Advertisement

Molecular Biology

, Volume 53, Issue 3, pp 323–334 | Cite as

Virus-Like Particles as an Instrument of Vaccine Production

  • B. V. SyominEmail author
  • Y. V. Ilyin
REVIEWS
  • 32 Downloads

Abstract—

The paper discusses the techniques which are currently implemented for vaccine production based on virus-like particles (VLPs). The factors which determine the characteristics of VLP monomers assembly are provided in detail. Analysis of the literature demonstrates that the development of the techniques of VLP production and immobilization of target antigens on their surface have led to the development of universal platforms which make it possible for virtually any known antigen to be exposed on the particle surface in a highly concentrated form. As a result, the focus of attention has shifted from the approaches to VLP production to the development of a precise interface between the organism’s immune system and the peptides inducing a strong immune response to pathogens or the organism’s own pathological cells. Immunome-specified methods for vaccine design and the prospects of immunoprophylaxis are discussed. Certain examples of vaccines against viral diseases and cancers are considered.

Keywords:

vaccines vaccinomics immunome nanoparticles virus-like particles 

Notes

REFERENCES

  1. 1.
    Lu Y., Chan W., Ko B.Y., Van Lang C.C., Swartz J.R. 2015. Assessing sequence plasticity of a virus-like nanoparticle by evolution toward a versatile scaffold for vaccines and drug delivery. Proc. Natl. Acad. Sci. U. S. A. 112, 12360–12365.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Ho S.C., Yang Y. 2014. Identifying and engineering promoters for high level and sustainable therapeutic recombinant protein production in cultured mammalian cells. Biotechnol. Lett. 36, 1569–1579.CrossRefPubMedGoogle Scholar
  3. 3.
    Mandl J.N., Schneider C., Schneider D.S., Baker M.L. 2018. Going to bat(s) for studies of disease tolerance. Front. Immunol. 9, 2112.  https://doi.org/10.3389/fimmu.2018.02112 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Zhang S., Yong L.K., Li D., Cubas R., Chen C., Yao Q. 2013. Mesothelin virus-like particle immunization controls pancreatic cancer growth through CD8+ T cell induction and reduction in the frequency of CD4+ foxp3+ ICOS- regulatory T cells. PLoS One. 8, e68303.  https://doi.org/10.1371/journal.pone.0068303 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Domingo E., Perales C. 2018. Quasispecies and virus. EurBiophys J. 47, 443–457.Google Scholar
  6. 6.
    Contreras M., Villar M., Alberdi P., de la Fuente J. 2016. Vaccinomics approach to tick vaccine development. Methods Mol. Biol. 1404, 275–286.CrossRefPubMedGoogle Scholar
  7. 7.
    De Groot A.S. 2004. Immunome-derived vaccines. Exp. Opin. Biol. Ther. 4, 767–772.CrossRefGoogle Scholar
  8. 8.
    Fiser A., Sali A. 2003. Modeller: Generation and refinement of homology-based protein structure models. Methods Enzymol. 374, 461–491.CrossRefPubMedGoogle Scholar
  9. 9.
    Zhang Y. 2007. Template-based modeling and free modeling by I-TASSER in CASP7. Proteins. 69 (Suppl. 8), 108–117.CrossRefPubMedGoogle Scholar
  10. 10.
    Reber H. 1973. Proceedings: basic considerations on the requirements to be met by disinfection procedures: The Swiss model. Zbl. Bakteriol. Orig. B. 157, 478–494.Google Scholar
  11. 11.
    Lambert C., Léonard N., De Bolle X., Depiereux E. 2002. ESyPred3D: Prediction of proteins 3D structures. Bioinformatics. 18, 1250–1256.CrossRefPubMedGoogle Scholar
  12. 12.
    Bates P.A., Kelley L.A., MacCallum R.M., Sternberg M.J. 2001. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins. 5, 39–46.CrossRefPubMedGoogle Scholar
  13. 13.
    Bennett-Lovsey R.M., Herbert A.D., Sternberg M.J., Kelley L.A. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins. 70, 611–625.CrossRefPubMedGoogle Scholar
  14. 14.
    Lund O., Frimand K., Gorodkin J., Bohr H., Bohr J., Hansen J., Brunak S. 1997. Protein distance constraints predicted by neural networks and probability density functions. Protein Eng. 10, 1241–1248.CrossRefPubMedGoogle Scholar
  15. 15.
    Guo J.T., Ellrott K., Xu Y. 2008. A historical perspective of template-based protein structure prediction. Methods Mol. Biol. 413, 3–42.PubMedGoogle Scholar
  16. 16.
    Qian B., Raman S., Das R., Bradley P., McCoy A.J., Read R.J., Baker D. 2007. High-resolution structure prediction and the crystallographic phase problem. Nature. 450, 259–264.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Zhang Y, Skolnick J. 2004. Scoring function for automated assessment of protein structure template quality. Proteins. 57, 702–710.CrossRefPubMedGoogle Scholar
  18. 18.
    Crooks E.T., Moore P.L., Franti M., Cayanan C.S., Zhu P., Jiang P., de Vries R.P., Wiley C., Zharkikh I., Schülke N., Roux K.H., Montefiori D.C., Burton D.R., Binley J.M. 2007. A comparative immunogenicity study of HIV-1 virus-like particles bearing various forms of envelope proteins, particles bearing no envelope and soluble monomeric gp120. Virology. 366, 245–262.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Medina-Ramírez M., Sanders R.W., Sattentau Q.J. 2017. Stabilized HIV-1 envelope glycoprotein trimers for vaccine use. Curr. Opin. HIV AIDS. 12, 241–249.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Maegawa K., Shibata T., Yamaguchi R., Hiroike K., Izzati U.Z., Kuroda K., Sugita S., Kawasaki K., Nerome R., Nerome K. 2018. Overexpression of a virus-like particle influenza vaccine in Eri silkworm pupae, using Autographa californica nuclear polyhedrosis virus and host-range expansion. Arch. Virol. 163, 2787–2797.CrossRefPubMedGoogle Scholar
  21. 21.
    Ding X., Liu D., Booth G., Gao W., Lu Y. 2018. Virus-like particle engineering: from rational design to versatile applications. Biotechnol. J. 13, e1700324.  https://doi.org/10.1002/biot.201700324 CrossRefPubMedGoogle Scholar
  22. 22.
    Elliott S.L., Suhrbier A., Miles J.J., Lawrence G., Pye S.J., Le T.T., Rosenstengel A., Nguyen T., Allworth A., Burrows S.R., Cox J., Pye D., Moss D.J., Bharadwaj M. 2008. Phase I trial of a CD8+ T cell peptide epitope-based vaccine for infectious mononucleosis. J. Virol. 82, 1448–1457.CrossRefPubMedGoogle Scholar
  23. 23.
    Madera R., Gong W., Wang L., Burakova Y., Lleellish K., Galliher-Beckley A., Nietfeld J., Henningson J., Jia K., Li P., Bai J., Schlup J., McVey S., Tu C., Shi J. 2016. Pigs immunized with a novel E2 subunit vaccine are protected from subgenotype heterologous classical swine fever virus challenge. BMC Vet. Res. 12 (1), 197.  https://doi.org/10.1186/s12917-016-0823-4 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Ahmed K.S., Hussein S.A., Ali A.H., Korma S.A., Lipeng Q., Jinghua C. 2018. Liposome: Composition, characterisation, preparation, and recent innovation in clinical applications. J. Drug Target. 1–20.  https://doi.org/10.1080/1061186X.2018.1527337
  25. 25.
    Gregory A.E., Titball R., Williamson D. 2013. Vaccine delivery using nanoparticles. Front. Cell. Infect. Microbiol. 3, 13.  https://doi.org/10.3389/fcimb.2013.00013 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Mustafaeva Z. 2016. Polymers in vaccine formulation. Sigma J. Eng. Nat. Sci. 34, 439–451.Google Scholar
  27. 27.
    Wang X., Cao F., Yan M., Liu Y., Zhu X., Sun H., Ma G. 2019. Alum-functionalized graphene oxide nanocomplexes for effective anticancer vaccination. Acta Biomater. 83, 390–399.CrossRefPubMedGoogle Scholar
  28. 28.
    Fadel T.R., Fahmy T.M. 2014. Immunotherapy applications of carbon nanotubes: From design to safe applications. Trends Biotechnol. 32, 198–209.CrossRefPubMedGoogle Scholar
  29. 29.
    Chackerian B., Frietze K.M. 2016. Moving towards a new class of vaccines for non-infectious chronic diseases. Expert. Rev. Vaccines. 15, 561–563.CrossRefPubMedGoogle Scholar
  30. 30.
    Bachmann M.F., Jennings G.T. 2010. Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 10, 787–796.CrossRefPubMedGoogle Scholar
  31. 31.
    Mohsen M.O., Gomes A.C., Vogel M., Bachmann M.F. 2018. Interaction of viral capsid-derived virus-like particles (VLPs) with the innate immune system. Vaccines (Basel). 6, pii: E37.  https://doi.org/10.3390/vaccines6030037 CrossRefPubMedGoogle Scholar
  32. 32.
    Moraes A.M., Jorge S.A., Astray R.M., Suazo C.A., CalderónRiquelme C.E., Augusto E.F., Tonso A., Pamboukian M.M., Piccoli R.A., Barral M.F., Pereira C.A. 2012. Drosophila melanogaster S2 cells for expression of heterologous genes: From gene cloning to bioprocess development. Biotechnol. Adv. 30, 613–628.CrossRefPubMedGoogle Scholar
  33. 33.
    Syomin B.V, Pelisson A., Ilyin Y.V, Bucheton A. 2004. Expression of the retrovirus Gypsy Gag in Spodopterafrugiperda cell culture with the recombinant baculovirus. Dokl. Biochem. Biophys. 398, 310–312.CrossRefPubMedGoogle Scholar
  34. 34.
    Ren J., Bell G., Coy D.H., Brunicardi F.C. 1997. Activation of human somatostatin receptor type 2 causes inhibition of cell growth in transfected HEK293 but not in transfected CHO cells. J. Surg. Res. 71, 13–18.CrossRefPubMedGoogle Scholar
  35. 35.
    Li K., Zhong B. 2018. Regulation of cellular antiviral signaling by modifications of ubiquitin and ubiquitin-like molecules. Immune Netw. 18, e4.  https://doi.org/10.4110/in.2018.18.e4 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Masavuli M.G., Wijesundara D.K., Torresi J., Gowans E.J., Grubor-Bauk B. 2017. Preclinical development and production of virus-like particles as vaccine candidates for hepatitis C. Front. Microbiol. 8, 2413.  https://doi.org/10.3389/fmicb.2017.02413 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Godi A., Bissett S.L., Miller E., Beddows S. 2015. Relationship between humoral immune responses against HPV16, HPV18, HPV31 and HPV45 in 12-15 year old girls receiving Cervarix® or Gardasil® Vaccine. PLoS One. 10, e0140926.  https://doi.org/10.1371/journal.pone.0140926 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Rustandi R.R., Wang F., Hamm C., Cuciniello J.J., Marley M.L. 2014. Development of imaged capillary isoelectric focusing method and use of capillary zone electrophoresis in hepatitis B vaccine RECOMBIVAX HB®. Electrophoresis. 35, 1072–1078.CrossRefPubMedGoogle Scholar
  39. 39.
    Shen C., Ku Z., Zhou Y., Li D., Wang L., Lan K., Liu Q., Huang Z. 2016. Virus-like particle-based vaccine against coxsackievirus A6 protects mice against lethal infections. Vaccine. 34, 4025–4031.CrossRefPubMedGoogle Scholar
  40. 40.
    Zheng X., Wang S., Zhang W., Liu X., Yi Y., Yang S., Xia X., Li Y., Zhang Z. 2016. Development of a VLP-based vaccine in silkworm pupae against rabbit hemorrhagic disease virus. Int. Immunopharmacol. 40, 164–169.CrossRefPubMedGoogle Scholar
  41. 41.
    Pan Q., He K., Huang K. 2008. Development of recombinant porcine parvovirus-like particles as an antigen carrier formed by the hybrid VP2 protein carrying immunoreactive epitope of porcine circovirus type 2. Vaccine. 26, 2119–2126.CrossRefPubMedGoogle Scholar
  42. 42.
    Patterson R., Eley T., Browne C., Martineau H.M., Werling D. 2015. Oral application of freeze-dried yeast particles expressing the PCV2b Cap protein on their surface induce protection to subsequent PCV2b challenge in vivo. Vaccine. 33, 6199–6205.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Zhang H., Qian P., Liu L., Qian S., Chen H., Li X. 2014. Virus-like particles of chimeric recombinant porcine circovirus type 2 as antigen vehicle carrying foreign epitopes. Viruses. 6, 4839–4855.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Li P.C., Qiao X.W., Zheng Q.S., Hou J.B. 2016. Immunogenicity and immunoprotection of porcine circovirus type 2 (PCV2) Cap protein displayed by Lactococcus lactis. Vaccine. 34, 696–702.CrossRefPubMedGoogle Scholar
  45. 45.
    Xiao Y., Chen H.Y., Wang Y., Yin B., Lv C., Mo X., Yan H., Xuan Y., Huang Y., Pang W., Li X., Yuan Y.A., Tian K. 2016. Large-scale production of foot-and-mouth disease virus (serotype Asia1) VLP vaccine in Escherichia coli and protection potency evaluation in cattle. BMC Biotechnol. 16 (1), 56.  https://doi.org/10.1186/s12896-016-0285-6 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Wang A., Gu L., Wu S., Zhu S. 2018. Duck hepatitis A virus structural proteins expressed in insect cells self-assemble into virus-like particles with strong immunogenicity in ducklings. Vet. Microbiol. 215, 23–28.CrossRefPubMedGoogle Scholar
  47. 47.
    Syomin B.V., Leonova O.G., Trendeleva T.A., Zviagil’skaia R.A., Ilyin Y.V., Popenko V.I. 2012. Effect of nucleocapsid on multimerization of gypsy structural protein Gag. Mol. Biol. (Moscow). 46, 270–278.CrossRefGoogle Scholar
  48. 48.
    Dong Y., Cai J., Chen H., Chen L. 2016. Protection of a novel epitope-RNA VLP double-effective VLP vaccine. Antiviral Res. 134, 108–116.CrossRefPubMedGoogle Scholar
  49. 49.
    Zhou Y., He C., Wang L., Ge B. 2017. Post-translational regulation of antiviral innate signaling. Eur. J. Immunol. 47, 1414–1426.CrossRefPubMedGoogle Scholar
  50. 50.
    Panda S.K., Kapur N., Paliwal D., Durgapal H. 2015. Recombinant hepatitis E virus like particles can function as RNA nanocarriers. J. Nanobiotechnol. 13, 44.  https://doi.org/10.1186/s12951-015-0101-9 CrossRefGoogle Scholar
  51. 51.
    Voronkova T., Kazaks A., Ose V., Scherneck S., Pumpens P., Ulrich R. 2007. Hamster polyomavirus-derived virus-like particles are able to transfer in vitro encapsidated plasmid DNA to mammalian cells. Virus Genes. 34, 303–314.CrossRefPubMedGoogle Scholar
  52. 52.
    Kimchi-Sarfaty C., Arora M., Sandalon Z., Oppenheim A., Gottesman M.M. 2003. High cloning capacity of in vitro packaged SV40 vectors with no SV40 virus sequences. Hum. Gene Ther. 14, 167–177.CrossRefPubMedGoogle Scholar
  53. 53.
    Barr S.M., Keck K., Aposhian H.V. 1979. Cell-free assembly of a polyoma-like particlefrom empty capside and DNA. Virology. 96, 656–659.CrossRefPubMedGoogle Scholar
  54. 54.
    Touzé A., Bousarghin L., Ster C., Combita A.L., Roingeard P., Coursaget P. 2001. Gene transfer using human polyomavirus BK virus-like particles expressed in insect cells. J. Gen. Virol. 82, 3005–3009.CrossRefPubMedGoogle Scholar
  55. 55.
    Syomin B.V., Ivanova L.A., Popenko V.I., Ilyin Y.V. 2011. The structural protein Gag of the gypsy retrovirus forms virus-like particles in the bacterial cell. Mol. Biol. (Moscow). 45, 472–478.CrossRefGoogle Scholar
  56. 56.
    Bush D.L., Vogt V.M. 2014. In vitro assembly of retroviruses. Annu. Rev. Virol. 1, 561–580.CrossRefPubMedGoogle Scholar
  57. 57.
    Strods A., Ose V., Bogans J., Cielens I., Kalnins G., Radovica I., Kazaks A., Pumpens P., Renhofa R. 2015. Preparation by alkaline treatment and detailed characterisation of empty hepatitis B virus core particles for vaccine and gene therapy applications. Sci. Rep. 5, 11639.  https://doi.org/10.1038/srep11639 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Sarkar K., Sadhukhan S., Han S.S., Vyas Y.M. 2015. SUMOylation-disrupting WAS mutation converts WASp from a transcriptional activator to a repressor of NF-κB response genes in T cells. Blood. 126, 1670–1682.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Syomin B.V., Malikova M.A., Stepanov A.S, Ilyin Y.V. 2002. Homologous and heterologous type 2 casein kinases have the same effect on the affinity for RNA of the Gag structural protein of gypsy (mdg4). Mol. Biol. (Moscow). 36, 28–29.CrossRefGoogle Scholar
  60. 60.
    Melchior F. 2000. SUMO—nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16, 591–626.CrossRefPubMedGoogle Scholar
  61. 61.
    Syomin B.V., Ilyin Y.V. 2004. The functional motifs that are revealed in the Gypsy gag amino acid sequence. Dokl. Biochem. Biophys. 398, 291–293.CrossRefPubMedGoogle Scholar
  62. 62.
    Gottwein E., Kräusslich H.G. 2005. Analysis of human immunodeficiency virus type 1 Gag ubiquitination. J. Virol. 79, 9134–9144.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Jäger S., Cimermancic P., Gulbahce N., Johnson J.R., McGovern K.E., Clarke S.C., Shales M., Mercenne G., Pache L., Li K., Hernandez H., Jang G.M., Roth S.L., Akiva E., Marlett J., et al. 2011. Global landscape of HIV-human protein complexes. Nature. 481, 365–370.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Lee D.H., Lee S.H., Kim A.R., Quan F.S. 2016. Virus-like nanoparticle vaccine confers protection against Toxoplasma gondii. PLoS One. 11, e0161231.  https://doi.org/10.1371/journal.pone.0161231 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Pleckaityte M., Bremer C.M., Gedvilaite A., Kucinskaite-Kodze I., Glebe D., Zvirbliene A. 2015. Construction of polyomavirus-derived pseudotype virus-like particles displaying a functionally active neutralizing antibody against hepatitis B virus surface antigen. BMC Biotechnology. 15, 85.  https://doi.org/10.1186/s12896-015-0203-3 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Sominskaya I., Skrastina D., Dislers A., Vasiljev D., Mihailova M., Ose V., Dreilina D., Pumpens P. 2010. Construction and immunological evaluation of multivalent hepatitis B virus (HBV. core virus-like particles carrying HBV and HCV epitopes. Clin. Vaccine Immunol. 17, 1027–1033.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Mastico R.A., Talbot S.J., Stockley P.G. 1993. Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. J. Gen. Virol. 74, 541–548.CrossRefPubMedGoogle Scholar
  68. 68.
    Dong Y., Zhang G., Huang X.J., Chen L., Chen H.T. 2015. Promising MS2 mediated virus-like particle vaccine against foot-and-mouth disease. Antiviral Res. 117, 39–43.CrossRefPubMedGoogle Scholar
  69. 69.
    Wong H.T., Cheng S.C., Chan E.W., Sheng Z.T., Yan W.Y., Zheng Z.X., Xie Y. 2000. Plasmids encoding foot-and-mouth disease virus VP1 epitopes elicited immune responses in mice and swine and protected swine against viral infection. Virology. 278, 27–35.CrossRefPubMedGoogle Scholar
  70. 70.
    Chen W., Liu M., Jiao Y., Yan W., Wei X., Chen J., Fei L., Liu Y., Zuo X., Yang F., Lu Y., Zheng Z. 2006. Adenovirus-mediated RNA interference against foot-and-mouth disease virus infection both in vitro and in vivo. J. Virol. 80, 3559–3566.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Shao J.J., Wong C.K., Lin T., Lee S.K., Cong G.Z., Sin F.W., Du J.Z., Gao S.D., Liu X.T., Cai X.P., Xie Y., Chang H.Y., Liu J.X. 2011. Promising multiple epitope recombinant vaccine against foot-and-mouth disease virus type O in swine. Clin. Vaccine Immunol. 18, 143–149.CrossRefPubMedGoogle Scholar
  72. 72.
    Schwarz B., Madden P., Avera J., Gordon B., Larson K., Miettinen H.M., Uchida M., LaFrance B., Basu G., Rynda-Apple A., Douglas T. 2015. Symmetry controlled, genetic presentation of bioactive proteins on the p22 virus-like particle using an external decoration protein. ACS Nano. 9, 9134–9147.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Syomin B.V., Fedorova L.I., Surkov S.A., Ilyin Y.V. 2001. Drosophila melanogaster endogenous retrovirus gypsy can propagate in Drosophila hydei cells. Mol. Gen. Genet. 264, 588–594.CrossRefPubMedGoogle Scholar
  74. 74.
    Syomin B.V., Popenko V.I., Malikova M.A., Stepanov A.S., Ilyin Y.V. 2001. Bacterially expressed polyprotein Gag of retroelement gypsy (MDG4) is able to form multimeric complexes. Dokl. Biochem. Biophys. 380, 322–324.CrossRefGoogle Scholar
  75. 75.
    Syomin B.V., Kandror K.V., Semakin A.B., Tsuprun V.L., Stepanov A.S. 1993. Presence of gypsy (mdg4) retrotransposon in the extracellular virus like particles. FEBS Lett. 323, 285–288.CrossRefPubMedGoogle Scholar
  76. 76.
    Syomin B.V., Samuilenko A.Ya. 2017. A novel strategy of veterinary vaccines production conditioned by the development of vaccinomics. Epizootol. Immunobiol. Farmakol. 1, 48–56.Google Scholar
  77. 77.
    Dorn D.C., Lawatscheck R., Zvirbliene A., Aleksaite E., Pecher G., Sasnauskas K., Ozel M., Raftery M., Schönrich G., Ulrich R.G., Gedvilaite A. 2008. Cellular and humoral immunogenicity of hamster polyoma virus-derived virus-like particles harboring a mucin 1 cytotoxic T-cell epitope. Viral Immunol. 21, 12–27.CrossRefPubMedGoogle Scholar
  78. 78.
    Smith M.T., Hawes A.K., Bundy B.C. 2013. Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr. Opin. Biotechnol. 24, 620–626.CrossRefPubMedGoogle Scholar
  79. 79.
    Sapsford K.E., Algar W.R., Berti L., Gemmill K.B., Casey B.J., Oh E., Stewart M.H., Medintz I.L. 2013. Functionalizing nanoparticles with biological molecules: Developing chemistries that facilitate nanotechnology. Chem. Rev. 113, 1904–2074.CrossRefPubMedGoogle Scholar
  80. 80.
    Jennings G.T., Bachmann M.F. 2009. Immunodrugs: Therapeutic VLP-based vaccines for chronic diseases. Annu. Rev. Pharmacol. Toxicol. 49, 303–326.  https://doi.org/10.1146/annurev-pharmtox-061008-103129 CrossRefPubMedGoogle Scholar
  81. 81.
    Koho T., Ihalainen T.O., Stark M., Uusi-Kerttula H., Wieneke R., Rahikainen R., Blazevic V., Marjomäki V., Tampé R., Kulomaa M.S., Hytönen V.P. 2015. His-tagged norovirus-like particles: A versatile platform for cellular delivery and surface display. Eur. J. Pharm. Biopharm. 96, 22–31.  https://doi.org/10.1016/j.ejpb.2015.07.002 CrossRefPubMedGoogle Scholar
  82. 82.
    Jegerlehner A., Tissot A., Lechner F., Sebbel P., Erdmann I., Kündig T., Bächi T., Storni T., Jennings G., Pumpens P., Renner W.A., Bachmann M.F. 2002. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine. 20, 3104–3112.CrossRefPubMedGoogle Scholar
  83. 83.
    Thrane S., Janitzek C.M., Matondo S., Resende M., Gustavsson T., de Jongh W.A., Clemmensen S., Roeffen W., van de Vegte-Bolmer M., van Gemert G.J., Sauerwein R., Schiller J.T., Nielsen M.A., Theander T.G., Salanti A., Sander A.F. 2016. Bacterial superglue enables easy development of efficient virus-like particle based vaccines. J. Nanobiotechnol. 14, 30.  https://doi.org/10.1186/s12951-016-0181-1 CrossRefGoogle Scholar
  84. 84.
    Zakeri B., Fierer J.O., Celik E., Chittock E.C., Schwarz-Linek U., Moy V.T., Howarth M. 2012. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl. Acad. Sci. U. S. A. 109 (12), E690–E697.  https://doi.org/10.1073/pnas.1115485109 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Singh S.K., Thrane S., Janitzek C.M., Nielsen M.A., Theander T.G., Theisen M., Salanti A., Sander A.F. 2017. Improving the malaria transmission-blocking activity of a Plasmodium falciparum 48/45 based vaccine antigen by SpyTag/SpyCatcher mediated virus-like display. Vaccine. 35 (30), 3726–3732.CrossRefPubMedGoogle Scholar
  86. 86.
    Palladini A., Thrane S., Janitzek C.M., Pihl J., Clemmensen S.B., de Jongh W.A, Clausen T.M., Nicoletti G., Landuzzi L., Penichet M.L., Balboni T., Ianzano M.L., Giusti V., Theander T.G., Nielsen M.A., et al. 2018. Virus-like particle display of HER2 induces potent anti-cancer responses. Oncoimmunology. 7 (3), e1408749.  https://doi.org/10.1080/2162402X.2017.1408749 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Xie J., Li K., Gao Y., Huang R., Lai Y., Shi Y., Yang S., Zhu G., Zhang Q., He J. 2016. Structural analysis and insertion study reveal the ideal sites for surface displaying foreign peptides on a betanodavirus-like particle. Vet. Res. 47, 16.  https://doi.org/10.1186/s13567-015-0294-9 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Wu T., Li S.W., Zhang J., Ng M.H., Xia N.S., Zhao Q. 2012. Hepatitis E vaccine development: A 14 year odyssey. Hum. Vaccin. Immunother. 8, 823–827.CrossRefPubMedGoogle Scholar
  89. 89.
    Vandoolaeghe P., Schuerman L. 2016. The RTS, S/AS01 malaria vaccine in children 5 to 17 months of age at first vaccination. Expert Rev. Vaccines. 15, 1481–1493.CrossRefPubMedGoogle Scholar
  90. 90.
    Mohsen M.O., Gomes A.C., Cabral-Miranda G., Krueger C.C., Leoratti F.M., Stein J.V., Bachmann M.F. 2017. Delivering adjuvants and antigens in separate nanoparticles eliminates the need of physical linkage for effective vaccination. J. Control. Release. 251, 92–100.CrossRefPubMedGoogle Scholar
  91. 91.
    Dranev Y., Kotsemir M., Syomin B. 2018. Diversity of research publications: Relation to agricultural productivity and possible implications for STI policy. Scientometrics. 116, 1565–1587.CrossRefGoogle Scholar
  92. 92.
    Bryson V., Swanstrom M. 1947. Immunization of mice against pneumococcal pneumonia by inhaled polysaccharide. J. Bacteriol. 54, 87.PubMedGoogle Scholar
  93. 93.
    Pisarevskii Yu.S. 1963. Anatomical and physiological features of the human and animal respiratory system in the genesis of immunity after aerosol vaccination: 1. Role of airway structure in mechanical retention of inhyaled material. Zh. Mikrobiol. Epidemiol. Immunobiol. 40, 57–61.PubMedGoogle Scholar
  94. 94.
    Fournier J.M., Gaudry D., Moreau Y., Balençon, Fontanges R. 2076. Dry aerosol vaccination against Newcastle disease: 1. Safety and activity controls on chickens. Dev. Biol. Stand. 33, 269–272.Google Scholar
  95. 95.
    Kunda N.K., Alfagih I.M., Dennison S.R., Tawfeek H.M., Somavarapu S., Hutcheon G.A., Saleem I.Y. 2015. Bovine serum albumin adsorbed PGA-co-PDL nanocarriers for vaccine delivery via dry powder inhalation. Pharmacol. Res. 32, 1341–1353.CrossRefGoogle Scholar
  96. 96.
    Bolton D.L., Song K., Tomaras G.D., Rao S., Roederer M. 2017. Unique cellular and humoral immunogenicity profiles generated by aerosol, intranasal, or parenteral vaccination in rhesus macaques. Vaccine. 35, 639–646.CrossRefPubMedGoogle Scholar
  97. 97.
    Ilic V., Dunet V., Le Pape A., Buchs M., Kosinski M., Bischof Delaloye A., Gerber S., Prior J.O. 2016. SPECT/CT study of bronchial deposition of inhaled particles. A human aerosol vaccination model against HPV. Nuklearmedizin. 55, 203–208.CrossRefPubMedGoogle Scholar
  98. 98.
    Bachmann M.F., Zabel F. 2016. Immunology of virus-like particles. In: Viral Nanotechnology. Eds. Khudyakov Y.E., Pumpens P. Boca Raton, CRC Press. pp. 121–128.Google Scholar
  99. 99.
    Shirbaghaee Z., Bolhassani A. 2016. Different applications of virus-like particles in biology and medicine: Vaccination and delivery systems. Biopolymers. 105, 113–132.  https://doi.org/10.1002/bip.22759 CrossRefPubMedGoogle Scholar
  100. 100.
    Wesołowska A., Kozak Ljunggren M., Jedlina L., Basałaj K., Legocki A., Wedrychowicz H., Kesik-Brodacka M. 2018. A preliminary study of a lettuce-based edible vaccine expressing the cysteine proteinase of Fasciola hepatica for fasciolosis control in livestock. Front. Immunol. 9, 2592.  https://doi.org/10.3389/fimmu.2018.02592 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Musiychuk K., Stephenson N., Bi H., Farrance C.E., Orozovic G., Brodelius M., Brodelius P., Horsey A., Ugulava N., Shamloul A.M., Mett V., Rabindran S., Streatfield S.J., Yusibov V. 2006. A launch vector for the production of vaccine antigens in plants. Influenza Other Respir. Viruses. 1, 19–25.CrossRefGoogle Scholar
  102. 102.
    O’Brien G.J., Bryant C.J., Voogd C., Greenberg H.B., Gardner R.C., Bellamy A.R. 2000. Rotavirus VP6 expressed by PVX vectors in Nicotiana benthamiana coats PVX rods and also assembles into virus-like particles. Virology. 270, 444–453.CrossRefPubMedGoogle Scholar
  103. 103.
    McCormick A.A., Corbo T.A., Wykoff-Clary S., Palmer K.E., Pogue G.P. 2006. Chemical conjugate TMV-peptide bivalent fusion vaccines improve cellular immunity and tumor protection. Bioconjug. Chem. 17, 1330–1338.CrossRefPubMedGoogle Scholar
  104. 104.
    Steinmetz N.F., Mertens M.E., Taurog R.E., Johnson J.E., Commandeur U., Fischer R., Manchester M. 2010. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 10, 305–312.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Zeltins A., West J., Zabel F., El Turabi A., Balke I., Haas S., Maudrich M., Storni F., Engeroff P., Jennings G.T., Kotecha A., Stuart D.I., Foerster J., Bachmann M.F. 2017. Incorporation of Tetanus-epitope into virus-like particles achieves vaccine responses even in older recipients in models of psoriasis, Alzheimer’s and cat allergy. NPJ Vaccines. 2, 30.  https://doi.org/10.1038/s41541-017-0030-8 CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Smith M.L., Lindbo J.A., Dillard-Telm S., Brosio P.M., Lasnik A.B., McCormick A.A., Nguyen L.V., Palmer K.E. 2006. Modified tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications. Virology. 348, 475–788.CrossRefPubMedGoogle Scholar
  107. 107.
    Balke I., Zeltins A. 2018. Use of plant viruses and virus-like particles for the creation of novel vaccines. Adv. Drug Deliv. Rev. pii: S0169-409X(18)30204-7.  https://doi.org/10.1016/j.addr.2018.08.007

Copyright information

© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  1. 1.Institute for Statistical Studies and Economics of Knowledge (ISSEK), National Research University Higher School of EconomicsMoscowRussia
  2. 2.Engelhardt Institute of Molecular Biology, Russian Academy of SciencesMoscowRussia

Personalised recommendations