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Molecular Farming in Plants: Recent Advances and Future Prospects pp 89–123Cite as

Seed Expression Systems for Molecular Farming

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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.

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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

    Article  CAS  Google Scholar 

  • Allison M (2010) As Genzyme flounders, competitors and activist investors swoop in. Nat Biotechnol 28:3–4

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Banki MR, Feng L, Wood DW (2005) Simple bioseparations using self-cleaving elastin-like polypeptide tags. Nat Methods 2:659–661

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Clarke LA (2008) The mucopolysaccharidoses: a success of molecular medicine. Expert Rev Mol Med 10:e 1

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • De Muynck B, Navarre C, Boutry M (2010) Production of antibodies in plants: status after twenty years. Plant Biotechnol J 8:529–563

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Desnick RJ, Schuchman EH (2002) Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat Rev Genet 3:954–966

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Faye L, Gomord V (2010) Success stories in molecular farming – a brief overview. Plant Biotechnol J 8:525–528

    Article  Google Scholar 

  • Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM (2004) Plant-based production of biopharmaceuticals. Curr Opin Plant Biol 7:152–158

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fong BA, Wu W-Y, Wood DW (2009) Optimization of ELP-intein mediated protein purification by salt substitution. Protein Expr Purif 66:198–202

    Article  CAS  Google Scholar 

  • Fox JL (2006) Turning plants into protein factories. Nat Biotechnol 24:1191–1193

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gallie DR (2002) The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res 30:3401–3411

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Giddings G, Allison G, Brooks D, Carter A (2000) Transgenic plants as factories for biopharmaceuticals. Nat Biotechnol 18:1151–1155

    Article  CAS  Google Scholar 

  • Gomord V, Faye L (2004) Post-translational modification of therapeutic proteins in plants. Curr Opin Plant Biol 7:171–181

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22:346–353

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jiang L, Sun SS (2002) Membrane anchors for vacuolar targeting: application in plant bioreactors. Trends Biotechnol 20:99–102

    Article  CAS  Google Scholar 

  • Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–770

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993–1001

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Karg SR, Kallio PT (2009) The production of biopharmaceuticals in plant systems. Biotechnol Adv 27:879–894

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kawaguchi R, Bailey-Serres J (2002) Regulation of translation initiation in plants. Curr Opin Plant Biol 5:460–465

    Article  CAS  Google Scholar 

  • Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 33:955–965

    Article  CAS  Google Scholar 

  • Kermode AR (1996) Mechanisms of intracellular protein transport and targeting. Crit Rev Plant Sci 15:285–423

    Article  CAS  Google Scholar 

  • Kermode AR (2006) Plants as factories for production of biopharmaceutical and bioindustrial proteins: lessons from cell biology. Can J Bot 84:679–694

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kozak M (1991) A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr 1:111–115

    CAS  Google Scholar 

  • Lau OS, Sun SSM (2009) Plant seeds as bioreactors for recombinant protein production. Biotechnol Adv 27:1015–1022

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ma JK-C, Drake PMW, Christou P (2003) The production of recombinant pharmaceutical proteins in plants. Nat Rev Genet 4:794–805

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schmidt MA, Herman EM (2008) Proteome rebalancing in soybean seeds can be exploited to enhance foreign protein accumulation. Plant Biotechnol J 6:832–842

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • van Rooijen GJ, Moloney MM (1995) Plant seed oil-bodies as carriers for foreign proteins. Biotechnology (NY) 13:72–77

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vitale A, Boston RS (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9:1581–1588

    Article  CAS  Google Scholar 

  • Vitale A, Hinz G (2005) Sorting of proteins to storage vacuoles: how many mechanisms? Trends Plant Sci 10:316–323

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Walsh G, Jefferis R (2006) Post-translational modifications in the context of therapeutic proteins. Nat Biotechnol 24:1241–1252

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Werber Y (2004) Lysosomal storage diseases market. Nat Rev 3:9–10

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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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.

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  1. Department of Biological Sciences, Simon Fraser University, 8888 University Dr., Burnaby, BC, V5A 1S6, Canada

    Allison R. Kermode

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  1. Agriculture and Agri-Food Canada, Sandford Street 1391, London, N5V 4T3, Ontario, Canada

    Aiming Wang

  2. , Immunology and Transplantation, Lawson Health Research Institute/Plantig, South Street 375, London, N6A4G5, Ontario, Canada

    Shengwu Ma

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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

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