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Review

Plant-derived virus-like particles as vaccines

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Pages 26-49 | Received 20 Jul 2012, Accepted 13 Sep 2012, Published online: 20 Sep 2012

References

  • Roldão A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. Virus-like particles in vaccine development. Expert Rev Vaccines 2010; 9:1149 - 76; http://dx.doi.org/10.1586/erv.10.115; PMID: 20923267
  • Chackerian B. Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 2007; 6:381 - 90; http://dx.doi.org/10.1586/14760584.6.3.381; PMID: 17542753
  • Townsend A, Bodmer H. Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol 1989; 7:601 - 24; http://dx.doi.org/10.1146/annurev.iy.07.040189.003125; PMID: 2469442
  • Kovacsovics-Bankowski M, Clark K, Benacerraf B, Rock KL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci USA 1993; 90:4942 - 6; http://dx.doi.org/10.1073/pnas.90.11.4942; PMID: 8506338
  • Bachmann MF, Lutz MB, Layton GT, Harris SJ, Fehr T, Rescigno M, et al. Dendritic cells process exogenous viral proteins and virus-like particles for class I presentation to CD8+ cytotoxic T lymphocytes. Eur J Immunol 1996; 26:2595 - 600; http://dx.doi.org/10.1002/eji.1830261109; PMID: 8921944
  • Fifis T, Gamvrellis A, Crimeen-Irwin B, Pietersz GA, Li J, Mottram PL, et al. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J Immunol 2004; 173:3148 - 54; PMID: 15322175
  • Roozendaal R, Mebius RE, Kraal G. The conduit system of the lymph node. Int Immunol 2008; 20:1483 - 7; http://dx.doi.org/10.1093/intimm/dxn110; PMID: 18824503
  • Lenz P, Day PM, Pang YY, Frye SA, Jensen PN, Lowy DR, et al. Papillomavirus-like particles induce acute activation of dendritic cells. J Immunol 2001; 166:5346 - 55; PMID: 11313370
  • Bosio CM, Moore BD, Warfield KL, Ruthel G, Mohamadzadeh M, Aman MJ, et al. Ebola and Marburg virus-like particles activate human myeloid dendritic cells. Virology 2004; 326:280 - 7; http://dx.doi.org/10.1016/j.virol.2004.05.025; PMID: 15302213
  • Bachmann MF, Zinkernagel RM. The influence of virus structure on antibody responses and virus serotype formation. Immunol Today 1996; 17:553 - 8; http://dx.doi.org/10.1016/S0167-5699(96)10066-9; PMID: 8991286
  • Fehr T, Skrastina D, Pumpens P, Zinkernagel RM. T cell-independent type I antibody response against B cell epitopes expressed repetitively on recombinant virus particles. Proc Natl Acad Sci USA 1998; 95:9477 - 81; http://dx.doi.org/10.1073/pnas.95.16.9477; PMID: 9689105
  • Bachmann MF, Rohrer UH, Kündig TM, Bürki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science 1993; 262:1448 - 51; http://dx.doi.org/10.1126/science.8248784; PMID: 8248784
  • Bachmann MF, Zinkernagel RM. Neutralizing antiviral B cell responses. Annu Rev Immunol 1997; 15:235 - 70; http://dx.doi.org/10.1146/annurev.immunol.15.1.235; PMID: 9143688
  • Chang MH, Chen CJ, Lai MS, Hsu HM, Wu TC, Kong MS, et al, Taiwan Childhood Hepatoma Study Group. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. N Engl J Med 1997; 336:1855 - 9; http://dx.doi.org/10.1056/NEJM199706263362602; PMID: 9197213
  • Mao C, Koutsky LA, Ault KA, Wheeler CM, Brown DR, Wiley DJ, et al. Efficacy of human papillomavirus-16 vaccine to prevent cervical intraepithelial neoplasia: a randomized controlled trial. Obstet Gynecol 2006; 107:18 - 27; http://dx.doi.org/10.1097/01.AOG.0000192397.41191.fb; PMID: 16394035
  • Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, et al, HPV Vaccine Study group. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 2006; 367:1247 - 55; http://dx.doi.org/10.1016/S0140-6736(06)68439-0; PMID: 16631880
  • Pattenden LK, Middelberg APJ, Niebert M, Lipin DI. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol 2005; 23:523 - 9; http://dx.doi.org/10.1016/j.tibtech.2005.07.011; PMID: 16084615
  • Grgacic EVL, Anderson DA. Virus-like particles: passport to immune recognition. Methods 2006; 40:60 - 5; http://dx.doi.org/10.1016/j.ymeth.2006.07.018; PMID: 16997714
  • Edman JC, Hallewell RA, Valenzuela P, Goodman HM, Rutter WJ. Synthesis of hepatitis B surface and core antigens in E. coli. Nature 1981; 291:503 - 6; http://dx.doi.org/10.1038/291503a0; PMID: 6262658
  • Michel ML, Tiollais P. Hepatitis B vaccines: protective efficacy and therapeutic potential. Pathol Biol (Paris) 2010; 58:288 - 95; http://dx.doi.org/10.1016/j.patbio.2010.01.006; PMID: 20382485
  • Wildt S, Gerngross TU. The humanization of N-glycosylation pathways in yeast. Nat Rev Microbiol 2005; 3:119 - 28; http://dx.doi.org/10.1038/nrmicro1087; PMID: 15685223
  • Harrison RL, Jarvis DL, Bryony C. Bonning KMaAJS. Protein N-Glycosylation in the Baculovirus-Insect Cell Expression System and Engineering of Insect Cells to Produce “Mammalianized” Recombinant Glycoproteins. Advances in Virus Research: Academic Press, 2006:159-91.
  • Pushko P, Tumpey TM, Bu F, Knell J, Robinson R, Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 2005; 23:5751 - 9; http://dx.doi.org/10.1016/j.vaccine.2005.07.098; PMID: 16143432
  • Chen Q. Expression and Purification of Pharmaceutical Proteins in Plants Biological Engineering 2008; 1:291 - 321
  • Chen Q. Expression and manufacture of pharmaceutical proteins in genetically engineered horticultural plants. In: Mou B, Scorza R, eds. Transgenic Horticultural Crops: Challenges and Opportunities - Essays by Experts. Boca Raton: Taylor & Francis 2011:86-126.
  • Chen Q. Turning a new leaf. European Biopharm Rev 2011; 2:64 - 8
  • Lai H, Chen Q. Bioprocessing of plant-derived virus-like particles of Norwalk virus capsid protein under current Good Manufacture Practice regulations. Plant Cell Rep 2012; 31:573 - 84; http://dx.doi.org/10.1007/s00299-011-1196-6; PMID: 22134876
  • Faye L, Gomord V. Success stories in molecular farming-a brief overview. Plant Biotechnol J 2010; 8:525 - 8; http://dx.doi.org/10.1111/j.1467-7652.2010.00521.x; PMID: 20500680
  • Lai H, Engle M, Fuchs A, Keller T, Johnson S, Gorlatov S, et al. Monoclonal antibody produced in plants efficiently treats West Nile virus infection in mice. Proc Natl Acad Sci USA 2010; 107:2419 - 24; http://dx.doi.org/10.1073/pnas.0914503107; PMID: 20133644
  • Lai H, He J, Engle M, Diamond MS, Chen Q. Robust production of virus-like particles and monoclonal antibodies with geminiviral replicon vectors in lettuce. Plant Biotechnol J 2012; 10:95 - 104; http://dx.doi.org/10.1111/j.1467-7652.2011.00649.x; PMID: 21883868
  • Davies HM. Review article: commercialization of whole-plant systems for biomanufacturing of protein products: evolution and prospects. Plant Biotechnol J 2010; 8:845 - 61; http://dx.doi.org/10.1111/j.1467-7652.2010.00550.x; PMID: 20731788
  • Chen Q, Tacket CO, Mason H, Mor T, Cardineau GA, Arntzen C. Subunit vaccines produced using plant biotechnology. In: Levine MM, ed. New Generation Vaccines. New York: Informa Healthcare USA, Inc., 2009:306-15.
  • Komarova TV, Baschieri S, Donini M, Marusic C, Benvenuto E, Dorokhov YL. Transient expression systems for plant-derived biopharmaceuticals. Expert Rev Vaccines 2010; 9:859 - 76; http://dx.doi.org/10.1586/erv.10.85; PMID: 20673010
  • Lico C, Chen Q, Santi L. Viral vectors for production of recombinant proteins in plants. J Cell Physiol 2008; 216:366 - 77; http://dx.doi.org/10.1002/jcp.21423; PMID: 18330886
  • Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol Bioeng 2009; 103:706 - 14; http://dx.doi.org/10.1002/bit.22299; PMID: 19309755
  • Santi L, Batchelor L, Huang Z, Hjelm B, Kilbourne J, Arntzen CJ, et al. An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 2008; 26:1846 - 54; http://dx.doi.org/10.1016/j.vaccine.2008.01.053; PMID: 18325641
  • He J, Lai H, Brock C, Chen Q.. A Novel System for Rapid and Cost-Effective Production of Detection and Diagnostic Reagents of West Nile Virus in Plants. J Biomedicine and Biotechnology 2012; 2012:1 - 10
  • Saldaña S, Esquivel Guadarrama F, Olivera Flores TdeJ, Arias N, López S, Arias C, 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; 19:42 - 53; http://dx.doi.org/10.1089/vim.2006.19.42; PMID: 16553549
  • Yang Y, Li X, Yang H, Qian Y, Zhang Y, Fang R, et al. Immunogenicity and virus-like particle formation of rotavirus capsid proteins produced in transgenic plants. Sci China Life Sci 2011; 54:82 - 9; http://dx.doi.org/10.1007/s11427-010-4104-3; PMID: 21104033
  • Santi L, Huang Z, Mason H. Virus-like particles production in green plants. Methods 2006; 40:66 - 76; http://dx.doi.org/10.1016/j.ymeth.2006.05.020; PMID: 16997715
  • Tacket CO, Pasetti MF, Edelman R, Howard JA, Streatfield S. Immunogenicity of recombinant LT-B delivered orally to humans in transgenic corn. Vaccine 2004; 22:4385 - 9; http://dx.doi.org/10.1016/j.vaccine.2004.01.073; PMID: 15474732
  • Kapusta J, Modelska A, Figlerowicz M, Pniewski T, Letellier M, Lisowa O, et al. A plant-derived edible vaccine against hepatitis B virus. FASEB J 1999; 13:1796 - 9; PMID: 10506582
  • Yusibov V, Hooper DC, Spitsin SV, Fleysh N, Kean RB, Mikheeva T, et al. Expression in plants and immunogenicity of plant virus-based experimental rabies vaccine. Vaccine 2002; 20:3155 - 64; http://dx.doi.org/10.1016/S0264-410X(02)00260-8; PMID: 12163267
  • Villa LL, Costa RLR, Petta CA, Andrade RP, Ault KA, Giuliano AR, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 2005; 6:271 - 8; http://dx.doi.org/10.1016/S1470-2045(05)70101-7; PMID: 15863374
  • Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, et al, GlaxoSmithKline HPV Vaccine Study Group. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004; 364:1757 - 65; http://dx.doi.org/10.1016/S0140-6736(04)17398-4; PMID: 15541448
  • Herbst-Kralovetz M, Mason HS, Chen Q. Norwalk virus-like particles as vaccines. Expert Rev Vaccines 2010; 9:299 - 307; http://dx.doi.org/10.1586/erv.09.163; PMID: 20218858
  • Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science 1999; 286:287 - 90; http://dx.doi.org/10.1126/science.286.5438.287; PMID: 10514371
  • Jiang X, Wang M, Graham DY, Estes MK. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol 1992; 66:6527 - 32; PMID: 1328679
  • Ausar SF, Foubert TR, Hudson MH, Vedvick TS, Middaugh CR. Conformational stability and disassembly of Norwalk virus-like particles. Effect of pH and temperature. J Biol Chem 2006; 281:19478 - 88; http://dx.doi.org/10.1074/jbc.M603313200; PMID: 16675449
  • Huang Z, Elkin G, Maloney BJ, Beuhner N, Arntzen CJ, Thanavala Y, et al. Virus-like particle expression and assembly in plants: hepatitis B and Norwalk viruses. Vaccine 2005; 23:1851 - 8; http://dx.doi.org/10.1016/j.vaccine.2004.11.017; PMID: 15734055
  • Zhang X, Buehner NA, Hutson AM, Estes MK, Mason HS. Tomato is a highly effective vehicle for expression and oral immunization with Norwalk virus capsid protein. Plant Biotechnol J 2006; 4:419 - 32; http://dx.doi.org/10.1111/j.1467-7652.2006.00191.x; PMID: 17177807
  • Chen Q, He J, Phoolcharoen W, Mason HS. Geminiviral vectors based on bean yellow dwarf virus for production of vaccine antigens and monoclonal antibodies in plants. Hum Vaccin 2011; 7:331 - 8; http://dx.doi.org/10.4161/hv.7.3.14262; PMID: 21358270
  • Keating GM, Noble S. Recombinant hepatitis B vaccine (Engerix-B): a review of its immunogenicity and protective efficacy against hepatitis B. Drugs 2003; 63:1021 - 51; http://dx.doi.org/10.2165/00003495-200363100-00006; PMID: 12699402
  • Venters C, Graham W, Cassidy W. Recombivax-HB: perspectives past, present and future. Expert Rev Vaccines 2004; 3:119 - 29; http://dx.doi.org/10.1586/14760584.3.2.119; PMID: 15056038
  • Wynne SA, Crowther RA, Leslie AGW. The crystal structure of the human hepatitis B virus capsid. Mol Cell 1999; 3:771 - 80; http://dx.doi.org/10.1016/S1097-2765(01)80009-5; PMID: 10394365
  • Lobaina Y, Palenzuela D, Pichardo D, Muzio V, Guillén G, Aguilar JC. Immunological characterization of two hepatitis B core antigen variants and their immunoenhancing effect on co-delivered hepatitis B surface antigen. Mol Immunol 2005; 42:289 - 94; http://dx.doi.org/10.1016/j.molimm.2004.09.005; PMID: 15589316
  • Aguilar JC, Lobaina Y, Muzio V, García D, Pentón E, Iglesias E, et al. Development of a nasal vaccine for chronic hepatitis B infection that uses the ability of hepatitis B core antigen to stimulate a strong Th1 response against hepatitis B surface antigen. Immunol Cell Biol 2004; 82:539 - 46; http://dx.doi.org/10.1111/j.0818-9641.2004.01278.x; PMID: 15479440
  • Tsuda S, Yoshioka K, Tanaka T, Iwata A, Yoshikawa A, Watanabe Y, et al. Application of the human hepatitis B virus core antigen from transgenic tobacco plants for serological diagnosis. Vox Sang 1998; 74:148 - 55; http://dx.doi.org/10.1046/j.1423-0410.1998.7430148.x; PMID: 9595641
  • Huang Z, Santi L, LePore K, Kilbourne J, Arntzen CJ, Mason HS. Rapid, high-level production of hepatitis B core antigen in plant leaf and its immunogenicity in mice. Vaccine 2006; 24:2506 - 13; http://dx.doi.org/10.1016/j.vaccine.2005.12.024; PMID: 16417953
  • Warzecha H, Mason HS, Lane C, Tryggvesson A, Rybicki E, Williamson AL, et al. Oral immunogenicity of human papillomavirus-like particles expressed in potato. J Virol 2003; 77:8702 - 11; http://dx.doi.org/10.1128/JVI.77.16.8702-8711.2003; PMID: 12885889
  • Varsani AWA-L, Williamson AL, Rose RC, Jaffer M, Rybicki EP. Expression of Human papillomavirus type 16 major capsid protein in transgenic Nicotiana tabacum cv. Xanthi. Arch Virol 2003; 148:1771 - 86; http://dx.doi.org/10.1007/s00705-003-0119-4; PMID: 14505089
  • Varsani A, Williamson A-L, Stewart D, Rybicki EP. Transient expression of Human papillomavirus type 16 L1 protein in Nicotiana benthamiana using an infectious tobamovirus vector. Virus Res 2006; 120:91 - 6; http://dx.doi.org/10.1016/j.virusres.2006.01.022; PMID: 16530873
  • Fernández-San Millán A, Ortigosa SM, Hervás-Stubbs S, Corral-Martínez P, Seguí-Simarro JM, Gaétan J, et al. Human papillomavirus L1 protein expressed in tobacco chloroplasts self-assembles into virus-like particles that are highly immunogenic. Plant Biotechnol J 2008; 6:427 - 41; http://dx.doi.org/10.1111/j.1467-7652.2008.00338.x; PMID: 18422886
  • Maclean J, Koekemoer M, Olivier AJ, Stewart D, Hitzeroth II, Rademacher T, et al. Optimization of human papillomavirus type 16 (HPV-16) L1 expression in plants: comparison of the suitability of different HPV-16 L1 gene variants and different cell-compartment localization. J Gen Virol 2007; 88:1460 - 9; http://dx.doi.org/10.1099/vir.0.82718-0; PMID: 17412974
  • Šmídková M, Müller M, Thönes N, Piuko K, Angelisová P, Velemínský J, et al. Transient expression of human papillomavirus type 16 virus-like particles in tobacco and tomato using a tobacco rattle virus expression vector. Biol Plant 2010; 54:451 - 60; http://dx.doi.org/10.1007/s10535-010-0081-4
  • Biemelt S, Sonnewald U, Galmbacher P, Willmitzer L, Müller M. Production of human papillomavirus type 16 virus-like particles in transgenic plants. J Virol 2003; 77:9211 - 20; http://dx.doi.org/10.1128/JVI.77.17.9211-9220.2003; PMID: 12915537
  • Warzecha H, Mason HS, Lane C, Tryggvesson A, Rybicki E, Williamson AL, et al. Oral immunogenicity of human papillomavirus-like particles expressed in potato. J Virol 2003; 77:8702 - 11; http://dx.doi.org/10.1128/JVI.77.16.8702-8711.2003; PMID: 12885889
  • Zheng H, Yu L, Wei C, Hu D, Shen Y, Chen Z, et al. Assembly of double-shelled, virus-like particles in transgenic rice plants expressing two major structural proteins of rice dwarf virus. J Virol 2000; 74:9808 - 10; http://dx.doi.org/10.1128/JVI.74.20.9808-9810.2000; PMID: 11000259
  • Maloney BJ , Takeda N, Suzaki Y, Ami Y, Li TC, Miyamura T, Arntzen CJ, et al. Challenges in creating a vaccine to prevent hepatitis E. Vaccine 2005; 23:1870 - 4; PMID: 15734058
  • Bragard C, Duncan GH, Wesley SV, Naidu RA, Mayo MA. Virus-like particles assemble in plants and bacteria expressing the coat protein gene of Indian peanut clump virus. J Gen Virol 2000; 81:267 - 72; PMID: 10640566
  • Patzer EJ, Nakamura GR, Yaffe A. Intracellular transport and secretion of hepatitis B surface antigen in mammalian cells. J Virol 1984; 51:346 - 53; PMID: 6748160
  • Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol 2007; 18:537 - 45; http://dx.doi.org/10.1016/j.copbio.2007.10.013; PMID: 18083549
  • Krugman S, Overby LR, Mushahwar IK, Ling CM, Frösner GG, Deinhardt F. Viral hepatitis, type B. Studies on natural history and prevention re-examined. N Engl J Med 1979; 300:101 - 6; http://dx.doi.org/10.1056/NEJM197901183000301; PMID: 758598
  • Mason HS, Lam DM, Arntzen CJ. Expression of hepatitis B surface antigen in transgenic plants. Proc Natl Acad Sci USA 1992; 89:11745 - 9; http://dx.doi.org/10.1073/pnas.89.24.11745; PMID: 1465391
  • Streatfield SJ. Mucosal immunization using recombinant plant-based oral vaccines. Methods 2006; 38:150 - 7; http://dx.doi.org/10.1016/j.ymeth.2005.09.013; PMID: 16431131
  • Thanavala Y, Yang YF, Lyons P, Mason HS, Arntzen C. Immunogenicity of transgenic plant-derived hepatitis B surface antigen. Proc Natl Acad Sci USA 1995; 92:3358 - 61; http://dx.doi.org/10.1073/pnas.92.8.3358; PMID: 7724566
  • Kong Q, Richter L, Yang YF, Arntzen CJ, Mason HS, Thanavala Y. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci USA 2001; 98:11539 - 44; http://dx.doi.org/10.1073/pnas.191617598; PMID: 11553782
  • Lou XM, Yao QH, Zhang Z, Peng RH, Xiong AS, Wang HK. Expression of the human hepatitis B virus large surface antigen gene in transgenic tomato plants. Clin Vaccine Immunol 2007; 14:464 - 9; http://dx.doi.org/10.1128/CVI.00321-06; PMID: 17314228
  • Pniewski T, Kapusta J, Bociąg P, Kostrzak A, Fedorowicz-Strońska O, Czyż M, et al. Plant expression, lyophilisation and storage of HBV medium and large surface antigens for a prototype oral vaccine formulation. Plant Cell Rep 2012; 31:585 - 95; http://dx.doi.org/10.1007/s00299-011-1223-7; PMID: 22246107
  • Kang SM, Song JM, Quan FS, Compans RW. Influenza vaccines based on virus-like particles. Virus Res 2009; 143:140 - 6; http://dx.doi.org/10.1016/j.virusres.2009.04.005; PMID: 19374929
  • Chen BJ, Leser GP, Morita E, Lamb RA. Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J Virol 2007; 81:7111 - 23; http://dx.doi.org/10.1128/JVI.00361-07; PMID: 17475660
  • Bright RA, Carter DM, Daniluk S, Toapanta FR, Ahmad A, Gavrilov V, et al. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007; 25:3871 - 8; http://dx.doi.org/10.1016/j.vaccine.2007.01.106; PMID: 17337102
  • D’Aoust MA, Couture MM, Charland N, Trépanier S, Landry N, Ors F, et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J 2010; 8:607 - 19; http://dx.doi.org/10.1111/j.1467-7652.2009.00496.x; PMID: 20199612
  • Saint-Jore-Dupas C, Faye L, Gomord V. From planta to pharma with glycosylation in the toolbox. Trends Biotechnol 2007; 25:317 - 23; http://dx.doi.org/10.1016/j.tibtech.2007.04.008; PMID: 17493697
  • D’Aoust MA, Lavoie PO, Couture MM, Trépanier S, Guay JM, Dargis M, et al. 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; 6:930 - 40; http://dx.doi.org/10.1111/j.1467-7652.2008.00384.x; PMID: 19076615
  • Shoji Y, Farrance CE, Bautista J, Bi H, Musiychuk K, Horsey A, et al. A plant-based system for rapid production of influenza vaccine antigens. Influenza Other Respi Viruses 2012; 6:204 - 10; http://dx.doi.org/10.1111/j.1750-2659.2011.00295.x; PMID: 21974811
  • D'Aoust M, Couture M, Ors F, Trépanier S, Lavoie P-O, Dargis M, et al. Recombinant influenza virus-like particles (VLPs) produced in transgenic plants expressing hemagglutinin. International Patent application WO2009/076778 2009.
  • D’Aoust MA, Couture MM, Charland N, Trépanier S, Landry N, Ors F, et al. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol J 2010; 8:607 - 19; http://dx.doi.org/10.1111/j.1467-7652.2009.00496.x; PMID: 20199612
  • Landry N, Ward BJ, Trépanier S, Montomoli E, Dargis M, Lapini G, et al. Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS ONE 2010; 5:e15559; http://dx.doi.org/10.1371/journal.pone.0015559; PMID: 21203523
  • Meyers A, Chakauya E, Shephard E, Tanzer FL, Maclean J, Lynch A, et al. Expression of HIV-1 antigens in plants as potential subunit vaccines. BMC Biotechnol 2008; 8:53; http://dx.doi.org/10.1186/1472-6750-8-53; PMID: 18573204
  • Scotti N, Alagna F, Ferraiolo E, Formisano G, Sannino L, Buonaguro L, et al. High-level expression of the HIV-1 Pr55gag polyprotein in transgenic tobacco chloroplasts. Planta 2009; 229:1109 - 22; http://dx.doi.org/10.1007/s00425-009-0898-2; PMID: 19234717
  • Deml L, Speth C, Dierich MP, Wolf H, Wagner R. Recombinant HIV-1 Pr55gag virus-like particles: potent stimulators of innate and acquired immune responses. Mol Immunol 2005; 42:259 - 77; http://dx.doi.org/10.1016/j.molimm.2004.06.028; PMID: 15488613
  • Davis BS, Chang GJ, Cropp B, Roehrig JT, Martin DA, Mitchell CJ, et al. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J Virol 2001; 75:4040 - 7; http://dx.doi.org/10.1128/JVI.75.9.4040-4047.2001; PMID: 11287553
  • Kanagaraj AP, Verma D, Daniell H. Expression of dengue-3 premembrane and envelope polyprotein in lettuce chloroplasts. Plant Mol Biol 2011; 76:323 - 33; http://dx.doi.org/10.1007/s11103-011-9766-0; PMID: 21431782
  • Greco R, Michel M, Guetard D, Cervantes-Gonzalez M, Pelucchi N, Wain-Hobson S, et al. Production of recombinant HIV-1/HBV virus-like particles in Nicotiana tabacum and Arabidopsis thaliana plants for a bivalent plant-based vaccine. Vaccine 2007; 25:8228 - 40; http://dx.doi.org/10.1016/j.vaccine.2007.09.061; PMID: 17976876
  • Huang Z, Mason HS. Conformational analysis of hepatitis B surface antigen fusions in an Agrobacterium-mediated transient expression system. Plant Biotechnol J 2004; 2:241 - 9; http://dx.doi.org/10.1111/j.1467-7652.2004.00068.x; PMID: 17147615
  • Qian B, Shen H, Liang W, Guo X, Zhang C, Wang Y, et al. Immunogenicity of recombinant hepatitis B virus surface antigen fused with preS1 epitopes expressed in rice seeds. Transgenic Res 2008; 17:621 - 31; http://dx.doi.org/10.1007/s11248-007-9135-6; PMID: 17882531
  • Shchelkunov SN, Salyaev RK, Pozdnyakov SG, Rekoslavskaya NI, Nesterov AE, Ryzhova TS, et al. Immunogenicity of a novel, bivalent, plant-based oral vaccine against hepatitis B and human immunodeficiency viruses. Biotechnol Lett 2006; 28:959 - 67; http://dx.doi.org/10.1007/s10529-006-9028-4; PMID: 16794774
  • Kessans S, Frater J. Plant expression of chimeric Gag/gp41 virus-like particles as a mucosally-targeted subunit vaccine against HIV-1. Retrovirology 2009; 6:15; http://dx.doi.org/10.1186/1742-4690-6-S3-P15; PMID: 19216757
  • Ramqvist T, Andreasson K, Dalianis T. Vaccination, immune and gene therapy based on virus-like particles against viral infections and cancer. Expert Opin Biol Ther 2007; 7:997 - 1007; http://dx.doi.org/10.1517/14712598.7.7.997; PMID: 17665989
  • Jegerlehner A, Storni T, Lipowsky G, Schmid M, Pumpens P, Bachmann MF. Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation. Eur J Immunol 2002; 32:3305 - 14; http://dx.doi.org/10.1002/1521-4141(200211)32:11<3305::AID-IMMU3305>3.0.CO;2-J; PMID: 12555676
  • Jegerlehner A, Wiesel M, Dietmeier K, Zabel F, Gatto D, Saudan P, et al. Carrier induced epitopic suppression of antibody responses induced by virus-like particles is a dynamic phenomenon caused by carrier-specific antibodies. Vaccine 2010; 28:5503 - 12; http://dx.doi.org/10.1016/j.vaccine.2010.02.103; PMID: 20307591
  • Fiers W, De Filette M, El Bakkouri K, Schepens B, Roose K, Schotsaert M, et al. M2e-based universal influenza A vaccine. Vaccine 2009; 27:6280 - 3; http://dx.doi.org/10.1016/j.vaccine.2009.07.007; PMID: 19840661
  • Peters BS, Cheingsong-Popov R, Callow D, Foxall R, Patou G, Hodgkin K, et al. A pilot phase II study of the safety and immunogenicity of HIV p17/p24:VLP (p24-VLP) in asymptomatic HIV seropositive subjects. J Infect 1997; 35:231 - 5; http://dx.doi.org/10.1016/S0163-4453(97)92814-0; PMID: 9459393
  • Buonaguro L, Tagliamonte M, Tornesello ML, Buonaguro FM. Developments in virus-like particle-based vaccines for infectious diseases and cancer. Expert Rev Vaccines 2011; 10:1569 - 83; http://dx.doi.org/10.1586/erv.11.135; PMID: 22043956
  • Bendahmane M, Koo M, Karrer E, Beachy RN. Display of epitopes on the surface of tobacco mosaic virus: impact of charge and isoelectric point of the epitope on virus-host interactions. J Mol Biol 1999; 290:9 - 20; http://dx.doi.org/10.1006/jmbi.1999.2860; PMID: 10388554
  • Murawski MR, McGinnes LW, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, et al. Newcastle disease virus-like particles containing respiratory syncytial virus G protein induced protection in BALB/c mice, with no evidence of immunopathology. J Virol 2010; 84:1110 - 23; http://dx.doi.org/10.1128/JVI.01709-09; PMID: 19889768
  • Ravin NV, Kotlyarov RY, Mardanova ES, Kuprianov VV, Migunov AI, Stepanova LA, et al. Plant-produced recombinant influenza vaccine based on virus-like HBc particles carrying an extracellular domain of M2 protein. Biochemistry (Mosc) 2012; 77:33 - 40; http://dx.doi.org/10.1134/S000629791201004X; PMID: 22339631
  • Paz De la Rosa G, Monroy-García A, Mora-García MdeL, Peña CG, Hernández-Montes J, Weiss-Steider B, et al. An HPV 16 L1-based chimeric human papilloma virus-like particles containing a string of epitopes produced in plants is able to elicit humoral and cytotoxic T-cell activity in mice. Virol J 2009; 6:2; http://dx.doi.org/10.1186/1743-422X-6-2; PMID: 19126233
  • Matić S, Rinaldi R, Masenga V, Noris E. Efficient production of chimeric human papillomavirus 16 L1 protein bearing the M2e influenza epitope in Nicotiana benthamiana plants. BMC Biotechnol 2011; 11:106; http://dx.doi.org/10.1186/1472-6750-11-106; PMID: 22085463
  • Natilla A, Nemchinov LG. Improvement of PVX/CMV CP expression tool for display of short foreign antigens. Protein Expr Purif 2008; 59:117 - 21; http://dx.doi.org/10.1016/j.pep.2008.01.011; PMID: 18280751
  • Mason H, Ball J, Shi JJ, Jiang X, Estes MK, Arntzen CJ. Expression and Immunogenicity of Norwalk virus capsid protien from transgenic tobacco and potato. Proc Natl Acad Sci USA 1996; 93:5335 - 40; http://dx.doi.org/10.1073/pnas.93.11.5335; PMID: 8643575
  • Thanavala Y, Mahoney M, Pal S, Scott A, Richter L, Natarajan N, et al. Immunogenicity in humans of an edible vaccine for hepatitis B 10.1073/pnas.0409899102. Proceedings of the National Academy of Sciences 2005; 102:3378-82.
  • Guetard D, Greco R, Cervantes Gonzalez M, Celli S, Kostrzak A, Langlade-Demoyen P, et al. Immunogenicity and tolerance following HIV-1/HBV plant-based oral vaccine administration. Vaccine 2008; 26:4477 - 85; http://dx.doi.org/10.1016/j.vaccine.2008.06.059; PMID: 18601967
  • Röhn TA, Jennings GT, Hernandez M, Grest P, Beck M, Zou Y, et al. Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. Eur J Immunol 2006; 36:2857 - 67; http://dx.doi.org/10.1002/eji.200636658; PMID: 17048275
  • Jennings GT, Bachmann MF. The coming of age of virus-like particle vaccines. Biol Chem 2008; 389:521 - 36; http://dx.doi.org/10.1515/BC.2008.064; PMID: 18953718
  • Maurer P, Jennings GT, Willers J, Rohner F, Lindman Y, Roubicek K, et al. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and Phase I safety and immunogenicity. Eur J Immunol 2005; 35:2031 - 40; http://dx.doi.org/10.1002/eji.200526285; PMID: 15971275
  • Lechner F, Jegerlehner A, Tissot AC, Maurer P, Sebbel P, Renner WA, et al. Virus-like particles as a modular system for novel vaccines. Intervirology 2002; 45:212 - 7; http://dx.doi.org/10.1159/000067912; PMID: 12566703
  • Chackerian B, Rangel M, Hunter Z, Peabody DS. Virus and virus-like particle-based immunogens for Alzheimer’s disease induce antibody responses against amyloid-beta without concomitant T cell responses. Vaccine 2006; 24:6321 - 31; http://dx.doi.org/10.1016/j.vaccine.2006.05.059; PMID: 16806604
  • Werner S, Marillonnet S, Hause G, Klimyuk V, Gleba Y. Immunoabsorbent nanoparticles based on a tobamovirus displaying protein A. Proc Natl Acad Sci USA 2006; 103:17678 - 83; http://dx.doi.org/10.1073/pnas.0608869103; PMID: 17090664
  • McCormick AA, Palmer KE. Genetically engineered Tobacco mosaic virus as nanoparticle vaccines. Expert Rev Vaccines 2008; 7:33 - 41; http://dx.doi.org/10.1586/14760584.7.1.33; PMID: 18251692
  • Sainsbury F, Cañizares MC, Lomonossoff GP. Cowpea mosaic virus: the plant virus-based biotechnology workhorse. Annu Rev Phytopathol 2010; 48:437 - 55; http://dx.doi.org/10.1146/annurev-phyto-073009-114242; PMID: 20455698
  • Cañizares MC, Nicholson L, Lomonossoff GP. Use of viral vectors for vaccine production in plants. Immunol Cell Biol 2005; 83:263 - 70; http://dx.doi.org/10.1111/j.1440-1711.2005.01339.x; PMID: 15877604
  • Fitchen J, Beachy RN, Hein MB. Plant virus expressing hybrid coat protein with added murine epitope elicits autoantibody response. Vaccine 1995; 13:1051 - 7; http://dx.doi.org/10.1016/0264-410X(95)00075-C; PMID: 7491811
  • Modelska A, Dietzschold B, Sleysh N, Fu ZF, Steplewski K, Hooper DC, et al. Immunization against rabies with plant-derived antigen. Proc Natl Acad Sci USA 1998; 95:2481 - 5; http://dx.doi.org/10.1073/pnas.95.5.2481; PMID: 9482911
  • Plotkin SA. Rabies. Clin Infect Dis 2000; 30:4 - 12; http://dx.doi.org/10.1086/313632; PMID: 10619725
  • Lico C, Mancini C, Italiani P, Betti C, Boraschi D, Benvenuto E, et al. Plant-produced potato virus X chimeric particles displaying an influenza virus-derived peptide activate specific CD8+ T cells in mice. Vaccine 2009; 27:5069 - 76; http://dx.doi.org/10.1016/j.vaccine.2009.06.045; PMID: 19563889
  • Dalsgaard K, Uttenthal A, Jones TD, Xu F, Merryweather A, Hamilton WD, et al. Plant-derived vaccine protects target animals against a viral disease. Nat Biotechnol 1997; 15:248 - 52; http://dx.doi.org/10.1038/nbt0397-248; PMID: 9062924
  • Langeveld JP, Brennan FR, Martínez-Torrecuadrada JL, Jones TD, Boshuizen RS, Vela C, et al. Inactivated recombinant plant virus protects dogs from a lethal challenge with canine parvovirus. Vaccine 2001; 19:3661 - 70; http://dx.doi.org/10.1016/S0264-410X(01)00083-4; PMID: 11395200
  • Koo M, Bendahmane M, Lettieri GA, Paoletti AD, Lane TE, Fitchen JH, et al. Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carries an MHV epitope. Proc Natl Acad Sci USA 1999; 96:7774 - 9; http://dx.doi.org/10.1073/pnas.96.14.7774; PMID: 10393897
  • Jiang L, Li Q, Li M, Zhou Z, Wu L, Fan J, et al. A modified TMV-based vector facilitates the expression of longer foreign epitopes in tobacco. Vaccine 2006; 24:109 - 15; http://dx.doi.org/10.1016/j.vaccine.2005.09.060; PMID: 16337317
  • Wu L, Jiang L, Zhou Z, Fan J, Zhang Q, Zhu H, et al. Expression of foot-and-mouth disease virus epitopes in tobacco by a tobacco mosaic virus-based vector. Vaccine 2003; 21:4390 - 8; http://dx.doi.org/10.1016/S0264-410X(03)00428-6; PMID: 14505922
  • Brennan FR, Gilleland LB, Staczek J, Bendig MM, Hamilton WD, Gilleland HE Jr.. A chimaeric plant virus vaccine protects mice against a bacterial infection. Microbiology 1999; 145:2061 - 7; http://dx.doi.org/10.1099/13500872-145-8-2061; PMID: 10463172
  • Rennermalm A, Li YH, Bohaufs L, Jarstrand C, Brauner A, Brennan FR, et al. Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat. Vaccine 2001; 19:3376 - 83; http://dx.doi.org/10.1016/S0264-410X(01)00080-9; PMID: 11348701
  • Smith ML, Lindbo JA, Dillard-Telm S, Brosio PM, Lasnik AB, McCormick AA, et al. Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology 2006; 348:475 - 88; http://dx.doi.org/10.1016/j.virol.2005.12.039; PMID: 16466765
  • McCormick AA, Corbo TA, Wykoff-Clary S, Nguyen LV, Smith ML, Palmer KE, et al. TMV-peptide fusion vaccines induce cell-mediated immune responses and tumor protection in two murine models. Vaccine 2006; 24:6414 - 23; http://dx.doi.org/10.1016/j.vaccine.2006.06.003; PMID: 16860441
  • Rudd PM, Wormald MR, Stanfield RL, Huang M, Mattsson N, Speir JA, et al. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J Mol Biol 1999; 293:351 - 66; http://dx.doi.org/10.1006/jmbi.1999.3104; PMID: 10529350
  • Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, Smith JM, et al. Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines. J Virol 2007; 81:1821 - 37; http://dx.doi.org/10.1128/JVI.02098-06; PMID: 17151111
  • Robertson JS. Sequence analysis of the haemagglutinin of A/Taiwan/1/86, a new variant of human influenza A(H1N1) virus. J Gen Virol 1987; 68:1205 - 8; http://dx.doi.org/10.1099/0022-1317-68-4-1205; PMID: 3572359
  • Chapel C, Garcia C, Roingeard P, Zitzmann N, Dubuisson J, Dwek RA, et al. Antiviral effect of alpha-glucosidase inhibitors on viral morphogenesis and binding properties of hepatitis C virus-like particles. J Gen Virol 2006; 87:861 - 71; http://dx.doi.org/10.1099/vir.0.81503-0; PMID: 16528036
  • Shirato K, Miyoshi H, Goto A, Ako Y, Ueki T, Kariwa H, et al. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J Gen Virol 2004; 85:3637 - 45; http://dx.doi.org/10.1099/vir.0.80247-0; PMID: 15557236
  • Goto A, Yoshii K, Obara M, Ueki T, Mizutani T, Kariwa H, et al. Role of the N-linked glycans of the prM and E envelope proteins in tick-borne encephalitis virus particle secretion. Vaccine 2005; 23:3043 - 52; http://dx.doi.org/10.1016/j.vaccine.2004.11.068; PMID: 15811651
  • Branco LM, Grove JN, Geske FJ, Boisen ML, Muncy IJ, Magliato SA, et al. Lassa virus-like particles displaying all major immunological determinants as a vaccine candidate for Lassa hemorrhagic fever. Virol J 2010; 7:279; http://dx.doi.org/10.1186/1743-422X-7-279; PMID: 20961433
  • Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C, Michaud D, et al. Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 2010; 8:564 - 87; http://dx.doi.org/10.1111/j.1467-7652.2009.00497.x; PMID: 20233335
  • FDA. FDA approves new orphan drug to treat a form of Gaucher disease. http://wwwfdagov/NewsEvents/Newsroom/PressAnnouncements/ucm302549htm 2012; (accessed July 05 2012).
  • Strasser R, Castilho A, Stadlmann J, Kunert R, Quendler H, Gattinger P, et al. Improved virus neutralization by plant-produced anti-HIV antibodies with a homogeneous β1,4-galactosylated N-glycan profile. J Biol Chem 2009; 284:20479 - 85; http://dx.doi.org/10.1074/jbc.M109.014126; PMID: 19478090
  • Castilho A, Gattinger P, Grass J, Jez J, Pabst M, Altmann F, et al. N-glycosylation engineering of plants for the biosynthesis of glycoproteins with bisected and branched complex N-glycans. Glycobiology 2011; 21:813 - 23; http://dx.doi.org/10.1093/glycob/cwr009; PMID: 21317243
  • Castilho A, Pabst M, Leonard R, Veit C, Altmann F, Mach L, et al. Construction of a functional CMP-sialic acid biosynthesis pathway in Arabidopsis. Plant Physiol 2008; 147:331 - 9; http://dx.doi.org/10.1104/pp.108.117572; PMID: 18326787
  • Castilho A, Strasser R, Stadlmann J, Grass J, Jez J, Gattinger P, et al. In planta protein sialylation through overexpression of the respective mammalian pathway. J Biol Chem 2010; 285:15923 - 30; http://dx.doi.org/10.1074/jbc.M109.088401; PMID: 20305285
  • Strasser R, Stadlmann J, Schähs M, Stiegler G, Quendler H, Mach L, et al. Generation of glyco-engineered Nicotiana benthamiana for the production of monoclonal antibodies with a homogeneous human-like N-glycan structure. Plant Biotechnol J 2008; 6:392 - 402; http://dx.doi.org/10.1111/j.1467-7652.2008.00330.x; PMID: 18346095
  • Schähs M, Strasser R, Stadlmann J, Kunert R, Rademacher T, Steinkellner H. Production of a monoclonal antibody in plants with a humanized N-glycosylation pattern. Plant Biotechnol J 2007; 5:657 - 63; http://dx.doi.org/10.1111/j.1467-7652.2007.00273.x; PMID: 17678502
  • Cox KM, Sterling JD, Regan JT, Gasdaska JR, Frantz KK, Peele CG, et al. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat Biotechnol 2006; 24:1591 - 7; http://dx.doi.org/10.1038/nbt1260; PMID: 17128273
  • Pedro L, Soares SS, Ferreira GNM. Purification of Bionanoparticles. Chem Eng Technol 2008; 31:815 - 25; http://dx.doi.org/10.1002/ceat.200800176
  • Lai WB, Middelberg AP. The production of human papillomavirus type 16 L1 vaccine product from Escherichia coli inclusion bodies. Bioprocess Biosyst Eng 2002; 25:121 - 8; http://dx.doi.org/10.1007/s00449-002-0289-6; PMID: 14505012
  • Zhang W, Carmichael J, Ferguson J, Inglis S, Ashrafian H, Stanley M. Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation, renaturation, and self-assembly of virus-like particles in vitro. Virology 1998; 243:423 - 31; http://dx.doi.org/10.1006/viro.1998.9050; PMID: 9568041
  • Venkataram Prasad BV, Hardy ME, Estes MK. Structural studies of recombinant Norwalk capsids. J Infect Dis 2000; 181:Suppl 2 S317 - 21; http://dx.doi.org/10.1086/315576; PMID: 10804144
  • Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Estes MK. Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 2003; 108:241 - 7; http://dx.doi.org/10.1016/S1521-6616(03)00120-7; PMID: 14499247
  • Estes MK. Virus like particle (VLP) vaccines. In: Levine MM, ed. New generation vaccines. New York: Academic Press, 2004:283-94.
  • Ausar SF, Foubert TR, Hudson MH, Vedvick TS, Middaugh CR. Conformational stability and disassembly of Norwalk virus-like particles. Effect of pH and temperature. J Biol Chem 2006; 281:19478 - 88; http://dx.doi.org/10.1074/jbc.M603313200; PMID: 16675449
  • Rolland D, Gauthier M, Dugua JM, Fournier C, Delpech L, Watelet B, et al. Purification of recombinant HBc antigen expressed in Escherichia coli and Pichia pastoris: comparison of size-exclusion chromatography and ultracentrifugation. J Chromatogr B Biomed Sci Appl 2001; 753:51 - 65; http://dx.doi.org/10.1016/S0378-4347(00)00538-7; PMID: 11302448
  • Rodrigues T, Carvalho A, Roldão A, Carrondo MJ, Alves PM, Cruz PE. Screening anion-exchange chromatographic matrices for isolation of onco-retroviral vectors. J Chromatogr B Analyt Technol Biomed Life Sci 2006; 837:59 - 68; http://dx.doi.org/10.1016/j.jchromb.2006.03.061; PMID: 16697280
  • Morenweiser R. Downstream processing of viral vectors and vaccines. Gene Ther 2005; 12:Suppl 1 S103 - 10; http://dx.doi.org/10.1038/sj.gt.3302624; PMID: 16231042
  • Vicente T, Roldão A, Peixoto C, Carrondo MJT, Alves PM. Large-scale production and purification of VLP-based vaccines. J Invertebr Pathol 2011; 107:Suppl S42 - 8; http://dx.doi.org/10.1016/j.jip.2011.05.004; PMID: 21784230
  • Vicente T, Sousa MFQ, Peixoto C, Mota JPB, Alves PM, Carrondo MJT. Anion-exchange membrane chromatography for purification of rotavirus-like particles. J Membr Sci 2008; 311:270 - 83; http://dx.doi.org/10.1016/j.memsci.2007.12.021
  • Wolff MW, Siewert C, Hansen SP, Faber R, Reichl U. Purification of cell culture-derived modified vaccinia ankara virus by pseudo-affinity membrane adsorbers and hydrophobic interaction chromatography. Biotechnol Bioeng 2010; 107:312 - 20; http://dx.doi.org/10.1002/bit.22797; PMID: 20506129
  • Shelly D, Cleave V. Parvovirus B19 VLP vaccine manufacturing. Genet Eng Biotechnol News 2009; 29:1 - 4
  • Kim HJ, Lim SJ, Kwag HL, Kim HJ. The choice of resin-bound ligand affects the structure and immunogenicity of column-purified human papillomavirus type 16 virus-like particles. PLoS ONE 2012; 7:e35893; http://dx.doi.org/10.1371/journal.pone.0035893; PMID: 22563414
  • Cook JC, Joyce JG, George HA, Schultz LD, Hurni WM, Jansen KU, et al. Purification of virus-like particles of recombinant human papillomavirus type 11 major capsid protein L1 from Saccharomyces cerevisiae. Protein Expr Purif 1999; 17:477 - 84; http://dx.doi.org/10.1006/prep.1999.1155; PMID: 10600468
  • Kee GS, Jin J, Balasundaram B, Bracewell DG, Pujar NS, Titchener-Hooker NJ. Exploiting the intracellular compartmentalization characteristics of the S. cerevisiae host cell for enhancing primary purification of lipid-envelope virus-like particles. Biotechnol Prog 2010; 26:26 - 33; PMID: 19856403
  • Ferreira GN, Cabral JM, Prazeres DM. Anion exchange purification of plasmid DNA using expanded bed adsorption. Bioseparation 2000; 9:1 - 6; http://dx.doi.org/10.1023/A:1008134822673; PMID: 10840595
  • Ferreira GN, Cabral JM, Prazeres DM. Studies on the batch adsorption of plasmid DNA onto anion-exchange chromatographic supports. Biotechnol Prog 2000; 16:416 - 24; http://dx.doi.org/10.1021/bp0000196; PMID: 10835244
  • Lyddiatt A. Process chromatography: current constraints and future options for the adsorptive recovery of bioproducts. Curr Opin Biotechnol 2002; 13:95 - 103; http://dx.doi.org/10.1016/S0958-1669(02)00293-8; PMID: 11950558
  • Vicente T, Mota JP, Peixoto C, Alves PM, Carrondo MJ. Analysis of adsorption of a baculovirus bioreaction bulk on an ion-exchange surface by surface plasmon resonance. J Biotechnol 2010; 148:171 - 81; http://dx.doi.org/10.1016/j.jbiotec.2010.05.005; PMID: 20566345
  • Peixoto C, Ferreira TB, Sousa MF, Carrondo MJ, Alves PM. Towards purification of adenoviral vectors based on membrane technology. Biotechnol Prog 2008; 24:1290 - 6; http://dx.doi.org/10.1002/btpr.25; PMID: 19194943
  • Palomares LA, Ramírez OT. Challenges for the production of virus-like particles in insect cells: The case of rotavirus-like particles. Biochem Eng J 2009; 45:158 - 67; http://dx.doi.org/10.1016/j.bej.2009.02.006
  • Vicente T, Sousa MFQ, Peixoto C, Mota JPB, Alves PM, Carrondo MJT. Anion-exchange membrane chromatography for purification of rotavirus-like particles. J Membr Sci 2008; 311:270 - 83; http://dx.doi.org/10.1016/j.memsci.2007.12.021
  • Vicente T, Peixoto C, Carrondo MJ, Alves PM. Purification of recombinant baculoviruses for gene therapy using membrane processes. Gene Ther 2009; 16:766 - 75; http://dx.doi.org/10.1038/gt.2009.33; PMID: 19340018
  • Vicente T, Mota JP, Peixoto C, Alves PM, Carrondo MJ. Rational design and optimization of downstream processes of virus particles for biopharmaceutical applications: current advances. Biotechnol Adv 2011; 29:869 - 78; http://dx.doi.org/10.1016/j.biotechadv.2011.07.004; PMID: 21784144
  • Hammonds J, Chen X, Zhang X, Lee F, Spearman P. Advances in methods for the production, purification, and characterization of HIV-1 Gag-Env pseudovirion vaccines. Vaccine 2007; 25:8036 - 48; http://dx.doi.org/10.1016/j.vaccine.2007.09.016; PMID: 17936444
  • Sweeney SF, Woehrle GH, Hutchison JE. Rapid purification and size separation of gold nanoparticles via diafiltration. J Am Chem Soc 2006; 128:3190 - 7; http://dx.doi.org/10.1021/ja0558241; PMID: 16522099
  • Giritch A, Marillonnet S, Engler C, van Eldik G, Botterman J, Klimyuk V, et al. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci USA 2006; 103:14701 - 6; http://dx.doi.org/10.1073/pnas.0606631103; PMID: 16973752
  • Huang Z, Phoolcharoen W, Lai H, Piensook K, Cardineau G, Zeitlin L, et al. High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol Bioeng 2010; 106:9 - 17; PMID: 20047189
  • Sainsbury F, Lomonossoff GP. Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol 2008; 148:1212 - 8; http://dx.doi.org/10.1104/pp.108.126284; PMID: 18775971
  • Platis D, Labrou NE. Affinity chromatography for the purification of therapeutic proteins from transgenic maize using immobilized histamine. J Sep Sci 2008; 31:636 - 45; http://dx.doi.org/10.1002/jssc.200700481; PMID: 18307162
  • Roque ACA, Lowe CR, Taipa MA. Antibodies and genetically engineered related molecules: production and purification. Biotechnol Prog 2004; 20:639 - 54; http://dx.doi.org/10.1021/bp030070k; PMID: 15176864
  • Desvoyes B, Dulieu P. Purification by monoclonal antibody affinity chromatography of virus-like particles associated with the '447' cytoplasmic male sterility of Vicia faba and investigation of their antigenic composition. Plant Sci 1996; 116:239 - 46; http://dx.doi.org/10.1016/0168-9452(96)04390-7
  • Potera C. Vaccine Manufacturing Gets Boost from Tobacco Plants: Canada-Based Medicago Opens U.S. Facility to Exploit Its Influenza Vaccine Production Method. Genetic Engineering & Biotechnology News 2012; 32:8 - 10; http://dx.doi.org/10.1089/gen.32.6.02
  • Medicago. Clinical Trials Update: Avian flu vaccine. Genetic Engineering & Biotechnology News 2011; 31:61; http://dx.doi.org/10.1089/gen.31.14.28
  • Medicago. Medicago reports positive U.S. clinical trial results for its H1N1 / seasonal influenza vaccine. http://wwwmedicagocom/English/news/News-Releases/News-ReleaseDetails/2011/Medicago-reports-positive-US-clinical-trial-results-for-its-H1N1–seasonal-influenza-vaccine1125593/defaultaspx 2011; (accessed on July 04 2012).
  • Tacket CO, Mason HS, Losonsky G, Estes MK, Levine MM, Arntzen CJ. Human immune responses to a novel norwalk virus vaccine delivered in transgenic potatoes. J Infect Dis 2000; 182:302 - 5; http://dx.doi.org/10.1086/315653; PMID: 10882612
  • Kapusta J, Modelska A, Pniewski T, Figlerowicz M, Jankowski K, Lisowa O, et al. 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
  • Bayer ME, Blumberg BS, Werner B. Particles associated with Australia antigen in the sera of patients with leukaemia, Down’s Syndrome and hepatitis. Nature 1968; 218:1057 - 9; http://dx.doi.org/10.1038/2181057a0; PMID: 4231935
  • Fernández-Fernández MR, Martínez-Torrecuadrada JL, Casal JI, García JA. Development of an antigen presentation system based on plum pox potyvirus. FEBS Lett 1998; 427:229 - 35; http://dx.doi.org/10.1016/S0014-5793(98)00429-3; PMID: 9607317
  • Palmer KE, Benko A, Doucette SA, Cameron TI, Foster T, Hanley KM, et al. Protection of rabbits against cutaneous papillomavirus infection using recombinant tobacco mosaic virus containing L2 capsid epitopes. Vaccine 2006; 24:5516 - 25; http://dx.doi.org/10.1016/j.vaccine.2006.04.058; PMID: 16725236
  • Usha R, Rohll JB, Spall VE, Shanks M, Maule AJ, Johnson JE, et al. Expression of an animal virus antigenic site on the surface of a plant virus particle. Virology 1993; 197:366 - 74; http://dx.doi.org/10.1006/viro.1993.1598; PMID: 7692669
  • Wigdorovitz A, Pérez Filgueira DM, Robertson N, Carrillo C, Sadir AM, Morris TJ, et al. Protection of mice against challenge with foot and mouth disease virus (FMDV) by immunization with foliar extracts from plants infected with recombinant tobacco mosaic virus expressing the FMDV structural protein VP1. Virology 1999; 264:85 - 91; http://dx.doi.org/10.1006/viro.1999.9923; PMID: 10544132
  • Andrianova EP, Krementsugskaia SR, Lugovskaia NN, Mayorova TK, Borisov VV, Eldarov MA, et al. Foot and mouth disease virus polyepitope protein produced in bacteria and plants induces protective immunity in guinea pigs. Biochemistry (Mosc) 2011; 76:339 - 46; http://dx.doi.org/10.1134/S0006297911030072; PMID: 21568869
  • Nuzzaci M, Bochicchio I, De Stradis A, Vitti A, Natilla A, Piazzolla P, et al. Structural and biological properties of Cucumber mosaic virus particles carrying hepatitis C virus-derived epitopes. J Virol Methods 2009; 155:118 - 21; http://dx.doi.org/10.1016/j.jviromet.2008.10.005; PMID: 18992770
  • Piazzolla G, Nuzzaci M, Tortorella C, Panella E, Natilla A, Boscia D, et al. Immunogenic properties of a chimeric plant virus expressing a hepatitis C virus (HCV)-derived epitope: new prospects for an HCV vaccine. J Clin Immunol 2005; 25:142 - 52; http://dx.doi.org/10.1007/s10875-005-2820-4; PMID: 15821891
  • Nemchinov LG, Liang TJ, Rifaat MM, Mazyad HM, Hadidi A, Keith JM. Development of a plant-derived subunit vaccine candidate against hepatitis C virus. Arch Virol 2000; 145:2557 - 73; http://dx.doi.org/10.1007/s007050070008; PMID: 11205105
  • Joelson T, Akerblom L, Oxelfelt P, Strandberg B, Tomenius K, Morris TJ. Presentation of a foreign peptide on the surface of tomato bushy stunt virus. J Gen Virol 1997; 78:1213 - 7; PMID: 9191910
  • McLain L, Durrani Z, Wisniewski LA, Porta C, Lomonossoff GP, Dimmock NJ. Stimulation of neutralizing antibodies to human immunodeficiency virus type 1 in three strains of mice immunized with a 22 amino acid peptide of gp41 expressed on the surface of a plant virus. Vaccine 1996; 14:799 - 810; http://dx.doi.org/10.1016/0264-410X(95)00229-T; PMID: 8817828
  • McLain L, Porta C, Lomonossoff GP, Durrani Z, Dimmock NJ. Human immunodeficiency virus type 1-neutralizing antibodies raised to a glycoprotein 41 peptide expressed on the surface of a plant virus. AIDS Res Hum Retroviruses 1995; 11:327 - 34; http://dx.doi.org/10.1089/aid.1995.11.327; PMID: 7786579
  • Marusic C, Rizza P, Lattanzi L, Mancini C, Spada M, Belardelli F, et al. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. J Virol 2001; 75:8434 - 9; http://dx.doi.org/10.1128/JVI.75.18.8434-8439.2001; PMID: 11507188
  • Cerovska N, Hoffmeisterova H, Moravec T, Plchova H, Folwarczna J, Synkova H, et al. Transient expression of Human papillomavirus type 16 L2 epitope fused to N- and C-terminus of coat protein of Potato virus X in plants. J Biosci 2012; 37:125 - 33; http://dx.doi.org/10.1007/s12038-011-9177-z; PMID: 22357210
  • Meshcheriakova IuA, El’darov MA, Migunov AI, Stepanova LA, Repko IA, Kiselev OI, et al. [Cowpea mosaic virus chimeric particles bearing ectodomain of matrix protein 2 (M2E) of influenza A virus: production and characteristics]. Mol Biol (Mosk) 2009; 43:741 - 50; PMID: 19807038
  • Brennan FR, Jones TD, Gilleland LB, Bellaby T, Xu F, North PC, et al. Pseudomonas aeruginosa outer-membrane protein F epitopes are highly immunogenic in mice when expressed on a plant virus. Microbiology 1999; 145:211 - 20; http://dx.doi.org/10.1099/13500872-145-1-211; PMID: 10206701
  • Gilleland HE, Gilleland LB, Staczek J, Harty RN, García-Sastre A, Palese P, et al. Chimeric animal and plant viruses expressing epitopes of outer membrane protein F as a combined vaccine against Pseudomonas aeruginosa lung infection. FEMS Immunol Med Microbiol 2000; 27:291 - 7; http://dx.doi.org/10.1111/j.1574-695X.2000.tb01442.x; PMID: 10727884
  • Staczek J, Bendahmane M, Gilleland LB, Beachy RN, Gilleland HE Jr.. Immunization with a chimeric tobacco mosaic virus containing an epitope of outer membrane protein F of Pseudomonas aeruginosa provides protection against challenge with P. aeruginosa. Vaccine 2000; 18:2266 - 74; http://dx.doi.org/10.1016/S0264-410X(99)00571-X; PMID: 10717347
  • Belanger H, Fleysh N, Cox S, Bartman G, Deka D, Trudel M, et al. Human respiratory syncytial virus vaccine antigen produced in plants. FASEB J 2000; 14:2323 - 8; http://dx.doi.org/10.1096/fj.00-0144com; PMID: 11053254
  • Yusibov V, Mett V, Mett V, Davidson C, Musiychuk K, Gilliam S, et al. Peptide-based candidate vaccine against respiratory syncytial virus. Vaccine 2005; 23:2261 - 5; http://dx.doi.org/10.1016/j.vaccine.2005.01.039; PMID: 15755607

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