Production of monoclonal antibodies against botulinum neurotoxin in Nicotiana benthamiana

References

• Lacy DB, Stevens RC. Sequence homology and structural analysis of the clostridial neurotoxins11Edited by G. Von Heijne. J Mol Biol. 1999;291(5):1091–11. doi:10.1006/jmbi.1999.2945.
   PubMed Web of Science ®Google Scholar
• Barash JR, Arnon SS. A novel strain of clostridium botulinum that produces Type B and Type H Botulinum Toxins. J Infect Dis. 2013;209:183–91. doi:10.1093/infdis/jit449.
   PubMed Web of Science ®Google Scholar
• Austin JW. CLOSTRIDIUM | Occurrence of clostridium botulinum. In: Caballero B. editor. Encyclopedia of food sciences and nutrition. 2nd ed. Oxford: Academic Press; 2003. p. 1407–13.
   Google Scholar
• Saeidi S, Dadpour B, Jarahi L, Ghamsari AA, Nooghabi MJ. Clinical predictive values in botulism: a 10-year survey. Indian J Crit Care Med. 2021;25(4):411–5. doi:10.5005/jp-journals-10071-23777.
   PubMed Web of Science ®Google Scholar
• Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Hauer J, Layton M. et al. Botulinum toxin as a biological weapon: medical and public health management. JAMA. 2001;285(8):1059–70. doi:10.1001/jama.285.8.1059.
   PubMed Web of Science ®Google Scholar
• Crawford CA. Principles of biotechnology. Massachusetts and Amenia (NY): Salem Press, a division of EBSCO Information Services; 2018.
   Google Scholar
• Dressler D. Chapter 17 Botulinum toxin mechanisms of action. In: Hallett M; Phillips L; Schomer D, and Massey J. editors. Supplements to clinical neurophysiology. Amsterdam (Netherlands): Elsevier; 2004. p. 159–66.
   Google Scholar
• Hodowanec A, Bleck TP. 247 - Botulism (Clostridium botulinum). In: Bennett J; Dolin R Blaser M. editors. Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. 8th ed. Philadelphia: W.B. Saunders; 2015. p. 2763–7.e2.
   Google Scholar
• Pirazzini M, Rossetto O, Eleopra R, Montecucco C, Witkin JM. Botulinum neurotoxins: biology, pharmacology, and toxicology. Pharmacol Rev. 2017;69:200–35. doi:10.1124/pr.116.012658.
   PubMed Web of Science ®Google Scholar
• Simpson LL. Identification of the major steps in botulinum toxin action. Annu Rev Pharmacol Toxicol. 2004;44(1):167–93. doi:10.1146/annurev.pharmtox.44.101802.121554.
   PubMedGoogle Scholar
• Tacket CO, Shandera WX, Mann JM, Hargrett NT, Blake PA. Equine antitoxin use and other factors that predict outcome in type a foodborne botulism. Am J Med. 1984;76(5):794–8. doi:10.1016/0002-9343(84)90988-4.
   PubMed Web of Science ®Google Scholar
• Parrera GS, Astacio H, Tunga P, Anderson DM, Hall CL, Richardson JS. Use of botulism antitoxin heptavalent (A, B, C, D, E, F, G)—(equine) (BAT®) in clinical study subjects and patients: a 15-year systematic safety review. Toxins. 2021;14(1):14. doi:10.3390/toxins14010019.
   PubMed Web of Science ®Google Scholar
• Bregenholt S, Haurum J. Pathogen-specific recombinant human polyclonal antibodies: biodefence applications. Expert Opin Biol Ther. 2004;4(3):387–96. doi:10.1517/14712598.4.3.387.
   PubMed Web of Science ®Google Scholar
• Ko K, Koprowski H. Plant biopharming of monoclonal antibodies. Virus Res. 2005;111(1):93–100. doi:10.1016/j.virusres.2005.03.016.
   PubMed Web of Science ®Google Scholar
• Kelley B. Industrialization of mAb production technology: the bioprocessing industry at a crossroads. Mabs-austin. 2009;1(5):443–52. doi:10.4161/mabs.1.5.9448.
   PubMed Web of Science ®Google Scholar
• Werner RG. Economic aspects of commercial manufacture of biopharmaceuticals. J Biotechnol. 2004;113(1–3):171–82. doi:10.1016/j.jbiotec.2004.04.036.
   PubMed Web of Science ®Google Scholar
• D’Aoust M-A, Couture MM-J, Charland N, Trépanier S, Landry N, Ors F, Vézina L-P. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J. 2010;8:607–19. doi:10.1111/j.1467-7652.2009.00496.x.
   PubMed Web of Science ®Google Scholar
• Joshi L, Lopez LC. Bioprospecting in plants for engineered proteins. Curr Opin Plant Biol. 2005;8(2):223–6. doi:10.1016/j.pbi.2005.01.003.
   PubMed Web of Science ®Google Scholar
• Phakham T, Bulaon CJI, Khorattanakulchai N, Shanmugaraj B, Buranapraditkun S, Boonkrai C, Sooksai S, Hirankarn N, Abe Y, Strasser R. et al. Functional characterization of pembrolizumab produced in Nicotiana benthamiana using a rapid transient expression system. Front Plant Sci. 2021;12:12. doi:10.3389/fpls.2021.736299.
   Web of Science ®Google Scholar
• Bulaon CJI, Khorattanakulchai N, Rattanapisit K, Sun H, Pisuttinusart N, Strasser R, Tanaka S, Soon-Shiong P, Phoolcharoen W. Antitumor effect of plant-produced anti-CTLA-4 monoclonal antibody in a murine model of colon cancer. Front Plant Sci. 2023;14:14. doi:10.3389/fpls.2023.1149455.
   Web of Science ®Google Scholar
• Rattanapisit K, Bulaon CJI, Strasser R, Sun H, Phoolcharoen W. In vitro and in vivo studies of plant-produced atezolizumab as a potential immunotherapeutic antibody. Sci Rep. 2023;13(1):14146. doi:10.1038/s41598-023-41510-w.
   PubMed Web of Science ®Google Scholar
• Bulaon CJI, Shanmugaraj B, Oo Y, Rattanapisit K, Chuanasa T, Chaotham C, Phoolcharoen W. Rapid transient expression of functional human vascular endothelial growth factor in Nicotiana benthamiana and characterization of its biological activity. Biotechnol Rep. 2020;27:e00514. doi:10.1016/j.btre.2020.e00514.
   Google Scholar
• Bulaon CJI, Sun H, Malla A, Phoolcharoen W. Therapeutic efficacy of plant-produced nivolumab in transgenic C57BL/6-hPD-1 mouse implanted with MC38 colon cancer. Biotechnol Rep. 2023;38:e00794. doi:10.1016/j.btre.2023.e00794.
   Google Scholar
• Goodin MM, Zaitlin D, Naidu RA, Lommel SA. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Molecular plant-microbe interactions. MPMI. 2008;21:1015–26. doi:10.1094/MPMI-21-8-1015.
   PubMed Web of Science ®Google Scholar
• Tremblay R, Wang D, Jevnikar AM, Ma S. Tobacco, a highly efficient green bioreactor for production of therapeutic proteins. Biotechnol Adv. 2010;28(2):214–21. doi:10.1016/j.biotechadv.2009.11.008.
   PubMed Web of Science ®Google Scholar
• Daniell H, Streatfield SJ, Wycoff K. Medical molecular farming: production of antibodies, biopharmaceuticals and edible vaccines in plants. Trends Plant Sci. 2001;6(5):219–26. doi:10.1016/S1360-1385(01)01922-7.
   PubMed Web of Science ®Google Scholar
• Conrad U, Fiedler U. Compartment-specific accumulation of recombinant immunoglobulins in plant cells: an essential tool for antibody production and immunomodulation of physiological functions and pathogen activity. Plant Mol Biol. 1998;38(1/2):101–9. doi:10.1023/A:1006029617949.
   PubMed Web of Science ®Google Scholar
• Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol. 2003;21(3):255–61. doi:10.1038/nbt0303-255.
   PubMed Web of Science ®Google Scholar
• Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science. 2001;291(5512):2364–9. doi:10.1126/science.291.5512.2364.
   PubMed Web of Science ®Google Scholar
• Henderson J, Bauly JM, Ashford DA, Oliver SC, Hawes CR, Lazarus CM, Venis MA, Napier RM. Retention of maize auxin-binding protein in the endoplasmic reticulum: quantifying escape and the role of auxin. Planta. 1997;202:313–23. doi:10.1007/s004250050133.
   PubMed Web of Science ®Google Scholar
• Bauly JM, Sealy IM, Macdonald H, Brearley J, Dröge S, Hillmer S, Robinson DG, Venis MA, Blatt MR, Lazarus CM. et al. Overexpression of auxin-binding protein enhances the sensitivity of guard cells to auxin. Plant Physiol. 2000;124(3):1229–38. doi:10.1104/pp.124.3.1229.
   PubMed Web of Science ®Google Scholar
• Sharp JM, Doran PM. Characterization of monoclonal antibody fragments produced by plant cells. Biotechnol Bioeng. 2001;73(5):338–46. doi:10.1002/bit.1067.
   PubMed Web of Science ®Google Scholar
• Williams RC Jr., Osterland CK, Margherita S, Tokuda S, Messner RP. Studies of biologic and serologic activities of rabbit-IgG antibody depleted of carbohydrate Residues1. J Immunol. 1973;111(6):1690–8. doi:10.4049/jimmunol.111.6.1690.
   PubMed Web of Science ®Google Scholar
• Koide N, Nose M, Muramatsu T. Recognition of IgG by fc receptor and complement: effects of glycosidase digestion. Biochem Bioph Res Co. 1977;75(4):838–44. doi:10.1016/0006-291X(77)91458-9.
   PubMed Web of Science ®Google Scholar
• Nose M, Wigzell H. Biological significance of carbohydrate chains on monoclonal antibodies. Proc Natl Acad Sci U S A. 1983;80(21):6632–6. doi:10.1073/pnas.80.21.6632.
   PubMed Web of Science ®Google Scholar
• Amersdorfer P, Wong C, Chen S, Smith T, Deshpande S, Sheridan R, Finnern R, Marks JD. Molecular characterization of murine humoral immune response to botulinum neurotoxin type A binding domain as assessed by using phage antibody libraries. Infect Immun. 1997;65:3743–52. doi:10.1128/iai.65.9.3743-3752.1997.
   PubMed Web of Science ®Google Scholar
• Garcia-Rodriguez C, Geren IN, Lou J, Conrad F, Forsyth C, Wen W, Chakraborti S, Zao H, Manzanarez G, Smith TJ. et al. Neutralizing human monoclonal antibodies binding multiple serotypes of botulinum neurotoxin. Protein Eng Des Sel. 2011;24(3):321–31. doi:10.1093/protein/gzq111.
   PubMed Web of Science ®Google Scholar
• Matsumura T, Amatsu S, Misaki R, Yutani M, Du A, Kohda T, Fujiyama K, Ikuta K, Fujinaga Y. Fully human monoclonal antibodies effectively neutralizing botulinum neurotoxin serotype B. Toxins. 2020;12:12. doi:10.3390/toxins12050302.
   Web of Science ®Google Scholar
• Przedpelski A, Tepp WH, Zuverink M, Johnson EA, Pellet S, Barbieri JT. Enhancing toxin-based vaccines against botulism. Vaccine. 2018;36(6):827–32. doi:10.1016/j.vaccine.2017.12.064.
   PubMed Web of Science ®Google Scholar
• Nigam PK, Nigam A. Botulinum toxin. Indian J Dermatol. 2010;55(1):8–14. doi:10.4103/0019-5154.60343.
   PubMedGoogle Scholar
• Fox CK, Keet CA, Strober JB. Recent advances in infant botulism. Pediatr Neurol. 2005;32(3):149–54. doi:10.1016/j.pediatrneurol.2004.10.001.
   PubMed Web of Science ®Google Scholar
• Pifko E, Price A, Sterner S. Infant botulism and indications for administration of botulism immune globulin. Pediatr Emerg Care. 2014;30:120–4. doi:10.1097/PEC.0000000000000079.
   PubMed Web of Science ®Google Scholar
• Cenci Di Bello I, Poulain B, Shone CC, Tauc L, Dolly JO. Antagonism of the intracellular action of botulinum neurotoxin type a with monoclonal antibodies that map to light-chain epitopes. Eur J Biochem. 1994;219(1–2):161–9. doi:10.1111/j.1432-1033.1994.tb19926.x.
   PubMedGoogle Scholar
• Brown DR, Lloyd JP, Schmidt JJ. Identification and characterization of a neutralizing monoclonal antibody against botulinum neurotoxin serotype F, following vaccination with active toxin. Hybridoma. 1997;16:447–56. doi:10.1089/hyb.1997.16.447.
   PubMedGoogle Scholar
• Pless DD, Torres ER, Reinke EK, Bavari S, Clements JD. High-affinity, protective antibodies to the binding domain of botulinum neurotoxin type A. Infect Immun. 2001;69(1):570–4. doi:10.1128/IAI.69.1.570-574.2001.
   PubMed Web of Science ®Google Scholar
• Wu HC, Yeh CT, Huang YL, Tarn LJ, Lung CC. Characterization of neutralizing antibodies and identification of neutralizing epitope mimics on the clostridium botulinum neurotoxin type A. Appl Environ Microbiol. 2001;67(7):3201–7. doi:10.1128/AEM.67.7.3201-3207.2001.
   PubMed Web of Science ®Google Scholar
• Desrosiers L, Knoepp LR. Botulinum toxin a: a review of potential uses in treatment of female urogenital and pelvic floor disorders. Ochsner J. 2020;20(4):400–9. doi:10.31486/toj.19.0076.
   PubMed Web of Science ®Google Scholar
• Nandi S, Kwong AT, Holtz BR, Erwin RL, Marcel S, McDonald KA. Techno-economic analysis of a transient plant-based platform for monoclonal antibody production. Mabs-austin. 2016;8(8):1456–66. doi:10.1080/19420862.2016.1227901.
   PubMed Web of Science ®Google Scholar
• Zischewski J, Sack M, Fischer R. Overcoming low yields of plant-made antibodies by a protein engineering approach. Biotechnol J. 2016;11(1):107–16. doi:10.1002/biot.201500255.
   PubMed Web of Science ®Google Scholar
• Buyel JF, 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. 2015;10(4):584–91. doi:10.1002/biot.201400611.
   PubMed Web of Science ®Google Scholar
• Buyel JF, Twyman RM, Fischer R. Very-large-scale production of antibodies in plants: the biologization of manufacturing. Biotechnol Adv. 2017;35(4):458–65. doi:10.1016/j.biotechadv.2017.03.011.
   PubMed Web of Science ®Google Scholar
• Lim J, Patkar A, McDonagh G, Sinclair A, Lucy P. Modeling bioprocess cost: process economic benefits of expression technology based on pseudomonas fluorescens. Bioprocess Int. 2010;8:62–70.
   Google Scholar
• Buyel JF, Fischer R. Scale-down models to optimize a filter train for the downstream purification of recombinant pharmaceutical proteins produced in tobacco leaves. Biotechnol J. 2014;9(3):415–25. doi:10.1002/biot.201300369.
   PubMed Web of Science ®Google Scholar
• Hassan S, Keshavarz-Moore E, Ma J, Thomas C. Breakage of transgenic tobacco roots for monoclonal antibody release in an ultra-scale down shearing device. Biotechnol Bioeng. 2014;111(1):196–201. doi:10.1002/bit.25006.
   PubMed Web of Science ®Google Scholar
• Barak I, Bader B. Lifecycle cost analysis for single-use systems. BioPharm Int. 2008;21:30–43.
   Google Scholar
• Levine HL, Stock R, Lilja JE, Gaasvik A, Hummel H, Ransohoff T, Jones SD. Single-use technology and modular construction. Bioprocess Int. 2013;11:40–5.
   Google Scholar
• Rogge P, Müller D, Schmidt S. The single-use or stainless steel decision process. Bioprocess Int. 2015;13:10–15.
   Google Scholar
• Sack M, Rademacher T, Spiegel H, Boes A, Hellwig S, Drossard J, Stoger E, Fischer R. From gene to harvest: insights into upstream process development for the GMP production of a monoclonal antibody in transgenic tobacco plants. Plant Biotechnol J. 2015;13:1094–105. doi:10.1111/pbi.12438.
   PubMed Web of Science ®Google Scholar
• Buyel JF. Plant molecular farming – integration and exploitation of side streams to achieve sustainable biomanufacturing. Front Plant Sci. 2019;9. doi:10.3389/fpls.2018.01893.
   PubMed Web of Science ®Google Scholar
• Buyel JF. Product safety aspects of plant molecular farming. Front Bioeng Biotechnol. 2023;11:11. doi:10.3389/fbioe.2023.1238917.
   Web of Science ®Google Scholar
• Nowakowski A, Wang C, Powers DB, Amersdorfer P, Smith TJ, Montgomery VA, Sheridan R, Blake R, Smith LA, Marks JD. Potent neutralization of botulinum neurotoxin by recombinant oligoclonal antibody. Proc Natl Acad Sci USA. 2002;99:11346–50. doi:10.1073/pnas.172229899.
   PubMed Web of Science ®Google Scholar
• Garcia-Rodriguez C, Geren IN, Lou J, Conrad F, Forsyth C, Wen W, Chakraborti S, Zao H, Manzanarez G, Smith TJ. et al. Neutralizing human monoclonal antibodies binding multiple serotypes of botulinum neurotoxin. Protein Eng Des Sel. 2010;24:321–31. doi:10.1093/protein/gzq111.
   PubMed Web of Science ®Google Scholar
• Phetphoung T, Malla A, Rattanapisit K, Pisuttinusart N, Damrongyot N, Joyjamras K, Chanvorachote P, Phakham T, Wongtangprasert T, Strasser R. et al. Expression of plant-produced anti-PD-L1 antibody with anoikis sensitizing activity in human lung cancer cells via., suppression on epithelial-mesenchymal transition. PLoS One. 2022;17(11):e0274737. doi:10.1371/journal.pone.0274737.
   PubMed Web of Science ®Google Scholar
• Phakham T, Bulaon CJI, Khorattanakulchai N, Shanmugaraj B, Buranapraditkun S, Boonkrai C, Sooksai S, Hirankarn N, Abe Y, Strasser R. et al. Functional characterization of pembrolizumab produced in nicotiana benthamiana using a rapid transient expression system. Front Plant Sci. 2021;12:736299. doi:10.3389/fpls.2021.736299.
   PubMed Web of Science ®Google Scholar
• Zhang X, Han L, Zong H, Ding K, Yuan Y, Bai J, Zhou Y, Zhang B, Zhu J. Enhanced production of anti-PD1 antibody in CHO cells through transient co-transfection with anti-apoptotic genes bcl-x L and mcl-1. Bioprocess Biosyst Eng. 2018;41:633–40. doi:10.1007/s00449-018-1898-z.
   PubMed Web of Science ®Google Scholar
• Dodev TS, Karagiannis P, Gilbert AE, Josephs DH, Bowen H, James LK, Bax HJ, Beavil R, Pang MO, Gould HJ. et al. A tool kit for rapid cloning and expression of recombinant antibodies. Sci Rep. 2014;4(1):5885. doi:10.1038/srep05885.
   PubMed Web of Science ®Google Scholar
• Ahmadi S, Davami F, Davoudi N, Nematpour F, Ahmadi M, Ebadat S, Azadmanesh K, Barkhordari F, Mahboudi F. Monoclonal antibodies expression improvement in CHO cells by piggybac transposition regarding vectors ratios and design. PLoS One. 2017;12(6):e0179902. doi:10.1371/journal.pone.0179902.
   PubMed Web of Science ®Google Scholar
• Kroon C, Breuer L, Jones L, An J, Akan A, Mohamed Ali EA, Busch F, Fislage M, Ghosh B, Hellrigel-Holderbaum M. et al. Blind spots on western blots: assessment of common problems in western blot figures and methods reporting with recommendations to improve them. PLoS Biol. 2022;20(9):e3001783. doi:10.1371/journal.pbio.3001783.
   PubMed Web of Science ®Google Scholar
• Vidarsson G, Dekkers G, Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front Immunol. 2014;5. doi:10.3389/fimmu.2014.00520.
   PubMed Web of Science ®Google Scholar
• Peng Chen Z, Morris JG, Rodriguez RL, Wagle Shukla A, Tapia-Núñez J, Okun MS. Emerging opportunities for serotypes of botulinum neurotoxins. Toxins. 2012;4:1196–222. doi:10.3390/toxins4111196.
   PubMed Web of Science ®Google Scholar
• Smith TJ, Lou J, Geren IN, Forsyth CM, Tsai R, Laporte SL, Tepp WH, Bradshaw M, Johnson EA, Smith LA. et al. Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infect Immun. 2005;73(9):5450–7. doi:10.1128/IAI.73.9.5450-5457.2005.
   PubMed Web of Science ®Google Scholar
• Mukherjee J, McCann C, Ofori K, Hill J, Baldwin K, Shoemaker CB, Harrison P, Tzipori S. Sheep monoclonal antibodies prevent systemic effects of botulinum neurotoxin A1. Toxins. 2012;4:1565–81. doi:10.3390/toxins4121565.
   PubMed Web of Science ®Google Scholar