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Research Articles

Structure-based virtual screening and molecular dynamics simulation of SARS-CoV-2 Guanine-N7 methyltransferase (nsp14) for identifying antiviral inhibitors against COVID-19

ORCID Icon, ORCID Icon, , , & ORCID Icon
Pages 4582-4593 | Received 04 May 2020, Accepted 01 Jun 2020, Published online: 22 Jun 2020

References

  • Aanouz, I., Belhassan, A., El-Khatabi, K., Lakhlifi, T., El-Ldrissi, M., & Bouachrine, M. (2020). Moroccan medicinal plants as inhibitors against SARS-CoV-2 main protease: Computational investigations. Journal of Biomolecular Structure and Dynamics, 1–9. https://doi.org/10.1080/07391102.2020.1758790
  • Abdelli, I., Hassani, F., Bekkel Brikci, S., & Ghalem, S. (2020). In silico study the inhibition of Angiotensin converting enzyme 2 receptor of COVID-19 by Ammoides verticillata components harvested from western Algeria. Journal of Biomolecular Structure and Dynamics, 1–17. https://doi.org/10.1080/07391102.2020.1763199
  • Aksoydan, B., Kantarcioglu, I., Erol, I., Salmas, R. E., & Durdagi, S. (2018). Structure-based design of hERG-neutral antihypertensive oxazalone and imidazolone derivatives. Journal of Molecular Graphics & Modelling, 79, 103–117. https://doi.org/10.1016/j.jmgm.2017.10.011
  • Alogheli, H., Olanders, G., Schaal, W., Brandt, P., & Karlen, A. (2017). Docking of macrocycles: Comparing rigid and flexible docking in glide. Journal of Chemical Information and Modeling, 57(2), 190–202. https://doi.org/10.1021/acs.jcim.6b00443
  • Andersen, K. G., Rambaut, A., Lipkin, W. I., Holmes, E. C., & Garry, R. F. (2020). The proximal origin of SARS-CoV-2. Nature Medicine, 26(4), 450–452. https://doi.org/10.1038/s41591-020-0820-9
  • Bandaru, S., Alvala, M., Nayarisseri, A., Sharda, S., Goud, H., Mundluru, H. P., & Singh, S. K. (2017). Molecular dynamic simulations reveal suboptimal binding of salbutamol in T164I variant of β2 adrenergic receptor. PLoS One, 12(10), e0186666. https://doi.org/10.1371/journal.pone.0186666
  • Bawono, P., & Heringa, J. (2014). PRALINE: A versatile multiple sequence alignment toolkit. Methods in Molecular Biology, 1079, 245–262. https://doi.org/10.1007/978-1-62703-646-7_16
  • Boopathi, S., Poma, A. B., & Kolandaivel, P. (2020). Novel 2019 coronavirus structure, mechanism of action, antiviral drug promises and rule out against its treatment. Journal of Biomolecular Structure and Dynamics, 1–10. https://doi.org/10.1080/07391102.2020.1758788
  • Chavez Thielemann, H., Cardellini, A., Fasano, M., Bergamasco, L., Alberghini, M., Ciorra, G., Chiavazzo, E., & Asinari, P. (2019). From GROMACS to LAMMPS: GRO2LAM: A converter for molecular dynamics software. Journal of Molecular Modeling, 25(6), 147. https://doi.org/10.1007/s00894-019-4011-x
  • Chen, Y., Cai, H., Pan, J., Xiang, N., Tien, P., Ahola, T., & Guo, D. (2009). Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3484–3489. https://doi.org/10.1073/pnas.0808790106
  • Chen, Y., & Guo, D. (2016). Molecular mechanisms of coronavirus RNA capping and methylation. Virologica Sinica, 31(1), 3–11. https://doi.org/10.1007/s12250-016-3726-4
  • Childers, M. C., & Daggett, V. (2018). Validating molecular dynamics simulations against experimental observables in light of underlying conformational ensembles. The Journal of Physical Chemistry B, 122(26), 6673–6689. https://doi.org/10.1021/acs.jpcb.8b02144
  • Chinnasamy, S., Selvaraj, G., Kaushik, A. C., Kaliamurthi, S., Chandrabose, S., Singh, S. K., Thirugnanasambandam, R., Gu, K., & Wei, D. Q. (2019). Molecular docking and molecular dynamics simulation studies to identify potent AURKA inhibitors: Assessing the performance of density functional theory, MM-GBSA and mass action kinetics calculations. Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2019.1674695
  • Chinnasamy, S., Selvaraj, G., Selvaraj, C., Kaushik, A. C., Kaliamurthi, S., Khan, A., Singh, S. K., & Wei, D. Q. (2020). Combining in silico and in vitro approaches to identification of potent inhibitor against phospholipase A2 (PLA2). International Journal of Biological Macromolecules, 144, 53–66. https://doi.org/10.1016/j.ijbiomac.2019.12.091
  • Das, S., Sarmah, S., Lyndem, S., & Singha Roy, A. (2020). An investigation into the identification of potential inhibitors of SARS-CoV-2 main protease using molecular docking study. Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2020.1763201
  • Decroly, E., Ferron, F., Lescar, J., & Canard, B. (2011). Conventional and unconventional mechanisms for capping viral mRNA. Nature Reviews. Microbiology, 10(1), 51–65. https://doi.org/10.1038/nrmicro2675
  • DiMaio, D., Enquist, L. W., & Dermody, T. S. (2020). Introduction: A new coronavirus emerges, this time causing a pandemic. Annual Review of Virology, 1–4. https://doi.org/10.1146/annurev-vi-07-042020-100001
  • Elmezayen, A. D., Al-Obaidi, A., Sahin, A. T., & Yelekci, K. (2020). Drug repurposing for coronavirus (COVID-19): in silico screening of known drugs against coronavirus 3CL hydrolase and protease enzymes. Journal of Biomolecular Structure and Dynamics, 1–13. https://doi.org/10.1080/07391102.2020.1758791
  • Fazil, M. H., Kumar, S., Rao, N. S., Selvaraj, C., Singh, S. K., Pandey, H. P., & Singh, D. V. (2012). Comparative structural analysis of two proteins belonging to quorum sensing system in Vibrio cholerae. Journal of Biomolecular Structure & Dynamics, 30(5), 574–584. https://doi.org/10.1080/07391102.2012.687523
  • Ferron, F., Decroly, E., Selisko, B., & Canard, B. (2012). The viral RNA capping machinery as a target for antiviral drugs. Antiviral Research, 96(1), 21–31. https://doi.org/10.1016/j.antiviral.2012.07.007
  • Fung, T. S., & Liu, D. X. (2019). Human Coronavirus: Host-pathogen interaction. Annual Review of Microbiology, 73, 529–557. https://doi.org/10.1146/annurev-micro-020518-115759
  • Grover, A., Katiyar, S. P., Singh, S. K., Dubey, V. K., & Sundar, D. (2012). A leishmaniasis study: Structure-based screening and molecular dynamics mechanistic analysis for discovering potent inhibitors of spermidine synthase. Biochimica et Biophysica Acta, 1824(12), 1476–1483. https://doi.org/10.1016/j.bbapap.2012.05.016
  • Gupta, M. K., Vemula, S., Donde, R., Gouda, G., Behera, L., & Vadde, R. (2020). In-silico approaches to detect inhibitors of the human severe acute respiratory syndrome coronavirus envelope protein ion channel. Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2020.1751300
  • Gyebi, G. A., Ogunro, O. B., Adegunloye, A. P., Ogunyemi, O. M., & Afolabi, S. O. (2020). Potential inhibitors of Coronavirus 3-Chymotrypsin-Like protease (3CL(pro)): An in silico screening of alkaloids and terpenoids from African medicinal plants. Journal of Biomolecular Structure and Dynamics, 1–19. https://doi.org/10.1080/07391102.2020.1764868
  • Harder, E., Damm, W., Maple, J., Wu, C., Reboul, M., Xiang, J. Y., Wang, L., Lupyan, D., Dahlgren, M. K., Knight, J. L., Kaus, J. W., Cerutti, D. S., Krilov, G., Jorgensen, W. L., Abel, R., & Friesner, R. A. (2016). OPLS3: A force field providing broad coverage of drug-like small molecules and proteins. Journal of Chemical Theory and Computation, 12(1), 281–296. https://doi.org/10.1021/acs.jctc.5b00864
  • Hercik, K., Brynda, J., Nencka, R., & Boura, E. (2017). Structural basis of Zika virus methyltransferase inhibition by sinefungin. Archives of Virology, 162(7), 2091–2096. https://doi.org/10.1007/s00705-017-3345-x
  • Kawatkar, S., Wang, H., Czerminski, R., & Joseph-McCarthy, D. (2009). Virtual fragment screening: An exploration of various docking and scoring protocols for fragments using Glide. Journal of Computer-Aided Molecular Design, 23(8), 527–539. https://doi.org/10.1007/s10822-009-9281-4
  • Khan, R. J., Jha, R. K., Amera, G. M., Jain, M., Singh, E., Pathak, A., Singh, R. P., Muthukumaran, J., & Singh, A. K. (2020). Targeting SARS-CoV-2: A systematic drug repurposing approach to identify promising inhibitors against 3C-like proteinase and 2’-O-ribose methyltransferase. Journal of Biomolecular Structure and Dynamics, 1–14. https://doi.org/10.1080/07391102.2020.1753577
  • Koonin, E. V., & Moss, B. (2010). Viruses know more than one way to don a cap. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3283–3284. https://doi.org/10.1073/pnas.0915061107
  • Kumar, A., Liang, B., Aarthy, M., Singh, S. K., Garg, N., Mysorekar, I. U., & Giri, R. (2018). Hydroxychloroquine inhibits Zika Virus NS2B-NS3 protease. ACS Omega, 3(12), 18132–18141. https://doi.org/10.1021/acsomega.8b01002
  • Kumar, D., Kumari, K., Jayaraj, A., Kumar, V., Kumar, R. V., Dass, S. K., Chandra, R., & Singh, P. (2020). Understanding the binding affinity of noscapines with protease of SARS-CoV-2 for COVID-19 using MD simulations at different temperatures. Journal of Biomolecular Structure and Dynamics, 1–14. https://doi.org/10.1080/07391102.2020.1752310
  • Lai, M. M., & Stohlman, S. A. (1981). Comparative analysis of RNA genomes of mouse hepatitis viruses. Journal of Virology, 38(2), 661–670. http://www.ncbi.nlm.nih.gov/pubmed/6165837 https://doi.org/10.1128/JVI.38.2.661-670.1981
  • Lionta, E., Spyrou, G., Vassilatis, D. K., & Cournia, Z. (2014). Structure-based virtual screening for drug discovery: Principles, applications and recent advances. Current Topics in Medicinal Chemistry, 14(16), 1923–1938. https://doi.org/10.2174/1568026614666140929124445
  • Lobo-Galo, N., Terrazas-Lopez, M., Martinez-Martinez, A., & Diaz-Sanchez, A. G. (2020). FDA-approved thiol-reacting drugs that potentially bind into the SARS-CoV-2 main protease, essential for viral replication. Journal of Biomolecular Structure and Dynamics., 1–12. https://doi.org/10.1080/07391102.2020.1764393
  • Ma, Y., Wu, L., Shaw, N., Gao, Y., Wang, J., Sun, Y., Lou, Z., Yan, L., Zhang, R., & Rao, Z. (2015). Structural basis and functional analysis of the SARS coronavirus nsp14-nsp10 complex. Proceedings of the National Academy of Sciences of the United States of America, 112(30), 9436–9441. https://doi.org/10.1073/pnas.1508686112
  • Ma, Y., Zhou, K., Fan, J., & Sun, S. (2016). Traditional Chinese medicine: Potential approaches from modern dynamical complexity theories. Frontiers of Medicine, 10(1), 28–32. https://doi.org/10.1007/s11684-016-0434-2
  • Martinez, L. (2015). Automatic identification of mobile and rigid substructures in molecular dynamics simulations and fractional structural fluctuation analysis. PLoS One, 10(3), e0119264. https://doi.org/10.1371/journal.pone.0119264
  • Minskaia, E., Hertzig, T., Gorbalenya, A. E., Campanacci, V., Cambillau, C., Canard, B., & Ziebuhr, J. (2006). Discovery of an RNA virus 3'->5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proceedings of the National Academy of Sciences of the United States of America, 103(13), 5108–5113. https://doi.org/10.1073/pnas.0508200103
  • Muralidharan, N., Sakthivel, R., Velmurugan, D., & Gromiha, M. M. (2020). Computational studies of drug repurposing and synergism of lopinavir, oseltamivir and ritonavir binding with SARS-CoV-2 protease against COVID-19. Journal of Biomolecular Structure and Dynamics, 1–6. https://doi.org/10.1080/07391102.2020.1752802
  • Nakagawa, K., Lokugamage, K. G., & Makino, S. (2016). Viral and cellular mRNA translation in Coronavirus-infected cells. Advances in Virus Research, 96, 165–192. https://doi.org/10.1016/bs.aivir.2016.08.001
  • Nguyen, T. T., Viet, M. H., & Li, M. S. (2014). Effects of water models on binding affinity: Evidence from all-atom simulation of binding of tamiflu to A/H5N1 neuraminidase. The Scientific World Journal, 2014, 536084. https://doi.org/10.1155/2014/536084
  • Onufriev, A. V., & Alexov, E. (2013). Protonation and pK changes in protein-ligand binding. Quarterly Reviews of Biophysics, 46(2), 181–209. https://doi.org/10.1017/S0033583513000024
  • Pant, S., Singh, M., Ravichandiran, V., Murty, U. S. N., & Srivastava, H. K. (2020). Peptide-like and small-molecule inhibitors against Covid-19. Journal of Biomolecular Structure and Dynamics, 1–10. https://doi.org/10.1080/07391102.2020.1757510
  • Patidar, K., Deshmukh, A., Bandaru, S., Lakkaraju, C., Girdhar, A., Vr, G., Banerjee, T., Nayarisseri, A., & Singh, S. K. (2016). Virtual screening approaches in identification of bioactive compounds akin to delphinidin as potential HER2 inhibitors for the treatment of breast cancer. Asian Pacific Journal of Cancer Prevention: APJCP, 17(4), 2291–2295. https://doi.org/10.7314/apjcp.2016.17.4.2291
  • Pontius, J., Richelle, J., & Wodak, S. J. (1996). Deviations from standard atomic volumes as a quality measure for protein crystal structures. Journal of Molecular Biology, 264(1), 121–136. https://doi.org/10.1006/jmbi.1996.0628
  • Rakhshani, H., Dehghanian, E., & Rahati, A. (2019). Enhanced GROMACS: Toward a better numerical simulation framework. Journal of Molecular Modeling, 25(12), 355https://doi.org/10.1007/s00894-019-4232-z
  • Rapp, C., Kalyanaraman, C., Schiffmiller, A., Schoenbrun, E. L., & Jacobson, M. P. (2011). A molecular mechanics approach to modeling protein-ligand interactions: Relative binding affinities in congeneric series. Journal of Chemical Information and Modeling, 51(9), 2082–2089. https://doi.org/10.1021/ci200033n
  • Rayalu, D. J., Selvaraj, C., Singh, S. K., Ganeshan, R., Kumar, N. U., & Seshapani, P. (2012). Homology modeling, active site prediction, and targeting the anti hypertension activity through molecular docking on endothelin - B receptor domain. Bioinformation, 8(2), 81–86. https://doi.org/10.6026/97320630008081
  • Sarma, P., Sekhar, N., Prajapat, M., Avti, P., Kaur, H., Kumar, S., Singh, S., Kumar, H., Prakash, A., Dhibar, D. P., & Medhi, B. (2020). In-silico homology assisted identification of inhibitor of RNA binding against 2019-nCoV N-protein (N terminal domain). Journal of Biomolecular Structure and Dynamics, 1–11. https://doi.org/10.1080/07391102.2020.1753580
  • Sastry, G. M., Adzhigirey, M., Day, T., Annabhimoju, R., & Sherman, W. (2013). Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments. Journal of Computer-Aided Molecular Design, 27(3), 221–234. https://doi.org/10.1007/s10822-013-9644-8
  • Schuttelkopf, A. W., & van Aalten, D. M. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica. Section D, Biological Crystallography, 60(Pt 8), 1355–1363. https://doi.org/10.1107/S0907444904011679
  • Selvaraj, C., Bharathi Priya, R., & Singh, S. K. (2014). Communication of γ phage lysin plyG enzymes binding toward SrtA for inhibition of Bacillus anthracis: protein-protein interaction and molecular dynamics study. Cell Communication & Adhesion, 21(5), 257–265. https://doi.org/10.3109/15419061.2014.927444
  • Selvaraj, C., Omer, A., Singh, P., & Singh, S. K. (2015). Molecular insights of protein contour recognition with ligand pharmacophoric sites through combinatorial library design and MD simulation in validating HTLV-1 PR inhibitors. Molecular Biosystems, 11(1), 178–189. https://doi.org/10.1039/c4mb00486h
  • Selvaraj, C., Sakkiah, S., Tong, W., & Hong, H. (2018). Molecular dynamics simulations and applications in computational toxicology and nanotoxicology. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 112, 495–506. https://doi.org/10.1016/j.fct.2017.08.028
  • Selvaraj, C., Singh, P., & Singh, S. K. (2014a). Molecular insights on analogs of HIV PR inhibitors toward HTLV-1 PR through QM/MM interactions and molecular dynamics studies: Comparative structure analysis of wild and mutant HTLV-1 PR. Journal of Molecular Recognition: JMR, 27(12), 696–706. https://doi.org/10.1002/jmr.2395
  • Selvaraj, C., Singh, P., & Singh, S. K. (2014b). Molecular modeling studies and comparative analysis on structurally similar HTLV and HIV protease using HIV-PR inhibitors. Journal of Receptor and Signal Transduction Research, 34(5), 361–371. https://doi.org/10.3109/10799893.2014.898659
  • Selvaraj, C., & Singh, S. K. (2014). Validation of potential inhibitors for SrtA against Bacillus anthracis by combined approach of ligand-based and molecular dynamics simulation. Journal of Biomolecular Structure & Dynamics, 32(8), 1333–1349. https://doi.org/10.1080/07391102.2013.818577
  • Selvaraj, C., Sivakamavalli, J., Baskaralingam, V., & Singh, S. K. (2014). Virtual screening of LPXTG competitive SrtA inhibitors targeting signal transduction mechanism in Bacillus anthracis: A combined experimental and theoretical study. Journal of Receptor and Signal Transduction Research, 34(3), 221–232. https://doi.org/10.3109/10799893.2013.876044
  • Selvaraj, C., Sivakamavalli, J., Vaseeharan, B., Singh, P., & Singh, S. K. (2014). Examine the characterization of biofilm formation and inhibition by targeting SrtA mechanism in Bacillus subtilis: A combined experimental and theoretical study. Journal of Molecular Modeling, 20(8), 2364. https://doi.org/10.1007/s00894-014-2364-8
  • Shafreen, R. M., Selvaraj, C., Singh, S. K., & Pandian, S. K. (2013). Exploration of fluoroquinolone resistance in Streptococcus pyogenes: Comparative structure analysis of wild-type and mutant DNA gyrase. Journal of Molecular Recognition, 26(6), 276–285. https://doi.org/10.1002/jmr.2270
  • Sivakamavalli, J., Selvaraj, C., Singh, S. K., & Vaseeharan, B. (2014). Interaction investigations of crustacean β-GBP recognition toward pathogenic microbial cell membrane and stimulate upon prophenoloxidase activation. Journal of Molecular Recognition: JMR, 27(4), 173–183. https://doi.org/10.1002/jmr.2348
  • Sliwoski, G., Kothiwale, S., Meiler, J., & Lowe, E. W. Jr.(2014). Computational methods in drug discovery. Pharmacological Reviews, 66(1), 334–395. https://doi.org/10.1124/pr.112.007336
  • Swegat, W., Schlitter, J., Kruger, P., & Wollmer, A. (2003). MD simulation of protein-ligand interaction: Formation and dissociation of an insulin-phenol complex. Biophysical Journal, 84(3), 1493–1506. https://doi.org/10.1016/S0006-3495(03)74962-5
  • Tripathi, S. K., Singh, S. K., Singh, P., Chellaperumal, P., Reddy, K. K., & Selvaraj, C. (2012). Exploring the selectivity of a ligand complex with CDK2/CDK1: A molecular dynamics simulation approach. Journal of Molecular Recognition: JMR, 25(10), 504–512. https://doi.org/10.1002/jmr.2216
  • Umesh, K. D., Selvaraj, C., Singh, S. K., & Dubey, V. K. (2020). Identification of new anti-nCoV drug chemical compounds from Indian spices exploiting SARS-CoV-2 main protease as target. Journal of Biomolecular Structure and Dynamics, 1–9. https://doi.org/10.1080/07391102.2020.1763202
  • van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., & Vriend, G. (1996). PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. Journal of Computer-Aided Molecular Design, 10(3), 255–262. https://doi.org/10.1007/BF00355047
  • Verma, P., Tiwari, M., & Tiwari, V. (2018). In silico high-throughput virtual screening and molecular dynamics simulation study to identify inhibitor for AdeABC efflux pump of Acinetobacter baumannii. Journal of Biomolecular Structure & Dynamics, 36(5), 1182–1194. https://doi.org/10.1080/07391102.2017.1317025
  • Vijayalakshmi, P., Selvaraj, C., Singh, S. K., Nisha, J., Saipriya, K., & Daisy, P. (2013). Exploration of the binding of DNA binding ligands to Staphylococcal DNA through QM/MM docking and molecular dynamics simulation. Journal of Biomolecular Structure & Dynamics, 31(6), 561–571. https://doi.org/10.1080/07391102.2012.706080
  • Wang, J., Wong, Y. K., & Liao, F. (2018). What has traditional Chinese medicine delivered for modern medicine? Expert Reviews in Molecular Medicine, 20, e4. https://doi.org/10.1017/erm.2018.3
  • Wang, P., Li, K., Tao, Y., Li, D., Zhang, Y., Xu, H., & Yang, H. (2019). TCM-ADMEpred: A novel strategy for poly-pharmacokinetics prediction of traditional Chinese medicine based on single constituent pharmacokinetics, structural similarity, and mathematical modeling. Journal of Ethnopharmacology, 236, 277–287. https://doi.org/10.1016/j.jep.2018.07.008
  • Wang, Q., Zhang, Y., Wu, L., Niu, S., Song, C., Zhang, Z., Lu, G., Qiao, C., Hu, Y., Yuen, K. Y., Wang, Q., Zhou, H., Yan, J., & Qi, J. (2020). Structural and functional basis of SARS-CoV-2 entry by using human ACE2. Cell, 181(4), 894–904. https://doi.org/10.1016/j.cell.2020.03.045
  • Webb, B., & Sali, A. (2016). Comparative protein structure modeling using MODELLER. Current Protocols in Bioinformatics, 54, 1–37. https://doi.org/10.1002/cpbi.3
  • Webb, B., & Sali, A. (2017). Protein structure modeling with MODELLER. Methods in Molecular Biology, 1654, 39–54. https://doi.org/10.1007/978-1-4939-7231-9_4
  • Wohlert, J., & Edholm, O. (2004). The range and shielding of dipole-dipole interactions in phospholipid bilayers. Biophysical Journal, 87(4), 2433–2445. https://doi.org/10.1529/biophysj.104.044222
  • Zhou, S. F., Zhou, Z. W., Yang, L. P., & Cai, J. P. (2009). Substrates, inducers, inhibitors and structure-activity relationships of human Cytochrome P450 2C9 and implications in drug development. Current Medicinal Chemistry, 16(27), 3480–3675. https://doi.org/10.2174/092986709789057635

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