Very-large-scale production of antibodies in plants: The biologization of manufacturing

Biotechnology Advances

Volumn 35, Issue 4, 2017, Pages 458-465

  Buyel, J F ^a,b   Twyman, R M ^c   Fischer, R ^a,b  

^a RWTH AACHEN UNIVERSITY   (Germany)

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

^c TRM Ltd   (United Kingdom)

Author keywords

Biologization; Molecular farming; Monoclonal antibodies; Plant based production; Process economy; Very large scale production

Indexed keywords

CELL CULTURE; MANUFACTURE; MONOCLONAL ANTIBODIES; SURFACE PLASMON RESONANCE;

BIOLOGIZATION; BIOPHARMACEUTICAL PRODUCTS; BIOPHARMACEUTICAL PROTEINS; LARGE SCALE PRODUCTIONS; MOLECULAR FARMING; MONOCLONAL ANTIBODIES (MABS); PRACTICAL REQUIREMENTS; THERAPEUTIC POTENTIALS;

ANTIBODIES;

ANTIBODY; DRUG DEVELOPMENT; ECONOMIC ACTIVITY; GENETIC ENGINEERING; MANUFACTURING; MOLECULAR ANALYSIS;

MONOCLONAL ANTIBODY;

BIOTECHNOLOGY; GENETICS; METABOLISM; MOLECULAR FARMING; TRANSGENIC PLANT;

ANTIBODIES, MONOCLONAL; BIOTECHNOLOGY; MOLECULAR FARMING; PLANTS, GENETICALLY MODIFIED;

EID: 85016615591     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2017.03.011     Document Type: Review

References (63)

1. Anderson, M.J., Whitcomb, P.J., Response Surface Methods Simplified. 2005, Productivity Press.
2. Angarita, M., Muller-Spath, T., Baur, D., Lievrouw, R., Lissens, G., Morbidelli, M., Twin-column CaptureSMB: a novel cyclic process for protein A affinity chromatography. J. Chromatogr. A 1389 (2015), 85–95.
3. Baur, D., Angarita, M., Muller-Spath, T., Morbidelli, M., Pareto-optimal design of the twin-column CaptureSMB process improves capacity utilization and productivity in protein A affinity capture. Biotechnol. J. 11 (2015), 135–145.
4. Buyel, J.F., Process development strategies in plant molecular farming. Curr. Pharm. Biotechnol. 16 (2015), 966–982.
5. Buyel, J.F., Fischer, R., Predictive models for transient protein expression in tobacco (Nicotiana tabacum L.) can optimize process time, yield, and downstream costs. Biotechnol. Bioeng. 109 (2012), 2575–2588.
6. Buyel, J.F., Fischer, R., Processing heterogeneous biomass: overcoming the hurdles in model building. Bioengineered 4 (2013), 21–24.
7. Buyel, J.F., Fischer, R., Downstream processing of biopharmaceutical proteins produced in plants: the pros and cons of flocculants. Bioengineered 5 (2014), 138–142.
8. Buyel, J.F., Fischer, R., Flocculation increases the efficacy of depth filtration during the downstream processing of recombinant pharmaceutical proteins produced in tobacco. Plant Biotechnol. J. 12 (2014), 240–252.
9. Buyel, J.F., Fischer, R., A juice extractor can simplify the downstream processing of plant-derived biopharmaceutical proteins compared to blade-based homogenizers. Process Biochem. 50 (2014), 859–866.
10. Buyel, J.F., Fischer, R., Scale-down models to optimize a filter train for the downstream purification of recombinant pharmaceutical proteins produced in tobacco leaves. Biotechnol. J. 9 (2014), 415–425.
11. Buyel, J.F., Gruchow, H.M., Boes, A., Fischer, R., Rational design of a host cell protein heat precipitation step simplifies the subsequent purification of recombinant proteins from tobacco. Biochem. Eng. J. 88 (2014), 162–170.
12. Buyel, J.F., Opdensteinen, P., Fischer, R., Cellulose-based filter aids increase the capacity of depth filters during the downstream processing of plant-derived biopharmaceutical proteins. Biotechnol. J. 10 (2014), 584–591.
13. Buyel, J.F., Gruchow, H.M., Fischer, R., Depth filters containing diatomite achieve more efficient particle retention than filters solely containing cellulose fibers. Front. Plant Sci. 6 (2015), 1–11.
14. Buyel, J.F., Twyman, R.M., Fischer, R., Extraction and downstream processing of plant-derived recombinant proteins. Biotechnol. Adv. 33 (2015), 902–913.
15. Chhatre, S., Pampel, L., Titchener-Hooker, N.J., Integrated use of ultra scale-down and financial modeling to identify optimal conditions for the precipitation and centrifugal recovery of milk proteins. Biotechnol. Prog. 27 (2011), 998–1008.
16. Chollangi, S., Jaffe, N.E., Cai, H., Accelerating purification process development of an early phase mAb with high-throughput automation part 2. BioProcess International, 12, 2014, 48–52.
17. Ecker, D.M., Jones, S.D., Levine, H.L., The therapeutic monoclonal antibody market. MAbs 7 (2015), 9–14.
18. Espuny Garcia Del Real, G., Davies, J., Bracewell, D.G., Scale-down characterization of post-centrifuge flocculation processes for high-throughput process development. Biotechnol. Bioeng. 111 (2014), 2486–2498.
19. Fischer, R., Schillberg, S., Hellwig, S., Twyman, R.M., Drossard, J., GMP issues for recombinant plant-derived pharmaceutical proteins. Biotechnol. Adv. 30 (2012), 434–439.
20. Fischer, R., Schillberg, S., Buyel, J.F., Twyman, R.M., Commercial aspects of pharmaceutical protein production in plants. Curr. Pharm. Des. 19 (2013), 5471–5477.
21. Fleming, A., On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzæ. Br. J. Exp. Pathol. 10 (1929), 226–236.
22. Goody, J., Industrial food. Towards the development of a world cuisine. Counihan, C., van Esterik, P., (eds.) Food and Culture, 1997, Routledge, London, 338–356.
23. Hassan, S., van Dolleweerd, C.J., Ioakeimidis, F., Keshavarz-Moore, E., Ma, J.K., Considerations for extraction of monoclonal antibodies targeted to different subcellular compartments in transgenic tobacco plants. Plant Biotechnol. J. 6 (2008), 733–748.
24. Hertrampf, A., Muller, H., Menezes, J.C., Herdling, T., A PAT-based qualification of pharmaceutical excipients produced by batch or continuous processing. J. Pharm. Biomed. Anal. 114 (2015), 208–215.
25. Holtz, B.R., Berquist, B.R., Bennett, L.D., Kommineni, V.J., Munigunti, R.K., White, E.L., et al. Commercial-scale biotherapeutics manufacturing facility for plant-made pharmaceuticals. Plant Biotechnol. J. 13 (2015), 1180–1190.
26. Houdelet, M., Galinski, A., Holland, T., Wenzel, K., Schillberg, S., Buyel, J.F., Animal component-free Agrobacterium tumefaciens cultivation media for better GMP-compliance increases biomass yield and pharmaceutical protein expression in Nicotiana benthamiana. Biotechnol. J., 2017 (In press).
27. Jackewitz, A., Development of a high capacity, mixed-mode resin for high conductivity mAb feedstocks. Biopharm Int. 10 (2012), 82–84.
28. Jackson, D.A., Symons, R.H., Berg, P., Biochemical method for inserting new genetic information into DNA of Simian Virus 40: circular SV40 DNA molecules containing lambda phage genes and the galactose operon of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 69 (1972), 2904–2909.
29. Kandula, S., Babu, S., Jin, M., Shukla, A.A., Design of a filter train for precipitate removal in monoclonal antibody downstream processing. Biotechnol. Appl. Biochem. 54 (2009), 149–155.
30. Keller, W.R., Evans, S.T., Ferreira, G., Robbins, D., Cramer, S.M., Use of MiniColumns for linear isotherm parameter estimation and prediction of benchtop column performance. J. Chromatogr. A 1418 (2015), 94–102.
31. Kelley, B., Very large scale monoclonal antibody purification: the case for conventional unit operations. Biotechnol. Prog. 23 (2007), 995–1008.
32. Klutz, S., Magnus, J., Lobedann, M., Schwan, P., Maiser, B., Niklas, J., et al. Developing the biofacility of the future based on continuous processing and single-use technology. J. Biotechnol. 213 (2015), 120–130.
33. Kolb, D., Kolb, K.E., Petroleum chemistry. J. Chem. Educ., 56, 1979, 465.
34. Kress-Rogers, E., Brimelow, C.J.B., Instrumentation and Sensors for the Food Industry. 2001, Woodhead, Cambridge, UK.
35. Lightfoot, E.N., Cockrem, M.C.M., Complex fitness diagrams: downstream processing of biologicals. Sep. Sci. Technol. 48 (2013), 1753–1757.
36. Lim, J.A.C., Patkar, A., McDonagh, G., Sinclair, A., Lucy, P., Modeling bioprocess cost. BioProcess International, 8, 2010, 62–70.
37. Lokhorst, H.M., Plesner, T., Laubach, J.P., Nahi, H., Gimsing, P., Hansson, M., et al. Targeting CD38 with daratumumab monotherapy in multiple myeloma. N. Engl. J. Med. 373 (2015), 1207–1219.
38. Lolas, A., Microbial Control Strategies in Bioprocessing Falling Short of Assuring Product Quality and Satisfying Regulatory Expectations. American Pharmaceutical Review. 2013, Fishers: CompareNetworks.
39. Ma, J.K., Drossard, J., Lewis, D., Altmann, F., Boyle, J., Christou, P., et al. Regulatory approval and a first-in-human phase I clinical trial of a monoclonal antibody produced in transgenic tobacco plants. Plant Biotechnol. J. 13 (2015), 1106–1120.
40. MedCap Advisors, Biologics Revolution. MedCap Viewpoint. 2016, MedCap Advisors, Cambridge, MA, 5.
41. Menzel, S., Holland, T., Boes, A., Spiegel, H., Bolzenius, J., Fischer, R., et al. Optimized blanching reduces the host cell protein content and substantially enhances the recovery and stability of two plant-derived malaria vaccine candidates. Front. Plant Sci. 7 (2016), 1–15.
42. Oo, C., Kalbag, S.S., Leveraging the attributes of biologics and small molecules, and releasing the bottlenecks: a new wave of revolution in drug development. Expert. Rev. Clin. Pharmacol. 9 (2016), 747–749.
43. PhRMA, PhRMA, (eds.) Biopharmaceutical Research Industry Profile, 1 ed., 2015, Pharmaceutical Research and Manufacturers of America, Washington, D.C., USA, 1–76 Profile.
44. Rathore, A.S., Roadmap for implementation of quality by design (QbD) for biotechnology products. Trends Biotechnol. 27 (2009), 546–553.
45. Rouet, R., Lowe, D., Christ, D., Stability engineering of the human antibody repertoire. FEBS Lett. 588 (2014), 269–277.
46. Roush, D.J., Lu, Y.F., Advances in primary recovery: centrifugation and membrane technology. Biotechnol. Prog. 24 (2008), 488–495.
47. Sack, M., Rademacher, T., Spiegel, H., Boes, A., Hellwig, S., Drossard, J., et al. 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 (2015), 1094–1105.
48. Shoji, Y., Farrance, C.E., Bautista, J., Bi, H., Musiychuk, K., Horsey, A., et al. A plant-based system for rapid production of influenza vaccine antigens. Influenza Other Respir. Viruses 6 (2012), 204–210.
49. Shukla, A.A., Gottschalk, U., Single-use disposable technologies for biopharmaceutical manufacturing. Trends Biotechnol. 31 (2013), 147–154.
50. Singh, J.A., Christensen, R., Wells, G.A., Suarez-Almazor, M.E., Buchbinder, R., Lopez-Olivo, M.A., et al. Biologics for rheumatoid arthritis: an overview of cochrane reviews. Cochrane Database Syst. Rev., 2009, CD007848.
51. Stoger, E., Sack, M., Perrin, Y., Vaquero, C., Torres, E., Twyman, R.M., et al. Practical considerations for pharmaceutical antibody production in different crop systems. Mol. Breed. 9 (2002), 149–158.
52. Stoger, E., Fischer, R., Moloney, M., Ma, J.K.C., Plant molecular pharming for the treatment of chronic and infectious diseases. Annu. Rev. Plant Biol. 65 (2014), 743–768.
53. The CMC Biotech Working Group, A-Mab: a case study in bioprocess development. A-Mab: A Case Study in Bioprocess Development, 2.1 ed., 2009, CASSS - An International Separation Science Society, Emeryville, CA, USA, 1–278.
54. Thommes, J., Etzel, M., Alternatives to chromatographic separations. Biotechnol. Prog. 23 (2007), 42–45.
55. Tschofen, M., Knopp, D., Hood, E., Stoger, E., Plant molecular farming: much more than medicines. Annu. Rev. Anal. Chem. 9 (2016), 271–294.
56. della Valle, F., Gambardella, A., ‘Biological’ revolution and strategies for innovation in pharmaceutical companies. R&D Manag. 23 (1993), 287–302.
57. Varadaraju, H., Schneiderman, S., Zhang, L.F., Fong, H., Menkhaus, T.J., Process and economic evaluation for monoclonal antibody purification using a membrane-only process. Biotechnol. Prog. 27 (2011), 1297–1305.
58. Vasconcellos, J.A., Quality Assurance for the Food Industry: A Practical Approach. 2003, CRC Press, New York, NY.
59. Wirz, H., Sauer-Budge, A.F., Briggs, J., Sharpe, A., Shu, S.D., Sharon, A., Automated production of plant-based vaccines and pharmaceuticals. J. Lab. Autom. 17 (2012), 449–457.
60. Woodard, S.L., Wilken, L.R., Barros, G.O.F., White, S.G., Nikolov, Z.L., Evaluation of monoclonal antibody and phenolic extraction from transgenic Lemna for purification process development. Biotechnol. Bioeng. 104 (2009), 562–571.
61. Xenopoulos, A., A new, integrated, continuous purification process template for monoclonal antibodies: process modeling and cost of goods studies. J. Biotechnol. 213 (2015), 42–53.
62. Xu, J.F., Dolan, M.C., Medrano, G., Cramer, C.L., Weathers, P.J., Green factory: plants as bioproduction platforms for recombinant proteins. Biotechnol. Adv. 30 (2012), 1171–1184.
63. Zischewski, J., Sack, M., Fischer, R., Overcoming low yields of plant-made antibodies by a protein engineering approach. Biotechnol. J. 11 (2015), 107–116.