The role of plant expression platforms in biopharmaceutical development: possibilities for the future

References

• Fischer R, Stoger E, Schillberg S, et al. Plant-based production of biopharmaceuticals. Curr Opin Plant Biol. 2004 Apr;7(2):152–158.
   PubMed Web of Science ®Google Scholar
• Boehm R. Bioproduction of therapeutic proteins in the 21st century and the role of plants and plant cells as production platforms. Ann N Y Acad Sci. 2007 Apr;1102:121–134.
   PubMed Web of Science ®Google Scholar
• Twyman RM, Stoger E, Schillberg S, et al. Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 2003 Dec;21(12):570–578.
   PubMed Web of Science ®Google Scholar
• Takeyama N, Kiyono H, Yuki Y. Plant-based vaccines for animals and humans: recent advances in technology and clinical trials. Ther Adv Vaccines. 2015 Sep;3(5–6):139–154. .
   PubMedGoogle Scholar
• Loh HS, Green BJ, Yusibov V. Using transgenic plants and modified plant viruses for the development of treatments for human diseases. Curr Opin Virol. Oct 2017;26:81–89.
   PubMed Web of Science ®Google Scholar
• Haq TA, Mason HS, Clements JD, et al. Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science. 1995 May 5;268(5211):714–716.
   PubMed Web of Science ®Google Scholar
• Yu J, Langridge WH. A plant-based multicomponent vaccine protects mice from enteric diseases. Nat Biotechnol. 2001 Jun;19(6):548–552.
   PubMed Web of Science ®Google Scholar
• Saldaña S, Esquivel Guadarrama F, Olivera Flores Tde J, et al. Production of rotavirus-like particles in tomato (Lycopersicon esculentum L.) fruit by expression of capsid proteins VP2 and VP6 and immunological studies. Viral Immunol. 2006 Spring;19(1):42–53.
   PubMed Web of Science ®Google Scholar
• Pniewski T, Czyż M, Wyrwa K, et al. Micropropagation of transgenic lettuce containing HBsAg as a method of mass-scale production of standardised plant material for biofarming purposes. Plant Cell Rep. 2017 Jan;36(1):49–60. Epub 2016 Sep 21. .
   PubMed Web of Science ®Google Scholar
• 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 Mar;31(3):527–537. Epub 2011 Sep 22. .
   PubMed Web of Science ®Google Scholar
• Chan HT, Daniell H. Plant-made oral vaccines against human infectious diseases-Are we there yet? Plant Biotechnol J. 2015 Oct;13(8):1056–1070.
   PubMed Web of Science ®Google Scholar
• Lössl AG, Waheed MT. Chloroplast-derived vaccines against human diseases: achievements, challenges and scopes. Plant Biotechnol J. 2011 Jun;9(5):527–539. Epub 2011 Mar 2. .
   PubMed Web of Science ®Google Scholar
• Scotti N, Alagna F, Ferraiolo E, et al. High‐level expression of the HIV‐1 Pr55gag polyprotein in transgenic tobacco chloroplasts. Planta. 2009;229:1109–1122.
   PubMed Web of Science ®Google Scholar
• Chan HT, Xiao Y, Weldon WC, et al. Cold chain and virus-free chloroplast-made booster vaccine to confer immunity against different poliovirus serotypes. Plant Biotechnol J. 2016 Nov;14(11):2190–2200. Epub 2016 Jun 1.
   PubMed Web of Science ®Google Scholar
• Rosales-Mendoza S, Monreal-Escalante E, González-Ortega O, et al. Transplastomic plants yield a multicomponent vaccine against cysticercosis. J Biotechnol. 2018 Jan 20;266:124–132.
   PubMed Web of Science ®Google Scholar
• Kim HS, Jeon JH, Lee KJ, et al. N-glycosylation modification of plant-derived virus-like particles: an application in vaccines. Biomed Res Int. 2014:249519 Epub 2014 May 25. DOI:10.1155/2014/249519.
   PubMed Web of Science ®Google Scholar
• Margolin E, Chapman R, Williamson AL, et al. Production of complex viral glycoproteins in plants as vaccine immunogens. Plant Biotechnol J. 2018 Jun 11;16:1531–1545. Epub ahead of print.
   Web of Science ®Google Scholar
• Saxena P, Thuenemann EC, Sainsbury F, et al. Virus-derived vectors for the expression of multiple proteins in plants. Methods Mol Biol. 2016;1385:39–54.
   PubMedGoogle Scholar
• Gleba YY, Tusé D, Giritch A. Plant viral vectors for delivery by Agrobacterium. Curr Top Microbiol Immunol. 2014;375:155–192. Review.
   PubMed Web of Science ®Google Scholar
• Klimyuk V, Pogue G, Herz S, et al. Production of recombinant antigens and antibodies in Nicotiana benthamiana using ‘magnifection’ technology: GMP-compliant facilities for small- and large-scale manufacturing. Curr Top Microbiol Immunol. 2014;375:127–154.
   PubMed Web of Science ®Google Scholar
• Yoshimura K. Current status of HIV/AIDS in the ART era. J Infect Chemother. 2017 Jan;23(1):12–16. Epub 2016 Nov 5.
   PubMed Web of Science ®Google Scholar
• Lotter-Stark HC, Rybicki EP, Chikwamba RK. Plant made anti-HIV microbicides–a field of opportunity. Biotechnol Adv. 2012 Nov-Dec;30(6):1614–1626. Epub 2012 Jun 28.
   PubMed Web of Science ®Google Scholar
• Rosales-Mendoza S, Rubio-Infante N, Govea-Alonso DO, et al. Current status and perspectives of plant-based candidate vaccines against the human immunodeficiency virus (HIV). Plant Cell Rep. 2012 Mar;31(3):495–511. Epub 2011 Dec 13.
   PubMed Web of Science ®Google Scholar
• Cervera L, Gòdia F, Tarrés-Freixas F, et al. Production of HIV-1-based virus-like particles for vaccination: achievements and limits. Appl Microbiol Biotechnol. 2019 Sep;103(18):7367–7384. Epub 2019 Aug 1.
   PubMed Web of Science ®Google Scholar
• Hoelscher M, Tiller N, Teh AY, et al. High-level expression of the HIV entry inhibitor griffithsin from the plastid genome and retention of biological activity in dried tobacco leaves. Plant Mol Biol. 2018 Jul;97(4–5):357–370. Epub 2018 Jun 9.
   PubMed Web of Science ®Google Scholar
• Vamvaka E, Farré G, Molinos-Albert LM, et al. Unexpected synergistic HIV neutralization by a triple microbicide produced in rice endosperm. Proc Natl Acad Sci USA. 2018 Aug 14;115(33):E7854–E62. Epub 2018 Jul 30.
   PubMed Web of Science ®Google Scholar
• Rybicki EP. Plant-made vaccines and reagents for the one health initiative. Hum Vaccin Immunother. 2017 Dec 2;13(12):2912–2917. Epub 2017 Aug 28.
   PubMed Web of Science ®Google Scholar
• Pillet S, Couillard J, Trépanier S, et al. Immunogenicity and safety of a quadrivalent plant-derived virus like particle influenza vaccine candidate-Two randomized Phase II clinical trials in 18 to 49 and ≥50 years old adults. PLoS One. 2019 Jun 5;14(6):e0216533.
   PubMed Web of Science ®Google Scholar
• Makarkov AI, Chierzi S, Pillet S, et al. Plant-made virus-like particles bearing influenza hemagglutinin (HA) recapitulate early interactions of native influenza virions with human monocytes/macrophages. Vaccine. 2017 Aug 16;35(35 Pt B):4629–4636. Epub 2017 Jul 13.
   PubMed Web of Science ®Google Scholar
• Yusibov V, Kushnir N, Streatfield SJ. Advances and challenges in the development and production of effective plant-based influenza vaccines. Expert Rev Vaccines. 2015 Apr;14(4):519–535. Epub 2014 Dec 9.
   PubMed Web of Science ®Google Scholar
• Marsian J, Lomonossoff GP. Molecular pharming - VLPs made in plants. Curr Opin Biotechnol. 2016 Feb;37:201–206. Epub 2016 Jan 14.
   PubMed Web of Science ®Google Scholar
• D’Aoust MA, Couture MM, Charland N, et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and saferesponse to pandemic influenza. Plant Biotechnol J. 2010 Jun;8(5):607–619. Epub 2010 Feb 18.
   PubMed Web of Science ®Google Scholar
• Lindsay BJ, Bonar MM, Costas-Cancelas IN, et al. Morphological characterization of a plant-made virus-like particle vaccine bearing influenza virus hemagglutinins by electron microscopy. Vaccine. 2018 Apr 12;36(16):2147–2154. Epub 2018 Mar 14.
   PubMed Web of Science ®Google Scholar
• Márquez-Escobar VA, Rosales-Mendoza S, Beltrán-López JI, et al. Plant-based vaccines against respiratory diseases: current status and future prospects. Expert Rev Vaccines. 2017 Feb;16(2):137–149. Epub 2016 Sep 16.
   PubMed Web of Science ®Google Scholar
• Coltart CE, Lindsey B, Ghinai I, et al. The Ebola outbreak, 2013-2016: old lessons for new epidemics. Philos Trans R Soc Lond B Biol Sci. 2017 May 26;372(1721):ii: 20160297.
   Web of Science ®Google Scholar
• McCarthy M. US signs contract with ZMapp maker to accelerate development of the Ebola drug. BMJ. 2014 Sep 4;349: g5488.
   PubMed Web of Science ®Google Scholar
• Zeitlin L, Pettitt J, Scully C, et al. Enhanced potency of a fucose‐free monoclonal antibody being developed as an Ebola virus immunoprotectant. Proc Natl Acad Sci USA. 2011;108:20690–20694.
   PubMed Web of Science ®Google Scholar
• Monreal-Escalante E, Ramos-Vega AA, Salazar-González JA, et al. Expression of the VP40 antigen from the Zaire ebolavirus in tobacco plants. Planta. 2017 Jul;246(1):123–132. Epub 2017 Apr 7.
   PubMed Web of Science ®Google Scholar
• Rosales-Mendoza S, Nieto-Gómez R, Angulo C. A perspective on the development of plant-made vaccines in the fight against ebola virus. Front Immunol. 2017 Mar 10;8:252.
   PubMed Web of Science ®Google Scholar
• Triunfol M. A new mosquito-borne threat to pregnant women in Brazil. Lancet Infect Dis. 2016 Feb;16(2):156–157.
   PubMed Web of Science ®Google Scholar
• Yang M, Sun H, Lai H, et al. Plant-produced Zika virus envelope protein elicits neutralizing immune responses that correlate with protective immunity against Zika virus in mice. Plant Biotechnol J. 2018 Feb;16(2):572–580. Epub 2017 Aug 23.
   PubMed Web of Science ®Google Scholar
• Grubaugh ND, Ebel GD. Dynamics of West Nile virus evolution in mosquito vectors. Curr Opin Virol. 2016 Dec;21:132–138. Epub 2016 Oct 24.
   PubMed Web of Science ®Google Scholar
• Lai H, Paul AM, Sun H, et al. A plant-produced vaccine protects mice against lethal West Nile virus infection without enhancing Zika or dengue virus infectivity. Vaccine. 2018 Mar 27;36(14):1846–1852. Epub 2018 Feb 26.
   PubMed Web of Science ®Google Scholar
• Chen Q. Plant-made vaccines against West Nile virus are potent, safe, and economically feasible. Biotechnol J. 2015 May;10(5):671–680. Epub 2015 Feb 9.
   PubMed Web of Science ®Google Scholar
• Mbewana S, Meyers AE, Rybicki EP. Chimaeric rift valley fever virus-like particle vaccine candidate production in nicotiana benthamiana. Biotechnol J. 2018Nov;28:e1800238.
   Google Scholar
• Kalbina I, Lagerqvist N, Moiane B, et al. Arabidopsis thaliana plants expressing Rift Valley fever virus antigens: mice exhibit systemic immune responses as the result of oral administration of the transgenic plants. Protein Expr Purif. 2016 Nov;127:61–67. Epub 2016 Jul 8.
   PubMed Web of Science ®Google Scholar
• Salazar-González JA, Angulo C, Rosales-Mendoza S. Chikungunya virus vaccines: current strategies and prospects for developing plant-made vaccines. Vaccine. 2015 Jul 17;33(31):3650–3658. Epub 2015 Jun 12.
   PubMed Web of Science ®Google Scholar
• Cardona-Ospina JA, Sepúlveda-Arias JC, Mancilla L, et al. Plant expression systems, a budding way to confront chikungunya and Zika in developing countries? F1000Res. 2016 Aug 31;5:2121. eCollection 2016.
   PubMedGoogle Scholar
• Hemida MG, Elmoslemany A, Al-Hizab F, et al. Camels and the transmission of Middle East respiratory syndrome coronavirus (MERS-CoV). Transbound Emerg Dis. 2017 Apr;64(2):344–353. Epub 2015 Aug 10.
   PubMed Web of Science ®Google Scholar
• Posgai AL, Wasserfall CH, Kwon KC, et al. Plant-based vaccines for oral delivery of type 1 diabetes-related autoantigens: evaluating oral tolerance mechanisms and disease prevention in NOD mice. Sci Rep. 2017 Feb 13;7: 42372.
   PubMed Web of Science ®Google Scholar
• Ishiura S, Yoshida T. Plant-based vaccines for Alzheimer’s disease. Proc Jpn Acad Ser B Phys Biol Sci. 2019 Jun 11;95(6):290–294.
   PubMed Web of Science ®Google Scholar
• Röder J, Fischer R, Commandeur U. Adoption of the 2A ribosomal skip principle to tobacco mosaic virus for peptide display. Front Plant Sci. 2017 Jun 28;8:1125.
   PubMed Web of Science ®Google Scholar
• Mechtcheriakova IA, Eldarov MA, Nicholson L, et al. The use of viral vectors to produce hepatitis B virus core particles in plants. J Virol Methods. 2006;131:10–15.
   PubMed Web of Science ®Google Scholar
• Shukla S, Myers JT, Woods SE, et al. Plant viral nanoparticles-based HER2 vaccine: immune response influenced by differential transport, localization and cellular interactions of particulate carriers. Biomaterials. 2017 Mar;121:15–27. Epub 2016 Dec 27.
   PubMed Web of Science ®Google Scholar
• Yusibov V, Streatfield SJ, Kushnir N, et al. Hybrid viral vectors for vaccine and antibody production in plants. Curr Pharm Des. 2013;19(31): 5574–5586. Review.
   PubMed Web of Science ®Google Scholar
• Czapar AE, Steinmetz NF. Plant viruses and bacteriophages for drug delivery in medicine and biotechnology. Curr Opin Chem Biol. 2017 Jun;38:108–116. Epub 2017 Apr 17.
   PubMed Web of Science ®Google Scholar
• Eiben S, Koch C, Altintoprak K, et al. Plant virus-based materials for biomedical applications: trends and prospects. Adv Drug Deliv Rev. 2018 Aug 31. ii: S0169-409X(18)30209-6. DOI:10.1016/j.addr.2018.08.011.
   PubMed Web of Science ®Google Scholar
• Hefferon KL. Repurposing Plant Virus Nanoparticles. Vaccines (Basel). 2018 Feb 14;6(1):ii: E11.
   PubMed Web of Science ®Google Scholar
• Lizotte PH, Wen AM, Sheen MR, et al. In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer. Nat Nanotechnol. 2016;11:295–303.
   PubMed Web of Science ®Google Scholar
• Bruckman MA, Czapar AE, Steinmetz NF. Drug-loaded plant-virus based nanoparticles for cancer drug delivery. Methods Mol Biol. 2018;1776:425–436. .
   PubMedGoogle Scholar
• Madden AJ, Oberhardt B, Lockney D, et al. Pharmacokinetics and efficacy of doxorubicin-loaded plant virus nanoparticles in preclinical models of cancer. Nanomedicine (Lond). 2017 Oct;12(20):2519–2532. Epub 2017 Sep 27.
   PubMed Web of Science ®Google Scholar
• Holtz BR, Berquist BR, Bennett LD, et al. Commercial-scale biotherapeutics manufacturing facility for plant-made pharmaceuticals. Plant Biotechnol J. 2015 Oct;13(8):1180–1190.
   PubMed Web of Science ®Google Scholar
• Schmidt JA, McGrath JM, Hanson MR, et al. Field-grown tobacco plants maintain robust growth while accumulating large quantities of a bacterial cellulase in chloroplasts. Nat Plants. 2019 Jul;5(7):715–721. Epub 2019 Jul 8.
   PubMed Web of Science ®Google Scholar
• Phoolcharoen W, Dye JM, Kilbourne J, et al. A nonreplicating subunit vaccine protects mice against lethal Ebola virus challenge. Proc Natl Acad Sci USA. 2011;108:20695–20700.
   PubMed Web of Science ®Google Scholar