Pumpens P, Pushko P. Virus-like particles, a comprehensive guide. Boca Raton, FL: CRC Press; 2022.

Nooraei S, Bahrulolum H, Hoseini ZS, Katalani C, Hajizade A, Easton AJ, et al. Virus-like particles: preparation, immunogenicity and their roles as nanovaccines and drug nanocarriers. J Nanobiotechnol. 2021;19:59.

CAS  Article  Google Scholar 

Heddle JG, Chakraborti S, Iwasaki K. Natural and artificial protein cages: design, structure and therapeutic applications. Curr Opin Struct Biol. 2017;43:148–55.

CAS  PubMed  Article  Google Scholar 

Arevalo MT, Wong TM, Ross TM. Expression and purification of virus-like particles for vaccination. J Vis Exp. 2016;112:54041.

Mohsen MO, Gomes AC, Vogel M, Bachmann MF. Interaction of viral capsid-derived virus-like particles (VLPs) with the innate immune system. Vaccines. 2018;6:37.

Moradi Vahdat M, Hemmati F, Ghorbani A, Rutkowska D, Afsharifar A, Eskandari MH, et al. Hepatitis B core-based virus-like particles: a platform for vaccine development in plants. Biotechnol Rep. 2021;29:e00605.

CAS  Article  Google Scholar 

Cheng L, Wang Y, Du J. Human papillomavirus vaccines: an updated review. Vaccines. 2020;8:391.

de Oliveira CM, Fregnani J, Villa LL. HPV vaccine: updates and highlights. Acta Cytol. 2019;63:159–68.

PubMed  Article  CAS  Google Scholar 

Cao Y, Bing Z, Guan S, Zhang Z, Wang X. Development of new hepatitis E vaccines. Hum Vaccin Immunother. 2018;14:2254–62.

PubMed  PubMed Central  Article  Google Scholar 

Bachmann MF, Rohrer UH, Kundig TM, Burki K, Hengartner H, Zinkernagel RM. The influence of antigen organization on B cell responsiveness. Science. 1993;262:1448–51.

CAS  PubMed  Article  Google Scholar 

Dintzis HM, Dintzis RZ, Vogelstein B. Molecular determinants of immunogenicity: the immunon model of immune response. Proc Natl Acad Sci USA 1976;73:3671–5.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Link A, Zabel F, Schnetzler Y, Titz A, Brombacher F, Bachmann MF. Innate immunity mediates follicular transport of particulate but not soluble protein antigen. J Immunol. 2012;188:3724–33.

CAS  PubMed  Article  Google Scholar 

Zinkhan S, Ogrina A, Balke I, Resevica G, Zeltins A, de Brot S, et al. The impact of size on particle drainage dynamics and antibody response. J Control Rel. 2021;331:296–308.

CAS  Article  Google Scholar 

Mohsen MO, Augusto G, Bachmann MF. The 3Ds in virus-like particle based-vaccines: “design, delivery and dynamics”. Immunol Rev. 2020;296:155–68.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Krueger CC, Thoms F, Keller E, Vogel M, Bachmann MF. Virus-specific secondary plasma cells produce elevated levels of high-avidity antibodies but are functionally short lived. Front Immunol. 2019;10:1831.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Chang X, Krenger P, Krueger CC, Zha L, Han J, Yermanos A, et al. TLR7 signaling shapes and maintains antibody diversity upon virus-like particle immunization. Front Immunol. 2021;12:827256.

CAS  PubMed  Article  Google Scholar 

Gomes AC, Roesti ES, El-Turabi A, Bachmann MF. Type of RNA packed in VLPs impacts IgG class switching-implications for an influenza vaccine design. Vaccines. 2019;7:47.

Ebrahim SH, Maher AD, Kanagasabai U, Alfaraj SH, Alzahrani NA, Alqahtani SA, et al. MERS-CoV Confirmation among 6,873 suspected persons and relevant Epidemiologic and Clinical Features, Saudi Arabia-2014 to 2019. Eclinicalmedicine. 2021;41:101191.

Rabaan AA, Bazzi AM, Al-Ahmed SH, Al-Tawfiq JA. Molecular aspects of MERS-CoV. Front Med. 2017;11:365–77.

PubMed  PubMed Central  Article  Google Scholar 

Alharbi NK. Vaccines against Middle East respiratory syndrome coronavirus for humans and camels. Rev Med Virol. 2017;27:e1917.

Cabral-Miranda G, Lim SM, Mohsen MO, Pobelov IV, Roesti ES, Heath MD, et al. Zika virus-derived E-DIII protein displayed on immunologically optimized VLPs induces neutralizing antibodies without causing enhancement of dengue virus infection. Vaccines Basel. 2019;7:72. 2020;8.

CAS  PubMed Central  Article  Google Scholar 

Thoms F, Jennings GT, Maudrich M, Vogel M, Haas S, Zeltins A, et al. Immunization of cats to induce neutralizing antibodies against Fel d 1, the major feline allergen in human subjects. J Allergy Clin Immun. 2019;144:193–203.

CAS  PubMed  Article  Google Scholar 

Bachmann MF, Zeltins A, Kalnins G, Balke I, Fischer N, Rostaher A, et al. Vaccination against IL-31 for the treatment of atopic dermatitis in dogs. J Allergy Clin Immun. 2018;142:279–81.

CAS  PubMed  Article  Google Scholar 

Olomski F, Fettelschoss V, Jonsdottir S, Birkmann K, Thoms F, Marti E, et al. Interleukin 31 in insect bite hypersensitivity-Alleviating clinical symptoms by active vaccination against itch. Allergy. 2020;75:862–71.

CAS  PubMed  Article  Google Scholar 

Mohsen MO, Rothen D, Balke I, Martina B, Zeltina V, Inchakalody V, et al. Neutralization of MERS coronavirus through a scalable nanoparticle vaccine. NPJ Vaccines. 2021;6:107.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Wang C, Zheng X, Gai W, Zhao Y, Wang H, Wang H, et al. MERS-CoV virus-like particles produced in insect cells induce specific humoural and cellular imminity in rhesus macaques. Oncotarget. 2017;8:12686–94.

PubMed  Article  Google Scholar 

Wang C, Zheng X, Gai W, Wong G, Wang H, Jin H, et al. Novel chimeric virus-like particles vaccine displaying MERS-CoV receptor-binding domain induce specific humoral and cellular immune response in mice. Antivir Res. 2017;140:55–61.

CAS  PubMed  Article  Google Scholar 

J C. COVID-19 vaccine tracker. 2022. https://www.raps.org/news-and-articles/news-articles/2020/3/covid-19-vaccine-tracker.

Zha L, Chang X, Zhao H, Mohsen MO, Hong L, Zhou Y, et al. Development of a vaccine against SARS-CoV-2 based on the receptor-binding domain displayed on virus-like particles. Vaccines. 2021;9:395.

Chang X, Liu X, Mohsen MO, Zeltins A, Martina B, Vogel M, et al. Induction of broadly cross-reactive antibodies by displaying receptor binding domains of SARS-CoV-2 on virus-like particles. Vaccines. 2022;10:307.

Rothen DA, Krenger PS, Nonic A, Balke I, Vogt AS, Chang X, et al. Intranasal administration of a VLP-based vaccine induces neutralizing antibodies against SARS-CoV-2 and variants of concern. Allergy. 2022. https://doi.org/10.1111/all.15311.

Mohsen MO, Balke I, Zinkhan S, Zeltina V, Liu X, Chang X, et al. A scalable and highly immunogenic virus-like particle-based vaccine against SARS-CoV-2. Allergy. 2022;77:243–57.

CAS  PubMed  Article  Google Scholar 

Liu X, Chang X, Rothen D, Derveni M, Krenger P, Roongta S, et al. AP205 VLPs based on dimerized capsid proteins accommodate RBM domain of SARS-CoV-2 and serve as an attractive vaccine candidate. Vaccines (Basel). 2021;9:403.

Chang X, Zeltins A, Mohsen MO, Gharailoo Z, Zha L, Liu X, et al. A novel double mosaic virus-like particle-based vaccine against SARS-CoV-2 incorporates both receptor binding motif (RBM) and fusion domain. Vaccines (Basel). 2021;9:1287.

Tan TK, Rijal P, Rahikainen R, Keeble AH, Schimanski L, Hussain S, et al. A COVID-19 vaccine candidate using SpyCatcher multimerization of the SARS-CoV-2 spike protein receptor-binding domain induces potent neutralising antibody responses. Nat Commun. 2021;12:542.

Yilmaz IC, Ipekoglu EM, Bulbul A, Turay N, Yildirim M, Evcili I, et al. Development and preclinical evaluation of virus-like particle vaccine against COVID-19 infection. Allergy. 2022;77:258–70.

CAS  PubMed  Article  Google Scholar 

Moon KB, Jeon JH, Choi H, Park JS, Park SJ, Lee HJ, et al. Construction of SARS-CoV-2 virus-like particles in plant. Sci Rep. 2022;12:1005.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Pillet S, Arunachalam PS, Andreani G, Golden N, Fontenot J, Aye PP, et al. Safety, immunogenicity, and protection provided by unadjuvanted and adjuvanted formulations of a recombinant plant-derived virus-like particle vaccine candidate for COVID-19 in nonhuman primates. Cell Mol Immunol. 2022;19:222–33.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Jazayeri SD, Poh CL. Development of universal influenza vaccines targeting conserved viral proteins. Vaccines (Basel). 2019;7:169.

Krammer F, Garcia-Sastre A, Paleseu P. 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. 2018;10:a028845.

Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med. 1999;5:1157–63.

CAS  PubMed  Article  Google Scholar 

Buffin S, Peubez I, Barriere F, Nicolai MC, Tapia T, Dhir V, et al. Influenza A and B virus-like particles produced in mammalian cells are highly immunogenic and induce functional antibodies. Vaccine. 2019;37:6857–67.

CAS  PubMed  Article  Google Scholar 

Jegerlehner A, Zabel F, Langer A, Dietmeier K, Jennings GT, Saudan P, et al. Bacterially produced recombinant influenza vaccines based on virus-like particles. PLoS One. 2013;8:e78947.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Skibinski DA, Hanson BJ, Lin Y, von Messling V, Jegerlehner A, Tee JB, et al. Enhanced neutralizing antibody titers and Th1 polarization from a novel Escherichia coli derived pandemic influenza vaccine. PLoS One. 2013;8:e76571.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Low JG, Lee LS, Ooi EE, Ethirajulu K, Yeo P, Matter A, et al. 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. 2014;32:5041–8.

CAS  PubMed  Article  Google Scholar 

Skibinski DAG, Jones LA, Zhu YO, Xue LW, Au B, Lee B, et al. Induction of human T-cell and cytokine responses following vaccination with a novel influenza vaccine. Sci Rep. 2018;8:18007.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Kanekiyo M, Wei CJ, Yassine HM, McTamney PM, Boyington JC, Whittle JR, et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature. 2013;499:102–6.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Tsybalova LM, Stepanova LA, Kuprianov VV, Blokhina EA, Potapchuk MV, Korotkov AV, et al. Development of a candidate influenza vaccine based on virus-like particles displaying influenza M2e peptide into the immunodominant region of hepatitis B core antigen: broad protective efficacy of particles carrying four copies of M2e. Vaccine. 2015;33:3398–406.

CAS  PubMed  Article  Google Scholar 

Fiers W, De Filette M, Birkett A, Neirynck S, Min Jou WA. “universal” human influenza A vaccine. Virus Res. 2004;103:173–6.

CAS  PubMed  Article  Google Scholar 

Jegerlehner A, Schmitz N, Storni T, Bachmann MF. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J Immunol. 2004;172:5598–605.