Design and characterization of chimeric Rabies-SARS-CoV-2 virus-like particles for vaccine purposes.
Chimeric
RBD
Rabies
Spike
VLP
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
02
12
2022
accepted:
17
04
2023
revised:
16
03
2023
medline:
15
5
2023
pubmed:
1
5
2023
entrez:
1
5
2023
Statut:
ppublish
Résumé
Due to the high number of doses required to achieve adequate coverage in the context of COVID-19 pandemics, there is a great need for novel vaccine developments. In this field, there have been research approaches that focused on the production of SARS-CoV-2 virus-like particles. These are promising vaccine candidates as their structure is similar to that of native virions but they lack the genome, constituting a biosafe alternative. In order to produce these structures using mammal cells, it has been established that all four structural proteins must be expressed. Here we report the generation and characterization of a novel chimeric virus-like particle (VLP) that can be produced by the expression of a single novel fusion protein that contains SARS-CoV-2 spike (S) ectodomain fused to rabies glycoprotein membrane anchoring region in HEK293 cells. This protein is structurally similar to native S and can autonomously bud forming enveloped VLPs that resemble native virions both in size and in morphology, displaying S ectodomain and receptor binding domain (RBD) on their surface. As a proof of concept, we analyzed the immunogenicity of this vaccine candidate in mice and confirmed the generation of anti-S, anti-RBD, and neutralizing antibodies. KEY POINTS: • A novel fusion rabies glycoprotein containing S ectodomain was designed. • Fusion protein formed cVLPs that were morphologically similar to SARS-CoV-2 virions. • cVLPs induced anti-S, anti-RBD, and neutralizing antibodies in mice.
Identifiants
pubmed: 37126083
doi: 10.1007/s00253-023-12545-w
pii: 10.1007/s00253-023-12545-w
pmc: PMC10150342
doi:
Substances chimiques
Viral Vaccines
0
Antibodies, Viral
0
Antibodies, Neutralizing
0
Spike Glycoprotein, Coronavirus
0
spike protein, SARS-CoV-2
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3495-3508Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Arista-Romero M, Delcanale P, Pujals S, Albertazzi L (2021) Nanoscale mapping of recombinant viral proteins: from cells to virus-like particles. ACS Photonics 9:101–109. https://doi.org/10.1021/acsphotonics.1c01154
doi: 10.1021/acsphotonics.1c01154
pubmed: 35083366
pmcid: 8778639
Aston-Deaville S, Carlsson E, Saleem M, Thistlethwaite A, Chan H, Maharjan S, Facchetti A, Feavers IM, Alistair Siebert C, Collins RF, Roseman A, Derrick JP (2020) An assessment of the use of hepatitis B virus core protein virus-like particles to display heterologous antigens from Neisseria meningitidis. Vaccine 38:3201–3209. https://doi.org/10.1016/j.vaccine.2020.03.001
doi: 10.1016/j.vaccine.2020.03.001
pubmed: 32178907
pmcid: 7113836
Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, McGettigan J, Khetan S, Segall N, Solis J, Brosz A, Fierro C, Schwartz H, Neuzil K, Corey L et al (2021) Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med 384:403–416. https://doi.org/10.1056/NEJMOA2035389/SUPPL_FILE/NEJMOA2035389_DATA-SHARING.PDF
doi: 10.1056/NEJMOA2035389/SUPPL_FILE/NEJMOA2035389_DATA-SHARING.PDF
pubmed: 33378609
Barda N, Dagan N, Cohen C, Hernán MA, Lipsitch M, Kohane IS, Reis BY, Balicer RD (2021) Effectiveness of a third dose of the BNT162b2 mRNA COVID-19 vaccine for preventing severe outcomes in Israel: an observational study. Lancet 398:2093–2100. https://doi.org/10.1016/S0140-6736(21)02249-2
doi: 10.1016/S0140-6736(21)02249-2
pubmed: 34756184
pmcid: 8555967
Battagliotti JM, Fontana D, Etcheverrigaray M, Kratje R, Prieto C (2020) Characterization of hepatitis B virus surface antigen particles expressed in stably transformed mammalian cell lines containing the large, middle and small surface protein. Antiviral Res 183:104936. https://doi.org/10.1016/j.antiviral.2020.104936
doi: 10.1016/j.antiviral.2020.104936
pubmed: 32979402
Bertona D, Pujato N, Bontempi I, Gonzalez V, Cabrera G, Gugliotta L, Hozbor D, Nicastro A, Calvinho L, Marcipar IS (2017) Development and assessment of a new cage-like particle adjuvant. J Pharm Pharmacol 69(10):1293–1303. https://doi.org/10.1111/jphp.12768
doi: 10.1111/jphp.12768
pubmed: 28664569
Bidart J, Kornuta C, Gammella M, Gnazzo V, Soria I, Langellotti C, Mongini C, Galarza R, Calvinho L, Lupi G, Quattrocchi V, Marcipar I, Zamorano P (2020) A new cage-like particle adjuvant enhances protection of foot-and-mouth disease vaccine. Front Vet Sci 7:1–12. https://doi.org/10.3389/fvets.2020.00396
doi: 10.3389/fvets.2020.00396
Bidart J, Mignaqui A, Kornuta C, Lupi G, Gammella M, Soria I, Galarza R, Ferella A, Cardillo S, Langellotti C, Quattrocchi V, Durocher Y, Wigdorovitz A, Marcipar I, Zamorano P (2021) FMD empty capsids combined with the immunostimulant particle adjuvant -ISPA or ISA206 induce protective immunity against foot and mouth disease virus. Virus Res 297:198339. https://doi.org/10.1016/j.virusres.2021.198339
doi: 10.1016/j.virusres.2021.198339
pubmed: 33596405
Callaway HM, Zyla D, Larrous F, de Melo GD, Hastie KM, Avalos RD, Agarwal A, Corti D, Bourhy H, Saphire EO (2022) Structure of the rabies virus glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Sci Adv 8:eabp9151. https://doi.org/10.1126/sciadv.abp9151
doi: 10.1126/sciadv.abp9151
pubmed: 35714192
pmcid: 9205594
Cervera L, Gutiérrez-Granados S, Martínez M, Blanco J, Gòdia F, Segura MM (2013) Generation of HIV-1 Gag VLPs by transient transfection of HEK 293 suspension cell cultures using an optimized animal-derived component free medium. J Biotechnol 166:152–165. https://doi.org/10.1016/j.jbiotec.2013.05.001
doi: 10.1016/j.jbiotec.2013.05.001
pubmed: 23688724
Coria LM, Saposnik LM, Pueblas Castro C, Castro EF, Bruno LA, Stone WB, Pérez PS, Darriba ML, Chemes LB, Alcain J, Mazzitelli I, Varese A, Salvatori M, Auguste AJ, Álvarez DE, Pasquevich KA, Cassataro J (2022) A novel bacterial protease inhibitor adjuvant in RBD-based COVID-19 vaccine formulations containing alum increases neutralizing antibodies, specific germinal center B cells and confers protection against SARS-CoV-2 infection in mice. Front Immunol 13:604. https://doi.org/10.3389/FIMMU.2022.844837/BIBTEX
doi: 10.3389/FIMMU.2022.844837/BIBTEX
Crawford KHD, Eguia R, Dingens AS, Loes AN, Malone KD, Wolf CR, Chu HY, Tortorici MA, Veesler D, Murphy M, Pettie D, King NP, Balazs AB, Bloom JD (2020) Protocol and reagents for pseudotyping lentiviral particles with SARS-CoV-2 spike protein for neutralization assays. Viruses 12:513. https://doi.org/10.3390/V12050513
doi: 10.3390/V12050513
pubmed: 32384820
pmcid: 7291041
Cutler DM, Summers LH (2020) The COVID-19 pandemic and the $16 trillion virus. JAMA 324:1495–1496. https://doi.org/10.1001/JAMA.2020.19759
doi: 10.1001/JAMA.2020.19759
pubmed: 33044484
pmcid: 7604733
Czarnota A, Anna O, Pihl AF, Prentoe J (2020) Specific antibodies induced by immunization with hepatitis B virus-like particles carrying hepatitis C virus envelope glycoprotein 2 epitopes show differential neutralization e ffi ciency. Vaccine 8:1–19. https://doi.org/10.3390/vaccines8020294
doi: 10.3390/vaccines8020294
del Carmen M-GA, Rivera-Toledo E, Echeverría O, Vázquez-Nin G, Gómez B, Bustos-Jaimes I (2016) Peptide presentation on primate erythroparvovirus 1 virus-like particles: in vitro assembly, stability and immunological properties. Virus Res 224:12–18. https://doi.org/10.1016/j.virusres.2016.08.007
doi: 10.1016/j.virusres.2016.08.007
Donaldson B, Lateef Z, Walker GF, Young SL, Ward VK (2018) Virus-like particle vaccines: immunology and formulation for clinical translation. Expert Rev Vaccines 17:833–849. https://doi.org/10.1080/14760584.2018.1516552
doi: 10.1080/14760584.2018.1516552
pubmed: 30173619
pmcid: 7103734
Etzion O, Novack V, Perl Y, Abel O, Schwartz D, Munteanu D, Abufreha N, Ben-Yaakov G, Maoz ED, Moshaklo A, Dizingf V, Fich A (2016) Sci-B-VacTM Vs ENGERIX-B vaccines for hepatitis B virus in patients with inflammatory bowel diseases: a randomised controlled trial. J Crohns Colitis 10:905. https://doi.org/10.1093/ECCO-JCC/JJW046
doi: 10.1093/ECCO-JCC/JJW046
pubmed: 26928962
pmcid: 5007589
Fluckiger AC, Ontsouka B, Bozic J, Diress A, Ahmed T, Berthoud T, Tran A, Duque D, Liao M, McCluskie M, Diaz-Mitoma F, Anderson DE, Soare C (2021) An enveloped virus-like particle vaccine expressing a stabilized prefusion form of the SARS-CoV-2 spike protein elicits highly potent immunity. Vaccine 39:4988–5001. https://doi.org/10.1016/J.VACCINE.2021.07.034
doi: 10.1016/J.VACCINE.2021.07.034
pubmed: 34304928
pmcid: 8282453
Fontana D, Kratje R, Etcheverrigaray M, Prieto C (2014) Rabies virus-like particles expressed in HEK293 cells. Vaccine 32:2799–2804. https://doi.org/10.1016/j.vaccine.2014.02.031
doi: 10.1016/j.vaccine.2014.02.031
pubmed: 24631077
Fontana D, Kratje R, Etcheverrigaray M, Prieto C (2015a) Immunogenic virus-like particles continuously expressed in mammalian cells as a veterinary rabies vaccine candidate. Vaccine 33:4238–4246. https://doi.org/10.1016/j.vaccine.2015.03.088
doi: 10.1016/j.vaccine.2015.03.088
pubmed: 25869890
Fontana D, Kratje R, Etcheverrigaray M, Prieto C (2015b) Immunogenic virus-like particles continuously expressed in mammalian cells as a veterinary rabies vaccine candidate. Vaccine 33:4238–4246. https://doi.org/10.1016/J.VACCINE.2015.03.088
doi: 10.1016/J.VACCINE.2015.03.088
pubmed: 25869890
Fontana D, Etcheverrigaray M, Kratje R, Prieto C (2016) Development of rabies virus-like particles for vaccine applications: production, characterization, and protection studies. Methods Mol Biol 1403:155–166. https://doi.org/10.1007/978-1-4939-3387-7_7
doi: 10.1007/978-1-4939-3387-7_7
pubmed: 27076129
Fontana D, Marsili F, Garay E, Battagliotti J, Etcheverrigaray M, Kratje R, Prieto C (2019) A simplified roller bottle platform for the production of a new generation VLPs rabies vaccine for veterinary applications. Comp Immunol Microbiol Infect Dis 65:70–75. https://doi.org/10.1016/j.cimid.2019.04.009
doi: 10.1016/j.cimid.2019.04.009
pubmed: 31300130
Fontana D, Marsili F, Etcheverrigaray M, Kratje R, Prieto C (2020) Rabies VLPs adjuvanted with saponin-based liposomes induce enhanced immunogenicity mediated by neutralizing antibodies in cattle , dogs and cats. J Virol Methods 286:113966. https://doi.org/10.1016/j.jviromet.2020.113966
doi: 10.1016/j.jviromet.2020.113966
pubmed: 32905818
Fontana D, Garay E, Cervera L, Kratje R, Prieto C (2021a) Chimeric VLPs based on HIV-1 Gag and a fusion rabies glycoprotein induce specific antibodies against rabies and foot-and-mouth disease virus. Vaccines 9(3):251. https://doi.org/10.3390/vaccines9030251
doi: 10.3390/vaccines9030251
pubmed: 33809060
pmcid: 7999769
Fontana D, Garay E, Cevera L, Kratje R, Prieto C, Gòdia F (2021b) Chimeric vlps based on hiv-1 gag and a fusion rabies glycoprotein induce specific antibodies against rabies and foot-and-mouth disease virus. Vaccines 9:251. https://doi.org/10.3390/vaccines9030251
doi: 10.3390/vaccines9030251
pubmed: 33809060
pmcid: 7999769
Garay E, Fontana D, Leschiutta L, Kratje R, Prieto C (2022) Rational design of novel fusion rabies glycoproteins displaying a major antigenic site of foot-and-mouth disease virus for vaccine applications. Appl Microbiol Biotechnol 106:579–592. https://doi.org/10.1007/s00253-021-11747-4
doi: 10.1007/s00253-021-11747-4
pubmed: 34971413
Garçon N, Vaughn DW, Didierlaurent AM (2012) Development and evaluation of AS03, an adjuvant system containing α-tocopherol and squalene in an oil-in-water emulsion. Expert Rev Vaccines 11:349–366. https://doi.org/10.1586/ERV.11.192
doi: 10.1586/ERV.11.192
pubmed: 22380826
Gutiérrez-Granados S, Cervera L, Gòdia F, Segura MM (2013) Characterization and quantitation of fluorescent Gag virus-like particles. BMC Proc 7:P62. https://doi.org/10.1186/1753-6561-7-S6-P62
doi: 10.1186/1753-6561-7-S6-P62
pmcid: 3980646
Hager KJ, Marc GP, Gobeil P, Diaz RS, Heizer G, Llapur C, Makarkov AI, Vasconcellos E, Pillet S, Riera F, Saxena P, Wolff PG, Bhutada K, Wallace G, Aazami H, Jones CE, Polack FP, Ferrara L, Atkins J et al (2022) Efficacy and safety of a recombinant plant-based adjuvanted Covid-19 vaccine. N Engl J Med 386:2084–2096. https://doi.org/10.1056/NEJMOA2201300
doi: 10.1056/NEJMOA2201300
pubmed: 35507508
Heath PT, Galiza EP, Baxter DN, Boffito M, Browne D, Burns F, Chadwick DR, Clark R, Cosgrove C, Galloway J, Goodman AL, Heer A, Higham A, Iyengar S, Jamal A, Jeanes C, Kalra PA, Kyriakidou C, McAuley DF et al (2021) Safety and efficacy of NVX-CoV2373 Covid-19 vaccine. N Engl J Med 385:1172–1183. https://doi.org/10.1056/NEJMOA2107659/SUPPL_FILE/NEJMOA2107659_DATA-SHARING.PDF
doi: 10.1056/NEJMOA2107659/SUPPL_FILE/NEJMOA2107659_DATA-SHARING.PDF
pubmed: 34192426
Hennrich AA, Sawatsky B, Santos-Mandujano R, Banda DH, Oberhuber M, Schopf A, Pfaffinger V, Wittwer K, Riedel C, Pfaller CK, Conzelmann KK (2021) Safe and effective two-in-one replicon-and-VLP minispike vaccine for COVID-19: protection of mice after a single immunization. PLoS Pathog 17:1–25. https://doi.org/10.1371/journal.ppat.1009064
doi: 10.1371/journal.ppat.1009064
Hung IFN, Poland GA (2021) Single-dose Oxford–AstraZeneca COVID-19 vaccine followed by a 12-week booster. Lancet 397:854. https://doi.org/10.1016/S0140-6736(21)00528-6
doi: 10.1016/S0140-6736(21)00528-6
pubmed: 33676614
pmcid: 8086170
Jaron M, Lehky M, Zarà M, Zaydowicz CN, Lak A, Ballmann R, Heine PA, Wenzel EV, Schneider KT, Bertoglio F, Kempter S, Köster RW, Barbieri SS, van den Heuvel J, Hust M, Dübel S, Schubert M (2022) Baculovirus-Free SARS-CoV-2 virus-like particle production in insect cells for rapid neutralization assessment. Viruses 14:2087. https://doi.org/10.3390/V14102087/S1
doi: 10.3390/V14102087/S1
pubmed: 36298643
pmcid: 9606917
Larson ME, Sherman MA, Greimel S, Kuskowski M, Schneider A, Bennett DA, Lesné SE (2006) Rabies virus glycoprotein as a carrier for anthrax protective antigen. Virology 32:10253–10266. https://doi.org/10.1523/JNEUROSCI.0581-12.2012.Soluble
doi: 10.1523/JNEUROSCI.0581-12.2012.Soluble
Laurens MB (2020) RTS,S/AS01 vaccine (Mosquirix
doi: 10.1080/21645515.2019.1669415
pubmed: 31545128
Lavado-García J, Cervera L, Gòdia F (2020) An alternative perfusion approach for the intensification of virus-like particle production in HEK293 cultures. Front Bioeng Biotechnol 8:617. https://doi.org/10.3389/FBIOE.2020.00617
doi: 10.3389/FBIOE.2020.00617
pubmed: 32637402
pmcid: 7318772
Liu X, Fang Y, Zhou P, Lu Y, Zhang Q, Xiao S, Dong Z, Pan L, Lv J, Zhang Z, Zhang Y, Wang Y (2017) Chimeric virus-like particles elicit protective immunity against serotype O foot-and-mouth disease virus in guinea pigs. Appl Microbiol Biotechnol 101(12):4905–4914. https://doi.org/10.1007/s00253-017-8246-0
doi: 10.1007/s00253-017-8246-0
pubmed: 28365796
Loubet P, Laureillard D, Martin A, Larcher R, Sotto A (2021) Why promoting a COVID-19 vaccine booster dose? Anaesth Crit Care Pain Med 40:100967. https://doi.org/10.1016/J.ACCPM.2021.100967
doi: 10.1016/J.ACCPM.2021.100967
pubmed: 34924154
pmcid: 8675238
Lua LHL, Connors NK, Sainsbury F, Chuan YP, Wibowo N, Middelberg APJ (2014) Bioengineering virus-like particles as vaccines. Biotechnol Bioeng 111:425–440. https://doi.org/10.1002/bit.25159
doi: 10.1002/bit.25159
pubmed: 24347238
Mareze VA, Borio CS, Bilen MF, Fleith R, Mirazo S, Mansur DS, Arbiza J, Lozano ME, Bruña-Romero O (2016) Tests in mice of a dengue vaccine candidate made of chimeric Junin virus-like particles and conserved dengue virus envelope sequences. Appl Microbiol Biotechnol 100:125–133. https://doi.org/10.1007/s00253-015-6973-7
doi: 10.1007/s00253-015-6973-7
pubmed: 26386688
Menter T, Haslbauer JD, Nienhold R, Savic S, Hopfer H, Deigendesch N, Frank S, Turek D, Willi N, Pargger H, Bassetti S, Leuppi JD, Cathomas G, Tolnay M, Mertz KD, Tzankov A (2020) Postmortem examination of COVID-19 patients reveals diffuse alveolar damage with severe capillary congestion and variegated findings in lungs and other organs suggesting vascular dysfunction. Histopathology 77:198–209. https://doi.org/10.1111/HIS.14134
doi: 10.1111/HIS.14134
pubmed: 32364264
pmcid: 7496150
Mohsen MO, Zha L, Cabral-Miranda G, Bachmann MF (2017) Major findings and recent advances in virus–like particle (VLP)-based vaccines. Semin Immunol 34:123–132. https://doi.org/10.1016/j.smim.2017.08.014
doi: 10.1016/j.smim.2017.08.014
pubmed: 28887001
Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Pérez Marc G, Moreira ED, Zerbini C, Bailey R, Swanson KA, Roychoudhury S, Koury K, Li P, Kalina WV, Cooper D, Frenck RW, Hammitt LL et al (2020) Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med 383:2603–2615. https://doi.org/10.1056/NEJMOA2034577/SUPPL_FILE/NEJMOA2034577_PROTOCOL.PDF
doi: 10.1056/NEJMOA2034577/SUPPL_FILE/NEJMOA2034577_PROTOCOL.PDF
pubmed: 33301246
Prieto C, Fontana D, Etcheverrigaray M, Kratje R (2011) A strategy to obtain recombinant cell lines with high expression levels. Lentiviral vector-mediated transgenesis. BMC Proc 5(Suppl 8):P7. https://doi.org/10.1186/1753-6561-5-S8-P7
doi: 10.1186/1753-6561-5-S8-P7
pubmed: 22373510
pmcid: 3284990
Rothen DA, Krenger PS, Nonic A, Balke I, Vogt ACS, Chang X, Manenti A, Vedovi F, Resevica G, Walton SM, Zeltins A, Montomoli E, Vogel M, Bachmann MF, Mohsen MO (2022) Intranasal administration of a VLP-based vaccine induces neutralizing antibodies against SARS-CoV-2 and variants of concern. Allergy 77:2446–2458. https://doi.org/10.1111/ALL.15311
doi: 10.1111/ALL.15311
pubmed: 35403221
Sadoff J, Le Gars M, Shukarev G, Heerwegh D, Truyers C, de Groot AM, Stoop J, Tete S, Van Damme W, Leroux-Roels I, Berghmans P-J, Kimmel M, Van Damme P, de Hoon J, Smith W, Stephenson KE, De Rosa SC, Cohen KW, McElrath MJ et al (2021) Interim results of a phase 1–2a trial of Ad26.COV2.S Covid-19 vaccine. N Engl J Med 384:1824–1835. https://doi.org/10.1056/NEJMOA2034201/SUPPL_FILE/NEJMOA2034201_DATA-SHARING.PDF
doi: 10.1056/NEJMOA2034201/SUPPL_FILE/NEJMOA2034201_DATA-SHARING.PDF
pubmed: 33440088
Schiller JT, Castellsagué X, Garland SM (2012) A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 30:F123. https://doi.org/10.1016/J.VACCINE.2012.04.108
doi: 10.1016/J.VACCINE.2012.04.108
pubmed: 23199956
pmcid: 4636904
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
doi: 10.1038/nmeth.2019
pubmed: 22743772
Stalls V, Janowska K, Acharya P (2022) Transient transfection and purification of SARS-CoV-2 spike protein from mammalian cells. STAR Protoc 3:101603. https://doi.org/10.1016/J.XPRO.2022.101603
doi: 10.1016/J.XPRO.2022.101603
pubmed: 35983170
pmcid: 9283606
Swann H, Sharma A, Preece B, Peterson A, Eldridge C, Belnap DM, Vershinin M (2020) Saffarian S (2020) Minimal system for assembly of SARS-CoV-2 virus like particles. Sci Rep 101(10):1–5. https://doi.org/10.1038/s41598-020-78656-w
doi: 10.1038/s41598-020-78656-w
Tai W, He L, Zhang X, Pu J, Voronin D, Jiang S, Zhou Y, Du L (2020) Characterization of the receptor-binding domain (RBD) of 2019 novel coronavirus: implication for development of RBD protein as a viral attachment inhibitor and vaccine. Cell Mol Immunol 17(6):613–620. https://doi.org/10.1038/s41423-020-0400-4
doi: 10.1038/s41423-020-0400-4
pubmed: 32203189
pmcid: 7091888
Tanriover MD, Doğanay HL, Akova M, Güner HR, Azap A, Akhan S, Köse Ş, Erdinç FŞ, Akalın EH, Tabak ÖF, Pullukçu H, Batum Ö, Şimşek Yavuz S, Turhan Ö, Yıldırmak MT, Köksal İ, Taşova Y, Korten V, Yılmaz G et al (2021) Efficacy and safety of an inactivated whole-virion SARS-CoV-2 vaccine (CoronaVac): interim results of a double-blind, randomised, placebo-controlled, phase 3 trial in Turkey. Lancet (London, England) 398:213–222. https://doi.org/10.1016/S0140-6736(21)01429-X
doi: 10.1016/S0140-6736(21)01429-X
pubmed: 34246358
Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel A, Mehra MR, Scholkmann F, Schüpbach R, Ruschitzka F, Moch H (2020) Electron microscopy of SARS-CoV-2: a challenging task – Authors’ reply. Lancet 395:e100. https://doi.org/10.1016/S0140-6736(20)31185-5
doi: 10.1016/S0140-6736(20)31185-5
pubmed: 32442527
pmcid: 7237177
Venereo-Sanchez A, Gilbert R, Simoneau M, Caron A, Chahal P, Chen W, Ansorge S, Li X, Henry O, Kamen A (2016) Hemagglutinin and neuraminidase containing virus-like particles produced in HEK-293 suspension culture: an effective influenza vaccine candidate. Vaccine 34:3371–3380. https://doi.org/10.1016/j.vaccine.2016.04.089
doi: 10.1016/j.vaccine.2016.04.089
pubmed: 27155499
Venereo-Sánchez A, Fulton K, Koczka K, Twine S, Chahal P, Ansorge S, Gilbert R, Henry O, Kamen A (2019) Characterization of influenza H1N1 Gag virus-like particles and extracellular vesicles co-produced in HEK-293SF. Vaccine 37:7100–7107. https://doi.org/10.1016/j.vaccine.2019.07.057
doi: 10.1016/j.vaccine.2019.07.057
pubmed: 31358407
Voysey M, Clemens SAC, Madhi SA, Weckx LY, Folegatti PM, Aley PK, Angus B, Baillie VL, Barnabas SL, Bhorat QE, Bibi S, Briner C, Cicconi P, Collins AM, Colin-Jones R, Cutland CL, Darton TC, Dheda K, Duncan CJA et al (2021) Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: an interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet 397:99–111. https://doi.org/10.1016/S0140-6736(20)32661-1
doi: 10.1016/S0140-6736(20)32661-1
pubmed: 33306989
pmcid: 7723445
Walls AC, Park Y, Tortorici MA, Wall A, McGuire AT, Veesler D (2020) Structure, function, and antigenicity of the SARS- CoV-2 spike glycoprotein. Cell 180:281–292
doi: 10.1016/j.cell.2020.02.058
Watson OJ, Barnsley G, Toor J, Hogan AB, Winskill P, Ghani AC (2022) Global impact of the first year of COVID-19 vaccination: a mathematical modelling study. Lancet Infect Dis 22(9):1293–1302. https://doi.org/10.1016/s1473-3099(22)00320-6
doi: 10.1016/s1473-3099(22)00320-6
pubmed: 35753318
pmcid: 9225255
Xia S, Zhang Y, Wang Y, Wang H, Yang Y, Gao GF, Tan W, Wu G, Xu M, Lou Z, Huang W, Xu W, Huang B, Wang H, Wang W, Zhang W, Li N, Xie Z, Ding L et al (2021) Safety and immunogenicity of an inactivated SARS-CoV-2 vaccine, BBIBP-CorV: a randomised, double-blind, placebo-controlled, phase 1/2 trial. Lancet Infect Dis 21:39–51. https://doi.org/10.1016/S1473-3099(20)30831-8
doi: 10.1016/S1473-3099(20)30831-8
pubmed: 33069281
Xu L, He D, Yang L, Li Z, Ye X, Yu H, Zhao H, Li S, Yuan L, Qian H, Que Y, Kuo Shih JW, Zhu H, Li Y, Cheng T, Xia N (2015) A broadly cross-protective vaccine presenting the neighboring epitopes within the VP1 GH loop and VP2 EF loop of Enterovirus 71. Sci Rep 5:12973. https://doi.org/10.1038/srep12973
doi: 10.1038/srep12973
pubmed: 26243660
pmcid: 4525384
Xu R, Shi M, Li J, Song P, Li N (2020) Construction of SARS-CoV-2 virus-like particles by mammalian expression system. Front Bioeng Biotechnol 8:862. https://doi.org/10.3389/fbioe.2020.00862
doi: 10.3389/fbioe.2020.00862
pubmed: 32850726
pmcid: 7409377
Yi C, Sun X, Ye J, Ding L, Liu M, Yang Z, Lu X, Zhang Y, Ma L, Gu W, Qu A, Xu J, Shi Z, Ling Z (2020) Sun B (2020) Key residues of the receptor binding motif in the spike protein of SARS-CoV-2 that interact with ACE2 and neutralizing antibodies. Cell Mol Immunol 176(17):621–630. https://doi.org/10.1038/s41423-020-0458-z
doi: 10.1038/s41423-020-0458-z