Toward innovative veterinary nanoparticle vaccines

Meiqi Sun1(), Aldryan Cristianto Pratama1(), He Qiu1(), Zehui Liu1,4(), Fang He1,2,3()

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Animal Diseases ›› 2024, Vol. 4 ›› Issue (1) : 14. DOI: 10.1186/s44149-024-00119-w
Review

Toward innovative veterinary nanoparticle vaccines

  • Meiqi Sun1(), Aldryan Cristianto Pratama1(), He Qiu1(), Zehui Liu1,4(), Fang He1,2,3()
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Abstract

Nanoparticles are significant for veterinary vaccine development because they are safer and more effective than conventional formulations. One promising area of research involves self-assembled protein nanoparticles (SAPNs), which have shown potential for enhancing antigen-presenting cell uptake, B-cell activation, and lymph node trafficking. Numerous nanovaccines have been utilized in veterinary medicine, including natural self-assembled protein nanoparticles, rationally designed self-assembled protein nanoparticles, animal virus-derived nanoparticles, bacteriophage-derived nanoparticles, and plant-derived nanoparticles, which will be discussed in this review. SAPN vaccines can produce robust cellular and humoral immune responses and have been shown to protect against various animal infectious diseases. This article attempts to summarize these diverse nanovaccine types and their recent research progress in the field of veterinary medicine. Furthermore, this paper highlights their disadvantages and methods for improving their immunogenicity.

Keywords

Nanoparticles / Veterinary vaccine / Self-assembling protein nanoparticles (SAPNs) / Virus-like nanoparticles (VLPs) / Immune responses / Animal infectious diseases / Optimization strategies

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Meiqi Sun, Aldryan Cristianto Pratama, He Qiu, Zehui Liu, Fang He. Toward innovative veterinary nanoparticle vaccines. Animal Diseases, 2024, 4(1): 14 https://doi.org/10.1186/s44149-024-00119-w

References

[1]
Abrams, C.C., A.M. King, and G.J. Belsham. 1995. Assembly of foot-and-mouth disease virus empty capsids synthesized by a vaccinia virus expression system. J Gen Virol 76 (Pt 12): 3089–3098. https://doi.org/10.1099/0022-1317-76-12-3089.
[2]
Al-Barwani, F., S.L. Young, M.A. Baird, D.S. Larsen, and V.K. Ward. 2014. Mannosylation of virus-like particles enhances internalization by antigen presenting cells. PLoS One 9: e104523. https://doi.org/10.1371/journal.pone.0104523.
[3]
Alam, M.M., Jarvis, C.M., Hincapie, R., McKay, C.S., Schimer, J., Sanhueza, C.A., Xu, K., Diehl, R.C., Finn, M.G., Kiessling, L.L. 2021. Glycan-modified virus-like particles evoke T helper type 1-like immune responses. ACS Nano 15: 309–321. https://doi.org/10.1021/acsnano.0c03023.
[4]
Antonis, A.F., Bruschke, C.J., Rueda, P., Maranga, L., Casal, J.I., Vela, C., Hilgers, L.A., Belt, P.B., Weerdmeester, K., Carrondo, M.J., Langeveld, JP. 2006. A novel recombinant virus-like particle vaccine for prevention of porcine parvovirus-induced reproductive failure. Vaccine 24: 5481–5490. https://doi.org/10.1016/j.vaccine.2006.03.089.
[5]
Anwar, M.N., Jiang, C., Di D., Zhang, J., Guo, S., Wang, X., Hameed, M., Wahaab, A., Shao, D., Li, Z., Liu, K., Li, B., Qiu, Y., Ma, Z., Wei, J. 2021. A Novel recombinant virus-Like particles displaying B and T cell epitopes of Japanese encephalitis virus offers protective immunity in mice and guinea pigs. Vaccines (Basel) 9. https://doi.org/10.3390/vaccines9090980.
[6]
Bachmann, M.F., and G.T. Jennings. 2010. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10: 787–796. https://doi.org/10.1038/nri2868.
[7]
Bárcena, J., Verdaguer, N., Roca, R., Morales, M., Angulo, I., Risco, C., Carrascosa, J.L., Torres, J.M., Castón, J.R. 2004. The coat protein of rabbit hemorrhagic disease virus contains a molecular switch at the N-terminal region facing the inner surface of the capsid. Virology 322: 118–134. https://doi.org/10.1016/j.virol.2004.01.021.
[8]
Bárcena, J., Guerra, B., Angulo, I., González, J., Valcárcel, F., Mata, C.P., Castón, J.R., Blanco, E., Alejo, A. 2015. Comparative analysis of rabbit hemorrhagic disease virus (RHDV) and new RHDV2 virus antigenicity, using specific virus-like particles. Vet Res 46: 106. https://doi.org/10.1186/s13567-015-0245-5.
[9]
Baz, M.A., Becher, D., Koernig, S., Silva, A., Drane, D., Maraskovsky, E. 2012. ISCOMATRIX: a novel adjuvant for use in prophylactic and therapeutic vaccines against infectious diseases. J Med Microbiol 61: 935–943. https://doi.org/10.1099/jmm.0.040857-0.
[10]
Bertagnoli, S., Gelfi, J., Petit, F., Vautherot, J.F., Rasschaert, D., Laurent ,S., Le Gall, G., Boilletot, E., Chantal, J., Boucraut-Baralon, C. 1996. Protection of rabbits against rabbit viral haemorrhagic disease with a vaccinia-RHDV recombinant virus. Vaccine 14: 506–510. https://doi.org/10.1016/0264-410x(95)00232-p.
[11]
Bertagnoli S., Gelfi J., Le Gall G., Boilletot E., Vautherot J.F., Rasschaert D., Laurent S., Petit F., Boucraut-Baralon C., Milon A. 1996. Protection against myxomatosis and rabbit viral hemorrhagic disease with recombinant myxoma viruses expressing rabbit hemorrhagic disease virus capsid protein. J Virol 70: 5061–5066. https://doi.org/10.1128/jvi.70.8.5061-5066.1996.
[12]
Bleckley, S., and S.J. Schroeder. 2012. Incorporating global features of RNA motifs in predictions for an ensemble of secondary structures for encapsidated MS2 bacteriophage RNA. Rna 18: 1309–1318. https://doi.org/10.1261/rna.032326.112.
[13]
Boga, J.A., Casais, R., Marin, M.S., Martin-Alonso, J.M., Carmenes, R.S., Prieto, M., Parra, F. 1994. Molecular cloning, sequencing and expression in Escherichia coli of the capsid protein gene from rabbit haemorrhagic disease virus (Spanish isolate AST/89). J Gen Virol 75 (Pt 9): 2409–2413. https://doi.org/10.1099/0022-1317-75-9-2409.
[14]
Bolduc, M., Baz, M., Laliberté-Gagné ,M.è., Carignan, D., Garneau, C., Russel, A., Boivin, G., Savard, P., Leclerc ,D. 2018. The quest for a nanoparticle-based vaccine inducing broad protection to influenza viruses. Nanomedicine 14: 2563–2574. https://doi.org/10.1016/j.nano.2018.08.010.
[15]
Bromley, E.H., K. Channon, E. Moutevelis, and D.N. Woolfson. 2008. Peptide and protein building blocks for synthetic biology: from programming biomolecules to self-organized biomolecular systems. ACS Chem Biol 3: 38–50. https://doi.org/10.1021/cb700249v.
[16]
Bruun, T.U.J., A.C. Andersson, S.J. Draper, and M. Howarth. 2018. Engineering a Rugged Nanoscaffold To Enhance Plug-and-Display Vaccination. ACS Nano 12: 8855–8866. https://doi.org/10.1021/acsnano.8b02805.
[17]
Bucarey, S.A., Noriega, J., Reyes, P., Tapia, C., Sáenz, L., Zu?iga, A., Tobar, J.A. 2009. The optimized capsid gene of porcine circovirus type 2 expressed in yeast forms virus-like particles and elicits antibody responses in mice fed with recombinant yeast extracts. Vaccine 27: 5781–5790. https://doi.org/10.1016/j.vaccine.2009.07.061.
[18]
Buonaguro, L., Tornesello, M.L., Tagliamonte, M., Gallo, R.C., Wang, L.X., Kamin-Lewis, R., Abdelwahab, S., Lewis, G.K., Buonaguro, F.M. 2006. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J Virol 80: 9134–9143. https://doi.org/10.1128/jvi.00050-06.
[19]
Butler, P.J. 1984. The current picture of the structure and assembly of tobacco mosaic virus. J Gen Virol 65 (Pt 2): 253–279. https://doi.org/10.1099/0022-1317-65-2-253.
[20]
Cai, M., Gan, P., Hu, X., Mai, Z., Ji, C., Yi, H., Li, M., Li, S., Ji, Y., Huang, J., Zhang, G., Gong, L. 2022. Protective effect of bivalent H1N1 and H3N2 VLP vaccines against Eurasian avian-like H1N1 and recent human-like H3N2 influenza viruses in a mouse model. Veterinary Microbiology 266: 109370. https://doi.org/10.1016/j.vetmic.2022.109370.
[21]
Cai, M., Gan, P., Hu, X., Mai, Z., Ji, C., Yi, H., Li, M., Li, S., Ji ,Y., Huang, J., Zhang, G., Gong, L. 2022. Protective effect of bivalent H1N1 and H3N2 VLP vaccines against Eurasian avian-like H1N1 and recent human-like H3N2 influenza viruses in a mouse model. Vet Microbiol 266: 109370. https://doi.org/10.1016/j.vetmic.2022.109370.
[22]
Caldeira, J.C., and D.S. Peabody. 2011. Thermal stability of RNA phage virus-like particles displaying foreign peptides. J Nanobiotechnology 9: 22. https://doi.org/10.1186/1477-3155-9-22.
[23]
Carignan, D., Thérien, A., Rioux, G., Paquet, G., Gagné, M.L., Bolduc, M., Savard, P., Leclerc, D. 2015. Engineering of the PapMV vaccine platform with a shortened M2e peptide leads to an effective one dose influenza vaccine. Vaccine 33: 7245–7253. https://doi.org/10.1016/j.vaccine.2015.10.123.
[24]
Chen, Y., Y. Hu, H. Chen, X. Li, and P. Qian. 2020. A ferritin nanoparticle vaccine for foot-and-mouth disease virus elicited partial protection in mice. Vaccine 38: 5647–5652. https://doi.org/10.1016/j.vaccine.2020.06.063.
[25]
Cho, K.J., Shin, H.J., Lee, J.H., Kim, K.J., Park, S.S., Lee, Y., Lee, C., Park, S.S., Kim, K.H. 2009. The crystal structure of ferritin from Helicobacter pylori reveals unusual conformational changes for iron uptake. J Mol Biol 390: 83–98. https://doi.org/10.1016/j.jmb.2009.04.078.
[26]
Chung, K.Y., Coyle, E.M., Jani, D., King, L.R., Bhardwaj, R., Fries, L., Smith, G., Glenn, G., Golding, H., Khurana, S. 2015. ISCOMATRIX? adjuvant promotes epitope spreading and antibody affinity maturation of influenza A H7N9 virus like particle vaccine that correlate with virus neutralization in humans. Vaccine 33: 3953–3962. https://doi.org/10.1016/j.vaccine.2015.06.047.
[27]
Coffman, R.L., A. Sher, and R.A. Seder. 2010. Vaccine adjuvants: putting innate immunity to work. Immunity 33: 492–503. https://doi.org/10.1016/j.immuni.2010.10.002.
[28]
Cohen, A.A., Yang, Z., Gnanapragasam, P.N.P., Ou, S., Dam, K.A., Wang, H., Bjorkman, P.J. 2021. Construction, characterization, and immunization of nanoparticles that display a diverse array of influenza HA trimers. PLoS One 16: e0247963. https://doi.org/10.1371/journal.pone.0247963.
[29]
Cox, M.M., Hashimoto, Y. A fast track influenza virus vaccine produced in insect cells. J Invertebr Pathol 2011;107(Suppl:S31-41). https://doi.org/10.1016/j.jip.2011.05.003.
[30]
Crisci, E., Fraile, L., Moreno, N., Blanco, E., Cabezón, R., Costa, C., Mussá, T., Baratelli, M., Martinez-Orellana, P., Ganges, L., Martínez, J., Bárcena, J., Montoya, M. 2012. Chimeric calicivirus-like particles elicit specific immune responses in pigs. Vaccine 30: 2427–2439. https://doi.org/10.1016/j.vaccine.2012.01.069.
[31]
Cubas, R., Zhang, S., Kwon, S., Sevick-Muraca, E.M., Li, M., Chen, C., Yao, Q. 2009. Virus-like particle (VLP) lymphatic trafficking and immune response generation after immunization by different routes. J Immunother 32: 118–128. https://doi.org/10.1097/CJI.0b013e31818f13c4.
[32]
Dalton, K.P., Alvarado, C., Reytor, E., Del Carmen Nu?ez, M., Podadera, A., Martínez-Alonso, D., Alonso, J.M.M., Nicieza, I., Gómez-Sebastián, S., Dalton, R.M., Parra, F. et al. 2021. Chimeric VLPs bearing VP60 from two serotypes of rabbit haemorrhagic disease virus are protective against both viruses. Vaccines (Basel) 9. https://doi.org/10.3390/vaccines9091005.
[33]
De Gregorio, E., E. Caproni, and J.B. Ulmer. 2013. Vaccine adjuvants: mode of action. Front Immunol 4: 214. https://doi.org/10.3389/fimmu.2013.00214.
[34]
Desmet, C.J., and K.J. Ishii. 2012. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 12: 479–491. https://doi.org/10.1038/nri3247.
[35]
Ding, P., Jin, Q., Chen, X., Yang, S., Guo, J., Xing, G., Deng, R., Wang, A., Zhang, G. 2019. Nanovaccine confers dual protection against influenza a virus and porcine circovirus type 2. Int J Nanomedicine 14: 7533–7548. https://doi.org/10.2147/ijn.S218057.
[36]
Doll, T.A., S. Raman, R. Dey, and P. Burkhard. 2013. Nanoscale assemblies and their biomedical applications. J R Soc Interface 10: 20120740. https://doi.org/10.1098/rsif.2012.0740.
[37]
Dong, Y.M., G.G. Zhang, X.J. Huang, L. Chen, and H.T. Chen. 2015. Promising MS2 mediated virus-like particle vaccine against foot-and-mouth disease. Antiviral Res 117: 39–43. https://doi.org/10.1016/j.antiviral.2015.01.005.
[38]
Dongye, Z., J. Li, and Y. Wu. 2022. Toll-like receptor 9 agonists and combination therapies: strategies to modulate the tumour immune microenvironment for systemic anti-tumour immunity. Br J Cancer 127: 1584–1594. https://doi.org/10.1038/s41416-022-01876-6.
[39]
Escribano, J.M., Cid, M., Reytor, E., Alvarado, C., Nu?ez, M.C., Martínez-Pulgarín, S., Dalton, R.M. 2020. Chrysalises as natural production units for recombinant subunit vaccines. J Biotechnol 324s: 100019. https://doi.org/10.1016/j.btecx.2020.100019.
[40]
Felberbaum, R.S. 2015. The baculovirus expression vector system: A commercial manufacturing platform for viral vaccines and gene therapy vectors. Biotechnol J 10: 702–714. https://doi.org/10.1002/biot.201400438.
[41]
Fernández-Fernández, M.R., Mouri?o, M., Rivera, J., Rodríguez, F., Plana-Durán, J., García, J.A. 2001. Protection of rabbits against rabbit hemorrhagic disease virus by immunization with the VP60 protein expressed in plants with a potyvirus-based vector. Virology 280: 283–291. https://doi.org/10.1006/viro.2000.0762.
[42]
Figdor, C.G., Y. van Kooyk, and G.J. Adema. 2002. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2: 77–84. https://doi.org/10.1038/nri723.
[43]
Firdaus, F.Z., M. Skwarczynski, and I. Toth. 2022. Developments in Vaccine Adjuvants. Methods Mol Biol 2412: 145–178. https://doi.org/10.1007/978-1-0716-1892-9_8.
[44]
Ford, G.C., Harrison, P.M., Rice, D.W., Smith, J.M., Treffry, A., White, J.L., Yariv, J. 1984. Ferritin: design and formation of an iron-storage molecule. Philos Trans R Soc Lond B Biol Sci 304: 551–565. https://doi.org/10.1098/rstb.1984.0046.
[45]
Fu, Y., and J. Li. 2016. A novel delivery platform based on Bacteriophage MS2 virus-like particles. Virus Res 211: 9–16. https://doi.org/10.1016/j.virusres.2015.08.022.
[46]
Fujita, Y., and H. Taguchi. 2011. Current status of multiple antigen-presenting peptide vaccine systems: Application of organic and inorganic nanoparticles. Chem Cent J 5: 48. https://doi.org/10.1186/1752-153x-5-48.
[47]
García-Vallejo, J.J., Ambrosini, M., Overbeek, A., van Riel, W.E., Bloem, K., Unger, W.W., Chiodo, F., Bolscher, J.G., Nazmi, K., Kalay, H., et al. 2013. Multivalent glycopeptide dendrimers for the targeted delivery of antigens to dendritic cells. Mol Immunol 53: 387–397. https://doi.org/10.1016/j.molimm.2012.09.012.
[48]
Golmohammadi, R., K. Fridborg, M. Bundule, K. Valeg?rd, and L. Liljas. 1996. The crystal structure of bacteriophage Q beta at 3.5 A resolution. Structure 4: 543–554. https://doi.org/10.1016/s0969-2126(96)00060-3.
[49]
Gullberg, M., Muszynski, B., Organtini, L.J., Ashley, R.E., Hafenstein, S.L., Belsham, G.J., Polacek, C. 2013. Assembly and characterization of foot-and-mouth disease virus empty capsid particles expressed within mammalian cells. J Gen Virol 94: 1769–1779. https://doi.org/10.1099/vir.0.054122-0.
[50]
Guo, H., Zhu, J., Tan, Y., Li, C., Chen, Z., Sun, S., Liu, G. 2016. Self-assembly of virus-like particles of rabbit hemorrhagic disease virus capsid protein expressed in Escherichia coli and their immunogenicity in rabbits. Antiviral Res 131: 85–91. https://doi.org/10.1016/j.antiviral.2016.04.011.
[51]
Guo, H.C., Sun, S.Q., Jin, Y., Yang, S.L., Wei, Y.Q., Sun, D.H., Yin, S.H., Ma, J.W., Liu, Z.X., Guo, J.H., et al. 2013. Foot-and-mouth disease virus-like particles produced by a SUMO fusion protein system in Escherichia coli induce potent protective immune responses in guinea pigs, swine and cattle. Vet Res 44: 48. https://doi.org/10.1186/1297-9716-44-48.
[52]
Guo, C., Z. Zhong, and Y. Huang. 2014. Production and immunogenicity of VP2 protein of porcine parvovirus expressed in Pichia pastoris. Arch Virol 159: 963–970. https://doi.org/10.1007/s00705-013-1907-0.
[53]
Han, S.C., H.C. Guo, and S.Q. Sun. 2015. Three-dimensional structure of foot-and-mouth disease virus and its biological functions. Arch Virol 160: 1–16. https://doi.org/10.1007/s00705-014-2278-x.
[54]
Harrison, P.M., and P. Arosio. 1996. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275: 161–203. https://doi.org/10.1016/0005-2728(96)00022-9.
[55]
Haynes, J.R. 2009. Influenza virus-like particle vaccines. Expert Rev Vaccines 8: 435–445. https://doi.org/10.1586/erv.09.8.
[56]
Hsia, Y., Bale, J.B., Gonen, S., Shi, D., Sheffler, W., Fong, K.K., Nattermann, U., Xu, C., Huang, P.S., Ravichandran, R., et al. 2016. Design of a hyperstable 60-subunit protein dodecahedron. [corrected]. Nature 535: 136–139. https://doi.org/10.1038/nature18010.
[57]
Hu, G., Wang, N., Yu, W., Wang, Z., Zou, Y., Zhang, Y., Wang, A., Deng, Z., Yang, Y. 2016. Generation and immunogenicity of porcine circovirus type 2 chimeric virus-like particles displaying porcine reproductive and respiratory syndrome virus GP5 epitope B. Vaccine 34: 1896–1903. https://doi.org/10.1016/j.vaccine.2016.02.047.
[58]
Hua, T., Zhang, D., Tang, B., Chang, C., Liu, G., Zhang, X. The immunogenicity of the virus-like particles derived from the VP2 protein of porcine parvovirus. Veterinary Microbiology 248, 108795 (2020). https://doi.org/10.1016/j.vetmic.2020.108795.
[59]
Hua T., Zhang D., Tang B., Chang C., Liu G., Zhang X. 2020. The immunogenicity of the virus-like particles derived from the VP2 protein of porcine parvovirus. Vet Microbiol 248: 108795. https://doi.org/10.1016/j.vetmic.2020.108795.
[60]
Indelicato, G., Wahome, N., Ringler, P., Müller, S.A., Nieh, M.P., Burkhard, P., Twarock, R. 2016. Principles governing the self-assembly of coiled-coil protein nanoparticles. Biophys J 110: 646–660. https://doi.org/10.1016/j.bpj.2015.10.057.
[61]
Irvine, D.J., and B.J. Read. 2020. Shaping humoral immunity to vaccines through antigen-displaying nanoparticles. Curr Opin Immunol 65: 1–6. https://doi.org/10.1016/j.coi.2020.01.007.
[62]
Ivashkiv, L.B. 2018. IFNγ: signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy. Nat Rev Immunol 18: 545–558. https://doi.org/10.1038/s41577-018-0029-z.
[63]
Jegerlehner, A., Zabel, F., Langer, A., Dietmeier, K., Jennings, G.T., Saudan, P., Bachmann, M.F. 2013. Bacterially produced recombinant influenza vaccines based on virus-like particles. PLoS One 8: e78947. https://doi.org/10.1371/journal.pone.0078947.
[64]
Jennings, G.T., and M.F. Bachmann. 2008. The coming of age of virus-like particle vaccines. Biol Chem 389: 521–536. https://doi.org/10.1515/bc.2008.064.
[65]
Jensen, F.C., J.R. Savary, J.P. Diveley, and J.C. Chang. 1998. Adjuvant activity of incomplete Freund’s adjuvant. Adv Drug Deliv Rev 32: 173–186. https://doi.org/10.1016/s0169-409x(98)00009-x.
[66]
Jia, J., Zhang, Y., Xin, Y., Jiang, C., Yan, B., Zhai, S. 2018. Interactions between nanoparticles and dendritic cells: from the perspective of cancer immunotherapy. Front Oncol 8: 404. https://doi.org/10.3389/fonc.2018.00404.
[67]
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: 109–115. https://doi.org/10.1016/j.vaccine.2005.09.060.
[68]
Johannssen, T., and B. Lepenies. 2017. Glycan-Based Cell Targeting To Modulate Immune Responses. Trends Biotechnol 35: 334–346. https://doi.org/10.1016/j.tibtech.2016.10.002.
[69]
Jung, B.-K., H.-R. Kim, H. Jang, and K.-S. Chang. 2020. Replacing the decoy epitope of PCV2 capsid protein with epitopes of GP3 and/or GP5 of PRRSV enhances the immunogenicity of bivalent vaccines in mice. Journal of Virological Methods 284: 113928. https://doi.org/10.1016/j.jviromet.2020.113928.
[70]
Jung, B.K., H.R. Kim, H. Jang, and K.S. Chang. 2020. Replacing the decoy epitope of PCV2 capsid protein with epitopes of GP3 and/or GP5 of PRRSV enhances the immunogenicity of bivalent vaccines in mice. J Virol Methods 284: 113928. https://doi.org/10.1016/j.jviromet.2020.113928.
[71]
Kak, G., M. Raza, and B.K. Tiwari. 2018. Interferon-gamma (IFN-γ): Exploring its implications in infectious diseases. Biomol Concepts 9: 64–79. https://doi.org/10.1515/bmc-2018-0007.
[72]
Kanekiyo, M., Wei, C.J., Yassine, H.M., McTamney, P.M., Boyington, J.C., Whittle, J.R., Rao, S.S., Kong, W.P., Wang, L., Nabel, G.J. 2013. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499: 102–106. https://doi.org/10.1038/nature12202.
[73]
Kang, H.J., Chu, K.B., Kim, M.J., Lee, S.H., Park, H., Jin, H., Moon, E.K., Quan, F.S. 2021. Protective immunity induced by CpG ODN-adjuvanted virus-like particles containing Toxoplasma gondii proteins. Parasite Immunol 43: e12799. https://doi.org/10.1111/pim.12799.
[74]
Kang, S., Uchida, M., O'Neil, A., Li, R., Prevelige, P.E., Douglas, T. 2010. Implementation of p22 viral capsids as nanoplatforms. Biomacromolecules 11: 2804–2809. https://doi.org/10.1021/bm100877q.
[75]
Kang, S.J., Bae, S.M., Lee, H.J., Jeong, Y.J., Lee, M.A., You, S.H., Lee, H.S., Hyun, B.H., Lee, N., Cha, S.H.l. 2021. Porcine circovirus (PCV) genotype 2d-based virus-like particles (VLPs) induced broad cross-neutralizing antibodies against diverse genotypes and provided protection in dual-challenge infection of a PCV2d virus and a type 1 porcine reproductive and respiratory syndrome virus (PRRSV). Pathogens 10. https://doi.org/10.3390/pathogens10091145.
[76]
Khayat, R., Brunn, N, Speir, J.A., Hardham, J.M., Ankenbauer, R.G., Schneemann, A., Johnson, J.E. 2011. The 2.3-angstrom structure of porcine circovirus 2. J Virol 85: 7856–7862. https://doi.org/10.1128/jvi.00737-11.
[77]
Khoshnejad, M., H. Parhiz, V.V. Shuvaev, I.J. Dmochowski, and V.R. Muzykantov. 2018. Ferritin-based drug delivery systems: Hybrid nanocarriers for vascular immunotargeting. J Control Release 282: 13–24. https://doi.org/10.1016/j.jconrel.2018.02.042.
[78]
Kischkel, B., Rossi, S.A., Santos, S.R., Nosanchuk, J.D., Travassos, L.R., Taborda, C.P. 2020. Therapies and vaccines based on nanoparticles for the treatment of systemic fungal infections. Front Cell Infect Microbiol 10: 463. https://doi.org/10.3389/fcimb.2020.00463.
[79]
Laurent, S., J.F. Vautherot, M.F. Madelaine, G. Le Gall, and D. Rasschaert. 1994. Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into viruslike particles and induces protection. J Virol 68: 6794–6798. https://doi.org/10.1128/jvi.68.10.6794-6798.1994.
[80]
Lee, K.Z., Basnayake, Pussepitiyalage, V., Lee, Y.H., Loesch-Fries, L.S., Harris, M.T., Hemmati, S., Solomon, K.V. 2021. Engineering tobacco mosaic virus and its virus-like-particles for synthesis of biotemplated nanomaterials. Biotechnol J 16: e2000311. https://doi.org/10.1002/biot.202000311.
[81]
Lei, X., X. Cai, and Y. Yang. 2020. Genetic engineering strategies for construction of multivalent chimeric VLPs vaccines. Expert Rev Vaccines 19: 235–246. https://doi.org/10.1080/14760584.2020.1738227.
[82]
Leuthold, M.M., K.P. Dalton, and G.S. Hansman. 2015. Structural analysis of a rabbit hemorrhagic disease virus binding to histo-blood group antigens. J Virol 89: 2378–2387. https://doi.org/10.1128/jvi.02832-14.
[83]
Li, Chester Q., Elizabeth Soistman, and Daniel C. Carter. 2006. Ferritin nanoparticle technology... A new platform for antigen presentation and vaccine development. Industrial Biotechnology 2: 143–147. https://doi.org/10.1089/ind.2006.2.143.
[84]
Li, G., Liu, L., Xu, B., Hu, J., Kuang, H., Wang, X., Wang, L., Cui, X., Sun, H., Rong, J. 2021. Displaying epitope B and epitope 7 of porcine reproductive and respiratory syndrome virus on virus like particles of porcine circovirus type 2 provides partial protection to pigs. J Vet Med Sci 83: 1263–1272. https://doi.org/10.1292/jvms.20-0543.
[85]
Li, X., Meng, X., Wang, S., Li, Z., Yang, L., Tu, L., Diao, W., Yu, C., Yu, Y., Yan, C., et al. 2018. Virus-like particles of recombinant PCV2b carrying FMDV-VP1 epitopes induce both anti-PCV and anti-FMDV antibody responses. Appl Microbiol Biotechnol 102: 10541–10550. https://doi.org/10.1007/s00253-018-9361-2.
[86]
Li, Z., Cui, K., Wang, H., Liu, F., Huang, K., Duan, Z., Wang, F., Shi, D., Liu, Q. 2019. A milk-based self-assemble rotavirus VP6-ferritin nanoparticle vaccine elicited protection against the viral infection. J Nanobiotechnology 17: 13. https://doi.org/10.1186/s12951-019-0446-6.
[87]
Liu, G., Qiao, X., Chang, C., Hua, T., Wang, J., Tang, B., Zhang, D. 2020. Reduction of postweaning multisystemic wasting syndrome-associated clinical symptoms by virus-Like particle vaccine against porcine parvovirus and porcine circovirus type 2. Viral Immunol 33: 444–456. https://doi.org/10.1089/vim.2019.0201.
[88]
Liu, R., R.A. Vaishnav, A.M. Roberts, and R.P. Friedland. 2013. Humans have antibodies against a plant virus: evidence from tobacco mosaic virus. PLoS One 8: e60621. https://doi.org/10.1371/journal.pone.0060621.
[89]
Liu, X., Fang, Y., Zhou, P., Lu, Y., Zhang, Q., Xiao, S., Dong, Z., Pan, L., Lv, J., Zhang, Z., et al. 2017. Chimeric virus-like particles elicit protective immunity against serotype O foot-and-mouth disease virus in guinea pigs. Appl Microbiol Biotechnol 101: 4905–4914. https://doi.org/10.1007/s00253-017-8246-0.
[90]
Liu, X., Y. Liu, Y. Zhang, F. Zhang, and E. Du. 2020. Incorporation of a truncated form of flagellin (TFlg) into porcine circovirus type 2 virus-like particles enhances immune responses in mice. BMC Vet Res 16: 45. https://doi.org/10.1186/s12917-020-2253-6.
[91]
Liu, Z.H., Xu, H.L., Han, G.W., Tao, L.N., Lu, Y., Zheng, S.Y., Fang, W.H., He, F. 2021. Self-assembling nanovaccine enhances protective efficacy against CSFV in pigs. Front Immunol 12:689187. https://doi.org/10.3389/fimmu.2021.689187.
[92]
Liu, Z.H., Xu, H.L., Han, G.W., Tao, L.N., Lu, Y., Zheng, S.Y., Fang, W.H., He, F. 2021. A self-assembling nanoparticle: Implications for the development of thermostable vaccine candidates. Int J Biol Macromol 183: 2162–2173. https://doi.org/10.1016/j.ijbiomac.2021.06.024.
[93]
Liu, Z.H., Z.F. Deng, Y. Lu, W.H. Fang, and F. He. 2022. A modular and self-adjuvanted multivalent vaccine platform based on porcine circovirus virus-like nanoparticles. J Nanobiotechnology 20: 493. https://doi.org/10.1186/s12951-022-01710-4.
[94]
Lomonossoff, G.P., and C. Wege. 2018. TMV Particles: The Journey From Fundamental Studies to Bionanotechnology Applications. Adv Virus Res 102: 149–176. https://doi.org/10.1016/bs.aivir.2018.06.003.
[95]
Look, M., A. Bandyopadhyay, J.S. Blum, and T.M. Fahmy. 2010. Application of nanotechnologies for improved immune response against infectious diseases in the developing world. Adv Drug Deliv Rev 62: 378–393. https://doi.org/10.1016/j.addr.2009.11.011.
[96]
López-Sagaseta, J., E. Malito, R. Rappuoli, and M.J. Bottomley. 2016. Self-assembling protein nanoparticles in the design of vaccines. Comput Struct Biotechnol J 14: 58–68. https://doi.org/10.1016/j.csbj.2015.11.001.
[97]
López-Vidal, J., Gómez-Sebastián, S., Bárcena, J., Nu?ez Mdel, C., Martínez-Alonso, D., Dudognon, B., Guijarro, E., Escribano, J.M. 2015. Improved production efficiency of virus-Like particles by the baculovirus expression vector system. PLoS One 10: e0140039. https://doi.org/10.1371/journal.pone.0140039.
[98]
Lu, Y., Liu, Z., Li, Y., Deng, Z., Fang, W., He, F. 2022. The truncated form of flagellin (tFlic) provides the 2dCap subunit vaccine with better immunogenicity and protective effects in mice. Anim Dis 2: 11. https://doi.org/10.1186/s44149-022-00043-x.
[99]
Lu, Y., Liu, Z.H., Li, Y.X., Xu, H.L., Fang, W.H., He, F. 2022. Targeted delivery of nanovaccine to dendritic cells via DC-binding peptides induces potent antiviral immunity in vivo. Int J Nanomedicine 17: 1593–1608. https://doi.org/10.2147/ijn.S357462.
[100]
Ma, H., Li, X., Li, J., Zhao, Z., Zhang, H., Hao, G., Chen, H., Qian, P. 2021. Immunization with a recombinant fusion of porcine reproductive and respiratory syndrome virus modified GP5 and ferritin elicits enhanced protective immunity in pigs. Virology 552: 112–120. https://doi.org/10.1016/j.virol.2020.10.007.
[101]
Machida, K., and H. Imataka. 2015. Production methods for viral particles. Biotechnol Lett 37: 753–760. https://doi.org/10.1007/s10529-014-1741-9.
[102]
Mai, Z., Cai, M., Hu, X., Li, M., Ji, Y., Li, S., Huang, J., Liang, Q., Ji, C., Yi,H., et al. 2023. Protection efficacy of the H1 and H3 bivalent virus-like particle vaccine against swine influenza virus infection. Veterinary Microbiology 280: 109719. https://doi.org/10.1016/j.vetmic.2023.109719.
[103]
Mai, Z., Cai, M., Hu, X., Li, M., Ji, Y., Li, S., Huang, J., Liang, Q., Ji, C., Yi, H., et al. 2023. Protection efficacy of the H1 and H3 bivalent virus-like particle vaccine against swine influenza virus infection. Vet Microbiol 280: 109719. https://doi.org/10.1016/j.vetmic.2023.109719.
[104]
Mallajosyula, J.K., Hiatt, E., Hume, S., Johnson, A., Jeevan, T., Chikwamba, R., Pogue, G.P., Bratcher, B., Haydon, H., Webby, R.J., et al. 2014. Single-dose monomeric HA subunit vaccine generates full protection from influenza challenge. Hum Vaccin Immunother 10: 586–595. https://doi.org/10.4161/hv.27567.
[105]
Makabenta, J.M.V., Nabawy, A., Li, C.H., Schmidt-Malan, S., Patel, R., Rotello, V.M. 2021. Nanomaterial-based therapeutics for antibiotic-resistant bacterial infections. Nat Rev Microbiol 19: 23–36. https://doi.org/10.1038/s41579-020-0420-1.
[106]
Manolova, V., Flace, A., Bauer, M., Schwarz, K., Saudan, P., Bachmann, M.F. 2008. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 38: 1404–1413. https://doi.org/10.1002/eji.200737984.
[107]
Mansour, A.A., Banik, S., Suresh, R.V., Kaur, H., Malik, M., McCormick, A.A., Bakshi, C.S. 2018. An improved Tobacco mosaic virus (TMV)-conjugated multiantigen subunit vaccine against respiratory tularemia. Front Microbiol 9: 1195. https://doi.org/10.3389/fmicb.2018.01195.
[108]
Margine, I., L. Martinez-Gil, Y.Y. Chou, and F. Krammer. 2012. Residual baculovirus in insect cell-derived influenza virus-like particle preparations enhances immunogenicity. PLoS One 7. https://doi.org/10.1371/journal.pone.0051559.
[109]
Mastico, R.A., S.J. Talbot, and P.G. Stockley. 1993. Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. J Gen Virol 74 (Pt 4): 541–548. https://doi.org/10.1099/0022-1317-74-4-541.
[110]
Mazzoni, A., and D.M. Segal. 2004. Controlling the Toll road to dendritic cell polarization. J Leukoc Biol 75: 721–730. https://doi.org/10.1189/jlb.1003482.
[111]
McFall-Boegeman, H., and X. Huang. 2022. Mechanisms of cellular and humoral immunity through the lens of VLP-based vaccines. Expert Rev Vaccines 21: 453–469. https://doi.org/10.1080/14760584.2022.2029415.
[112]
Mizel, S.B., and J.T. Bates. 2010. Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 185: 5677–5682. https://doi.org/10.4049/jimmunol.1002156.
[113]
Mo, X., Li, X., Yin, B., Deng, J., Tian, K., Yuan, A. 2019. Structural roles of PCV2 capsid protein N-terminus in PCV2 particle assembly and identification of PCV2 type-specific neutralizing epitope. PLoS Pathog 15: e1007562. https://doi.org/10.1371/journal.ppat.1007562.
[114]
Molitor, T.W., H.S. Joo, and M.S. Collett. 1983. Porcine parvovirus: virus purification and structural and antigenic properties of virion polypeptides. J Virol 45: 842–854. https://doi.org/10.1128/jvi.45.2.842-854.1983.
[115]
Munro, H.N., and M.C. Linder. 1978. Ferritin: structure, biosynthesis, and role in iron metabolism. Physiol Rev 58: 317–396. https://doi.org/10.1152/physrev.1978.58.2.317.
[116]
Nguyen, B. & Tolia, N. H. 2021. Protein-based antigen presentation platforms for nanoparticle vaccines. NPJ Vaccines 6. https://doi.org/10.1038/s41541-021-00330-7.
[117]
Nooraei, S., Bahrulolum, H., Hoseini, ZS., Katalani, C., Hajizade, A., Easton, A.J., Ahmadian, G. 2021. Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J Nanobiotechnology 19: 59. https://doi.org/10.1186/s12951-021-00806-7.
[118]
O’Neil, A., C. Reichhardt, B. Johnson, P.E. Prevelige, and T. Douglas. 2011. Genetically programmed in vivo packaging of protein cargo and its controlled release from bacteriophage P22. Angew Chem Int Ed Engl 50: 7425–7428. https://doi.org/10.1002/anie.201102036.
[119]
Oem, J.K., Park, J.H., Lee, K.N., Kim, Y.J., Kye, S.J., Park, J.Y., Song, H.J. 2007. Characterization of recombinant foot-and-mouth disease virus pentamer-like structures expressed by baculovirus and their use as diagnostic antigens in a blocking ELISA. Vaccine 25: 4112–4121. https://doi.org/10.1016/j.vaccine.2006.08.046.
[120]
Oyewumi, M.O., A. Kumar, and Z. Cui. 2010. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vaccines 9: 1095–1107. https://doi.org/10.1586/erv.10.89.
[121]
Pagot, E., Rigaut, M., Roudaut, D., Panzavolta, L., Jolie, R., Duivon, D. 2017. Field efficacy of Porcilis? PCV M Hyo versus a licensed commercially available vaccine and placebo in the prevention of PRDC in pigs on a French farm: a randomized controlled trial. Porcine Health Manag 3: 3. https://doi.org/10.1186/s40813-016-0051-0.
[122]
Papapostolou, D., and S. Howorka. 2009. Engineering and exploiting protein assemblies in synthetic biology. Mol Biosyst 5: 723–732. https://doi.org/10.1039/b902440a.
[123]
Peabody, D.S. 1997. Subunit fusion confers tolerance to peptide insertions in a virus coat protein. Arch Biochem Biophys 347: 85–92. https://doi.org/10.1006/abbi.1997.0312.
[124]
Pérez-Filgueira, D.M., Resino-Talaván, P., Cubillos, C., Angulo, I., Barderas, M.G., Barcena, J., Escribano, J.M. 2007. Development of a low-cost, insect larvae-derived recombinant subunit vaccine against RHDV. Virology 364: 422–430. https://doi.org/10.1016/j.virol.2007.03.016.
[125]
Pliasas, V.C., Menne, Z., Aida, V., Yin, J.H., Naskou, M.C., Neasham, P.J., North, J.F., Wilson, D., Horzmann, K.A., Jacob, J., et al. 2022. A novel neuraminidase virus-like particle vaccine offers protection against heterologous H3N2 influenza virus infection in the porcine model. Front Immunol 13: 915364. https://doi.org/10.3389/fimmu.2022.915364.
[126]
Prevelige, P.E., Jr., D. Thomas, and J. King. 1988. Scaffolding protein regulates the polymerization of P22 coat subunits into icosahedral shells in vitro. J Mol Biol 202: 743–757. https://doi.org/10.1016/0022-2836(88)90555-4.
[127]
Pulendran, B., and R. Ahmed. 2011. Immunological mechanisms of vaccination. Nat Immunol 12: 509–517. https://doi.org/10.1038/ni.2039.
[128]
Qu, Z., Li, M., Guo, Y., Liu, Y., Wang, J., Gao, M. 2020. Expression, purification, and characterisation of recombinant ferritin in insect cells using the baculovirus expression system. Biotechnol Lett 42: 57–65. https://doi.org/10.1007/s10529-019-02755-6.
[129]
Rangel, G., Bárcena, J., Moreno, N., Mata, C.P., Castón, J.R., Alejo, A., Blanco, E. 2021. Chimeric RHDV virus-Like particles displaying Foot-and-Mouth disease virus epitopes elicit neutralizing antibodies and confer partial protection in Pigs. Vaccines (Basel) 9. https://doi.org/10.3390/vaccines9050470.
[130]
Ren, Z., Zhao, Y., Liu, J., Ji, X., Meng, L., Wang, T., Sun, W., Zhang, K., Sang, X., Yu, Z., et al. 2018. Inclusion of membrane-anchored LTB or flagellin protein in H5N1 virus-like particles enhances protective responses following intramuscular and oral immunization of mice. Vaccine 36: 5990–5998. https://doi.org/10.1016/j.vaccine.2018.08.053.
[131]
Ridpath, J.F., and W.L. Mengeling. 1988. Uptake of porcine parvovirus into host and nonhost cells suggests host specificity is determined by intracellular factors. Virus Res 10: 17–27. https://doi.org/10.1016/0168-1702(88)90054-8.
[132]
Rodrigues, M. Q., Alves, P. M. & Rold?o, A. 2021. Functionalizing Ferritin Nanoparticles for Vaccine Development. Pharmaceutics 13. https://doi.org/10.3390/pharmaceutics13101621.
[133]
Ruiz, V., Mignaqui, A.C., Nu?ez, M.C., Reytor, E., Escribano, J.M., Wigdorovitz, A. 2014. Comparison of strategies for the production of FMDV empty capsids using the baculovirus vector system. Mol Biotechnol 56: 963–970. https://doi.org/10.1007/s12033-014-9775-8.
[134]
Ryan, M.D., G.J. Belsham, and A.M. King. 1989. Specificity of enzyme-substrate interactions in foot-and-mouth disease virus polyprotein processing. Virology 173: 35–45. https://doi.org/10.1016/0042-6822(89)90219-5.
[135]
Sandrock, C., and T. Kelly. 2007. Clinical review: update of avian influenza A infections in humans. Crit Care 11: 209. https://doi.org/10.1186/cc5675.
[136]
Sharma, J., Shepardson, K., Johns, L.L., Wellham, J., Avera, J., Schwarz, B., Rynda-Apple, A., Douglas, T. 2020. A self-adjuvanted, modular, antigenic VLP for rapid response to influenza virus variability. ACS Appl Mater Interfaces 12: 18211–18224. https://doi.org/10.1021/acsami.9b21776.
[137]
Shi, X., Yang, K., Song, H., Teng, Z., Zhang, Y., Ding, W., Wang, A., Tan, S., Dong, H., Sun, S., et al. 2022. Development and efficacy evaluation of a novel nano-emulsion adjuvant for a Foot-and-Mouth disease virus-like particles vaccine based on squalane. Nanomaterials (Basel) 12. https://doi.org/10.3390/nano12223934.
[138]
Silva, T.M., Olinda, R.G., Rodrigues, C.M., Camara, A.C., Lopes, F.C., Coelho, W.A., Ribeiro, M.F., Freitas, C.I., Teixeira, M.M., Batista, J.S. 2013. Pathogenesis of reproductive failure induced by Trypanosoma vivax in experimentally infected pregnant ewes. Vet Res 44: 1. https://doi.org/10.1186/1297-9716-44-1.
[139]
Singleton R.L., Sanders C.A., Jones K., Thorington B., Egbo T., Coats M.T., Waffo A.B. 2018. Function of the RNA coliphage Qβ proteins in medical In vitro evolution. Methods Protoc 1. https://doi.org/10.3390/mps1020018.
[140]
Sit, T.L., M.G. Abouhaidar, and S. Holy. 1989. Nucleotide sequence of papaya mosaic virus RNA. J Gen Virol 70 (Pt 9): 2325–2331. https://doi.org/10.1099/0022-1317-70-9-2325.
[141]
Skamel, C., S.G. Aller, and Waffo A. Bopda. 2014. In vitro evolution and affinity-maturation with Coliphage qβ display. PLoS One 9: e113069. https://doi.org/10.1371/journal.pone.0113069.
[142]
Spickler, A.R., and J.A. Roth. 2003. Adjuvants in veterinary vaccines: modes of action and adverse effects. J Vet Intern Med 17: 273–281. https://doi.org/10.1111/j.1939-1676.2003.tb02448.x.
[143]
Tan, T.K., Rijal, P., Rahikainen, R., Keeble, A.H., Schimanski, L., Hussain, S., Harvey, R., Hayes, J.W.P., Edwards, J.C., McLean, R.K., et al. 2021. A COVID-19 vaccine candidate using SpyCatcher multimerization of the SARS-CoV-2 spike protein receptor-binding domain induces potent neutralising antibody responses. Nat Commun 12: 542. https://doi.org/10.1038/s41467-020-20654-7.
[144]
Taylor, D.N., Treanor, J.J., Sheldon, E.A., Johnson, C., Umlauf, S., Song, L., Kavita, U., Liu, G., Tussey, L., Ozer, K., et al. 2012. Development of VAX128, a recombinant hemagglutinin (HA) influenza-flagellin fusion vaccine with improved safety and immune response. Vaccine 30: 5761–5769. https://doi.org/10.1016/j.vaccine.2012.06.086.
[145]
Terhuja, M., P. Saravanan, and R.P. Tamilselvan. 2015. Comparative efficacy of virus like particle (VLP) vaccine of foot-and-mouth-disease virus (FMDV) type O adjuvanted with poly I: C or CpG in guinea pigs. Biologicals 43: 437–443. https://doi.org/10.1016/j.biologicals.2015.09.004.
[146]
Tiwari, R., Gupta, R.P., Singh, V.K., Kumar, A., Rajneesh, Madhukar, P., Sundar, S., Gautam, V., Kumar, R. 2023. Nanotechnology-based strategies in parasitic disease management: from prevention to diagnosis and treatment. ACS Omega 8: 42014–42027. https://doi.org/10.1021/acsomega.3c04587.
[147]
Theil, E.C. 2013. Ferritin: the protein nanocage and iron biomineral in health and in disease. Inorg Chem 52: 12223–12233. https://doi.org/10.1021/ic400484n.
[148]
Turley, C.B., Rupp, R.E., Johnson, C., Taylor, D.N., Wolfson, J., Tussey, L., Kavita, U., Stanberry, L., Shaw, A. 2011. Safety and immunogenicity of a recombinant M2e-flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine 29: 5145–5152. https://doi.org/10.1016/j.vaccine.2011.05.041.
[149]
Valícek, L., B. Smíd, L. Rodák, and J. Kudrna. 1990. Electron and immunoelectron microscopy of rabbit haemorrhagic disease virus (RHDV). Arch Virol 112: 271–275. https://doi.org/10.1007/bf01323171.
[150]
Vartak, A. & Sucheck, S. J. 2016. Recent Advances in Subunit Vaccine Carriers. Vaccines (Basel) 4. https://doi.org/10.3390/vaccines4020012
[151]
Veerapen, V.P., A.R. van Zyl, A. Wigdorovitz, E.P. Rybicki, and A.E. Meyers. 2018. Novel expression of immunogenic foot-and-mouth disease virus-like particles in Nicotiana benthamiana. Virus Res 244: 213–217. https://doi.org/10.1016/j.virusres.2017.11.027.
[152]
Wang, B.Z., Quan, F.S., Kang, S.M., Bozja, J., Skountzou, I., Compans, R.W. 2008. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J Virol 82: 11813–11823. https://doi.org/10.1128/jvi.01076-08.
[153]
Wang, B.Z., Xu, R., Quan, F.S., Kang, S.M., Wang, L., Compans, R.W. 2010. Intranasal immunization with influenza VLPs incorporating membrane-anchored flagellin induces strong heterosubtypic protection. PLoS One 5: e13972. https://doi.org/10.1371/journal.pone.0013972.
[154]
Wang, C., J. Tu, J. Liu, and I.J. Molineux. 2019. Structural dynamics of bacteriophage P22 infection initiation revealed by cryo-electron tomography. Nat Microbiol 4: 1049–1056. https://doi.org/10.1038/s41564-019-0403-z.
[155]
Wang, G., Liu, Y., Feng, H., Chen, Y., Yang, S., Wei, Q., Wang, J., Liu, D., Zhang, G. 2018. Immunogenicity evaluation of MS2 phage-mediated chimeric nanoparticle displaying an immunodominant B cell epitope of foot-and-mouth disease virus. PeerJ 6: e4823. https://doi.org/10.7717/peerj.4823.
[156]
Wang, J., Liu, Y., Chen, Y., Wang, A., Wei, Q., Liu, D., Zhang, G. 2020. Large-scale manufacture of VP2 VLP vaccine against porcine parvovirus in Escherichia coli with high-density fermentation. Appl Microbiol Biotechnol 104: 3847–3857. https://doi.org/10.1007/s00253-020-10483-5.
[157]
Wang, J., Liu, Y., Chen, Y., Zhang, T., Wang, A., Wei, Q., Liu, D., Wang, F., Zhang, G. 2021. Capsid assembly is regulated by amino acid residues asparagine 47 and 48 in the VP2 protein of porcine parvovirus. Veterinary Microbiology 253: 108974. https://doi.org/10.1016/j.vetmic.2020.108974.
[158]
Wang, N., Zhan, Y., Wang, A., Zhang, L., Khayat, R., Yang, Y. 2016. In silico analysis of surface structure variation of PCV2 capsid resulting from loop mutations of its capsid protein (Cap). J Gen Virol 97: 3331–3344. https://doi.org/10.1099/jgv.0.000634.
[159]
Wang, X., Xu, F., Liu, J., Gao, B., Liu, Y., Zhai, Y., Ma, J., Zhang, K., Baker, T.S., Schulten, K. 2013. Atomic model of rabbit hemorrhagic disease virus by cryo-electron microscopy and crystallography. PLoS Pathog 9: e1003132. https://doi.org/10.1371/journal.ppat.1003132.
[160]
Weidenbacher, P.A., Sanyal, M., Friedland, N., Tang, S., Arunachalam, P.S., Hu, M., Kumru, O.S., Morris, M.K., Fontenot ,J., Shirreff, L., et al. 2023. A ferritin-based COVID-19 nanoparticle vaccine that elicits robust, durable, broad-spectrum neutralizing antisera in non-human primates. Nat Commun 14: 2149. https://doi.org/10.1038/s41467-023-37417-9.
[161]
Wilson, N.S., Duewell, P., Yang, B., Li Y., Marsters, S., Koernig, S., Latz, E., Maraskovsky, E., Morelli, A.B., Schnurr, M., et al. 2014. Inflammasome-dependent and -independent IL-18 production mediates immunity to the ISCOMATRIX adjuvant. J Immunol 192: 3259–3268. https://doi.org/10.4049/jimmunol.1302011.
[162]
Win, S.J., V.K. Ward, P.R. Dunbar, S.L. Young, and M.A. Baird. 2011. Cross-presentation of epitopes on virus-like particles via the MHC I receptor recycling pathway. Immunol Cell Biol 89: 681–688. https://doi.org/10.1038/icb.2010.161.
[163]
Xiao, Y., Chen, H.Y., Wang, Y., Yin, B., Lv, C., Mo, X., Yan, H., Xuan, Y., Huang, Y., Pang, W. 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: 56. https://doi.org/10.1186/s12896-016-0285-6.
[164]
Xiao, Y., Zhang, S., Yan, H., Geng, X., Wang, Y., Xu, X., Wang, M., Zhang, H., Huang, B., Pang, W., et al. 2021. The high immunity induced by the virus-like particles of foot-and-mouth disease virus serotype O. Front Vet Sci 8: 633706. https://doi.org/10.3389/fvets.2021.633706.
[165]
Yang, D., Chen, L., Duan, J., Yu, Y., Zhou, J., Lu, H. 2021. Investigation of kluyveromyces marxianus as a novel host for large-scale production of porcine parvovirus virus-like particles. Microb Cell Fact 20: 24. https://doi.org/10.1186/s12934-021-01514-5.
[166]
Yin, S., Sun, S., Yang, S., Shang, Y., Cai, X., Liu, X. 2010. Self-assembly of virus-like particles of porcine circovirus type 2 capsid protein expressed from Escherichia coli. Virol J 7: 166. https://doi.org/10.1186/1743-422x-7-166.
[167]
Yassine, H.M., Boyington, J.C., McTamney, P.M., Wei, C.J., Kanekiyo, M., Kong, W.P., Gallagher, J.R., Wang, L., Zhang, Y., Joyce, M.G., et al. 2015. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med 21: 1065–1070. https://doi.org/10.1038/nm.3927.
[168]
Zabel, F., T.M. Kündig, and M.F. Bachmann. 2013. Virus-induced humoral immunity: on how B cell responses are initiated. Curr Opin Virol 3: 357–362. https://doi.org/10.1016/j.coviro.2013.05.004.
[169]
Zhao, Z., Chen, X., Chen, Y., Li, H., Fang, K., Chen, H., Li, X., Qian, P. 2021. A Self-assembling ferritin nanoplatform for designing classical swine fever vaccine: Elicitation of potent neutralizing antibody. Vaccines (Basel) 9. https://doi.org/10.3390/vaccines9010045.
[170]
Zhou, H., G. Yao, and S. Cui. 2010. Production and purification of VP2 protein of porcine parvovirus expressed in an insect-baculovirus cell system. Virology Journal 7: 366. https://doi.org/10.1186/1743-422X-7-366.
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