424
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Exploring the role of framework mutations in enabling breadth of a cross-reactive antibody (CR3022) against the SARS-CoV-2 RBD and its variants of concern

ORCID Icon, ORCID Icon, ORCID Icon, , , ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 2341-2354 | Received 11 Oct 2021, Accepted 12 Jan 2022, Published online: 31 Jan 2022

References

  • Zhao, F. (2021). Broadening a SARS-CoV-1 neutralizing antibody for potent SARS-CoV-2 neutralization through directed evolution. bioRxiv, https://doi.org/10.1101/2021.05.29.443900
  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1-2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
  • Ahamad, S., Hema, K., & Gupta, D. (2021). Structural stability predictions and molecular dynamics simulations of RBD and HR1 mutations associated with SARS-CoV-2 spike glycoprotein. Journal of Biomolecular Structure and Dynamics, https://doi.org/10.1080/07391102.2021.1889671
  • Ahamad, S., Kanipakam, H. & Gupta, D. (2020). Insights into the structural and dynamical changes of spike glycoprotein mutations associated with SARS-CoV-2 host receptor binding. J. Biomol. Struct. Dyn, 40, 1.
  • Barnes, C. O., Jette, C. A., Abernathy, M. E., Dam, K.-M A., Esswein, S. R., Gristick, H. B., Malyutin, A. G., Sharaf, N. G., Huey-Tubman, K. E., Lee, Y. E., Robbiani, D. F., Nussenzweig, M. C., West, A. P., & Bjorkman, P. J. (2020). SARS-CoV-2 neutralizing antibody structures inform therapeutic strategies. Nature, 588(7839), 682–687. 2020 588 https://doi.org/10.1038/s41586-020-2852-1
  • Bates, T. A., Weinstein, J. B., Leier, H. C., Messer, W. B., & Tafesse, F. G. (2021). Cross-reactivity of SARS-CoV structural protein antibodies against SARS-CoV-2. Cell Rep., 34(7), 108737.
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Bonvin Lab. (2020). HADDOCK2.4 antibody - Antigen tutorial using PDB-tools webserver. https://www.bonvinlab.org/education/HADDOCK24/HADDOCK24-antibody-antigen/.
  • CDC. (2021). SARS-CoV-2 variants of concern. https://www.cdc.gov/coronavirus/2019-ncov/cases-updates/variant-surveillance/variant-info.html.
  • Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., & Richardson, D. C. (2010). MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D, Biological Crystallography, 66(Pt 1), 12–21. https://doi.org/10.1107/S0907444909042073
  • Cui, J., Li, F., & Shi, Z. L. (2019). Origin and evolution of pathogenic coronaviruses. Nature Reviews Microbiology, 17(3), 181–192. https://doi.org/10.1038/s41579-018-0118-9
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
  • Fehr, A. R., & Perlman, S. (2015). Coronaviruses: An overview of their replication and pathogenesis. In Coronaviruses: Methods and protocols (pp. 1–23). Springer. https://doi.org/10.1007/978-1-4939-2438-7_1
  • Fraley, E., LeMaster, C., Banerjee, D., Khanal, S., Selvarangan, R., & Bradley, T. (2021). Cross-reactive antibody immunity against SARS-CoV-2 in children and adults. Cellular & Molecular Immunology, 18(7), 1826–1828. 2021 18 https://doi.org/10.1038/s41423-021-00700-0
  • Greaney, A. J., Starr, T. N., Gilchuk, P., Zost, S. J., Binshtein, E., Loes, A. N., Hilton, S. K., Huddleston, J., Eguia, R., Crawford, K. H. D., Dingens, A. S., Nargi, R. S., Sutton, R. E., Suryadevara, N., Rothlauf, P. W., Liu, Z., Whelan, S. P. J., Carnahan, R. H., Crowe, J. E., & Bloom, J. D. (2021). Complete mapping of mutations to the SARS-CoV-2 spike receptor-binding domain that escape antibody recognition. Cell Host & Microbe, 29(1), 44–57.e9. https://doi.org/10.1016/j.chom.2020.11.007
  • Guex, N., & Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis, 18(15), 2714–2723. https://doi.org/10.1002/elps.1150181505
  • Heo, L., Park, H., & Seok, C. (2013). GalaxyRefine: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
  • Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., de Groot, B. L., Grubmüller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73. https://doi.org/10.1038/nmeth.4067
  • Jo, S., Kim, T., Iyer, V. G., & Im, W. (2008). CHARMM-GUI: A web-based graphical user interface for CHARMM. Journal of Computational Chemistry, 29(11), 1859–1865.
  • Johnson, C. R., Yu, W., & Murtaugh, M. P. (2007). Cross-reactive antibody responses to nsp1 and nsp2 of porcine reproductive and respiratory syndrome virus. The Journal of General Virology, 88(Pt 4), 1184–1195. https://doi.org/10.1099/vir.0.82587-0
  • Klein, F., Diskin, R., Scheid, J. F., Gaebler, C., Mouquet, H., Georgiev, I. S., Pancera, M., Zhou, T., Incesu, R.-B., Fu, B. Z., Gnanapragasam, P. N. P., Oliveira, T. Y., Seaman, M. S., Kwong, P. D., Bjorkman, P. J., & Nussenzweig, M. C. (2013). Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell, 153(1), 126–138. https://doi.org/10.1016/j.cell.2013.03.018
  • Krawczyk, K., Liu, X., Baker, T., Shi, J., & Deane, C. M. (2014). Improving B-cell epitope prediction and its application to global antibody-antigen docking. Bioinformatics (Oxford, England), 30(16), 2288–2294. https://doi.org/10.1093/bioinformatics/btu190
  • Letunic, I., & Bork, P. (2021). Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49(W1), W293–W296. https://doi.org/10.1093/nar/gkab301
  • Liberis, E., Veličković, P., Sormanni, P., Vendruscolo, M., & Liò, P. (2018). Parapred: Antibody paratope prediction using convolutional and recurrent neural networks. Bioinformatics (Oxford, England), 34(17), 2944–2950. https://doi.org/10.1093/bioinformatics/bty305
  • Masters, P. S. (2006). The Molecular Biology of Coronaviruses. Advances in Virus Research, 65, 193–292.
  • Meireles, L. M. C., D�Mling, A. S., & Camacho, C. J. (2010). ANCHOR: A web server and database for analysis of protein-protein interaction binding pockets for drug discovery. Nucleic Acids Research, 38(Web Server issue), W407–W411. https://doi.org/10.1093/nar/gkq502
  • Meyers, L. M., Gutiérrez, A. H., Boyle, C. M., Terry, F., McGonnigal, B. G., Salazar, A., Princiotta, M. F., Martin, W. D., De Groot, A. S., & Moise, L. (2021). Highly conserved, non-human-like, and cross-reactive SARS-CoV-2 T cell epitopes for COVID-19 vaccine design and validation. Npj Vaccines, 6(1), 1–14. https://doi.org/10.1038/s41541-021-00331-6
  • Mortola, E., & Roy, P. (2004). Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Letters, 576(1–2), 174–178. https://doi.org/10.1016/j.febslet.2004.09.009
  • Narayanan, K., Ramirez, S. I., Lokugamage, K. G., & Makino, S. (2015). Coronavirus nonstructural protein 1: Common and distinct functions in the regulation of host and viral gene expression. Virus Research, 202, 89–100. https://doi.org/10.1016/j.virusres.2014.11.019
  • Nelson-Sathi, S., P. K. Umasankar, E. Sreekumar, R. Radhakrishnan Nair, Iype Joseph, Sai Ravi Chandra Nori, Jamiema Sara Philip, Roshny Prasad, K. V. Navyasree, Shikha Ramesh, Heera Pillai, Sanu Ghosh, T. R. Santosh Kumar & M. Radhakrishna Pillai. (2022). Mutational landscape and in silico structure models of SARS-CoV-2 spike receptor binding domain reveal key molecular determinants for virus-host interaction. BMC Mol. Cell Biol., 23, 1–12.
  • Niu, L., Wittrock, K. N., Clabaugh, G. C., Srivastava, V., & Cho, M. W. (2021). A Structural landscape of neutralizing antibodies against SARS-CoV-2 receptor binding domain. Frontiers in Immunology, 12, 1427. https://doi.org/10.3389/fimmu.2021.647934
  • Ovchinnikov, V., Louveau, J. E., Barton, J. P., Karplus, M., & Chakraborty, A. K. (2018). Role of framework mutations and antibody flexibility in the evolution of broadly neutralizing antibodies. eLife, 7, e33038. https://doi.org/10.7554/eLife.33038
  • Peiris, J. S. M., Chu, C. M., Cheng, V. C. C., Chan, K. S., Hung, I. F. N., Poon, L. L. M., Law, K. I., Tang, B. S. F., Hon, T. Y. W., Chan, C. S., Chan, K. H., Ng, J. S. C., Zheng, B. J., Ng, W. L., Lai, R. W. M., Guan, Y., & Yuen, K. Y. (2003). Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: A prospective study. The Lancet, 361(9371), 1767–1772. https://doi.org/10.1016/S0140-6736(03)13412-5
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Meng, E. C., Couch, G. S., Croll, T. I., Morris, J. H., & Ferrin, T. E. (2021). UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Science : A Publication of the Protein Society, 30(1), 70–82. https://doi.org/10.1002/pro.3943
  • Pinto, D., Park, Y.-J., Beltramello, M., Walls, A. C., Tortorici, M. A., Bianchi, S., Jaconi, S., Culap, K., Zatta, F., De Marco, A., Peter, A., Guarino, B., Spreafico, R., Cameroni, E., Case, J. B., Chen, R. E., Havenar-Daughton, C., Snell, G., Telenti, A., … Corti, D. (2020). Cross-neutralization of SARS-CoV-2 by a human monoclonal SARS-CoV antibody. Nature, 583(7815), 290–295. 2020 583 https://doi.org/10.1038/s41586-020-2349-y
  • Public Health England. (2021). SARS-CoV-2 variants of concern and variants under investigation in England. Sage 1–50.
  • Safavi, A., Kefayat, A., Mahdevar, E., Abiri, A., & Ghahremani, F. (2020). Exploring the out of sight antigens of SARS-CoV-2 to design a candidate multi-epitope vaccine by utilizing immunoinformatics approaches. Vaccine, 38(48), 7612–7628. https://doi.org/10.1016/j.vaccine.2020.10.016
  • Scheid, J. F., Mouquet, H., Ueberheide, B., Diskin, R., Klein, F., Oliveira, T. Y., Pietzsch, J., Fenyo, D., Abadir, A., Velinzon, K., & Hurley, A. (2011). Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science, 333, 1633–1637.
  • Schritt, D., Li, S., Rozewicki, J., Katoh, K., Yamashita, K., Volkmuth, W., Cavet, G., & Standley, D. M. (2019). Repertoire builder: High-throughput structural modeling of B and T cell receptors. Molecular Systems Design & Engineering, 4(4), 761–768. https://doi.org/10.1039/C9ME00020H
  • Shah, M., Ahmad, B., Choi, S., & Woo, H. G. (2020). Mutations in the SARS-CoV-2 spike RBD are responsible for stronger ACE2 binding and poor anti-SARS-CoV mAbs cross-neutralization. Computational and Structural Biotechnology Journal, 18, 3402–3414. https://doi.org/10.1016/j.csbj.2020.11.002
  • Simonich, C. A. (2019). Kappa chain maturation helps drive rapid development of an infant HIV-1 broadly neutralizing antibody lineage. Nature Communications, 10(1), 1–12.
  • Sumbalova, L., Stourac, J., Martinek, T., Bednar, D., & Damborsky, J. (2018). HotSpot Wizard 3.0: Web server for automated design of mutations and smart libraries based on sequence input information. Nucleic Acids Research, 46(W1), W356–W362. https://doi.org/10.1093/nar/gky417
  • Tan, G. S., Leon, P. E., Albrecht, R. A., Margine, I., Hirsh, A., Bahl, J., & Krammer, F. (2016). Broadly-reactive neutralizing and non-neutralizing antibodies directed against the H7 influenza virus hemagglutinin reveal divergent mechanisms of protection. PLoS Pathogens, 12(4), e1005578. https://doi.org/10.1371/journal.ppat.1005578
  • Tea, F., Ospina Stella, A., Aggarwal, A., Ross Darley, D., Pilli, D., Vitale, D., Merheb, V., Lee, F. X. Z., Cunningham, P., Walker, G. J., Fichter, C., Brown, D. A., Rawlinson, W. D., Isaacs, S. R., Mathivanan, V., Hoffmann, M., Pöhlman, S., Mazigi, O., Christ, D., … Turville, S. G. (2021). SARS-CoV-2 neutralizing antibodies: Longevity, breadth, and evasion by emerging viral variants. PLoS Medicine, 18(7), e1003656. https://doi.org/10.1371/journal.pmed.1003656
  • Ter Meulen, J., van den Brink, E. N., Poon, L. L. M., Marissen, W. E., Leung, C. S. W., Cox, F., Cheung, C. Y., Bakker, A. Q., Bogaards, J. A., van Deventer, E., Preiser, W., Doerr, H. W., Chow, V. T., de Kruif, J., Peiris, J. S. M., & Goudsmit, J. (2006). Human monoclonal antibody combination against SARS coronavirus: Synergy and coverage of escape mutants. PLoS Medicine, 3(7), e237. https://doi.org/10.1371/journal.pmed.0030237
  • Tsumoto, K., Ogasahara, K., Ueda, Y., Watanabe, K., Yutani, K., & Kumagai, I. (1996). Role of Salt Bridge Formation in Antigen-Antibody interaction. Entropic contribution to the complex between hen egg white lysozyme and its monoclonal antibody HyHEL10*. The Journal of Biological Chemistry, 271(51), 32612–32616. https://doi.org/10.1074/jbc.271.51.32612
  • Wang, E., Sun, H., Wang, J., Wang, Z., Liu, H., Zhang, J. Z. H., & Hou, T. (2019). End-Point Binding Free Energy Calculation with MM/PBSA and MM/GBSA: Strategies and Applications in Drug Design. Chemical Reviews, 119(16), 9478–9508. https://doi.org/10.1021/acs.chemrev.9b00055
  • Weng, G., Wang, E., Wang, Z., Liu, H., Zhu, F., Li, D., & Hou, T. (2019). HawkDock: A web server to predict and analyze the protein-protein complex based on computational docking and MM/GBSA. Nucleic Acids Research, 47(W1), W322–W330. https://doi.org/10.1093/nar/gkz397
  • Wintjens, R., Bifani, A. M., & Bifani, P. (2020). Impact of glycan cloud on the B-cell epitope prediction of SARS-CoV-2 Spike protein. NPJ Vaccines, 5(1), 1–8. https://doi.org/10.1038/s41541-020-00237-9
  • Yuan, M. (2022). Structural basis of a shared antibody response to SARS-CoV-2. http://science.sciencemag.org/.
  • Yuan, M., Wu, N. C., Zhu, X., Lee, C.-C D., So, R. T. Y., Lv, H., Mok, C. K. P., & Wilson, I. A. (2020). A highly conserved cryptic epitope in the receptor binding domains of SARS-CoV-2 and SARS-CoV. Science (New York, N.Y.), 368(6491), 630–633. https://doi.org/10.1126/science.abb7269
  • Zhou, J. O., Zaidi, H. A., Ton, T., & Fera, D. (2020). The effects of framework mutations at the variable domain interface on antibody affinity maturation in an HIV-1 broadly neutralizing antibody lineage. Frontiers in Immunology, 11, 1529. https://doi.org/10.3389/fimmu.2020.01529

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.