Investigation of a monoclonal antibody against enterotoxigenic Escherichia coli, expressed as secretory IgA1 and IgA2 in plants

References

• Bourgeois AL, Wierzba TF, Walker RI. Status of vaccine research and development for enterotoxigenic Escherichia coli. Vaccine. 2016;34:2880–14. doi:10.1016/j.vaccine.2016.02.076.
   Google Scholar
• Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect Immun. 2007;75(8):3961–3968. doi:10.1128/IAI.00459-07.
   Google Scholar
• Khalil IA, Troeger C, Blacker BF, Rao PC, Brown A, Atherly DE, Brewer TG, Engmann CM, Houpt ER, Kang G, et al. Morbidity and mortality due to shigella and enterotoxigenic Escherichia coli diarrhoea: the global burden of disease study 1990–2016. The Lancet Infectious Diseases. 2016;34(11):2880–2886. doi:10.1016/S1473-3099(18)30475-4.
   Google Scholar
• Liu J, Platts-Mills JA, Juma J, Kabir F, Nkeze J, Okoi C, Operario DJ, Uddin J, Ahmed S, Alonso PL, et al. Use of quantitative molecular diagnostic methods to identify causes of diarrhoea in children: a reanalysis of the GEMS case-control study. Lancet. 2016;388:1291–1301. doi:10.1016/S0140-6736(16)31529-X.
   Google Scholar
• Zhang W, Sack DA. Progress and hurdles in the development of vaccines against enterotoxigenic Escherichia coli in humans. Expert Rev Vaccines. 2012;11(6):677–694. doi:10.1586/erv.12.37.
   Google Scholar
• Barrett J, Brown M. Travellers’ diarrhoea. Bmj-Brit Med J. 2016;353:i1937.
   Google Scholar
• Estrada-Garcia T, Cerna JF, Paheco-Gil L, Velazquez RF, Ochoa TJ, Torres J, DuPont HL. Drug-resistant diarrheogenic Escherichia coli, Mexico. Emerg Infect Dis. 2005;11(8):1306–1308. doi:10.3201/eid1108.050192.
   Google Scholar
• Paitan Y. Current trends in antimicrobial resistance of Escherichia coli. Curr Top Microbiol Immunol. 2018;416:181–211. doi:10.1007/82_2018_110.
   Google Scholar
• Levine MM. Escherichia-coli that cause diarrhea - enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987;155(3):377–389. doi:10.1093/infdis/155.3.377.
   Google Scholar
• Isidean SD, Riddle MS, Savarino SJ, Porter CK. A systematic review of ETEC epidemiology focusing on colonization factor and toxin expression. Vaccine. 2011;29(37):6167–6178. doi:10.1016/j.vaccine.2011.06.084.
   Google Scholar
• Jelinek T, Kollaritsch H. Vaccination with Dukoral against travelers’ diarrhea (ETEC) and cholera. Expert Rev Vaccines. 2008;7(5):561–567. doi:10.1586/14760584.7.5.561.
   Google Scholar
• Ahmed T, Bhuiyan TR, Zaman K, Sinclair D, Qadri F. Vaccines for preventing enterotoxigenic Escherichia coli (ETEC) diarrhoea. Cochrane Db Syst Rev. 2013. doi:10.1002/14651858.CD009029.pub2.
   Google Scholar
• Svennerholm AM, Tobias J. Vaccines against enterotoxigenic Escherichia coli. Expert Rev Vaccines. 2008;7(6):795–804. doi:10.1586/14760584.7.6.795.
   Google Scholar
• Steinsland H, Valentiner-Branth P, Gjessing HK, Aaby P, Molbak K, Sommerfelt H. Protection from natural infections with enterotoxigenic Escherichia coli: longitudinal study. Lancet. 2003;362:286–291. doi:10.1016/S0140-6736(03)13971-2.
   Google Scholar
• Chakraborty S, Harro C, DeNearing B, Ram M, Feller A, Cage A, Bauers N, Bourgeois AL, Walker R, Sack DA. Characterization of mucosal immune responses to enterotoxigenic escherichia coli vaccine antigens in a human challenge model: response profiles after primary infection and homologous rechallenge with strain H10407. Clin Vaccine Immunol. 2016;23(1):55–64. doi:10.1128/CVI.00617-15.
   Google Scholar
• McArthur MA, Maciel M, Pasetti MF. Human immune responses against Shigella and enterotoxigenic E-coli: current advances and the path forward. Vaccine. 2017;35(49):6803–6806. doi:10.1016/j.vaccine.2017.05.034.
   Google Scholar
• Holmgren J, Bourgeois L, Carlin N, Clements J, Gustafsson B, Lundgren A, Nygren E, Tobias J, Walker R, Svennerholm A-M, et al. Development and preclinical evaluation of safety and immunogenicity of an oral ETEC vaccine containing inactivated E. coli bacteria overexpressing colonization factors CFA/I, CS3, CS5 and CS6 combined with a hybrid LT/CT B subunit antigen, administered alone and together with dmLT adjuvant. Vaccine. 2013;31(20):2457–2464. doi:10.1016/j.vaccine.2013.03.027.
   Google Scholar
• Virdi V, Palaci J, Laukens B, Ryckaert S, Cox E, Vanderbeke E, Depicker A, Callewaert N. Yeast-secreted, dried and food-admixed monomeric IgA prevents gastrointestinal infection in a piglet model. Nat Biotechnol. 2019;37(5):527–+. doi:10.1038/s41587-019-0070-x.
   Google Scholar
• Qadri F, Das SK, Faruque AS, Fuchs GJ, Albert MJ, Sack RB, Svennerholm AM. Prevalence of toxin types and colonization factors in enterotoxigenic Escherichia coli isolated during a 2-year period from diarrheal patients in Bangladesh. J Clin Microbiol. 2000;38:27–31.
   Google Scholar
• Luiz WB, Rodrigues JF, Crabb JH, Savarino SJ, Ferreira LC, Young VB. Maternal vaccination with a fimbrial tip adhesin and passive protection of neonatal mice against lethal human enterotoxigenic Escherichia coli challenge. Infect Immun. 2015;83(12):4555–4564. doi:10.1128/IAI.00858-15.
   Google Scholar
• Savarino SJ, McKenzie R, Tribble DR, Porter CK, O’Dowd A, Cantrell JA, Sincock SA, Poole ST, DeNearing B, Woods CM, et al. Prophylactic efficacy of hyperimmune bovine colostral antiadhesin antibodies against enterotoxigenic escherichia coli diarrhea: a randomized, double-blind, placebo-controlled, phase 1 trial. J Infect Dis. 2017;216:7–13. doi:10.1093/infdis/jix144.
   Google Scholar
• Giuntini S, Stoppato M, Sedic M, Ejemel M, Pondish JR, Wisheart D, Schiller ZA, Thomas WD, Barry EM, Cavacini LA, et al. Identification and characterization of human monoclonal antibodies for immunoprophylaxis against enterotoxigenic escherichia coli infection. Infect Immun. 2018;86(12):e00713-18.
   Google Scholar
• Stoger E, Fischer R, Moloney M, Ma JK. Plant molecular pharming for the treatment of chronic and infectious diseases. Annu Rev Plant Biol. 2014;65(1):743–768. doi:10.1146/annurev-arplant-050213-035850.
   Google Scholar
• Ma JK, Christou P, Chikwamba R, Haydon H, Paul M, Ferrer MP, Ramalingam S, Rech E, Rybicki E, Wigdorowitz A, et al. Realising the value of plant molecular pharming to benefit the poor in developing countries and emerging economies. Plant Biotechnol J. 2013;11(9):1029–1033. doi:10.1111/pbi.12127.
   Google Scholar
• Ma JK, Drossard J, Lewis D, Altmann F, Boyle J, Christou P, Cole T, Dale P, van Dolleweerd CJ, Isitt V, 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. 2015;13(8):1106–1120. doi:10.1111/pbi.12416.
   Google Scholar
• Group PIW, Multi-National PIIST, Davey RT Jr., Dodd L, Proschan MA, Neaton J, et al. A randomized, controlled trial of ZMapp for ebola virus infection. N Engl J Med. 2016;375:1448–1456. https://www.nejm.org/doi/full/10.1056/nejmoa1604330
   Google Scholar
• Ma JK, Hiatt A, Hein M, Vine ND, Wang F, Stabila P, van Dolleweerd C, Mostov K, Lehner T. Generation and assembly of secretory antibodies in plants. Science. 1995;268(5211):716–719. doi:10.1126/science.7732380.
   Google Scholar
• Ma JK, Hikmat BY, Wycoff K, Vine ND, Chargelegue D, Yu L, Hein MB, Lehner T. Characterization of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. NatMed. 1998;4:601–606.
   Google Scholar
• Strasser R, Stadlmann J, Schahs M, Stiegler G, Quendler H, Mach L, Glössl J, Weterings K, Pabst M, Steinkellner H, et al. Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol J. 2008;6(4):392–402. doi:10.1111/j.1467-7652.2008.00330.x.
   Google Scholar
• Hu Y, Kumru OS, Xiong J, Antunez LR, Hickey J, Wang Y, Cavacini L, Klempner M, Joshi SB, Volkin DB. Preformulation characterization and stability assessments of secretory IgA monoclonal antibodies as potential candidates for passive immunization by oral administration. J Pharm Sci. 2019;109(1):407-421.
   Google Scholar
• Paul M, Reljic R, Klein K, Drake PM, van Dolleweerd C, Pabst M, Windwarder M, Arcalis E, Stoger E, Altmann F. Characterization of a plant-produced recombinant human secretory IgA with broad neutralizing activity against HIV. MAbs. 2011;29(6):6167–6178. doi:10.4161/mabs.36336.
   Google Scholar
• Virdi V, Coddens A, De Buck S, Millet S, Goddeeris BM, Cox E, De Greve H, Depicker A. Orally fed seeds producing designer IgAs protect weaned piglets against enterotoxigenic Escherichia coli infection. Proc Natl Acad Sci U S A. 2016;34(29):2880–2886. doi:10.1073/pnas.1301975110.
   Google Scholar
• Woof JM, Kerr MA. IgA function - variations on a theme. Immunology. 2004;113(2):175–177. doi:10.1111/j.1365-2567.2004.01958.x.
   Google Scholar
• Mestecky J, Russell MW, Elson CO. Intestinal IgA: novel views on its function in the defence of the largest mucosal surface. Gut. 1999;44(1):2–5. doi:10.1136/gut.44.1.2.
   Google Scholar
• Tarelli E, Smith AC, Hendry BM, Challacombe SJ, Pouria S. Human serum IgA1 is substituted with up to six O-glycans as shown by matrix assisted laser desorption ionisation time-of-flight mass spectrometry. Carbohyd Res. 2004;339(13):2329–2335. doi:10.1016/j.carres.2004.07.011.
   Google Scholar
• Furtado PB, Whitty PW, Robertson A, Eaton JT, Almogren A, Kerr MA, Woof JM, Perkins SJ. Solution structure determination of monomeric human IgA2 by X-ray and neutron scattering, analytical ultracentrifugation and constrained modelling: a comparison with monomeric human IgA1. J Mol Biol. 2004;338(5):921–941. doi:10.1016/j.jmb.2004.03.007.
   Google Scholar
• Qiu JZ, Brackee GP, Plaut AG. Analysis of the specificity of bacterial immunoglobulin A (IgA) proteases by a comparative study of ape serum IgAs as substrates. Infect Immun. 1996;64(3):933–937. doi:10.1128/IAI.64.3.933-937.1996.
   Google Scholar
• Almogren A, Senior BW, Kerr MA. A comparison of the binding of secretory component to immunoglobulin A (IgA) in human colostral S-IgA1 and S-IgA2. Immunology. 2007;120(2):273–280. doi:10.1111/j.1365-2567.2006.02498.x.
   Google Scholar
• Kirchhoff J, Raven N, Boes A, Roberts JL, Russell S, Treffenfeldt W, Fischer R, Schinkel H, Schiermeyer A, Schillberg S. Monoclonal tobacco cell lines with enhanced recombinant protein yields can be generated from heterogeneous cell suspension cultures by flow sorting. Plant Biotechnol J. 2012;10(8):936–944. doi:10.1111/j.1467-7652.2012.00722.x.
   Google Scholar
• Hehle VK, Paul MJ, Drake PM, Ma JK, van Dolleweerd CJ. Antibody degradation in tobacco plants: a predominantly apoplastic process. BMC Biotechnol. 2012;10(1):128. doi:10.1186/1472-6750-11-128.
   Google Scholar
• Steffen U, Koeleman CA, Sokolova MV, Bang H, Kleyer A, Rech J, Unterweger H, Schicht M, Garreis F, Hahn J, et al. IgA subclasses have different effector functions associated with distinct glycosylation profiles. Nat Commun. 2020;11(1):120.
   Google Scholar
• Kallolimath S, Castilho A, Strasser R, Grunwald-Gruber C, Altmann F, Strubl S, Galuska CE, Zlatina K, Galuska SP, Werner S, et al. Engineering of complex protein sialylation in plants. Proc Natl Acad Sci U S A. 2016;113(34):9498–9503. doi:10.1073/pnas.1604371113.
   Google Scholar
• Crottet P, Corthesy B. Secretory component delays the conversion of secretory IgA into antigen-binding competent F(ab ‘)(2): a possible implication for mucosal defense. Journal of Immunology. 1998;161:5445–5453.
   Google Scholar
• Dicker M, Tschofen M, Maresch D, Konig J, Juarez P, Orzaez D, Altmann F, Steinkellner H, Strasser R. Transient glyco-engineering to produce recombinant IgA1 with defined N- and O-Glycans in plants. Front Plant Sci. 2012;7:7. doi:10.3389/fpls.2016.00018.
   Google Scholar
• Ledford H. Antibody therapies could be a bridge to a coronavirus vaccine - but will the world benefit? Nature. 2020;584(7821):333-334.
   Google Scholar
• Kong QX, Richter L, Yang YF, Arntzen CJ, Mason HS, Thanavala Y. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci U S A. 2016;34(20):2880–2886. doi:10.1073/pnas.191617598.
   Google Scholar
• Tacket CO, Pasetti MF, Edelman R, Howard JA, Streatfield S. Immunogenicity of recombinant LT-B delivered orally to humans in transgenic corn. Vaccine. 2004;22(31–32):4385–4389. doi:10.1016/j.vaccine.2004.01.073.
   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. 2016;8:1456–1466.
   Google Scholar
• Schillberg S, Raven N, Spiegel H, Rasche S, Buntru M. Critical analysis of the commercial potential of plants for the production of recombinant proteins. Front Plant Sci. 2003;362:720. doi:10.3389/fpls.2019.00720.
   Google Scholar
• Strasser R, Altmann F, Mach L, Glossl J, Steinkellner H, Luiz WB, Rodrigues JF, Crabb JH, Savarino SJ. Generation of arabidopsis thaliana plants with complexN-glycans lacking β1,2-linked xylose and core α1,3-linked fucose. FEBS Lett. 2004;561(1–3):132–136. doi:10.1016/S0014-5793(04)00150-4.
   Google Scholar
• Teh AY, Maresch D, Klein K, Ma JK-C Characterization of VRC01, a potent and broadly neutralizing anti-HIV mAb, produced in transiently and stably transformed tobacco. Plant Biotechnol J 2013.
   Google Scholar
• Goritzer K, Maresch D, Altmann F, Obinger C, Strasser R. Exploring site-specific N-glycosylation of HEK293 and plant-produced human IgA isotypes. J Proteome Res. 2017;16(7):2560–2570. doi:10.1021/acs.jproteome.7b00121.
   Google Scholar
• Bolick DT, Kolling GL, Moore JH 2nd, de Oliveira LA, Tung K, Philipson C, Viladomiu M, Hontecillas R, Bassaganya-Riera J, Guerrant RL, et al. Zinc deficiency alters host response and pathogen virulence in a mouse model of enteroaggregative escherichia coli-induced diarrhea. Gut Microbes. 2014;5(5):618–627. doi:10.4161/19490976.2014.969642.
   Google Scholar
• Sack RB, Gorbach SL, Banwell JG, Jacobs B, Chatterjee BD, Mitra RC. Enterotoxigenic Escherichia coli isolated from patients with severe cholera-like disease. J Infect Dis. 1971;123(4):378–385. doi:10.1093/infdis/123.4.378.
   Google Scholar