{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T00:54:16Z","timestamp":1791075256213,"version":"4.1.0"},"reference-count":127,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,2,6]],"date-time":"2020-02-06T00:00:00Z","timestamp":1580947200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100012774","name":"Innovationsfonden","doi-asserted-by":"publisher","award":["8088-00032B"],"award-info":[{"award-number":["8088-00032B"]}],"id":[{"id":"10.13039\/100012774","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100012774","name":"Innovationsfonden","doi-asserted-by":"publisher","award":["8053-00175B"],"award-info":[{"award-number":["8053-00175B"]}],"id":[{"id":"10.13039\/100012774","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Capsid-like particles (CLPs) are multimeric, repetitive assemblies of recombinant viral capsid proteins, which are highly immunogenic due to their structural similarity to wild-type viruses. CLPs can be used as molecular scaffolds to enable the presentation of soluble vaccine antigens in a similar structural format, which can significantly increase the immunogenicity of the antigen. CLP-based antigen display can be obtained by various genetic and modular conjugation methods. However, these vary in their versatility as well as efficiency in achieving an immunogenic antigen display. Here, we make a comparative review of the major CLP-based antigen display technologies. The Tag\/Catcher-AP205 platform is highlighted as a particularly versatile and efficient technology that offers new qualitative and practical advantages in designing modular CLP vaccines. Finally, we discuss how split-protein Tag\/Catcher conjugation systems can help to further propagate and enhance modular CLP vaccine designs.<\/jats:p>","DOI":"10.3390\/v12020185","type":"journal-article","created":{"date-parts":[[2020,2,7]],"date-time":"2020-02-07T03:13:27Z","timestamp":1581045207000},"page":"185","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Advantages and Prospects of Tag\/Catcher Mediated Antigen Display on Capsid-Like Particle-Based Vaccines"],"prefix":"10.3390","volume":"12","author":[{"given":"Kara-Lee","family":"Aves","sequence":"first","affiliation":[{"name":"Faculty of Health Science, Institute for Immunology and Microbiology, University of Copenhagen, 2200 Copenhagen, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Louise","family":"Goks\u00f8yr","sequence":"additional","affiliation":[{"name":"Faculty of Health Science, Institute for Immunology and Microbiology, University of Copenhagen, 2200 Copenhagen, Denmark"},{"name":"AdaptVac Aps, Agern Alle 1, 2970 H\u00f8rsholm, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8782-7830","authenticated-orcid":false,"given":"Adam F.","family":"Sander","sequence":"additional","affiliation":[{"name":"Faculty of Health Science, Institute for Immunology and Microbiology, University of Copenhagen, 2200 Copenhagen, Denmark"},{"name":"AdaptVac Aps, Agern Alle 1, 2970 H\u00f8rsholm, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"6707","DOI":"10.1016\/j.vaccine.2016.10.025","article-title":"Vaccine impact: Benefits for human health","volume":"34","author":"Doherty","year":"2016","journal-title":"Vaccine"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2627","DOI":"10.1080\/21645515.2015.1096457","article-title":"Vaccine-preventable diseases in humanitarian emergencies among refugee and internally-displaced populations","volume":"11","author":"Lam","year":"2015","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1086\/498902","article-title":"Measles Transmission and Vaccine Effectiveness during a Large Outbreak on a Densely Populated Island: Implications for Vaccination Policy","volume":"42","author":"Marin","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1097\/00006454-198307000-00005","article-title":"Clinical efficacy of rubella vaccine","volume":"2","author":"Greaves","year":"1983","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1111\/j.0105-2896.2006.00392.x","article-title":"Immunity and immunological memory following smallpox vaccination","volume":"211","author":"Amanna","year":"2006","journal-title":"Immunol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1903","DOI":"10.1056\/NEJMoa066092","article-title":"Duration of Humoral Immunity to Common Viral and Vaccine Antigens","volume":"357","author":"Amanna","year":"2007","journal-title":"N. Engl. J. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1038\/nrmicro2668","article-title":"The development of vaccines: How the past led to the future","volume":"9","author":"Plotkin","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4064","DOI":"10.1016\/j.vaccine.2017.06.003","article-title":"The complexity and cost of vaccine manufacturing\u2013An overview","volume":"35","author":"Plotkin","year":"2017","journal-title":"Vaccine"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"695","DOI":"10.4269\/ajtmh.1991.45.695","article-title":"Safety and immunogenicity of a recombinant sporozoite malaria vaccine against Plasmodium vivax","volume":"45","author":"Herrington","year":"1991","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4536","DOI":"10.1016\/j.vaccine.2016.07.041","article-title":"A phase 2b randomized, controlled trial of the efficacy of the GMZ2 malaria vaccine in African children","volume":"34","author":"Sirima","year":"2016","journal-title":"Vaccine"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"7126","DOI":"10.1016\/j.vaccine.2015.09.101","article-title":"Preclinical and clinical development of a dengue recombinant subunit vaccine","volume":"33","author":"Manoff","year":"2015","journal-title":"Vaccine"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1038\/nrd2224","article-title":"More than one reason to rethink the use of peptides in vaccine design","volume":"6","author":"Purcell","year":"2007","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1080\/14760584.2019.1578216","article-title":"Immunological basis for enhanced immunity of nanoparticle vaccines","volume":"18","author":"Kelly","year":"2019","journal-title":"Expert Rev. Vaccines"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4768","DOI":"10.1016\/j.vaccine.2017.12.079","article-title":"Explanations for the high potency of HPV prophylactic vaccines","volume":"36","author":"Schiller","year":"2018","journal-title":"Vaccine"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"F123","DOI":"10.1016\/j.vaccine.2012.04.108","article-title":"A review of clinical trials of human papillomavirus prophylactic vaccines","volume":"30","author":"Schiller","year":"2012","journal-title":"Vaccine"},{"key":"ref_16","first-page":"999","article-title":"Long-term efficacy and safety of human papillomavirus vaccination","volume":"6","author":"Conte","year":"2014","journal-title":"Int. J. Womens. Health"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/0042-6822(91)90592-Y","article-title":"Expression of human papillomavirus proteins in yeast Saccharomyces cerevisiae","volume":"182","author":"Carter","year":"1991","journal-title":"Virology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/S0167-5699(96)10066-9","article-title":"The influence of virus structure on antibody responses and virus serotype formation","volume":"17","author":"Bachmann","year":"1996","journal-title":"Immunol. Today"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1002\/eji.200737984","article-title":"Nanoparticles target distinct dendritic cell populations according to their size","volume":"38","author":"Manolova","year":"2008","journal-title":"Eur. J. Immunol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3724","DOI":"10.4049\/jimmunol.1103312","article-title":"Innate Immunity Mediates Follicular Innate Immunity Mediates Follicular Transport of Particulate but Not Soluble Protein Antigen","volume":"188","author":"Brombacher","year":"2012","journal-title":"J. Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.jconrel.2017.02.031","article-title":"Delivering adjuvants and antigens in separate nanoparticles eliminates the need of physical linkage for effective vaccination","volume":"251","author":"Mohsen","year":"2017","journal-title":"J. Control. Release"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"26","DOI":"10.4049\/jimmunol.0901540","article-title":"Cutting Edge: Limited Specialization of Dendritic Cell Subsets for MHC Class II-Associated Presentation of Viral Particles","volume":"184","author":"Keller","year":"2010","journal-title":"J. Immunol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1038\/nri2868","article-title":"Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns","volume":"10","author":"Bachmann","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"7690","DOI":"10.1128\/JVI.02588-08","article-title":"Analysis of Modified Human Papillomavirus Type 16 L1 Capsomeres: The Ability To Assemble into Larger Particles Correlates with Higher Immunogenicity","volume":"83","author":"Schadlich","year":"2009","journal-title":"J. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5472","DOI":"10.1128\/JVI.02482-07","article-title":"A Direct Comparison of Human Papillomavirus Type 16 L1 Particles Reveals a Lower Immunogenicity of Capsomeres than Viruslike Particles with Respect to the Induced Antibody Response","volume":"82","author":"Thones","year":"2008","journal-title":"J. Virol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Mohsen, M., Gomes, A., Vogel, M., and Bachmann, M. (2018). Interaction of Viral Capsid-Derived Virus-Like Particles (VLPs) with the Innate Immune System. Vaccines, 6.","DOI":"10.3390\/vaccines6030037"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1159\/000150415","article-title":"Hepatitis B Virus Core Particles as Epitope Carriers","volume":"38","author":"Pumpens","year":"1995","journal-title":"Intervirology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1073\/pnas.96.5.1915","article-title":"Native display of complete foreign protein domains on the surface of hepatitis B virus capsids","volume":"96","author":"Kratz","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1099\/0022-1317-74-4-541","article-title":"Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid","volume":"74","author":"Mastico","year":"1993","journal-title":"J. Gen. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/s007260070072","article-title":"Insertion of foreign epitopes in HBcAg: How to make the chimeric particle assemble","volume":"18","author":"Karpenko","year":"2000","journal-title":"Amino Acid"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.jmb.2008.04.049","article-title":"Immunogenic Display of Diverse Peptides on Virus-like Particles of RNA Phage MS2","volume":"380","author":"Peabody","year":"2008","journal-title":"J. Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"13656","DOI":"10.1128\/JVI.79.21.13656-13666.2005","article-title":"Combinatorial Approach to Hepadnavirus-Like Particle Vaccine Design","volume":"79","author":"Billaud","year":"2005","journal-title":"J. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.coviro.2016.03.001","article-title":"Engineering virus-like particles as vaccine platforms","volume":"18","author":"Frietze","year":"2016","journal-title":"Curr. Opin. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Tyler, M., Tumban, E., Dziduszko, A., Ozbun, M.A., Peabody, D.S., and Chackerian, B. (2014). Immunization with a consensus epitope from Human Papillomavirus L2 induces antibodies that are broadly neutralizing. Vaccine.","DOI":"10.1016\/j.vaccine.2014.06.054"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"12360","DOI":"10.1073\/pnas.1510533112","article-title":"Assessing sequence plasticity of a virus-like nanoparticle by evolution toward a versatile scaffold for vaccines and drug delivery","volume":"112","author":"Lu","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_36","first-page":"381","article-title":"Virus-like particles: Flexible platforms for vaccine development","volume":"6","author":"Chackerian","year":"2007","journal-title":"Vaccines"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"5211","DOI":"10.1016\/j.febslet.2005.08.044","article-title":"In vitro assembly of mosaic hepatitis B virus capsid-like particles (CLPs): Rescue into CLPs of assembly-deficient core protein fusions and FRET-suited CLPs","volume":"579","author":"Vogel","year":"2005","journal-title":"FEBS Lett."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2441","DOI":"10.1002\/cbic.201100469","article-title":"Cell Targeting with Hybrid Q\u03b2 Virus-Like Particles Displaying Epidermal Growth Factor","volume":"12","author":"Pokorski","year":"2011","journal-title":"ChemBioChem"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12951-016-0181-1","article-title":"Bacterial superglue enables easy development of efficient virus \u2011 like particle based vaccines","volume":"14","author":"Thrane","year":"2016","journal-title":"J. Nanobiotechnol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1186\/s12936-016-1574-1","article-title":"Bacterial superglue generates a full-length circumsporozoite protein virus-like particle vaccine capable of inducing high and durable antibody responses","volume":"15","author":"Janitzek","year":"2016","journal-title":"Malar. J."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Palladini, A., Thrane, S., Janitzek, C.M., Pihl, J., Clemmensen, S.B., Adriaan De Jongh, W., Clausen, T.M., Nicoletti, G., Landuzzi, L., and Penichet, M.L. (2017). Virus-like particle display of HER2 induces potent anti-cancer responses. Oncoimmunology.","DOI":"10.1080\/2162402X.2017.1408749"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1172\/JCI11849","article-title":"Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies","volume":"108","author":"Chackerian","year":"2001","journal-title":"J. Clin. Investig."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fimmu.2018.01432","article-title":"New Routes and Opportunities for Modular Construction of Particulate Vaccines: Stick, Click, and Glue","volume":"9","author":"Brune","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Tissot, A.C., Renhofa, R., Schmitz, N., Cielens, I., Meijerink, E., Ose, V., Jennings, G.T., Saudan, P., Pumpens, P., and Bachmann, M.F. (2010). Versatile Virus-Like Particle Carrier for Epitope Based Vaccines. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009809"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/mtm.2014.48","article-title":"Preclinical efficacy and safety of an anti-IL-1\u03b2 vaccine for the treatment of type 2 diabetes","volume":"1","author":"Spohn","year":"2014","journal-title":"Mol. Ther. Methods Clin. Dev."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3104","DOI":"10.1016\/S0264-410X(02)00266-9","article-title":"A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses","volume":"20","author":"Jegerlehner","year":"2002","journal-title":"Vaccine"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1021\/cb400060x","article-title":"Boosting Immunity to Small Tumor-Associated Carbohydrates with Bacteriophage Q\u03b2 Capsids","volume":"8","author":"Yin","year":"2013","journal-title":"ACS Chem. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1021\/bc100367u","article-title":"Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry","volume":"22","author":"Patel","year":"2011","journal-title":"Bioconjug. Chem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.virol.2005.12.039","article-title":"Modified Tobacco mosaic virus particles as scaffolds for display of protein antigens for vaccine applications","volume":"348","author":"Smith","year":"2006","journal-title":"Virology"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.ejpb.2015.07.002","article-title":"His-tagged norovirus-like particles: A versatile platform for cellular delivery and surface display","volume":"96","author":"Koho","year":"2015","journal-title":"Eur. J. Pharm. Biopharm."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep19234","article-title":"Plug-and-Display: Decoration of Virus-Like Particles via isopeptide bonds for modular immunization","volume":"6","author":"Brune","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0181844","article-title":"Preclinical development of a vaccine against oligomeric alpha-synuclein based on virus-like particles","volume":"12","author":"Doucet","year":"2017","journal-title":"PLoS ONE"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Cornuz, J., Zwahlen, S., Jungi, W.F., Osterwalder, J., Klingler, K., van Melle, G., Bangala, Y., Guessous, I., M\u00fcller, P., and Willers, J. (2008). A Vaccine against Nicotine for Smoking Cessation: A Randomized Controlled Trial. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002547"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1038\/nchembio.720","article-title":"Choosing an effective protein bioconjugation strategy","volume":"7","author":"Stephanopoulos","year":"2011","journal-title":"Nat. Chem. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3811","DOI":"10.1038\/s41598-017-03798-3","article-title":"Nanoassembly routes stimulate conflicting antibody quantity and quality for transmission-blocking malaria vaccines","volume":"7","author":"Leneghan","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1002\/eji.200737989","article-title":"Active immunization with IL-1 displayed on virus-like particles protects from autoimmune arthritis","volume":"38","author":"Spohn","year":"2008","journal-title":"Eur. J. Immunol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1002\/bit.24903","article-title":"Escherichia coli-based cell free production of flagellin and ordered flagellin display on virus-like particles","volume":"110","author":"Lu","year":"2013","journal-title":"Biotechnol. Bioeng."},{"key":"ref_58","first-page":"289","article-title":"Growing applications of \u201cclick chemistry\u201d for bioconjugation in contemporary biomedical research","volume":"24","author":"Nwe","year":"2009","journal-title":"Cancer Biother. Radiopharm."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-08787-0","article-title":"Cell-permeable capsids as universal antigen carrier for the induction of an antigen-specific","volume":"7","author":"Akhras","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0143071","article-title":"A Novel Virus-Like Particle Based Vaccine Platform Displaying the Placental Malaria Antigen VAR2CSA","volume":"10","author":"Thrane","year":"2015","journal-title":"PLoS ONE"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"E690","DOI":"10.1073\/pnas.1115485109","article-title":"Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin","volume":"109","author":"Zakeri","year":"2012","journal-title":"PNAS"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.jmb.2013.10.021","article-title":"Structural Analysis and Optimization of the Covalent Association between SpyCatcher and a Peptide Tag","volume":"426","author":"Li","year":"2014","journal-title":"J. Mol. Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.1073\/pnas.1519214113","article-title":"Programmable polyproteams built using twin peptide superglues","volume":"113","author":"Veggiani","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0165074","article-title":"Kinetic Controlled Tag-Catcher Interactions for Directed Covalent Protein Assembly","volume":"11","author":"Tan","year":"2016","journal-title":"PLoS ONE"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"E1176","DOI":"10.1073\/pnas.1315776111","article-title":"SpyLigase peptide-peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture","volume":"111","author":"Fierer","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.1021\/jacs.7b13237","article-title":"SnoopLigase Catalyzes Peptide\u2013Peptide Locking and Enables Solid-Phase Conjugate Isolation","volume":"140","author":"Buldun","year":"2018","journal-title":"J. Am. Chem. Soc."},{"key":"ref_67","first-page":"1","article-title":"Spy&Go purification of SpyTag-proteins using pseudo-SpyCatcher to access an oligomerization toolbox","volume":"10","author":"Banerjee","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_68","first-page":"1","article-title":"Probing the potential of CnaB-type domains for the design of tag\/catcher systems","volume":"12","author":"Kraner","year":"2017","journal-title":"PLoS ONE"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"17474","DOI":"10.1021\/jacs.8b08250","article-title":"An Intrinsically Disordered Peptide-Peptide Stapler for Highly Efficient Protein Ligation Both in Vivo and in Vitro","volume":"140","author":"Wu","year":"2018","journal-title":"J. Am. Chem. Soc."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Keeble, A.H., Turkki, P., Stokes, S., Khairil Anuar, I.N.A., Rahikainen, R., Hyt\u00f6nen, V.P., and Howarth, M. (2019). Approaching infinite affinity through engineering of peptide\u2013protein interaction. PNAS, 1\u201311.","DOI":"10.1073\/pnas.1909653116"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"6405","DOI":"10.1016\/j.vaccine.2019.09.004","article-title":"Virus-like particle-display of the enterotoxigenic Escherichia coli heat-stable toxoid STh-A14T elicits neutralizing antibodies in mice","volume":"37","author":"Govasli","year":"2019","journal-title":"Vaccine"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1038\/s41586-019-1250-z","article-title":"Immunization expands B cells specific to HIV-1 V3 glycan in mice and macaques","volume":"570","author":"Escolano","year":"2019","journal-title":"Nature"},{"key":"ref_73","first-page":"858","article-title":"Cryo Electron Microscopy Reconstructions of the Leviviridae Unveil the Densest Icosahedral RNA Packing Possible","volume":"263","author":"Koning","year":"2006","journal-title":"J. Mol. Biol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"4267","DOI":"10.1016\/j.jmb.2016.08.025","article-title":"Structure of AP205 Coat Protein Reveals Circular Permutation in ssRNA Bacteriophages","volume":"428","author":"Shishovs","year":"2016","journal-title":"J. Mol. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1159\/000449503","article-title":"The True Story and Advantages of RNA Phage Capsids as Nanotools","volume":"59","author":"Pumpens","year":"2016","journal-title":"Intervirology"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"8855","DOI":"10.1021\/acsnano.8b02805","article-title":"Engineering a Rugged Nanoscaffold to Enhance Plug-and-Display Vaccination","volume":"12","author":"Bruun","year":"2018","journal-title":"ACS Nano"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fimmu.2019.02931","article-title":"A universal Plug-and-Display vaccine carrier based on HBsAg VLP to maximize effective antibody response","volume":"10","author":"Marini","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"4747","DOI":"10.2147\/IJN.S137222","article-title":"Dual-linker gold nanoparticles as adjuvanting carriers for multivalent display of recombinant influenza hemagglutinin trimers and flagellin improve the immunological responses in vivo and in vitro","volume":"12","author":"Wang","year":"2017","journal-title":"Int. J. Nanomed."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-019-41522-5","article-title":"A proof-of-concept study for the design of a VLP-based combinatorial HPV and placental malaria vaccine","volume":"9","author":"Janitzek","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1126\/science.8248784","article-title":"The Influence of Antigen Organization on B Cell Responsiveness","volume":"262","author":"Bachmann","year":"1993","journal-title":"Science"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"13988","DOI":"10.1021\/ja4076452","article-title":"Controlling macromolecular topology with genetically encoded SpyTag-SpyCatcher chemistry","volume":"135","author":"Zhang","year":"2013","journal-title":"J. Am. Chem. Soc."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/mBio.01860-17","article-title":"Retargeting lentiviruses via spyCatcher-spyTag chemistry for gene delivery into specific cell types","volume":"8","author":"Kasaraneni","year":"2017","journal-title":"MBio"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1080\/14760584.2017.1299576","article-title":"Strategies to induce broadly protective antibody responses to viral glycoproteins","volume":"16","author":"Krammer","year":"2017","journal-title":"Expert Rev. Vaccines"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1084\/jem.182.1.185","article-title":"Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer","volume":"182","author":"Sattentau","year":"1995","journal-title":"J. Exp. Med."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1111\/imr.12481","article-title":"Native-like Env trimers as a platform for HIV-1 vaccine design","volume":"275","author":"Sanders","year":"2017","journal-title":"Immunol. Rev."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms12041","article-title":"Presenting native-like trimeric HIV-1 antigens with self-assembling nanoparticles","volume":"7","author":"He","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1007\/s12033-012-9598-4","article-title":"Construction and characterization of virus-like particles: A review","volume":"53","author":"Zeltins","year":"2013","journal-title":"Mol. Biotechnol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1002\/bip.22759","article-title":"Different applications of virus-like particles in biology and medicine: Vaccination and delivery systems","volume":"105","author":"Shirbaghaee","year":"2016","journal-title":"Biopolymers"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Mohsen, M.O., Zha, L., Cabral-miranda, G., and Bachmann, M.F. (2017). Major findings and recent advances in virus \u2013 like particle (VLP) -based vaccines. Semin. Immunol., 1\u201310.","DOI":"10.1016\/j.smim.2017.08.014"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/s12951-019-0497-8","article-title":"Production and characterization of novel ssRNA bacteriophage virus-like particles from metagenomic sequencing data","volume":"17","author":"Akopjana","year":"2019","journal-title":"J. Nanobiotechnol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41541-017-0006-8","article-title":"Escherichia coli-derived virus-like particles in vaccine development","volume":"2","author":"Huang","year":"2017","journal-title":"Npj Vaccines"},{"key":"ref_92","first-page":"891","article-title":"Human Papillomavirus Type16-L1 VLP Production in Insect Cells","volume":"16","author":"Abdoli","year":"2013","journal-title":"Iran. J. Basic Med. Sci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"9211","DOI":"10.1128\/JVI.77.17.9211-9220.2003","article-title":"Production of Human Papillomavirus Type 16 Virus-Like Particles in Transgenic Plants","volume":"77","author":"Biemelt","year":"2003","journal-title":"J. Virol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13567-018-0600-4","article-title":"Safety and immunogenicity of plant-produced African horse sickness virus-like particles in horses","volume":"49","author":"Dennis","year":"2018","journal-title":"Vet. Res."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"26","DOI":"10.4161\/hv.22218","article-title":"Plant-derived virus-like particles as vaccines","volume":"9","author":"Chen","year":"2013","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_96","first-page":"1","article-title":"Plant molecular farming of virus-like nanoparticles as vaccines and reagents","volume":"1587","author":"Rybicki","year":"2019","journal-title":"Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol."},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Gomes, A.C., Roesti, E.S., El-Turabi, A., and Bachmann, M.F. (2019). Type of RNA packed in VLPs impacts IgG class switching\u2014implications for an influenza vaccine design. Vaccines, 7.","DOI":"10.3390\/vaccines7020047"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"5346","DOI":"10.4049\/jimmunol.166.9.5346","article-title":"Papillomavirus-Like Particles Induce Acute Activation of Dendritic Cells","volume":"166","author":"Lenz","year":"2001","journal-title":"J. Immunol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1002\/1521-4141(200203)32:3<818::AID-IMMU818>3.0.CO;2-U","article-title":"Cross-presentation of virus-like particles by skin-derived CD8\u2013 dendritic cells: A dispensable role for TAP","volume":"32","author":"Ruedl","year":"2002","journal-title":"Eur. J. Immunol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0001556","article-title":"Phase I Trial of an Alhydrogel Adjuvanted Hepatitis B Core Virus-Like Particle Containing Epitopes of Plasmodium falciparum Circumsporozoite Protein","volume":"3","author":"Gregson","year":"2008","journal-title":"PLoS ONE"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.4049\/jimmunol.172.3.1777","article-title":"Nonmethylated CG Motifs Packaged into Virus-Like Particles Induce Protective Cytotoxic T Cell Responses in the Absence of Systemic Side Effects","volume":"172","author":"Storni","year":"2004","journal-title":"J. Immunol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1038\/nrd1284","article-title":"Therapeutic vaccination for chronic diseases: A new class of drugs in sight","volume":"3","author":"Bachmann","year":"2004","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1212\/01.WNL.0000159740.16984.3C","article-title":"Clinical effects of A\u03b2 immunization (AN1792) in patients with AD in an interrupted trial","volume":"64","author":"Gilman","year":"2005","journal-title":"Neurology"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"5503","DOI":"10.1016\/j.vaccine.2010.02.103","article-title":"Carrier induced epitopic suppression of antibody responses induced by virus-like particles is a dynamic phenomenon caused by carrier-specific antibodies","volume":"28","author":"Jegerlehner","year":"2010","journal-title":"Vaccine"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"6503","DOI":"10.1016\/j.vaccine.2008.09.038","article-title":"Universal influenza A M2e-HBc vaccine protects against disease even in the presence of pre-existing anti-HBc antibodies","volume":"26","author":"Martens","year":"2008","journal-title":"Vaccine"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-bioeng-071811-150124","article-title":"The Effect of Nanoparticle Size, Shape, and Surface Chemistry on Biological Systems","volume":"14","author":"Albanese","year":"2012","journal-title":"Annu. Rev. Biomed. Eng."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1586\/erv.10.89","article-title":"Nano-microparticles as immune adjuvants: Correlating particle sizes and the resultant immune responses","volume":"9","author":"Oyewumi","year":"2010","journal-title":"Expert Rev. Vaccines"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/j.ejpb.2010.12.017","article-title":"Relationship between the size of nanoparticles and their adjuvant activity: Data from a study with an improved experimental design","volume":"78","author":"Li","year":"2011","journal-title":"Eur. J. Pharm. Biopharm."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.immuni.2018.08.012","article-title":"B Cells Are the Dominant Antigen-Presenting Cells that Activate Naive CD4 + T Cells upon Immunization with a Virus-Derived Nanoparticle Antigen","volume":"49","author":"Hong","year":"2018","journal-title":"Immunity"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1007\/s11705-017-1620-8","article-title":"Functional ferritin nanoparticles for biomedical applications","volume":"11","author":"Wang","year":"2017","journal-title":"Front. Chem. Sci. Eng."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"3671","DOI":"10.1073\/pnas.73.10.3671","article-title":"Molecular determinants of immunogenicity: The immunon model of immune response","volume":"73","author":"Dintzis","year":"1976","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"6120","DOI":"10.4049\/jimmunol.169.11.6120","article-title":"Determinants of Autoantibody Induction by Conjugated Papillomavirus Virus-Like Particles","volume":"169","author":"Chackerian","year":"2002","journal-title":"J. Immunol."},{"key":"ref_113","first-page":"1","article-title":"Self-Antigens Displayed on Liposomal Nanoparticles above a Threshold of Epitope Density Elicit Class-Switched Autoreactive Antibodies Independent of T Cell Help","volume":"204","author":"Chen","year":"2019","journal-title":"J. Immunol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1073\/pnas.79.3.884","article-title":"Specific cellular stimulation in the primary immune response: Experimental test of a quantized model","volume":"79","author":"Dintzis","year":"1982","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"3305","DOI":"10.1002\/1521-4141(200211)32:11<3305::AID-IMMU3305>3.0.CO;2-J","article-title":"Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation","volume":"32","author":"Jegerlehner","year":"2002","journal-title":"Eur. J. Immunol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.vaccine.2016.12.049","article-title":"Nanoparticles decorated with viral antigens are more immunogenic at low surface density","volume":"35","author":"Brewer","year":"2017","journal-title":"Vaccine"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"464","DOI":"10.3748\/wjg.v4.i6.464","article-title":"Immune response against HBsAg vaccine","volume":"4","author":"Honorati","year":"1998","journal-title":"World J. Gastroenterol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/S0140-6736(15)60721-8","article-title":"Efficacy and safety of RTS,S\/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: Final results of a phase 3, individually randomised, controlled trial","volume":"386","author":"RTS","year":"2015","journal-title":"Lancet"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-018-34853-2","article-title":"Enhancing Humoral Responses Against HIV Envelope Trimers via Nanoparticle Delivery with Stabilized Synthetic Liposomes","volume":"8","author":"Tokatlian","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"2273","DOI":"10.1016\/j.vaccine.2018.03.036","article-title":"Neutralization effects of antibody elicited by chimeric HBV S antigen viral-like particles presenting HCV neutralization epitopes","volume":"36","author":"Wei","year":"2018","journal-title":"Vaccine"},{"key":"ref_121","doi-asserted-by":"crossref","unstructured":"Chackerian, B., and Peabody, D.S. (2020). Factors That Govern the Induction of Long-Lived Antibody Responses. Viruses, 12.","DOI":"10.3390\/v12010074"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"2832","DOI":"10.1056\/NEJMcp041507","article-title":"Prevention of Hepatitis B with the Hepatitis B Vaccine","volume":"351","author":"Poland","year":"2004","journal-title":"N. Engl. J. Med."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"1731","DOI":"10.1517\/14712598.7.11.1731","article-title":"Review of hepatitis B surface antigen-1018 ISS adjuvant-containing vaccine safety and efficacy","volume":"7","author":"Barry","year":"2007","journal-title":"Expert Opin. Biol. Ther."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12916-019-1277-x","article-title":"Induction and decay of functional complement-fixing antibodies by the RTS,S malaria vaccine in children, and a negative impact of malaria exposure","volume":"17","author":"Kurtovic","year":"2019","journal-title":"BMC Med."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0005165","article-title":"Insights into Long-Lasting Protection Induced by RTS,S\/AS02A Malaria Vaccine: Further Results from a Phase IIb Trial in Mozambican Children","volume":"4","author":"Guinovart","year":"2009","journal-title":"PLoS ONE"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ygyno.2009.01.011","article-title":"Long-term persistence of anti-HPV-16 and -18 antibodies induced by vaccination with the AS04-adjuvanted cervical cancer vaccine: Modeling of sustained antibody responses","volume":"115","author":"David","year":"2009","journal-title":"Gynecol. Oncol."},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1093\/infdis\/jiu648","article-title":"Raising expectations for subunit vaccine","volume":"211","author":"Schiller","year":"2015","journal-title":"J. Infect. 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