Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

A Review on Edible Vaccines and Biopharmaceutical Products from Plants

Author(s): Pankaj Kumar Paradia, Rameshwar Bhavale, Tejas Agnihotri and Aakanchha Jain*

Volume 24, Issue 4, 2023

Published on: 16 September, 2022

Page: [495 - 509] Pages: 15

DOI: 10.2174/1389201023666220803151039

Price: $65

Abstract

Plants have substantial potential for the development of various biopharmaceuticals. Plants provide a cost-effective and direct source for the production of biopharmaceuticals such as vaccines, antibodies, proteins, enzymes, and hormones. In most cases, purification is an important and expensive step in the production of these substances. The problem can be resolved when it is produced in plants and the whole plant can be consumed. Direct ingestion of plant materials may help in overcoming the purification step. Being produced in seeds, fruits and tubers, it helps in providing more immunization in developing countries at a cheaper rate. Moreover, it can be administered more efficiently than any other dosage forms. This review focuses on various immunization and therapeutic products that are produced in plants along with currently available formulations in each category.

Keywords: Biopharmaceutical, edible vaccine, glycosylation, mass vaccination, plantibodies, transgenic plant.

« Previous Next »
Graphical Abstract

[1]
Wang, A.; Ma, S. Molecular farming in plants: Recent advances and future prospects. Mol. Farm. Plants Recent Adv. Futur. Prospect., 2012, 201283274963
[http://dx.doi.org/10.1007/978-94-007-2217-0]
[2]
Jhansi Rani, S.; Usha, R. Transgenic plants: Types, benefits, public concerns and future. J. Pharm. Res., 2013, 6(8), 879-883.
[http://dx.doi.org/10.1016/j.jopr.2013.08.008]
[3]
Loh, H.S.; Green, B.J.; Yusibov, V. Using transgenic plants and modified plant viruses for the development of treatments for human diseases. Curr. Opin. Virol., 2017, 26, 81-89.
[http://dx.doi.org/10.1016/j.coviro.2017.07.019] [PMID: 28800551]
[4]
Chan, H.T.; Daniell, H. Plant made oral vaccines against human infectious diseases are we there yet? Plant Biotechnol. J., 2015, 13(8), 1056-1070.
[http://dx.doi.org/10.1111/pbi.12471] [PMID: 26387509]
[5]
Esqueda, A.; Chen, Q. Development and expression of subunit vaccines against viruses in plants. Methods Mol. Biol., 2021, 2225, 25-38.
[http://dx.doi.org/10.1007/978-1-0716-1012-1_2] [PMID: 33108655]
[6]
Oluwayelu, D.O.; Adebiyi, A.I. Plantibodies in human and animal health: A review. Afr. Health Sci., 2016, 16(2), 640-645.
[http://dx.doi.org/10.4314/ahs.v16i2.35] [PMID: 27605982]
[7]
Scotti, N.; Rybicki, E.P. Virus like particles produced in plants as potential vaccines. Expert Rev. Vaccines, 2013, 12(2), 211-224.
[http://dx.doi.org/10.1586/erv.12.147] [PMID: 23414411]
[8]
Khan, M.S.; Mustafa, G.; Joyia, F.A. Enzymes: Plant based production and their applications. Protein Pept. Lett., 2018, 25(2), 136-147.
[http://dx.doi.org/10.2174/0929866525666180122123722] [PMID: 29359656]
[9]
Stöger, E.; Vaquero, C.; Torres, E.; Sack, M.; Nicholson, L.; Drossard, J.; Williams, S.; Keen, D.; Perrin, Y.; Christou, P.; Fischer, R. Cereal crops as viable production and storage systems for pharmaceutical SCFV antibodies. Plant Mol. Biol., 2000, 42(4), 583-590.
[http://dx.doi.org/10.1023/A:1006301519427] [PMID: 10809004]
[10]
Kashima, K.; Yuki, Y.; Mejima, M.; Kurokawa, S.; Suzuki, Y.; Minakawa, S.; Takeyama, N.; Fukuyama, Y.; Azegami, T.; Tanimoto, T.; Kuroda, M.; Tamura, M.; Gomi, Y.; Kiyono, H. Good manufacturing practices production of a purification free oral cholera vaccine expressed in transgenic rice plants. Plant Cell Rep., 2016, 35(3), 667-679.
[http://dx.doi.org/10.1007/s00299-015-1911-9] [PMID: 26661780]
[11]
Merlin, M.; Pezzotti, M.; Avesani, L. Edible plants for oral delivery of biopharmaceuticals. Br. J. Clin. Pharmacol., 2017, 83(1), 71-81.
[http://dx.doi.org/10.1111/bcp.12949] [PMID: 27037892]
[12]
Komarova, T.V.; Baschieri, S.; Donini, M.; Marusic, C.; Benvenuto, E.; Dorokhov, Y.L. Transient expression systems for plant derived biopharmaceuticals. Expert Rev. Vaccines, 2010, 9(8), 859-876.
[http://dx.doi.org/10.1586/erv.10.85] [PMID: 20673010]
[13]
Canto, T. Transient expression systems in plants: Potentialities and constraints. Adv. Exp. Med. Biol., 2016, 896, 287-301.
[http://dx.doi.org/10.1007/978-3-319-27216-0_18] [PMID: 27165332]
[14]
Baltes, N.J.; Gil, H.J.; Voytas, D.F. Genome engineering and agriculture: Opportunities and challenges. Prog. Mol. Biol. Transl. Sci., 2017, 149, 1-26.
[http://dx.doi.org/10.1016/bs.pmbts.2017.03.011] [PMID: 28712492]
[15]
Gleba, Y.; Klimyuk, V.; Marillonnet, S. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol., 2007, 18(2), 134-141.
[http://dx.doi.org/10.1016/j.copbio.2007.03.002] [PMID: 17368018]
[16]
Lico, C.; Chen, Q.; Santi, L. Viral vectors for production of recombinant proteins in plants. J. Cell. Physiol., 2008, 216(2), 366-377.
[http://dx.doi.org/10.1002/jcp.21423] [PMID: 18330886]
[17]
Tusé, D.; Ku, N.; Bendandi, M.; Becerra, C.; Collins, R., Jr; Langford, N.; Sancho, S.I.; López, A.; Pastor, F.; Kandzia, R.; Thieme, F.; Jarczowski, F.; Krause, D.; Ma, J.K.; Pandya, S.; Klimyuk, V.; Gleba, Y.; Butler, J.E. Clinical safety and immunogenicity of tumor targeted, plant made Id KLH conjugate vaccines for follicular lymphoma. BioMed Res. Int., 2015, 2015648143
[http://dx.doi.org/10.1155/2015/648143] [PMID: 26425548]
[18]
Gleba, Y.; Klimyuk, V.; Marillonnet, S. Magnifection a new platform for expressing recombinant vaccines in plants. Vaccine, 2005, 23(17-18), 2042-2048.
[http://dx.doi.org/10.1016/j.vaccine.2005.01.006] [PMID: 15755568]
[19]
Zischewski, J.; Sack, M.; Fischer, R. Overcoming low yields of plant made antibodies by a protein engineering approach. Biotechnol. J., 2016, 11(1), 107-116.
[http://dx.doi.org/10.1002/biot.201500255] [PMID: 26632507]
[20]
Saxena, P.; Thuenemann, E.C.; Sainsbury, F.; Lomonossoff, G.P. Virus derived vectors for the expression of multiple proteins in plants. Methods Mol. Biol., 2016, 1385, 39-54.
[http://dx.doi.org/10.1007/978-1-4939-3289-4_3] [PMID: 26614280]
[21]
Sainsbury, F.; Sack, M.; Stadlmann, J.; Quendler, H.; Fischer, R.; Lomonossoff, G.P. Rapid transient production in plants by replicating and non replicating vectors yields high quality functional anti HIV antibody. PLoS One, 2010, 5(11)e13976
[http://dx.doi.org/10.1371/journal.pone.0013976] [PMID: 21103044]
[22]
Margolin, E.; Chapman, R.; Williamson, A.L.; Rybicki, E.P.; Meyers, A.E. Production of complex viral glycoproteins in plants as vaccine immunogens. Plant Biotechnol. J., 2018, 16(9), 1531-1545.
[http://dx.doi.org/10.1111/pbi.12963] [PMID: 29890031]
[23]
Jin, C.; Altmann, F.; Strasser, R.; Mach, L.; Schähs, M.; Kunert, R.; Rademacher, T.; Glössl, J.; Steinkellner, H. A plant derived human monoclonal antibody induces an anti-carbohydrate immune response in rabbits. Glycobiology, 2008, 18(3), 235-241.
[http://dx.doi.org/10.1093/glycob/cwm137] [PMID: 18203810]
[24]
Bosch, D.; Schots, A. Plant glycans: Friend or foe in vaccine development? In: Expert Review of Vaccines, 2010, 9(8), 835-842.
[http://dx.doi.org/10.1586/erv.10.83] [PMID: 20673008]
[25]
Montero, L.; Steinkellner, H. Advanced plant based glycan engineering. Front. Bioeng. Biotechnol., 2018, 6, 81.
[http://dx.doi.org/10.3389/fbioe.2018.00081] [PMID: 29963553]
[26]
Steinkellner, H.; Castilho, A. N-glyco-engineering in plants: Update on strategies and major achievements; In: Glyco. Engin. Methods Protoc, 2015, pp. 195-212.
[http://dx.doi.org/10.1007/978-1-4939-2760-9_14]
[27]
Marusic, C.; Pioli, C.; Stelter, S.; Novelli, F.; Lonoce, C.; Morrocchi, E.; Benvenuto, E.; Salzano, A.M.; Scaloni, A.; Donini, M. N glycan engineering of a plant produced anti-CD20-hIL-2 immunocytokine significantly enhances its effector functions. Biotechnol. Bioeng., 2018, 115(3), 565-576.
[http://dx.doi.org/10.1002/bit.26503] [PMID: 29178403]
[28]
Qiu, X.; Wong, G.; Audet, J.; Bello, A.; Fernando, L.; Alimonti, J.B.; Fausther-Bovendo, H.; Wei, H.; Aviles, J.; Hiatt, E.; Johnson, A.; Morton, J.; Swope, K.; Bohorov, O.; Bohorova, N.; Goodman, C.; Kim, D.; Pauly, M.H.; Velasco, J.; Pettitt, J.; Olinger, G.G.; Whaley, K.; Xu, B.; Strong, J.E.; Zeitlin, L.; Kobinger, G.P. Reversion of advanced Ebola virus disease in nonhuman primates with Z Mapp. Nature, 2014, 514(7520), 47-53.
[http://dx.doi.org/10.1038/nature13777] [PMID: 25171469]
[29]
Stern, A.M.; Markel, H. The history of vaccines and immunization: Familiar patterns, new challenges. Health Aff., 2005, 24(3), 611-621.
[http://dx.doi.org/10.1377/hlthaff.24.3.611] [PMID: 15886151]
[30]
Kurup, V.M.; Thomas, J. Edible vaccines: Promises and challenges. Mol. Biotechnol., 2020, 62(2), 79-90.
[http://dx.doi.org/10.1007/s12033-019-00222-1] [PMID: 31758488]
[31]
Saxena, J.; Rawat, S. Edible vaccines. Adv. Biotechnol., 2014, 9788132215(1), 207-226.
[http://dx.doi.org/10.1007/978-81-322-1554-7_12]
[32]
Pelosi, A.; Shepherd, R.; Walmsley, A.M. Delivery of plant made vaccines and therapeutics. Biotechnol. Adv., 2012, 30(2), 440-448.
[http://dx.doi.org/10.1016/j.biotechadv.2011.07.018] [PMID: 21843627]
[33]
Kolotilin, I.; Topp, E.; Cox, E.; Devriendt, B.; Conrad, U.; Joensuu, J.; Stöger, E.; Warzecha, H.; McAllister, T.; Potter, A.; McLean, M.D.; Hall, J.C.; Menassa, R. Plant-based solutions for veterinary immunotherapeutics and prophylactics. Vet. Res., 2014, 45, 117.
[http://dx.doi.org/10.1186/s13567-014-0117-4] [PMID: 25559098]
[34]
Shahid, N.; Daniell, H. Plant based oral vaccines against zoonotic and non-zoonotic diseases. Plant Biotechnol. J., 2016, 14(11), 2079-2099.
[http://dx.doi.org/10.1111/pbi.12604] [PMID: 27442628]
[35]
Pasetti, M.F.; Simon, J.K.; Sztein, M.B.; Levine, M.M. Immunology of gut mucosal vaccines. Immunol. Rev., 2011, 239(1), 125-148.
[http://dx.doi.org/10.1111/j.1600-065X.2010.00970.x] [PMID: 21198669]
[36]
Huang, L.; Ikejiri, A.; Shimizu, Y.; Adachi, T.; Goto, Y.; Toyama, J.; Tanaka, H.; Akashi, R.; Uchida, K.; Miyata, H.; Haga, T. Immunoadjuvant activity of crude lectin extracted from Momordica charantia seed. J. Vet. Med. Sci., 2008, 70(5), 533-535.
[http://dx.doi.org/10.1292/jvms.70.533] [PMID: 18525182]
[37]
Petrovsky, N. Novel human polysaccharide adjuvants with dual Th1 and Th2 potentiating activity. Vaccine, 2006, 24(Suppl. 2), 26-29.
[http://dx.doi.org/10.1016/j.vaccine.2005.01.107]
[38]
Sparg, S.G.; Light, M.E.; van Staden, J. Biological activities and distribution of plant saponins. J. Ethnopharmacol., 2004, 94(2-3), 219-243.
[http://dx.doi.org/10.1016/j.jep.2004.05.016] [PMID: 15325725]
[39]
Chaitanya, V.; Kumar, J.U. An overview on edible vaccines: A novel approach to oral immunization. IJRIAS, 2018, 3(8), 1-14.
[40]
Kim, T.G.; Yang, M.S. Current trends in edible vaccine development using transgenic plants. Biotechnol. Bioprocess Eng., 2010, 15(1), 61-65.
[http://dx.doi.org/10.1007/s12257-009-3084-2]
[41]
Hernández, M.; Rosas, G.; Cervantes, J.; Fragoso, G.; Rosales-Mendoza, S.; Sciutto, E. Transgenic plants: A 5-year update on oral antipathogen vaccine development. Expert Rev. Vaccines, 2014, 13(12), 1523-1536.
[http://dx.doi.org/10.1586/14760584.2014.953064] [PMID: 25158836]
[42]
Lamphear, B.J.; Jilka, J.M.; Kesl, L.; Welter, M.; Howard, J.A.; Streatfield, S.J. A corn-based delivery system for animal vaccines: An oral transmissible gastroenteritis virus vaccine boosts lactogenic immunity in swine. Vaccine, 2004, 22(19), 2420-2424.
[http://dx.doi.org/10.1016/j.vaccine.2003.11.066] [PMID: 15193404]
[43]
Sharma, P.; Mondal, H.; Mondal, S.; Majumder, R. Plant-based vaccines: Potentiality against severe acute respiratory syndrome coronavirus 2. Biomed. Biotechnol. Res J., 2021, 5(4), 366-373.
[http://dx.doi.org/10.4103/bbrj.bbrj_185_21]
[44]
Jelaska, S. Mihaljević, S.; Bauer, N. Production of biopharmaceuticals, antibodies and edible vaccines in transgenic plants. Drugs, 2006, 4(5), 121-128.
[45]
Wang, X.; Sherman, A.; Liao, G.; Leong, K.W.; Daniell, H.; Terhorst, C.; Herzog, R.W. Mechanism of oral tolerance induction to therapeutic proteins. Adv. Drug Deliv. Rev., 2013, 65(6), 759-773.
[http://dx.doi.org/10.1016/j.addr.2012.10.013] [PMID: 23123293]
[46]
Khadwal, S.; Singh, R.; Singh, K.; Sharma, V.; Sharma, A.K. Probing into the edible vaccines: Newer paradigms, scope and relevance. Plant Arch., 2020, 20(2), 5483-5495.
[47]
Mason, H.S.; Lam, D.M.K.; Arntzen, C.J. Expression of hepatitis B surface antigen in transgenic plants. Proc. Natl. Acad. Sci. USA, 1992, 89(24), 11745-11749.
[http://dx.doi.org/10.1073/pnas.89.24.11745] [PMID: 1465391]
[48]
Tuboly, T.; Yu, W.; Bailey, A.; Degrandis, S.; Du, S.; Erickson, L.; Nagy, E. Immunogenicity of porcine transmissible gastroenteritis virus spike protein expressed in plants. Vaccine, 2000, 18(19), 2023-2028.
[http://dx.doi.org/10.1016/S0264-410X(99)00525-3] [PMID: 10706964]
[49]
Varsani, A.; Williamson, A.L.; Rose, R.C.; Jaffer, M.; Rybicki, E.P. Expression of human papillomavirus type 16 major capsid protein in transgenic Nicotiana tabacum. Xanthi. Arch. Virol., 2003, 148(9), 1771-1786.
[http://dx.doi.org/10.1007/s00705-003-0119-4] [PMID: 14505089]
[50]
Kohl, T.; Hitzeroth, I.I.; Stewart, D.; Varsani, A.; Govan, V.A.; Christensen, N.D.; Williamson, A.L.; Rybicki, E.P. Plant-produced cottontail rabbit papillomavirus L1 protein protects against tumor challenge: A proof of concept study. Clin. Vaccine Immunol., 2006, 13(8), 845-853.
[http://dx.doi.org/10.1128/CVI.00072-06] [PMID: 16893983]
[51]
Kota, S.; Subramanian, M.; Shanmugaraj, B.M.; Challa, H.; Ponanna, N.M. Subunit vaccine based on plant expressed recombinant Eimeria gametocyte antigen Gam82 elicit protective immune response against chicken coccidiosis. J. Vaccines Vaccin., 2017, 8, 6.
[http://dx.doi.org/10.4172/2157-7560.1000374]
[52]
Pérez Filgueira, D.M.; Zamorano, P.I.; Domínguez, M.G.; Taboga, O.; Del Médico Zajac, M.P.; Puntel, M.; Romera, S.A.; Morris, T.J.; Borca, M.V.; Sadir, A.M. Bovine herpes virus gD protein produced in plants using a recombinant tobacco mosaic virus (TMV) vector possesses authentic antigenicity. Vaccine, 2003, 21(27-30), 4201-4209.
[http://dx.doi.org/10.1016/S0264-410X(03)00495-X] [PMID: 14505899]
[53]
Joensuu, J.J.; Verdonck, F.; Ehrström, A.; Peltola, M.; Siljander-Rasi, H.; Nuutila, A.M.; Oksman, K.M.; Teeri, T.H.; Cox, E.; Goddeeris, B.M.; Niklander, V. F4 (K88) fimbrial adhesin FAEG expressed in alfalfa reduces F4+ enterotoxigenic Escherichia coli excretion in weaned piglets. Vaccine, 2006, 24(13), 2387-2394.
[http://dx.doi.org/10.1016/j.vaccine.2005.11.056] [PMID: 16378664]
[54]
Peréz Aguirreburualde, M.S.; Gómez, M.C.; Ostachuk, A.; Wolman, F.; Albanesi, G.; Pecora, A.; Odeon, A.; Ardila, F.; Escribano, J.M.; Dus Santos, M.J.; Wigdorovitz, A. Efficacy of a BVDV subunit vaccine produced in alfalfa transgenic plants. Vet. Immunol. Immunopathol., 2013, 151(3-4), 315-324.
[http://dx.doi.org/10.1016/j.vetimm.2012.12.004] [PMID: 23291101]
[55]
Huang, Z.; LePore, K.; Elkin, G.; Thanavala, Y.; Mason, H.S. High yield rapid production of hepatitis B surface antigen in plant leaf by a viral expression system. Plant Biotechnol. J., 2008, 6(2), 202-209.
[http://dx.doi.org/10.1111/j.1467-7652.2007.00316.x]
[56]
D’Aoust, M.A.; Lavoie, P.O.; Couture, M.M.J.; Trépanier, S.; Guay, J.M.; Dargis, M.; Mongrand, S.; Landry, N.; Ward, B.J.; Vézina, L.P. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J., 2008, 6(9), 930-940.
[http://dx.doi.org/10.1111/j.1467-7652.2008.00384.x] [PMID: 19076615]
[57]
Santi, L.; Batchelor, L.; Huang, Z.; Hjelm, B.; Kilbourne, J.; Arntzen, C.J.; Chen, Q.; Mason, H.S. An efficient plant viral expression system generating orally immunogenic Norwalk virus like particles. Vaccine, 2008, 26(15), 1846-1854.
[http://dx.doi.org/10.1016/j.vaccine.2008.01.053] [PMID: 18325641]
[58]
Kalthoff, D.; Giritch, A.; Geisler, K.; Bettmann, U.; Klimyuk, V.; Hehnen, H.R.; Gleba, Y.; Beer, M. Immunization with plant expressed hemagglutinin protects chickens from lethal highly pathogenic avian influenza virus H5N1 challenge infection. J. Virol., 2010, 84(22), 12002-12010.
[http://dx.doi.org/10.1128/JVI.00940-10] [PMID: 20810729]
[59]
Shoji, Y.; Farrance, C.E.; Bautista, J.; Bi, H.; Musiychuk, K.; Horsey, A.; Park, H.; Jaje, J.; Green, B.J.; Shamloul, M.; Sharma, S.; Chichester, J.A.; Mett, V.; Yusibov, V. A plant based system for rapid production of influenza vaccine antigens. Influenza Respir. Viruses, 2012, 6(3), 204-210.
[http://dx.doi.org/10.1111/j.1750-2659.2011.00295.x] [PMID: 21974811]
[60]
Kanagarajan, S.; Tolf, C.; Lundgren, A.; Waldenström, J.; Brodelius, P.E. Transient expression of hemagglutinin antigen from low pathogenic avian influenza A (H7N7) in Nicotiana benthamiana. PLoS One, 2012, 7(3)e33010
[http://dx.doi.org/10.1371/journal.pone.0033010] [PMID: 22442675]
[61]
Gómez, E.; Lucero, M.S.; Chimeno Zoth, S.; Carballeda, J.M.; Gravisaco, M.J.; Berinstein, A. Transient expression of VP2 in Nicotiana benthamiana and its use as a plant based vaccine against infectious bursal disease virus. Vaccine, 2013, 31(23), 2623-2627.
[http://dx.doi.org/10.1016/j.vaccine.2013.03.064] [PMID: 23583894]
[62]
Thuenemann, E.C.; Meyers, A.E.; Verwey, J.; Rybicki, E.P.; Lomonossoff, G.P. A method for rapid production of heteromultimeric protein complexes in plants: Assembly of protective bluetongue virus like particles. Plant Biotechnol. J., 2013, 11(7), 839-846.
[http://dx.doi.org/10.1111/pbi.12076] [PMID: 23647743]
[63]
Mathew, L.G.; Herbst-Kralovetz, M.M.; Mason, H.S. Norovirus Narita 104 virus like particles expressed in Nicotiana benthamiana induce serum and mucosal immune responses. BioMed Res. Int., 2014, 2014807539
[http://dx.doi.org/10.1155/2014/807539] [PMID: 24949472]
[64]
Mbewana, S.; Mortimer, E.; Pêra, F.F.P.G.; Hitzeroth, I.I.; Rybicki, E.P. Production of H5N1 influenza virus matrix protein 2 ectodomain protein bodies in tobacco plants and in insect cells as a candidate universal influenza vaccine. Front. Bioeng. Biotechnol., 2015, 3, 197.
[http://dx.doi.org/10.3389/fbioe.2015.00197] [PMID: 26697423]
[65]
Kim, M.Y.; Jang, Y.S.; Yang, M.S.; Kim, T.G. High expression of consensus dengue virus envelope glycoprotein domain III using a viral expression system in tobacco. Plant Cell Tissue Organ Cult., 2015, 122(2), 445-451.
[http://dx.doi.org/10.1007/s11240-015-0781-8]
[66]
Marsian, J.; Fox, H.; Bahar, M.W.; Kotecha, A.; Fry, E.E.; Stuart, D.I.; Macadam, A.J.; Rowlands, D.J.; Lomonossoff, G.P. Plant made polio type 3 stabilized VLPSA candidate synthetic polio vaccine. Nat. Commun., 2017, 8(1), 245.
[http://dx.doi.org/10.1038/s41467-017-00090-w] [PMID: 28811473]
[67]
Iyappan, G.; Shanmugaraj, B.M.; Inchakalody, V.; Ma, J.K-C.; Ramalingam, S. Potential of plant biologics to tackle the epidemic like situations case studies involving viral and bacterial candidates. Int. J. Infect. Dis., 2018, 73, 363.
[http://dx.doi.org/10.1016/j.ijid.2018.04.4236]
[68]
Yang, M.; Sun, H.; Lai, H.; Hurtado, J.; Chen, Q. Plant produced Zika virus envelope protein elicits neutralizing immune responses that correlate with protective immunity against Zika virus in mice. Plant Biotechnol. J., 2018, 16(2), 572-580.
[http://dx.doi.org/10.1111/pbi.12796] [PMID: 28710796]
[69]
Gunter, C.J.; Regnard, G.L.; Rybicki, E.P.; Hitzeroth, I.I. Immunogenicity of plant-produced porcine circovirus like particles in mice. Plant Biotechnol. J., 2019, 17(9), 1751-1759.
[http://dx.doi.org/10.1111/pbi.13097] [PMID: 30791210]
[70]
Margolin, E.; Chapman, R.; Meyers, A.E.; van Diepen, M.T.; Ximba, P.; Hermanus, T. Production and immunogenicity of soluble plant produced HIV-1 subtype C envelope gp140 immunogens. Front. Plant Sci., 2019, 10, 1-13.
[71]
Smith, T.; O’Kennedy, M.M.; Wandrag, D.B.R.; Adeyemi, M.; Abolnik, C. Efficacy of a plant produced virus like particle vaccine in chickens challenged with Influenza A H6N2 virus. Plant Biotechnol. J., 2020, 18(2), 502-512.
[http://dx.doi.org/10.1111/pbi.13219] [PMID: 31350931]
[72]
Castañón, S.; Marín, M.S.; Martín, J.M.; Boga, J.A.; Casais, R.; Humara, J.M.; Ordás, R.J.; Parra, F. Immunization with potato plants expressing VP60 protein protects against rabbit hemorrhagic disease virus. J. Virol., 1999, 73(5), 4452-4455.
[http://dx.doi.org/10.1128/JVI.73.5.4452-4455.1999] [PMID: 10196345]
[73]
Zhou, J.Y.; Cheng, L.Q.; Zheng, X.J.; Wu, J.X.; Shang, S.B.; Wang, J.Y.; Chen, J.G. Generation of the transgenic potato expressing full length spike protein of infectious bronchitis virus. J. Biotechnol., 2004, 111(2), 121-130.
[http://dx.doi.org/10.1016/j.jbiotec.2004.03.012] [PMID: 15219399]
[74]
Thanavala, Y.; Mahoney, M.; Pal, S.; Scott, A.; Richter, L.; Natarajan, N.; Goodwin, P.; Arntzen, C.J.; Mason, H.S. Immunogenicity in humans of an edible vaccine for hepatitis B. Proc. Natl. Acad. Sci. USA, 2005, 102(9), 3378-3382.
[http://dx.doi.org/10.1073/pnas.0409899102] [PMID: 15728371]
[75]
Koya, V.; Moayeri, M.; Leppla, S.H.; Daniell, H. Plant-based vaccine: mice immunized with chloroplast derived anthrax protective antigen survive anthrax lethal toxin challenge. Infect. Immun., 2005, 73(12), 8266-8274.
[http://dx.doi.org/10.1128/IAI.73.12.8266-8274.2005] [PMID: 16299323]
[76]
Scotti, N.; Alagna, F.; Ferraiolo, E.; Formisano, G.; Sannino, L.; Buonaguro, L.; De Stradis, A.; Vitale, A.; Monti, L.; Grillo, S.; Buonaguro, F.M.; Cardi, T. High-level expression of the HIV-1 Pr55gag polyprotein in transgenic tobacco chloroplasts. Planta, 2009, 229(5), 1109-1122.
[http://dx.doi.org/10.1007/s00425-009-0898-2] [PMID: 19234717]
[77]
Gottschamel, J.; Lössl, A.; Ruf, S.; Wang, Y.; Skaugen, M.; Bock, R.; Clarke, J.L. Production of dengue virus envelope protein domain III-based antigens in tobacco chloroplasts using inducible and constitutive expression systems. Plant Mol. Biol., 2016, 91(4-5), 497-512.
[http://dx.doi.org/10.1007/s11103-016-0484-5] [PMID: 27116001]
[78]
Guerrero, O.; Loza, E.; Olivera, T.; Fehérvári, T.; Gómez, M.A. Expression of the Newcastle disease virus fusion protein in transgenic maize and immunological studies. Transgenic Res., 2006, 15(4), 455-463.
[http://dx.doi.org/10.1007/s11248-006-0017-0] [PMID: 16906446]
[79]
Tacket, C.O.; Mason, H.S.; Losonsky, G.; Clements, J.D.; Levine, M.M.; Arntzen, C.J. Immunogenicity in humans of a recombinant bacterial antigen delivered in a transgenic potato. Nat. Med., 1998, 4(5), 607-609.
[http://dx.doi.org/10.1038/nm0598-607] [PMID: 9585236]
[80]
Bhatia, S.; Dahiya, R. Plant based biotechnological products with their production host, modes of delivery systems, and stability testing. In: Modern Applications of Plant Biotechnology in Pharmaceutical Sciences; Elsevier: Amsterdam, 2015, pp. 293-331.
[http://dx.doi.org/10.1016/B978-0-12-802221-4.00008-X]
[81]
Grilo, A.L.; Mantalaris, A. The increasingly human and profitable monoclonal antibody market. Trends Biotechnol., 2019, 37(1), 9-16.
[http://dx.doi.org/10.1016/j.tibtech.2018.05.014] [PMID: 29945725]
[82]
Donini, M.; Marusic, C. Current state of the art in plant based antibody production systems. Biotechnol. Lett., 2019, 41(3), 335-346.
[http://dx.doi.org/10.1007/s10529-019-02651-z] [PMID: 30684155]
[83]
Ecker, D.M.; Jones, S.D.; Levine, H.L. The therapeutic monoclonal antibody market. MAbs, 2015, 7(1), 9-14.
[http://dx.doi.org/10.4161/19420862.2015.989042] [PMID: 25529996]
[84]
Chen, Q.; Davis, K.R. The potential of plants as a system for the development and production of human biologics. F1000 Res., 2016, 5, F1000.
[http://dx.doi.org/10.12688/f1000research.8010.1]
[85]
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(8), 1094-1105.
[http://dx.doi.org/10.1111/pbi.12438] [PMID: 26214282]
[86]
Mir, P.; Twyman, R.M.; Alvarez, D.; Cerda Bennasser, P.; Balcells, M.; Christou, P.; Capell, T. A simplified techno economic model for the molecular pharming of antibodies. Biotechnol. Bioeng., 2019, 116(10), 2526-2539.
[http://dx.doi.org/10.1002/bit.27093] [PMID: 31209856]
[87]
Alam, A.; Jiang, L.; Kittleson, G.A.; Steadman, K.D.; Nandi, S.; Fuqua, J.L.; Palmer, K.E.; Tusé, D.; McDonald, K.A. Technoeconomic modeling of plant based griffithsin manufacturing. Front. Bioeng. Biotechnol., 2018, 6, 102.
[http://dx.doi.org/10.3389/fbioe.2018.00102] [PMID: 30087892]
[88]
Nandi, S.; Kwong, A.T.; Holtz, B.R.; Erwin, R.L.; Marcel, S.; McDonald, K.A. Techno-economic analysis of a transient plant-based platform for monoclonal antibody production. MAbs, 2016, 8(8), 1456-1466.
[http://dx.doi.org/10.1080/19420862.2016.1227901] [PMID: 27559626]
[89]
Bouquin, T.; Thomsen, M.; Nielsen, L.K.; Green, T.H.; Mundy, J.; Dziegiel, M.H. Human anti rhesus D IgG1 antibody produced in transgenic plants. Trans. Res., 2002, 11(2), 115-122.
[http://dx.doi.org/10.1023/A:1015226418688] [PMID: 12054345]
[90]
Zeitlin, L.; Olmsted, S.S.; Moench, T.R.; Co, M.S.; Martinell, B.J.; Paradkar, V.M.; Russell, D.R.; Queen, C.; Cone, R.A.; Whaley, K.J. A humanized monoclonal antibody produced in transgenic plants for immunoprotection of the vagina against genital herpes. Nat. Biotechnol., 1998, 16(13), 1361-1364.
[http://dx.doi.org/10.1038/4344] [PMID: 9853620]
[91]
Ma, J.K-C.J.; Drossard, J.; Lewis, D.; Altmann, F.; Boyle, J.; Christou, P.; Cole, T.; Dale, P.; van Dolleweerd, C.J.; Isitt, V.; Katinger, D.; Lobedan, M.; Mertens, H.; Paul, M.J.; Rademacher, T.; Sack, M.; Hundleby, P.A.; Stiegler, G.; Stoger, E.; Twyman, R.M.; Vcelar, B.; Fischer, R. 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.
[http://dx.doi.org/10.1111/pbi.12416] [PMID: 26147010]
[92]
Tripathy, S.; Dassarma, B.; Bhattacharya, M.; Matsabisa, M.G. Plant-based vaccine research development against viral diseases with emphasis on Ebola virus disease: A review study. Curr. Opin. Pharmacol., 2021, 60, 261-267.
[http://dx.doi.org/10.1016/j.coph.2021.08.001] [PMID: 34481336]
[93]
Nochi, T.; Yuki, Y.; Katakai, Y.; Shibata, H.; Tokuhara, D.; Mejima, M.; Kurokawa, S.; Takahashi, Y.; Nakanishi, U.; Ono, F.; Mimuro, H.; Sasakawa, C.; Takaiwa, F.; Terao, K.; Kiyono, H. A rice based oral cholera vaccine induces macaque-specific systemic neutralizing antibodies but does not influence pre-existing intestinal immunity. J. Immunol., 2009, 183(10), 6538-6544.
[http://dx.doi.org/10.4049/jimmunol.0901480] [PMID: 19880451]
[94]
Corthésy, B. Multi-faceted functions of secretory IgA at mucosal surfaces. Front. Immunol., 2013, 4(7), 185.
[http://dx.doi.org/10.3389/fimmu.2013.00185] [PMID: 23874333]
[95]
Juarez, P.; Virdi, V.; Depicker, A.; Orzaez, D. Biomanufacturing of protective antibodies and other therapeutics in edible plant tissues for oral applications. Plant Biotechnol. J., 2016, 14(9), 1791-1799.
[http://dx.doi.org/10.1111/pbi.12541] [PMID: 26873071]
[96]
Komarova, T.V.; Sheshukova, E.V.; Dorokhov, Y.L. Plant made antibodies: Properties and therapeutic applications. Curr. Med. Chem., 2019, 26(3), 381-395.
[http://dx.doi.org/10.2174/0929867325666171212093257] [PMID: 29231134]
[97]
Virdi, V.; Coddens, A.; De Buck, S.; Millet, S.; Goddeeris, B.M.; 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. USA, 2013, 110(29), 11809-11814.
[http://dx.doi.org/10.1073/pnas.1301975110] [PMID: 23801763]
[98]
Paul, M.; Reljic, R.; Klein, K.; Drake, P.M.W.; van Dolleweerd, C.; Pabst, M.; Windwarder, M.; Arcalis, E.; Stoger, E.; Altmann, F.; Cosgrove, C.; Bartolf, A.; Baden, S.; Ma, J.K. Characterization of a plant produced recombinant human secretory IgA with broad neutralizing activity against HIV. MAbs, 2014, 6(6), 1585-1597.
[http://dx.doi.org/10.4161/mabs.36336] [PMID: 25484063]
[99]
Ramessar, K.; Rademacher, T.; Sack, M.; Stadlmann, J.; Platis, D.; Stiegler, G.; Labrou, N.; Altmann, F.; Ma, J.; Stöger, E.; Capell, T.; Christou, P. Cost-effective production of a vaginal protein microbicide to prevent HIV transmission. Proc. Natl. Acad. Sci. USA, 2008, 105(10), 3727-3732.
[http://dx.doi.org/10.1073/pnas.0708841104] [PMID: 18316741]
[100]
Davey, R.T., Jr; Dodd, L.; Proschan, M.A.; Neaton, J.; Neuhaus Nordwall, J.; Koopmeiners, J.S.; Beigel, J.; Tierney, J.; Lane, H.C.; Fauci, A.S.; Massaquoi, M.B.F.; Sahr, F.; Malvy, D. A randomized, controlled trial of ZMapp for ebola virus infection. N. Engl. J. Med., 2016, 375(15), 1448-1456.
[http://dx.doi.org/10.1056/NEJMoa1604330] [PMID: 27732819]
[101]
Weintraub, J.A.; Hilton, J.F.; White, J.M.; Hoover, C.I.; Wycoff, K.L.; Yu, L.; Larrick, J.W.; Featherstone, J.D. Clinical trial of a plant derived antibody on recolonization of mutans streptococci. Caries Res., 2005, 39(3), 241-250.
[http://dx.doi.org/10.1159/000084805] [PMID: 15914988]
[102]
Gavilondo, J.V.; Larrick, J.W. Antibody engineering at the millennium. Biotechniques, 2000, 29(1), 128-132.
[http://dx.doi.org/10.2144/00291ov01] [PMID: 10907088]
[103]
Kesik, M. Progress in biopharmaceutical development. Biotechnol. Appl. Biochem., 2018, 65(3), 306-322.
[http://dx.doi.org/10.1002/bab.1617] [PMID: 28972297]
[104]
Yao, J.; Weng, Y.; Dickey, A.; Wang, K.Y. Plants as factories for human pharmaceuticals: Applications and challenges. Int. J. Mol. Sci., 2015, 16(12), 28549-28565.
[http://dx.doi.org/10.3390/ijms161226122] [PMID: 26633378]
[105]
Tekoah, Y.; Shulman, A.; Kizhner, T.; Ruderfer, I.; Fux, L.; Nataf, Y.; Bartfeld, D.; Ariel, T.; Gingis, S.; Hanania, U.; Shaaltiel, Y. Large scale production of pharmaceutical proteins in plant cell culture the Protalix experience. Plant Biotechnol. J., 2015, 13(8), 1199-1208.
[http://dx.doi.org/10.1111/pbi.12428] [PMID: 26102075]
[106]
Dumont, J.; Euwart, D.; Mei, B.; Estes, S.; Kshirsagar, R. Human cell lines for biopharmaceutical manufacturing: History, status, and future perspectives. Crit. Rev. Biotechnol., 2016, 36(6), 1110-1122.
[http://dx.doi.org/10.3109/07388551.2015.1084266] [PMID: 26383226]
[107]
RxList. Elelyso. Available from: https://www.rxlist.com/elelyso-drug.htm (Accessed on: 31 December 2021).
[108]
Ou, J.; Guo, Z.; Shi, J.; Wang, X.; Liu, J.; Shi, B.; Guo, F.; Zhang, C.; Yang, D. Transgenic rice endosperm as a bioreactor for molecular pharming. Plant Cell Rep., 2014, 33(4), 585-594.
[http://dx.doi.org/10.1007/s00299-013-1559-2] [PMID: 24413763]
[109]
Giddings, G.; Allison, G.; Brooks, D.; Carter, A. Transgenic plants as factories for biopharmaceuticals. Nat. Biotechnol., 2000, 18(11), 1151-1155.
[http://dx.doi.org/10.1038/81132] [PMID: 11062432]
[110]
Goldstein, D.A.; Thomas, J.A. Biopharmaceuticals derived from genetically modified plants. Int. J. Med., 2004, 97(11), 705-716.
[http://dx.doi.org/10.1093/qjmed/hch121] [PMID: 15496527]
[111]
Sharifi Tabar, M.; Habashi, A.A.; Rajabi Memari, H. Human granulocyte colony stimulating factor (hG-CSF) expression in plastids of Lactuca sativa. Iran. Biomed. J., 2013, 17(3), 158-164.
[http://dx.doi.org/10.6091/IBJ.1180.2013] [PMID: 23748895]
[112]
Urreta, I.; Casta, S. Transgenic plants as biofactories for the production of biopharmaceuticals: A case study of human placental lactogen.In: Transgenic Plants - Advances and Limitations; IntechOpen: Spain, 2012, pp. 305-328.
[http://dx.doi.org/10.5772/31515]
[113]
Urreta, I.; Oyanguren, I.; Castañón, S. Tobacco as biofactory for biologically active hPL production: A human hormone with potential applications in type-1 diabetes. Trans. Res., 2011, 20(4), 721-733.
[http://dx.doi.org/10.1007/s11248-010-9452-z] [PMID: 20960057]
[114]
Vandekerckhove, J.; Van Damme, J.; Van Lijsebettens, M.; Botterman, J.; De Block, M.; Vandewiele, M. Enkephalins produced in transgenic plants using modified 2S seed storage proteins. Biotechnology, 1989, 7(9), 929-932.
[http://dx.doi.org/10.1038/nbt0989-929]
[115]
Goddijn, O.; Pen, J. Plants as bioreactors. Trends Biotechnol., 1995, 13(9), 379-387.
[http://dx.doi.org/10.1016/S0167-7799(00)88985-4]
[116]
Sijmons, P.C.; Dekker, B.M.; Schrammeijer, B.; Verwoerd, T.C.; van den Elzen, P.J.; Hoekema, A. Production of correctly processed human serum albumin in transgenic plants. Biotechnology, 1990, 8(3), 217-221.
[http://dx.doi.org/10.1038/nbt0390-217] [PMID: 1366404]
[117]
Cramer, C.; Weissenborn, D. Bioproduction of human enzymes in transgenic tobacco. Ann. Acad. Sci., 1996, 792, 62-71.
[http://dx.doi.org/10.1111/j.1749-6632.1996.tb32492.x]
[118]
Cramer, C.L.; Boothe, J.G.; Oishi, K.K. Transgenic plants for therapeutic proteins: Linking upstream and downstream strategies. Curr. Top. Microbiol. Immunol., 1999, 240, 95-118.
[http://dx.doi.org/10.1007/978-3-642-60234-4_5] [PMID: 10394717]
[119]
Halling, B.; Nors Nielsen, S.; Lanzky, P.F.; Ingerslev, F.; Holten, H.C.; Jørgensen, S.E. Occurrence, fate and effects of pharmaceutical substances in the environment- A review. Chemosphere, 1998, 36(2), 357-393.
[http://dx.doi.org/10.1016/S0045-6535(97)00354-8] [PMID: 9569937]
[120]
Hamamoto, H.; Sugiyama, Y.; Nakagawa, N.; Hashida, E.; Matsunaga, Y.; Takemoto, S.; Watanabe, Y.; Okada, Y. A new tobacco mosaic virus vector and its use for the systemic production of angiotensin-I-converting enzyme inhibitor in transgenic tobacco and tomato. Biotechnology, 1993, 11(8), 930-932.
[http://dx.doi.org/10.1038/nbt0893-930] [PMID: 7763916]
[121]
Zhong, G.Y.; Peterson, D.; Delaney, D.E.; Bailey, M.; Witcher, D.R.; Register, J.C. Commercial production of aprotinin in transgenic maize seeds. Mol. Breed., 1999, 5(4), 345-356.
[http://dx.doi.org/10.1023/A:1009677809492]
[122]
Burkhardt, P.K.; Beyer, P.; Wünn, J.; Klöti, A.; Armstrong, G.A.; Schledz, M.; von Lintig, J.; Potrykus, I. Transgenic rice (Oryza sativa) endosperm expressing daffodil (Narcissus pseudonarcissus) phytoene synthase accumulates phytoene, a key intermediate of provitamin A biosynthesis. Plant J., 1997, 11(5), 1071-1078.
[http://dx.doi.org/10.1046/j.1365-313X.1997.11051071.x] [PMID: 9193076]
[123]
Rybicki, E.P. Plant made vaccines for humans and animals. Plant Biotechnol. J., 2010, 8(5), 620-637.
[http://dx.doi.org/10.1111/j.1467-7652.2010.00507.x] [PMID: 20233333]
[124]
Yusibov, V.; Kushnir, N.; Streatfield, S.J. Advances and challenges in the development and production of effective plant based influenza vaccines. Expert Rev. Vaccines, 2015, 14(4), 519-535.
[http://dx.doi.org/10.1586/14760584.2015.989988] [PMID: 25487788]
[125]
Shaaltiel, Y.; Bartfeld, D.; Hashmueli, S.; Baum, G.; Brill, E.; Galili, G.; Dym, O.; Boldin-Adamsky, S.A.; Silman, I.; Sussman, J.L.; Futerman, A.H.; Aviezer, D. Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher’s disease using a plant cell system. Plant Biotechnol. J., 2007, 5(5), 579-590.
[http://dx.doi.org/10.1111/j.1467-7652.2007.00263.x] [PMID: 17524049]
[126]
Traynor, K. Taliglucerase alfa approved for Gaucher disease. Am. J. Health Syst. Pharm., 2012, 69(12), 1009.
[http://dx.doi.org/10.2146/news120041] [PMID: 22644968]

Rights & Permissions Print Cite
Article Metrics
1
© 2024 Bentham Science Publishers | Privacy Policy