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Virus-Like Particle Vaccines Against Respiratory Viruses and Protozoan Parasites

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Nanoparticles for Rational Vaccine Design

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 433))

Abstract

The field of vaccinology underwent massive advances over the past decades with the introduction of virus-like particles (VLPs), a supra-molecular nanoparticle vaccine platform that resembles viral structures without the ability to replicate in hosts. This innovative approach has been remarkably effective, as evidenced by its profound immunogenicity and safety. These highly desirable intrinsic properties enabled their further development as vaccines against a multitude of diseases. To date, several VLP-based vaccines have already been commercialized and many more are undergoing clinical evaluation prior to FDA approval. However, efficacious vaccines against a plethora of pathogens are still lacking, which imposes a tremendous socioeconomic burden and continues to threaten public health throughout the globe. This is especially the case for several respiratory pathogens and protozoan parasites. In this review, we briefly describe the fundamentals of VLP vaccines and the unique properties that enable these to be such valuable vaccine candidates and summarize current advances in VLP-based vaccines targeting respiratory and parasitic diseases of global importance.

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References

  • Akerlind-Stopner B, Hu A, Mufson MA, Utter G, Norrby E (1993) Antibody responses of children to the C-terminal peptide of the SH protein of respiratory syncytial virus and the immunological characterization of this protein. J Med Virol 40(2):112–120

    Article  CAS  PubMed  Google Scholar 

  • Almeida AP, Dias MO, Vieira Cde A, Chávez-Olórtegui C, Gazzineli RT, Rodrigues MM, Fujiwara RT, Bruna-Romero O (2014) Long-lasting humoral and cellular immune responses elicited by immunization with recombinant chimeras of the plasmodium vivax circumsporozoite protein. Vaccine 32(19):2181–2187

    Article  CAS  PubMed  Google Scholar 

  • Alves E, Salman AM, Leoratti F, Lopez-Camacho C, Viveros-Sandoval ME, Lall A, El-Turabi A, Bachmann MF, Hill AV, Janse CJ, Khan SM et al (2017) Evaluation of plasmodium vivax cell-traversal protein for ookinetes and sporozoites as a preerythrocytic P. Vivax vaccine. Clin Vaccine Immunol 24(4):e00501–16

    Google Scholar 

  • Andersson AC, Resende M, Salanti A, Nielsen MA, Holst PJ (2017) Novel adenovirus encoded virus-like particles displaying the placental malaria associated var2csa antigen. Vaccine 35(8):1140–1147

    Article  CAS  PubMed  Google Scholar 

  • Atcheson E, Bauza K, Salman AM, Alves E, Blight J, Viveros-Sandoval ME, Janse CJ, Khan SM, Hill AVS, Reyes-Sandoval A (2018) Tailoring a plasmodium vivax vaccine to enhance efficacy through a combination of a csp virus-like particle and trap viral vectors. Infect Immun 24(4):e00114–18

    Google Scholar 

  • Bachmann MF, Jennings GT (2010) Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10(11):787–796

    Article  CAS  PubMed  Google Scholar 

  • Bachmann MF, Rohrer UH, Kündig TM, Bürki K, Hengartner H, Zinkernagel RM (1993) The influence of antigen organization on b cell responsiveness. Science 262(5138):1448–1451

    Article  CAS  PubMed  Google Scholar 

  • Berlanda Scorza F, Tsvetnitsky V, Donnelly JJ (2016) Universal influenza vaccines: shifting to better vaccines. Vaccine 34(26):2926–2933

    Article  PubMed  PubMed Central  Google Scholar 

  • Black MW, Boothroyd JC (2000) Lytic cycle of toxoplasma gondii. Microbiol Mol Biol Rev 64(3):607–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanco JCG, Pletneva LM, McGinnes-Cullen L, Otoa RO, Patel MC, Fernando LR, Boukhvalova MS, Morrison TG (2018) Efficacy of a respiratory syncytial virus vaccine candidate in a maternal immunization model. Nat Commun 9(1):1904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bragard C, Duncan GH, Wesley SV, Naidu RA, Mayo MA (2000) Virus-like particles assemble in plants and bacteria expressing the coat protein gene of Indian peanut clump virus. J Gen Virol 81(Pt 1):267–272

    CAS  PubMed  Google Scholar 

  • Brune KD, Howarth M (2018) New routes and opportunities for modular construction of particulate vaccines: stick, click, and glue. Front Immunol 9:1432

    Google Scholar 

  • Brune KD, Leneghan DB, Brian IJ, Ishizuka AS, Bachmann MF, Draper SJ, Biswas S, Howarth M (2016) Plug-and-display: decoration of virus-like particles via isopeptide bonds for modular immunization. Sci Rep 6:19234

    Google Scholar 

  • Brune KD, Buldun CM, Li Y, Taylor IJ, Brod F, Biswas S, Howarth M (2017) Dual plug-and-display synthetic assembly using orthogonal reactive proteins for twin antigen immunization. Bioconjug Chem 28(5):1544–1551

    Article  CAS  PubMed  Google Scholar 

  • Cabral-Miranda G, Heath MD, Mohsen MO, Gomes AC, Engeroff P, Flaxman A, Leoratti FMS, El-Turabi A, Reyes-Sandoval A, Skinner MA, Kramer MF et al (2015) Virus-like particle (VLP) plus microcrystalline tyrosine (mct) adjuvants enhance vaccine efficacy improving t and b cell immunogenicity and protection against plasmodium berghei/vivax. Vaccines (Basel) 5(2)

    Google Scholar 

  • Cabral-Miranda G, Salman AM, Mohsen MO, Storni FL, Roesti ES, Skinner MA, Heath MD, Kramer MF, Khan SM, Janse CJ, Hill AVS et al (2018) Dops adjuvant confers enhanced protection against malaria for VLP-trap based vaccines. Diseases 6(4):107

    Google Scholar 

  • Cane PA (2001) Molecular epidemiology of respiratory syncytial virus. Rev Med Virol 11(2):103–116

    Article  CAS  PubMed  Google Scholar 

  • Chackerian B (2007) Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 6(3):381–390

    Article  CAS  PubMed  Google Scholar 

  • Charlton Hume HK, Lua LHL (2017) Platform technologies for modern vaccine manufacturing. Vaccine 35(35 Pt A):4480–4485

    Google Scholar 

  • Chichester JA, Green BJ, Jones RM, Shoji Y, Miura K, Long CA, Lee CK, Ockenhouse CF, Morin MJ, Streatfield SJ, Yusibov V (2018) Safety and immunogenicity of a plant-produced Pfs25 virus-like particle as a transmission blocking vaccine against malaria: a phase 1 dose-escalation study in healthy adults. Vaccine 36(39):5865–5871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung KY, Coyle EM, Jani D, King LR, 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(32):3953–3962

    Google Scholar 

  • Cimica V, Boigard H, Bhatia B, Fallon JT, Alimova A, Gottlieb P, Galarza JM (2016) Novel respiratory syncytial virus-like particle vaccine composed of the postfusion and prefusion conformations of the f glycoprotein. Clin Vaccine Immunol 23(6):451–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins PL, Fearns R, Graham BS (2013) Respiratory syncytial virus: virology, reverse genetics, and pathogenesis of disease. Curr Top Microbiol Immunol 372:3–38

    Google Scholar 

  • Collins KA, Snaith R, Cottingham MG, Gilbert SC, Hill AVS (2017) Enhancing protective immunity to malaria with a highly immunogenic virus-like particle vaccine. Sci Rep 7:46621

    Google Scholar 

  • Cox MM, Hollister JR (2009) Flublok, a next generation influenza vaccine manufactured in insect cells. Biologicals 37(3):182–189

    Article  CAS  PubMed  Google Scholar 

  • Cullen LM, Boukhvalova MS, Blanco JCG, Morrison TG (2020) Comparisons of antibody populations in different pre-fusion f VLP-immunized cotton rat dams and their offspring. Vaccines (Basel) 8(1):133

    Google Scholar 

  • Danwang C, Bigna JJ, Nzalie RNT, Robert A (2020) Epidemiology of clinical congenital and neonatal malaria in endemic settings: A systematic review and meta-analysis. Malar J 19(1):312

    Article  PubMed  PubMed Central  Google Scholar 

  • DiMiceli L, Pool V, Kelso JM, Shadomy SV, Iskander J (2006) Vaccination of yeast sensitive individuals: review of safety data in the US vaccine adverse event reporting system (vaers). Vaccine 24(6):703–707

    Article  PubMed  Google Scholar 

  • Donaldson B, Al-Barwani F, Young V, Scullion S, Ward V, Young S (2015) Virus-like particles, a versatile subunit vaccine platform. In: Foged C, Rades T, Perrie Y, Hook S (eds) Subunit vaccine delivery. New York, NY, Springer, New York, pp 159–180

    Chapter  Google Scholar 

  • Dubey JP (2009) Toxoplasmosis in sheep–the last 20 years. Vet Parasitol 163(1–2):1–14

    Article  CAS  PubMed  Google Scholar 

  • Duffy PE, Patrick Gorres J (2000) Malaria vaccines since 2000: Progress, priorities, products. NPJ Vaccines 5:48

    Google Scholar 

  • Effio CL, Hubbuch J (2015) Next generation vaccines and vectors: designing downstream processes for recombinant protein-based virus-like particles. Biotechnol J 10(5):715–727

    Article  CAS  PubMed  Google Scholar 

  • Efstathiou C, Abidi SH, Harker J, Stevenson NJ (2020) Revisiting respiratory syncytial virus’s interaction with host immunity, towards novel therapeutics. Cell Mol Life Sci 1–14

    Google Scholar 

  • Eichinger KM, Kosanovich JL, Gidwani SV, Zomback A, Lipp MA, Perkins TN, Oury TD, Petrovsky N, Marshall CP, Yondola MA, Empey KM (2020) Prefusion rsv f immunization elicits th2-mediated lung pathology in mice when formulated with a th2 (but not a th1/th2-balanced) adjuvant despite complete viral protection. Front Immunol 11:1673

    Google Scholar 

  • Fehr T, Skrastina D, Pumpens P, Zinkernagel RM (1998) T cell-independent type i antibody response against b cell epitopes expressed repetitively on recombinant virus particles. Proc Natl Acad Sci U S A 95(16):9477–9481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frey SJ, Varner C, Arsiwala A, Currier MG, Moore ML, Kane RS (2020) The design of vaccines based on the shielding of antigenic site Ú of a respiratory syncytial virus fusion protein immunogen. Adv Healthc Mater e2000714

    Google Scholar 

  • Gause KT, Wheatley AK, Cui J, Yan Y, Kent SJ, Caruso F (2017) Immunological principles guiding the rational design of particles for vaccine delivery. ACS Nano 11(1):54–68

    Article  CAS  PubMed  Google Scholar 

  • Giles BM, Ross TM (2011) A computationally optimized broadly reactive antigen (cobra) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets. Vaccine 29(16):3043–3054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes AC, Mohsen M, Bachmann MF (2017) Harnessing nanoparticles for immunomodulation and vaccines. Vaccines (Basel) 5(1):6

    Google Scholar 

  • Guo J, Zhou A, Sun X, Sha W, Ai K, Pan G, Zhou C, Zhou H, Cong H, He S (2009) Immunogenicity of a virus-like-particle vaccine containing multiple antigenic epitopes of toxoplasma gondii against acute and chronic toxoplasmosis in mice. Front Immunol 10:592

    Google Scholar 

  • Ha B, Yang JE, Chen X, Jadhao SJ, Wright ER, Anderson LJ (2020) Two rsv platforms for g, f, or g+f proteins vlps. Viruses 12(9):906

    Google Scholar 

  • Harmsen C, Turner L, Thrane S, Sander AF, Theander TG, Lavstsen T (2020) Immunization with virus-like particles conjugated to cidrα1 domain of plasmodium falciparum erythrocyte membrane protein 1 induces inhibitory antibodies. Malar J 19(1):132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hervas-Stubbs S, Rueda P, Lopez L, Leclerc C (2007) Insect baculoviruses strongly potentiate adaptive immune responses by inducing type I IFN. J Immunol 178(4):2361–2369

    Article  CAS  PubMed  Google Scholar 

  • Hodgins B, Pillet S, Landry N, Ward BJ (2019) A plant-derived vlp influenza vaccine elicits a balanced immune response even in very old mice with co-morbidities. PLoS ONE 14(1):e0210009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Z, Santi L, LePore K, Kilbourne J, Arntzen CJ, Mason HS (2006) Rapid, high-level production of hepatitis b core antigen in plant leaf and its immunogenicity in mice. Vaccine 24(14):2506–2513

    Article  CAS  PubMed  Google Scholar 

  • Hwang HS, Kwon YM, Lee JS, Yoo SE, Lee YN, Ko EJ, Kim MC, Cho MK, Lee YT, Jung YJ, Lee JY et al (2014) Co-immunization with virus-like particle and DNA vaccines induces protection against respiratory syncytial virus infection and bronchiolitis. Antiviral Res 110:115–123

    Google Scholar 

  • Hwang HS, Lee YT, Kim KH, Park S, Kwon YM, Lee Y, Ko EJ, Jung YJ, Lee JS, Kim YJ, Lee YN et al (2016) Combined virus-like particle and fusion protein-encoding DNA vaccination of cotton rats induces protection against respiratory syncytial virus without causing vaccine-enhanced disease. Virology 494:215–224

    Google Scholar 

  • Hwang HS, Kim KH, Lee Y, Lee YT, Ko EJ, Park S, Lee JS, Lee BC, Kwon YM, Moore ML, Kang SM (2017a) Virus-like particle vaccines containing f or f and g proteins confer protection against respiratory syncytial virus without pulmonary inflammation in cotton rats. Hum Vaccin Immunother 13(5):1031–1039

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang HS, Lee YT, Kim KH, Ko EJ, Lee Y, Kwon YM, Kang SM (2017b) Virus-like particle vaccine primes immune responses preventing inactivated-virus vaccine-enhanced disease against respiratory syncytial virus. Virology 511:142–151

    Google Scholar 

  • Jang YH, Seong BL (2020) Call for a paradigm shift in the design of universal influenza vaccines by harnessing multiple correlates of protection. Expert Opin Drug Discov 15(12):1441–1455

    Google Scholar 

  • Janitzek CM, Matondo S, Thrane S, Nielsen MA, Kavishe R, Mwakalinga SB, Theander TG, Salanti A, Sander AF (2016) Bacterial superglue generates a full-length circumsporozoite protein virus-like particle vaccine capable of inducing high and durable antibody responses. Malar J 15(1):545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jennings GT, Bachmann MF (2008) The coming of age of virus-like particle vaccines. Biol Chem 389(5):521–536

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Wang S, Chen H, Ren H, Huang X, Wang G, Chen Z, Chen L, Chen Z, Zhou P (2017) A bivalent heterologous DNA virus-like-particle prime-boost vaccine elicits broad protection against both group 1 and 2 influenza a viruses. J Virol 91(9):e02052–16

    Google Scholar 

  • Jin J, Tarrant RD, Bolam EJ, Angell-Manning P, Soegaard M, Pattinson DJ, Dulal P, Silk SE, Marshall JM, Dabbs RA, Nugent FL et al (2018) Production, quality control, stability, and potency of cGMP-produced plasmodium falciparum RH5.1 protein vaccine expressed in drosophila s2 cells. NPJ Vaccines 3:32

    Google Scholar 

  • Jones RM, Chichester JA, Mett V, Jaje J, Tottey S, Manceva S, Casta LJ, Gibbs SK, Musiychuk K, Shamloul M, Norikane J et al (2013) A plant-produced Pfs25 VLP malaria vaccine candidate induces persistent transmission blocking antibodies against plasmodium falciparum in immunized mice. PLoS ONE 8(11):e79538

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang HJ, Baker EN (2011) Intramolecular isopeptide bonds: protein crosslinks built for stress? Trends Biochem Sci 36(4):229–237

    Article  CAS  PubMed  Google Scholar 

  • Kang HJ, Lee SH, Kim MJ, Chu KB, Lee DH, Chopra M, Choi HJ, Park H, Jin H, Quan FS (2019) Influenza virus-like particles presenting both toxoplasma gondii rop4 and rop13 enhance protection against T. Gondii infection. Pharmaceutics 11(7):342

    Google Scholar 

  • Kang HJ, Chu KB, Lee SH, Kim MJ, Park H, Jin H, Moon EK, Quan FS (2020) Toxoplasma gondii virus-like particle vaccination alleviates inflammatory response in the brain upon T. gondii infection. Parasite Immunol 42(6):e12716

    Article  CAS  PubMed  Google Scholar 

  • Khurana S, Wu J, Verma N, Verma S, Raghunandan R, Manischewitz J, King LR, Kpamegan E, Pincus S, Smith G, Glenn G et al (2011) H5n1 virus-like particle vaccine elicits cross-reactive neutralizing antibodies that preferentially bind to the oligomeric form of influenza virus hemagglutinin in humans. J Virol 85(21):10945–10954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khuu D, Eberhard ML, Bristow BN, Javanbakht M, Ash LR, Shafir SC, Sorvillo FJ (2019) Economic impact of malaria-related hospitalizations in the united states, 2000–2014. J Infect Public Health 12(3):424–433

    Article  PubMed  Google Scholar 

  • Kim MC, Song JM, O E, Kwon YM, Lee YJ, Compans RW, Kang SM (2013) Virus-like particles containing multiple m2 extracellular domains confer improved cross-protection against various subtypes of influenza virus. Mol Ther 21(2):485–492

    Google Scholar 

  • Kim MC, Lee YN, Ko EJ, Lee JS, Kwon YM, Hwang HS, Song JM, Song BM, Lee YJ, Choi JG, Kang HM et al (2014) Supplementation of influenza split vaccines with conserved m2 ectodomains overcomes strain specificity and provides long-term cross protection. Mol Ther 22(7):1364–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KH, Lee YT, Hwang HS, Kwon YM, Kim MC, Ko EJ, Lee JS, Lee Y, Kang SM (2015) Virus-like particle vaccine containing the f protein of respiratory syncytial virus confers protection without pulmonary disease by modulating specific subsets of dendritic cells and effector t cells. J Virol 89(22):11692–11705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YJ, Lee YT, Kim MC, Lee YN, Kim KH, Ko EJ, Song JM, Kang SM (2017) Cross-protective efficacy of influenza virus m2e containing virus-like particles is superior to hemagglutinin vaccines and variable depending on the genetic backgrounds of mice. Front Immunol 8:1730

    Google Scholar 

  • Kim AR, Lee DH, Lee SH, Rubino I, Choi HJ, Quan FS (2018) Protection induced by virus-like particle vaccine containing tandem repeat gene of respiratory syncytial virus g protein. PLoS ONE 13(1):e0191277

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim MJ, Lee SH, Kang HJ, Chu KB, Park H, Jin H, Moon EK, Kim SS, Quan FS (2020) Virus-like particle vaccine displaying toxoplasma gondii apical membrane antigen 1 induces protection against T. Gondii ME49 infection in mice. Microb Pathog 142:104090

    Google Scholar 

  • Kingston NJ, Kurtovic L, Walsh R, Joe C, Lovrecz G, Locarnini S, Beeson JG, Netter HJ (2019) Hepatitis B virus-like particles expressing plasmodium falciparum epitopes induce complement-fixing antibodies against the circumsporozoite protein. Vaccine 37(12):1674–1684

    Article  CAS  PubMed  Google Scholar 

  • Ko EJ, Kwon YM, Lee JS, Hwang HS, Yoo SE, Lee YN, Lee YT, Kim MC, Cho MK, Lee YR, Quan FS et al (2015) Virus-like nanoparticle and DNA vaccination confers protection against respiratory syncytial virus by modulating innate and adaptive immune cells. Nanomedicine 11(1):99–108

    Article  CAS  PubMed  Google Scholar 

  • Krammer F, Palese P (2015) Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14(3):167–182

    Article  CAS  PubMed  Google Scholar 

  • Kramer F, García-Sastre A, Palese P (2018) Is it possible to develop a “universal” influenza virus vaccine? Potential target antigens and critical aspects for a universal influenza vaccine. Cold Spring Harb Perspect Biol 10(7):a028845

    Google Scholar 

  • Krietsch Boerner L (2020) The flu shot and the egg. ACS Cent Sci 6(2):89–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kushnir N, Streatfield SJ, 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(1):58–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landry N, Ward BJ, Trépanier S, Montomoli E, Dargis M, Lapini G, Vézina LP (2010) Preclinical and clinical development of plant-made virus-like particle vaccine against avian h5n1 influenza. PLoS ONE 5(12):e15559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landry N, Pillet S, Favre D, Poulin JF, Trépanier S, Yassine-Diab B, Ward BJ (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(2):164–177

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Quan FS, Kwon Y, Sakamoto K, Kang SM, Compans RW, Moore ML (2014) Additive protection induced by mixed virus-like particles presenting respiratory syncytial virus fusion or attachment glycoproteins. Antiviral Res 111:129–135

    Google Scholar 

  • Lee DH, Lee SH, Kim AR, Quan FS (2016a) Virus-like nanoparticle vaccine confers protection against toxoplasma gondii. PLoS ONE 11(8):e0161231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee DH, Kim AR, Lee SH, Quan FS (2016b) Cross-protection induced by toxoplasma gondii virus-like particle vaccine upon intraperitoneal route challenge. Acta Trop 164:77–83

    Google Scholar 

  • Lee Y, Lee YT, Ko EJ, Kim KH, Hwang HS, Park S, Kwon YM, Kang SM (2017a) Soluble f proteins exacerbate pulmonary histopathology after vaccination upon respiratory syncytial virus challenge but not when presented on virus-like particles. Hum Vaccin Immunother 13(11):2594–2605

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee SH, Kim AR, Lee DH, Rubino I, Choi HJ, Quan FS (2017b) Protection induced by virus-like particles containing toxoplasma gondii microneme protein 8 against highly virulent RH strain of toxoplasma gondii infection. PLoS ONE 12(4):e0175644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee SH, Kang HJ, Lee DH, Kang SM, Quan FS (2018a) Virus-like particle vaccines expressing toxoplasma gondii rhoptry protein 18 and microneme protein 8 provide enhanced protection. Vaccine 36(38):5692–5700

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Kang HJ, Lee DH, Quan FS (2018b) Protective immunity induced by incorporating multiple antigenic proteins of toxoplasma gondii into influenza virus-like particles. Front Immunol 9:3073

    Google Scholar 

  • Lee DH, Chu KB, Kang HJ, Lee SH, Chopra M, Choi HJ, Moon EK, Inn KS, Quan FS (2019a) Protection induced by malaria virus-like particles containing codon-optimized AMA-1 of plasmodium berghei. Malar J 18(1):394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YT, Kim KH, Ko EJ, Kim MC, Lee YN, Hwang HS, Lee Y, Jung YJ, Kim YJ, Santos J, Perez DR et al (2019b) Enhancing the cross protective efficacy of live attenuated influenza virus vaccine by supplemented vaccination with m2 ectodomain virus-like particles. Virology 529:111–121

    Google Scholar 

  • Lee SH, Chu KB, Kang HJ, Basak S, Kim MJ, Park H, Jin H, Moon EK, Quan FS (2020a) Virus-like particles expressing plasmodium berghei msp-8 induce protection against P. Berghei infection. Parasite Immunol 42(11):e12781

    Google Scholar 

  • Lee SH, Kang HJ, Chu KB, Basak S, Lee DH, Moon EK, Quan FS (2020b) Protective immunity induced by virus-like particle containing merozoite surface protein 9 of plasmodium berghei. Vaccines (Basel) 8(3):428

    Google Scholar 

  • Leneghan DB, Miura K, Taylor IJ, Li Y, Jin J, Brune KD, Bachmann MF, Howarth M, Long CA, Biswas S (2017) Nanoassembly routes stimulate conflicting antibody quantity and quality for transmission-blocking malaria vaccines. Sci Rep 7(1):3811

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Y, Zhou H (2018) Moving towards improved vaccines for toxoplasma gondii. Expert Opin Biol Ther 18(3):273–280

    Article  PubMed  CAS  Google Scholar 

  • Lindsay BJ, Bonar MM, Costas-Cancelas IN, Hunt K, Makarkov AI, Chierzi S, Krawczyk CM, Landry N, Ward BJ, Rouiller I (2018) Morphological characterization of a plant-made virus-like particle vaccine bearing influenza virus hemagglutinins by electron microscopy. Vaccine 36(16):2147–2154

    Article  CAS  PubMed  Google Scholar 

  • Ling HY, Edwards AM, Gantier MP, Deboer KD, Neale AD, Hamill JD, Walmsley AM (2012) An interspecific Nicotiana hybrid as a useful and cost-effective platform for production of animal vaccines. PLoS ONE 7(4):e35688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, Wu X, Li L, Liu Z, Wang Z (2013) Use of baculovirus expression system for generation of virus-like particles: successes and challenges. Protein Expr Purif 90(2):104–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lomonossoff GP, D’Aoust MA (2016) Plant-produced biopharmaceuticals: a case of technical developments driving clinical deployment. Science 353(6305):1237–1240

    Article  CAS  PubMed  Google Scholar 

  • López-Macías C, Ferat-Osorio E, Tenorio-Calvo A, Isibasi A, Talavera J, Arteaga-Ruiz O, Arriaga-Pizano L, Hickman SP, Allende M, Lenhard K, Pincus S et al (2011) Safety and immunogenicity of a virus-like particle pandemic influenza a (H1N1) 2009 vaccine in a blinded, randomized, placebo-controlled trial of adults in Mexico. Vaccine 29(44):7826–7834

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Low JG, Lee LS, Ooi EE, Ethirajulu K, Yeo P, Matter A, Connolly JE, Skibinski DA, Saudan P, Bachmann M, Hanson BJ et al (2014) Safety and immunogenicity of a virus-like particle pandemic influenza a (H1N1) 2009 vaccine: results from a double-blinded, randomized phase i clinical trial in healthy Asian volunteers. Vaccine 32(39):5041–5048

    Article  CAS  PubMed  Google Scholar 

  • Lua LH, Connors NK, Sainsbury F, Chuan YP, Wibowo N, Middelberg AP (2014) Bioengineering virus-like particles as vaccines. Biotechnol Bioeng 111(3):425–440

    Article  CAS  PubMed  Google Scholar 

  • Luo WY, Lin SY, Lo KW, Lu CH, Hung CL, Chen CY, Chang CC, Hu YC (2013) Adaptive immune responses elicited by baculovirus and impacts on subsequent transgene expression in vivo. J Virol 87(9):4965–4973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madhi SA, Polack FP, Piedra PA, Munoz FM, Trenholme AA, Simões EAF, Swamy GK, Agrawal S, Ahmed K, August A, Baqui AH et al (2020) Respiratory syncytial virus vaccination during pregnancy and effects in infants. N Engl J Med 383(5):426–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malaria: World Health Organization, Geneva (2020). https://www.who.int/news-room/fact-sheets/detail/malaria

  • Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF (2008) Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 38(5):1404–1413

    Article  CAS  PubMed  Google Scholar 

  • Marini A, Zhou Y, Li Y, Taylor IJ, Leneghan DB, Jin J, Zaric M, Mekhaiel D, Long CA, Miura K, Biswas S (2019) A universal plug-and-display vaccine carrier based on HBsAg VLP to maximize effective antibody response. Front Immunol 10:2931

    Google Scholar 

  • Mason HS, Ball JM, Shi JJ, Jiang X, Estes MK, Arntzen CJ (1996) Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc Natl Acad Sci U S A 93(11):5335–5340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazur NI, Higgins D, Nunes MC, Melero JA, Langedijk AC, Horsley N, Buchholz UJ, Openshaw PJ, McLellan JS, Englund JA, Mejias A et al (2018) The respiratory syncytial virus vaccine landscape: lessons from the graveyard and promising candidates. Lancet Infect Dis 18(10):e295–e311

    Article  PubMed  Google Scholar 

  • McGinnes LW, Gravel KA, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, Schmidt MR, Morrison TG (2011) Assembly and immunological properties of newcastle disease virus-like particles containing the respiratory syncytial virus f and g proteins. J Virol 85(1):366–377

    Article  CAS  PubMed  Google Scholar 

  • McGinnes Cullen L, Schmidt MR, Kenward SA, Woodland RT, Morrison TG (2015) Murine immune responses to virus-like particle-associated pre- and postfusion forms of the respiratory syncytial virus f protein. J Virol 89(13):6835–6847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McGinnes Cullen L, Schmidt MR, Morrison TG (2019) Effect of previous respiratory syncytial virus infection on murine immune responses to f and g protein-containing virus-like particles. J Virol 93(9):e00087–19

    Google Scholar 

  • McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A et al (2013) Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340(6136):1113–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohsen MO, Zha L, Cabral-Miranda G, Bachmann MF (2017a) Major findings and recent advances in virus-like particle (vlp)-based vaccines. Semin Immunol 34:123–132

    Google Scholar 

  • Mohsen MO, Gomes AC, Cabral-Miranda G, Krueger CC, Leoratti FM, Stein JV, Bachmann MF (2017b) Delivering adjuvants and antigens in separate nanoparticles eliminates the need of physical linkage for effective vaccination. J Control Release 251:92–100

    Google Scholar 

  • Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB (2007) The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25(27):5086–5096

    Article  PubMed  Google Scholar 

  • Montazeri M, Mikaeili Galeh T, Moosazadeh M, Sarvi S, Dodangeh S, Javidnia J, Sharif M, Daryani A (2020) The global serological prevalence of toxoplasma gondii in felids during the last five decades (1967–2017): a systematic review and meta-analysis. Parasit Vectors 13(1):82

    Article  PubMed  PubMed Central  Google Scholar 

  • Morón G, Rueda P, Casal I, Leclerc C (2002) Cd8alpha- cd11b+ dendritic cells present exogenous virus-like particles to cd8+ t cells and subsequently express cd8alpha and cd205 molecules. J Exp Med 195(10):1233–1245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moyle PM, Toth I (2013) Modern subunit vaccines: Development, components, and research opportunities. ChemMedChem 8(3):360–376

    Article  CAS  PubMed  Google Scholar 

  • Murawski MR, McGinnes LW, Finberg RW, Kurt-Jones EA, Massare MJ, Smith G, Heaton PM, Fraire AE, Morrison TG (2010) Newcastle disease virus-like particles containing respiratory syncytial virus g protein induced protection in BALB/c mice, with no evidence of immunopathology. J Virol 84(2):1110–1123

    Article  CAS  PubMed  Google Scholar 

  • Music N, Reber AJ, Kim MC, York IA, Kang SM (2016) Supplementation of H1N1pdm09 split vaccine with heterologous tandem repeat m2e5x virus-like particles confers improved cross-protection in ferrets. Vaccine 34(4):466–473

    Article  CAS  PubMed  Google Scholar 

  • Ngwuta JO, Chen M, Modjarrad K, Joyce MG, Kanekiyo M, Kumar A, Yassine HM, Moin SM, Killikelly AM, Chuang GY, Druz A et al (2015) Prefusion f-specific antibodies determine the magnitude of RSV neutralizing activity in human sera. Sci Transl Med 7(309):309ra162

    Google Scholar 

  • Olotu A, Fegan G, Wambua J, Nyangweso G, Leach A, Lievens M, Kaslow DC, Njuguna P, Marsh K, Bejon P (2016) Seven-year efficacy of RTS, S/AS01 malaria vaccine among young African children. N Engl J Med 374(26):2519–2529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: global status of toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 39(12):1385–1394

    Article  PubMed  Google Scholar 

  • Park YC, Song JM (2017) Preparation and immunogenicity of influenza virus-like particles using nitrocellulose membrane filtration. Clin Exp Vaccine Res 6(1):61–66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pattinson DJ, Apte SH, Wibowo N, Chuan YP, Rivera-Hernandez T, Groves PL, Lua LH, Middelberg APJ, Doolan DL (2019) Chimeric murine polyomavirus virus-like particles induce plasmodium antigen-specific cd8(+) t cell and antibody responses. Front Cell Infect Microbiol 9:215

    Google Scholar 

  • Pillet S, Couillard J, Trépanier S, Poulin JF, Yassine-Diab B, Guy B, Ward BJ, Landry N (2019) Immunogenicity and safety of a quadrivalent plant-derived virus like particle influenza vaccine candidate-two randomized phase ii clinical trials in 18 to 49 and ≥50 years old adults. PLoS ONE 14(6):e0216533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plotkin S (2014) History of vaccination. Proc Natl Acad Sci U S A 111(34):12283–12287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plotkin S, Robinson JM, Cunningham G, Iqbal R, Larsen S (2017) The complexity and cost of vaccine manufacturing—an overview. Vaccine 35(33):4064–4071

    Article  PubMed  PubMed Central  Google Scholar 

  • Puente-Massaguer E, Gòdia F, Lecina M (2020) Development of a non-viral platform for rapid virus-like particle production in sf9 cells. J Biotechnol 322:43–53

    Google Scholar 

  • Qin J, Zhang Y, Shen X, Gong L, Peng O, Liu Y, Xue C, Cao Y (2018) H7 virus-like particles assembled by hemagglutinin containing H3N2 transmembrane domain and m1 induce broad homologous and heterologous protection in mice. Vaccine 36(33):5030–5036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan FS, Vunnava A, Compans RW, Kang SM (2010) Virus-like particle vaccine protects against 2009 h1n1 pandemic influenza virus in mice. PLoS ONE 5(2):e9161

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quan FS, Kim Y, Lee S, Yi H, Kang SM, Bozja J, Moore ML, Compans RW (2011) Virus like particle vaccine induces protection against respiratory syncytial virus infection in mice. J Infect Dis 204(7):987–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan FS, Kim MC, Lee BJ, Song JM, Compans RW, Kang SM (2012) Influenza M1 VLPS containing neuraminidase induce heterosubtypic cross-protection. Virology 430(2):127–135

    Article  CAS  PubMed  Google Scholar 

  • Quan FS, Basak S, Chu KB, Kim SS, Kang SM (2020) Progress in the development of virus-like particle vaccines against respiratory viruses. Expert Rev Vaccines 19(1):11–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghunandan R, Lu H, Zhou B, Xabier MG, Massare MJ, Flyer DC, Fries LF, Smith GE, Glenn GM (2014) An insect cell derived respiratory syncytial virus (RSV) f nanoparticle vaccine induces antigenic site ii antibodies and protects against RSV challenge in cotton rats by active and passive immunization. Vaccine 32(48):6485–6492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rezaei F, Sarvi S, Sharif M, Hejazi SH, Pagheh AS, Aghayan SA, Daryani A (2019) A systematic review of toxoplasma gondii antigens to find the best vaccine candidates for immunization. Microb Pathog 126:172–184

    Google Scholar 

  • Rohovie MJ, Nagasawa M, Swartz JR (2017) Virus-like particles: next-generation nanoparticles for targeted therapeutic delivery. Bioeng Transl Med 2(1):43–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roldão A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM (2010) Virus-like particles in vaccine development. Expert Rev Vaccines 9(10):1149–1176

    Article  PubMed  Google Scholar 

  • Rueda P, Fominaya J, Langeveld JP, Bruschke C, Vela C, Casal JI (2000) Effect of different baculovirus inactivation procedures on the integrity and immunogenicity of porcine parvovirus-like particles. Vaccine 19(7–8):726–734

    Article  CAS  PubMed  Google Scholar 

  • Ryu S, Cowling BJ (2020) Human influenza epidemiology. Cold Spring Harb Perspect Med

    Google Scholar 

  • Salman AM, Montoya-Díaz E, West H, Lall A, Atcheson E, Lopez-Camacho C, Ramesar J, Bauza K, Collins KA, Brod F, Reis F et al (2017) Rational development of a protective p. Vivax vaccine evaluated with transgenic rodent parasite challenge models. Sci Rep 7:46482

    Google Scholar 

  • Sarma N, Patouillard E, Cibulskis RE, Arcand JL (2019) The economic burden of malaria: revisiting the evidence. Am J Trop Med Hyg 101(6):1405–1415

    Article  PubMed  PubMed Central  Google Scholar 

  • Schepens B, Sedeyn K, Vande Ginste L, De Baets S, Schotsaert M, Roose K, Houspie L, Van Ranst M, Gilbert B, van Rooijen N, Fiers W et al (2014) Protection and mechanism of action of a novel human respiratory syncytial virus vaccine candidate based on the extracellular domain of small hydrophobic protein. EMBO Mol Med 6(11):1436–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartzman LM, Cathcart AL, Pujanauski LM, Qi L, Kash JC, Taubenberger JK (2015) An intranasal virus-like particle vaccine broadly protects mice from multiple subtypes of influenza a virus. MBio 6(4):e01044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi T, McAllister DA, O’Brien KL, Simoes EAF, Madhi SA, Gessner BD, Polack FP, Balsells E, Acacio S, Aguayo C, Alassani I et al (2017) Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: A systematic review and modelling study. Lancet 390(10098):946–958

    Article  PubMed  PubMed Central  Google Scholar 

  • Short KR, Richard M, Verhagen JH, van Riel D, Schrauwen EJ, van den Brand JM, Mänz B, Bodewes R, Herfst S (2015) One health, multiple challenges: the inter-species transmission of influenza a virus. One Health 1:1–13

    Google Scholar 

  • Singh SK, Thrane S, Janitzek CM, Nielsen MA, Theander TG, Theisen M, Salanti A, Sander AF (2017) Improving the malaria transmission-blocking activity of a plasmodium falciparum 48/45 based vaccine antigen by SpyTag/SpyCatcher mediated virus-like display. Vaccine 35(30):3726–3732

    Article  CAS  PubMed  Google Scholar 

  • Singh SK, Thrane S, Chourasia BK, Teelen K, Graumans W, Stoter R, van Gemert GJ, van de Vegte-Bolmer MG, Nielsen MA, Salanti A, Sander AF et al (2019) Pfs230 and pfs48/45 fusion proteins elicit strong transmission-blocking antibody responses against plasmodium falciparum. Front Immunol 10:1256

    Google Scholar 

  • Skibinski DAG, Jones LA, Zhu YO, Xue LW, Au B, Lee B, Naim ANM, Lee A, Kaliaperumal N, Low JGH, Lee LS et al (2018) Induction of human t-cell and cytokine responses following vaccination with a novel influenza vaccine. Sci Rep 8(1):18007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song JM, Hossain J, Yoo DG, Lipatov AS, Davis CT, Quan FS, Chen LM, Hogan RJ, Donis RO, Compans RW, Kang SM (2010) Protective immunity against H5N1 influenza virus by a single dose vaccination with virus-like particles. Virology 405(1):165–175

    Article  CAS  PubMed  Google Scholar 

  • Song JM, Van Rooijen N, Bozja J, Compans RW, Kang SM (2011) Vaccination inducing broad and improved cross protection against multiple subtypes of influenza a virus. Proc Natl Acad Sci U S A 108(2):757–761

    Article  CAS  PubMed  Google Scholar 

  • Song BM, Kang HM, Lee EK, Jung SC, Kim MC, Lee YN, Kang SM, Lee YJ (2016) Supplemented vaccination with tandem repeat m2e virus-like particles enhances protection against homologous and heterologous hpai h5 viruses in chickens. Vaccine 34(5):678–686

    Article  CAS  PubMed  Google Scholar 

  • Thrane S, Janitzek CM, Matondo S, Resende M, Gustavsson T, de Jongh WA, Clemmensen S, Roeffen W, van de Vegte-Bolmer M, van Gemert GJ, Sauerwein R et al (2016) Bacterial superglue enables easy development of efficient virus-like particle based vaccines. J Nanobiotechnology 14:30

    Google Scholar 

  • Tretyakova I, Hidajat R, Hamilton G, Horn N, Nickols B, Prather RO, Tumpey TM, Pushko P (2016) Preparation of quadri-subtype influenza virus-like particles using bovine immunodeficiency virus gag protein. Virology 487:163–171

    Google Scholar 

  • Urakami A, Sakurai A, Ishikawa M, Yap ML, Flores-Garcia Y, Haseda Y, Aoshi T, Zavala FP, Rossmann MG, Kuno S, Ueno R et al (2017) Development of a novel virus-like particle vaccine platform that mimics the immature form of alphavirus. Clin Vaccine Immunol 24(7):e00090–17

    Google Scholar 

  • Valero-Pacheco N, Pérez-Toledo M, Villasís-Keever M, Núñez-Valencia A, Boscó-Gárate I, Lozano-Dubernard B, Lara-Puente H, Espitia C, Alpuche-Aranda C, Bonifaz LC, Arriaga-Pizano L et al (2016) Antibody persistence in adults two years after vaccination with an h1n1 2009 pandemic influenza virus-like particle vaccine. PLoS ONE 11(2):e0150146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Viboud C, Gostic K, Nelson MI, Price GE, Perofsky A, Sun K, Sequeira Trovão N, Cowling BJ, Epstein SL, Spiro DJ (2020) Beyond clinical trials: evolutionary and epidemiological considerations for development of a universal influenza vaccine. PLoS Pathog 16(9):e1008583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walpita P, Johns LM, Tandon R, Moore ML (2015) Mammalian cell-derived respiratory syncytial virus-like particles protect the lower as well as the upper respiratory tract. PLoS ONE 10(7):e0130755

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang JL, Zhang NZ, Li TT, He JJ, Elsheikha HM, Zhu XQ (2019) Advances in the development of anti-toxoplasma gondii vaccines: challenges, opportunities, and perspectives. Trends Parasitol 35(3):239–253

    Article  CAS  PubMed  Google Scholar 

  • Ward BJ, Landry N, Trépanier S, Mercier G, Dargis M, Couture M, D’Aoust MA, Vézina LP (2014) Human antibody response to n-glycans present on plant-made influenza virus-like particle (vlp) vaccines. Vaccine 32(46):6098–6106

    Article  CAS  PubMed  Google Scholar 

  • Weiss DJ, Lucas TCD, Nguyen M, Nandi AK, Bisanzio D, Battle KE, Cameron E, Twohig KA, Pfeffer DA, Rozier JA, Gibson HS et al (2019) Mapping the global prevalence, incidence, and mortality of plasmodium falciparum, 2000–17: a spatial and temporal modelling study. Lancet 394(10195):322–331

    Article  PubMed  PubMed Central  Google Scholar 

  • Wetzel D, Chan JA, Suckow M, Barbian A, Weniger M, Jenzelewski V, Reiling L, Richards JS, Anderson DA, Kouskousis B, Palmer C et al (2019) Display of malaria transmission-blocking antigens on chimeric duck hepatitis B virus-derived virus-like particles produced in Hansenula polymorpha. PLoS ONE 14(9):e0221394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitacre DC, Espinosa DA, Peters CJ, Jones JE, Tucker AE, Peterson DL, Zavala FP, Milich DR (2015) P. Falciparum and P. Vivax epitope-focused VLPS elicit sterile immunity to blood stage infections. PLoS One 10(5):e0124856

    Google Scholar 

  • Yenkoidiok-Douti L, Williams AE, Canepa GE, Molina-Cruz A, Barillas-Mury C (2019) Engineering a virus-like particle as an antigenic platform for a pfs47-targeted malaria transmission-blocking vaccine. Sci Rep 9(1):16833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U, Moy VT, Howarth M (2012) Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc Natl Acad Sci U S A 109(12):E690-697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zambon MC (1999) Epidemiology and pathogenesis of influenza. J Antimicrob Chemother 44 Suppl B:3–9

    Google Scholar 

  • Zeltins A (2013) Construction and characterization of virus-like particles: a review. Mol Biotechnol 53(1):92–107

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wei M, Pan H, Lin Z, Wang K, Weng Z, Zhu Y, Xin L, Zhang J, Li S, Xia N et al (2014) Robust manufacturing and comprehensive characterization of recombinant hepatitis e virus-like particles in hecolin(®). Vaccine 32(32):4039–4050

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Akmar LZ, Bailey F, Rath BA, Alchikh M, Schweiger B, Lucero MG, Nillos LT, Kyaw MH, Kieffer A, Tong S et al (2020) Cost of respiratory syncytial virus-associated acute lower respiratory infection management in young children at the regional and global level: a systematic review and meta-analysis. J Infect Dis 222(Supplement_7):S680–S687

    Google Scholar 

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Funding

This work was supported by grants from the Ministry of Health and Welfare, Republic of Korea (HV20C0085, HV20C0142), and the National Research Foundation of Korea (NRF) (2018R1A6A1A03025124).

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Authors and Affiliations

  1. Department of Biomedical Science, Graduate School, Kyung Hee University, Seoul, 02447, Republic of Korea

    Ki-Back Chu

  2. 26, Kyungheedae-ro, Dongdaemun-gu, Seoul, 02447, Republic of Korea

    Fu-Shi Quan

  3. Department of Medical Zoology, School of Medicine, Kyung Hee University, Seoul, 02447, Republic of Korea

    Fu-Shi Quan

  4. Medical Research Center for Bioreaction To Reactive Oxygen Species and Biomedical Science Institute, School of Medicine, Kyung Hee University, Graduate school, Seoul, 02447, Republic of Korea

    Fu-Shi Quan

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  1. Ki-Back Chu
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Correspondence to Fu-Shi Quan .

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Editors and Affiliations

  1. Department of Chemical Engineering, Texas Tech University, Lubbock, TX, USA

    Harvinder Singh Gill

  2. Department of Microbiology and Immunology, Emory University, Atlanta, GA, USA

    Richard W. Compans

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Chu, KB., Quan, FS. (2021). Virus-Like Particle Vaccines Against Respiratory Viruses and Protozoan Parasites. In: Gill, H.S., Compans, R.W. (eds) Nanoparticles for Rational Vaccine Design. Current Topics in Microbiology and Immunology, vol 433. Springer, Cham. https://doi.org/10.1007/82_2021_232

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