168
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Comprehensive deep mutational scanning reveals the pH induced stability and binding differences between SARS-CoV-2 spike RBD and human ACE2

, , , , , , & ORCID Icon show all
Pages 15207-15218 | Received 14 Nov 2022, Accepted 25 Feb 2023, Published online: 30 Mar 2023

References

  • Ahamad, S., Hema, K., Ahmad, S., Kumar, V., & Gupta, D. (2022). Insights into the structure and dynamics of SARS-CoV-2 spike glycoprotein double mutant L452R-E484Q. 3 Biotech, 12(4), 87. https://doi.org/10.1007/s13205-022-03151-0 [pii]
  • Alam, I., Radovanovic, A., Incitti, R., Kamau, A. A., Alarawi, M., Azhar, E. I., & Gojobori, T. (2021). CovMT: An interactive SARS-CoV-2 mutation tracker, with a focus on critical variants. Lancet Infectious Diseases. 21(5), 602. https://doi.org/10.1016/S1473-3099(21)00078-5
  • Ali, N., Khan, R., AlAsmari, A. F., & Kumar, V. (2022). In silico investigations of heparin binding to SARS-CoV-2 variants with a focus at the RBD/ACE2 interface. Process Biochemistry (Barking, London, England), 115, 70–79. https://doi.org/10.1016/j.procbio.2022.02.012 S1359-5113(22)00056-3 [pii]
  • Cai, Y., Zhang, J., Xiao, T., Peng, H., Sterling, S. M., Walsh, R. M., Rawson, S., Rits-Volloch, S., & Chen, B. (2020). Distinct conformational states of SARS-CoV-2 spike protein. Science (New York, N.Y.), 369(6511), 1586–1592. https://doi.org/10.1126/science.abd4251[Mismatch] science.abd4251 [pii]
  • Chan, K. K., Dorosky, D., Sharma, P., Abbasi, S. A., Dye, J. M., Kranz, D. M., Herbert, A. S., & Procko, E. (2020). Engineering human ACE2 to optimize binding to the spike protein of SARS coronavirus 2. Science (New York, N.Y.), 369(6508), 1261–1265. https://doi.org/10.1126/science.abc0870
  • Charles, J., McCann, N., Ploplis, V. A., & Castellino, F. J. (2023). Spike protein receptor-binding domains from SARS-CoV-2 variants of interest bind human ACE2 more tightly than the prototype spike protein. Biochemical and Biophysical Research Communications, 641, 61–66. https://doi.org/10.1016/j.bbrc.2022.12.011
  • Chen, C., Boorla, V. S., Banerjee, D., Chowdhury, R., Cavener, V. S., Nissly, R. H., Gontu, A., Boyle, N. R., Vandegrift, K., Nair, M. S., Kuchipudi, S. V., & Maranas, C. D. (2021). Computational prediction of the effect of amino acid changes on the binding affinity between SARS-CoV-2 spike RBD and human ACE2. Proceedings of the National Academy of Sciences, 118(42), e2106480118. https://doi.org/10.1073/pnas.2106480118
  • Chen, J., Wang, R., Wang, M., & Wei, G. W. (2020). Mutations strengthened SARS-CoV-2 infectivity. Journal of Molecular Biology, 432(19), 5212–5226. https://doi.org/10.1016/j.jmb.2020.07.009
  • Cheng, T. M., Goehring, L., Jeffery, L., Lu, Y. E., Hayles, J., Novak, B., & Bates, P. A. (2012). A structural systems biology approach for quantifying the systemic consequences of missense mutations in proteins. PLoS Computational Biology, 8(10), e1002738. https://doi.org/10.1371/journal.pcbi.1002738
  • Davies, N. G., Abbott, S., Barnard, R. C., Jarvis, C. I., Kucharski, A. J., Munday, J. D., Pearson, C. A. B., Russell, T. W., Tully, D. C., Washburne, A. D., Wenseleers, T., Gimma, A., Waites, W., Wong, K. L. M., van Zandvoort, K., Silverman, J. D., Diaz-Ordaz, K., Keogh, R., Eggo, R. M., … Edmunds, W. J., CMMID COVID-19 Working Group. (2021). Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science, 372(6538), eabg3055. https://doi.org/10.1126/science.abg3055
  • Dejnirattisai, W., Zhou, D., Supasa, P., Liu, C., Mentzer, A. J., Ginn, H. M., Zhao, Y., Duyvesteyn, H. M., Tuekprakhon, A., Nutalai, R., Wang, B., López-Camacho, C., Slon-Campos, J., Walter, T. S., Skelly, D., Costa Clemens, S. A., Naveca, F. G., Nascimento, V., Nascimento, F., … Screaton, G. R. (2021). Antibody evasion by the P.1 strain of SARS-CoV-2. Cell, 184(11), 2939–2954.e9. https://doi.org/10.1016/j.cell.2021.03.055
  • Gan, H. H., Twaddle, A., Marchand, B., & Gunsalus, K. C. (2021). Structural modeling of the SARS-CoV-2 Spike/human ACE2 complex interface can identify high-affinity variants associated with increased transmissibility. Journal of Molecular Biology, 433(15), 167051. https://doi.org/10.1016/j.jmb.2021.167051
  • 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., Dingens, A. S., Nargi, R. S., Sutton, R. E., Suryadevara, N., Rothlauf, P. W., Liu, Z., Whelan, S. P., 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 e49. https://doi.org/10.1016/j.chom.2020.11.007
  • Guerois, R., Nielsen, J. E., & Serrano, L. (2002). Predicting changes in the stability of proteins and protein complexes: A study of more than 1000 mutations. Journal of Molecular Biology, 320(2), 369–387. https://doi.org/10.1016/S0022-2836(02)00442-4 S0022-2836(02)00442-4 [pii]
  • Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N.-H., Nitsche, A., Müller, M. A., Drosten, C., & Pöhlmann, S. (2020). SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell, 181(2), 271–280 e278. https://doi.org/10.1016/j.cell.2020.02.052
  • Kyriakidis, N. C., Lopez-Cortes, A., Gonzalez, E. V., Grimaldos, A. B., & Prado, E. O. (2021). SARS-CoV-2 vaccines strategies: A comprehensive review of phase 3 candidates. NPJ Vaccines, 6(1), 28. https://doi.org/10.1038/s41541-021-00292-w
  • Lan, J., Ge, J., Yu, J., Shan, S., Zhou, H., Fan, S., Zhang, Q., Shi, X., Wang, Q., Zhang, L., & Wang, X. (2020). Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature, 581(7807), 215–220. https://doi.org/10.1038/s41586-020-2180-5[pii]
  • Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51(10), 2778–2786. https://doi.org/10.1021/ci200227u
  • Laurini, E., Marson, D., Aulic, S., Fermeglia, A., & Pricl, S. (2021). Computational mutagenesis at the SARS-CoV-2 spike protein/angiotensin-converting enzyme 2 binding interface: Comparison with experimental evidence. ACS Nano, 15(4), 6929–6948. https://doi.org/10.1021/acsnano.0c10833
  • Li, Q., Wu, J., Nie, J., Zhang, L., Hao, H., Liu, S., Zhao, C., Zhang, Q., Liu, H., Nie, L., Qin, H., Wang, M., Lu, Q., Li, X., Sun, Q., Liu, J., Zhang, L., Li, X., Huang, W., & Wang, Y. (2020). The impact of mutations in SARS-CoV-2 spike on viral infectivity and antigenicity. Cell, 182(5), 1284–1294.e9. https://doi.org/10.1016/j.cell.2020.07.012
  • Mannar, D., Saville, J. W., Zhu, X., Srivastava, S. S., Berezuk, A. M., Tuttle, K. S., Marquez, A. C., Sekirov, I., & Subramaniam, S. (2022). SARS-CoV-2 Omicron variant: Antibody evasion and cryo-EM structure of spike protein-ACE2 complex. Science, 375(6582), 760–764. https://doi.org/10.1126/science.abn7760
  • Moreira, R. A., Chwastyk, M., Baker, J. L., Guzman, H. V., & Poma, A. B. (2020). Quantitative determination of mechanical stability in the novel coronavirus spike protein. Nanoscale, 12(31), 16409–16413. https://doi.org/10.1039/D0NR03969A
  • Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F., & Serrano, L. (2005). The FoldX web server: An online force field. Nucleic Acids Research, 33(Web Server), W382–W388. 10.1093/nar/gki387
  • Shang, J., Wan, Y., Luo, C., Ye, G., Geng, Q., Auerbach, A., & Li, F. (2020). Cell entry mechanisms of SARS-CoV-2. Proceedings of the National Academy of Sciences, 117(21), 11727–11734. 2003138117 [pii] https://doi.org/10.1073/pnas.2003138117
  • Starr, T. N., Greaney, A. J., Addetia, A., Hannon, W. W., Choudhary, M. C., Dingens, A. S., Li, J. Z., & Bloom, J. D. (2021). Prospective mapping of viral mutations that escape antibodies used to treat COVID-19. Science, 371(6531), 850–854. ] https://doi.org/10.1126/science.abf9302
  • Starr, T. N., Greaney, A. J., Hilton, S. K., Ellis, D., Crawford, K. H., Dingens, A. S., Navarro, M. J., Bowen, J. E., Tortorici, M. A., Walls, A. C., King, N. P., Veesler, D., & Bloom, J. D. (2020). Deep mutational scanning of SARS-CoV-2 receptor binding domain reveals constraints on folding and ACE2 binding. Cell, 182(5), 1295–1310.e20. https://doi.org/10.1016/j.cell.2020.08.012
  • 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. Cellular & Molecular Immunology, 17(6), 613–620.[pii] https://doi.org/10.1038/s41423-020-0400-4
  • Teng, S., Madej, T., Panchenko, A., & Alexov, E. (2009). Modeling effects of human single nucleotide polymorphisms on protein-protein interactions. Biophysical Journal, 96(6), 2178–2188. S0006-3495(09)00325-7 [pii] https://doi.org/10.1016/j.bpj.2008.12.3904
  • Teng, S., Sobitan, A., Rhoades, R., Liu, D., & Tang, Q. (2021). Systemic effects of missense mutations on SARS-CoV-2 spike glycoprotein stability and receptor-binding affinity. Briefings in Bioinformatics, 22(2), 1239–1253. 5917277 [pii] https://doi.org/10.1093/bib/bbaa233
  • Tian, F., Tong, B., Sun, L., Shi, S., Zheng, B., Wang, Z., Dong, X., & Zheng, P. (2021). N501Y mutation of spike protein in SARS-CoV-2 strengthens its binding to receptor ACE2. eLife, 10, e69091. [pii] https://doi.org/10.7554/eLife.69091
  • Vedithi, S. C., Rodrigues, C. H., Portelli, S., Skwark, M. J., Das, M., Ascher, D. B., Blundell, T. L., & Malhotra, S. (2020). Computational saturation mutagenesis to predict structural consequences of systematic mutations in the beta subunit of RNA polymerase in Mycobacterium leprae. Computational and Structural Biotechnology Journal, 18, 271–286. S2001-0370(19)30291-0 [pii] https://doi.org/10.1016/j.csbj.2020.01.002
  • Walls, A. C., Park, Y. J., Tortorici, M. A., Wall, A., McGuire, A. T., & Veesler, D. (2020). Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell, 181(2), 281–292.e6. https://doi.org/10.1016/j.cell.2020.02.058
  • Wang, R., Hozumi, Y., Yin, C., & Wei, G. W. (2020). Decoding SARS-CoV-2 transmission and evolution and ramifications for COVID-19 diagnosis, vaccine, and medicine. Journal of Chemical Information and Modeling, 60(12), 5853–5865. https://doi.org/10.1021/acs.jcim.0c00501
  • Wang, Q., Zhang, Y., Wu, L., Niu, S., Song, C., Zhang, Z., Lu, G., Qiao, C., Hu, Y., Yuen, K.-Y., Wang, Q., Zhou, H., Yan, J., & Qi, J. (2020). Structural and functional basis of SARS-CoV-2 entry by using human ACE2. Cell, 181(4), 894–904.e9. https://doi.org/10.1016/j.cell.2020.03.045
  • Wibmer, C. K., Ayres, F., Hermanus, T., Madzivhandila, M., Kgagudi, P., Oosthuysen, B., Lambson, B. E., de Oliveira, T., Vermeulen, M., van der Berg, K., Rossouw, T., Boswell, M., Ueckermann, V., Meiring, S., von Gottberg, A., Cohen, C., Morris, L., Bhiman, J. N., & Moore, P. L. (2021). SARS-CoV-2 501Y.V2 escapes neutralization by South African COVID-19 donor plasma. Nature Medicine, 27(4), 622–625.[pii] https://doi.org/10.1038/s41591-021-01285-x
  • Wrapp, D., Wang, N., Corbett, K. S., Goldsmith, J. A., Hsieh, C.-L., Abiona, O., Graham, B. S., & McLellan, J. S. (2020). Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science, 367(6483), 1260–1263. ] https://doi.org/10.1126/science.abb2507
  • Wrobel, A. G., Benton, D. J., Xu, P., Roustan, C., Martin, S. R., Rosenthal, P. B., Skehel, J. J., & Gamblin, S. J. (2020). SARS-CoV-2 and bat RaTG13 spike glycoprotein structures inform on virus evolution and furin-cleavage effects. Nature Structural & Molecular Biology, 27(8), 763–767. https://doi.org/10.1038/s41594-020-0468-7[pii]
  • Wu, F., Zhao, S., Yu, B., Chen, Y.-M., Wang, W., Song, Z.-G., Hu, Y., Tao, Z.-W., Tian, J.-H., Pei, Y.-Y., Yuan, M.-L., Zhang, Y.-L., Dai, F.-H., Liu, Y., Wang, Q.-M., Zheng, J.-J., Xu, L., Holmes, E. C., & Zhang, Y.-Z. (2020). A new coronavirus associated with human respiratory disease in China. Nature, 579(7798), 265–269.[pii] 2008 [pii] https://doi.org/10.1038/s41586-020-2008-3
  • Wu, F., Zhao, S., Yu, B., Chen, Y.-M., Wang, W., … Zhang, Y.-Z. (2020). Complete genome characterisation of a novel coronavirus associated with severe human respiratory disease in Wuhan, China. bioRxiv 2020.01.24.919183. https://doi.org/10.1101/2020.01.24.919183
  • Xie, X., Liu, Y., Liu, J., Zhang, X., Zou, J., Fontes-Garfias, C. R., Xia, H., Swanson, K. A., Cutler, M., Cooper, D., Menachery, V. D., Weaver, S. C., Dormitzer, P. R., & Shi, P.-Y. (2021). Neutralization of SARS-CoV-2 spike 69/70 deletion, E484K and N501Y variants by BNT162b2 vaccine-elicited sera. Nature Medicine, 27(4), 620–621. https://doi.org/10.1038/s41591-021-01270-4[pii]
  • Xu, S., Wang, Y., Wang, Y., Zhang, C., Hong, Q., Gu, C., Xu, R., Wang, T., Yang, Y., Zang, J., Zhou, Y., Li, Z., Liu, Q., Zhou, B., Bai, L., Zhu, Y., Deng, Q., Wang, H., Lavillette, D., … Huang, Z. (2022). Mapping cross-variant neutralizing sites on the SARS-CoV-2 spike protein. Emerging Microbes & Infections, 11(1), 351–367. https://doi.org/10.1080/22221751.2021.2024455
  • Xue, B., Li, R., Ma, H., Rahaman, A., & Kumar, V. (2022). Comprehensive mapping of mutations in the C9ORF72 that affect folding and binding to SMCR8 protein. Process Biochemistry, 121, 312–321. https://doi.org/10.1016/j.procbio.2022.07.013
  • Xue, L. C., Rodrigues, J. P., Kastritis, P. L., Bonvin, A. M., & Vangone, A. (2016). PRODIGY: A web server for predicting the binding affinity of protein-protein complexes. Bioinformatics, 32(23), 3676–3678. https://doi.org/10.1093/bioinformatics/btw514
  • Xue, X., Shi, J., Xu, H., Qin, Y., Yang, Z., Feng, S., Liu, D., Jian, L., Hua, L., Wang, Y., Zhang, Q., Huang, X., Zhang, X., Li, X., Chen, C., Guo, J., Tang, W., & Liu, J. (2021). Dynamics of binding ability prediction between spike protein and human ACE2 reveals the adaptive strategy of SARS-CoV-2 in humans. Scientific Reports, 11(1), 3187. https://doi.org/10.1038/s41598-021-82938-2 3187[pii] 82938 [pii]
  • Zhang, L., Jackson, C. B., Mou, H., Ojha, A., Peng, H., Quinlan, B. D., Rangarajan, E. S., Pan, A., Vanderheiden, A., Suthar, M. S., Li, W., Izard, T., Rader, C., Farzan, M., & Choe, H. (2020). SARS-CoV-2 spike-protein D614G mutation increases virion spike density and infectivity. Nature Communications, 11(1), 6013. https://doi.org/10.1038/s41467-020-19808-4[pii]
  • Zhang, J., Xiao, T., Cai, Y., Lavine, C. L., Peng, H., Zhu, H., Anand, K., Tong, P., Gautam, A., Mayer, M. L., Walsh, R. M., Rits-Volloch, S., Wesemann, D. R., Yang, W., Seaman, M. S., Lu, J., & Chen, B. (2021). Membrane fusion and immune evasion by the spike protein of SARS-CoV-2 Delta variant. Science (New York, N.Y.), 374(6573), 1353–1360. https://doi.org/10.1126/science.abl9463
  • Zhou, T., Tsybovsky, Y., Gorman, J., Rapp, M., Cerutti, G., Chuang, G.-Y., Katsamba, P. S., Sampson, J. M., Schön, A., Bimela, J., Boyington, J. C., Nazzari, A., Olia, A. S., Shi, W., Sastry, M., Stephens, T., Stuckey, J., Teng, I.-T., Wang, P., … Kwong, P. D. (2020). Cryo-EM structures of SARS-CoV-2 spike without and with ACE2 reveal a pH-dependent switch to mediate endosomal positioning of receptor-binding domains. Cell Host & Microbe. 28(6), 867–879.e5. https://doi.org/10.1016/j.chom.2020.11.004

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.