A systematic drug repurposing approach to identify promising inhibitors from FDA-approved drugs against Nsp4 protein of SARS-CoV-2

References

• Andersen, H. C. (1983). Rattle: A “velocity” version of the shake algorithm for molecular dynamics calculations. Journal of Computational Physics, 52(1), 24–34. https://doi.org/10.1016/0021-9991(83)90014-1
   Web of Science ®Google Scholar
• Beigel, J. H., Tomashek, K. M., Dodd, L. E., Mehta, A. K., Zingman, B. S., Kalil, A. C., Hohmann, E., Chu, H. Y., Luetkemeyer, A., Kline, S., Lopez de Castilla, D., Finberg, R. W., Dierberg, K., Tapson, V., Hsieh, L., Patterson, T. F., Paredes, R., Sweeney, D. A., Short, W. R., … Lane, H. C. (2020). Remdesivir for the treatment of Covid-19 — Final report. New England Journal of Medicine, 383(19), 1813–1826. https://doi.org/10.1056/NEJMoa2007764
   PubMed Web of Science ®Google Scholar
• Best, R. B., Zhu, X., Shim, J., Lopes, P. E. M., Mittal, J., Feig, M., & Mackerell, A. D. (2012). Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ(1) and χ(2) dihedral angles. Journal of Chemical Theory and Computation, 8(9), 3257–3273. https://doi.org/10.1021/ct300400x
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics, 126, 014101. https://doi.org/10.1063/1.2408420
   Google Scholar
• Chen, J., Wang, J., Xu, B., Zhu, W., & Li, G. (2011). Insight into mechanism of small molecule inhibitors of the MDM2-p53 interaction: Molecular dynamics simulation and free energy analysis. Journal of Molecular Graphics & Modelling, 30, 46–53. https://doi.org/10.1016/j.jmgm.2011.06.003
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science: A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• Di Leva, F., D'Adamo, P., Cubellis, M. V., D'Eustacchio, A., Errichiello, M., Saulino, C., Auletta, G., Giannini, P., Donaudy, F., Ciccodicola, A., Gasparini, P., Franzè, A., & Marciano, E. (2006). Identification of a novel mutation in the myosin VIIA motor domain in a family with autosomal dominant hearing loss (DFNA11). Audiology & Neuro-Otology, 11(3), 157–164. https://doi.org/10.1159/000091199
   PubMed Web of Science ®Google Scholar
• Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340
   PubMed Web of Science ®Google Scholar
• FDA. (2021a). Know your treatment for options COVID-19. https://www.fda.gov/consumers/consumer-updates/know-your-treatment-options-covid-19
   Google Scholar
• FDA. (2021b). Emergency use authorization. https://www.fda.gov/emergency-preparedness-and-response/mcm-legal-regulatory-and-policy-framework/emergency-use-authorization
   Google Scholar
• Gorbalenya, A. E., Baker, S. C., Baric, R. S., de Groot, R. J., Drosten, C., & Gulyaeva, A. A. (2020). The species severe acute respiratory syndrome-related coronavirus: Classifying 2019-nCoV and naming it SARS-CoV-2. Nature Microbiology, 5, 536–544. https://doi.org/10.1038/s41564-020-0695-z
   PubMed Web of Science ®Google Scholar
• Greenidge, P. A., Kramer, C., Mozziconacci, J. C., & Wolf, R. M. (2013). MM/GBSA binding energy prediction on the PDBbind data set: Successes, failures, and directions for further improvement. Journal of Chemical Information and Modeling, 53(1), 201–209. https://doi.org/10.1021/ci300425v
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38, 27–28. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jackson, L. A., Anderson, E. J., Rouphael, N. G., Roberts, P. C., Makhene, M., Coler, R. N., McCullough, M. P., Chappell, J. D., Denison, M. R., Stevens, L. J., Pruijssers, A. J., McDermott, A., Flach, B., Doria-Rose, N. A., Corbett, K. S., Morabito, K. M., O'Dell, S., Schmidt, S. D., Swanson, P. A., … Beigel, J. H. for the mRNA-1273 Study Group. (2020). An mRNA vaccine against SARS-CoV-2 – Preliminary report. The New England Journal of Medicine, 383(20), 1920–1931. https://doi.org/10.1056/NEJMoa2022483
   PubMed Web of Science ®Google Scholar
• Jain, S., & Vahdat, L. T. (2011). Eribulin mesylate. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 17(21), 6615–6622. https://doi.org/10.1158/1078-0432.CCR-11-1807
   PubMed Web of Science ®Google Scholar
• Kadioglu, O., Saeed, M., Greten, H. J., & Efferth, T. (2021). Identification of novel compounds against three targets of SARS CoV-2 coronavirus by combined virtual screening and supervised machine learning. Computers in Biology and Medicine, 133, 104359. https://doi.org/10.1016/j.compbiomed.2021.104359
   PubMed Web of Science ®Google Scholar
• Kalhotra, P., Chittepu, V. C. S. R., Osorio-Revilla, G., & Gallardo-Velazquez, T. (2021). Field-template, QSAR, ensemble molecular docking, and 3D-RISM solvation studies expose potential of FDA-approved marine drugs as SARS-CoVID-2 main protease inhibitors. Molecules, 26(4), 936. https://doi.org/10.3390/molecules26040936
   PubMed Web of Science ®Google Scholar
• Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845–858. https://doi.org/10.1038/nprot.2015-053
   PubMed Web of Science ®Google Scholar
• Kulkarni, S. A., Nagarajan, S. K., Ramesh, V., Palaniyandi, V., Selvam, S. P., & Madhavan, T. (2020). Computational evaluation of major components from plant essential oils as potent inhibitors of SARS-CoV-2 spike protein. Journal of Molecular Structure, 1221, 128823. https://doi.org/10.1016/j.molstruc.2020.128823
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Lee, M. S., Feig, M., Salsbury, F. R., & Brooks, C. L. (2003). New analytic approximation to the standard molecular volume definition and its application to generalized born calculations. Journal of Computational Chemistry, 24(11), 1348–1356. https://doi.org/10.1002/jcc.10272
   PubMed Web of Science ®Google Scholar
• Lin, F.-Y., & MacKerell, A. D. (2019). Improved modeling of halogenated ligand-protein interactions using the drude polarizable and CHARMM additive empirical force fields. Journal of Chemical Information and Modeling, 59(1), 215–228. https://doi.org/10.1021/acs.jcim.8b00616
   PubMed Web of Science ®Google Scholar
• Maity, A., Choudhury, A. R., & Chakrabarti, R. (2021). Effect of stapling on the thermodynamics of mdm2-p53 binding. Journal of Chemical Information and Modeling, 61(4), 1989–2000. https://doi.org/10.1021/acs.jcim.1c00219
   PubMed Web of Science ®Google Scholar
• Manolaridis, I., Wojdyla, J. A., Panjikar, S., Snijder, E. J., Gorbalenya, A. E., Berglind, H., Nordlund, P., Coutard, B., & Tucker, P. A. (2009). Structure of the C-terminal domain of nsp4 from feline coronavirus. Acta Crystallographica. Section D, Biological Crystallography, 65(Pt 8), 839–846. https://doi.org/10.1107/S0907444909018253
   PubMedGoogle Scholar
• Mark, P., & Nilsson, L. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. https://doi.org/10.1021/jp003020w
   Web of Science ®Google Scholar
• Messaoudi, A., Belguith, H., & Ben Hamida, J. (2013). Homology modeling and virtual screening approaches to identify potent inhibitors of VEB-1 β-lactamase. Theoretical Biology & Medical Modelling, 10, 1–10. https://doi.org/10.1186/1742-4682-10-22
   PubMed Web of Science ®Google Scholar
• Mulligan, M. J., Lyke, K. E., Kitchin, N., Absalon, J., Gurtman, A., Lockhart, S., Neuzil, K., Raabe, V., Bailey, R., Swanson, K. A., Li, P., Koury, K., Kalina, W., Cooper, D., Fontes-Garfias, C., Shi, P.-Y., Türeci, Ö., Tompkins, K. R., Walsh, E. E., … Jansen, K. U. (2020). Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults. Nature, 586(7830), 589–593. https://doi.org/10.1038/s41586-020-2639-4
   PubMed Web of Science ®Google Scholar
• Odhar, H. A., Ahjel, S. W., Albeer, A. A. M. A., Hashim, A. F., Rayshan, A. M., & Humadi, S. S. (2020). Molecular docking and dynamics simulation of FDA approved drugs with the main protease from 2019 novel coronavirus. Bioinformation, 16(3), 236–244. https://doi.org/10.6026/97320630016236
   PubMed Web of Science ®Google Scholar
• Oudshoorn, D., Rijs, K., Limpens, R. W. A. L., Groen, K., Koster, A. J., Snijder, E. J., Kikkert, M., & Bárcena, M. (2017). Expression and cleavage of Middle East respiratory syndrome coronavirus nsp3-4 polyprotein induce the formation of double-membrane vesicles that mimic those associated with coronaviral RNA replication. mBio, 8(6), 1–17. https://doi.org/10.1128/mBio.01658-17
   Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• Priya, P., Maity, A., Majumdar, S., & Ghosh Dastidar, S. (2015). Interactions between Bcl-xl and its inhibitors: Insights into ligand design from molecular dynamics simulation. Journal of Molecular Graphics & Modelling, 59, 1–13. https://doi.org/10.1016/j.jmgm.2015.02.005
   PubMed Web of Science ®Google Scholar
• Ramírez-Salinas, G. L., Martínez-Archundia, M., Correa-Basurto, J., & García-Machorro, J. (2020). Repositioning of ligands that target the spike glycoprotein as potential drugs for SARS-CoV-2 in an in silico study. Molecules, 25(23), 5615. https://doi.org/10.3390/molecules25235615
   PubMed Web of Science ®Google Scholar
• Rawat, K., Kumari, P., & Saha, L. (2021). COVID-19 vaccine: A recent update in pipeline vaccines, their design and development strategies. European Journal of Pharmacology, 892, 173751. https://doi.org/10.1016/j.ejphar.2020.173751
   PubMed Web of Science ®Google Scholar
• Robert, X., & Gouet, P. (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42, 320–324. https://doi.org/10.1093/nar/gku316
   PubMed Web of Science ®Google Scholar
• Salentin, S., Schreiber, S., Haupt, V. J., Adasme, M. F., & Schroeder, M. (2015). PLIP: Fully automated protein-ligand interaction profiler. Nucleic Acids Research, 43(W1), W443–W447. https://doi.org/10.1093/nar/gkv315
   PubMed Web of Science ®Google Scholar
• Sayers, E. W., Agarwala, R., Bolton, E. E., Brister, J. R., Canese, K., Clark, K., Connor, R., Fiorini, N., Funk, K., Hefferon, T., Holmes, J. B., Kim, S., Kimchi, A., Kitts, P. A., Lathrop, S., Lu, Z., Madden, T. L., Marchler-Bauer, A., Phan, L., … Ostell, J. (2019). Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 47(D1), D23–D28. https://doi.org/10.1093/nar/gky1069
   PubMed Web of Science ®Google Scholar
• Trott, O., & Olson, A. J. (2009). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31, 455–461. https://doi.org/10.1002/jcc.21334
   Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (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 Hemert, M. J., Van Den Worm, S. H. E., Knoops, K., Mommaas, A. M., Gorbalenya, A. E., & Snijder, E. J. (2008). SARS-coronavirus replication/transcription complexes are membrane-protected and need a host factor for activity in vitro. PLoS Pathogens, 4(5), e1000054. https://doi.org/10.1371/journal.ppat.1000054
   PubMed Web of Science ®Google Scholar
• Vanhoof, G., Goossens, F., De Meester, I., Hendriks, D., & Scharpé, S. (1995). Proline motifs in peptides and their biological processing. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 9(9), 736–744. https://doi.org/10.1096/fasebj.9.9.7601338
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Wallner, B., & Elofsson, A. (2003). Can correct protein models be identified? Protein Science: A Publication of the Protein Society, 12(5), 1073–1086. https://doi.org/10.1110/ps.0236803
   PubMed Web of Science ®Google Scholar
• Wang, M., Cao, R., Zhang, L., Yang, X., Liu, J., Xu, M., Shi, Z., Hu, Z., Zhong, W., & Xiao, G. (2020a). Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Research, 30(3), 269–271. https://doi.org/10.1038/s41422-020-0282-0
   PubMed Web of Science ®Google Scholar
• Wang, Y., Zhang, D., Du, G., Du, R., Zhao, J., Jin, Y., Fu, S., Gao, L., Cheng, Z., Lu, Q., Hu, Y., Luo, G., Wang, K., Lu, Y., Li, H., Wang, S., Ruan, S., Yang, C., Mei, C., … Wang, C. (2020b). Remdesivir in adults with severe COVID-19: A randomised, double-blind, placebo-controlled, multicentre trial. Lancet (London, England), 395(10236), 1569–1578. https://doi.org/10.1016/S0140-6736(20)31022-9
   PubMed Web of Science ®Google Scholar
• WHO. Coronavirus Disease. (2019). (COVID-19) situation reports. https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19–-18-may-2021
   Google Scholar
• Wiederstein, M., & Sippl, M. J. (2007). ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research, 35, 407–410. https://doi.org/10.1093/nar/gkm290
   PubMed Web of Science ®Google Scholar
• Winrow, C. J., Gotter, A. L., Cox, C. D., Doran, S. M., Tannenbaum, P. L., Breslin, M. J., Garson, S. L., Fox, S. V., Harrell, C. M., Stevens, J., Reiss, D. R., Cui, D., Coleman, P. J., & Renger, J. J. (2011). Promotion of sleep by suvorexant-a novel dual orexin receptor antagonist. Journal of Neurogenetics, 25(1–2), 52–61. https://doi.org/10.3109/01677063.2011.566953
   PubMed Web of Science ®Google Scholar
• Wymore, T., Hempel, J., Cho, S. S., MacKerell, A. D., Nicholas, H. B., & Deerfield, D. W. (2004). Molecular recognition of aldehydes by aldehyde dehydrogenase and mechanism of nucleophile activation. Proteins: Structure, Function and Genetics, 57(4), 758–771. https://doi.org/10.1002/prot.20256
   PubMed Web of Science ®Google Scholar
• Xu, X., Lou, Z., Ma, Y., Chen, X., Yang, Z., Tong, X., Zhao, Q., Xu, Y., Deng, H., Bartlam, M., & Rao, Z. (2009). Crystal structure of the C-terminal cytoplasmic domain of non-structural protein 4 from mouse hepatitis virus A59. PLoS One, 4(7), e6217. https://doi.org/10.1371/journal.pone.0006217
   PubMed Web of Science ®Google Scholar
• Xu, Z., Shi, L., Wang, Y., Zhang, J., Huang, L., Zhang, C., Liu, S., Zhao, P., Liu, H., Zhu, L., Tai, Y., Bai, C., Gao, T., Song, J., Xia, P., Dong, J., Zhao, J., & Wang, F.-S. (2020). Case report pathological findings of COVID-19 associated with acute respiratory distress syndrome. The Lancet Respiratory Medicine, 8(4), 420–422. https://doi.org/10.1016/S2213-2600(20)30076-X
   PubMed Web of Science ®Google Scholar
• Ye, Z. W., Yuan, S., Yuen, K. S., Fung, S. Y., Chan, C. P., & Jin, D. Y. (2020). Zoonotic origins of human coronaviruses. International Journal of Biological Sciences, 16(10), 1686–1697. https://doi.org/10.7150/ijbs.45472
   PubMed Web of Science ®Google Scholar
• Zhang, Z., Li, Y., Lin, B., Schroeder, M., & Huang, B. (2011). Identification of cavities on protein surface using multiple computational approaches for drug binding site prediction. Bioinformatics (Oxford, England), 27(15), 2083–2088. https://doi.org/10.1093/bioinformatics/btr331
   PubMed Web of Science ®Google Scholar