Seeds as Economical Production Platform for Recombinant Proteins

Author(s): Muhammad Sarwar Khan*, Faiz Ahmad Joyia, Ghulam Mustafa.

Journal Name: Protein & Peptide Letters

Volume 27 , Issue 2 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

The cost-effective production of high-quality and biologically active recombinant molecules especially proteins is extremely desirable. Seed-based recombinant protein production platforms are considered as superior choice owing to lack of human/animal pathogenic organisms, lack of cold chain requirements for transportation and long-term storage, easy scalability and development of edible biopharmaceuticals in plants with objective to be used in purified or partially processed form is desirable. This review article summarizes the exceptional features of seed-based biopharming and highlights the needs of exploiting it for commercial purposes. Plant seeds offer a perfect production platform for high-value molecules of industrial as well as therapeutic nature owing to lower water contents, high protein storage capacity, weak protease activity and long-term storage ability at ambient temperature. Exploiting extraordinarily high protein accumulation potential, vaccine antigens, antibodies and other therapeutic proteins can be stored without effecting their stability and functionality up to years in seeds. Moreover, ability of direct oral consumption and post-harvest stabilizing effect of seeds offer unique feature of oral delivery of pharmaceutical proteins and vaccine antigens for immunization and disease treatment through mucosal as well as oral route.

Keywords: Seed, biopharming, protein storage vacuoles, targeting, seed-specific promoters, therapeutic proteins.

[1]
Gecchele, E.; Merlin, M.; Brozzetti, A.; Falorni, A.; Pezzotti, M.; Avesani, L. A comparative analysis of recombinant protein expression in different biofactories: Bacteria, insect cells and plant systems. J. Vis. Exp., 2015, 97(97) e52459
[http://dx.doi.org/10.3791/52459] [PMID: 25867956]
[2]
Boothe, J.; Nykiforuk, C.; Shen, Y.; Zaplachinski, S.; Szarka, S.; Kuhlman, P.; Murray, E.; Morck, D.; Moloney, M.M. Seed-based expression systems for plant molecular farming. Plant Biotechnol. J., 2010, 8(5), 588-606.
[http://dx.doi.org/10.1111/j.1467-7652.2010.00511.x] [PMID: 20500681]
[3]
Khan, I.; Twyman, R.M.; Arcalis, E.; Stoger, E. Using storage organelles for the accumulation and encapsulation of recombinant proteins. Biotechnol. J., 2012, 7(9), 1099-1108.
[http://dx.doi.org/10.1002/biot.201100089] [PMID: 22396218]
[4]
Sack, M.; Hofbauer, A.; Fischer, R.; Stoger, E. The increasing value of plant-made proteins. Curr. Opin. Biotechnol., 2015, 32, 163-170.
[http://dx.doi.org/10.1016/j.copbio.2014.12.008] [PMID: 25578557]
[5]
Jozala, A.F.; Geraldes, D.C.; Tundisi, L.L.; Feitosa, V.A.; Breyer, C.A.; Cardoso, S.L.; Mazzola, P.G.; Oliveira-Nascimento, L.; Rangel-Yagui, C.O.; Magalhães, P.O.; Oliveira, M.A.; Pessoa, A., Jr Biopharmaceuticals from microorganisms: From production to purification. Braz. J. Microbiol., 2016, 47(Suppl. 1), 51-63.
[http://dx.doi.org/10.1016/j.bjm.2016.10.007] [PMID: 27838289]
[6]
Demain, A.L.; Vaishnav, P. Production of recombinant proteins by microbes and higher organisms. Biotechnol. Adv., 2009, 27(3), 297-306.
[http://dx.doi.org/10.1016/j.biotechadv.2009.01.008] [PMID: 19500547]
[7]
Ferrer-Miralles, N.; Domingo-Espín, J.; Corchero, J.L.; Vázquez, E.; Villaverde, A. Microbial factories for recombinant pharmaceuticals. Microb. Cell Fact., 2009, 8, 17.
[http://dx.doi.org/10.1186/1475-2859-8-17] [PMID: 19317892]
[8]
Svahn, K.S.; Chryssanthou, E.; Olsen, B.; Bohlin, L.; Göransson, U. Penicillium nalgiovense Laxa isolated from Antarctica is a new source of the antifungal metabolite amphotericin B. Fungal Biol. Biotechnol., 2015, 2, 1.
[http://dx.doi.org/10.1186/s40694-014-0011-x] [PMID: 28955453]
[9]
Wurm, F.M. Production of recombinant protein therapeutics in cultivated mammalian cells. Nat. Biotechnol., 2004, 22(11), 1393-1398.
[http://dx.doi.org/10.1038/nbt1026] [PMID: 15529164]
[10]
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]
[11]
Dyck, M.K.; Lacroix, D.; Pothier, F.; Sirard, M.A. Making recombinant proteins in animals--different systems, different applications. Trends Biotechnol., 2003, 21(9), 394-399.
[http://dx.doi.org/10.1016/S0167-7799(03)00190-2] [PMID: 12948672]
[12]
Bertolini, L.R.; Meade, H.; Lazzarotto, C.R.; Martins, L.T.; Tavares, K.C.; Bertolini, M.; Murray, J.D. The transgenic animal platform for biopharmaceutical production. Transgenic Res., 2016, 25(3), 329-343.
[http://dx.doi.org/10.1007/s11248-016-9933-9] [PMID: 26820414]
[13]
Harvey, A.J.; Speksnijder, G.; Baugh, L.R.; Morris, J.A.; Ivarie, R. Expression of exogenous protein in the egg white of transgenic chickens. Nat. Biotechnol., 2002, 20(4), 396-399.
[http://dx.doi.org/10.1038/nbt0402-396] [PMID: 11923848]
[14]
Faye, L.; Gomord, V. Recombinant proteins from plants Methods and Protocols; Humana Press: New York, USA, 2009.
[http://dx.doi.org/10.1007/978-1-59745-407-0]
[15]
Daniell, H.; Khan, M.S.; Allison, L. Milestones in chloroplast genetic engineering: An environmentally friendly era in biotechnology. Trends Plant Sci., 2002, 7(2), 84-91.
[http://dx.doi.org/10.1016/S1360-1385(01)02193-8] [PMID: 11832280]
[16]
Reggi, S.; Marchetti, S.; Patti, T.; De Amicis, F.; Cariati, R.; Bembi, B.; Fogher, C. Recombinant human acid beta-glucosidase stored in tobacco seed is stable, active and taken up by human fibroblasts. Plant Mol. Biol., 2005, 57(1), 101-113.
[http://dx.doi.org/10.1007/s11103-004-6832-x] [PMID: 15821871]
[17]
Khan, M.S.; Khan, I.A. Biopharming: A biosecurity measure to combat newcastle disease for household food security. Biosafety (Los Angel.), 2015, 4e156
[http://dx.doi.org/10.4172/2167-0331.1000e156]
[18]
Fischer, R.; Stoger, E.; Schillberg, S.; Christou, P.; Twyman, R.M. Plant-based production of biopharmaceuticals. Curr. Opin. Plant Biol., 2004, 7(2), 152-158.
[http://dx.doi.org/10.1016/j.pbi.2004.01.007] [PMID: 15003215]
[19]
Sheludko, Y.V.; Sindarovska, Y.R.; Gerasymenko, I.M.; Bannikova, M.A.; Kuchuk, N.V. Comparison of several Nicotiana species as hosts for high-scale Agrobacterium-mediated transient expression. Biotechnol. Bioeng., 2007, 96(3), 608-614.
[http://dx.doi.org/10.1002/bit.21075] [PMID: 16983697]
[20]
Wydro, M.; Kozubek, E.; Lehmann, P. Optimization of transient Agrobacterium-mediated gene expression system in leaves of Nicotiana benthamiana. Acta Biochim. Pol., 2006, 53(2), 289-298.
[PMID: 16582986]
[21]
Sainsbury, F.; Lomonossoff, G.P. Transient expressions of synthetic biology in plants. Curr. Opin. Plant Biol., 2014, 19, 1-7.
[http://dx.doi.org/10.1016/j.pbi.2014.02.003] [PMID: 24631883]
[22]
Cañizares, M.C.; Nicholson, L.; Lomonossoff, G.P. Use of viral vectors for vaccine production in plants. Immunol. Cell Biol., 2005, 83(3), 263-270.
[http://dx.doi.org/10.1111/j.1440-1711.2005.01339.x] [PMID: 15877604]
[23]
Lomonossoff, G.P. Antigen Delivery Systems: Use of Recombinant Plant Viruses. In: Mucosal Immunology; Mestecky, J.; Bienenstock, J.; Lamm, M.E.; Mayer, L.; McGhee, J.R.; Strober, W., Eds.; Elsevier: Amsterdam, 2005; pp. 1061-1072.
[24]
Porta, C.; Lomonossoff, G.P. Viruses as vectors for the expression of foreign sequences in plants. Biotechnol. Genet. Eng. Rev., 2002, 19, 245-291.
[http://dx.doi.org/10.1080/02648725.2002.10648031] [PMID: 12520880]
[25]
Gleba, Y.; Marillonnet, S.; Klimyuk, V. Engineering viral expression vectors for plants: the ‘full virus’ and the ‘deconstructed virus’ strategies. Curr. Opin. Plant Biol., 2004, 7(2), 182-188.
[http://dx.doi.org/10.1016/j.pbi.2004.01.003] [PMID: 15003219]
[26]
Cañizares, M.C.; Liu, L.; Perrin, Y.; Tsakiris, E.; Lomonossoff, G.P. A bipartite system for the constitutive and inducible expression of high levels of foreign proteins in plants. Plant Biotechnol. J., 2006, 4(2), 183-193.
[http://dx.doi.org/10.1111/j.1467-7652.2005.00170.x] [PMID: 17177795]
[27]
Yusibov, V.; Rabindran, S.; Commandeur, U.; Twyman, R.M.; Fischer, R. The potential of plant virus vectors for vaccine production. Drugs R&D., 2006, 7(4), 203-217.
[http://dx.doi.org/10.2165/00126839-200607040-00001] [PMID: 16784246]
[28]
Alamillo, J.M.; Monger, W.; Sola, I.; García, B.; Perrin, Y.; Bestagno, M.; Burrone, O.R.; Sabella, P.; Plana-Durán, J.; Enjuanes, L.; Lomonossoff, G.P.; García, J.A. Use of virus vectors for the expression in plants of active full-length and single chain anti-coronavirus antibodies. Biotechnol. J., 2006, 1(10), 1103-1111.
[http://dx.doi.org/10.1002/biot.200600143] [PMID: 17004304]
[29]
Kapila, J.; De Rycke, R.; Van Montagu, M.; Angenon, G. An Agrobacterium mediated transient gene expression system for intact leaves. Plant Sci., 1997, 122, 101-108.
[http://dx.doi.org/10.1016/S0168-9452(96)04541-4]
[30]
Kopertekh, L.; Schiemann, J. Transient production of recombinant pharmaceutical proteins in plants: Evolution and perspectives. Curr. Med. Chem., 2019, 26(3), 365-380.
[http://dx.doi.org/10.2174/0929867324666170718114724] [PMID: 28721831]
[31]
Stoger, E.; Ma, J.K.C.; Fischer, R.; Christou, P. Sowing the seeds of success: Pharmaceutical proteins from plants. Curr. Opin. Biotechnol., 2005, 16(2), 167-173.
[http://dx.doi.org/10.1016/j.copbio.2005.01.005] [PMID: 15831382]
[32]
Barta, A.; Sommergruber, K.; Thompson, D.; Hartmuth, K.; Matzke, M.A.; Matzke, A.J. The expression of a nopaline synthase - human growth hormone chimaeric gene in transformed tobacco and sunflower callus tissue. Plant Mol. Biol., 1986, 6(5), 347-357.
[http://dx.doi.org/10.1007/BF00034942] [PMID: 24307385]
[33]
Sijmons, P.C.; Dekker, B.M.M.; Schrammeijer, B.; Verwoerd, T.C.; van den Elzen, P.J.M.; Hoekema, A. Production of correctly processed human serum albumin in transgenic plants. Biotechnology (N. Y.), 1990, 8(3), 217-221.
[PMID: 1366404]
[34]
Twyman, R.M.; Schillberg, S.; Fischer, R. Transgenic plants in the biopharmaceutical market. Expert Opin. Emerg. Drugs, 2005, 10(1), 185-218.
[http://dx.doi.org/10.1517/14728214.10.1.185] [PMID: 15757412]
[35]
Khan, M.S.; Nurjis, F. Synthesis and expression of recombinant interferon alpha-5 gene in tobacco chloroplasts, a non-edible plant. Mol. Biol. Rep., 2012, 39(4), 4391-4400.
[http://dx.doi.org/10.1007/s11033-011-1227-y] [PMID: 21938433]
[36]
Paul, M.; Ma, J.K. Plant-made pharmaceuticals: Leading products and production platforms. Biotechnol. Appl. Biochem., 2011, 58(1), 58-67.
[http://dx.doi.org/10.1002/bab.6] [PMID: 21446960]
[37]
Hefferon, K. Clinical trials fuel the promise of plant-derived vaccines. Am. J. Chin. Med., 2010, 7, 30-37.
[38]
Ma, J.K.; Chikwamba, R.; Sparrow, P.; Fischer, R.; Mahoney, R.; Twyman, R.M. Plant-derived pharmaceuticals--the road forward. Trends Plant Sci., 2005, 10(12), 580-585.
[http://dx.doi.org/10.1016/j.tplants.2005.10.009] [PMID: 16290220]
[39]
Kohl, T.O.; Hitzeroth, I.I.; Christensen, N.D.; Rybicki, E.P. Expression of HPV-11 L1 protein in transgenic Arabidopsis thaliana and Nicotiana tabacum. BMC Biotechnol., 2007, 7, 56.
[http://dx.doi.org/10.1186/1472-6750-7-56] [PMID: 17850660]
[40]
Kalbina, I.; Engstrand, L.; Andersson, S.; Strid, A. Expression of Helicobacter pylori TonB protein in transgenic Arabidopsis thaliana: Toward production of vaccine antigens in plants. Helicobacter, 2010, 15(5), 430-437.
[http://dx.doi.org/10.1111/j.1523-5378.2010.00786.x] [PMID: 21083749]
[41]
Karaman, S.; Cunnick, J.; Wang, K. Expression of the cholera toxin B subunit (CT-B) in maize seeds and a combined mucosal treatment against cholera and traveler’s diarrhea. Plant Cell Rep., 2012, 31(3), 527-537.
[http://dx.doi.org/10.1007/s00299-011-1146-3] [PMID: 21938449]
[42]
Ramírez, Y.J.P.; Tasciotti, E.; Gutierrez-Ortega, A.; Donayre Torres, A.J.; Olivera Flores, M.T.; Giacca, M.; Gómez Lim, M.A. Fruit-specific expression of the human immunodeficiency virus type 1 tat gene in tomato plants and its immunogenic potential in mice. Clin. Vaccine Immunol., 2007, 14(6), 685-692.
[http://dx.doi.org/10.1128/CVI.00028-07] [PMID: 17460112]
[43]
Qin, Y.; Teixeira da Silva, J.A.; Zhang, L.; Zhang, S. Transgenic strawberry: State of the art for improved traits. Biotechnol. Adv., 2008, 26(3), 219-232.
[http://dx.doi.org/10.1016/j.biotechadv.2007.12.004] [PMID: 18280082]
[44]
Joung, Y.H.; Youm, J.W.; Jeon, J.H.; Lee, B.C.; Ryu, C.J.; Hong, H.J.; Kim, H.C.; Joung, H.; Kim, H.S. Expression of the hepatitis B surface S and preS2 antigens in tubers of Solanum tuberosum. Plant Cell Rep., 2004, 22(12), 925-930.
[http://dx.doi.org/10.1007/s00299-004-0775-1] [PMID: 15048583]
[45]
Cox, K.M.; Sterling, J.D.; Regan, J.T.; Gasdaska, J.R.; Frantz, K.K.; Peele, C.G.; Black, A.; Passmore, D.; Moldovan-Loomis, C.; Srinivasan, M.; Cuison, S.; Cardarelli, P.M.; Dickey, L.F. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat. Biotechnol., 2006, 24(12), 1591-1597.
[http://dx.doi.org/10.1038/nbt1260] [PMID: 17128273]
[46]
Sunil Kumar, G.B.; Ganapathi, T.R.; Srinivas, L.; Revathi, C.J.; Bapat, V.A. Expression of hepatitis B surface antigen in potato hairy roots. Plant Sci., 2006, 170, 918-925.
[http://dx.doi.org/10.1016/j.plantsci.2005.12.015]
[47]
Tran, M.; Zhou, B.; Pettersson, P.L.; Gonzalez, M.J.; Mayfield, S.P. Synthesis and assembly of a full-length human monoclonal antibody in algal chloroplasts. Biotechnol. Bioeng., 2009, 104(4), 663-673.
[http://dx.doi.org/10.1002/bit.22446] [PMID: 19562731]
[48]
Rasala, B.A.; Muto, M.; Lee, P.A.; Jager, M.; Cardoso, R.M.; Behnke, C.A.; Kirk, P.; Hokanson, C.A.; Crea, R.; Mendez, M.; Mayfield, S.P. Production of therapeutic proteins in algae, analysis of expression of seven human proteins in the chloroplast of Chlamydomonas reinhardtii. Plant Biotechnol. J., 2010, 8(6), 719-733.
[http://dx.doi.org/10.1111/j.1467-7652.2010.00503.x] [PMID: 20230484]
[49]
Smith, M.L.; Mason, H.S.; Shuler, M.L. Hepatitis B surface antigen (HBsAg) expression in plant cell culture: Kinetics of antigen accumulation in batch culture and its intracellular form. Biotechnol. Bioeng., 2002, 80(7), 812-822.
[http://dx.doi.org/10.1002/bit.10444] [PMID: 12402327]
[50]
Sojikul, P.; Buehner, N.; Mason, H.S. A plant signal peptide-hepatitis B surface antigen fusion protein with enhanced stability and immunogenicity expressed in plant cells. Proc. Natl. Acad. Sci. USA, 2003, 100(5), 2209-2214.
[http://dx.doi.org/10.1073/pnas.0438037100] [PMID: 12601177]
[51]
Zhang, B.; Shanmugaraj, B.; Daniell, H. Expression and functional evaluation of biopharmaceuticals made in plant chloroplasts. Curr. Opin. Chem. Biol., 2017, 38, 17-23.
[http://dx.doi.org/10.1016/j.cbpa.2017.02.007] [PMID: 28229907]
[52]
Nochi, T.; Takagi, H.; Yuki, Y.; Yang, L.; Masumura, T.; Mejima, M.; Nakanishi, U.; Matsumura, A.; Uozumi, A.; Hiroi, T.; Morita, S.; Tanaka, K.; Takaiwa, F.; Kiyono, H. Rice-based mucosal vaccine as a global strategy for cold-chain- and needle-free vaccination. Proc. Natl. Acad. Sci. USA, 2007, 104(26), 10986-10991.
[http://dx.doi.org/10.1073/pnas.0703766104] [PMID: 17573530]
[53]
Oszvald, M.; Kang, T.J.; Tomoskozi, S.; Jenes, B.; Kim, T.G.; Cha, Y.S.; Tamas, L.; Yang, M.S. Expression of cholera toxin B subunit in transgenic rice endosperm. Mol. Biotechnol., 2008, 40(3), 261-268.
[http://dx.doi.org/10.1007/s12033-008-9083-2] [PMID: 18618297]
[54]
Meshcheryakova, Y.A.; Eldarov, M.A.; Migunov, A.I.; Stepanova, L.A.; Repco, I.A. Cowpea mosaic virus chimeric particles bearing the ectodomain of matrix protein 2 (M2E) of the influenza A virus production and characterization. Appl. Mol. Bio., 2009, 43, 685-694.
[http://dx.doi.org/10.1134/S0026893309040219]
[55]
Burnett, M.J.B.; Burnett, A.C. Therapeutic recombinant protein production in plants: Challenges and opportunities; Plants People Planet, 2019.
[http://dx.doi.org/10.1002/ppp3.10073]
[56]
Takagi, H.; Saito, S.; Yang, L.; Nagasaka, S.; Nishizawa, N.; Takaiwa, F. Oral immunotherapy against a pollen allergy using a seed-based peptide vaccine. Plant Biotechnol. J., 2005, 3(5), 521-533.
[http://dx.doi.org/10.1111/j.1467-7652.2005.00143.x] [PMID: 17173638]
[57]
Lau, O.S.; Sun, S.S.M. Plant seeds as bioreactors for recombinant protein production. Biotechnol. Adv., 2009, 27(6), 1015-1022.
[http://dx.doi.org/10.1016/j.biotechadv.2009.05.005] [PMID: 19460423]
[58]
Yand, M.; Gao, X.; Dong, J.; Gandhi, N.; Cai, H.; Wettstein, D.H.; Rustgi, S.; Wen, S. Pattern of protein expression in developing wheat grains identified through proteomic analysis. Front. Plant Sci., 2017, 8(962), 1-13.
[http://dx.doi.org/10.3389%2Ffpls.2017.00962]
[59]
Takaiwa, F.; Takagi, H.; Hirose, S.; Wakasa, Y. Endosperm tissue is good production platform for artificial recombinant proteins in transgenic rice. Plant Biotechnol. J., 2007, 5(1), 84-92.
[http://dx.doi.org/10.1111/j.1467-7652.2006.00220.x] [PMID: 17207259]
[60]
Erlendsson, L.S.; Muench, M.O.; Hellman, U.; Hrafnkelsdóttir, S.M.; Jonsson, A.; Balmer, Y.; Mäntylä, E.; Orvar, B.L. Barley as a green factory for the production of functional Flt3 ligand. Biotechnol. J., 2010, 5(2), 163-171.
[http://dx.doi.org/10.1002/biot.200900111] [PMID: 19844912]
[61]
Chaudhary, S.; Parmenter, D.L.; Moloney, M.M. Transgenic Brassica carinata as a vehicle for the production of recombinant proteins in seeds. Plant Cell Rep., 1998, 17(3), 195-200.
[http://dx.doi.org/10.1007/s002990050377] [PMID: 30736499]
[62]
Downing, W.L.; Galpin, J.D.; Clemens, S.; Lauzon, S.M.; Samuels, A.L.; Pidkowich, M.S.; Clarke, L.A.; Kermode, A.R. Synthesis of enzymatically active human alpha-L-iduronidase in Arabidopsis cgl (complex glycan-deficient) seeds. Plant Biotechnol. J., 2006, 4(2), 169-181.
[http://dx.doi.org/10.1111/j.1467-7652.2005.00166.x] [PMID: 17177794]
[63]
Zimmermann, J.; Saalbach, I.; Jahn, D.; Giersberg, M.; Haehnel, S.; Wedel, J.; Macek, J.; Zoufal, K.; Glünder, G.; Falkenburg, D.; Kipriyanov, S.M. Antibody expressing pea seeds as fodder for prevention of gastrointestinal parasitic infections in chickens. BMC Biotechnol., 2009, 9, 79.
[http://dx.doi.org/10.1186/1472-6750-9-79] [PMID: 19747368]
[64]
Cunha, N.B.; Murad, A.M.; Ramos, G.L.; Maranhão, A.Q.; Brígido, M.M.; Araújo, A.C.; Lacorte, C.; Aragão, F.J.; Covas, D.T.; Fontes, A.M.; Souza, G.H.; Vianna, G.R.; Rech, E.L. Accumulation of functional recombinant human coagulation factor IX in transgenic soybean seeds. Transgenic Res., 2011, 20(4), 841-855.
[http://dx.doi.org/10.1007/s11248-010-9461-y] [PMID: 21069460]
[65]
Nykiforuk, C.L.; Shen, Y.; Murray, E.W.; Boothe, J.G.; Busseuil, D.; Rhéaume, E.; Tardif, J.C.; Reid, A.; Moloney, M.M. Expression and recovery of biologically active recombinant Apolipoprotein AI (Milano) from transgenic safflower (Carthamus tinctorius) seeds. Plant Biotechnol. J., 2011, 9(2), 250-263.
[http://dx.doi.org/10.1111/j.1467-7652.2010.00546.x] [PMID: 20618764]
[66]
Nadal, A.; Montero, M.; Company, N.; Badosa, E.; Messeguer, J.; Montesinos, L.; Montesinos, E.; Pla, M. Constitutive expression of transgenes encoding derivatives of the synthetic antimicrobial peptide BP100: Impact on rice host plant fitness. BMC Plant Biol., 2012, 12, 159.
[http://dx.doi.org/10.1186/1471-2229-12-159] [PMID: 22947243]
[67]
De Jaeger, G.; Scheffer, S.; Jacobs, A.; Zambre, M.; Zobell, O.; Goossens, A.; Depicker, A.; Angenon, G. Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat. Biotechnol., 2002, 20(12), 1265-1268.
[http://dx.doi.org/10.1038/nbt755] [PMID: 12415287]
[68]
Xu, R.; Li, D.; Li, H.; Li, J.; Yang, Y.; Qin, R.; Li, L.; Wei, P.; Yang, J. Isolation of four rice seed-specifi promoters and evaluation of endosperm activity. Plant Cell Tissue Organ Cult., 2017, 128(1), 125-132.
[http://dx.doi.org/10.1007/s11240-016-1091-5]
[69]
Yang, D.; Guo, F.; Liu, B.; Huang, N.; Watkins, S.C. Expression and localization of human lysozyme in the endosperm of transgenic rice. Planta, 2003, 216(4), 597-603.
[PMID: 12569401]
[70]
Wu, J.; Yu, L.; Li, L.; Hu, J.; Zhou, J.; Zhou, X. Oral immunization with transgenic rice seeds expressing VP2 protein of infectious bursal disease virus induces protective immune responses in chickens. Plant Biotechnol. J., 2007, 5(5), 570-578.
[http://dx.doi.org/10.1111/j.1467-7652.2007.00270.x] [PMID: 17561926]
[71]
Yang, L.; Tada, Y.; Yamamoto, M.P.; Zhao, H.; Yoshikawa, M.; Takaiwa, F. A transgenic rice seed accumulating an anti-hypertensive peptide reduces the blood pressure of spontaneously hypertensive rats. FEBS Lett., 2006, 580(13), 3315-3320.
[http://dx.doi.org/10.1016/j.febslet.2006.04.092] [PMID: 16697378]
[72]
Yang, L.; Suzuki, K.; Hirose, S.; Wakasa, Y.; Takaiwa, F. Development of transgenic rice seed accumulating a major Japanese cedar pollen allergen (Cry j 1) structurally disrupted for oral immunotherapy. Plant Biotechnol. J., 2007, 5(6), 815-826.
[http://dx.doi.org/10.1111/j.1467-7652.2007.00287.x] [PMID: 17714439]
[73]
Jeong, H.J.; Choi, J.Y.; Shin, H.Y.; Bae, J.M.; Shin, J.S. Seed-specific expression of seven Arabidopsis promoters. Gene, 2014, 553(1), 17-23.
[http://dx.doi.org/10.1016/j.gene.2014.09.051] [PMID: 25261846]
[74]
Goossens, A.; Dillen, W.; De Clercq, J.; Van Montagu, M.; Angenon, G. The arcelin-5 gene of Phaseolus vulgaris directs high seed-specific expression in transgenic Phaseolus acutifolius and Arabidopsis plants. Plant Physiol., 1999, 120(4), 1095-1104.
[http://dx.doi.org/10.1104/pp.120.4.1095] [PMID: 10444093]
[75]
Hood, E.E.; Bailey, M.R.; Beifuss, K.; Magallanes-Lundback, M.; Horn, M.E.; Callaway, E.; Drees, C.; Delaney, D.E.; Clough, R.; Howard, J.A. Criteria for high-level expression of a fungal laccase gene in transgenic maize. Plant Biotechnol. J., 2003, 1(2), 129-140.
[http://dx.doi.org/10.1046/j.1467-7652.2003.00014.x] [PMID: 17147750]
[76]
Wu, L.; El-Mezawy, A.; Shah, S. A seed coat outer integument-specific promoter for Brassica napus. Plant Cell Rep., 2011, 30(1), 75-80.
[http://dx.doi.org/10.1007/s00299-010-0945-2] [PMID: 21052676]
[77]
Esfandiari, E.; Jin, Z.; Abdeen, A.; Griffiths, J.S.; Western, T.L.; Haughn, G.W. Identification and analysis of an outer-seed-coat-specific promoter from Arabidopsis thaliana. Plant Mol. Biol., 2013, 81(1-2), 93-104.
[http://dx.doi.org/10.1007/s11103-012-9984-0] [PMID: 23115000]
[78]
Shi, J.; Wang, H.; Schellin, K.; Li, B.; Faller, M.; Stoop, J.M.; Meeley, R.B.; Ertl, D.S.; Ranch, J.P.; Glassman, K. Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol., 2007, 25(8), 930-937.
[http://dx.doi.org/10.1038/nbt1322] [PMID: 17676037]
[79]
Kumar, V.; Saha, D.; Thakare, D.R.; Jajoo, A.; Jain, P.K.; Bhat, S.R.; Srinivasan, R. A part of the upstream promoter region of SHN2 gene directs trichome specific expression in Arabidopsis thaliana and heterologous plants. Plant Sci., 2017, 264, 138-148.
[http://dx.doi.org/10.1016/j.plantsci.2017.09.005] [PMID: 28969794]
[80]
Ma, L.; Wang, Y.; Liu, W.; Liu, Z. Expression analysis of seed-specific genes in four angiosperm species with an emphasis on the unconserved expression patterns of homologous genes. Seed Sci. Res., 2013, 23, 223-231.
[http://dx.doi.org/10.1017/S0960258513000305]
[81]
Bäumlein, H.; Nagy, I.; Villarroel, R.; Inzé, D.; Wobus, U. Cis-analysis of a seed protein gene promoter: The conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant J., 1992, 2(2), 233-239.
[PMID: 1338774]
[82]
Lelievre, J.M.; Oliveira, L.O.; Nielsen, N.C. 5′-CATGCAT-3′ elements modulate the expression of glycinin genes. Plant Physiol., 1992, 98(1), 387-391.
[http://dx.doi.org/10.1104/pp.98.1.387] [PMID: 16668640]
[83]
Wu, C.Y.; Suzuki, A.; Washida, H.; Takaiwa, F. The GCN4 motif in a rice glutelin gene is essential for endosperm-specific gene expression and is activated by Opaque-2 in transgenic rice plants. Plant J., 1998, 14(6), 673-683.
[http://dx.doi.org/10.1046/j.1365-313x.1998.00167.x] [PMID: 9681032]
[84]
Albani, D.; Hammond-Kosack, M.C.; Smith, C.; Conlan, S.; Colot, V.; Holdsworth, M.; Bevan, M.W. The wheat transcriptional activator SPA: A seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell, 1997, 9(2), 171-184.
[PMID: 9061949]
[85]
Rademacher, T.; Sack, M.; Arcalis, E.; Stadlmann, J.; Balzer, S.; Altmann, F.; Quendler, H.; Stiegler, G.; Kunert, R.; Fischer, R.; Stoger, E. Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol. J., 2008, 6(2), 189-201.
[http://dx.doi.org/10.1111/j.1467-7652.2007.00306.x] [PMID: 17979949]
[86]
Liu, X.; Li, S.; Yang, W.; Mu, B.; Jiao, Y.; Zhou, X.; Zhang, C.; Fan, Y.; Chen, R. xzSynthesis of seed-specific bidirectional promoters for metabolic engineering of anthocyanin-rich maize. Plant Cell Physiol., 2018, 59(10), 1942-1955.
[http://dx.doi.org/10.1093/pcp/pcy110] [PMID: 29917151]
[87]
Aoyagi, T.; Kobayashi, M.; Kozaki, A. Design of a seed-specific chimeric promoter with a modified expression profile to improve seed oil content. Int. J. Mol. Sci., 2018, 19(6), 1667.
[http://dx.doi.org/10.3390/ijms19061667] [PMID: 29874815]
[88]
Dure, L.; Waters, L. Long-lived messenger RNA: Evidence from cotton seed germination. Science, 1965, 147(3656), 410-412.
[http://dx.doi.org/10.1126/science.147.3656.410] [PMID: 14221492]
[89]
Zhang, X.; Guo, H. mRNA decay in plants: Both quantity and quality matter. Curr. Opin. Plant Biol., 2017, 35, 138-144.
[http://dx.doi.org/10.1016/j.pbi.2016.12.003] [PMID: 28011423]
[90]
Shoemaker, C.J.; Green, R. Translation drives mRNA quality control. Nat. Struct. Mol. Biol., 2012, 19(6), 594-601.
[http://dx.doi.org/10.1038/nsmb.2301] [PMID: 22664987]
[91]
Basbouss-Serhal, I.; Soubigou-Taconnat, L.; Bailly, C. Leymarie. Germination potential of dormant and non-dormant Arabidopsis seeds is driven by distinct recruitment of mRNAs to polysomes. Plant Physiol., 2015, 168, 1049-1065.
[http://dx.doi.org/10.1104/pp.15.00510] [PMID: 26019300]
[92]
Bai, B.; Peviani, A.; van der Horst, S.; Gamm, M.; Snel, B.; Bentsink, L.; Hanson, J. Extensive translational regulation during seed germination revealed by polysomal profiling. New Phytol., 2017, 214(1), 233-244.
[http://dx.doi.org/10.1111/nph.14355] [PMID: 27935038]
[93]
Gustafsson, C.; Govindarajan, S.; Minshull, J. Codon bias and heterologous protein expression. Trends Biotechnol., 2004, 22(7), 346-353.
[http://dx.doi.org/10.1016/j.tibtech.2004.04.006] [PMID: 15245907]
[94]
Streatfield, S.J. Approaches to achieve high-level heterologous protein production in plants. Plant Biotechnol. J., 2007, 5(1), 2-15.
[http://dx.doi.org/10.1111/j.1467-7652.2006.00216.x] [PMID: 17207252]
[95]
Park, M.; Kim, S.J.; Vitale, A.; Hwang, I. Identification of the protein storage vacuole and protein targeting to the vacuole in leaf cells of three plant species. Plant Physiol., 2004, 134(2), 625-639.
[http://dx.doi.org/10.1104/pp.103.030635]
[96]
Vitale, A.; Pedrazzini, E. Recombinant pharmaceuticals from plants: The plant endomembrane system as bioreactor. Mol. Interv., 2005, 5(4), 216-225.
[http://dx.doi.org/10.1124/mi.5.4.5] [PMID: 16123536]
[97]
Bellucci, M.; Marchis, F.D.; Pompa, A. The endoplasmic reticulum is a hub to sort proteins toward unconventional traffic pathways and endosymbiotic organelles. J. Exp. Bot., 2018, 69(1), 7-20.
[http://dx.doi.org/10.1093/jxb/erx286]
[98]
Avesani, L.; Merlin, M.; Gecchele, E.; Capaldi, S.; Brozzetti, A.; Falorni, A.; Pezzotti, M. Comparative analysis of different biofactories for the production of a major diabetes autoantigen. Transgenic Res., 2014, 23(2), 281-291.
[http://dx.doi.org/10.1007/s11248-013-9749-9] [PMID: 24142387]
[99]
Jiang, L.; Phillips, T.E.; Rogers, S.W.; Rogers, J.C. Biogenesis of the protein storage vacuole crystalloid. J. Cell Biol., 2000, 150(4), 755-770.
[http://dx.doi.org/10.1083/jcb.150.4.755] [PMID: 10953001]
[100]
Jiang, L.; Sun, S.S. Membrane anchors for vacuolar targeting: Application in plant bioreactors. Trends Biotechnol., 2002, 20(3), 99-102.
[http://dx.doi.org/10.1016/S0167-7799(02)01882-6] [PMID: 11841859]
[101]
Xiang, L.; Etxeberria, E.; Van den Ende, W. Vacuolar protein sorting mechanisms in plants. FEBS J., 2013, 280(4), 979-993.
[http://dx.doi.org/10.1111/febs.12092] [PMID: 23241209]
[102]
Nishizawa, K.; Maruyama, N.; Satoh, R.; Fuchikami, Y.; Higasa, T.; Utsumi, S. A C-terminal sequence of soybean β-conglycinin α′ subunit acts as a vacuolar sorting determinant in seed cells. Plant J., 2003, 34(5), 647-659.
[http://dx.doi.org/10.1046/j.1365-313X.2003.01754.x] [PMID: 12787246]
[103]
Vitale, A.; Ceriotti, A. Protein quality control mechanisms and protein storage in the endoplasmic reticulum. A conflict of interests? Plant Physiol., 2004, 136(3), 3420-3426.
[http://dx.doi.org/10.1104/pp.104.050351] [PMID: 15542495]
[104]
Herman, E.M.; Larkins, B.A. Protein storage bodies and vacuoles. Plant Cell, 1999, 11(4), 601-614.
[http://dx.doi.org/10.1105/tpc.11.4.601] [PMID: 10213781]
[105]
Pelham, H.R. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem. Sci., 1990, 15(12), 483-486.
[http://dx.doi.org/10.1016/0968-0004(90)90303-S] [PMID: 2077689]
[106]
Wandelt, C.I.; Khan, M.R.; Craig, S.; Schroeder, H.E.; Spencer, D.; Higgins, T.J. Vicilin with carboxy-terminal KDEL is retained in the endoplasmic reticulum and accumulates to high levels in the leaves of transgenic plants. Plant J., 1992, 2(2), 181-192.
[PMID: 1302048]
[107]
Vaquero, C.; Sack, M.; Schuster, F.; Finnern, R.; Drossard, J.; Schumann, D. A carcinoembryonic antigen-specific diabody produced in tobacco. FASEB J., 2002, 16(3), 408-410.
[http://dx.doi.org/10.1096/fj.01-0363fje]
[108]
Moravec, T.; Schmidt, M.A.; Herman, E.M.; Woodford-Thomas, T. Production of Escherichia coli heat labile toxin (LT) B subunit in soybean seed and analysis of its immunogenicity as an oral vaccine. Vaccine, 2007, 25(9), 1647-1657.
[http://dx.doi.org/10.1016/j.vaccine.2006.11.010] [PMID: 17188785]
[109]
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]
[110]
Ko, K.; Tekoah, Y.; Rudd, P.M.; Harvey, D.J.; Dwek, R.A.; Spitsin, S.; Hanlon, C.A.; Rupprecht, C.; Dietzschold, B.; Golovkin, M.; Koprowski, H. Function and glycosylation of plant-derived antiviral monoclonal antibody. Proc. Natl. Acad. Sci. USA, 2003, 100(13), 8013-8018.
[http://dx.doi.org/10.1073/pnas.0832472100] [PMID: 12799460]
[111]
Ma, J.K.; Drake, P.M.; Christou, P. The production of recombinant pharmaceutical proteins in plants. Nat. Rev. Genet., 2003, 4(10), 794-805.
[http://dx.doi.org/10.1038/nrg1177] [PMID: 14526375]
[112]
Gomord, V.; Chamberlain, P.; Jefferis, R.; Faye, L. Biopharmaceutical production in plants: Problems, solutions and opportunities. Trends Biotechnol., 2005, 23(11), 559-565.
[http://dx.doi.org/10.1016/j.tibtech.2005.09.003] [PMID: 16168504]
[113]
Bakker, H.; Bardor, M.; Molthoff, J.W.; Gomord, V.; Elbers, I.; Stevens, L.H.; Jordi, W.; Lommen, A.; Faye, L.; Lerouge, P.; Bosch, D. Galactose-extended glycans of antibodies produced by transgenic plants. Proc. Natl. Acad. Sci. USA, 2001, 98(5), 2899-2904.
[http://dx.doi.org/10.1073/pnas.031419998] [PMID: 11226338]
[114]
Giddings, G. Transgenic plants as protein factories. Curr. Opin. Biotechnol., 2001, 12(5), 450-454.
[http://dx.doi.org/10.1016/S0958-1669(00)00244-5] [PMID: 11604319]
[115]
Evangelista, R.L.; Kusnadi, A.R.; Howard, J.A.; Nikolov, Z.L. Process and economic evaluation of the extraction and purification of recombinant beta-glucuronidase from transgenic corn. Biotechnol. Prog., 1998, 14(4), 607-614.
[http://dx.doi.org/10.1021/bp980047c] [PMID: 9694683]
[116]
Shanmugaraj, B.M.; Ramalingam, S. Plant expression platform for the production of recombinant pharmaceutical proteins. Austin. J. Biotechnol. Bioeng., 2014, 1(6), 4.
[117]
Ramessar, K.; Capell, T.; Christou, P. Molecular pharming in cereal crops. Phytochem. Rev., 2008, 7, 579-592.
[http://dx.doi.org/10.1007/s11101-008-9087-3]
[118]
Peters, J.; Stoger, E. Transgenic crops for the production of recombinant vaccines and anti-microbial antibodies. Hum. Vaccin., 2011, 7(3), 367-374.
[http://dx.doi.org/10.4161/hv.7.3.14303] [PMID: 21346415]
[119]
Stoger, E.; Sack, M.; Perrin, Y.; Vaquero, C.; Torres, E.; Twyman, R.M.; Christou, P.; Fischer, R. Practical considerations for pharmaceutical antibody production in different crop systems. Mol. Breed., 2002, 9, 149-158.
[http://dx.doi.org/10.1023/A:1019714614827]
[120]
Sengupta-Gopalan, C.; Reichert, N.A.; Barker, R.F.; Hall, T.C.; Kemp, J.D. Developmentally regulated expression of the bean beta-phaseolin gene in tobacco seed. Proc. Natl. Acad. Sci. USA, 1985, 82(10), 3320-3324.
[http://dx.doi.org/10.1073/pnas.82.10.3320] [PMID: 16578787]
[121]
Huang, N. High-level protein expression system uses self-pollinating crops as hosts. Bioprocess Int., 2004, 2, 54-59.
[122]
Nandi, S.; Yalda, D.; Lu, S.; Nikolov, Z.; Misaki, R.; Fujiyama, K.; Huang, N. Process development and economic evaluation of recombinant human lactoferrin expressed in rice grain. Transgenic Res., 2005, 14(3), 237-249.
[http://dx.doi.org/10.1007/s11248-004-8120-6] [PMID: 16145832]
[123]
Rachmawati, D.; Mori, T.; Hosaka, T.; Takaiwa, F.; Inoue, E.; Anzai, H. Production and characterization of recombinant human lactoferrin in transgenic Javanica rice. Breed. Sci., 2005, 55, 213-222.
[http://dx.doi.org/10.1270/jsbbs.55.213]
[124]
Ding, S.H.; Huang, L.Y.; Wang, Y.D.; Sun, H.C.; Xiang, Z.H. High-level expression of basic fibroblast growth factor in transgenic soybean seeds and characterization of its biological activity. Biotechnol. Lett., 2006, 28(12), 869-875.
[http://dx.doi.org/10.1007/s10529-006-9018-6] [PMID: 16786271]
[125]
Sardana, R.; Dudani, A.K.; Tackaberry, E.; Alli, Z.; Porter, S.; Rowlandson, K.; Ganz, P.; Altosaar, I. Biologically active human GM-CSF produced in the seeds of transgenic rice plants. Transgenic Res., 2007, 16(6), 713-721.
[http://dx.doi.org/10.1007/s11248-006-9062-y] [PMID: 17985214]
[126]
Markley, N.; Nykiforuk, C.; Boothe, J.; Moloney, M. Producing proteins using transgenic oilbody-oleosin technology. Biopharm Int., 2006, 19, 34-57.
[127]
Sugita, K.; Endo-Kasahara, S.; Tada, Y.; Lijun, Y.; Yasuda, H.; Hayashi, Y.; Jomori, T.; Ebinuma, H.; Takaiwa, F. Genetically modified rice seeds accumulating GLP-1 analogue stimulate insulin secretion from a mouse pancreatic beta-cell line. FEBS Lett., 2005, 579(5), 1085-1088.
[http://dx.doi.org/10.1016/j.febslet.2004.12.082] [PMID: 15710395]
[128]
Perrin, Y.; Vaquero, C.; Gerrard, I.; Sack, M.; Drossard, J.; Stöger, E.; Christou, P.; Fischer, R. Transgenic pea seeds as bioreactors for the production of a single-chain Fv fragment (scFV) antibody used in cancer diagnosis and therapy. Mol. Breed., 2000, 6, 345-352.
[http://dx.doi.org/10.1023/A:1009657701588]
[129]
Qian, B.; Shen, H.; Liang, W.; Guo, X.; Zhang, C.; Wang, Y.; Li, G.; Wu, A.; Cao, K.; Zhang, D. Immunogenicity of recombinant hepatitis B virus surface antigen fused with preS1 epitopes expressed in rice seeds. Transgenic Res., 2008, 17(4), 621-631.
[http://dx.doi.org/10.1007/s11248-007-9135-6] [PMID: 17882531]
[130]
Zhou, Y.X.; Lee, M.Y.T.; Ng, J.M.H.; Chye, M.L.; Yip, W.K.; Zee, S.Y.; Lam, E. A truncated hepatitis E virus ORF2 protein expressed in tobacco plastids is immunogenic in mice. World J. Gastroenterol., 2006, 12(2), 306-312.
[http://dx.doi.org/10.3748/wjg.v12.i2.306] [PMID: 16482635]
[131]
Evangelista Dyr, J.; Suttnar, J. Separation used for purification of recombinant proteins. J. Chromatogr. B Biomed. Sci. Appl., 1997, 699(1-2), 383-401.
[http://dx.doi.org/10.1016/S0378-4347(97)00201-6] [PMID: 9392384]
[132]
Buyel, J.F. Process development strategies in plant molecular farming. Curr. Pharm. Biotechnol., 2015, 16(11), 966-982.
[http://dx.doi.org/10.2174/138920101611150902115413] [PMID: 26343135]
[133]
Phan, H.T.; Hause, B.; Hause, G.; Arcalis, E.; Stoger, E.; Maresch, D.; Altmann, F.; Joensuu, J.; Conrad, U. Influence of elastin-like polypeptide and hydrophobin on recombinant hemagglutinin accumulations in transgenic tobacco plants. PLoS One, 2014, 9(6)e99347
[http://dx.doi.org/10.1371/journal.pone.0099347] [PMID: 24914995]
[134]
Reuter, L.J.; Bailey, M.J.; Joensuu, J.J.; Ritala, A. Scale-up of hydrophobin-assisted recombinant protein production in tobacco BY-2 suspension cells. Plant Biotechnol. J., 2014, 12(4), 402-410.
[http://dx.doi.org/10.1111/pbi.12147] [PMID: 24341724]
[135]
Nykiforuk, C.L.; Boothe, J.G. Transgenic expression of therapeutic proteins in Arabidopsis thaliana seed. Methods Mol. Biol., 2012, 899, 239-264.
[http://dx.doi.org/10.1007/978-1-61779-921-1_16] [PMID: 22735958]
[136]
Aspelund, M.T.; Glatz, C.E. Purification of recombinant plant-made proteins from corn extracts by ultrafiltration. J. Membr. Sci., 2010, 353, 103-110.
[http://dx.doi.org/10.1016/j.memsci.2010.02.036]
[137]
Azzoni, A.R.; Kusnadi, A.R.; Miranda, E.A.; Nikolov, Z.L. Recombinant aprotinin produced in transgenic corn seed: Extraction and purification studies. Biotechnol. Bioeng., 2002, 80(3), 268-276.
[http://dx.doi.org/10.1002/bit.10408] [PMID: 12226858]
[138]
Kusnadi, A.R.; Evangelista, R.L.; Hood, E.E.; Howard, J.A.; Nikolov, Z.L. Processing of transgenic corn seed and its effect on the recovery of recombinant beta-glucuronidase. Biotechnol. Bioeng., 1998, 60(1), 44-52.
[http://dx.doi.org/10.1002/(SICI)1097-0290(19981005)60:1<44:AID-BIT5>3.0.CO;2-0] [PMID: 10099404]
[139]
Woodard, S.L.; Mayor, J.M.; Bailey, M.R.; Barker, D.K.; Love, R.T.; Lane, J.R.; Delaney, D.E.; McComas-Wagner, J.M.; Mallubhotla, H.D.; Hood, E.E.; Dangott, L.J.; Tichy, S.E.; Howard, J.A. Maize (Zea mays)-derived bovine trypsin: Characterization of the first large-scale, commercial protein product from transgenic plants. Biotechnol. Appl. Biochem., 2003, 38(Pt 2), 123-130.
[http://dx.doi.org/10.1042/BA20030026] [PMID: 12749769]
[140]
Bai, Y.; Glatz, C.E. Capture of a recombinant protein from unclarified canola extract using streamline expanded bed anion exchange. Biotechnol. Bioeng., 2003, 81(7), 855-864.
[http://dx.doi.org/10.1002/bit.10532] [PMID: 12557319]
[141]
Gregory, J.; Barany, S. Adsorption and flocculation by polymers and polymer mixtures. Adv. Colloid Interface Sci., 2011, 169(1), 1-12.
[http://dx.doi.org/10.1016/j.cis.2011.06.004] [PMID: 21762869]
[142]
Buyel, J.F.; Fischer, R. Downstream processing of biopharmaceutical proteins produced in plants: The pros and cons of flocculants. Bioengineered, 2014, 5(2), 138-142.
[http://dx.doi.org/10.4161/bioe.28061] [PMID: 24637706]
[143]
Barany, S.; Szepesszentgyörgyi, A. Flocculation of cellular suspensions by polyelectrolytes. Adv. Colloid Interface Sci., 2004, 111(1-2), 117-129.
[http://dx.doi.org/10.1016/j.cis.2004.07.003] [PMID: 15571665]
[144]
Parikh, K.; Duysen, E.G.; Snow, B.; Jensen, N.S.; Manne, V.; Lockridge, O.; Chilukuri, N. Gene-delivered butyrylcholinesterase is prophylactic against the toxicity of chemical warfare nerve agents and organophosphorus compounds. J. Pharmacol. Exp. Ther., 2011, 337, 92-101.
[145]
Egelkrout, E.; Hayden, C.; Wales, M.; Walker, J.; Novikov, B.; Grimsley, J.; Howard, J. Production of the bio scavenger butyrylcholinesterase in maize. Mol. Breed., 2017, 37, 136.
[http://dx.doi.org/10.1007/s11032-017-0731-8]
[146]
Mazzio, E.; Badisa, R.; Eyunni, S.; Ablordeppey, S.; George, B.; Soliman, K.F.A. Bioactivity-guided isolation of neuritogenic factor from the seeds of the gac plant (Momordica cochinchinensis). Evid. Based Complement. Alternat. Med., 2018.20188953958
[http://dx.doi.org/10.1155/2018/8953958] [PMID: 29955238]
[147]
Streatfield, S.J.; Jilka, J.M.; Hood, E.E.; Turner, D.D.; Bailey, M.R.; Mayor, J.M.; Woodard, S.L.; Beifuss, K.K.; Horn, M.E.; Delaney, D.E.; Tizard, I.R.; Howard, J.A. Plant-based vaccines: Unique advantages. Vaccine, 2001, 19(17-19), 2742-2748.
[http://dx.doi.org/10.1016/S0264-410X(00)00512-0] [PMID: 11257418]
[148]
Tacket, C.O.; Pasetti, M.F.; Edelman, R.; Howard, J.A.; Streatfield, S. Immunogenicity of recombinant LT-B delivered orally to humans in transgenic corn. Vaccine, 2004, 22(31-32), 4385-4389.
[http://dx.doi.org/10.1016/j.vaccine.2004.01.073] [PMID: 15474732]
[149]
Tacket, C.O. Plant-based vaccines against diarrheal diseases. Trans. Am. Clin. Climatol. Assoc., 2007, 118, 79-87.
[PMID: 18528491]
[150]
Kapusta, J.; Modelska, A.; Figlerowicz, M.; Pniewski, T.; Letellier, M.; Lisowa, O.; Yusibov, V.; Koprowski, H.; Plucienniczak, A.; Legocki, A.B. A plant-derived edible vaccine against hepatitis B virus. FASEB J., 1999, 13(13), 1796-1799.
[http://dx.doi.org/10.1096/fasebj.13.13.1796] [PMID: 10506582]
[151]
Kapusta, J.; Modelska, A.; Pniewski, T.; Figlerowicz, M.; Jankowski, K.; Lisowa, O.; Plucienniczak, A.; Koprowski, H.; Legocki, A.B. Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Adv. Exp. Med. Biol., 2001, 495, 299-303.
[http://dx.doi.org/10.1007/978-1-4615-0685-0_41] [PMID: 11774582]
[152]
Yusibov, V.; Hooper, D.C.; Spitsin, S.V.; Fleysh, N.; Kean, R.B.; Mikheeva, T.; Deka, D.; Karasev, A.; Cox, S.; Randall, J.; Koprowski, H. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine, 2002, 20(25-26), 3155-3164.
[http://dx.doi.org/10.1016/S0264-410X(02)00260-8] [PMID: 12163267]
[153]
Zhong, Q.; Gu, Z.; Glatz, C.E. Extraction of recombinant dog gastric lipase from transgenic corn seed. J. Agric. Food Chem., 2006, 54(21), 8086-8092.
[http://dx.doi.org/10.1021/jf061921h] [PMID: 17032014]
[154]
Sharma, A.K.; Sharma, M.K. Plants as bioreactors: Recent developments and emerging opportunities. Biotechnol. Adv., 2009, 27(6), 811-832.
[http://dx.doi.org/10.1016/j.biotechadv.2009.06.004] [PMID: 19576278]
[155]
Basaran, P.; Rodríguez-Cerezo, E. Plant molecular farming: Opportunities and challenges. Crit. Rev. Biotechnol., 2008, 28(3), 153-172.
[http://dx.doi.org/10.1080/07388550802046624] [PMID: 18937106]
[156]
Hood, E.E.; Witcher, D.R.; Maddock, S.; Meyer, T.; Baszczynski, C.; Bailey, M. Commercial production of avidin from transgenic maize: Characterization of transformant, production, processing, extraction and purification. Mol. Breed., 1997, 3, 291-306.
[http://dx.doi.org/10.1023/A:1009676322162]
[157]
Hood, E.E.; Howard, J.A. Over-expression of Novel Proteins in Maize. In: Molecular Genetic Approaches to Maize Improvement. Biotechnology in Agriculture and Forestry; Kriz, A.L.; Larkins, B.A., Eds.; Springer: Berlin, Heidelberg, 2009; Vol. 63, pp. 91-105.
[http://dx.doi.org/10.1007/978-3-540-68922-5_8]
[158]
Kaiser, J. Is the drought over for pharming? Science, 2008, 320(5875), 473-475.
[http://dx.doi.org/10.1126/science.320.5875.473] [PMID: 18436771]
[159]
Spök, A. Molecular farming on the rise--GMO regulators still walking a tightrope. Trends Biotechnol., 2007, 25(2), 74-82.
[http://dx.doi.org/10.1016/j.tibtech.2006.12.003] [PMID: 17174425]
[160]
Gomes, C.; Oliveira, F.; Vieira, S.I.; Duque, A.S. Prospects for the production of recombinant therapeutic proteins and peptides in plants. Special focus on angiotensin i-converting enzyme inhibitory (ACEI). Peptides, 2019, 1-27.
[http://dx.doi.org/10.5772/intechopen.8449]
[161]
Laible, P.D.; Scott, H.N.; Henry, L.; Hanson, D.K. Towards higher-throughput membrane protein production for structural genomics initiatives. J. Struct. Funct. Genomics, 2004, 5(1-2), 167-172.
[http://dx.doi.org/10.1023/B:JSFG.0000029201.33710.46] [PMID: 15263855]
[162]
Tokunaga, H.; Arakawa, T.; Tokunaga, M. Novel soluble expression technologies derived from unique properties of halophilic proteins. Appl. Microbiol. Biotechnol., 2010, 88(6), 1223-1231.
[http://dx.doi.org/10.1007/s00253-010-2832-8] [PMID: 20838790]
[163]
Guo, X.Q.; Wei, Y.M.; Yu, B. Recombinant Mycobacterium smegmatis expressing Hsp65-hIL-2 fusion protein and its influence on lymphocyte function in mice. Asian Pac. J. Trop. Med., 2012, 5(5), 347-351.
[http://dx.doi.org/10.1016/S1995-7645(12)60056-X] [PMID: 22546648]
[164]
Kikuchi, Y.; Itaya, H.; Date, M.; Matsui, K.; Wu, L.F. Production of Chryseobacterium proteolyticum protein-glutaminase using the twin-arginine translocation pathway in Corynebacterium glutamicum. Appl. Microbiol. Biotechnol., 2008, 78(1), 67-74.
[http://dx.doi.org/10.1007/s00253-007-1283-3] [PMID: 18064454]
[165]
Deb, P.; Talukdar, S.A.; Mohsina, K.; Sarker, P.K.; Sayem, S.A. Production and partial characterization of extracellular amylase enzyme from P-001. Springerplus, 2013, 2, 154.
[http://dx.doi.org/10.1186/2193-1801-2-154] [PMID: 23626928]
[166]
Jin, H.; Cantin, G.T.; Maki, S.; Chew, L.C.; Resnick, S.M.; Ngai, J.; Retallack, D.M. Soluble periplasmic production of human granulocyte colony-stimulating factor (G-CSF) in Pseudomonas fluorescens. Protein Expr. Purif., 2011, 78(1), 69-77.
[http://dx.doi.org/10.1016/j.pep.2011.03.002] [PMID: 21396452]
[167]
Porceddu, A.; Falorni, A.; Ferradini, N. Transgenic plants expressing human glutamic acid decarboxylase (GAD65), a major autoantigen in insulin-dependent diabetes mellitus. Mol. Breed., 1999, 5, 553-560.
[http://dx.doi.org/10.1023/A:1009605729268]
[168]
Nausch, H.; Mikschofsky, H.; Koslowski, R.; Meyer, U.; Broer, I.; Huckauf, J. High-level transient expression of ER-targeted human interleukin 6 in Nicotiana benthamiana. PLoS One, 2012, 7, 11.
[http://dx.doi.org/10.1371/journal.pone.0048938]
[169]
Zhang, X.; Buehner, N.A.; Hutson, A.M.; Estes, M.K.; Mason, H.S. Tomato is a highly effective vehicle for expression and oral immunization with Norwalk virus capsid protein. Plant Biotechnol. J., 2006, 4(4), 419-432.
[http://dx.doi.org/10.1111/j.1467-7652.2006.00191.x] [PMID: 17177807]
[170]
McGarvey, P.B.; Hammond, J.; Dienelt, M.M.; Hooper, D.C.; Fu, Z.F.; Dietzschold, B.; Koprowski, H.; Michaels, F.H. Expression of the rabies virus glycoprotein in transgenic tomatoes. Biotechnology (N. Y.), 1995, 13(13), 1484-1487.
[PMID: 9636308]
[171]
Yang, H.; Li, Q.; Han, Z.; Hu, J. High level expression of recombinant human antithrombin in the mammary gland of rabbits by adenoviral vectors infection. Anim. Biotechnol., 2012, 23(2), 89-100.
[http://dx.doi.org/10.1080/10495398.2011.644647] [PMID: 22537058]
[172]
Xiao, B.; Li, Q.; Feng, B.; Han, Z.; Gao, D.; Zhao, R.; Li, J.; Li, K.; Zhi, X.; Yang, H.; Liu, Z. Expression of recombinant human nerve growth factor beta in milk of goats by recombinant replication-defective adenovirus. Appl. Biochem. Biotechnol., 2009, 157(3), 357-366.
[http://dx.doi.org/10.1007/s12010-008-8346-5] [PMID: 18754080]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 27
ISSUE: 2
Year: 2020
Page: [89 - 104]
Pages: 16
DOI: 10.2174/0929866526666191014151237
Price: $65

Article Metrics

PDF: 21
HTML: 3