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Research Articles

Examining sialic acid derivatives as potential inhibitors of SARS-CoV-2 spike protein receptor binding domain

, , , , &
Pages 6342-6358 | Received 02 May 2023, Accepted 01 Jul 2023, Published online: 09 Jul 2023

References

  • Adhikary, P., Kandel, S., Mamani, U. F., Mustafa, B., Hao, S., Qiu, J., Fetse, J., Liu, Y., Ibrahim, N. M., Li, Y., Lin, C. Y., Omoscharka, E., & Cheng, K. (2021). Discovery of small anti-ACE2 peptides to inhibit SARS-CoV-2 infectivity. Advanced Therapeutics, 4(7), 2100087. https://doi.org/10.1002/adtp.202100087
  • Ali, A., & Vijayan, R. (2020). Dynamics of the ACE2-SARS-CoV-2/SARS-CoV spike protein interface reveal unique mechanisms. Scientific Reports, 10(1), 14214. https://doi.org/10.1038/s41598-020-71188-3
  • Aminpour, M., Cannariato, M., Zucco, A., Di Gregorio, E., Israel, S., Perioli, A., Tucci, D., Rossi, F., Pionato, S., Marino, S., Deriu, M. A., Velpula, K. K., & Tuszynski, J. A. (2021). Computational study of potential galectin-3 inhibitors in the treatment of COVID-19. Biomedicines, 9(9), 1208. https://doi.org/10.3390/biomedicines9091208
  • Baker, A. N., Richards, S. J., Guy, C. S., Congdon, T. R., Hasan, M., Zwetsloot, A. J., Gallo, A., Lewandowski, J. R., Stansfeld, P. J., Straube, A., Walker, M., Chessa, S., Pergolizzi, G., Dedola, S., Field, R. A., & Gibson, M. I. (2020). The SARS-COV-2 spike protein binds sialic acids and enables rapid detection in a lateral flow point of care diagnostic device. ACS Central Science, 6(11), 2046–2052. https://doi.org/10.1021/acscentsci.0c00855
  • Baker, E. N., & Hubbard, R. E. (1984). Hydrogen bonding in globular proteins. Progress in Biophysics and Molecular Biology, 44(2), 97–179. https://doi.org/10.1016/0079-6107(84)90007-5
  • Bera, K. (2022). Binding and inhibitory effect of ravidasvir on 3CLpro of SARS-CoV‐2: A molecular docking, molecular dynamics and MM/PBSA approach. Journal of Biomolecular Structure & Dynamics, 40(16), 7303–7310. https://doi.org/10.1080/07391102.2021.1896388
  • Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., Dinola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. J Chem Phys,.81(8), 3684–3690. https://doi.org/10.1063/1.448118
  • Bò, L., Miotto, M., Di Rienzo, L., Milanetti, E., & Ruocco, G. (2020). Exploring the association between sialic acid and SARS-CoV-2 spike protein through a molecular dynamics-based approach. Frontiers in Medical Technology, 2(614652), 614652. https://doi.org/10.3389/fmedt.2020.614652
  • Bongini, P., Trezza, A., Bianchini, M., Spiga, O., & Niccolai, N. (2020). A possible strategy to fight COVID-19: Interfering with spike glycoprotein trimerization. Biochemical and Biophysical Research Communications, 528(1), 35–38. https://doi.org/10.1016/j.bbrc.2020.04.007
  • Borea, P. A., Varani, K., Gessi, S., Gilli, P., & Dalpiaz, A. (1998). Receptor binding thermodynamics as a tool for linking drug efficacy and affinity. Farmaco (Societa Chimica Italiana : 1989), 53(4), 249–254. https://doi.org/10.1016/s0014-827x(98)00017-2
  • Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: the biomolecular simulation program. Journal of Computational Chemistry, 30(10), 1545–1614. https://doi.org/10.1002/jcc.21287
  • Buitrón-González, I., Aguilera-Durán, G., & Romo-Mancillas, A. (2021). In-silico drug repurposing study: amprenavir, enalaprilat, and plerixafor, potential drugs for destabilizing the SARS-CoV-2 S-protein-angiotensin-converting enzyme 2 complex. Results in Chemistry, 3(100094), 100094. https://doi.org/10.1016/j.rechem.2020.100094
  • Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
  • Cao, W., Dong, C., Kim, S., Hou, D., Tai, W., Du, L., Im, W., & Zhang, X. F. (2021). Biomechanical characterization of SARS-CoV-2 spike RBD and human ACE2 protein-protein interaction. Biophysical Journal, 120(6), 1011–1019. https://doi.org/10.1016/j.bpj.2021.02.007
  • Chen, D., Oezguen, N., Urvil, P., Ferguson, C., Dann, S. M., & Savidge, T. C. (2016). Regulation of protein-ligand binding affinity by hydrogen bond pairing. Science Advances, 2(3), e1501240. https://doi.org/10.1126/sciadv.1501240
  • Colizzi, F., Perozzo, R., Scapozza, L., Recanatini, M., & Cavalli, A. (2010). Single-molecule pulling simulations can discern active from inactive enzyme inhibitors. Journal of the American Chemical Society, 132(21), 7361–7371. https://doi.org/10.1021/ja100259r
  • Darden, T., Perera, L., Li, L., & Pedersen, L. (1999). New tricks for modelers from the crystallography toolkit: The particle mesh ewald algorithm and its use in nucleic acid simulations. Structure (London, England : 1993), 7(3), R55–R60. https://doi.org/10.1016/s0969-2126(99)80033-1
  • Day, C. J., Bailly, B., Guillon, P., Dirr, L., Jen, F. E. C., Spillings, B. L., Mak, J., von Itzstein, M., Haselhorst, T., & Jennings, M. P. (2021). Multidisciplinary approaches identify compounds that bind to human ACE2 or SARS-CoV-2 spike protein as candidates to block SARS-CoV-2–Ace2 receptor interactions. mBio, 12(2), e03681-20. https://doi.org/10.1128/mBio.03681-20
  • Drosten, C., Günther, S., Preiser, W., van der Werf, S., Brodt, H.-R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R. A. M., Berger, A., Burguière, A.-M., Cinatl, J., Eickmann, M., Escriou, N., Grywna, K., Kramme, S., Manuguerra, J.-C., Müller, S., … Doerr, H. W. (2003). Identification of a novel coronavirus in patients with severe acute respiratory syndrome. The New England Journal of Medicine, 348(20), 1967–1976. https://doi.org/10.1056/NEJMoa030747
  • Du, X., Li, Y., Xia, Y. L., Ai, S. M., Liang, J., Sang, P., Ji, X. L., & Liu, S. Q. (2016). Insights into protein–ligand interactions: mechanisms, models, and methods. International Journal of Molecular Sciences, 17(2), 144. https://doi.org/10.3390/ijms17020144
  • Ghahremanian, S., Rashidi, M. M., Raeisi, K., & Toghraie, D. (2022). Molecular Dynamics Simulation Approach for Discovering Potential Inhibitors against SARS-CoV-2: A Structural Review. Journal of Molecular Liquids, 354, 118901. https://doi.org/10.1016/j.molliq.2022.118901
  • Ghorbani, M., Brooks, B. R., & Klauda, J. B. (2021). Exploring dynamics and network analysis of spike glycoprotein of SARS-COV-2. Biophysical Journal, 120(14), 2902–2913. https://doi.org/10.1016/j.bpj.2021.02.047
  • Gil, C., Ginex, T., Maestro, I., Nozal, V., Barrado-Gil, L., Cuesta-Geijo, M. Á., Urquiza, J., Ramírez, D., Alonso, C., Campillo, N. E., & Martinez, A. (2020). COVID-19: drug targets and potential treatments. Journal of Medicinal Chemistry, 63(21), 12359–12386. https://doi.org/10.1021/acs.jmedchem.0c00606
  • Gilson, M. K., & Zhou, H. X. (2007). Calculation of protein-ligand binding affinities. Annual Review of Biophysics and Biomolecular Structure, 36, 21–42. https://doi.org/10.1146/annurev.biophys.36.040306.132550
  • Grant, O. C., Montgomery, D., Ito, K., & Woods, R. J. (2020). Analysis of the SARS-CoV-2 spike protein glycan shield reveals implications for immune recognition. Scientific Reports, 10(1), 14991. https://doi.org/10.1038/s41598-020-71748-7
  • Guo, Y. R., Cao, Q. D., Hong, Z. S., Tan, Y. Y., Chen, S. D., Jin, H. J., Tan, K. S., Wang, D. Y., & Yan, Y. (2020). The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) Outbreak- an update on the status. Military Medical Research, 7(1), 11. https://doi.org/10.1186/s40779-020-00240-0
  • 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
  • Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review A, General Physics, 31(3), 1695–1697. https://doi.org/10.1103/physreva.31.1695
  • 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
  • Irani, A. H., Steyn-Ross, D. A., Steyn-Ross, M. L., Voss, L., & Sleigh, J. (2022). The molecular dynamics of possible inhibitors for SARS-CoV-2. Journal of Biomolecular Structure & Dynamics, 40(20), 10023–10032. https://doi.org/10.1080/07391102.2021.1942215
  • 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. https://doi.org/10.1002/jcc.20945
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. J Chem Phys,.79(2), 926–935. https://doi.org/10.1063/1.445869
  • Karimi Alavijeh, M., Meyer, A. S., Gras, S. L., & Kentish, S. E. (2020). Simulation and economic assessment of large-scale enzymatic N-acetyllactosamine manufacture. Biochem Eng J,.154, 107459. https://doi.org/10.1016/j.bej.2019.107459
  • Karimi Alavijeh, M., Meyer, A. S., Gras, S. L., & Kentish, S. E. (2021). Synthesis of N-acetyllactosamine and N-acetyllactosamine-based bioactives. Journal of Agricultural and Food Chemistry, 69(27), 7501–7525. https://doi.org/10.1021/acs.jafc.1c00384
  • Kim, S., Liu, Y., Lei, Z., Dicker, J., Cao, Y., Zhang, X. F., & Im, W. (2021). Differential interactions between human ACE2 and Spike RBD of SARS-CoV-2 variants of concern. Journal of Chemical Theory and Computation, 17(12), 7972–7979. https://doi.org/10.1021/acs.jctc.1c00965
  • Koirala, R. P., Thapa, B., Khanal, S. P., Powrel, J., Adhikari, R. P., & Adhikari, N. P. (2021). Binding of SARS-CoV-2/SARS-CoV spike protein with human ACE2 receptor. Journal of Physics Communications, 5(3), 035010. https://doi.org/10.1088/2399-6528/abea27
  • Ksiazek, T. G., Erdman, D., Goldsmith, C. S., Zaki, S. R., Peret, T., Emery, S., Tong, S., Urbani, C., Comer, J. A., Lim, W., Rollin, P. E., Dowell, S. F., Ling, A.-E., Humphrey, C. D., Shieh, W.-J., Guarner, J., Paddock, C. D., Rota, P., Fields, B., … Anderson, L. J, SARS Working Group. (2003). A novel coronavirus associated with severe acute respiratory syndrome. The New England Journal of Medicine, 348(20), 1953–1966. https://doi.org/10.1056/NEJMoa030781
  • Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A., & Rosenberg, J. M. (1992). The weighted histogram analysis method for free-energy calculations on biomolecules. I. The Method. Journal of Computational Chemistry, 13(8), 1011–1021. https://doi.org/10.1002/jcc.540130812
  • Lemkul, J. A., & Bevan, D. R. (2010). Assessing the stability of alzheimer’s amyloid protofibrils using molecular dynamics. The Journal of Physical Chemistry. B, 114(4), 1652–1660. https://doi.org/10.1021/jp9110794
  • Li, B., Wang, L., Ge, H., Zhang, X., Ren, P., Guo, Y., Chen, W., Li, J., Zhu, W., Chen, W., Zhu, L., & Bai, F. (2021). Identification of potential binding sites of sialic acids on the RBD domain of SARS-CoV-2 spike protein. Frontiers in Chemistry, 9(349), 659764. https://doi.org/10.3389/fchem.2021.659764
  • Li, F., Li, W., Farzan, M., & Harrison, S. C. (2005). Structural biology: Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science (New York, N.Y.), 309(5742), 1864–1868. https://doi.org/10.1126/science.1116480
  • Limongelli, V. (2020). Ligand binding free energy and kinetics calculation in 2020. WIREs Computational Molecular Science, 10(4), e1455. https://doi.org/10.1002/wcms.1455
  • 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
  • Liu, D. X., Liang, J. Q., Fung, T. S., & Human, C.-2. (2021). OC43, -NL63, and -HKU1 (Coronaviridae); Elsevier. Encyclopedia of Virology, 2021, 428–440. https://doi.org/10.1016/b978-0-12-809633-8.21501-x
  • 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[
  • Lupala, C. S., Li, X., Lei, J., Chen, H., Qi, J., Liu, H., & Su, X.-D. (2021). Computational simulations reveal the binding dynamics between human ACE2 and the receptor binding domain of SARS-CoV-2 spike protein. Quantitative Biology, 9(1), 61–72. https://doi.org/10.15302/J-QB-020-0231
  • Malykh, Y. N., Schauer, R., & Shaw, L. (2001). N-glycolylneuraminic acid in human tumours. Biochimie, 83(7), 623–634. https://doi.org/10.1016/s0300-9084(01)01303-7
  • Miyagi, T., & Yamaguchi, K. (2007). Sialic acids. Comprehensive Glycoscience: From Chemistry to Systems Biology, 3(4), 297–323. https://doi.org/10.1016/b978-044451967-2/00055-6
  • Mohammed Ali, H. S. H., Altayb, H. N., Bayoumi, A. A. M., El Omri, A., Firoz, A., & Chaieb, K. (2023). In silico screening of the effectiveness of natural compounds from algae as SARS-CoV-2 inhibitors: molecular docking, ADMT profile and molecular dynamic studies. Journal of Biomolecular Structure & Dynamics, 41(7), 3129–3144. https://doi.org/10.1080/07391102.2022.2046640
  • Morris, G. M., Ruth, H., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
  • Mosquera-Yuqui, F., Lopez-Guerra, N., & Moncayo-Palacio, E. A. (2022). Targeting the 3CLpro and RdRp of SARS-CoV-2 with phytochemicals from medicinal plants of the andean region: molecular docking and molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 40(5), 2010–2023. https://doi.org/10.1080/07391102.2020.1835716
  • Münster, A. K., Eckhardt, M., Potvin, B., Mühlenhoff, M., Stanley, P., & Gerardy-Schahn, R. (1998). Mammalian cytidine 5′-monophosphate N-acetylneuraminic acid synthetase: A nuclear protein with evolutionary conserved structural motifs. Proceedings of the National Academy of Sciences of the United States of America, 95(16), 9140–9145. https://doi.org/10.1073/pnas.95.16.9140
  • Murphy, B. R., Alling, D. W., Snyder, M. H., Walsh, E. E., Prince, G. A., Chanock, R. M., Hemming, V. G., Rodriguez, W. J., Kim, H. W., & Graham, B. S. (1986). Effect of age and preexisting antibody on serum antibody response of infants and children to the F and G glycoproteins during respiratory syncytial virus infection. Journal of Clinical Microbiology, 24(5), 894–898. https://doi.org/10.1128/jcm.24.5.894-898.1986
  • Ngo, V. A., & Jha, R. K. (2021). Identifying key determinants and dynamics of SARS-CoV-2/ACE2 tight interaction. PLoS One, 16(9), e0257905. https://doi.org/10.1371/journal.pone.0257905
  • Nguyen, H. L., Thai, N. Q., Truong, D. T., & Li, M. S. (2020). Remdesivir strongly binds to both RNA-dependent RNA polymerase and main protease of SARS-COV-2: Evidence from molecular simulations. The Journal of Physical Chemistry. B, 124(50), 11337–11348. https://doi.org/10.1021/acs.jpcb.0c07312
  • Nguyen, L., McCord, K. A., Bui, D. T., Bouwman, K. M., Kitova, E. N., Elaish, M., Kumawat, D., Daskhan, G. C., Tomris, I., Han, L., Chopra, P., Yang, T. J., Willows, S. D., Mason, A. L., Mahal, L. K., Lowary, T. L., West, L. J., Hsu, S. T. D., Hobman, T., … Klassen, J. S. (2022). Sialic acid-containing glycolipids mediate binding and viral entry of SARS-CoV-2. Nature Chemical Biology, 18(1), 81–90. https://doi.org/10.1038/s41589-021-00924-1
  • Nosé, S. (1984). A unified formulation of the constant temperature molecular dynamics methods. J Chem Phys,.81(1), 511–519. https://doi.org/10.1063/1.447334
  • Panigrahi, S. K., & Desiraju, G. R. (2007). Strong and weak hydrogen bonds in the protein-ligand interface. Proteins: Structure, Function and Genetics, 67(1), 128–141. https://doi.org/10.1002/prot.21253
  • Park, S. J., & Seo, M. K. (2011). Solid-solid interfaces. Interface Science and Technology, 18, 253–331. https://doi.org/10.1016/B978-0-12-375049-5.00004-9
  • Parrinello, M., & Rahman, A. (1980). Crystal structure and pair potentials: a molecular-dynamics study. Physical Review Letters, 45(14), 1196–1199. https://doi.org/10.1103/PhysRevLett.45.1196
  • Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: a new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
  • Qing, E., Hantak, M., Perlman, S., & Gallagher, T. (2020). Distinct roles for sialoside and protein receptors in coronavirus infection. mBio, 11(1), e02764-19. https://doi.org/10.1128/mBio.02764-19
  • Robson, B. (2020). Bioinformatics studies on a function of the SARS-CoV-2 Spike glycoprotein as the binding of host sialic acid glycans. Computers in Biology and Medicine, 122, 103849. https://doi.org/10.1016/j.compbiomed.2020.103849
  • Roux, B. (1995). The calculation of the potential of mean force using computer Simulations. Comput Phys Commun,.91(1-3), 275–282. https://doi.org/10.1016/0010-4655(95)00053-I
  • Sakkiah, S., Guo, W., Pan, B., Ji, Z., Yavas, G., Azevedo, M., Hawes, J., Patterson, T. A., & Hong, H. (2021). Elucidating interactions between sars-cov-2 trimeric spike protein and ACE2 using homology modeling and molecular dynamics simulations. Frontiers in Chemistry, 8, 1247. https://doi.org/10.3389/fchem.2020.622632
  • Salentin, S., Haupt, V. J., Daminelli, S., & Schroeder, M. (2014). Polypharmacology rescored: protein-ligand interaction profiles for remote binding site similarity assessment. Progress in Biophysics and Molecular Biology, 116(2-3), 174–186. https://doi.org/10.1016/j.pbiomolbio.2014.05.006
  • Steinbrecher, T., & Labahn, A. (2010). Towards accurate free energy calculations in ligand protein-binding studies. Current Medicinal Chemistry, 17(8), 767–785. https://doi.org/10.2174/092986710790514453
  • Suan Li, M., & Khanh Mai, B. (2012). Steered molecular dynamics-a promising tool for drug design. Current Bioinformatics, 7(4), 342–351. https://doi.org/10.2174/157489312803901009
  • Sui, J., Li, W., Murakami, A., Tamin, A., Matthews, L. J., Wong, S. K., Moore, M. J., Tallarico, A. S. C., Olurinde, M., Choe, H., Anderson, L. J., Bellini, W. J., Farzan, M., & Marasco, W. A. (2004). Potent neutralization of Severe Acute Respiratory Syndrome (SARS) coronavirus by a human MAB to S1 protein that blocks receptor association. Proceedings of the National Academy of Sciences of the United States of America, 101(8), 2536–2541. https://doi.org/10.1073/pnas.0307140101
  • Suleman, M., Yousafi, Q., Ali, J., Ali, S. S., Hussain, Z., Ali, S., Waseem, M., Iqbal, A., Ahmad, S., Khan, A., Wang, Y., & Wei, D. Q. (2021). Bioinformatics analysis of the differences in the binding profile of the wild-type and mutants of the SARS-CoV-2 spike protein variants with the ACE2 receptor. Computers in Biology and Medicine, 138, 104936. https://doi.org/10.1016/j.compbiomed.2021.104936
  • Sun, F., Li, P., Ding, Y., Wang, L., Bartlam, M., Shu, C., Shen, B., Jiang, H., Li, S., & Rao, Z. (2003). Design and structure-based study of new potential FKBP12 inhibitors. Biophysical Journal, 85(5), 3194–3201. https://doi.org/10.1016/S0006-3495(03)74737-7
  • Sun, X.-L. (2021). The role of cell surface sialic acids for SARS-CoV-2 infection. Glycobiology, 31(10), 1245–1253. https://doi.org/10.1093/glycob/cwab032
  • Tan, K. P., Singh, K., Hazra, A., & Madhusudhan, M. S. (2021). Peptide bond planarity constrains hydrogen bond geometry and influences secondary structure conformations. Current Research in Structural Biology, 3, 1–8. https://doi.org/10.1016/j.crstbi.2020.11.002
  • 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
  • Tortorici, M. A., Walls, A. C., Lang, Y., Wang, C., Li, Z., Koerhuis, D., Boons, G. J., Bosch, B. J., Rey, F. A., de Groot, R. J., & Veesler, D. (2019). Structural basis for human coronavirus attachment to sialic acid receptors. Nature Structural & Molecular Biology, 26(6), 481–489. https://doi.org/10.1038/s41594-019-0233-y
  • Trezza, A., Iovinelli, D., Santucci, A., Prischi, F., & Spiga, O. (2020). An integrated drug repurposing strategy for the rapid identification of potential SARS-CoV-2 VIRAL INHIBITORS. Scientific Reports, 10(1), 13866. https://doi.org/10.1038/s41598-020-70863-9
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
  • Troyano-Hernáez, P., Reinosa, R., & Holguín, Á. (2021). Evolution of SARS-CoV-2 envelope, membrane, nucleocapsid, and spike structural proteins from the beginning of the pandemic to september 2020: A global and regional approach by epidemiological week. Viruses, 13(2), 243–258. https://doi.org/10.3390/v13020243
  • Truong, D. T., & Li, M. S. (2018). Probing the binding affinity by jarzynski’s nonequilibrium binding free energy and rupture time. The Journal of Physical Chemistry. B, 122(17), 4693–4699. https://doi.org/10.1021/acs.jpcb.8b02137
  • Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. https://doi.org/10.1002/jcc.21367
  • Wang, Q., Wang, Y., Yang, S., Lin, C., Aliyu, L., Chen, Y., Parsons, L., Tian, Y., Jia, H., Pekosz, A., Betenbaugh, M. J., & Cipollo, J. F. (2021). A linkage-specific sialic acid labeling strategy reveals different site-specific glycosylation patterns in SARS-CoV-2 spike protein produced in CHO and HEK cell substrates. Frontiers in Chemistry, 9, 735558. https://doi.org/10.3389/fchem.2021.735558
  • Wen, L., Zheng, Y., Li, T., & Wang, P. G. (2016). Enzymatic synthesis of 3-Deoxy-d-Manno-Octulosonic Acid (KDO) and its application for LPS assembly. Bioorganic & Medicinal Chemistry Letters, 26(12), 2825–2828. https://doi.org/10.1016/j.bmcl.2016.04.061
  • WHO. (2020). WHO Director-General’s opening remarks at the media briefing on COVID-19–11. https://www.who.int/director-general/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19–11-march-2020
  • WHO. (2021). WHO Coronavirus (COVID-19) Dashboard with Vaccination Data. https://covid19.who.int/
  • Woo, H. J., & Roux, B. (2005). Calculation of absolute protein-ligand binding free energy from computer simulations. Proceedings of the National Academy of Sciences of the United States of America, 102(19), 6825–6830. https://doi.org/10.1073/pnas.0409005102
  • 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 (New York, N.Y.), 367(6483), 1260–1263. https://doi.org/10.1126/science.abb2507
  • Xiang, Y., Nambulli, S., Xiao, Z., Liu, H., Sang, Z., Duprex, W. P., Schneidman-Duhovny, D., Zhang, C., & Shi, Y. (2020). Versatile and multivalent nanobodies efficiently neutralize SARS-CoV-2. Science (New York, N.Y.), 370(6523), 1479–1484. https://doi.org/10.1126/science.abe4747
  • Yan, R., Zhang, Y., Li, Y., Xia, L., Guo, Y., & Zhou, Q. (2020). Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science (New York, N.Y.), 367(6485), 1444–1448. https://doi.org/10.1126/science.abb2762
  • Yang, J., Petitjean, S. J. L., Koehler, M., Zhang, Q., Dumitru, A. C., Chen, W., Derclaye, S., Vincent, S. P., Soumillion, P., & Alsteens, D. (2020). Molecular interaction and inhibition of SARS-CoV-2 binding to the ACE2 receptor. Nature Communications, 11(1), 4541. https://doi.org/10.1038/s41467-020-18319-6
  • Yousefi, N., Yazdani-Jahromi, M., Tayebi, A., Kolanthai, E., Neal, C. J., Banerjee, T., Gosai, A., Balasubramanian, G., Seal, S., & Garibay, O. O. (2023). BindingSiteAugmentedDTA: enabling a next-generation pipeline for interpretable prediction models in drug-repurposing. Briefings in Bioinformatics, 24(3), 1–13. https://doi.org/10.1093/bib/bbad136
  • Zaki, A. M., van Boheemen, S., Bestebroer, T. M., Osterhaus, A. D. M. E., & Fouchier, R. A. M. (2012). Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. The New England Journal of Medicine, 367(19), 1814–1820. https://doi.org/10.1056/NEJMoa1211721

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