Advertisement

Virus Genes

, Volume 54, Issue 5, pp 623–637 | Cite as

Recombinant helical plant virus-based nanoparticles for vaccination and immunotherapy

  • Kannan Badri Narayanan
  • Sung Soo Han
Article

Abstract

Plant virus-based nanoparticles (PVNs) are self-assembled capsid proteins of plant viruses, and can be virus-like nanoparticles (VLPs) or virus nanoparticles (VNPs). Plant viruses showing helical capsid symmetry are used as a versatile platform for the presentation of multiple copies of well-arrayed immunogenic antigens of various disease pathogens. Helical PVNs are non-infectious, biocompatible, and naturally immunogenic, and thus, they are suitable antigen carriers for vaccine production and can trigger humoral and/or cellular immune responses. Furthermore, recombinant PVNs as vaccines and adjuvants can be expressed in prokaryotic and eukaryotic systems, and plant expression systems can be used to produce cost-effective antigenic peptides on the surfaces of recombinant helical PVNs. This review discusses various recombinant helical PVNs based on different plant viral capsid shells that have been developed as prophylactic and/or therapeutic vaccines against bacterial, viral, and protozoal diseases, and cancer.

Keywords

Helical plant virus Coat protein Nanoparticle Antigens Vaccine Immunotherapy 

Notes

Acknowledgements

This study was supported by a Yeungnam University Research grant (2018) and by Basic the Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (grant no. 2016R1D1A3B03931483).

Compliance with Ethical Standards

Conflict of interest

The authors have no conflict of interest to declare.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in this article.

References

  1. 1.
    Irvine DJ, Hanson MC, Rakhra K, Tokatlian T (2015) Synthetic nanoparticles for vaccines and immunotherapy. Chem Rev 115:11109–11146CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Narayanan KB, Park HH (2015) Purification and analysis of the interactions of caspase-1 and ASC for assembly of the inflammasome. Appl Biochem Biotechnol 175:2883–2894CrossRefPubMedGoogle Scholar
  3. 3.
    Lebel ME, Chartrand K, Leclerc D, Lamarre A (2015) Plant viruses as nanoparticle-based vaccines and adjuvants. Vaccines 3:620–637CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Salyaev RK, Rigano MM, Rekoslavskaya NI (2010) Development of plant-based mucosal vaccine against widespread infectious disease. Expert Rev Vaccines 9:937–946CrossRefPubMedGoogle Scholar
  5. 5.
    Narayanan KB, Han SS (2017) Helical plant viral nanoparticles-bioinspired synthesis of nanomaterials and nanostructures. Bioinspir Biomim 12:031001CrossRefPubMedGoogle Scholar
  6. 6.
    Zang F, Gerasopoulos K, Fan XZ, Brown AD, Culver JN, Ghodssi R (2014) An electrochemical sensor for selective TNT sensing based on tobacco mosaic virus-like particle binding agents. Chem Commun 50:12977–12980CrossRefGoogle Scholar
  7. 7.
    Lopez-Sagaseta J, Malito E, Rappuoli R, Bottomley MJ (2016) Self-assembling protein nanoparticles in the design of vaccines. Comput Struct Biotechnol J 14:58–68CrossRefPubMedGoogle Scholar
  8. 8.
    Schwarz B, Uchida M, Douglas T (2017) Biomedical and catalytic opportunities of virus-like particles in nanotechnology. Adv Virus Res 97:1–60CrossRefPubMedGoogle Scholar
  9. 9.
    Narayanan KB, Han SS (2017) Icosahedral plant viral nanoparticles—bioinspired synthesis of nanomaterials/nanostructures. Adv Colloid Interface Sci 248:1–19CrossRefPubMedGoogle Scholar
  10. 10.
    Sinkovics J, Horvath J, Horak A (1998) The origin and evolution of viruses (a review). Acta Microbiol Immunol Hung 45:349–390PubMedGoogle Scholar
  11. 11.
    Salazar-Gonzalez JA, Rosales-Mendoza S, Banuelos-Hernandez B (2014) Genetically engineered plants as a source of vaccines against wide spread diseases—an integrated view. In: Rosales-Mendoza S (ed) Springer, New York, pp 43–60Google Scholar
  12. 12.
    McCormick AA, Palmer KE (2008) Genetically engineered tobacco mosaic virus as nanoparticle vaccines. Expert Rev Vaccines 7:33–41CrossRefPubMedGoogle Scholar
  13. 13.
    Lin MT, Kitajima EW, Cupertino FP, Costa CL (1977) Partial purification and some properties of bamboo mosaic virus. Phytopathology 67:1439–1443CrossRefGoogle Scholar
  14. 14.
    Hsu YH, Lin NS (2004) Bamboo mosaic. In: Lapierre H, Signoret PA (eds) Viruses and virus disease of Poaceae (Gramineae). Institut National de la Recherche Agronomique, Paris, pp 723–726Google Scholar
  15. 15.
    Woolhouse M, Chase-Topping M, Haydon D, Friar J, Matthews L, Hughes G, Shaw D, Wilesmith J, Donaldson A, Cornell S, Keeling M, Grenfell B (2001) Epidemiology. Foot-and-mouth disease under control in the UK. Nature 411:258–259CrossRefPubMedGoogle Scholar
  16. 16.
    Yang CD, Liao JT, Lai CY, Jong MH, Liang CM, Lin YL, Lin NS, Hsu YH, Liang SM (2007) Induction of protective immunity in swine by recombinant bamboo mosaic virus expressing foot-and-mouth disease virus epitopes. BMC Biotechnol 7:62CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    McDonald M, Kendall A, Bian W, McCullough I, Lio E, Havens WM, Ghabrial SA, Stubbs G (2010) Architecture of the potyviruses. Virology 405:309–313CrossRefPubMedGoogle Scholar
  18. 18.
    Jagadish MN, Edwards SJ, Hayden MB, Grusovin J, Vandenberg K, Schoofs P, Hamilton RC, Shukla DD, Kalnins H, McNamara M, Haynes J, Nisbet IT, Ward CW, Pye D (1996) Chimeric potyvirus-like particles as vaccine carriers. Intervirology 39:85–92CrossRefPubMedGoogle Scholar
  19. 19.
    Jacob T, Usha R (2002) Expression of Cardamom mosaic virus coat protein in Escherichia coli and its assembly into filamentous aggregates. Virus Res 86:133–141CrossRefPubMedGoogle Scholar
  20. 20.
    Jacob T, Jebasingh T, Venugopal MN, Usha R (2003) High genetic diversity in the coat protein and 3′ untranslated regions among geographical isolates of Cardamom mosaic virus from south India. J Biosci 28:589–595CrossRefPubMedGoogle Scholar
  21. 21.
    Damodharan S, Gujar R, Pattabiraman S, Nesakumar M, Hanna LE, Vadakkuppattu RD, Usha R (2013) Expression and immunological characterization of cardamom mosaic virus coat protein displaying HIV gp41 epitopes. Microbiol Immunol 57:374–385CrossRefPubMedGoogle Scholar
  22. 22.
    Kumar V, Damodharan S, Pandaranayaka EPJ, Madathiparambil MG, Tennyson J (2016) Molecular modeling and in-silico engineering of Cardamom mosaic virus coat protein for the presentation of immunogenic epitopes of Leptospira LipL32. J Biomol Struct Dyn 34:42–56CrossRefPubMedGoogle Scholar
  23. 23.
    Taylor RH, Pares RD (1968) The relationship between sugar-cane mosaic virus and mosaic viruses of maize and Johnson grass in Australia. Aust J Agric Res 19:767–773CrossRefGoogle Scholar
  24. 24.
    Gough KH, Azad AA, Hanna PJ, Shukla DD (1987) Nucleotide sequence of the capsid and nuclear inclusion protein genes from the Johnson grass strain of sugarcane mosaic virus RNA. J Gen Virol 68:297–304CrossRefGoogle Scholar
  25. 25.
    Hawkes N (2015) European medicines agency approves first malaria vaccine. BMJ 351:h4067CrossRefPubMedGoogle Scholar
  26. 26.
    Fuenmayor J, Godia F, Cervera L (2017) Production of virus-like particles for vaccines. New Biotechnol 39:174–180CrossRefGoogle Scholar
  27. 27.
    Saul A, Lord R, Jones GL, Spencer L (1992) Protective immunization with invariant peptides of the Plasmodium falciparum antigen MSA2. J Immunol 148:208–211PubMedGoogle Scholar
  28. 28.
    Smith DB, Davern KM, Board PG, Tiu WU, Garcia EG, Mitchell GF (1986) Mr 26,000 antigen of Schistosoma japonicum recognized by resistant WEHI 129/J mice is a parasite glutathione S-transferase. Proc Natl Acad Sci USA 83:8703–8707CrossRefPubMedGoogle Scholar
  29. 29.
    Jagadish MN, Hamilton RC, Fernandez CS, Schoofs P, Davern KM, Kalnins H, Ward CW, Nisbet IT (1993) High level production of hybrid potyvirus-like particles carrying repetitive copies of foreign antigens in Escherichia coli. Biotechnology 11:1166–1170PubMedGoogle Scholar
  30. 30.
    Saini M, Vrati S (2003) A Japanese encephalitis virus peptide present on Johnson grass mosaic virus-like particles induces virus-neutralizing antibodies and protects mice against lethal challenge. J Virol 77:3487–3494CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Kurth BE, Digilio L, Snow P, Bush LA, Wolkowicz M, Shetty J et al (2008) Immunogenicity of a multi-component recombinant human acrosomal protein vaccine in female Macaca fascicularis. J Reprod Immunol 77:126–141CrossRefPubMedGoogle Scholar
  32. 32.
    Naz RK, Zhu X, Kadam AL (2000) Identification of human sperm peptide sequence involved in egg binding for immunocontraception. Biol Reprod 62:318–324CrossRefPubMedGoogle Scholar
  33. 33.
    Choudhury S, Kakkar V, Suman P, Chakrabarti K, Vrati S, Gupta SK (2009) Immunogenicity of zona pellucida glycoprotein-3 and spermatozoa YLP12 peptides presented on Johnson grass mosaic virus-like particles. Vaccine 27:2948–2953CrossRefPubMedGoogle Scholar
  34. 34.
    Fraser HM, Gunn A (1973) Effects of antibodies to luteinizing hormone-releasing hormone in the male rabbit and on the rat oestrous cycle. Nature 244:160–161CrossRefPubMedGoogle Scholar
  35. 35.
    Hammond JM, Sproat KW, Wise TG, Hyatt AD, Jagadish MN, Coupar BEH (1998) Expression of the potyvirus coat protein mediated by recombinant vaccinia virus and assembly of potyvirus-like particles in mammalian cells. Arch Virol 143:1433–1439CrossRefPubMedGoogle Scholar
  36. 36.
    Sit TL, Abouhaidar MG, Holy S (1989) Nucleotide sequence of papaya mosaic virus RNA. J Gen Virol 70:2325–2331CrossRefPubMedGoogle Scholar
  37. 37.
    Lecours K, Tremblay MH, Gagne ME, Gagne SM, Leclerc D (2006) Purification and biochemical characterization of a monomeric form of papaya mosaic potexvirus coat protein. Prot Expr Purif 47:273–280CrossRefGoogle Scholar
  38. 38.
    Denis J, Majeau N, Acosta-Ramirez E, Savard C, Bedard MC, Simard S, Lecours K, Bolduc M, Pare C, Willems B, Shoukry N, Tessier P, Lacasse P, Lamarre A, Lapointe R, Lopez Macias C, Leclerc D (2007) Immunogenicity of papaya mosaic virus-like particles fused to a hepatitis C virus epitope: evidence for the critical function of multimerization. Virology 363:59–68CrossRefPubMedGoogle Scholar
  39. 39.
    Denis J, Acosta-Ramirez E, Zhao Y, Hamelin ME, Koukavica I, Baz M, Abed Y, Savard C, Pare C, Lopez Macias C, Boivin G, Leclerc D (2008) Development of a universal influenza A vaccine based on the M2e peptide fused to the papaya mosaic virus (PapMV) vaccine platform. Vaccine 26:3395–3403CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Leclerc D, Beausegle D, Denis J, Morin H, Pare C, Lamarre A, Lapointe R (2007) Proteasome-independent major histocompatibility complex class I cross-presentation mediated by Papaya mosaic virus-like particles leads to expansion of specific human T cells. J Virol 81:1319–1326CrossRefPubMedGoogle Scholar
  41. 41.
    Rioux G, Babin C, Majeau N, Leclerc D (2012) Engineering of papaya mosaic virus (PapMV) nanoparticles through fusion of the HA11 peptide to several putative surface-exposed sites. PLoS ONE 7:e31925CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Laliberte Gagne ME, Lecours K, Gagne S, Leclerc D (2008) The F13 residue is critical for interaction among the coat protein subunits of papaya mosaic virus. FEBS J 275:1474–1484CrossRefPubMedGoogle Scholar
  43. 43.
    Babin C, Majeau N, Leclerc D (2013) Engineering of papaya mosaic virus (PapMV) nanoparticles with a CTL epitope derived from influenza NP. J Nanobiotechnol 11:10CrossRefGoogle Scholar
  44. 44.
    Mathieu C, Rioux G, Dumas MC, Leclerc D (2013) Induction of innate immunity in lungs with virus-like nanoparticles leads to protection against influenza and Streptococcus pneumoniae challenge. Nanomedicine 9:839–848CrossRefPubMedGoogle Scholar
  45. 45.
    Lebel ME, Daudelin JF, Chartrand K, Tarrab E, Kalinke U, Savard P, Labrecque N, Leclerc D, Lamarre A (2014) Nanoparticle adjuvant sensing by TLR7 enhances CD8+ T cell-mediated protection from Listeria monocytogenes infection. J Immunol 192:1071–1078CrossRefPubMedGoogle Scholar
  46. 46.
    Narayanan KB, Ali M, Barclay BJ et al (2015) Disruptive environmental chemicals and cellular mechanisms that confer resistance to cell death. Carcinogenesis 36:S89–S110CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Lebel ME, Chartrand K, Tarrab E, Savard P, Leclerc D, Lamarre A (2016) Potentiating cancer immunotherapy using papaya mosaic virus-derived nanoparticles. Nano Lett 16:1826–1832CrossRefPubMedGoogle Scholar
  48. 48.
    Gonsalves D, Ishii M (1980) Purification and serology of papaya ringspot virus. Phytopathology 70:1028–1032CrossRefGoogle Scholar
  49. 49.
    Guerrero-Rodriguez J, Manuel-Cabrera CA, Palomino-Hermosillo YA, Delgado-Guzman PG, Escoto-Delgadillo M, Silva-Rosales L, Herrera-Rodriquez SE, Sanchez-Hernandez C, Gutierrez-Ortega A (2014) Virus-like particles from Escherichia coli-derived untagged papaya ringspot virus capsid protein purified by immobilized metal affinity chromatography enhance the antibody response against a soluble antigen. Mol Biotechnol 56:1110–1120CrossRefPubMedGoogle Scholar
  50. 50.
    Chatchen S, Juricek M, Rueda P, Kertbundit S (2006) Papaya ringspot virus coat protein gene for antigen presentation in Escherichia coli. J Biochem Mol Biol 39:16–21PubMedGoogle Scholar
  51. 51.
    Gubler DJ (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11:480–496PubMedPubMedCentralGoogle Scholar
  52. 52.
    Libsittikul S, Khongwichit S, Smith DR, Yap YK (2015) Evaluation of papaya ringspot virus as a vector for expression of dengue E protein domain III in cucurbita pepo (zucchini) plants. J Anim Plant Sci 25:809–815Google Scholar
  53. 53.
    Garcia JA, Glasa M, Cambra M, Candresse T (2014) Plum pox virus and sharka: a model potyvirus and a major disease. Mol Plant Pathol 15:226–241CrossRefPubMedGoogle Scholar
  54. 54.
    Riechmann JL, Sain S, Garcia JA (1989) The genome-linked protein and 5′ end RNA sequence of plum pox potyvirus. J Gen Virol 70:2785–2789CrossRefPubMedGoogle Scholar
  55. 55.
    Fernandez-Fernandez MR, Martinez-Torrecuadrada JL, Casal JI, Garcia JA (1998) Development of an antigen presentation system based on plum pox potyvirus. FEBS Lett 427:229–235CrossRefPubMedGoogle Scholar
  56. 56.
    Fernandez-Fernandez MR, Martinez-Torrecuadrada JL, Roncal F, Dominquez E, Garcia JA (2002) Identification of immunogenic hot spots within plum pox potyvirus capsid protein for efficient antigen presentation. J Virol 76:12646–12653CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Koenig R, Lesemann DE (1989) Potato virus X, potexvirus group. Assoc Appl Biol Warwick 354:1–5Google Scholar
  58. 58.
    Richardson JF, Tollin P, Bancroft JB (1981) The architecture of the potexviruses. Virology 112:34–39CrossRefPubMedGoogle Scholar
  59. 59.
    Parker L, Kendall A, Stubbs G (2002) Surface features of potato virus X from fiber diffraction. Virology 300:291–295CrossRefPubMedGoogle Scholar
  60. 60.
    Kendall A, McDonald M, Bian W, Bowles T, Baumgarten SC, Shi J, Stewart PL, Bullitt E, Gore D, Irving TC, Havens WM, Ghabrial SA, Wall JS, Stubbs G (2008) Structure of flexible filamentous plant viruses. J Virol 82:9546–9554CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Cruz SS, Chapman S, Roberts AG, Roberts IM, Prior DA, Oparka KJ (1996) Assembly and movement of a plant virus carrying a green fluorescent protein overcoat. Proc Natl Acad Sci USA 93:6286–6290CrossRefPubMedGoogle Scholar
  62. 62.
    Marusic C, Rizza P, Lattanzi L, Mancini C, Spada M, Belardelli F, Benvenuto E, Capone I (2001) Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. J Virol 75:8434–8439CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Fauquet CM, Mayo MA, Virus taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) (Elsevier/Academic Press, London, 2005), pp 739–1128Google Scholar
  64. 64.
    Heermann N, Goldmann U, Schwartz W, Seyffarth T, Baumgarten H, Gerlich W (1984) Large surface proteins of hepatitis B virus containing the pre-s sequence. J Virol 52:396–402PubMedPubMedCentralGoogle Scholar
  65. 65.
    Hong HJ, Ryu CJ, Hur H, Kim S, Oh HK, Oh MS, Park SY (2004) In vivo neutralization of hepatitis B virus infection by an anti-preS1 humanized antibody in chimpanzees. Virology 318:134–141CrossRefPubMedGoogle Scholar
  66. 66.
    Steele JFC, Peyret H, Saunders K, Castells-Graells R, Marsian J, Meshcheriakova Y, Lomonossoff GP (2017) Synthetic plant virology for nanobiotechnology and nanomedicine. WIREs Nanomed Nanobiotechnol 9:e1447CrossRefGoogle Scholar
  67. 67.
    Kalnciema I, Skrastina D, Ose V, Pumpens P, Zeltins A (2012) Potato virus Y-like particles as a new carrier for the presentation of foreign protein stretches. Mol Biotechnol 52:129–139CrossRefPubMedGoogle Scholar
  68. 68.
    Narayanan KB, Han SS (2017) Genetic modifications of icosahedral plant virus-based nanoparticles for vaccine and immunotherapy applications. Curr Protein Pept Sci 18:1141–1151CrossRefPubMedGoogle Scholar
  69. 69.
    Friedland RP, Tedesco JM, Wilson AC, Atwood CS, Smith MA, Perry G, Zagorski MG (2008) Antibodies to potato virus Y bind the amyloid β peptide immunohistochemical and NMR studies. J Biol Chem 283:22550–22556CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Lunney JK, Fang Y, Ladinig A, Chen N, Li Y, Rowland B, Renukaradhya GJ (2016) Porcine reproductive and respiratory syndrome virus (PRRSV): pathogenesis and interaction with the immune system. Annu Rev Anim Biosci 4:129–154CrossRefPubMedGoogle Scholar
  71. 71.
    Manuel-Cabrera CA, Vallejo-Cardona AA, Padilla-Camberos E, Hernandez-Gutierrez R, Herrera-Rodriguez SE, Gutierrez-Ortega A (2016) Self-assembly of hexahistidine-tagged tobacco etch virus capsid protein into microfilaments that induce IgG2-specific response against a soluble porcine reproductive and respiratory syndrome virus chimeric protein. Virol J 13:196CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Namba K, Stubbs G (1985) Solving the phase problem in fiber diffraction. Application to tobacco mosaic virus at 3.6 Å resolution. Acta Crystallogr A 41:252–262CrossRefGoogle Scholar
  73. 73.
    Atabekov J, Nikitin N, Arkhipenko M, Chirkov S, Karpova O (2011) Thermal transition of native tobacco mosaic virus and RNA-free viral proteins into spherical nanoparticles. J Gen Virol 92:453–456CrossRefPubMedGoogle Scholar
  74. 74.
    Bruckman MA, Hern S, Jiang K, Flask CA, Yu X, Steinmetz NF (2013) Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. J Mater Chem B 1:1482–1490CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Van Regenmortel MHV (1990) Structure of viral B-cell epitopes. Res Microbiol 141:747–756CrossRefPubMedGoogle Scholar
  76. 76.
    Van Regenmortel MHV (1999) The antigenicity of tobacco mosaic virus. Philos Trans R Soc Lond B 354:559–568CrossRefGoogle Scholar
  77. 77.
    Karasev A, Foulke S, Wellens C, Rich A, Shon KJ, Zwierzynski I, Hone D, Koprowski H, Reitz M (2005) Plant based HIV-1 vaccine candidate: Tat protein produced in spinach. Vaccine 23:1875–1880CrossRefPubMedGoogle Scholar
  78. 78.
    Sugiyama Y, Hamamoto H, Takemoto S, Watanabe Y, Okada Y (1995) Systemic production of foreign peptides on the particle surface of tobacco mosaic virus. FEBS Lett 359:247–250CrossRefPubMedGoogle Scholar
  79. 79.
    Smith ML, Lindbo JA, Dillard-Telm S, Brosio PM, Lasnik AB, McCormick AA, Nguyen LV, Palmer KE (2006) Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology 348:475–488CrossRefPubMedGoogle Scholar
  80. 80.
    Embers ME, Budgeon LR, Pickel M, Christensen ND (2002) Protective immunity to rabbit oral and cutaneous papillomaviruses by immunization with short peptides of L2, the minor capsid protein. J Virol 76:9798–9805CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Palmer KE, Benko A, Doucette SA, Cameron TI, Foster T, Hanley KM, McCormick AA, McCulloch M, Pogue GP, Smith ML, Christensen ND (2006) Protection of rabbits against cutaneous papillomavirus infection using recombinant tobacco mosaic virus containing L2 capsid epitopes. Vaccine 24:5516–5525CrossRefPubMedGoogle Scholar
  82. 82.
    Venuti A, Massa S, Mett V, Vedova LD, Paolini F, Franconi R, Yusibov V (2009) An E7-based therapeutic vaccine protects mice against HPV16 associated cancer. Vaccine 27:3395–3397CrossRefPubMedGoogle Scholar
  83. 83.
    Noris E, Poli A, Cojoca R, Ritta M, Cavallo F, Vaglio S, Matic S, Landolfo S (2011) A human papillomavirus 8 E7 protein produced in plants is able to trigger the mouse immune system and delay the development of skin lesions. Arch Virol 156:587–595CrossRefPubMedGoogle Scholar
  84. 84.
    Nemchinov LG, Liang TJ, Rifaat MM (2000) Development of a plant-derived subunit vaccine candidate against hepatitis C virus. Arch Virol 145:2557–2573CrossRefPubMedGoogle Scholar
  85. 85.
    Saejung W, Fujiyama K, Takasaki T, Ito M, Hori K, Malasit P, Watanabe Y, Kurane I, Seki T (2007) Production of dengue 2 envelope domain III in plant using TMV-based vector system. Vaccine 25:6646–6654CrossRefPubMedGoogle Scholar
  86. 86.
    McCormick AA, Kumagai MH, Hanley K, Turpen TH, Hakim I, Grill LK, Tuse D, Levy S, Levy R (1999) Rapid production of specific vaccines for lymphoma by expression of the tumor-derived single-chain Fv epitopes in tobacco plants. Proc Natl Acad Sci USA 96:703–708CrossRefPubMedGoogle Scholar
  87. 87.
    McCormick AA, Reddy S, Reinl SJ, Cameron TI, Czerwinkski DK, Vojdani F, Hanley KM, Garger SJ, White EL, Novak J, Barrett J, Holtz RB, Tuse D, Levy R (2008) Plant-produced idiotype vaccines for the treatment of non-Hodgkin’s lymphoma: safety and immunogenicity in a phase I clinical study. Proc Natl Acad Sci USA 105:10131–10136CrossRefPubMedGoogle Scholar
  88. 88.
    Cavanagh D, Brian DA, Enjuanes L, Holmes KV, Lai MM, Laude H, Siddell SG, Spaan W, Taguchi F, Talbot PJ (1990) Recommendations of the coronavirus study group for the nomenclature of the structural proteins, mRNAs, and genes of coronaviruses. Virology 176:306–307CrossRefPubMedGoogle Scholar
  89. 89.
    Koo M, Bendahmane M, Lettieri GA, Paoletti AD, Lane TE, Fitchen JH, Buchmeier MJ, Beachy RN (1999) Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carrier an MHV epitope. Proc Natl Acad Sci USA 96:7774–7779CrossRefPubMedGoogle Scholar
  90. 90.
    Bendahmane M, Koo M, Karrer E, Beachy RN (1999) 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 290:9–20CrossRefPubMedGoogle Scholar
  91. 91.
    Haynes JR, Cunningham J, von Seefried A, Lennick M, Garvin RT, Shen SH (1986) Development of a genetically-engineered, candidate polio vaccine employing the self-assembling properties of the tobacco mosaic virus coat protein. Nat Biotechnol 4:637–641CrossRefGoogle Scholar
  92. 92.
    Pogue GP, Lindbo JA, McCulloch MJ, Lawrence JE, Gross CS, Garger SJ (2004) Parvovirus vaccine as viral coat protein fusions. US Patent No. 6730306 B1Google Scholar
  93. 93.
    Wu L, Jiang L, Zhou Z, Fan J, Zhang Q, Zhu H, Han Q, Xu Z (2003) Expression of foot-and-mouth disease virus epitopes in tobacco by a tobacco mosaic virus-based vector. Vaccine 21:4390–4398CrossRefPubMedGoogle Scholar
  94. 94.
    Jiang L, Li Q, Li M, Zhou Z, Wu L, Fan J, Zhang Q, Zhu H, Xu Z (2006) A modified TMV-based vector facilitates the expression of longer foreign epitopes in tobacco. Vaccine 24:109–115CrossRefPubMedGoogle Scholar
  95. 95.
    Banik S, Mansour AA, Suresh RV, Wykoff-Clary S, Malik M, McCormick AA, Bakshi CS (2015) Development of a multivalent subunit vaccine against tularemia using tobacco mosaic virus (TMV) based delivery system. PLoS ONE 10:e0130858CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Mansouri E, Gabelsberger J, Knapp B, Hundt E, Lenz U, Hungerer KD, Gilleland HE Jr, Staczek J, Domdey H (1999) B.U. von Specht, Safety and immunogenicity of a Pseudomonas aeruginosa hybrid outer membrane protein F-I vaccine in human volunteers. Infect Immun 67:1461–1470PubMedPubMedCentralGoogle Scholar
  97. 97.
    Staczek J, Bendahmane M, Gilleland LB, Beachy RN, Gilleland HE Jr (2000) 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 18:2266–2274CrossRefPubMedGoogle Scholar
  98. 98.
    Turpen TH, Reinl SJ, Charoenvit Y, Hoffman SL, Fallarme V, Grill LK (1995) Malarial epitopes expressed on the surface of recombinant tobacco mosaic virus. Biotechnology 13:53–57PubMedGoogle Scholar
  99. 99.
    Webster DE, Wang L, Mulcair M, Ma C, Santi L, Mason HS, Wesselingh SL, Coppel RL (2009) Production and characterization of an orally immunogenic Plasmodium antigen in plants using a virus-based expression system. Plant Biotechnol J 7:846–855CrossRefPubMedGoogle Scholar
  100. 100.
    McCormick AA, Corbo TA, Wykoff-Clary S, Nguyen LV, Smith ML, Palmer KE, Pogue GP (2006) TMV-peptide fusion vaccines induce cell-mediated immune responses and tumor protection in two murine models. Vaccine 24:6414–6423CrossRefPubMedGoogle Scholar
  101. 101.
    McCormick AA, Corbo TA, Wykoff-Clary S, Palmer KE, Pogue GP (2006) Chemical conjugate TMV-peptide bivalent fusion vaccines improve cellular immunity and tumor protection. Bioconjugate Chem 17:1330–1338CrossRefGoogle Scholar
  102. 102.
    Yin Z, Nguyen HG, Chowdhury S, Bentley P, Bruckman MA, Miermont A, Gildersleeve JC, Wang Q, Huang X (2012) Tobacco mosaic virus as a new carrier for tumor associated carbohydrate antigens. Bioconjugate Chem 23:1694–1703CrossRefGoogle Scholar
  103. 103.
    Frolova OY, Petrunia IV, Komarov TV, Kosorukov VS, Sheval EV, Gleba YY, Dorokhov YL (2010) Trastuzumab-binding peptide display by tobacco mosaic virus. Virology 407:7–13CrossRefPubMedGoogle Scholar
  104. 104.
    Fitchen J, Beachy RN, Hein MB (1995) Plant virus expressing hybrid coat protein with added murine epitope elicits autoantibody response. Vaccine 13:1051–1057CrossRefPubMedGoogle Scholar
  105. 105.
    Shukla DD, Ward CW (1989) Structure of potyvirus coat proteins and its application in the taxonomy of the potyvirus group. Adv Virus Res 36:273–314CrossRefPubMedGoogle Scholar
  106. 106.
    Desbiez C, Lecoq H (1997) Zucchini yellow mosaic virus. Plant Pathol 46:809–829CrossRefGoogle Scholar
  107. 107.
    Arazi T, Shiboleth YM, Gal-On A (2001) A nonviral peptide can replace the entire N terminus of zucchini yellow mosaic potyvirus coat protein and permits viral systemic infection. J Virol 75:6329–6336CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Arazi T, Slutsky SG, Shiboleth YM, Wang Y, Rubinstein M, Barak S, Yang J, Gal-On A (2001) Engineering zucchini yellow mosaic potyvirus as a non-pathogenic vector for expression of heterologous proteins in cucurbits. J Biotechnol 87:67–82CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Chemical EngineeringYeungnam UniversityGyeongsanRepublic of Korea
  2. 2.Department of Nano, Medical & Polymer Materials, College of EngineeringYeungnam UniversityGyeongsanRepublic of Korea

Personalised recommendations