Interfacial water molecules contribute to antibody binding to the receptor-binding domain of SARS-CoV-2 spike protein

References

• Ahmad, B., Batool, M., Kim, M. S., & Choi, S. (2021). Computational-driven epitope verification and affinity maturation of TLR4-targeting antibodies. International Journal of Molecular Science, 22(11), 5989. https://doi.org/10.3390/ijms22115989.
   Web of Science ®Google Scholar
• Ahmad, M., Gu, W., Geyer, T., & Helms, V. (2011). Adhesive water networks facilitate binding of protein interfaces. Nature Communications, 2, 261. https://doi.org/10.1038/ncomms1258
   PubMed Web of Science ®Google Scholar
• Andricioaei, I., & Karplus, M. (2001). On the calculation of entropy from covariance matrices of the atomic fluctuations. Journal of Chemical Physics, 115(14), 6289–6292. https://doi.org/10.1063/1.1401821
   Web of Science ®Google Scholar
• Andrio, P., Hospital, A., Conejero, J., Jorda, L., Del Pino, M., Codo, L., Soiland-Reyes, S., Goble, C., Lezzi, D., Badia, R. M., Orozco, M., & Gelpi, J. L. (2019). BioExcel Building Blocks, a software library for interoperable biomolecular simulation workflows. Scientific Data, 6(1), 169. https://doi.org/10.1038/s41597-019-0177-4
   PubMedGoogle Scholar
• Bekker, G. J., Fukuda, I., Higo, J., & Kamiya, N. (2020). Mutual population-shift driven antibody-peptide binding elucidated by molecular dynamics simulations. Scientific Reports, 10(1), 1406. https://doi.org/10.1038/s41598-020-58320-z
   PubMed Web of Science ®Google Scholar
• Berne, B. J., Weeks, J. D., & Zhou, R. (2009). Dewetting and hydrophobic interaction in physical and biological systems. Annual Review of Physical Chemistry, 60, 85–103. https://doi.org/10.1146/annurev.physchem.58.032806.104445
   PubMed Web of Science ®Google Scholar
• Bhattacharjee, N., & Biswas, P. (2011). Structure of hydration water in proteins: a comparison of molecular dynamics simulations and database analysis. Biophysical Chemistry, 158(1), 73–80. https://doi.org/10.1016/j.bpc.2011.05.009
   PubMed Web of Science ®Google Scholar
• Cai, Y., Zhang, J., Xiao, T., Peng, H., Sterling, S. M., Walsh, R. M., Jr., Rawson, S., Rits-Volloch, S., & Chen, B. (2020). Distinct conformational states of SARS-CoV-2 spike protein. Science (New York, NY), 369(6511), 1586–1592. https://doi.org/10.1126/science.abd4251
   Google Scholar
• Chen, X., Weber, I., & Harrison, R. W. (2008). Hydration water and bulk water in proteins have distinct properties in radial distributions calculated from 105 atomic resolution crystal structures. The Journal of Physical Chemistry. B, 112(38), 12073–12080. https://doi.org/10.1021/jp802795a
   PubMed Web of Science ®Google Scholar
• Concepcion, J., Witte, K., Wartchow, C., Choo, S., Yao, D., Persson, H., Wei, J., Li, P., Heidecker, B., Ma, W., Varma, R., Zhao, L. S., Perillat, D., Carricato, G., Recknor, M., Du, K., Ho, H., Ellis, T., Gamez, J., … Tan, H. (2009). Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization. Combinatorial Chemistry & High Throughput Screening, 12(8), 791–800. https://doi.org/10.2174/138620709789104915
   PubMed Web of Science ®Google Scholar
• Covell, D. G., & Wallqvist, A. (1997). Analysis of protein-protein interactions and the effects of amino acid mutations on their energetics. The importance of water molecules in the binding epitope. Journal of Molecular Biology, 269(2), 281–297. https://doi.org/10.1006/jmbi.1997.1028
   PubMed Web of Science ®Google Scholar
• Duan, L., Liu, X., & Zhang, J. Z. (2016). Interaction entropy: A new paradigm for highly efficient and reliable computation of protein-ligand binding free energy. Journal of the American Chemical Society, 138(17), 5722–5728. https://doi.org/10.1021/jacs.6b02682
   PubMed Web of Science ®Google Scholar
• Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
   PubMed Web of Science ®Google Scholar
• Gilson, M. K., & Zhou, H. X. (2007). Calculation of protein-ligand binding affinities. Annual Review of Biophysics and Biomolecular Structure, 36(1), 21–42. https://doi.org/10.1146/annurev.biophys.36.040306.132550
   PubMedGoogle Scholar
• Hansson, T., Marelius, J., & Aqvist, J. (1998). Ligand binding affinity prediction by linear interaction energy methods. Journal of Computer-Aided Molecular Design, 12(1), 27–35. https://doi.org/10.1023/a:1007930623000
   PubMed Web of Science ®Google Scholar
• Homola, J. (2008). Surface plasmon resonance sensors for detection of chemical and biological species. Chemical Reviews, 108(2), 462–493. https://doi.org/10.1021/cr068107d
   PubMed Web of Science ®Google Scholar
• Hus, M., & Urbic, T. (2012). Strength of hydrogen bonds of water depends on local environment. The Journal of Chemical Physics, 136(14), 144305. https://doi.org/10.1063/1.3701616
   PubMed Web of Science ®Google Scholar
• Ieong, P., Amaro, R. E., & Li, W. W. (2015). Molecular dynamics analysis of antibody recognition and escape by human H1N1 influenza hemagglutinin. Biophysical Journal, 108(11), 2704–2712. https://doi.org/10.1016/j.bpj.2015.04.025
   PubMed Web of Science ®Google Scholar
• Jackson, C. B., Farzan, M., Chen, B., & Choe, H. (2022). Mechanisms of SARS-CoV-2 entry into cells. Nature Reviews. Molecular Cell Biology, 23(1), 3–20. https://doi.org/10.1038/s41580-021-00418-x
   PubMed Web of Science ®Google Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham 3rd, T. E. (2000). Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Kralj, S., Hodoscek, M., Podobnik, B., Kunej, T., Bren, U., Janezic, D., & Konc, J. (2021). Molecular dynamics simulations reveal interactions of an IgG1 antibody with selected Fc receptors. Frontiers in Chemistry, 9, 705931. https://doi.org/10.3389/fchem.2021.705931
   PubMed Web of Science ®Google Scholar
• Ladbury, J. E., & Chowdhry, B. Z. (1996). Sensing the heat: the application of isothermal titration calorimetry to thermodynamic studies of biomolecular interactions. Chemistry & Biology, 3(10), 791–801. https://doi.org/10.1016/s1074-5521(96)90063-0
   PubMedGoogle Scholar
• Li, W. H., Moore, M. J., Vasilieva, N., Sui, J. H., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., Choe, H., & Farzan, M. (2003). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature, 426(6965), 450–454. https://doi.org/10.1038/nature02145
   PubMed Web of Science ®Google Scholar
• Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: a package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306–317. https://doi.org/10.1007/s008940100045
   Web of Science ®Google Scholar
• Livingstone, J. R. (1996). Antibody characterization by isothermal titration calorimetry. Nature, 384(6608), 491–492. https://doi.org/10.1038/384491a0
   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., Bi, Y., Ma, X., Zhan, F., Wang, L., Hu, T., Zhou, H., Hu, Z., Zhou, W., Zhao, L., … Tan, W. (2020). Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet (London, England), 395(10224), 565–574. https://doi.org/10.1016/S0140-6736(20)30251-8
   PubMed Web of Science ®Google Scholar
• Maffucci, I., & Contini, A. (2013). Explicit ligand hydration shells improve the correlation between MM-PB/GBSA binding energies and experimental activities. Journal of Chemical Theory and Computation, 9(6), 2706–2717. https://doi.org/10.1021/ct400045d
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. Journal of Chemical Theory and Computation, 11(8), 3696–3713. https://doi.org/10.1021/acs.jctc.5b00255
   PubMed Web of Science ®Google Scholar
• McCammon, J. A., Gelin, B. R., & Karplus, M. (1977). Dynamics of folded proteins. Nature, 267(5612), 585–590. https://doi.org/10.1038/267585a0
   PubMed Web of Science ®Google Scholar
• Mikulskis, P., Genheden, S., & Ryde, U. (2014). Effect of explicit water molecules on ligand-binding affinities calculated with the MM/GBSA approach. Journal of Molecular Modeling, 20(6), 2273. https://doi.org/10.1007/s00894-014-2273-x
   PubMed Web of Science ®Google Scholar
• Park, Y. J., De Marco, A., Starr, T. N., Liu, Z., Pinto, D., Walls, A. C., Zatta, F., Zepeda, S. K., Bowen, J. E., Sprouse, K. R., Joshi, A., Giurdanella, M., Guarino, B., Noack, J., Abdelnabi, R., Foo, S. C., Rosen, L. E., Lempp, F. A., Benigni, F., … Veesler, D. (2022). Antibody-mediated broad sarbecovirus neutralization through ACE2 molecular mimicry. Science (New York, NY), 375(6579), 449–454. https://doi.org/10.1126/science.abm8143
   Google Scholar
• 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. https://doi.org/10.1038/s41586-020-2349-y
   PubMed Web of Science ®Google Scholar
• Rao, S. N., Singh, U. C., Bash, P. A., & Kollman, P. A. (1987). Free energy perturbation calculations on binding and catalysis after mutating Asn 155 in subtilisin. Nature, 328(6130), 551–554. https://doi.org/10.1038/328551a0
   PubMed Web of Science ®Google Scholar
• Setny, P., Wang, Z., Cheng, L. T., Li, B., McCammon, J. A., & Dzubiella, J. (2009). Dewetting-controlled binding of ligands to hydrophobic pockets. Physical Review Letters, 103(18), 187801. https://doi.org/10.1103/PhysRevLett.103.187801
   PubMed Web of Science ®Google Scholar
• Sheng, Y. J., Yin, Y. W., Ma, Y. Q., & Ding, H. M. (2021). Improving the performance of MM/PBSA in protein-protein interactions via the screening electrostatic energy. Journal of Chemical Information and Modeling, 61(5), 2454–2462. https://doi.org/10.1021/acs.jcim.1c00410
   PubMed Web of Science ®Google Scholar
• Singh, U. C., & Benkovic, S. J. (1988). A free-energy perturbation study of the binding of methotrexate to mutants of dihydrofolate reductase. Proceedings of the National Academy of Sciences of the United States of America, 85(24), 9519–9523. https://doi.org/10.1073/pnas.85.24.9519
   PubMed Web of Science ®Google Scholar
• Sun, H., Duan, L., Chen, F., Liu, H., Wang, Z., Pan, P., Zhu, F., Zhang, J. Z. H., & Hou, T. (2018). Assessing the performance of MM/PBSA and MM/GBSA methods. 7. Entropy effects on the performance of end-point binding free energy calculation approaches. Physical Chemistry Chemical Physics: PCCP, 20(21), 14450–14460. https://doi.org/10.1039/c7cp07623a
   PubMed Web of Science ®Google Scholar
• Sun, Z., Yan, Y. N., Yang, M., & Zhang, J. Z. (2017). Interaction entropy for protein-protein binding. The Journal of Chemical Physics, 146(12), 124124. https://doi.org/10.1063/1.4978893
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• van Gunsteren, W. F., & Berendsen, H. J. (1987). Thermodynamic cycle integration by computer simulation as a tool for obtaining free energy differences in molecular chemistry. Journal of Computer-Aided Molecular Design, 1(2), 171–176. https://doi.org/10.1007/BF01676960
   PubMedGoogle Scholar
• Wade, R. C., & McCammon, J. A. (1992). Binding of an antiviral agent to a sensitive and a resistant human rhinovirus. Computer simulation studies with sampling of amino acid side-chain conformations. II. Calculation of free-energy differences by thermodynamic integration. Journal of Molecular Biology, 225(3), 697–712. https://doi.org/10.1016/0022-2836(92)90395-z
   PubMed Web of Science ®Google Scholar
• Wang, C., Greene, D., Xiao, L., Qi, R., & Luo, R. (2017). Recent Developments and Applications of the MMPBSA Method. Frontiers in Molecular Biosciences, 4, 87. https://doi.org/10.3389/fmolb.2017.00087
   PubMed Web of Science ®Google Scholar
• Wong, S., Amaro, R. E., & McCammon, J. A. (2009). MM-PBSA captures key role of intercalating water molecules at a protein-protein interface. Journal of Chemical Theory and Computation, 5(2), 422–429. https://doi.org/10.1021/ct8003707
   PubMed Web of Science ®Google Scholar
• Zhang, L., Dutta, S., Xiong, S., Chan, M., Chan, K. K., Fan, T. M., Bailey, K. L., Lindeblad, M., Cooper, L. M., Rong, L., Gugliuzza, A. F., Shukla, D., Procko, E., Rehman, J., & Malik, A. B. (2022). Engineered ACE2 decoy mitigates lung injury and death induced by SARS-CoV-2 variants. Nature Chemical Biology, 18(3), 342–351. https://doi.org/10.1038/s41589-021-00965-6
   PubMed Web of Science ®Google Scholar
• Zhu, Y. X., Sheng, Y. J., Ma, Y. Q., & Ding, H. M. (2022). Assessing the performance of screening MM/PBSA in protein-ligand interactions. The Journal of Physical Chemistry. B, 126(8), 1700–1708. https://doi.org/10.1021/acs.jpcb.1c09424
   PubMed Web of Science ®Google Scholar