation of plant N-linked glycans from soluble proteins for analysis by MALDI-TOF mass spectrometry. Plant Physiol Biochem 47:160–166
Karnoup AS, Kuppannan K, Young SA (2007) A novel HPLC-UV-MS method for quantitative analysis of protein glycosylation. J Chromatogr B Anal Technol Biomed Life Sci 859:178–191
Kawaguchi R, Bailey-Serres J (2002) Regulation of translation initiation in plants. Curr Opin Plant Biol 5:460–465
Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 33:955–965
Kermode AR (1996) Mechanisms of intracellular protein transport and targeting. Crit Rev Plant Sci 15:285–423
Kermode AR (2006) Plants as factories for production of biopharmaceutical and bioindustrial proteins: lessons from cell biology. Can J Bot 84:679–694
Kermode AR, Zeng Y, Hu X, Lauson S, Abrams SR, He X (2007) Ectopic expression of a conifer Abscisic Acid Insensitive3 transcription factor induces high-level synthesis of recombinant human α-L-iduronidase in transgenic tobacco leaves. Plant Mol Biol 63:763–776
Ko K, Tekoah Y, Rudd PM, Harvey DJ, Dwek RA, Spitsin S, Hanlon CA, Rupprecht C, Dietzschold B, Golovkin M, Koprowski H (2003) Function and glycosylation of plant-derived antiviral monoclonal antibody. Proc Natl Acad Sci USA 100:8013–8018
Kogan MJ, Dalcol I, Gorostiza P, Lopez-Iglesias C, Pons M, Sanz F, Ludevid D, Giralt E (2001) Self-assembly of the amphipathic helix (VHLPPP)8. A mechanism for zein protein body formation. J Mol Biol 312:907–913
Kogelberg H, Tolner B, Sharma SK, Lowdell MW, Qureshi U, Robson M, Hillyer T, Pedley RB, Vervecken W, Contreras R, Begent RH, Chester KA (2007) Clearance mechanism of a mannosylated antibody-enzyme fusion protein used in experimental cancer therapy. Glycobiology 17:36–45, Erratum in: Glycobiol 17: 1030
Koprivova A, Stemmer C, Altmann F, Hoffmann A, Kopriva S, Gorr G, Reski R, Decker EL (2004) Targeted knockouts of Physcomitrella lacking plant-specific immunogenic N-glycans. Plant Biotechnol J 2:517–523
Kozak M (1991) A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr 1:111–115
Lau OS, Sun SSM (2009) Plant seeds as bioreactors for recombinant protein production. Biotechnol Adv 27:1015–1022
Lerouge P, Cabanes-Macheteau M, Rayon C, Fischette-Lainé A-C, Gomord V, Faye L (1998) N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol Biol 38:31–48
Liu WX, Liu HL, Chai ZJ, Xu XP, Song YR, Qu LQ (2010) Evaluation of seed storage-protein gene 5′ untranslated regions in enhancing gene expression in transgenic rice seed. Theor Appl Genet 121:1267–1274
Llop-Tous I, Madurga S, Giralt E, Marzabal P, Torrent M, Ludevid MD (2010) Relevant elements of a maize gamma-zein domain involved in protein body biogenesis. J Biol Chem 285:35633–35644
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
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 thaliana. Plant Physiol 155:2036–2048
Ma JK-C, Drake PMW, Christou P (2003) The production of recombinant pharmaceutical proteins in plants. Nat Rev Genet 4:794–805
Ma S, Huang Y, Davis A, Yin Z, Mi Q, Menassa R, Brandle JE, Jevnikar AM (2005) Production of biologically active human interleukin-4 in transgenic tobacco and potato. Plant Biotechnol J 3:309–318
Mainieri D, Rossi M, Archinti M, Bellucci M, De Marchis F, Vavassori S, Pompa A, Arcioni S, Vitale A (2004) Zeolin. A new recombinant storage protein constructed using maize γ-zein and bean phaseolin. Plant Physiol 136:3447–3456
Matsuo K, Matsumura T (2011) Deletion of fucose residues in plant N-glycans by repression of the GDP-mannose 4,6-dehydratase gene using virus-induced gene silencing and RNA interference. Plant Biotechnol J 9:264–281
Misaki R, Kimura Y, Palacpac NQ, Yoshida S, Fujiyama K, Seki T (2003) Plant cultured cells expressing human beta-(1,4)-galactosyltransferase secrete glycoproteins with galactose-extended N-linked glycans. Glycobiology 13:199–205
Morandini F, Avesani L, Bortesi L, Van Droogenbroeck B, De Wilde K, Arcalis E, Bazzoni F, Santi L, Brozzetti A, Falorni A, Stoger E, Depicker A, Pezzotti M (2011) Non-food⁄feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol J 1–11. doi:10.1111/j.1467-7652.2011.00605.x
Moravec T, Schmidt MA, Herman EM, Woodford-Thomas T (2007) Production of Escherichia coli heat labile toxin (LT) B subunit in soybean seed and analysis of its immunogenicity as an oral vaccine. Vaccine 25:1647–1657
Nicholson L, Gonzales-Melendi P, van Dolleweerd C, Tuck H, Perrin Y, Ma JK-C, Fischer R, Christou P, Stoger E (2005) A recombinant multimeric immunoglobin expressed in rice shows assembly-dependent subcellular localization in endosperm cells. Plant Biotechnol J 3:115–127
Niimura Y, Terabe M, Gojobori T, Miura K (2003) Comparative analysis of the base biases at the gene terminal portions in seven eukaryote genomes. Nucleic Acids Res 31:5195–5201
Nykiforuk CL, Boothe JG, Murray EW, Keon RG, Goren HJ, Markley NA, Moloney MM (2006) Transgenic expression and recovery of biologically active recombinant human insulin from Arabidopsis thaliana seeds. Plant Biotechnol J 4:77–85
Palacpac NQ, Yoshida S, Sakai H, Kimura Y, Fujiyama K, Yoshida T, Seki T (1999) Stable expression of human beta1,4-galactosyltransferase in plant cells modifies N-linked glycosylation patterns. Proc Natl Acad Sci USA 96:4692–4697
Petruccelli S, Otegui MS, Lareu F, Tran Dinh O, 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
Pooggin MM, Skryabin KG (1992) The 5′-untranslated leader sequence of potato virus X RNA enhances the expression of a heterologous gene in vivo. Mol Gen Genet 234:329–331
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-gycans. Plant Biotechnol J 6:189–201
Reggi S, Marchetti S, Patti T, De Amicis F, Cariati R, Bembi B, Fogher C (2005) Recombinant human acid β-glucosidase stored in tobacco seed is stable, active and taken up by fibroblasts. Plant Mol Biol 57:101–113
Richter LJ, Thanavala Y, Arntzen CJ, Mason HS (2000) Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol 18:1167–1171
Saito Y, Kishida K, Takata K, Takahashi H, Shimada T, Tanaka K, Morita S, Satoh S, Masumura T (2009) A green fluorescent protein fused to rice prolamin forms protein body-like structures in transgenic rice. J Exp Bot 60:615–627
Sawant SV, Kiran K, Singh PK, Tuli R (2001) Sequence architecture downstream of the initiator codon enhances gene expression and protein stability in plants. Plant Physiol 126:1630–1636
Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H (2007) Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J 5:657–663
Scheller J, Leps M, Conrad U (2006) Forcing single-chain variable fragment production in tobacco seeds by fusion to elastin-like polypeptides. Plant Biotechnol J 4:243–249
Schinkel H, Schiermeyer A, Soeur R, Fischer R, Schillberg S (2005) Production of an active recombinant thrombomodulin derivative in transgenic tobacco plants and suspension cells. Transgenic Res 14:251–259
Schmidt MA, Herman EM (2008) Proteome rebalancing in soybean seeds can be exploited to enhance foreign protein accumulation. Plant Biotechnol J 6:832–842
Semenyuk EG, Schmidt MA, Beachy RN, Moravec T, Woodford-Thomas T (2010) Adaptation of an ecdysone-based genetic switch for transgene expression in soybean seeds. Transgenic Res 19:987–999
Shaaltiel Y, Bartfeld D, Hashmueli S, Baum G, Brill-Almon E, Galili G, Dym O, Boldin-Adamsky SA, Silman I, Sussman JL, Futerman 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
Sijmons PC, Dekker BM, Schrammeijer B, Verwoerd TC, van den Elzen PJ, Hoekema A (1990) Production of correctly processed human serum albumin in transgenic plants. Biotechnology 8:217–221
Sourrouille C, Marquet-Blouin E, D’Aoust MA, Kiefer-Meyer M-C, Séveno M, Pagny-Salehabadi S, Bardor M, Durambur G, Lerouge P, Vezina L, Gomord V (2008) Down-regulated expression of plant-specific glycoepitopes in alfalfa. Plant Biotechnol J 6:702–721
Sriraman R, Bardor M, Sack M, Vaquero C, Faye L, Fischer R, Finnern R, Lerouge P (2004) Recombinant anti-hCG antibodies retained in the endoplasmic reticulum of transformed plants lack core-xylose and core-alpha(1,3)-fucose residues. Plant Biotechnol J 2:279–287
Stoger E, Ma JK-C, Fischer R, Christou P (2005) Sowing the seeds of success: pharmaceutical proteins from plants. Curr Opin Biotechnol 16:167–173
Strasser R, Altmann F, Mach L, Glössl J, Stadlmann J, Steinkellner H (2004) Generation of Arabidopsis thaliana plants with complex N-glycans lacking beta1,2-linked xylose and core alpha1,3-linked fucose. FEBS Lett 561:132–136
Strasser R, Stadlmann J, Schähs M, Stiegler G, Quendler H, Mach L, Glössl 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
Tekoah Y, Ko K, Koprowski H, Harvey DJ, Wormald MR, Dwek RA, Rudd PM (2004) Controlled glycosylation of therapeutic antibodies in plants. Arch Biochem Biophys 426:266–278
Torrent M, Llompart B, Lasserre-Ramassamy S, Llop-Tous I, Bastida M, Marzabal P, Westerholm-Parvinen A, Saloheimo M, Heifetz PB, Ludevid MD (2009a) Eukaryotic protein production in designed storage organelles. BMC Biol 7:5
Torrent M, Llop-Tous I, Ludevid MD (2009b) Protein body induction: a new tool to produce and recover recombinant proteins in plants. Methods Mol Biol 483:193–208
Torres E, Gonzales-Melendi P, Stoger E, Shaw P, Twyman RM, Nicholson L, Vaquero C, Fischer R, Christou P, Perrin Y (2001) Native and artificial reticuloplasmins co-accumulate in distinct domains of the endoplasmic reticulum and in post-endoplasmic reticulum compartments. Plant Physiol 127:1212–1223
Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol 21:570–578
Vain P, Finer KR, Engler DE, Pratt RC, Finer JJ (1996) Intron-mediated enhancement of gene expression in maize (Zea Mays L.) and bluegrass (Poa pratensis L.). Plant Cell Rep 15:489–494
Van Hoof A, Green PJ (1997) Rare codons are not sufficient to destabilize a reporter gene transcript in tobacco. Plant Mol Biol 35:383–387
van Rooijen GJ, Moloney MM (1995) Plant seed oil-bodies as carriers for foreign proteins. Biotechnology (NY) 13:72–77
Vézina LP, Faye L, Lerouge P, D’Aoust MA, Marquet-Blouin E, Burel C, Lavoie PO, Bardor M, Gomord V (2009) Transient co-expression for fast and high-yield production of antibodies with human-like N-glycans in plants. Plant Biotechnol J 7:442–455
Vitale A, Boston RS (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9:1581–1588
Vitale A, Hinz G (2005) Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci 10:316–323
von Schaewen A, Sturm A, O’Neill J, Chrispeels MJ (1993) Isolation of a mutant Arabidopsis that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-mediated complex N-linked glycans. Plant Physiol 102:1109–1118
Walsh G, Jefferis R (2006) Post-translational modifications in the context of therapeutic proteins. Nat Biotechnol 24:1241–1252
Wang X, Shi F, Wösten HA, Hektor H, Poolman B, Robillard GT (2005) The SC3 hydrophobin self-assembles into a membrane with distinct mass transfer properties. Biophys J 88:3434–3443
Werber Y (2004) Lysosomal storage diseases market. Nat Rev 3:9–10
Yang D, Wu L, Hwang Y-S, Chen L, Huang N (2001) Expression of the REB transcriptional activator in rice grains improves the yield of recombinant proteins whose genes are controlled by a Reb-responsive promoter. Proc Natl Acad Sci USA 98:11438–11443
Yang DC, Guo FL, Liu B, Huang N, Watkins SC (2003) Expression and localization of human lysozyme in the endosperm of transgenic rice. Planta 216:597–603
Yang J, Barr LA, Fahnestock SR, Liu ZB (2005) High yield recombinant silk-like protein production in transgenic plants through protein targeting. Transgenic Res 14:313–324
Acknowledgement
This work was supported in part by a Natural Sciences and Engineering Research Council (NSERC) Strategic grant and by a Michael Smith Foundation for Health Research Senior Scholar Award. Dedicated to the loving memory of Virginia.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Kermode, A.R. (2012). Seed Expression Systems for Molecular Farming. In: Wang, A., Ma, S. (eds) Molecular Farming in Plants: Recent Advances and Future Prospects. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2217-0_5
Download citation
DOI: https://doi.org/10.1007/978-94-007-2217-0_5
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-2216-3
Online ISBN: 978-94-007-2217-0
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)