Immunological aspects of using plant cells as delivery vehicles for oral vaccines

References

• Yusibov V, Streatfield SJ, Kushnir N. Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond. Hum Vaccin 2011;7(3):313-21
   PubMed Web of Science ®Google Scholar
• Yuki Y, Mejima M, Kurokawa S, et al. Induction of toxin-specific neutralizing immunity by molecularly uniform rice-based oral cholera toxin B subunit vaccine without plant-associated sugar modification. Plant Biotechnol J 2013;11(7):799-808
   PubMed Web of Science ®Google Scholar
• Tacket CO. Plant-based oral vaccines: results of human trials. Curr Top Microbiol Immunol 2009;332:103-17
   PubMed Web of Science ®Google Scholar
• Peterson RK, Arntzen CJ. On risk and plant-based biopharmaceuticals. Trends Biotechnol 2004;22(2):64-6
   PubMed Web of Science ®Google Scholar
• Hofbauer A, Stoger E. Subcellular accumulation and modification of pharmaceutical proteins in different plant tissues. Curr Pharm Des 2013;19(31):5495-502
   PubMed Web of Science ®Google Scholar
• Melnik S, Stoger E. Green factories for biopharmaceuticals. Curr Med Chem 2013;20(8):1038-46
   PubMed Web of Science ®Google Scholar
• Pasetti MF, Simon JK, Sztein MB, Levine MM. Immunology of gut mucosal vaccines. Immunol Rev 2011;239(1):125-48
   PubMed Web of Science ®Google Scholar
• Gebert A, Rothkotter HJ, Pabst R. M cells in Peyer’s patches of the intestine. Int Rev Cytol 1996;167:91-159
   PubMed Web of Science ®Google Scholar
• Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells, gateways for mucosal infection and immunization. Cell 1996;86(3):345-8
   PubMed Web of Science ®Google Scholar
• Soloff AC, Barratt-Boyes SM. Enemy at the gates: dendritic cells and immunity to mucosal pathogens. Cell Res 2010;20(8):872-85
   PubMed Web of Science ®Google Scholar
• Johansson-Lindbom B, Agace WW. Generation of gut-homing T cells and their localization to the small intestinal mucosa. Immunol Rev 2007;215:226-42
   PubMed Web of Science ®Google Scholar
• McGhee JR, Kunisawa J, Kiyono H. Gut lymphocyte migration, we are halfway ‘home’. Trends Immunol 2007;28(4):150-3
   PubMed Web of Science ®Google Scholar
• Mora JR, Iwata M, Eksteen B, et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006;314(5802):1157-60
   PubMed Web of Science ®Google Scholar
• Siewert C, Menning A, Dudda J, et al. Induction of organ-selective CD4+ regulatory T cell homing. Eur J Immunol 2007;37(4):978-89
   PubMed Web of Science ®Google Scholar
• Mestecky J, Nguyen H, Czerkinsky C, Kiyono H. Oral immunization: an update. Curr Opin Gastroenterol 2008;24(6):713-19
   Google Scholar
• Bilsborough J, George TC, Norment A, Viney JL. Mucosal CD8alpha+ DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 2003;108(4):481-92
   PubMed Web of Science ®Google Scholar
• Worbs T, Bode U, Yan S, et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 2006;203(3):519-27
   PubMed Web of Science ®Google Scholar
• Guetard D, Greco R, Cervantes Gonzalez M, et al. Immunogenicity and tolerance following HIV-1/HBV plant-based oral vaccine administration. Vaccine 2008;26(35):4477-85
   PubMed Web of Science ®Google Scholar
• Arakawa T, Yu J, Chong DK, et al. A plant-based cholera toxin B subunit-insulin fusion protein protects against the development of autoimmune diabetes. Nat Biotechnol 1998;16(10):934-8
   PubMed Web of Science ®Google Scholar
• Carter JE, Odumosu O, Langridge WHR. Expression of a ricin toxin B subunit: insulin fusion protein in edible plant tissues. Mol Biotechnol 2010;44(2):90-100
   PubMed Web of Science ®Google Scholar
• Li C, Jiang Y, Guo W, Liu Z. Production of a chimeric allergen derived from the major allergen group 1 of house dust mite species in Nicotiana benthamiana. Hum Immunol 2013;74(5):531-7
   PubMed Web of Science ®Google Scholar
• Lee CC, Ho H, Lee KT, et al. Construction of a Der p2-transgenic plant for the alleviation of airway inflammation. Cell Mol Immunol 2011;8(5):404-14
   PubMed Web of Science ®Google Scholar
• Takaiwa F. A rice-based edible vaccine expressing multiple T-cell epitopes to induce oral tolerance and inhibit allergy. Immunol Allergy Clin North Am 2007;27(1):129-39
   PubMed Web of Science ®Google Scholar
• Wakasa Y, Takagi H, Hirose S, et al. Oral immunotherapy with transgenic rice seed containing destructed Japanese cedar pollinosis. Plant Biotechnol J 2013;11(1):66-76
   PubMed Web of Science ®Google Scholar
• Gebril A, Alsaadi M, Acevedo R, et al. Optimizing efficacy of mucosal vaccines. Expert Rev Vaccines 2012;11(9):1139-55
   PubMed Web of Science ®Google Scholar
• Stevceva L, Ferrari MG. Mucosal adjuvants. Curr Pharm Des 2005;11(6):801-11
   PubMed Web of Science ®Google Scholar
• Ernst WA, Kim HJ, Tumpey TM, et al. Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine 2006;24(24):5158-68
   PubMed Web of Science ®Google Scholar
• Hasegawa H, Ichinohe T, Strong P, et al. Protection against influenza virus infection by intranasal administration of hemagglutinin vaccine with chitin microparticles as an adjuvant. J Med Virol 2005;75(1):130-6
   PubMed Web of Science ®Google Scholar
• Reddy ST, Swartz MA, Hubbell JA. Targeting dendritic cells with biomaterials, developing the next generation of vaccines. Trends Immunol 2006;27(12):573-9
   PubMed Web of Science ®Google Scholar
• Sharma S, Mukkur TK, Benson HA, Chen Y. Pharmaceutical aspects of intranasal delivery of vaccines using particulate systems. J Pharm Sci 2009;98(3):812-43
   PubMed Web of Science ®Google Scholar
• Alving CR. Immunologic aspects of liposomes: presentation and processing of liposomal proteinand phospholipid antigens. Biochim Biophys Acta 1992;1113(3-4):307-22
   PubMed Web of Science ®Google Scholar
• Brochu H, Polidori A, Pucci B, Vermette P. Drug delivery systems using immobilized intact liposomes: a comparative and critical review. Curr Drug Deliv 2004;1(3):299-312
   PubMedGoogle Scholar
• Gregoriadis G. Immunological adjuvants: a role for liposomes. Immunol Today 1990;11(3):89-97
   PubMedGoogle Scholar
• Fujkuyama Y, Tokuhara D, Kataoka K, et al. Novel vaccine development strategies for inducing mucosal immunity. Expert Rev Vaccines 2012;11(3):367-79
   PubMed Web of Science ®Google Scholar
• Alvarez ML, Pinyerd HL, Crisantes JD, et al. Plant-made subunit vaccine against pneumonic and bubonic plague is orally immunogenic in mice. Vaccine 2006;24(14):2477-90
   PubMed Web of Science ®Google Scholar
• Pelosi A, Shepherd R, Guzman GD, et al. The release and induced immune responses of a plant-made and delivered antigen in the mouse gut. Curr Drug Deliv 2011;8(6):612-21
   PubMed Web of Science ®Google Scholar
• De Guzman G, Walmsley AM, Webster DE, Hamill JD. Hairy roots cultures from different Solanaceous species have varying capacities to produce E. coli B-subunit heat-labile toxin antigen. Biotechnol Lett 2011;33(12):2495-502
   PubMed Web of Science ®Google Scholar
• Pelosi A, Piedrafita D, De Guzman G, et al. The effect of plant tissue and vaccine formulation on the oral immunogenicity of a model plant-made antigen in sheep. PLoS One 2012;7(12):e52907
   PubMed Web of Science ®Google Scholar
• Rosales-Mendoza S, Soria-Guerra RE, Moreno-Fierros L, et al. Immunogenicity of nuclear-encoded LTB:ST fusion protein from Escherichia coli expressed in tobacco plants. Plant Cell Rep 2011;30(6):1145-52
   PubMed Web of Science ®Google Scholar
• Kostrzak A, Cervantes Gonzalez M, Guetard D, et al. Oral administration of low doses of plant-based HBsAg induced antigen-specific IgAs and IgGs in mice, without increasing levels of regulatory T cells. Vaccine 2009;27(35):4798-807
   PubMed Web of Science ®Google Scholar
• Pniewski T, Kapusta J, Bociag P, et al. Low-dose oral immunization with lyophilized tissue of herbicide-resistant lettuce expressing hepatitis B surface antigen for prototype plant-derived vaccine tablet formulation. J Appl Genet 2011;52(2):125-36
   PubMed Web of Science ®Google Scholar
• Renukuntla J, Vadlapudi AD, Patel A, et al. Approaches for enhancing oral bioavailability of peptides and proteins. Int J Pharm 2013;447(1-2):75-93
   PubMed Web of Science ®Google Scholar
• Khan I, Twyman RM, Arcalis E, Stoger E. Using storage organelles for the accumulation and encapsulation of recombinant proteins. Biotechnol J 2012;7(9):1099-108
   PubMed Web of Science ®Google Scholar
• Kong Q, Richter L, Yang YF, et al. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci USA 2001;98(20):11539-44
   PubMed Web of Science ®Google Scholar
• Flint HJ, Bayer EA. Plant cell wall breakdown by anaerobic microorganisms from the Mammalian digestive tract. Ann N Y Acad Sci 2008;1125:280-8
   PubMed Web of Science ®Google Scholar
• Arcalis E, Stadlmann J, Rademacher T, et al. Plant species and organ influence the structure and subcellular localization of recombinant glycoproteins. Plant Mol Biol 2013;83(1-2):105-17
   PubMed Web of Science ®Google Scholar
• Hoebler C, Karinthi A, Devaux M-F, et al. Physical and chemical transformations of cereal food during oral digestion in human subjects. Br J Nutr 1998;80(5):429-36
   PubMed Web of Science ®Google Scholar
• MacDougall AJ, Selvedran RR. Chemistry, architecture, and composition of dietary fiber from plant cell walls. In: Cho SS, Dreher ML, editors. Handbook of dietary fiber. Marcel Dekker Inc; New York, USA: 2001. p. 281-319
   Google Scholar
• van den Berg H. Carotenoids: factors affecting bioavailability. In Biologically-active phytochemicals in food. In: Pfannhuaser W, Fenwick GR, Khokhar S, editors. Analysis, metabolism, bioavailability and function. The Royal Society of Chemistry; Cambridge, UK: 2001. p. 407-15
   Google Scholar
• Tovar J, Defrancisco A, Björck I, Asp NG. Relationship between microstructure and in vitro digestibility of starch in precooked leguminous seed flours. Food Structure 1991;10(1):19-26
   Web of Science ®Google Scholar
• Slaughter SL, Ellis PR, Butterworth PJ. An investigation of the action of porcine pancreatic α-amylase on native and gelatinised starches. Biochim Biophys Acta 2001;1525(1-2):29-36
   PubMed Web of Science ®Google Scholar
• Lemmens L, Van Buggenhout S, Van Loey AM, Hendrickx ME. Particle size reduction leading to cell wall rupture is more important for the β-carotene bioaccessibility of raw compared to thermally processed carrots. J Agric Food Chem 2010;58(24):12769-76
   PubMed Web of Science ®Google Scholar
• Licciardi PV, Underwood JR. Plant-derived medicines: a novel class of immunological adjuvants. Int Immunopharmacol 2011;11(3):390-8
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang W, Li N, et al. Activation of antigen presenting cells by immunostimulatory plant DNA: a natural resource for potential adjuvant. Vaccine 2002;20(21-22):2764-71
   PubMed Web of Science ®Google Scholar
• Sun HX, Xie Y, Ye YP. Advances in saponin-based adjuvants. Vaccine 2009;27(12):1787-96
   PubMed Web of Science ®Google Scholar
• Granell A, Fernández del-Carmen A, Orzáez D. In planta production of plant-derived and non-plant-derived adjuvants. Expert Rev Vaccines 2010;9(8):843-58
   PubMed Web of Science ®Google Scholar
• Ganguly T, Sainis KB. Inhibition of cellular immune responses by Tylophora indica in experimental models. Phytomedicine 2001;8:348-55
   PubMed Web of Science ®Google Scholar
• Berg JM, Tymoczko JL, Stryer L. Lectins are specific carbohydrate-binding proteins. In: Biochemistry. 5th edition). W H Freeman; NY, USA: 2002; Section 11.4
   Google Scholar
• Lavelle EC, Grant G, Pusztai A, et al. Mistletoe lectins enhance immune responses to intranasally co-administered herpes simplex virus glycoprotein D2. Immunology 2002;107(2):268-74
   PubMed Web of Science ®Google Scholar
• Manocha M, Pal PC, Chitralekha KT, et al. Enhanced mucosal and systemic immune response with intranasal immunization of mice with HIV peptides entrapped in PLG microparticles in combination with Ulex europaeus-I lectin as M cell target. Vaccine 2005;23(48–49):5599-617
   PubMed Web of Science ®Google Scholar
• Huang L, Ikejiri A, Shimizu Y, et al. Immunoadjuvant activity of crude lectin extracted from Momordica charantia seed. J Vet Med Sci 2008;70(5):533-5
   PubMed Web of Science ®Google Scholar
• Sharma R, van Damme EJM, Peumans WJ, et al. Lectin binding reveals divergent carbohydrate expression in human and mouse Peyer’s patches. Histochem Cell Biol 1996;105:459-65
   PubMed Web of Science ®Google Scholar
• Schepetkin IA, Quinn MT. Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol 2006;6(3):317-33
   PubMed Web of Science ®Google Scholar
• da Silva BP, de Medeiros Silva G, Parente JP. Chemical properties and adjuvant activity of a galactoglucomannan from Acrocomia aculeata. Carbohydr Polym 2009;75(3):380-4
   Web of Science ®Google Scholar
• Lobigs M, Pavy M, Hall RA, et al. An inactivated Vero cell-grown Japanese encephalitis vaccine formulated with Advax, a novel inulin-based adjuvant, induces protective neutralizing antibody against homologous and heterologous flaviviruses. J Gen Virol 2010;91(6):1407-17
   PubMed Web of Science ®Google Scholar
• Petrovsky N. Novel human polysaccharide adjuvants with dual Th1 and Th2 potentiating activity. Vaccine 2006;24(Suppl 2):S2-26-9
   Google Scholar
• Stertman L, Strindelius L, Sjöholm I. Starch microparticles as an adjuvant in immunisation: effect of route of administration on the immune response in mice. Vaccine 2004;22(21–22):2863-72
   PubMed Web of Science ®Google Scholar
• Popov SV, Golovchenko VV, Ovodova RG, et al. Characterisation of the oral adjuvant effect of lemnan, a pectic polysaccharide of Lemna minor L. Vaccine 2006;24:5413-19
   PubMed Web of Science ®Google Scholar
• Sparg SG, Light ME, van Staden J. Biological activities and. distribution of plant saponins. J Ethnopharmacol 2004;94(2–3):219-43
   PubMed Web of Science ®Google Scholar
• Bomford R, Stapleton M, Winsor S, et al. The control of the antibody isotype response to recombinant immunodeficiency virus gp120 antigen by adjuvants. AIDS Res Hum Retroviruses 1992;8(10):1765-71
   PubMed Web of Science ®Google Scholar
• Moreno CA, Rodriguez R, Oliveira GA, et al. Preclinical evaluation of a synthetic Plasmodium falciparum MAP malaria vaccine in Aotus monkeys and mice. Vaccine 1999;18(1-2):89-99
   PubMed Web of Science ®Google Scholar
• Waite DC, Jacobson EW, Ennis FA, et al. Three double-blind, randomized trials evaluating the safety and tolerance of different formulations of the saponin adjuvant QS-21. Vaccine 2001;19(28–29):3957-67
   PubMed Web of Science ®Google Scholar
• Pickering RJ, Smith SD, Strugnell RA, et al. Crude saponins improve the immune response to an oral plant-made measles vaccine. Vaccine 2006;24(2):144-50
   PubMed Web of Science ®Google Scholar
• Hernandez M, Cabrera-Ponce JL, Fragoso G, et al. A new highly effective anticysticercosis vaccine expressed in transgenic papaya. Vaccine 2007;25(21):4252-60
   PubMed Web of Science ®Google Scholar
• Chapagain BP, Wiesman Z. Phyto-saponins as a natural adjuvant for delivery of agromaterials through plant cuticle membranes. J Agric Food Chem 2006;54:6277-85
   PubMed Web of Science ®Google Scholar
• Otsuki N, Dang NH, Kumagai E, et al. Aqueous extract of Carica papaya leaves exhibits anti-tumor activity and immunomodulatory effects. J Ethnopharmacol 2009;127:760-7
   PubMed Web of Science ®Google Scholar
• Garg NK, Mangal S, Khambete H, Tyagi RK. Mucosal delivery of vaccines: role of mucoadhesive/biodegradable polymers. Recent Pat Drug Deliv Formul 2010;4:114-28
   PubMedGoogle Scholar
• Maurya SK, Pathak K, Bali V. Therapeutic potential of mucoadhesive drug delivery systems--an updated patent review. Recent Pat Drug Deliv Formul 2010;4:256-65
   PubMedGoogle Scholar
• Mangal S, Pawar D, Agrawal U, et al. Evaluation of mucoadhesive carrier adjuvant: Toward an oral anthrax vaccine. Artif Cells Nanomed Biotechnol 2013;42(1):47-57
   PubMed Web of Science ®Google Scholar
• Bosch D, Schots A. Plant glycans: friend or foe in vaccine development? Expert Rev Vaccines 2010;9(8):835-42
   PubMed Web of Science ®Google Scholar
• Rosales-Mendoza S, Orellana-Escobedo L, Romero-Maldonado A, et al. The potential of Physcomitrella patens as a platform for the production of plant-based vaccines. Expert Rev Vaccines 2014;13(2):203-12
   PubMed Web of Science ®Google Scholar
• Scotti N, Rybicki EP. Virus-like particles produced in plants as potential vaccines. Expert Rev Vaccines 2013;12(2):211-24
   PubMed Web of Science ®Google Scholar
• Siepmann F, Siepmann J, Walther M, et al. Polymer blends for controlled release coatings. J Control Release 2008;125(1):1-15
   PubMed Web of Science ®Google Scholar
• Felton LA, Porter SC. An update on pharmaceutical film coating for drug delivery. Expert Opin Drug Deliv 2013;10(4):421-35
   Google Scholar
• Kang TJ, Lee WS, Choi EG, et al. Mass production of somatic embryos expressing Escherichia coli heat-labile enterotoxin B subunit in Siberian ginseng. J Biotechnol 2006;121(2):124-33
   PubMed Web of Science ®Google Scholar
• Nojima J, Ishii-Katsuno R, Futai E, et al. Production of anti-amyloid β antibodies in mice fed rice expressing amyloid β. Biosci Biotechnol Biochem 2011;75(2):396-400
   PubMed Web of Science ®Google Scholar
• Protalix. Available from: www.protalix.com/development-pipeline/prx-112-oral-gaucher-disease.asp [Last accessed 18 November 2013]
   Google Scholar
• Medina-Bolivar F, Wright R, Funk V, et al. A non-toxic lectin for antigen delivery of plant-based mucosal vaccines. Vaccine 2003;21(9–10):997-1005
   PubMed Web of Science ®Google Scholar
• Teixeira CR, Cavassani KA, Gomes RB, et al. Potential of KM+ lectin in immunization against Leishmania amazonensis infection. Vaccine 2006;24(15):3001-8
   PubMed Web of Science ®Google Scholar
• Song SK, Moldoveanu Z, Nguyen HH, et al. Intranasal immunization with influenza virus and Korean mistletoe lectin C (KML-C) induces heterosubtypic immunity in mice. Vaccine 2007;25(34):6359-66
   PubMed Web of Science ®Google Scholar
• Fuentes P, Cooper PD, Barnadas R, et al. Use of g-inulin/liposomes/vitamin E adjuvant combination in contraceptive vaccines. Int J Pharm 2003;257(1–2):85-95
   PubMed Web of Science ®Google Scholar
• Rydell N, Sjöholm I. Oral vaccination against diphtheria using polyacryl starch microparticles as adjuvant. Vaccine 2004;22(9–10):1265-74
   PubMed Web of Science ®Google Scholar
• Sun HX, Wang H, Xu HS, Nia Y. Novel polysaccharide adjuvant from the roots of Actinidia eriantha with dual Th1 and Th2 potentiating activity. Vaccine 2009;27(30):3984-91
   PubMed Web of Science ®Google Scholar
• Sun YX. Immunological adjuvant effect of a water-soluble polysaccharide, CPP, from the roots of Codonopsis pilosula on the immune responses to ovalbumin in mice. Chem Biodivers 2009;6(6):890-6
   PubMed Web of Science ®Google Scholar
• Krivorutchenko YL, Andronovskaja IB, Hinkula J, et al. Study of the adjuvant activity of new MDP derivatives and purified saponins and their influence on HIV-1 replication in vitro. Vaccine 1997;15(12-13):1479-86
   PubMed Web of Science ®Google Scholar
• Estrada A, Katselis GS, Laarveld B, Barl B. Isolation and evaluation of immunological adjuvant activities of saponins from Polygala senega L. Comp Immunol Microbiol Infect Dis 2000;23(1):27-43
   PubMed Web of Science ®Google Scholar
• Sun XH. Adjuvant effect of Achyranthes bidentata saponins on specific antibody and cellular response to ovalbumin in mice. Vaccine 2006;24(17):3432-9
   PubMed Web of Science ®Google Scholar
• Silveira F, Cibulski SP, Varela AP, et al. Quillaja brasiliensis saponins are less toxic than Quil A and have similar properties when used as an adjuvant for a viral antigen preparation. Vaccine 2011;29(49):9177-82
   PubMed Web of Science ®Google Scholar