Structural insight into the binding interactions of NTPs and nucleotide analogues to RNA dependent RNA polymerase of SARS-CoV-2

References

• Aftab, S. O., Ghouri, M. Z., Masood, M. U., Haider, Z., Khan, Z., Ahmad, A., & Munawar, N. (2020). Analysis of SARS-CoV-2 RNA-dependent RNA polymerase as a potential therapeutic drug target using a computational approach. Journal of Translational Medicine, 18(1), 275. https://doi.org/10.1186/s12967-020-02439-0
   PubMed Web of Science ®Google Scholar
• Allen, W. J., Balius, T. E., Mukherjee, S., Brozell, S. R., Moustakas, D. T., Lang, P. T., Case, D. A., Kuntz, I. D., & Rizzo, R. C. (2015). DOCK 6: Impact of new features and current docking performance. Journal of Computational Chemistry, 36(15), 1132–1156. https://doi.org/10.1002/jcc.23905
   PubMed Web of Science ®Google Scholar
• Appleby, T. C., Perry, J. K., Murakami, E., Barauskas, O., Feng, J., Cho, A., Fox, D., III, Wetmore, D. R., McGrath, M. E., Ray, A. S., Sofia, M. J., Swaminathan, S., & Edwards, T. E. (2015). Viral replication. Structural basis for RNA replication by the hepatitis C virus polymerase. Science (New York, N.Y.), 347(6223), 771–775. https://doi.org/10.1126/science.1259210
   PubMed Web of Science ®Google Scholar
• Balasubramaniam, M., & Reis, R. J. S. (2020). Computational target-based drug repurposing of elbasvir, an antiviral drug predicted to bind multiple SARS-CoV-2 proteins. ChemRxiv [Preprint]. https://doi.org/10.26434/chemrxiv.12084822
   Google Scholar
• Cattaneo, D., Capetti, A., & Rizzardini, G. (2019). Drug-drug interactions of a two-drug regimen of dolutegravir and lamivudine for HIV treatment. Expert Opinion on Drug Metabolism & Toxicology, 15(3), 245–252. https://doi.org/10.1080/17425255.2019.1577821
   PubMed Web of Science ®Google Scholar
• Chien, M., Anderson, T. K., Jockusch, S., Tao, C., Li, X., Kumar, S., Russo, J. J., Kirchdoerfer, R. N., & Ju, J. (2020). Nucleotide analogues as Inhibitors of SARS-CoV-2 polymerase, a key drug target for COVID-19. Journal of Proteome Research, 19(11), 4690-4697. https://doi.org/10.1021/acs.jproteome.0c00392
   Google Scholar
• Chodera, J. D., & Noé, F. (2014). Markov state models of biomolecular conformational dynamics. Current Opinion in Structural Biology, 25,135-144. https://doi.org/10.1016/j.sbi.2014.04.002
   Google Scholar
• Chodera, J. D., Singhal, N., Pande, V. S., Dill, K. A., & Swope, W. C. (2007). Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics. The Journal of Chemical Physics, 126(15), 155101–17461665. https://doi.org/10.1063/1.2714538
   PubMed Web of Science ®Google Scholar
• Case, D. A., Betz, R. M., Cerutti, D. S., Cheatham III, T. E., Darden, T. A., Duke, R. E., Giese, T. J., Gohlke, H., Goetz, A. W., Homeyer, N., Izadi, S., Janowski, P., Kaus, J., Kovalenko, A., Lee, T. S., LeGrand, S., Li, P., Lin, C., Luchko, T., … Kollman, P. A. (2016). AMBER 2016. University of California.
   Google Scholar
• De Clercq E. (2019). New nucleoside analogues for the treatment of hemorrhagic fever virus infections. Chemistry: An Asian Journal, 14(22), 3962-3968. https://doi.org/10.1002/asia.201900841
   Google Scholar
• Delang, L., Abdelnabi, R., & Neyts, J. (2018). Favipiravir as a potential countermeasure against neglected and emerging RNA viruses. Antiviral Research, 153, 85–94. https://doi.org/10.1016/j.antiviral.2018.03.003
   PubMed Web of Science ®Google Scholar
• Elfiky, A. A. (2020a). Ribavirin, Remdesivir, Sofosbuvir, Galidesivir, and Tenofovir against SARS-CoV-2 RNA dependent RNA polymerase (RdRp): A molecular docking study. Life Sciences, 253, 117592. https://doi.org/10.1016/j.lfs.2020.117592
   PubMed Web of Science ®Google Scholar
• Elfiky, A. A. (2020b). SARS-CoV-2 RNA dependent RNA polymerase (RdRp) targeting: an in silico perspective. Journal of Biomolecular Structure and Dynamics, 1-9. https://doi.org/10.1080/07391102.2020.1761882.
   Google Scholar
• Furuta, Y., Komeno, T., & Nakamura, T. (2017). Favipiravir (T-705), a broad spectrum inhibitor of viral RNA polymerase. Proceedings of the Japan Academy, Series B, 93(7), 449–463. https://doi.org/10.2183/pjab.93.027
   Google Scholar
• Gao, Y., Yan, L., Huang, Y., Liu, F., Zhao, Y., Cao, L., Wang, T., Sun, Q., Ming, Z., Zhang, L., Ge, J., Zheng, L., Zhang, Y., Wang, H., Zhu, Y., Zhu, C., Hu, T., Hua, T., Zhang, B., Yang, X., … Rao, Z. (2020). Structure of the RNA-dependent RNA polymerase from COVID-19 virus. Science (New York, N.Y.), 368(6492), 779–782. https://doi.org/10.1126/science.abb7498
   PubMed Web of Science ®Google Scholar
• Gaurav, A., & Al-Nema, M. (2019). Polymerases of coronaviruses: structure, function, and inhibitors. In Viral polymerases (pp. 271-300). Academic Press.
   Google Scholar
• Gordon, C. J., Tchesnokov, E. P., Woolner, E., Perry, J. K., Feng, J. Y., Porter, D. P., & Götte, M. (2020). Remdesivir is a direct-acting antiviral that inhibits RNA-dependent RNA polymerase from severe acute respiratory syndrome coronavirus 2 with high potency. The Journal of Biological Chemistry, 295(20), 6785–6797. https://doi.org/10.1074/jbc.RA120.013679
   PubMed Web of Science ®Google Scholar
• Graham, R. L., Donaldson, E. F., & Baric, R. S. (2013). A decade after SARS: Strategies for controlling emerging coronaviruses. Nature Reviews. Microbiology, 11(12), 836–848. https://doi.org/10.1038/nrmicro3143
   PubMed Web of Science ®Google Scholar
• Hemida, M. G., Chu, D. K. W., Perera, R. A. P. M., Ko, R. L. W., So, R. T. Y., Ng, B. C. Y., Chan, S. M. S., Chu, S., Alnaeem, A. A., Alhammadi, M. A., Webby, R. J., Poon, L. L. M., Balasuriya, U. B. R., & Peiris, M. (2017). Coronavirus infections in horses in Saudi Arabia and Oman. Transboundary and Emerging Diseases, 64(6), 2093–2103. https://doi.org/10.1111/tbed.12630
   PubMed Web of Science ®Google Scholar
• Jácome, R., Campillo-Balderas, J. A., Ponce de León, S., Becerra, A., & Lazcano, A. (2020). Sofosbuvir as a potential alternative to treat the SARS-CoV-2 epidemic. Scientific Reports, 10(1), 9294. https://doi.org/10.1038/s41598-020-66440-9
   PubMed Web of Science ®Google Scholar
• Jani, V., Sonavane, U., & Joshi, R. (2019). Detecting early stage structural changes in wild type, pathogenic and non-pathogenic prion variants using Markov state model. RSC Advances, 9(25), 14567–14579. https://doi.org/10.1039/C9RA01507H
   PubMed Web of Science ®Google Scholar
• Jia, H., & Gong, P. (2019). A structure-function diversity survey of the RNA-dependent RNA polymerases from the positive-strand RNA viruses. Frontiers in Microbiology, 10, 1945. https://doi.org/10.3389/fmicb.2019.01945
   PubMed Web of Science ®Google Scholar
• Khalili, J. S., Zhu, H., Mak, N. S. A., Yan, Y., & Zhu, Y. (2020). Novel coronavirus treatment with ribavirin: Groundwork for an evaluation concerning COVID-19. Journal of Medical Virology, 92(7), 740–746. https://doi.org/10.1002/jmv.25798
   PubMed Web of Science ®Google Scholar
• Kim, Y., Cheon, S., Min, C.-K., Sohn, K. M., Kang, Y. J., Cha, Y.-J., Kang, J.-I., Han, S. K., Ha, N.-Y., Kim, G., Aigerim, A., Shin, H. M., Choi, M.-S., Kim, S., Cho, H.-S., Kim, Y.-S., & Cho, N.-H. (2016). Spread of mutant middle east respiratory syndrome coronavirus with reduced affinity to human CD26 during the South Korean outbreak. mBio, 7(2), e00019. https://doi.org/10.1128/mBio.00019-16
   PubMed Web of Science ®Google Scholar
• Konkolova, E., Dejmek, M., Hřebabecký, H., Šála, M., Böserle, J., Nencka, R., & Boura, E. (2020). Remdesivir triphosphate can efficiently inhibit the RNA-dependent RNA polymerase from various flaviviruses. Antiviral Research, 182, 104899. https://doi.org/10.1016/j.antiviral.2020.104899
   PubMed Web of Science ®Google Scholar
• Koulgi, S., Jani, V., Uppuladinne, V. N. M., Sonavane, U., & Joshi, R. (2020). Remdesivir-bound and ligand-free simulations reveal the probable mechanism of inhibiting the RNA dependent RNA polymerase of severe acute respiratory syndrome coronavirus 2. RSC Advances, 10(45), 26792–26803. https://doi.org/10.1039/D0RA04743K
   PubMed Web of Science ®Google Scholar
• Ko, W. C., Rolain, J. M., Lee, N. Y., Chen, P. L., Huang, C. T., Lee, P. I., & Hsueh, P. R. (2020). Arguments in favour of remdesivir for treating SARS-CoV-2 infections. International Journal of Antimicrobial Agents, 55(4), 105933. https://doi.org/10.1016/j.ijantimicag.2020.105933
   PubMed Web of Science ®Google Scholar
• Ledford, H. (2020). Hopes rise for coronavirus drug remdesivir. Nature. https://doi.org/10.1038/d41586-020-01295-8
   Google Scholar
• Liang, C., Tian, L., Liu, Y., Hui, N., Qiao, G., Li, H., Shi, Z., Tang, Y., Zhang, D., Xie, X., & Zhao, X. (2020). A promising antiviral candidate drug for the COVID-19 pandemic: A mini-review of remdesivir. European Journal of Medicinal Chemistry, 201, 112527. https://doi.org/10.1016/j.ejmech.2020.112527
   PubMed Web of Science ®Google Scholar
• Lim, Y. X., Ng, Y. L., Tam, J. P., & Liu, D. X. (2016). Human coronaviruses: A review of virus-host interactions. Diseases, 4(4), 26. https://doi.org/10.3390/diseases4030026
   PubMedGoogle Scholar
• Li, Z., Wang, X., Cao, D., Sun, R., Li, C., & Li, G. (2020). Rapid review for the anti-coronavirus effect of remdesivir. Drug Discoveries & Therapeutics, 14(2), 73–76. https://doi.org/10.5582/ddt.2020.01015
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). Simmerling C. 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
• Miller, B. R., McGee, T. D., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Scherer, M. K., Trendelkamp-Schroer, B., Paul, F., Pérez-Hernández, G., Hoffmann, M., Plattner, N., Wehmeyer, C., Prinz, J.-H., & Noé, F. (2015). PyEMMA 2: A software package for estimation, validation, and analysis of Markov models. Journal of Chemical Theory and Computation, 11(11), 5525–5542. https://doi.org/10.1021/acs.jctc.5b00743
   PubMed Web of Science ®Google Scholar
• Moustafa, I. M., Shen, H., Morton, B., Colina, C. M., & Cameron, C. E. (2011). Molecular dynamics simulations of viral RNA polymerases link conserved and correlated motions of functional elements to fidelity. Journal of Molecular Biology, 410(1), 159–181. https://doi.org/10.1016/j.jmb.2011.04.078
   PubMed Web of Science ®Google Scholar
• Parang, K., El-Sayed, N. S., Kazeminy, A. J., & Tiwari, R. K. (2020). Comparative antiviral activity of Remdesivir and anti-HIV nucleoside analogs against human coronavirus 229E (HCoV-229E). Molecules, 25(10), 2343. https://doi.org/10.3390/molecules25102343
   Web of Science ®Google Scholar
• Pene, F., Merlat, A., Vabret, A., Rozenberg, F., Buzyn, A., Dreyfus, F., Cariou, A., Freymuth, F., & Lebon, P. (2003). Coronavirus 229E-related pneumonia in immunocompromised patients. Clinical Infectious Diseases, 37(7), 929–932. https://doi.org/10.1086/377612
   PubMed Web of Science ®Google Scholar
• Peters, M. B., Yang, Y., Wang, B., Füsti-Molnár, L., Weaver, M. N., & Merz, K. M. Jr. (2010). Structural survey of zinc containing proteins and the development of the zinc AMBER force field (ZAFF). Journal of Chemical Theory and Computation, 6(9), 2935–2947. https://doi.org/10.1021/ct1002626
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Prajapat, M., Sarma, P., Shekhar, N., Prakash, A., Avti, P., Bhattacharyya, A., Kaur, H., Kumar, S., Bansal, S., Sharma, A. R., & Medhi, B. (2020). Update on the target structures of SARS-CoV-2: A systematic review. Indian Journal of Pharmacology, 52(2), 142–149. https://doi.org/10.4103/ijp.IJP_338_20
   PubMed Web of Science ®Google Scholar
• Prinz, J. H., Wu, H., Sarich, M., Keller, B., Senne, M., Held, M., Chodera, J. D., Schütte, C., & Noé, F. (2011). Markov models of molecular kinetics: Generation and validation. The Journal of Chemical Physics, 134(17), 174105. https://doi.org/10.1063/1.3565032
   PubMed Web of Science ®Google Scholar
• R Core Team. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Austria.
   Google Scholar
• Roe, D. R., & Cheatham, T. E. (2018). Parallelization of CPPTRAJ enables large scale analysis of molecular dynamics trajectory data. Journal of Computational Chemistry, 39(25), 2110–2117. https://doi.org/10.1002/jcc.25382
   PubMed Web of Science ®Google Scholar
• Ruan, Z., Liu, C., Guo, Y., He, Z., Huang, X., Jia, X., & Yang, T. (2021). SARS-CoV-2 and SARS-CoV: Virtual screening of potential inhibitors targeting RNA-dependent RNA polymerase activity (NSP12). Journal of Medical Virology, 93(1), 389-400. https://doi.org/10.1002/jmv.26222
   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), W443–7. https://doi.org/10.1093/nar/gkv315
   PubMed Web of Science ®Google Scholar
• Sirur, A., De Sancho, D., & Best, R. B. (2016). Markov state models of protein misfolding. The Journal of Chemical Physics, 144(7), 075101. https://doi.org/10.1063/1.4941579
   PubMed Web of Science ®Google Scholar
• Srinivasan, S., Cui, H., Gao, Z., Liu, M., Lu, S., Mkandawire, W., Narykov, O., Sun, M., & Korkin, D. (2020). Structural genomics of SARS-CoV-2 indicates evolutionary conserved functional regions of viral proteins. Viruses, 12(4), 360. https://doi.org/10.3390/v12040360
   PubMed Web of Science ®Google Scholar
• Tchesnokov, E. P., Feng, J. Y., Porter, D. P., & Götte, M. (2019). Mechanism of inhibition of ebola virus RNA-dependent RNA polymerase by Remdesivir. Viruses, 11(4), 326. https://doi.org/10.3390/v11040326
   PubMed Web of Science ®Google Scholar
• Thompson, A. A., Albertini, R. A., & Peersen, O. B. (2007). Stabilization of poliovirus polymerase by NTP binding and fingers-thumb interactions. Journal of Molecular Biology, 366(5), 1459-1474. https://doi.org/10.1016/j.jmb.2006.11.070
   Google Scholar
• van der Hoek, L. (2007). Human coronaviruses: What do they cause? Antiviral Therapy, 12(4 Pt B), 651–658.
   PubMed Web of Science ®Google Scholar
• van Hemert, F. J., Zaaijer, H. L., & Berkhout, B. (2015). In silico prediction of ebolavirus RNA polymerase inhibition by specific combinations of approved nucleotide analogues. Journal of Clinical Virology, 73, 89–94. https://doi.org/10.1016/j.jcv.2015.10.020
   PubMed Web of Science ®Google Scholar
• Wallace, A. C., Laskowski, R. A., & Thornton, J. M. (1995). LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Engineering, 8(2), 127–134. https://doi.org/10.1093/protein/8.2.127
   PubMedGoogle Scholar
• Wang, H., Li, X., Li, T., Zhang, S., Wang, L., Wu, X., & Liu, J. (2020). The genetic sequence, origin, and diagnosis of SARS-CoV-2. European Journal of Clinical Microbiology & Infectious Diseases, 39(9), 1629–1627. https://doi.org/10.1007/s10096-020-03899-4
   PubMed Web of Science ®Google Scholar
• Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics & Modelling, 25(2), 247–260. https://doi.org/10.1016/j.jmgm.2005.12.005
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174. https://doi.org/10.1002/jcc.20035
   PubMed Web of Science ®Google Scholar
• Wang, Q., Wu, J., Wang, H., Gao, Y., Liu, Q., Mu, A., Ji, W., Yan, L., Zhu, Y., Zhu, C., Fang, X., Yang, X., Huang, Y., Gao, H., Liu, F., Ge, J., Sun, Q., Yang, X., Xu, W., … Rao, Z. (2020). Structural basis for RNA replication by the SARS-CoV-2 polymerase. Cell, 182(2), 417–428.e13. https://doi.org/10.1016/j.cell.2020.05.034
   PubMed Web of Science ®Google Scholar
• Wang, Y., Anirudhan, V., Du, R., Cui, Q., & Rong, L. (2021). RNA-dependent RNA polymerase of SARS-CoV-2 as a therapeutic target. Journal of Medical Virology, 93(1), 300-310. https://doi.org/10.1002/jmv.26264
   Google Scholar
• Xu, J., Zhao, S., Teng, T., Abdalla, A. E., Zhu, W., Xie, L., Wang, Y., & Guo, X. (2020). Systematic comparison of two animal-to-human transmitted human coronaviruses: SARS-CoV-2 and SARS-CoV. Viruses, 12(2), 244. https://doi.org/10.3390/v12020244
   PubMed Web of Science ®Google Scholar
• Xu, X., Liu, Y., Weiss, S., Arnold, E., Sarafianos, S. G., & Ding, J. (2003). Molecular model of SARS coronavirus polymerase: Implications for biochemical functions and drug design. Nucleic Acids Research, 31(24), 7117–7130. https://doi.org/10.1093/nar/gkg916
   PubMed Web of Science ®Google Scholar
• Zhang, L., & Zhou, R. (2020). Structural basis of the potential binding mechanism of Remdesivir to SARS-CoV-2 RNA-dependent RNA polymerase. The Journal of Physical Chemistry, B, 124(32), 6955–6962. https://doi.org/10.1021/acs.jpcb.0c04198
   PubMed Web of Science ®Google Scholar
• Zhao, Z., & Bourne, P. E. (2020). Structural insights into the binding modes of viral RNA-dependent RNA polymerases using a function-site interaction fingerprint method for RNA virus drug discovery. Journal of Proteome Research, 19(11), 4698-4705. https://doi.org/10.1021/acs.jproteome.0c00623
   Google Scholar
• Zhu, W., Chen, C. Z., Gorshkov, K., Xu, M., Lo, D. C., & Zheng, W. (2020). RNA-dependent RNA polymerase as a target for COVID-19 drug discovery. SLAS Discovery. https://doi.org/10.1177/2472555220942123
   Google Scholar