Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Antigen Delivery Systems: Past, Present, and Future

  • Hyun-Jeong Ko (Laboratory of Microbiology and Immunology, Department of Pharmacy, Kangwon National University) ;
  • Yeon-Jeong Kim (Laboratory of Microbiology and Immunology, College of Pharmacy, Inje University)
  • Received : 2023.01.09
  • Accepted : 2023.03.22
  • Published : 2023.07.01
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Abstract

The COVID-19 pandemic has increased demand for safe and effective vaccines. Research to develop vaccines against diseases including Middle East respiratory syndrome, Ebolavirus, human immunodeficiency virus, and various cancers would also contribute to global well-being. For successful vaccine development, the advancement of technologies such as antigen (Ag) screening, Ag delivery systems and adjuvants, and manufacturing processes is essential. Ag delivery systems are required not only to deliver a sufficient amount of Ag for vaccination, but also to enhance immune response. In addition, Ag types and their delivery systems determine the manufacturing processes of the vaccine product. Here, we analyze the characteristics of various Ag delivery systems: plasmids, viral vectors, bacterial vectors, nanoparticles, self-assembled particles, natural and artificial cells, and extracellular vesicles. This review provides insight into the current vaccine landscape and highlights promising avenues of research for the development and improvement of Ag delivery systems.

Keywords

Acknowledgement

This research was supported by a grant (21172MFDS722) from the Ministry of Food and Drug Safety in 2021.

References

  1. Ahmadipour, S., Mohsenzadeh, A., Alimadadi, H., Salehnia, M. and Fallahi, A. (2019) Treating viral diarrhea in children by probiotic and zinc supplements. Pediatr. Gastroenterol. Hepatol. Nutr. 22, 162-170. https://doi.org/10.5223/pghn.2019.22.2.162
  2. Ahrends, T., Busselaar, J., Severson, T. M., Babala, N., de Vries, E., Bovens, A., Wessels, L., van Leeuwen, F. and Borst, J. (2019) CD4+ T cell help creates memory CD8+ T cells with innate and help-independent recall capacities. Nat. Commun. 10, 5531.
  3. Alven, S. and Aderibigbe, B. A. (2020) The therapeutic efficacy of dendrimer and micelle formulations for breast cancer treatment. Pharmaceutics 12, 1212.
  4. Antrobus, R. D., Coughlan, L., Berthoud, T. K., Dicks, M. D., Hill, A. V., Lambe, T. and Gilbert, S. C. (2014) Clinical assessment of a novel recombinant simian adenovirus ChAdOx1 as a vectored vaccine expressing conserved Influenza A antigens. Mol. Ther. 22, 668-674. https://doi.org/10.1038/mt.2013.284
  5. Ascough, S., Vlachantoni, I., Kalyan, M., Haijema, B. J., Wallin-Weber, S., Dijkstra-Tiekstra, M., Ahmed, M. S., van Roosmalen, M., Grimaldi, R., Zhang, Q., Leenhouts, K., Openshaw, P. J. and Chiu, C. (2019) Local and systemic immunity against respiratory syncytial virus induced by a novel intranasal vaccine. A randomized, double-blind, placebo-controlled clinical trial. Am. J. Respir. Crit. Care Med. 200, 481-492. https://doi.org/10.1164/rccm.201810-1921OC
  6. Bachmann, M. F. and Jennings, G. T. (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. Bale, J. B., Gonen, S., Liu, Y., Sheffler, W., Ellis, D., Thomas, C., Cascio, D., Yeates, T. O., Gonen, T., King, N. P. and Baker, D. (2016) Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353, 389-394. https://doi.org/10.1126/science.aaf8818
  8. Bandola-Simon, J. and Roche, P. A. (2019) Dysfunction of antigen processing and presentation by dendritic cells in cancer. Mol. Immunol. 113, 31-37. https://doi.org/10.1016/j.molimm.2018.03.025
  9. Bashaw, A. A., Leggatt, G. R., Chandra, J., Tuong, Z. K. and Frazer, I. H. (2017) Modulation of antigen presenting cell functions during chronic HPV infection. Papillomavirus Res. 4, 58-65. https://doi.org/10.1016/j.pvr.2017.08.002
  10. Bates, T. A., McBride, S. K., Leier, H. C., Guzman, G., Lyski, Z. L., Schoen, D., Winders, B., Lee, J. Y., Lee, D. X., Messer, W. B., Curlin, M. E. and Tafesse, F. G. (2022) Vaccination before or after SARS-CoV-2 infection leads to robust humoral response and antibodies that effectively neutralize variants. Sci. Immunol. 7, eabn8014.
  11. Batich, K. A., Mitchell, D. A., Healy, P., Herndon, J. E., 2nd and Sampson, J. H. (2020) Once, twice, three times a finding: reproducibility of dendritic cell vaccine trials targeting cytomegalovirus in glioblastoma. Clin. Cancer Res. 26, 5297-5303. https://doi.org/10.1158/1078-0432.CCR-20-1082
  12. Biagi, C., Dondi, A., Scarpini, S., Rocca, A., Vandini, S., Poletti, G. and Lanari, M. (2020) Current state and challenges in developing respiratory syncytial virus vaccines. Vaccines (Basel) 8, 672.
  13. Campbell, F., Bos, F. L., Sieber, S., Arias-Alpizar, G., Koch, B. E., Huwyler, J., Kros, A. and Bussmann, J. (2018) Directing nanoparticle biodistribution through evasion and exploitation of stab2-dependent nanoparticle uptake. ACS Nano 12, 2138-2150. https://doi.org/10.1021/acsnano.7b06995
  14. Cao, Z. and Liu, J. (2020) Bacteria and bacterial derivatives as drug carriers for cancer therapy. J. Control. Release 326, 396-407. https://doi.org/10.1016/j.jconrel.2020.07.009
  15. Chang, M. L., Chen, J. C., Yeh, C. T., Chang, M. Y., Liang, C. K., Chiu, C. T., Lin, D. Y. and Liaw, Y. F. (2008) Gene gun bombardment with DNA-coated gold particles is a potential alternative to hydrodynamics-based transfection for delivering genes into superficial hepatocytes. Hum. Gene Ther. 19, 391-395. https://doi.org/10.1089/hum.2007.152
  16. Cheever, M. A. and Higano, C. S. (2011) PROVENGE (Sipuleucel-T) in prostate cancer: the first FDA-approved therapeutic cancer vaccine. Clin. Cancer Res. 17, 3520-3526. https://doi.org/10.1158/1078-0432.CCR-10-3126
  17. Chen, C. L., Wu, J. C., Chen, G. Y., Yuan, P. H., Tseng, Y. W., Li, K. C., Hwang, S. M. and Hu, Y. C. (2015) Baculovirus-mediated miRNA regulation to suppress hepatocellular carcinoma tumorigenicity and metastasis. Mol. Ther. 23, 79-88. https://doi.org/10.1038/mt.2014.126
  18. Chen, H., Wang, L., Zeng, X., Schwarz, H., Nanda, H. S., Peng, X. and Zhou, Y. (2021) Exosomes, a new star for targeted delivery. Front. Cell Dev. Biol. 9, 751079.
  19. Chowdhury, S., Toth, I. and Stephenson, R. J. (2022) Dendrimers in vaccine delivery: recent progress and advances. Biomaterials 280, 121303.
  20. Corthesy, B. and Bioley, G. (2017) Gas-filled microbubbles: novel mucosal antigen-delivery system for induction of anti-pathogen's immune responses in the gut. Gut Microbes 8, 511-519. https://doi.org/10.1080/19490976.2017.1334032
  21. Corthesy, B. and Bioley, G. (2018) Lipid-based particles: versatile delivery systems for mucosal vaccination against infection. Front. Immunol. 9, 431.
  22. Cosgrove, C. A., Lacey, C. J., Cope, A. V., Bartolf, A., Morris, G., Yan, C., Baden, S., Cole, T., Carter, D., Brodnicki, E., Shen, X., Joseph, S., DeRosa, S. C., Peng, L., Yu, X., Ferrari, G., Seaman, M., Montefiori, D. C., Frahm, N., Tomaras, G. D., Stohr, W., McCormack, S. and Shattock, R. J. (2016) Comparative immunogenicity of HIV-1 gp140 vaccine delivered by parenteral, and mucosal routes in female volunteers; MUCOVAC2, a randomized two centre study. PLoS One 11, e0152038. https://doi.org/10.1371/journal.pone.0152038
  23. da Silva, L. T., Santillo, B. T., de Almeida, A., Duarte, A. and Oshiro, T. M. (2018) Using dendritic cell-based immunotherapy to treat HIV: how can this strategy be improved? Front. Immunol. 9, 2993.
  24. Daleke-Schermerhorn, M. H., Felix, T., Soprova, Z., Ten Hagen-Jongman, C. M., Vikstrom, D., Majlessi, L., Beskers, J., Follmann, F., de Punder, K., van der Wel, N. N., Baumgarten, T., Pham, T. V., Piersma, S. R., Jimenez, C. R., van Ulsen, P., de Gier, J. W., Leclerc, C., Jong, W. S. and Luirink, J. (2014) Decoration of outer membrane vesicles with multiple antigens by using an autotransporter approach. Appl. Environ. Microbiol. 80, 5854-5865. https://doi.org/10.1128/AEM.01941-14
  25. Dolzhikova, I., Iliukhina, A., Kovyrshina, A., Kuzina, A., Gushchin, V., Siniavin, A., Pochtovyi, A., Shidlovskaya, E., Kuznetsova, N., Megeryan, M., Dzharullaeva, A., Erokhova, A., Izhaeva, F., Grousova, D., Botikov, A., Shcheblyakov, D., Tukhvatulin, A., Zubkova, O., Logunov, D. and Gintsburg, A. (2021) Sputnik Light booster after Sputnik V vaccination induces robust neutralizing antibody response to B.1.1.529 (Omicron) SARS-CoV-2 variant. medRxiv doi: 10.1101/2021.12.17.21267976 [Preprint].
  26. dos Santos Rodrigues, B., Lakkadwala, S., Sharma, D. and Singh, J. (2019) Chapter 15 - Chitosan for gene, DNA vaccines, and drug delivery. In Materials for Biomedical Engineering. (A.-M. Holban and A. M. Grumezescu, Eds.), pp. 515-550. Elsevier.
  27. Duc le, H., Hong, H. A., Fairweather, N., Ricca, E. and Cutting, S. M. (2003) Bacterial spores as vaccine vehicles. Infect. Immun. 71, 2810-2818. https://doi.org/10.1128/IAI.71.5.2810-2818.2003
  28. Elsana, H., Olusanya, T. O. B., Carr-wilkinson, J., Darby, S., Faheem, A. and Elkordy, A. A. (2019) Evaluation of novel cationic gene based liposomes with cyclodextrin prepared by thin film hydration and microfluidic systems. Sci. Rep. 9, 15120.
  29. Elshaghabee, F. M. F., Rokana, N., Gulhane, R. D., Sharma, C. and Panwar, H. (2017) Bacillus as potential probiotics: status, concerns, and future perspectives. Front. Microbiol. 8, 1490.
  30. Emir Diltemiz, S., Tavafoghi, M., de Barros, N. R., Kanada, M., Heinamaki, J., Contag, C., Seidlits, S. K. and Ashammakhi, N. (2021) Use of artificial cells as drug carriers. Mater. Chem. Front. 5, 6672-6692. https://doi.org/10.1039/D1QM00717C
  31. Gandhi, R. T., Kwon, D. S., Macklin, E. A., Shopis, J. R., McLean, A. P., McBrine, N., Flynn, T., Peter, L., Sbrolla, A., Kaufmann, D. E., Porichis, F., Walker, B. D., Bhardwaj, N., Barouch, D. H. and Kavanagh, D. G. (2016) Immunization of HIV-1-infected persons with autologous dendritic cells transfected with mRNA encoding HIV-1 Gag and Nef: results of a randomized, placebo-controlled clinical trial. J. Acquir. Immune Defic. Syndr. 71, 246-253. https://doi.org/10.1097/QAI.0000000000000852
  32. Gao, Y., Wijewardhana, C. and Mann, J. F. S. (2018) Virus-like particle, liposome, and polymeric particle-based vaccines against HIV1. Front. Immunol. 9, 345.
  33. Gebre, M. S., Brito, L. A., Tostanoski, L. H., Edwards, D. K., Carfi, A. and Barouch, D. H. (2021) Novel approaches for vaccine development. Cell 184, 1589-1603. https://doi.org/10.1016/j.cell.2021.02.030
  34. Ghasparian, A., Riedel, T., Koomullil, J., Moehle, K., Gorba, C., Svergun, D. I., Perriman, A. W., Mann, S., Tamborrini, M., Pluschke, G. and Robinson, J. A. (2011) Engineered synthetic virus-like particles and their use in vaccine delivery. Chembiochem 12, 100-109. https://doi.org/10.1002/cbic.201000536
  35. Gnjatic, S., Altorki, N. K., Tang, D. N., Tu, S. M., Kundra, V., Ritter, G., Old, L. J., Logothetis, C. J. and Sharma, P. (2009) NY-ESO-1 DNA vaccine induces T-cell responses that are suppressed by regulatory T cells. Clin. Cancer Res. 15, 2130-2139. https://doi.org/10.1158/1078-0432.CCR-08-2632
  36. Gonzalez-Mora, A., Hernandez-Perez, J., Iqbal, H. M. N., Rito-Palomares, M. and Benavides, J. (2020) Bacteriophage-based vaccines: a potent approach for antigen delivery. Vaccines (Basel) 8, 504.
  37. Gorski, A., Borysowski, J. and Miedzybrodzki, R. (2020) Phage therapy: towards a successful clinical trial. Antibiotics (Basel) 9, 827.
  38. Guevara, M. L., Persano, F. and Persano, S. (2020) Advances in lipid nanoparticles for mRNA-based cancer immunotherapy. Front. Chem. 8, 589959.
  39. Gustafson, H. H., Holt-Casper, D., Grainger, D. W. and Ghandehari, H. (2015) Nanoparticle uptake: the phagocyte problem. Nano Today 10, 487-510. https://doi.org/10.1016/j.nantod.2015.06.006
  40. Herrmann, I. K., Wood, M. J. A. and Fuhrmann, G. (2021) Extracellular vesicles as a next-generation drug delivery platform. Nat. Nanotechnol. 16, 748-759. https://doi.org/10.1038/s41565-021-00931-2
  41. Ho, J. K., Jeevan-Raj, B. and Netter, H. J. (2020) Hepatitis B virus (HBV) subviral particles as protective vaccines and vaccine platforms. Viruses 12, 126.
  42. Hobernik, D. and Bros, M. (2018) DNA vaccines-how far from clinical use? Int. J. Mol. Sci. 19, 3605.
  43. Hou, X., Zaks, T., Langer, R. and Dong, Y. (2021) Lipid nanoparticles for mRNA delivery. Nat. Rev. Mater. 6, 1078-1094. https://doi.org/10.1038/s41578-021-00358-0
  44. Huang, Y., Nieh, M. P., Chen, W. and Lei, Y. (2022) Outer membrane vesicles (OMVs) enabled bio-applications: a critical review. Biotechnol. Bioeng. 119, 34-47. https://doi.org/10.1002/bit.27965
  45. Iqbal, S., Qu, Y., Dong, Z., Zhao, J., Rauf Khan, A., Rehman, S. and Zhao, Z. (2020) Poly (β-amino esters) based potential drug delivery and targeting polymer; an overview and perspectives (review). Eur. Polym. J. 141, 110097.
  46. Jones, I. and Roy, P. (2021) Sputnik V COVID-19 vaccine candidate appears safe and effective. Lancet 397, 642-643. https://doi.org/10.1016/S0140-6736(21)00191-4
  47. Jong, W. S. P., Daleke-Schermerhorn, M. H., Vikstrom, D., ten Hagen-Jongman, C. M., de Punder, K., van der Wel, N. N., van de Sandt, C. E., Rimmelzwaan, G. F., Follmann, F., Agger, E. M., Andersen, P., de Gier, J.-W. and Luirink, J. (2014) An autotransporter display platform for the development of multivalent recombinant bacterial vector vaccines. Microb. Cell Fact. 13, 162.
  48. Jung, J. H., Rha, M.-S., Sa, M., Choi, H. K., Jeon, J. H., Seok, H., Park, D. W., Park, S.-H., Jeong, H. W., Choi, W. S. and Shin, E.-C. (2021) SARS-CoV-2-specific T cell memory is sustained in COVID-19 convalescent patients for 10 months with successful development of stem cell-like memory T cells. Nat. Commun. 12, 4043.
  49. 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. and Nabel, G. J. (2013) Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499, 102-106. https://doi.org/10.1038/nature12202
  50. Kang, S., Kim, J., Ahn, M., Kim, J., Heo, M.-G., Min, D.-H. and Won, C. (2020) RNAi nanotherapy for fibrosis: highly durable knockdown of CTGF/CCN-2 using siRNA-DegradaBALL (LEM-S401) to treat skin fibrotic diseases. Nanoscale 12, 6385-6393. https://doi.org/10.1039/C9NR10305H
  51. Kechagia, M., Basoulis, D., Konstantopoulou, S., Dimitriadi, D., Gyftopoulou, K., Skarmoutsou, N. and Fakiri, E. M. (2013) Health benefits of probiotics: a review. ISRN Nutr. 2013, 481651.
  52. Kim, J., Kang, S., Kim, K. W., Heo, M.-G., Park, D.-I., Lee, J.-H., Lim, N. J., Min, D.-H. and Won, C. (2022a) Nanoparticle delivery of recombinant IL-2 (BALLkine-2) achieves durable tumor control with less systemic adverse effects in cancer immunotherapy. Biomaterials 280, 121257.
  53. Kim, S. A., Kim, S., Kim, G. B., Goo, J., Kim, N., Lee, Y., Nam, G. H., Lim, S., Kim, T., Chang, K. H., Lee, T. G., Kim, I. S. and Lee, E. J. (2022b) A multivalent vaccine based on ferritin nanocage elicits potent protective immune responses against SARS-CoV-2 mutations. Int. J. Mol. Sci. 23, 6123.
  54. Kim, S. H. and Samal, S. K. (2016) Newcastle disease virus as a vaccine vector for development of human and veterinary vaccines. Viruses 8, 183.
  55. Kushnir, N., Streatfield, S. J. and Yusibov, V. (2012) Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 31, 58-83. https://doi.org/10.1016/j.vaccine.2012.10.083
  56. Lamb, Y. N. (2021) BNT162b2 mRNA COVID-19 vaccine: first approval. Drugs 81, 495-501. https://doi.org/10.1007/s40265-021-01480-7
  57. Landry, N., Pillet, S., Favre, D., Poulin, J.-F., Trepanier, S., Yassine-Diab, B. and Ward, B. J. (2014) Influenza virus-like particle vaccines made in Nicotiana benthamiana elicit durable, poly-functional and cross-reactive T cell responses to influenza HA antigens. Clin. Immunol. 154, 164-177. https://doi.org/10.1016/j.clim.2014.08.003
  58. Landry, N., Ward, B. J., Trepanier, S., Montomoli, E., Dargis, M., Lapini, G. and Vezina, L. P. (2010) Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS One 5, e15559.
  59. Lee, S. Y., Choi, J. H. and Xu, Z. (2003) Microbial cell-surface display. Trends Biotechnol. 21, 45-52. https://doi.org/10.1016/S0167-7799(02)00006-9
  60. Li, H., Guo, L., Zheng, H., Li, J., Zhao, X., Liang, Y., Yang, F., Zhao, Y., Yang, J., Xue, M., Zuo, Y., Zhou, J., Chen, Y., Yang, Z., Li, Y., Jin, W., Shi, H., He, Z., Li, Q. and Liu, L. (2021) Self-assembling nanoparticle vaccines displaying the receptor binding domain of SARS-CoV-2 elicit robust protective immune responses in rhesus monkeys. Bioconjug. Chem. 32, 1034-1046. https://doi.org/10.1021/acs.bioconjchem.1c00208
  61. Liu, S., Wang, X., Yu, X., Cheng, Q., Johnson, L. T., Chatterjee, S., Zhang, D., Lee, S. M., Sun, Y., Lin, T.-C., Liu, J. L. and Siegwart, D. J. (2021) Zwitterionic phospholipidation of cationic polymers facilitates systemic mRNA delivery to spleen and lymph nodes. J. Am. Chem. Soc. 143, 21321-21330. https://doi.org/10.1021/jacs.1c09822
  62. Lopes, A., Vandermeulen, G. and Preat, V. (2019) Cancer DNA vaccines: current preclinical and clinical developments and future perspectives. J. Exp. Clin. Cancer Res. 38, 146.
  63. Lou, B., De Koker, S., Lau, C. Y. J., Hennink, W. E. and Mastrobattista, E. (2019) mRNA polyplexes with post-conjugated GALA peptides efficiently target, transfect, and activate antigen presenting cells. Bioconjug. Chem. 30, 461-475. https://doi.org/10.1021/acs.bioconjchem.8b00524
  64. Lu, H. Y., Chen, Y. H. and Liu, H. J. (2012) Baculovirus as a vaccine vector. Bioengineered 3, 271-274. https://doi.org/10.4161/bioe.20679
  65. Mancini, F., Micoli, F., Necchi, F., Pizza, M., Berlanda Scorza, F. and Rossi, O. (2021) GMMA-based vaccines: the known and the unknown. Front. Immunol. 12, 715393.
  66. Marzi, A., Feldmann, F., Geisbert, T. W., Feldmann, H. and Safronetz, D. (2015) Vesicular stomatitis virus-based vaccines against Lassa and Ebola viruses. Emerg. Infect. Dis. 21, 305-307.
  67. Mascolo, D., Barba, P., De Berardinis, P., Di Rosa, F. and Del Pozzo, G. (2007) Phage display of a CTL epitope elicits a long-term in vivo cytotoxic response. FEMS Immunol. Med. Microbiol. 50, 59-66. https://doi.org/10.1111/j.1574-695X.2007.00229.x
  68. Mehand, M. S., Al-Shorbaji, F., Millett, P. and Murgue, B. (2018) The WHO R&D Blueprint: 2018 review of emerging infectious diseases requiring urgent research and development efforts. Antiviral Res. 159, 63-67. https://doi.org/10.1016/j.antiviral.2018.09.009
  69. Mendonca, S. A., Lorincz, R., Boucher, P. and Curiel, D. T. (2021) Adenoviral vector vaccine platforms in the SARS-CoV-2 pandemic. npj Vaccines 6, 97.
  70. Mitchell, M. J., Billingsley, M. M., Haley, R. M., Wechsler, M. E., Peppas, N. A. and Langer, R. (2021) Engineering precision nanoparticles for drug delivery. Nat. Rev. Drug Discov. 20, 101-124. https://doi.org/10.1038/s41573-020-0090-8
  71. Moss, P. (2022) The T cell immune response against SARSCoV-2. Nat. Immunol. 23, 186-193. https://doi.org/10.1038/s41590-021-01122-w
  72. Nicchi, S., Giuliani, M., Giusti, F., Pancotto, L., Maione, D., Delany, I., Galeotti, C. L. and Brettoni, C. (2021) Decorating the surface of Escherichia coli with bacterial lipoproteins: a comparative analysis of different display systems. Microb. Cell Factories 20, 33.
  73. Nitika, Wei, J. and Hui, A. M. (2022) The delivery of mRNA vaccines for therapeutics. Life (Basel) 12, 1254.
  74. Pena, S. A., Iyengar, R., Eshraghi, R. S., Bencie, N., Mittal, J., Aljohani, A., Mittal, R. and Eshraghi, A. A. (2020) Gene therapy for neurological disorders: challenges and recent advancements. J. Drug Target. 28, 111-128. https://doi.org/10.1080/1061186X.2019.1630415
  75. Perica, K., De Leon Medero, A., Durai, M., Chiu, Y. L., Bieler, J. G., Sibener, L., Niemoller, M., Assenmacher, M., Richter, A., Edidin, M., Oelke, M. and Schneck, J. (2014) Nanoscale artificial antigen presenting cells for T cell immunotherapy. Nanomedicine 10, 119-129. https://doi.org/10.1016/j.nano.2013.06.015
  76. Pigny, F., Lassus, A., Terrettaz, J., Tranquart, F., Corthesy, B. and Bioley, G. (2016) Intranasal vaccination with Salmonella-derived serodominant secreted effector protein B associated with gas-filled microbubbles partially protects against gut infection in mice. J. Infect. Dis. 214, 438-446. https://doi.org/10.1093/infdis/jiw162
  77. Plaza-Diaz, J., Ruiz-Ojeda, F. J., Gil-Campos, M. and Gil, A. (2019) Mechanisms of action of probiotics. Adv. Nutr. 10, S49-S66. https://doi.org/10.1093/advances/nmy063
  78. Ponce-de-Leon, S., Torres, M., Soto-Ramirez, L. E., Jose Calva, J., Santillan-Doherty, P., Carranza-Salazar, D. E., Carreno, J. M., Car-ranza, C., Juarez, E., Carreto-Binaghi, L. E., Ramirez-Martinez, L., la Rosa, G. P., Vigueras-Moreno, R., Ortiz-Stern, A., Lopez-Vidal, Y., Macias, A. E., Torres-Flores, J., Rojas-Martinez, O., SuarezMartinez, A., Peralta-Sanchez, G., Kawabata, H., GonzalezDominguez, I., Martinez-Guevara, J. L., Sun, W., Sarfati-Mizrahi, D., Soto-Priante, E., Chagoya-Cortes, H. E., Lopez-Macias, C., Castro-Peralta, F., Palese, P., Garcia-Sastre, A., Krammer, F. and Lozano-Dubernard, B. (2022) Safety and immunogenicity of a live recombinant Newcastle disease virus-based COVID-19 vaccine (Patria) administered via the intramuscular or intranasal route: interim results of a non-randomized open label phase I trial in Mexico. medRxiv doi: 10.1101/2022.02.08.22270676 [Preprint].
  79. Porrang, S., Davaran, S., Rahemi, N., Allahyari, S. and Mostafavi, E. (2022) How advancing are mesoporous silica nanoparticles? A comprehensive review of the literature. Int. J. Nanomedicine 17, 1803-1827. https://doi.org/10.2147/IJN.S353349
  80. Powell, A. E., Zhang, K., Sanyal, M., Tang, S., Weidenbacher, P. A., Li, S., Pham, T. D., Pak, J. E., Chiu, W. and Kim, P. S. (2021) A single immunization with spike-functionalized ferritin vaccines elicits neutralizing antibody responses against SARS-CoV-2 in mice. ACS Cent. Sci. 7, 183-199.
  81. Raut, S., Mooberry, L., Sabnis, N., Garud, A., Dossou, A. S. and Lacko, A. (2018) Reconstituted HDL: drug delivery platform for overcoming biological barriers to cancer therapy. Front. Pharmacol. 9, 1154.
  82. Reddy, S. T., Rehor, A., Schmoekel, H. G., Hubbell, J. A. and Swartz, M. A. (2006) In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J. Control. Release 112, 26-34. https://doi.org/10.1016/j.jconrel.2006.01.006
  83. Rezaee, M., Oskuee, R. K., Nassirli, H. and Malaekeh-Nikouei, B. (2016) Progress in the development of lipopolyplexes as efficient non-viral gene delivery systems. J. Control. Release 236, 1-14. https://doi.org/10.1016/j.jconrel.2016.06.023
  84. Santos, P. and Almeida, F. (2021) Exosome-based vaccines: history, current state, and clinical trials. Front. Immunol. 12, 711565.
  85. Sartorius, R., Bettua, C., D'Apice, L., Caivano, A., Trovato, M., Russo, D., Zanoni, I., Granucci, F., Mascolo, D., Barba, P., Del Pozzo, G. and De Berardinis, P. (2011) Vaccination with filamentous bacteriophages targeting DEC-205 induces DC maturation and potent anti-tumor T-cell responses in the absence of adjuvants. Eur. J. Immunol. 41, 2573-2584. https://doi.org/10.1002/eji.201141526
  86. Saunders, K. O., Lee, E., Parks, R., Martinez, D. R., Li, D., Chen, H., Edwards, R. J., Gobeil, S., Barr, M., Mansouri, K., Alam, S. M., Sutherland, L. L., Cai, F., Sanzone, A. M., Berry, M., Manne, K., Kapingidza, A. B., Azoitei, M., Tse, L. V., Scobey, T. D., Spreng, R. L., Rountree, R. W., DeMarco, C. T., Denny, T. N., Woods, C. W., Petzold, E. W., Oguin, T. H., Sempowski, G. D., Gagne, M., Douek, D. C., Tomai, M. A., Fox, C. B., Seder, R., Wiehe, K., Weissman, D., Pardi, N., Acharya, P., Andersen, H., Lewis, M. G., Moore, I. N., Montefiori, D. C., Baric, R. S. and Haynes, B. F. (2021) SARSCoV-2 vaccination induces neutralizing antibodies against pandemic and pre-emergent SARS-related coronaviruses in monkeys. bioRxiv doi: 10.1101/2021.02.17.431492 [Preprint].
  87. Saxena, M., van der Burg, S. H., Melief, C. J. M. and Bhardwaj, N. (2021) Therapeutic cancer vaccines. Nat. Rev. Cancer 21, 360-378. https://doi.org/10.1038/s41568-021-00346-0
  88. Schaad, U. B., Buhlmann, U., Burger, R., Ruedeberg, A., WilderSmith, A., Rutishauser, M., Sennhauser, F., Herzog, C., Zellmeyer, M. and Gluck, R. (2000) Comparison of immunogenicity and safety of a virosome influenza vaccine with those of a subunit influenza vaccine in pediatric patients with cystic fibrosis. Antimicrob. Agents Chemother. 44, 1163-1167. https://doi.org/10.1128/AAC.44.5.1163-1167.2000
  89. Sharif, N., Alzahrani, K. J., Ahmed, S. N. and Dey, S. K. (2021) Efficacy, immunogenicity and safety of COVID-19 vaccines: a systematic review and meta-analysis. Front. Immunol. 12, 714170.
  90. Shedlock, D. J. and Weiner, D. B. (2000) DNA vaccination: antigen presentation and the induction of immunity. J. Leukoc. Biol. 68, 793-806. https://doi.org/10.1189/jlb.68.6.793
  91. Shehata, M. M., Mostafa, A., Teubner, L., Mahmoud, S. H., Kandeil, A., Elshesheny, R., Frantz, R., La Pietra, L., Pleschka, S., Osman, A., Kayali, G., Chakraborty, T., Ali, M. A. and Mraheil, M. A. (2019) Bacterial outer membrane vesicles (OMVs)-based dual vaccine for influenza A H1N1 virus and MERS-CoV. Vaccines (Basel) 7, 46.
  92. Sheridan, C. (2021) First COVID-19 DNA vaccine approved, others in hot pursuit. Nat. Biotechnol. 39, 1479-1482. https://doi.org/10.1038/d41587-021-00023-5
  93. Shin, M. D., Shukla, S., Chung, Y. H., Beiss, V., Chan, S. K., Ortega-Rivera, O. A., Wirth, D. M., Chen, A., Sack, M., Pokorski, J. K. and Steinmetz, N. F. (2020) COVID-19 vaccine development and a potential nanomaterial path forward. Nat. Nanotechnol. 15, 646-655. https://doi.org/10.1038/s41565-020-0737-y
  94. Shirbaghaee, Z. and 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
  95. Singh, P., Pandit, S., Mokkapati, V., Garg, A., Ravikumar, V. and Mijakovic, I. (2018) Gold nanoparticles in diagnostics and therapeutics for human cancer. Int. J. Mol. Sci. 19, 1979.
  96. Soetaert, F., Korangath, P., Serantes, D., Fiering, S. and Ivkov, R. (2020) Cancer therapy with iron oxide nanoparticles: agents of thermal and immune therapies. Adv. Drug Deliv. Rev. 163-164, 65-83. https://doi.org/10.1016/j.addr.2020.06.025
  97. Stander, J., Mbewana, S. and Meyers, A. E. (2022) Plant-derived human vaccines: recent developments. BioDrugs 36, 573-589. https://doi.org/10.1007/s40259-022-00544-8
  98. Stobart, C. C., Rostad, C. A., Ke, Z., Dillard, R. S., Hampton, C. M., Strauss, J. D., Yi, H., Hotard, A. L., Meng, J., Pickles, R. J., Sakamoto, K., Lee, S., Currier, M. G., Moin, S. M., Graham, B. S., Boukhvalova, M. S., Gilbert, B. E., Blanco, J. C., Piedra, P. A., Wright, E. R. and Moore, M. L. (2016) A live RSV vaccine with engineered thermostability is immunogenic in cotton rats despite high attenuation. Nat. Commun. 7, 13916.
  99. Tenchov, R., Bird, R., Curtze, A. E. and Zhou, Q. (2021) Lipid nanoparticles-from liposomes to mRNA vaccine delivery, a landscape of research diversity and advancement. ACS Nano 15, 16982-17015. https://doi.org/10.1021/acsnano.1c04996
  100. Tregoning, J. S., Flight, K. E., Higham, S. L., Wang, Z. and Pierce, B. F. (2021) Progress of the COVID-19 vaccine effort: viruses, vaccines and variants versus efficacy, effectiveness and escape. Nat. Rev. Immunol. 21, 626-636. https://doi.org/10.1038/s41577-021-00592-1
  101. Tretiakova, D. S. and Vodovozova, E. L. (2022) Liposomes as adjuvants and vaccine delivery systems. Biochem. (Moscow), Suppl. Ser. 16, 1-20. https://doi.org/10.1134/S1990747822020076
  102. Van Braeckel-Budimir, N., Haijema, B. J. and Leenhouts, K. (2013) Bacterium-like particles for efficient immune stimulation of existing vaccines and new subunit vaccines in mucosal applications. Front. Immunol. 4, 282.
  103. van der Pol, L., Stork, M. and van der Ley, P. (2015) Outer membrane vesicles as platform vaccine technology. Biotechnol. J. 10, 1689-1706. https://doi.org/10.1002/biot.201400395
  104. Ward, B. J., Gobeil, P., Seguin, A., Atkins, J., Boulay, I., Charbonneau, P. Y., Couture, M., D'Aoust, M. A., Dhaliwall, J., Finkle, C., Hager, K., Mahmood, A., Makarkov, A., Cheng, M. P., Pillet, S., Schimke, P., St-Martin, S., Trepanier, S. and Landry, N. (2021) Phase 1 randomized trial of a plant-derived virus-like particle vaccine for COVID-19. Nat. Med. 27, 1071-1078. https://doi.org/10.1038/s41591-021-01370-1
  105. Weinstein, J. S., Hernandez, S. G. and Craft, J. (2012) T cells that promote B-Cell maturation in systemic autoimmunity. Immunol. Rev. 247, 160-171. https://doi.org/10.1111/j.1600-065X.2012.01122.x
  106. Wolf, J., Jannat, R., Dubey, S., Troth, S., Onorato, M. T., Coller, B. A., Hanson, M. E. and Simon, J. K. (2021) Development of pandemic vaccines: ERVEBO case study. Vaccines (Basel) 9, 190.
  107. Xia, J., Miao, Y., Wang, X., Huang, X. and Dai, J. (2022) Recent progress of dendritic cell-derived exosomes (Dex) as an anti-cancer nanovaccine. Biomed. Pharmacother. 152, 113250.
  108. Xie, X., Liao, J., Shao, X., Li, Q. and Lin, Y. (2017) The effect of shape on cellular uptake of gold nanoparticles in the forms of stars, rods, and triangles. Sci. Rep. 7, 3827.
  109. Xu, Q., Zhou, W., Ding, S., Lu, Y., Liu, S., Cao, J., Zhang, Z., Liu, S. and Yu, S. (2021) An Escherichia coli carrier vaccine with surface-displayed protein MAP3061c elicits protective immunity against Mycobacterium paratuberculosis in mice. Res. Vet. Sci. 141, 180-189. https://doi.org/10.1016/j.rvsc.2021.10.019
  110. Yahalom-Ronen, Y., Erez, N., Fisher, M., Tamir, H., Politi, B., Achdout, H., Melamed, S., Glinert, I., Weiss, S., Cohen-Gihon, I., Israeli, O., Izak, M., Mandelboim, M., Caraco, Y., Madar-Balakirski, N., Mechaly, A., Shinar, E., Zichel, R., Cohen, D., Beth-Din, A., Zvi, A., Marcus, H., Israely, T. and Paran, N. (2022) Neutralization of SARS-CoV-2 variants by rVSV-ΔG-spike-elicited human sera. Vaccines (Basel) 10, 291.
  111. Yahalom-Ronen, Y., Tamir, H., Melamed, S., Politi, B., Shifman, O., Achdout, H., Vitner, E. B., Israeli, O., Milrot, E., Stein, D., CohenGihon, I., Lazar, S., Gutman, H., Glinert, I., Cherry, L., Vagima, Y., Weiss, S., Ben-Shmuel, A., Avraham, R., Puni, R., Lupu, E., BarDavid, E., Sittner, A., Erez, N., Zichel, R., Mamroud, E., Mazor, O., Levy, H., Laskar, O., Yitzhaki, S., Shapira, S. C., Zvi, A., Beth-Din, A., Paran, N. and Israely, T. (2020) A single dose of recombinant VSV-ΔG-spike vaccine provides protection against SARS-CoV-2 challenge. Nat. Commun. 11, 6402. https://doi.org/10.1038/s41467-020-20228-7
  112. Yang, B., Jeang, J., Yang, A., Wu, T. C. and Hung, C. F. (2014) DNA vaccine for cancer immunotherapy. Hum. Vaccin. Immunother. 10, 3153-3164. https://doi.org/10.4161/21645515.2014.980686
  113. Yang, R., Deng, Y., Huang, B., Huang, L., Lin, A., Li, Y., Wang, W., Liu, J., Lu, S., Zhan, Z., Wang, Y., A, R., Wang, W., Niu, P., Zhao, L., Li, S., Ma, X., Zhang, L., Zhang, Y., Yao, W., Liang, X., Zhao, J., Liu, Z., Peng, X., Li, H. and Tan, W. (2021) A core-shell structured COVID-19 mRNA vaccine with favorable biodistribution pattern and promising immunity. Signal Transduct. Target. Ther. 6, 213.
  114. Yurina, V. (2018) Live bacterial vectors-A promising DNA vaccine delivery system. Med. Sci. (Basel) 6, 27.
  115. Zamarin, D. and Palese, P. (2012) Oncolytic Newcastle disease virus for cancer therapy: old challenges and new directions. Future Microbiol. 7, 347-367. https://doi.org/10.2217/fmb.12.4