Molecular farming – The slope of enlightenment

Aviezer, 2009, Novel enzyme replacement therapy for Gaucher disease: ongoing Phase III clinical trial with recombinant human glucocerebrosidase expressed in plant cells, Mol. Genet. Metab., 96, S13, 10.1016/j.ymgme.2008.11.009 Aviezer, 2009, A plant-derived recombinant human glucocerebrosidase enzyme – a preclinical and phase I investigation, PLoS One, 4, 10.1371/journal.pone.0004792 Bendandi, 2010, Rapid, high-yield production in plants of individualized idiotype vaccines for non-Hodgkin’s lymphoma, Ann. Oncol., 21, 2420, 10.1093/annonc/mdq256 Bertini, 2018, Design of a type-1 diabetes vaccine candidate using edible plants expressing a major autoantigen, Front. Plant Sci., 9, 572, 10.3389/fpls.2018.00572 Bock, 2015, Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology, Annu. Rev. Plant Biol., 66, 211, 10.1146/annurev-arplant-050213-040212 Boes, 2015, Analysis of a multi-component multi-stage malaria vaccine candidate – tackling the cocktail challenge, PLoS One, 10, 10.1371/journal.pone.0131456 Borisjuk, 1999, Production of recombinant proteins in plant root exudates, Nat. Biotechnol., 17, 466, 10.1038/8643 Bratbak, 1984, Bacterial dry matter content and biomass estimations, Appl. Environ. Microbiol., 48, 755, 10.1128/AEM.48.4.755-757.1984 Buntru, 2014, Tobacco BY-2 cell-free lysate: an alternative and highly-productive plant-based in vitro translation system, BMC Biotechnol., 14, 10.1186/1472-6750-14-37 Buyel, 2015, Process development strategies in plant molecular farming, Curr. Pharm. Biotechnol., 16, 966, 10.2174/138920101611150902115413 Buyel, 2019, Plant molecular farming – integration and exploitation of side streams to achieve sustainable biomanufacturing, Front. Plant Sci., 9, 1893, 10.3389/fpls.2018.01893 Buyel, 2012, Predictive models for transient protein expression in tobacco (Nicotiana tabacum L.) can optimize process time, yield, and downstream costs, Biotechnol. Bioeng., 109, 2575, 10.1002/bit.24523 Buyel, 2013, The use of quantitative structure–activity relationship models to develop optimized processes for the removal of tobacco host cell proteins during biopharmaceutical production, J. Chromatogr. A, 1322, 18, 10.1016/j.chroma.2013.10.076 Buyel, 2015, Extraction and downstream processing of plant-derived recombinant proteins, Biotechnol. Adv., 33, 902, 10.1016/j.biotechadv.2015.04.010 Buyel, 2017, Very-large-scale production of antibodies in plants: the biologization of manufacturing, Biotechnol. Adv., 35, 458, 10.1016/j.biotechadv.2017.03.011 Castilho, 2010, In planta protein sialylation through overexpression of the respective mammalian pathway, J. Biol. Chem., 285, 15923, 10.1074/jbc.M109.088401 Cox, 2006, Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor, Nat. Biotechnol., 24, 1591, 10.1038/nbt1260 Decker, 2012, Glycoprotein production in moss bioreactors, Plant Cell Rep., 31, 453, 10.1007/s00299-011-1152-5 EMEA, 2009, Committee for Proprietary Medicinal Products (CPMP) Everett, 2012, Development of a plant-made pharmaceutical production platform, Bioprocess Int., 10, 16 FDA/USDA, 2002, Draft guidance Fischer, 2000, Molecular farming of pharmaceutical proteins, Transgenic Res., 9, 279, 10.1023/A:1008975123362 Fischer, 2012, GMP issues for plant-derived recombinant proteins, Biotechnol. Adv., 30, 434, 10.1016/j.biotechadv.2011.08.007 Fischer, 2014, Molecular farming in plants: the long road to the market, Biotechnol. Agr. Forest., 68, 27, 10.1007/978-3-662-43836-7_3 Fischer, 2018, Glyco-engineering of plant-based expression systems, Adv. Biochem. Eng. Biotechnol. Francisco, 2014, First-quarter biotech job picture, Nat. Biotechnol., 32, 497, 10.1038/nbt.2901 Gomord, 2010, Plant-specific glycosylation patterns in the context of therapeutic protein production, Plant Biotechnol. J., 8, 564, 10.1111/j.1467-7652.2009.00497.x Goojani, 2013, Expression and large-scale production of human tissue plasminogen activator (t-PA) in transgenic tobacco plants using different signal peptides, Appl. Biochem. Biotechnol., 169, 1940, 10.1007/s12010-013-0115-4 Hanania, 2017, Establishment of a tobacco BY-2 cell line devoid of plant specific xylose and fucose as a platform for the production of biotherapeutic proteins, Plant Biotechnol. J., 15, 1120, 10.1111/pbi.12702 Hargreaves, 2018, Bayer to shed €600m factor VIII facility and 12,000 staff, BioPharma Report. Hiatt, 1989, Production of antibodies in transgenic plants, Nature, 342, 76, 10.1038/342076a0 Hiatt, 2015, The emergence of antibody therapies for Ebola, Hum. Antibod., 23, 49, 10.3233/HAB-150284 Hoelscher, 2018, High-level expression of the HIV entry inhibitor griffithsin from the plastid genome and retention of biological activity in dried tobacco leaves, Plant Mol. Biol., 97, 357, 10.1007/s11103-018-0744-7 Hofbauer, 2013, Subcellular accumulation and modification of pharmaceutical proteins in different plant tissues, Curr. Pharm. Des., 19, 5495, 10.2174/1381612811319310005 Holland, 2018, Bioreactor-based production of glycoproteins in plant cell suspension cultures, Methods Mol. Biol., 1674, 129, 10.1007/978-1-4939-7312-5_11 Holtz, 2015, Commercial-scale biotherapeutics manufacturing facility for plant-made pharmaceuticals, Plant Biotechnol. J., 13, 1180, 10.1111/pbi.12469 Hood, 2002, From green plants to industrial enzymes, Enzym. Microb. Technol., 30, 279, 10.1016/S0141-0229(01)00502-6 Hood, 1997, Commercial production of avidin from transgenic maize: characterization of transformant, production, processing, extraction and purification, Mol. Breed., 3, 291, 10.1023/A:1009676322162 Hundleby, 2018, Biosafety, risk assessment and regulation of molecular farming, 329 International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use (ICH), 2012, Q11. Development and manufacture of drug substances (chemical entities and biotechnological/biological entities), Fed. Regist., 77, 69634 Jansing, 2019, CRISPR/Cas9-mediated knockout of six glycosyltransferase genes in Nicotiana benthamiana for the production of recombinant proteins lacking β-1,2-xylose and core α-1,3-fucose, Plant Biotechnol. J., 17, 350, 10.1111/pbi.12981 Kastilan, 2017, Improvement of a fermentation process for the production of two PfAMA1-DiCo-based malaria vaccine candidates in Pichia pastoris, Sci. Rep., 7, 10.1038/s41598-017-11819-4 Kelley, 2009, Industrialization of mAb production technology: the bioprocessing industry at a crossroads, mAbs, 1, 443, 10.4161/mabs.1.5.9448 Knödler, 2019, Stability of recombinant proteins in plants is affected by seasonal changes, Front. Plant Sci., 10, 1245, 10.3389/fpls.2019.01245 Kusnadi, 1998, Processing of transgenic corn seed and its effect on the recovery of recombinant β-glucuronidase, Biotechnol. Bioeng., 60, 44, 10.1002/(SICI)1097-0290(19981005)60:1<44::AID-BIT5>3.0.CO;2-0 Kwon, 2018, Expression and assembly of largest foreign protein in chloroplasts: oral delivery of human FVIII made in lettuce chloroplasts robustly suppresses inhibitor formation in haemophilia A mice, Plant Biotechnol. J., 16, 1148, 10.1111/pbi.12859 Lamphear, 2002, Delivery of subunit vaccines in maize seed, J. Control. Release, 85, 169, 10.1016/S0168-3659(02)00282-1 Li, 2016, Multiplexed, targeted gene editing in Nicotiana benthamiana for glycoengineering and monoclonal antibody production, Plant Biotechnol. J., 14, 533, 10.1111/pbi.12403 Ma, 2003, The production of recombinant pharmaceutical proteins in plants, Nat. Rev. Genet., 4, 794, 10.1038/nrg1177 Ma, 2005, Molecular farming for new drugs and vaccines. Current perspectives on the production of pharmaceuticals in transgenic plants, EMBO Rep., 6, 593, 10.1038/sj.embor.7400470 Ma, 2015, Regulatory approval and a first-in-human phase I clinical trial of a monoclonal antibody produced in transgenic tobacco plants, Plant Biotechnol. J., 13, 1106, 10.1111/pbi.12416 Menkhaus, 2004, Considerations for the recovery of recombinant proteins from plants, Biotechnol. Prog., 20, 1001, 10.1021/bp040011m Mercx, 2017, Inactivation of the β(1,2)-xylosyltransferase and the α(1,3)-fucosyltransferase genes in Nicotiana tabacum BY-2 cells by a multiplex CRISPR/Cas9 strategy results in glycoproteins without plant-specific glycans, Front. Plant Sci., 8, 403, 10.3389/fpls.2017.00403 Merlin, 2017, Edible plants for oral delivery of biopharmaceuticals, Brit. J. Clin. Pharmacol., 83, 71, 10.1111/bcp.12949 Mir-Artigues, 2019, A simplified techno-economic model for the molecular pharming of antibodies, Biotechnol. Bioeng., 116, 2526, 10.1002/bit.27093 Mor, 2015, Molecular pharming’s foot in the FDA’s door: Protalix’s trailblazing story, Biotechnol. Lett., 37, 2147, 10.1007/s10529-015-1908-z Na, 2015, Ebola outbreak in Western Africa 2014: what is going on with Ebola virus?, Clin. Exp. Vaccine Res., 4, 17, 10.7774/cevr.2015.4.1.17 Nandi, 2005, Process development and economic evaluation of recombinant human lactoferrin expressed in rice grain, Transgenic Res., 14, 237, 10.1007/s11248-004-8120-6 Nandi, 2016, Techno-economic analysis of a transient plant-based platform for monoclonal antibody production, MAbs, 8, 1456, 10.1080/19420862.2016.1227901 Nikolov, 2004, Downstream processing of recombinant proteins from transgenic feedstock, Curr. Opin. Biotechnol., 15, 479, 10.1016/j.copbio.2004.08.006 Oey, 2009, Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic, Plant J., 57, 436, 10.1111/j.1365-313X.2008.03702.x Paul, 2015, Commercialization of new biotechnology: a systematic review of 16 commercial case studies in a novel manufacturing sector, Plant Biotechnol. J., 13, 1209, 10.1111/pbi.12426 Pillet, 2019, Immunogenicity and safety of a quadrivalent plant-derived virus like particle influenza vaccine candidate – two randomized Phase II clinical trials in 18 to 49 and ≥50 years old adults, PLoS One, 14, 10.1371/journal.pone.0216533 PREVAIL II Writing Group, Multi-National PREVAIL II Study Team, 2016, A randomized, controlled trial of ZMapp for Ebola virus infection, New Eng. J. Med., 375, 1448, 10.1056/NEJMoa1604330 Qiu, 2014, Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp, Nature, 514, 47, 10.1038/nature13777 Rademacher, 2008, Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans, Plant Biotechnol. J., 6, 189, 10.1111/j.1467-7652.2007.00306.x Rademacher, 2019, Plant cell packs: a scalable platform for recombinant protein production and metabolic engineering, Plant Biotechnol. J., 17, 1560, 10.1111/pbi.13081 Ramessar, 2008, Cost-effective production of a vaginal protein microbicide to prevent HIV transmission, Proc. Natl. Acad. Sci. U. S. A., 105, 3727, 10.1073/pnas.0708841104 Ramessar, 2010, Can microbicides turn the tide against HIV?, Curr. Pharm. Des., 16, 468, 10.2174/138161210790232202 Rosales-Mendoza, 2012, Chlamydomonas reinhardtii as a viable platform for the production of recombinant proteins: current status and perspectives, Plant Cell Rep., 31, 479, 10.1007/s00299-011-1186-8 Rybicki, 2019, Plant molecular farming of virus-like nanoparticles as vaccines and reagents, WIRES Nanomed. Nanobiotechnol. Sack, 2015, From gene to harvest: insights into upstream process development for the GMP production of a monoclonal antibody in transgenic tobacco plants, Plant Biotechnol. J., 13, 1094, 10.1111/pbi.12438 Sainsbury, 2008, Extremely high-level and rapid protein production in plants without the use of viral replication, Plant Physiol., 148, 1212, 10.1104/pp.108.126284 Sainsbury, 2010, Rapid transient production in plants by replicating and non-replicating vectors yields high quality functional anti-HIV antibody, PLoS One, 5, 10.1371/journal.pone.0013976 Santos, 2016, Putting the spotlight back on plant suspension cultures, Front. Plant Sci., 7, 297, 10.3389/fpls.2016.00297 Schillberg, 2013, Molecular farming of pharmaceutical proteins using plant suspension cell and tissue cultures, Curr. Pharm. Des., 19, 5531, 10.2174/1381612811319310008 Schillberg, 2017, Contained molecular farming using plant cell and tissue cultures, 261 Schillberg, 2019, Critical analysis of the commercial potential of plants for the production of recombinant proteins, Front. Plant Sci., 10, 720, 10.3389/fpls.2019.00720 Schmidt, 2019, Field-grown tobacco plants maintain robust growth while accumulating large quantities of a bacterial cellulase in chloroplasts, Nature Plants, 5, 715, 10.1038/s41477-019-0467-z Shaaltiel, 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, 10.1111/j.1467-7652.2007.00263.x Shiloach, 2005, Growing E. coli to high cell density – a historical perspective on method development, Biotechnol. Adv., 23, 345, 10.1016/j.biotechadv.2005.04.004 Shoji, 2008, Plant-expressed HA as a seasonal influenza vaccine candidate, Vaccine, 26, 2930, 10.1016/j.vaccine.2008.03.045 Shoji, 2011, Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza, Human Vaccines, 7, 41, 10.4161/hv.7.0.14561 Sijmons, 1990, Production of correctly processed human serum albumin in transgenic plants, Biotechnology (NY), 8, 217 Spiegel, 2018, Current status and perspectives of the molecular farming landscape, 3 Spök, 2008, Evolution of a regulatory framework for plant-made pharmaceuticals, Trends Biotechnol., 26, 506, 10.1016/j.tibtech.2008.05.007 Stoger, 2002, Practical considerations for pharmaceutical antibody production in different crop systems, Mol. Breed., 9, 149, 10.1023/A:1019714614827 Stoger, 2005, Sowing the seeds of success: pharmaceutical proteins from plants, Curr. Opin. Biotechnol., 16, 167, 10.1016/j.copbio.2005.01.005 Stoger, 2014, Plant molecular pharming for the treatment of chronic and infectious diseases, Annu. Rev. Plant Biol., 65, 743, 10.1146/annurev-arplant-050213-035850 Strasser, 2009, Improved virus neutralization by plant-produced anti-HIV antibodies with a homogeneous β1,4-galactosylated N-glycan profile, J. Biol. Chem., 284, 20479, 10.1074/jbc.M109.014126 Svab, 2007, Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment, Proc. Natl. Acad. Sci. U. S. A., 104, 7003, 10.1073/pnas.0700063104 Tekoah, 2013, Glycosylation and functionality of recombinant β-glucocerebrosidase from various production systems, Biosci. Rep., 33, 10.1042/BSR20130081 Tekoah, 2015, Large-scale production of pharmaceutical proteins in plant cell culture – the Protalix experience, Plant Biotechnol. J., 13, 1199, 10.1111/pbi.12428 Tremblay, 2010, Tobacco, a highly efficient green bioreactor for production of therapeutic proteins, Biotechnol. Adv., 28, 214, 10.1016/j.biotechadv.2009.11.008 Tschofen, 2016, Plant molecular farming – much more than medicines, Ann. Rev. Analyt. Chem., 9, 271, 10.1146/annurev-anchem-071015-041706 Tusé, 2014, Manufacturing economics of plant-made biologics: case studies in therapeutic and industrial enzymes, Biomed. Res. Int., 2014, 10.1155/2014/256135 Twyman, 2003, Molecular farming in plants: host systems and expression technology, Trends Biotechnol., 21, 570, 10.1016/j.tibtech.2003.10.002 Twyman, 2005, Transgenic plants in the biopharmaceutical market, Expert Opin. Emerg. Drugs, 10, 185, 10.1517/14728214.10.1.185 Twyman, 2013, Optimizing the yield of recombinant pharmaceutical proteins in plants, Curr. Pharm. Des., 19, 5486, 10.2174/1381612811319310004 Vamvaka, 2016, Rice endosperm is cost-effective for the production of recombinant griffithsin with potent activity against HIV, Plant Biotechnol. J., 14, 1427, 10.1111/pbi.12507 Vamvaka, 2016, Cyanovirin-N produced in rice endosperm offers effective pre-exposure prophylaxis against HIV-1BaL infection in vitro, Plant Cell Rep., 35, 1309, 10.1007/s00299-016-1963-5 Vamvaka, 2016, Rice endosperm produces an underglycosylated and potent form of the HIV-neutralizing monoclonal antibody 2G12, Plant Biotechnol. J., 14, 97, 10.1111/pbi.12360 Vamvaka, 2018, Unexpected synergistic HIV neutralization by a triple microbicide produced in rice endosperm, Proc. Natl. Acad. Sci. U. S. A., 115, E7854, 10.1073/pnas.1806022115 Vaquero, 1999, Transient expression of a tumor-specific single-chain fragment and a chimeric antibody in tobacco leaves, Proc. Natl. Acad. Sci. U. S. A., 96, 11128, 10.1073/pnas.96.20.11128 Waheed, 2015, Plastids: the green frontiers for vaccine production, Front. Plant Sci., 6, 1005, 10.3389/fpls.2015.01005 Whaley, 2011, Emerging antibody products and Nicotiana manufacturing, Human Vaccines, 7, 349, 10.4161/hv.7.3.14266 Wilken, 2012, Recovery and purification of plant-made recombinant proteins, Biotechnol. Adv., 30, 419, 10.1016/j.biotechadv.2011.07.020 Witcher, 1998, Commercial production of β-glucuronidase (GUS): a model system for the production of proteins in plants, Mol. Breed., 4, 301, 10.1023/A:1009622429758 Yusibov, 2011, Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond, Hum. Vaccines, 7, 313, 10.4161/hv.7.3.14207 Zimmermann, 2009, Antibody expressing pea seeds as fodder for prevention of gastrointestinal parasitic infections in chickens, BMC Biotechnol., 9, 79, 10.1186/1472-6750-9-79 Zischewski, 2016, Overcoming low yields of plant-made antibodies by a protein engineering approach, Biotechnol. J., 11, 107, 10.1002/biot.201500255