Structure-based design of oligomeric receptor-binding domain (RBD) recombinant proteins as potent vaccine candidates against SARS-CoV-2

References

• Muik A, Wallisch AK, Sänger B, Swanson KA, Mühl J, Chen W, Cai H, Maurus D, Sarkar R, Türeci Ö, et al. Neutralization of SARS-CoV-2 lineage B.1.1.7 pseudovirus by BNT162b2 vaccine–elicited human sera. Science. 2021;371(6534): 1152–9. doi:10.1126/science.abg6105.
   PubMed Web of Science ®Google Scholar
• Dai L, Gao L, Tao L, Hadinegoro SR, Erkin M, Ying Z, He P, Girsang RT, Vergara H, Akram J, et al. Efficacy and safety of the RBD-Dimer–based Covid-19 vaccine ZF2001 in adults. N Engl J Med. 2022;386(22): 2097–111. doi:10.1056/NEJMoa2202261.
   PubMed Web of Science ®Google Scholar
• Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, Wang W, Song H, Huang B, Zhu N, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020;395(10224): 565–74. doi:10.1016/S0140-6736(20)30251-8.
   PubMed Web of Science ®Google Scholar
• Wang Q, Zhang Y, Wu L, Niu S, Song C, Zhang Z, Lu G, Qiao C, Hu Y, Yuen KY, et al. Structural and functional basis of SARS-CoV-2 entry by using human ACE2. Cell. 2020;181(4): 894–904.e9. doi:10.1016/j.cell.2020.03.045.
   PubMed Web of Science ®Google Scholar
• Lan J, Ge J, Yu J, Shan S, Zhou H, Fan S, Zhang Q, Shi X, Wang Q, Zhang L, et al. Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature. 2020;581(7807): 215–20. doi:10.1038/s41586-020-2180-5.
   PubMed Web of Science ®Google Scholar
• Wrapp D, Wang N, Corbett KS, Goldsmith JA, Hsieh CL, Abiona O, Graham BS, McLellan JS. Cryo-EM structure of the 2019-nCov spike in the prefusion conformation. Science. ( 1979) 2020;367(6483):1260–63. doi:10.1126/science.abb2507.
   PubMed Web of Science ®Google Scholar
• Cao Y, Su B, Guo X, Sun W, Deng Y, Bao L, Zhu Q, Zhang X, Zheng Y, Geng C, et al. Potent neutralizing antibodies against SARS-CoV-2 identified by high-throughput single-cell sequencing of convalescent patients’ B Cells. Cell. 2020;182(1): 1–12. doi:10.1016/j.cell.2020.05.025.
   PubMed Web of Science ®Google Scholar
• Yuan M, Wu NC, Zhu X, Lee CCD, So RTY, Lv H, Mok CKP, Wilson IA. A highly conserved cryptic epitope in the receptor binding domains of SARS-CoV-2 and SARS-CoV. Science. ( 1979) 2020;368(6491):630–33. doi:10.1126/science.abb7269.
   PubMed Web of Science ®Google Scholar
• Jiang S, Hillyer C, Du L. Neutralizing antibodies against SARS-CoV-2 and other human coronaviruses. Trends Immunol. 2020;41(5):355–59. doi:10.1016/j.it.2020.03.007.
   PubMed Web of Science ®Google Scholar
• Hsieh C-L, Goldsmith JA, Schaub JM, DiVenere AM, Kuo H-C, Javanmardi K, Le KC, Wrapp D, Lee AG, Liu Y, et al. Structure-based design of prefusion-stabilized SARS-CoV-2 spikes. Science. 2020;369(6510): 1501–05. doi:10.1126/science.abd0826.
   PubMed Web of Science ®Google Scholar
• Wang MY, Zhao R, Gao LJ, Gao XF, Wang DP, Cao JM. SARS-CoV-2: structure, biology, and structure-based therapeutics development. Front Cell Infect Microbiol. 2020;10. doi:10.3389/fcimb.2020.587269.
   Web of Science ®Google Scholar
• Shang J, Wan Y, Luo C, Ye G, Geng Q, Auerbach A, Li F. Cell entry mechanisms of SARS-CoV-2. Proc Nat Acad Sci. 2020;117(21):11727–34. doi:10.1073/pnas.2003138117.
   PubMed Web of Science ®Google Scholar
• Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2): 271–80.e8. doi:10.1016/j.cell.2020.02.052.
   PubMed Web of Science ®Google Scholar
• Pallesen J, Wang N, Corbett KS, Wrapp D, Kirchdoerfer RN, Turner HL, Cottrell CA, Becker MM, Wang L, Shi W, et al. Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc Natl Acad Sci U S A. 2017;114(35): E7348–57. doi:10.1073/pnas.1707304114.
   PubMed Web of Science ®Google Scholar
• Tian JH, Patel N, Haupt R, Zhou H, Weston S, Hammond H, Logue J, Portnoff AD, Norton J, Guebre-Xabier M, et al. SARS-CoV-2 spike glycoprotein vaccine candidate NVX-CoV2373 immunogenicity in baboons and protection in mice. Nat Commun. 2021;12(1). doi:10.1038/s41467-020-20653-8.
   Web of Science ®Google Scholar
• Guebre-Xabier M, Patel N, Tian JH, Zhou B, Maciejewski S, Lam K, Portnoff AD, Massare MJ, Frieman MB, Piedra PA, et al. NVX-CoV2373 vaccine protects cynomolgus macaque upper and lower airways against SARS-CoV-2 challenge. Vaccine. 2020;38(50): 7892–96. doi:10.1016/j.vaccine.2020.10.064.
   PubMed Web of Science ®Google Scholar
• Keech C, Albert G, Cho I, Robertson A, Reed P, Neal S, Plested JS, Zhu M, Cloney-Clark S, Zhou H, et al. Phase 1–2 Trial of a SARS-CoV-2 recombinant spike protein nanoparticle vaccine. N Engl J Med. 2020;383(24): 2320–32. doi:10.1056/NEJMoa2026920.
   PubMed Web of Science ®Google Scholar
• V’kovski P, Kratzel A, Steiner S, Stalder H, Thiel V. Coronavirus biology and replication: implications for SARS-CoV-2. Nat Rev Microbiol. 2021;19(3):155–70. doi:10.1038/s41579-020-00468-6.
   PubMed Web of Science ®Google Scholar
• Yang J, Wang W, Chen Z, Lu S, Yang F, Bi Z, Bao L, Mo F, Li X, Huang Y, et al. A vaccine targeting the RBD of the S protein of SARS-CoV-2 induces protective immunity. Nature. 2020;586(7830): 572–77. doi:10.1038/s41586-020-2599-8.
   PubMed Web of Science ®Google Scholar
• Malladi SK, Singh R, Pandey S, Gayathri S, Kanjo K, Ahmed S, Khan MS, Kalita P, Girish N, Upadhyaya A, et al. Design of a highly thermotolerant, immunogenic SARS-CoV-2 spike fragment. J Biol Chem. 2021;296:100025. doi:10.1074/jbc.RA120.016284.
   PubMed Web of Science ®Google Scholar
• Pollet J, Chen WH, Versteeg L, Keegan B, Zhan B, Wei J, Liu Z, Lee J, Kundu R, Adhikari R, et al. SARS‑CoV-2 RBD219-N1C1: a yeast-expressed SARS-CoV-2 recombinant receptor-binding domain candidate vaccine stimulates virus neutralizing antibodies and T-cell immunity in mice. Hum Vaccin Immunother. 2021;17(8): 2356–66. doi:10.1080/21645515.2021.1901545.
   PubMed Web of Science ®Google Scholar
• Pino M, Abid T, Pereira Ribeiro S, Edara VV, Floyd K, Smith JC, Latif MB, Pacheco-Sanchez G, Dutta D, Wang S, et al. A yeast-expressed RBD-based SARS-CoV-2 vaccine formulated with 3M-052-alum adjuvant promotes protective efficacy in non-human primates. Sci Immunol. 2021;6(61). doi:10.1126/sciimmunol.abh3634.
   PubMed Web of Science ®Google Scholar
• Thuluva S, Paradkar V, Gunneri SR, Yerroju V, Mogulla R, Turaga K, Kyasani M, Manoharan SK, Medigeshi G, Singh J, et al. Evaluation of safety and immunogenicity of receptor-binding domain-based COVID-19 vaccine (Corbevax) to select the optimum formulation in open-label, multicentre, and randomised phase-1/2 and phase-2 clinical trials. EBioMedicine. 2022;83:104217. doi:10.1016/j.ebiom.2022.104217.
   PubMed Web of Science ®Google Scholar
• Thuluva S, Paradkar V, Gunneri S, Yerroju V, Mogulla RR, Suneetha PV, Turaga K, Kyasani M, Manoharan SK, Adabala S, et al. Safety, tolerability and immunogenicity of biological E’s CORBEVAX™ vaccine in children and adolescents: a prospective, randomised, double-blind, placebo controlled, phase-2/3 study. Vaccine. 2022;40(49): 7130–40. doi:10.1016/j.vaccine.2022.10.045.
   PubMed Web of Science ®Google Scholar
• Dai L, Zheng T, Xu K, Han Y, Xu L, Huang E, An Y, Cheng Y, Li S, Liu M, et al. A universal design of betacoronavirus vaccines against COVID-19, MERS, and SARS. Cell. 2020;182(3): 722–33.e11. doi:10.1016/j.cell.2020.06.035.
   PubMed Web of Science ®Google Scholar
• Sun S, Cai Y, Song TZ, Pu Y, Cheng L, Xu H, Sun J, Meng C, Lin Y, Huang H, et al. Interferon-armed RBD dimer enhances the immunogenicity of RBD for sterilizing immunity against SARS-CoV-2. Cell Res. 2021;31(9): 1011–23. doi:10.1038/s41422-021-00531-8.
   PubMed Web of Science ®Google Scholar
• Liu Z, Xu W, Xia S, Gu C, Wang X, Wang Q, Zhou J, Wu Y, Cai X, Qu D, et al. RBD-Fc-based COVID-19 vaccine candidate induces highly potent SARS-CoV-2 neutralizing antibody response. Signal Transduct Target Ther. 2020;5(1): 282. doi:10.1038/s41392-020-00402-5.
   PubMed Web of Science ®Google Scholar
• Malladi SK, Patel UR, Rajmani RS, Singh R, Pandey S, Kumar S, Khaleeq S, van Vuren PJ, Riddell S, Goldie S, et al. Immunogenicity and protective efficacy of a highly thermotolerant, trimeric SARS-CoV-2 receptor binding domain derivative. ACS Infect Dis. 2021;7(8): 2546–64. doi:10.1021/acsinfecdis.1c00276.
   PubMed Web of Science ®Google Scholar
• Zhang T, Wang Z, Xu X. Impact of glycosylation and length of RBD of SARS-CoV-2 S protein on the immunogenicity of RBD protein vaccines. Basic Clin Med. 2020;40:1645–50.
   Google Scholar
• Routhu NK, Cheedarla N, Bollimpelli VS, Gangadhara S, Edara VV, Lai L, Sahoo A, Shiferaw A, Styles TM, Floyd K, et al. SARS-CoV-2 RBD trimer protein adjuvanted with Alum-3M-052 protects from SARS-CoV-2 infection and immune pathology in the lung. Nat Commun. 2021;12(1): 3587. doi:10.1038/s41467-021-23942-y.
   PubMed Web of Science ®Google Scholar
• Kang YF, Sun C, Zhuang Z, Yuan RY, Zheng Q, Li JP, Zhou PP, Chen XC, Liu Z, Zhang X, et al. Rapid development of SARS-CoV-2 spike protein receptor-binding domain self-assembled nanoparticle vaccine candidates. ACS Nano. 2021;15(2): 2738–52. doi:10.1021/acsnano.0c08379.
   PubMed Web of Science ®Google Scholar
• Walls AC, Fiala B, Schäfer A, Wrenn S, Pham MN, Murphy M, Tse L, Shehata L, O’connor MA, Chen C, et al. Elicitation of potent neutralizing antibody responses by designed protein nanoparticle vaccines for SARS-CoV-2. Cell. 2020;183(5): 1367–82.e17. doi:10.1016/j.cell.2020.10.043.
   PubMed Web of Science ®Google Scholar
• Arunachalam PS, Feng Y, Ashraf U, Hu M, Walls AC, Edara VV, Zarnitsyna VI, Aye PP, Golden N, Miranda MC, et al. Durable protection against the SARS-CoV-2 Omicron variant is induced by an adjuvanted subunit vaccine. Sci Transl Med. 2022;14(658): 4130. doi:10.1126/scitranslmed.abq4130.
   Web of Science ®Google Scholar
• Arunachalam PS, Walls AC, Golden N, Atyeo C, Fischinger S, Li C, Aye P, Navarro MJ, Lai L, Edara VV, et al. Adjuvanting a subunit COVID-19 vaccine to induce protective immunity. Nature. 2021;594(7862): 253–58. doi:10.1038/s41586-021-03530-2.
   PubMed Web of Science ®Google Scholar
• Nie J, Li Q, Wu J, Zhao C, Hao H, Liu H, Zhang L, Nie L, Qin H, Wang M, et al. Establishment and validation of a pseudovirus neutralization assay for SARS-CoV-2. Emerg Microbes Infect. 2020;9(1): 680–86. doi:10.1080/22221751.2020.1743767.
   PubMed Web of Science ®Google Scholar
• Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M. ColabFold: making protein folding accessible to all. Nat Methods. 2022;19(6):679–82. doi:10.1038/s41592-022-01488-1.
   PubMed Web of Science ®Google Scholar
• Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873): 583–89. doi:10.1038/s41586-021-03819-2.
   PubMed Web of Science ®Google Scholar
• Du L, Zhao G, Chan CCS, Sun S, Chen M, Liu Z, Guo H, He Y, Zhou Y, Zheng BJ, et al. Recombinant receptor-binding domain of SARS-CoV spike protein expressed in mammalian, insect and E. coli cells elicits potent neutralizing antibody and protective immunity. Virology. 2009;393(1): 144–50. doi:10.1016/j.virol.2009.07.018.
   PubMed Web of Science ®Google Scholar
• Harbury PB, Zhang T, Kim PS, Alber T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science. ( 1979) 1993;262(5138):1401–07. doi:10.1126/science.8248779.
   PubMed Web of Science ®Google Scholar
• Pooladanda V, Thatikonda S, Godugu C. The current understanding and potential therapeutic options to combat COVID-19. Life Sci. 2020;254:117765. doi:10.1016/j.lfs.2020.117765.
   PubMed Web of Science ®Google Scholar
• Shen C, Wang Z, Zhao F, Yang Y, Li J, Yuan J, Wang F, Li D, Yang M, Xing L, et al. Treatment of 5 critically ill patients with COVID-19 with convalescent plasma. JAMA. 2020;323(16): 1582–89. doi:10.1001/jama.2020.4783.
   PubMed Web of Science ®Google Scholar
• Zost SJ, Gilchuk P, Case JB, Binshtein E, Chen RE, Nkolola JP, Schäfer A, Reidy JX, Trivette A, Nargi RS, et al. Potently neutralizing and protective human antibodies against SARS-CoV-2. Nature. 2020;584:443–49.
   PubMed Web of Science ®Google Scholar
• Liang JG, Su D, Song TZ, Zeng Y, Huang W, Wu J, Xu R, Luo P, Yang X, Zhang X, et al. S-trimer, a COVID-19 subunit vaccine candidate, induces protective immunity in nonhuman primates. Nat Commun. 2021;12(1). doi:10.1038/s41467-021-21634-1.
   Web of Science ®Google Scholar
• Lucas C, Vogels CBF, Yildirim I, Rothman JE, Lu P, Monteiro V, Gehlhausen JR, Campbell M, Silva J, Tabachnikova A, et al. Impact of circulating SARS-CoV-2 variants on mRNA vaccine-induced immunity. Nature. 2021;600(7889): 523–29. doi:10.1038/s41586-021-04085-y.
   PubMed Web of Science ®Google Scholar
• Cao Y, Wang J, Jian F, Xiao T, Song W, Yisimayi A, Huang W, Li Q, Wang P, An R, et al. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature. 2022;602(7898): 657–63. doi:10.1038/s41586-021-04385-3.
   PubMed Web of Science ®Google Scholar
• Cele S, Jackson L, Khoury DS, Khan K, Moyo-Gwete T, Tegally H, San JE, Cromer D, Scheepers C, Amoako DG, et al. Omicron extensively but incompletely escapes Pfizer BNT162b2 neutralization. Nature. 2022;602(7898): 654–56. doi:10.1038/s41586-021-04387-1.
   PubMed Web of Science ®Google Scholar
• Wang K, Jia Z, Bao L, Wang L, Cao L, Chi H, Hu Y, Li Q, Zhou Y, Jiang Y, et al. Memory B cell repertoire from triple vaccinees against diverse SARS-CoV-2 variants. Nature. 2022;603(7903): 919–25. doi:10.1038/s41586-022-04466-x.
   PubMed Web of Science ®Google Scholar
• He C, He X, Yang J, Lei H, Hong W, Song X, Yang L, Li J, Wang W, Shen G, et al. Spike protein of SARS‐CoV‐2 Omicron (B.1.1.529) variant have a reduced ability to induce the immune response. Signal Transduct Target Ther. 2022;7(1). doi:10.1038/s41392-022-00980-6.
   Web of Science ®Google Scholar