Publications arising from the Pharma-Planta project

The Pharma-Planta project has yielded an extraordinary number of publications in peer-reviewed journals, as shown in the alphabetiical list below. Further publications will be forthcoming after the completion of the pivotal phase I clinical trial.

Abranches R, Marcel S, Arcalis E, Altmann F, Fevereiro P, Stoger E (2005) Plants as bioreactors: a comparative study suggests that Medicago truncatula is a promising production system. J Biotechnol 120:121-134

Alamillo JM, Monger W, Sola I, Garcia B, Perrin Y, Bestagno M, Burrone OR, Sabella P, Plana-Duran J, Enjuanes L, Lomonossoff GP, Garcia JA (2006). Use of virus vectors for the expression in plants of active full-length and single chain anti-coronavirus antibodies. Biotechnol J 1:1103-1111

Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, Christou P, Daniell H, Datta K, Datta S, Dix PJ, Fauquet C, Huang N, Kohli A, Mooibroek H, Nicholson L, Nguyen TT, Nugent G, Raemakers K, Romano A, Somers DA, Stoger E, Taylor N, Visser R (2005) Particle bombardment and the genetic enhancement of crops: myths and realities. Mol Breeding 15:305-327

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-ER compartments of wheat endosperm. Plant Physiol 136:3457-3466

Avesani L (2006) I farmaci dalle piante, il futuro è già arrivato. L’informatore Agrario 31:73-74

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 6:560-675

Bellucci M, De Marchis F, Mannucci R, Bock R, Arcioni S (2005). Cytoplasm and chloroplast are not suitable sub-cellular localizations for β-zein accumulation in transgenic plants. J Exp Bot 56:1205-1212.

Bock R (2007) Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr Opin Biotechnol 18:100-106

Bock R, Khan MS (2004) Taming plastids for a green future. Trends Biotechnol 22:311-318

Bortesi L, Rossato M, Schuster F, Raven N, Stadlmann J, Avesani L, Falorni A, Bazzoni F, Bock R, Schillberg S, Pezzotti M (2009) Viral and murine interleukin-10 are correctly processed and retain their biological activity when produced in tobacco. BMC Biotechnol 9:22

Butaye KM, Goderis IJ, Wouters PF, Pues JM, Delaure SL, Broekaert WF, Depicker A, Cammue BP, De Bolle MF (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39:440-449

Cañizares MC, Lomonossoff GP, Nicholson L (2005) Development of cowpea mosaic virus-based vectors for the production of vaccines in plants. Expert Rev Vaccines 4:687-967

Cañizares MC, Nicholson L, Lomonossoff GP (2005) Use of viral vectors for vaccine production in plants. Immunol Cell Biol 83:263-270

Cañizares MC, Liu L, Perrin Y, Tsakiris E, Lomonossoff GP (2006) A bipartite system for the constitutive and inducible expression of high levels of foreign proteins in plants. Plant Biotechnol J 4:183-193

Capuano F, Beaudoin F, Napier JA, Shewry PR (2007) Properties and exploitation of oleosins. Biotechnol Adv 25:203-206

Chakauya E, Chikwamba R, Rybicki EP (2006) Riding the tide of biopharming in Africa: considerations for risk assessment. S Afr J Sci 102:284

DaSilva LL, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J (2005) Receptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17:132-148

De Buck S, Windels P, De Loose M, Depicker A (2004) Single copy T-DNAs integrated at different positions in the Arabidopsis genome display uniform and comparible β-glucuronidase accumulation levels. Cell Mol Life Sci 61:2632-2645

De Muynck B, Navarre C, Nizet Y, Stadlmann J, 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

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

Delannoy M, Alves G, Vertommen D, Ma JKC, Boutry M, Navarre C (2008) Identification of peptidases in the Nicotiana tabacum leaf intercellular fluid. Proteomics 8:2285-2298

Drake PM, Barbi T, Sexton A, McGowan E, Stadlmann J, Navarre C, Paul MJ, Ma JK (2009) Development of rhizosecretion as a production system for recombinant proteins from hydroponic cultivated tobacco. FASEB J 10:3581-3589.

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

Floss D, Sack M, Rademacher T, Fischer R, Conrad U (2008) Biochemical and functional characterization of anti-HIV antibody ELP fusion proteins from transgenic plants. Plant Biotechnol J 6:379-391

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, Mockey M, Zanello G, Brosson D, Diogon M, Frutos R, Bruel T, Rodrigues V, Garzon E, Chevaleyre C, Berri M, Salmon H, Conrad U, Dedieu L (2010) Expression and immunogenicity of the mycobacterial Ag85B/ESAT-6 antigens produced in transgenic plants by the elastin-like peptide (ELP) fusion strategy. J Biomed Biotechnol 2010:274346

Foresti O, De Marchis F, de Virgilio M, Klein EM, Arcioni S, Bellucci M, Vitale A (2008) Protein domains involved in assembly in the endoplasmic reticulum promote vacuolar delivery when fused to secretory GFP, indicating a protein quality control pathway for degradation in the plant vacuole. Mol Plant 1:1067-1076

Foresti O, Dasilva LL, Denecke J (2006). Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18:2275-2293

Frutos R, Denise H, Vivares C, Neuhaus JM, Vitale S, Pedrazzini E, Ma J, Dix P, Gray J, Pezzotti M, Conrad U, Robinson D (2008) Pharmaceutical proteins in plants. A strategic genetic engineering approach for the production of tuberculosis antigens. Ann NY Acad Sci 1149:275-280

Garcia-Perez RD, van Houdt H, Depicker A (2004) Spreading of post-transcriptional gene silencing along the target gene promotes systemic silencing. Plant J 38:594-602

Gattolin S, Sorieul M, Hunter PR, Khonsari RH, Frigerio L (2009). Expression mapping of the tonoplast intrinsic protein family in Arabidopsis root tissues. BMC Plant Biol 9:133

Gonzalez-Rabade N, McGowan EG, Zhou F, McCabe MS, Bock R, Dix PJ, Gray JC, Ma JKC (2011) Immunogenicity of chloroplast-derived HIV-1 p24 and a p24-Nef fusion protein following subcutaneous and oral administration in mice. Plant Biotechnol J 9:629-638

Hellwig S, Drossard J, Twyman RM, Fischer R (2004) Plant cell cultures for the production of recombinant proteins. Nature Biotechnol 22:1415-1422

Jin C, Altmann F, Strasser R, Mach L, Schähs M, Kunert R, Rademacher T, Glössl J, Steinkellner H (2008) A plant derived human monoclonal antibody induces an anti-carbohydrate immune response in rabbits. Glycobiology 18:235-241

Jin C, Hantusch G, Hemmer W, Stadlmann J, Altmann F (2008) Affinity of IgE and IgG against cross-reactive carbohydrate determinants on plant and insect glycoproteins. J Allergy Clin Immunol 121:185-190

Klein EM, Mascheroni L, Pompa A, Ragni L, Weimar T, Lilley KS, Dupree P, Vitale A (2006) Plant endoplasmin supports the protein secretory pathway and has a role in proliferating tissues. Plant J  48:657-673

Langhans M, Marcote MJ, Pimpl P, Virgili-Lopez G, Robinson DG, Aniento F (2008) In vivo trafficking and localization of p24 proteins in plant cells. Traffic 9:770-785

Liu L, Cañizares MC, Monger W, Perrin Y, Tsakiris E, Porta C, Shariat N, Nicholson L, Lomonossoff G P (2005) Cowpea mosaic virus-based systems for the production of antigens and antibodies in plants. Vaccine 23:1788-1792

Liu L, Lomonossoff GP (2006) A site-directed mutagenesis method utilising large double-stranded DNA templates for the simultaneous introduction of multiple changes and sequential multiple rounds of mutation: Application to the study of whole viral genomes. J Virol Methods 137:63-71

Lombardi R, Circelli P, Villani ME, Buriani G, Nardi L, Coppola V, Bianco L, Benvenuto E, Donini M, Marusic C (2009) High-level HIV-1 Nef transient expression in Nicotiana benthamiana using the P19 gene silencing suppressor protein of Artichoke mottled crinkle virus. BMC Biotechnol 9:96

Ma JK, 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

Ma JK, Chikwamba R, Sparrow P, Fischer R, Mahoney R, Twyman RM (2005) Plant-derived pharmaceuticals - the road forward. Trends Plant Sci 10:580-585

Maggio C, Barbante A, Ferro F, Frigerio L, Pedrazzini E (2007) Intracellular sorting of the tail-anchored protein cytochrome b5 in plants: a comparative study using different isoforms from rabbit and Arabidopsis. J Exp Bot 58:1365-1379

Marusic C, Vitale A, Pedrazzini E, Donini M, Frigerio L, Bock R, Dix PJ, McCabe MS, Bellucci M, Benvenuto E (2009) Plant-based strategies aimed at expressing HIV antigens and neutralizing antibodies at high levels. Nef as a case study. Transgenic Res 18:499-512

Marusic C, Nuttall J, Buriani G, Lico C, Lombardi R, Baschieri S, Benvenuto E, Frigerio L (2007) Expression, intracellular targeting and purification of HIV Nef variants in tobacco cells. BMC Biotechnol 7:12

McCabe MS, Klaas M, Gonzalez-Rabade N, Poage M, Badillo-Corona J, Zhou F, Karcher D, Bock R, Gray JC, Dix PJ (2008) Plastid transformation of high biomass tobacco variety Maryland Mammoth for production of HIV-1 p24 antigen. Plant Biotechnol J 6: 914-929

Navarre C, Delannoy M, Lefebvre B, Nader J, Vanham D, Boutry M (2006) Expression and secretion of recombinant outer-surface protein A from the Lyme disease agent, Borrelia burgdorferi, in Nicotiana tabacum suspension cells. Transgenic Res 15:325-335

Nicholson L, Gonzalez-Melendi P, van Dolleweerd C, Tuck H, Ma J KC, Fischer R, Christou P, Stoger E (2005) A recombinant multimeric immunoglobulin expressed in rice shows assembly-dependent subcellular localization in endosperm cells. Plant Biotechnol J 3:115-127

Nuttall J, Ma JKC, Frigerio L (2005) A functional antibody lacking N-linked glycans is efficiently folded, assembled and secreted by tobacco mesophyll protoplasts. Plant Biotechnol J 3:497-504

Obregon P, Chargelegue D, Drake PMW, Prada A, Nuttall J, Frigerio L, Ma JKC (2006) HIV-1 p24-immunoglobulin fusion molecule: A new strategy for plant-based protein production. Plant Biotechnol J 4:195-207

Pabst M, Bondili JS, Stadlmann J, Mach L, Altmann F (2007) Mass + retention time = structure: A strategy for the analysis of N-glycans by carbon LC-ESI-MS and its application to fibrin N-glycans. Anal Chem 79:5051-5057

Pedrazzini E (2009) Tail-anchored proteins in plants. J Plant Biol 52:88-101

Platis D, Maltezos A, Ma JK, Labrou NE (2009) Combinatorial de novo design and application of a biomimetic affinity ligand for the purification of human anti-HIV mAb 4E10 from transgenic tobacco. J Mol Recognition 22:415-424

Platis D, Labrou NE (2008) Affinity chromatography for the purification of therapeutic proteins from transgenic maize using immobilized histamine. J Sep Sci 31:636-645

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

Ramessar K, Peremarti A, Gomez Galera S, Naqvi S, Moralejo M, Muñoz M, Capell T, Christou P (2007) Biosafety and risk assessment framework for selectable marker genes in transgenic crop plants. A case of the science not supporting the politics. Transgenic Res 16:261-280

Ramessar K, Rademacher T, Sack M, Stadlmann J, Platis D, Stiegler G, Labrou N, Altmann F, Ma JKC, 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

Ramessar K, Sabalza M, Capell T, Christou P. Maize plants: an ideal production platform for effective and safe molecular pharming. Plant Sci 174:409-419

Sack M, Paetz A, Kunert R, Bomble M, Hesse F, Stiegler G, Fischer R, Katinger H, Stoeger E, Rademacher T (2007) Analysis of the broadly neutralizing human anti-HIV-1 antibody 2F5 produced in transgenic tobacco BY2 suspension cells. FASEB J 21:1655-1664

Sainsbury F, Lavoie P-O, D’Aoust M-A, Vezina L-P, Lomonossoff GP (2008) Expression of multiple proteins using full-length and deleted versions of Cowpea mosaic virus RNA-2. Plant Biotechnol J 6:82-92.

Sanders M, Lannoo N, Maddelein W, Depicker A, Van Montagu M, Cornelissen M, Jacobs J (2004) The preferred route for the degradation of silencing target RNAs in transgenic plants depends on pre-established silencing conditions. Nucleic Acids Res 32:3400-3409

Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H (2007) Production of monoclonal antibodies in plants with a humanized glycosylation pattern. Plant Biotechnol J 5:657-663

Schiermeyer A, Hartenstein H, Mandal MK, Otte B, Wahner V, Schillberg S (2009) A membrane-bound matrix-metalloproteinase from Nicotiana tabacum cv. BY-2 is induced by bacterial pathogens. BMC Plant Biol 9:83

Schiermeyer A, Schinkel H, Apel S, Fischer R, Schillberg S (2005). Production of Desmodus rotundus plasminogen activator α1 (DSPAα1) in tobacco is hampered by proteolysis. Biotechnol Bioeng 89:848-858

Schillberg S, Twyman RM, Fischer R (2005) Opportunities for recombinant antigen and antibody expression in transgenic plants - technology assessment. Vaccine 23:1764-1769

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

Snowden, CJ, Leborgne-Castel N, Wootton LJ, Hadlington JL, Denecke J (2007) In vivo analysis of the lumenal binding protein (BiP) reveals multiple functions of its ATPase domain. Plant J 52:987-1000

Sorrentino A, Schillberg S, Fischer R, Rao R, Porta R, Mariniello L (2005) Recombinant human tissue transglutaminase produced into tobacco suspension cell cultures is active and recognizes autoantibodies in the serum of coeliac patients. Int J Biochem Cell Biol 37:842-852

Sparkes IA, Frigerio L, Tolley N, Hawes C (2009) The plant endoplasmic reticulum: a cell-wide web. Biochem J 423:145-155

Sparrow PAC, Irwin JA, Dale PJ, Twyman RM, Ma JKC (2007) Pharma-Planta: road testing the developing regulatory guidelines for plant-made pharmaceuticals. Transgenic Res 16:147-161

Sparrow PAC, Twyman RM (2008) Biosafety and risk assessment of plant made pharmaceuticals. Methods Mol Biol 483:341-353

Spök A, Twyman RM, Fischer R, Ma JKC, Sparrow PAC (2008) Evolution of a regulatory framework for plant-made pharmaceuticals. Trends Biotechnol 26:506-517

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-α(1,3)-fucose residues. Plant Biotechnol J 2:279-287

Stadlmann J, Pabst M, Kolarich D, Kunert R, Altmann F (2008) Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8:2858–2871

Stadlmann J, Weber A, Pabst M, Anderle H, Kunert R, Ehrlich HJ, Peter Schwarz H, Altmann F (2009) A close look at human IgG sialylation and subclass distribution after lectin fractionation. Proteomics 9:4143-4153

Stoger E, Ma JKC, Fischer R, Christou P (2005) Sowing the seeds of success: pharmaceutical proteins from plants. Curr Opin Biotechnol 16:167-173

Stoger E, Sack M, Nicholson L, Fischer R, Christou P (2005) Recent progress in plantibody technology. J Curr Pharmaceutical Design 11:2439-2457

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 β-N-acetylhexosaminidases. Plant Physiol 145:5-16

Strasser R, Bondili JS, Vavra U, Schoberer J, Svoboda B, Glössl J, Léonard R,  Stadlmann J,  Altmann F, Steinkellner H, Mach L (2007) A unique β1,3-galactosyltransferase is indispensable for the biosynthesis of complex N-glycans in plants. Plant Cell 19:2278-2292

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

Twyman RM, Schillberg S, Fischer R (2005) The transgenic plant market in the pharmaceutical industry. Expert Opin Emerging Drugs 10:185-218

Van Droogenbroeck B, Cao J, Stadlmann J, Altmann F, Colanesi S, Hillmer S, Robinson DG, van Lerberge E, Terryn N, van Monatgu 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

Van Droogenbroeck B, De Wilde K, Depicker A (2008) Production of antibody fragments in Arabidopsis seeds. Methods Mol Biol 483:89-101

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

Vitale A, Pedrazzini E (2005) Recombinant pharmaceuticals from plants: the plant endomembrane system as bioreactor. Mol Interv 5:216-225

Yusibov V, Rabindran S, Commandeur U, Twyman RM, Fischer R (2006) The potential of plant virus vectors for vaccine production. Drugs in R&D 7:203-217