SARS-CoV-2 omicron RBD forms a weaker binding affinity to hACE2 compared to Delta RBD in in-silico studies

References

• Abeywardhana, S., Premathilaka, M., Bandaranayake, U., Perera, D., & Peiris, L. D. C. (2023). In silico study of SARS‐CoV‐2 spike protein RBD and human ACE‐2 affinity dynamics across variants and Omicron subvariants. Journal of Medical Virology, 95(1), e28406. https://doi.org/10.1002/jmv.28406
   PubMed Web of Science ®Google Scholar
• 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
   Google Scholar
• Andrews, N., Stowe, J., Kirsebom, F., Toffa, S., Rickeard, T., Gallagher, E., Gower, C., Kall, M., Groves, N., & O’Connell, A.-M. (2022). Covid-19 vaccine effectiveness against the Omicron (B. 1.1. 529) variant. The New England Journal of Medicine, 386(16), 1532–1546.
   PubMed Web of Science ®Google Scholar
• Arold, S., Franken, P., Strub, M.-P., Hoh, F., Benichou, S., Benarous, R., & Dumas, C. (1997). The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure (London, England: 1993), 5(10), 1361–1372. https://doi.org/10.1016/s0969-2126(97)00286-4
   PubMed Web of Science ®Google Scholar
• Augusto, G., Mohsen, M. O., Zinkhan, S., Liu, X., Vogel, M., & Bachmann, M. F. (2022). In vitro data suggest that Indian delta variant B. 1.617 of SARS‐CoV‐2 escapes neutralization by both receptor affinity and immune evasion. Allergy, 77(1), 111–117.
   PubMed Web of Science ®Google Scholar
• Barducci, A., Bonomi, M., & Parrinello, M. (2011). Metadynamics. WIREs Computational Molecular Science, 1(5), 826–843. https://doi.org/10.1002/wcms.31
   Google Scholar
• Bourne, Y., Watson, M. H., Hickey, M. J., Holmes, W., Rocque, W., Reed, S. I., & Tainer, J. A. (1996). Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle–regulatory protein CksHs1. Cell, 84(6), 863–874. https://doi.org/10.1016/s0092-8674(00)81065-x
   PubMed Web of Science ®Google Scholar
• Brandal, L. T., MacDonald, E., Veneti, L., Ravlo, T., Lange, H., Naseer, U., Feruglio, S., Bragstad, K., Hungnes, O., & Ødeskaug, L. E. (2021). Outbreak caused by the SARS-CoV-2 Omicron variant in Norway, November to December 2021. Eurosurveillance, 26(50), 2101147.
   Web of Science ®Google Scholar
• Buckle, A. M., Schreiber, G., & Fersht, A. R. (1994). Protein-protein recognition: Crystal structural analysis of a barnase-barstar complex at 2.0-. ANG. resolution. Biochemistry, 33(30), 8878–8889. https://doi.org/10.1021/bi00196a004
   PubMed Web of Science ®Google Scholar
• Cao, Y. R., Wang, J., Jian, F., Xiao, T., Song, W., Yisimayi, A., … & Xie, X. S. (2022). Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature, 602(7898), 657–663 . https://doi.org/10.1038/s41586-021-04385-3
   Google Scholar
• Cele, S., Jackson, L., Khoury, D. S., Khan, K., Moyo-Gwete, T., Tegally, H., … & Sigal, A. (2022). Omicron extensively but incompletely escapes Pfizer BNT162b2 neutralization. Nature, 602(7898), 654–656. https://doi.org/10.1038/s41586-021-04387-1
   Google Scholar
• Chen, J., & Wei, G.-W. (2022). Omicron BA.2 (B.1.1.529.2): High potential for becoming the next dominant variant. The Journal of Physical Chemistry Letters, 13, 3840–3849. https://doi.org/10.1021/acs.jpclett.2c00469
   PubMed Web of Science ®Google Scholar
• de Jong, D. H., Uusitalo, J. J., & Wassenaar, T. A. (2017). Martinize version 2.6. http://cgmartini.nl/index.php/tools2/proteins-and-bilayers.
   Google Scholar
• Espenhain, L., Funk, T., Overvad, M., Edslev, S. M., Fonager, J., Ingham, A. C., Rasmussen, M., Madsen, S. L., Espersen, C. H., & Sieber, R. N. (2021). Epidemiological characterisation of the first 785 SARS-CoV-2 Omicron variant cases in Denmark, December 2021. Eurosurveillance, 26(50), 2101146. https://doi.org/10.2807/1560-7917.ES.2021.26.50.2101146
   Web of Science ®Google Scholar
• Frigerio, F., Coda, A., Pugliese, L., Lionetti, C., Menegatti, E., Amiconi, G., Schnebli, H. P., Ascenzi, P., & Bolognesi, M. (1992). Crystal and molecular structure of the bovine α-chymotrypsin-eglin c complex at 2.0 Å resolution. Journal of Molecular Biology, 225(1), 107–123. https://doi.org/10.1016/0022-2836(92)91029-o
   PubMed Web of Science ®Google Scholar
• Gamble, T. R., Vajdos, F. F., Yoo, S., Worthylake, D. K., Houseweart, M., Sundquist, W. I., & Hill, C. P. (1996). Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell, 87(7), 1285–1294. https://doi.org/10.1016/s0092-8674(00)81823-1
   PubMed Web of Science ®Google Scholar
• Geng, Q., Shi, K., Ye, G., Zhang, W., Aihara, H., Li, F., & Gallagher, T. (2022). Structural basis for human receptor recognition by SARS-CoV-2 Omicron Variant BA.1. Journal of Virology, 96(8), e00249. https://doi.org/10.1128/jvi.00249-22
   PubMed Web of Science ®Google Scholar
• Genovese, L., Zaccaria, M., Farzan, M., Johnson, W., & Momeni, B. (2021). Investigating the mutational landscape of the SARS-CoV-2 Omicron variant via ab initio quantum mechanical modeling. BioRxiv, 2021-12. https://doi.org/10.1101/2021.12.01.470748
   Google Scholar
• Goher, S. S., Ali, F., & Amin, M. (2022). The Delta variant mutations in the receptor binding domain of SARS-CoV-2 show enhanced electrostatic interactions with the ACE2. Medicine in Drug Discovery, 13, 100114.
   Google Scholar
• Gowrisankar, A., Priyanka, T., & Banerjee, S. (2022). Omicron: A mysterious variant of concern. The European Physical Journal Plus, 137(1), 1–8. https://doi.org/10.1140/epjp/s13360-021-02321-y
   PubMed Web of Science ®Google Scholar
• Han, P., Li, L., Liu, S., Wang, Q., Zhang, D., Xu, Z., Han, P., Li, X., Peng, Q., Su, C., Huang, B., Li, D., Zhang, R., Tian, M., Fu, L., Gao, Y., Zhao, X., Liu, K., Qi, J., Gao, G. F., & Wang, P. (2022). Receptor binding and complex structures of human ACE2 to spike RBD from omicron and delta SARS-CoV-2. Cell, 185(4), 630–640.e10. https://doi.org/10.1016/j.cell.2022.01.001
   PubMed Web of Science ®Google Scholar
• Huang, M., Syed, R., Stura, E. A., Stone, M. J., Stefanko, R. S., Ruf, W., Edgington, T. S., & Wilson, I. A. (1998). The mechanism of an inhibitory antibody on TF-initiated blood coagulation revealed by the crystal structures of human tissue factor, Fab 5G9 and TF· 5G9 complex. Journal of Molecular Biology, 275(5), 873–894. https://doi.org/10.1006/jmbi.1997.1512
   PubMed Web of Science ®Google Scholar
• Huse, M., Chen, Y.-G., Massagué, J., & Kuriyan, J. (1999). Crystal structure of the cytoplasmic domain of the type I TGF β receptor in complex with FKBP12. Cell, 96(3), 425–436. https://doi.org/10.1016/s0092-8674(00)80555-3
   PubMed Web of Science ®Google Scholar
• Jiang, W., & Roux, B. (2010). Free energy perturbation Hamiltonian replica-exchange molecular dynamics (FEP/H-REMD) for absolute ligand binding free energy calculations. Journal of Chemical Theory and Computation, 6(9), 2559–2565. https://doi.org/10.1021/ct1001768
   PubMed Web of Science ®Google Scholar
• Jung, C., Kmiec, D., Koepke, L., Zech, F., Jacob, T., Sparrer, K. M., & Kirchhoff, F. (2022). Omicron: What makes the latest SARS-CoV-2 variant of concern so concerning? Journal of Virology, 96(6), e02077. https://doi.org/10.1128/jvi.02077-21
   PubMed Web of Science ®Google Scholar
• Kabsch, W., Mannherz, H. G., Suck, D., Pai, E. F., & Holmes, K. C. (1990). Atomic structure of the actin: DNase I complex. Nature, 347(6288), 37–44. https://doi.org/10.1038/347037a0
   PubMed Web of Science ®Google Scholar
• Kannan, S. R., Spratt, A. N., Sharma, K., Chand, H. S., Byrareddy, S. N., & Singh, K. (2022). Omicron SARS-CoV-2 variant: Unique features and their impact on pre-existing antibodies. Journal of Autoimmunity, 126, 102779. https://doi.org/10.1016/j.jaut.2021.102779
   PubMed Web of Science ®Google Scholar
• Karim, S. S. A., & Karim, Q. A. (2021). Omicron SARS-CoV-2 variant: A new chapter in the COVID-19 pandemic. Lancet (London, England), 398(10317), 2126–2128. https://doi.org/10.1016/S0140-6736(21)02758-6
   PubMed Web of Science ®Google Scholar
• Ke, Q., Gong, X., Liao, S., Duan, C., & Li, L. (2022). Effects of thermostats/barostats on physical properties of liquids by molecular dynamics simulations. Journal of Molecular Liquids, 365, 120116. https://doi.org/10.1016/j.molliq.2022.120116
   Web of Science ®Google Scholar
• Khan, A., Waris, H., Rafique, M., Suleman, M., Mohammad, A., Ali, S. S., Khan, T., Waheed, Y., Liao, C., & Wei, D.-Q. (2022). The Omicron (B. 1.1. 529) variant of SARS-CoV-2 binds to the hACE2 receptor more strongly and escapes the antibody response: Insights from structural and simulation data. International Journal of Biological Macromolecules, 200, 438–448. https://doi.org/10.1016/j.ijbiomac.2022.01.059
   PubMed Web of Science ®Google Scholar
• Khan, A., Zia, T., Suleman, M., Khan, T., Ali, S. S., Abbasi, A. A., Mohammad, A., & Wei, D. Q. (2021). Higher infectivity of the SARS‐CoV‐2 new variants is associated with K417N/T, E484K, and N501Y mutants: An insight from structural data. Journal of Cellular Physiology, 236(10), 7045–7057. https://doi.org/10.1002/jcp.30367
   PubMed Web of Science ®Google Scholar
• Kirkwood, J. G. (1935). Statistical mechanics of fluid mixtures. Journal of Chemical Physics, 3(5), 300–313. https://doi.org/10.1063/1.1749657
   Google Scholar
• Mai, N. T., Lan, N. T., Vu, T. Y., Duong, P. T. M., Tung, N. T., & Phung, H. T. T. (2020). Estimation of the ligand-binding free energy of checkpoint kinase 1 via non-equilibrium MD simulations. Journal of Molecular Graphics and Modelling, 100, 107648.
   PubMed Web of Science ®Google Scholar
• Makhov, D., Popović, D. M., & Stuchebrukhov, A. A. (2006). Improved density functional theory/electrostatic calculation of the His291 protonation state in cytochrome c oxidase: Self-consistent charges for solvation energy calculation. The Journal of Physical Chemistry. B, 110(24), 12162–12166. https://doi.org/10.1021/jp0608630
   PubMed Web of Science ®Google Scholar
• Mu, Y., Nguyen, P. H., & Stock, G. (2004). Energy landscape of a small peptide revealed by dihedral angle principal component analysis. Proteins: Structure, Function, and Bioinformatics, 58(1), 45–52. https://doi.org/10.1002/prot.20310
   Web of Science ®Google Scholar
• Ngo, S. T. (2022). 501Y.V2 spike protein resists the neutralizing antibody in atomistic simulations. Computational Biology and Chemistry, 97, 107636.
   PubMed Web of Science ®Google Scholar
• Ngo, S. T., Hung, H. M., & Nguyen, M. T. (2016). Fast and accurate determination of the relative binding affinities of small compounds to HIV‐1 protease using non‐equilibrium work. Journal of Computational Chemistry, 37(31), 2734–2742. https://doi.org/10.1002/jcc.24502
   PubMed Web of Science ®Google Scholar
• Ngo, S. T., Nguyen, T. H., Pham, D.-H., Tung, N. T., & Nam, P. C. (2021). Thermodynamics and kinetics in antibody resistance of the 501Y.V2 SARS-CoV-2 variant. RSC Advances, 11(53), 33438–33446. https://doi.org/10.1039/d1ra04134g
   PubMed Web of Science ®Google Scholar
• Ngo, S. T., Tam, N. M., Pham, M. Q., & Nguyen, T. H. (2021). Benchmark of popular free energy approaches revealing the inhibitors binding to SARS-CoV-2 Mpro. Journal of Chemical Information and Modelling, 61(5), 2302–2312.
   PubMed Web of Science ®Google Scholar
• Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics & Modelling, 27(8), 889–899. https://doi.org/10.1016/j.jmgm.2009.01.006
   PubMed Web of Science ®Google Scholar
• Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics and Modelling, 27(8), 889–899.
   PubMed Web of Science ®Google Scholar
• Park, S., & Schulten, K. (2004). Calculating potentials of mean force from steered molecular dynamics simulations. The Journal of Chemical Physics, 120(13), 5946–5961. https://doi.org/10.1063/1.1651473
   PubMed Web of Science ®Google Scholar
• Patrick, C., Upadhyay, V., Lucas, A., & Mallela, K. M. (2022). Biophysical fitness landscape of the SARS-CoV-2 Delta variant receptor binding domain. Journal of Molecular Biology, 434(13), 167622. https://doi.org/10.1016/j.jmb.2022.167622
   PubMed Web of Science ®Google Scholar
• Pham, M. Q., Vu, K. B., Pham, T. N. H., Tran, L. H., Tung, N. T., Vu, V. V., Nguyen, T. H., & Ngo, S. T. (2020). Rapid prediction of possible inhibitors for SARS-CoV-2 main protease using docking and FPL simulations. RSC Advances, 10(53), 31991–31996.
   PubMed Web of Science ®Google Scholar
• Popović, D., & Đorđević, I. (2020). Catalytic center of cytochrome c oxidase: Effects of protein environment on pKa values of Cub histidine ligands. Journal of the Serbian Chemical Society, 85(11), 1429–1444.
   Web of Science ®Google Scholar
• PyMOLWiki. (n.d.) Center of mass. https://pymolwiki.org/index.php/Center_of_mass.
   Google Scholar
• Qin, S., Cui, M., Sun, S., Zhou, J., Du, Z., Cui, Y., & Fan, H. (2021). Genome characterization and potential risk assessment of the novel SARS-CoV-2 variant Omicron (B. 1.1. 529). Zoonoses, 1(1). https://doi.org/10.15212/ZOONOSES-2021-0024
   Google Scholar
• Santra, D., Banerjee, A., & Maiti, S. (2022). Better binding informatics of delta variants (B. 1.617. 2) with ACE2 than wild, D614G or N501Y CoV-2 is fully blocked by 84 amino-acid cut of wild spike. Informatics in Medicine Unlocked, 29, 100900. https://doi.org/10.1016/j.imu.2022.100900
   Google Scholar
• Sevcik, J., Urbanikova, L., Dauter, Z., & Wilson, K. (1998). Recognition of RNase Sa by the inhibitor barstar: Structure of the complex at 1.7 A resolution. Acta Crystallographica. Section D, Biological Crystallography, 54(Pt 5), 954–963. https://doi.org/10.1107/s0907444998004429
   PubMedGoogle Scholar
• Shang, J., Ye, G., Shi, K., Wan, Y., Luo, C., Aihara, H., Geng, Q., Auerbach, A., & Li, F. (2020). Structural basis of receptor recognition by SARS-CoV-2. Nature, 581(7807), 221–224. https://doi.org/10.1038/s41586-020-2179-y
   PubMed Web of Science ®Google Scholar
• Singanayagam, A., Hakki, S., Dunning, J., Madon, K. J., Crone, M. A., Koycheva, A., Derqui-Fernandez, N., Barnett, J. L., Whitfield, M. G., Varro, R., Charlett, A., Kundu, R., Fenn, J., Cutajar, J., Quinn, V., Conibear, E., Barclay, W., Freemont, P. S., Taylor, G. P., … Lalvani, A., ATACCC Study Investigators. (2022). Community transmission and viral load kinetics of the SARS-CoV-2 delta (B. 1.617. 2) variant in vaccinated and unvaccinated individuals in the UK: A prospective, longitudinal, cohort study. The Lancet. Infectious Diseases, 22(2), 183–195. https://doi.org/10.1016/S1473-3099(21)00648-4
   PubMed Web of Science ®Google Scholar
• Souza, P. C. T., Alessandri, R., Barnoud, J., Thallmair, S., Faustino, I., Grünewald, F., Patmanidis, I., Abdizadeh, H., Bruininks, B. M. H., Wassenaar, T. A., Kroon, P. C., Melcr, J., Nieto, V., Corradi, V., Khan, H. M., Domański, J., Javanainen, M., Martinez-Seara, H., Reuter, N., … Marrink, S. J. (2021). Martini 3: A general purpose force field for coarse-grained molecular dynamics. Nature Methods, 18(4), 382–388. https://doi.org/10.1038/s41592-021-01098-3
   PubMed Web of Science ®Google Scholar
• Spensley, K. J., Gleeson, S., Martin, P., Thomson, T., Clarke, C. L., Pickard, G., Thomas, D., McAdoo, S. P., Randell, P., & Kelleher, P. (2022). Comparison of vaccine effectiveness against the omicron (B. 1.1. 529) variant in hemodialysis patients. Kidney International Reports, 7(6), 1406-1409. https://doi.org/10.1016/j.ekir.2022.04.005
   PubMed Web of Science ®Google Scholar
• Starr, T. N., Greaney, A. J., Hilton, S. K., Ellis, D., Crawford, K. H. D., 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
   PubMed Web of Science ®Google Scholar
• Stewart, M., Kent, H. M., & McCoy, A. J. (1998). Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the GDP-bound form of the Ras-family GTPase Ran. Journal of Molecular Biology, 277(3), 635–646. https://doi.org/10.1006/jmbi.1997.1602
   PubMed Web of Science ®Google Scholar
• Suzuki, R., Yamasoba, D., Kimura, I., Wang, L., Kishimoto, M., Ito, J., Morioka, Y., Nao, N., Nasser, H., Uriu, K., Kosugi, Y., Tsuda, M., Orba, Y., Sasaki, M., Shimizu, R., Kawabata, R., Yoshimatsu, K., Asakura, H., Nagashima, M., … Sato, K., The Genotype to Phenotype Japan (G2P-Japan) Consortium. (2022). Early assessment of the clinical severity of the SARS-CoV-2 omicron variant in South Africa: A data linkage study. The Lancet, 603(7902), 700–705. https://doi.org/10.1038/s41586-022-04462-1
   Google Scholar
• Tian, D., Sun, Y., Xu, H., & Ye, Q. (2022). The emergence and epidemic characteristics of the highly mutated SARS‐CoV‐2 Omicron variant. Journal of Medical Virology, 94(17), 2376–2383.
   PubMedGoogle Scholar
• Torrie, G. M., & Valleau, J. P. (1977). Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling. Journal of Computational Physics, 23(2), 187–199. https://doi.org/10.1016/0021-9991(77)90121-8
   Web of Science ®Google Scholar
• Townsend, J. P., Hassler, H. B., Wang, Z., Miura, S., Singh, J., Kumar, S., Ruddle, N. H., Galvani, A. P., & Dornburg, A. (2021). The durability of immunity against reinfection by SARS-CoV-2: A comparative evolutionary study. The Lancet. Microbe, 2(12), e666–e675. https://doi.org/10.1016/S2666-5247(21)00219-6
   PubMedGoogle Scholar
• Wang, Y., Chen, R., Hu, F., Lan, Y., Yang, Z., Zhan, C., Shi, J., Deng, X., Jiang, M., Zhong, S., Liao, B., Deng, K., Tang, J., Guo, L., Jiang, M., Fan, Q., Li, M., Liu, J., Shi, Y., … Tang, X. (2021). Transmission, viral kinetics and clinical characteristics of the emergent SARS-CoV-2 Delta VOC in Guangzhou, China. EClinicalMedicine, 40, 101129. https://doi.org/10.1016/j.eclinm.2021.101129
   PubMedGoogle Scholar
• Wiegand, G., Epp, O., & Huber, R. (1995). The crystal structure of porcine pancreatic α-amylase in complex with the microbial inhibitor Tendamistat. Journal of Molecular Biology, 247(1), 99–110. https://doi.org/10.1006/jmbi.1994.0125
   PubMed Web of Science ®Google Scholar
• Wu, L., Zhou, L., Mo, M., Liu, T., Wu, C., Gong, C., Lu, K., Gong, L., Zhu, W., & Xu, Z. (2022). SARS-CoV-2 Omicron RBD shows weaker binding affinity than the currently dominant Delta variant to human ACE2. Signal Transduction and Targeted Therapy, 7(1), 1–3. https://doi.org/10.1038/s41392-021-00863-2
   PubMed Web of Science ®Google Scholar
• Yang, T. J., Yu, P. Y., Chang, Y. C., Chang, N. E., Tsai, Y. X., Liang, K. H., … & Hsu, S. T. D. (2021). Structure-activity relationships of B. 1.617 and other SARS-CoV-2 spike variants. BioRxiv, 2021–09. https://doi.org/10.1101/2021.09.12.459978
   Google Scholar
• Zhang, L., Li, Q., Liang, Z., Li, T., Liu, S., Cui, Q., Nie, J., Wu, Q., Qu, X., & Huang, W. (2022). The significant immune escape of pseudotyped SARS-CoV-2 Variant Omicron. Emerging Microbes & Infections, 11(1), 1–5. https://doi.org/10.1080/22221751.2021.2017757
   PubMed Web of Science ®Google Scholar