Molecular docking, molecular dynamics simulation and MM-GBSA studies of the activity of glycyrrhizin relevant substructures on SARS-CoV-2 RNA-dependent-RNA polymerase

References

• Aamir, M., Singh, V. K., Dubey, M. K., Meena, M., Kashyap, S. P., Katari, S. K., Upadhyay, R. S., Umamaheswari, A., & Singh, S. (2018). In silico prediction, characterization, molecular docking, and dynamic studies on fungal SDRs as novel targets for searching potential fungicides against Fusarium wilt in tomato. Frontiers in Pharmacology, 9, 1038. https://doi.org/10.3389/fphar.2018.01038
   PubMed Web of Science ®Google Scholar
• Aatif, M., Muteeb, G., Alsultan, A., Alshoaibi, A., & Khelif, B. Y. (2021). Dieckol and its derivatives as potential inhibitors of SARS-CoV-2 spike protein (UK Strain: VUI 202012/01): A computational study. Marine Drugs, 19(5), 242. https://doi.org/10.3390/md19050242
   PubMed Web of Science ®Google Scholar
• Agostini, M. L., Andres, E. L., Sims, A. C., Graham, R. L., Sheahan, T. P., Lu, X., Smith, E. C., Case, J. B., Feng, J. Y., Jordan, R., Ray, A. S., Cihlar, T., Siegel, D., Mackman, R. L., Clarke, M. O., Baric, R. S., & Denison, M. R. (2018). Coronavirus susceptibility to the antiviral remdesivir (GS-5734) is mediated by the viral polymerase and the proofreading exoribonuclease. mBio, 9(2), e00221–18. https://doi.org/10.1128/mBio.00221-18
   PubMed Web of Science ®Google Scholar
• Ahmad, S., Waheed, Y., Abro, A., Abbasi, S. W., & Ismail, S. (2021). Molecular screening of glycyrrhizin-based inhibitors against ACE2 host receptor of SARS-CoV-2. Journal of Molecular Modeling, 27(7), 1–13. https://doi.org/10.1007/s00894-021-04816-y
   Web of Science ®Google Scholar
• Alnajjar, R., Mostafa, A., Kandeil, A., & Al-Karmalawy, A. A. (2020). Molecular docking, molecular dynamics, and in vitro studies reveal the potential of angiotensin II receptor blockers to inhibit the COVID-19 main protease. Heliyon, 6(12), e05641. https://doi.org/10.1016/j.heliyon.2020.e05641
   PubMed Web of Science ®Google Scholar
• Ashour, M. L., Youssef, F. S., Gad, H. A., & Wink, M. (2017). Inhibition of cytochrome P450 (CYP3A4) activity by extracts from 57 plants used in traditional chinese medicine (TCM). Pharmacognosy Magazine, 13(50), 300–308. https://doi.org/10.4103/0973-1296.204561
   PubMed Web of Science ®Google Scholar
• Bailly, C., & Vergoten, G. (2020). Glycyrrhizin: An alternative drug for the treatment of COVID-19 infection and the associated respiratory syndrome? Pharmacology & Therapeutics, 214, 107618. https://doi.org/10.1016/j.pharmthera.2020.107618
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., & Zardecki, C. (2002). The protein data bank. Acta Crystallographica. Section D, Biological Crystallography, 58(Pt 6 No 1), 899–907. https://doi.org/10.1107/s0907444902003451
   PubMedGoogle Scholar
• Bhowmick, S., Saha, A., Osman, S. M., Alasmary, F. A., Almutairi, T. M., & Islam, M. A. (2021). Structure-based identification of SARS-CoV-2 main protease inhibitors from anti-viral specific chemical libraries: an exhaustive computational screening approach. Molecular Diversity, 25(3), 1979–1919. https://doi.org/10.1007/s11030-021-10214-6
   PubMed Web of Science ®Google Scholar
• Chen, L., Xiong, J., Bao, L., & Shi, Y. (2020). Convalescent plasma as a potential therapy for COVID-19. The Lancet. Infectious Diseases , 20(4), 398–400. https://doi.org/10.1016/S1473-3099(20)30141-9
   PubMed Web of Science ®Google Scholar
• Cinatl, J., Morgenstern, B., Bauer, G., Chandra, P., Rabenau, H., & Doerr, H. (2003). Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. The Lancet, 361(9374), 2045–2046. https://doi.org/10.1016/S0140-6736(03)13615-X
   PubMed Web of Science ®Google Scholar
• D.K. Maurya, Evaluation of Yashtimadhu (Glycyrrhiza glabra) active phytochemicals against novel coronavirus (SARS-CoV-2), (2020).
   Google Scholar
• Dash, R., Junaid, M., Mitra, S., Arifuzzaman, M., & Hosen, S. Z. (2019). Structure-based identification of potent VEGFR-2 inhibitors from in vivo metabolites of a herbal ingredient. Journal of Molecular Modeling, 25(4), 1–15. https://doi.org/10.1007/s00894-019-3979-6
   Web of Science ®Google Scholar
• De Clercq, E., & Li, G. (2016). Approved Antiviral Drugs over the Past 50 Years. Clinical Microbiology Reviews, 29(3), 695–747. https://doi.org/10.1128/CMR.00102-15
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• El Hassab, M. A., Shoun, A. A., Al-Rashood, S. T., Al-Warhi, T., & Eldehna, W. M. (2020). Identification of a new potential SARS-COV-2 RNA-dependent RNA polymerase inhibitor via combining fragment-based drug design, docking, molecular dynamics, and MM-PBSA calculations. Frontiers in Chemistry, 8, 584894. https://doi.org/10.3389/fchem.2020.584894
   PubMed Web of Science ®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., … 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
• Gomaa, A. A., & Abdel-Wadood, Y. A. (2021). The potential of glycyrrhizin and licorice extract in combating COVID-19 and associated conditions. Phytomedicine Plus, 1(3), 100043. https://doi.org/10.1016/j.phyplu.2021.100043
   PubMedGoogle Scholar
• Greenwood, J. R., Calkins, D., Sullivan, A. P., & Shelley, J. C. (2010). Towards the comprehensive, rapid, and accurate prediction of the favorable tautomeric states of drug-like molecules in aqueous solution. Journal of Computer-Aided Molecular Design, 24(6-7), 591–604. https://doi.org/10.1007/s10822-010-9349-1
   PubMed Web of Science ®Google Scholar
• Hoever, G., Baltina, L., Michaelis, M., Kondratenko, R., Baltina, L., Tolstikov, G. A., Doerr, H. W., & Cinatl, J. (2005). Antiviral activity of glycyrrhizic acid derivatives against SARS-coronavirus. Journal of Medicinal Chemistry, 48(4), 1256–1259. https://doi.org/10.1021/jm0493008
   PubMed Web of Science ®Google Scholar
• Huan, C., Xu, Y., Zhang, W., Guo, T., Pan, H., & Gao, S. (2021). Research Progress on the Antiviral Activity of Glycyrrhizin and its Derivatives in Liquorice. Frontiers in Pharmacology, 12, 680674. https://doi.org/10.3389/fphar.2021.680674
   PubMed Web of Science ®Google Scholar
• Kampf, G., Todt, D., Pfaender, S., & Steinmann, E. (2020). Persistence of coronaviruses on inanimate surfaces and its inactivation with biocidal agents. Journal of Hospital Infection, 104(3), 246–251. https://doi.org/10.1016/j.jhin.2020.01.022
   PubMed Web of Science ®Google Scholar
• Khan, S., Fakhar, Z., Hussain, A., Ahmad, A., Jairajpuri, D. S., Alajmi, M. F., & Hassan, M. I. (2020). Structure-based identification of potential SARS-CoV-2 main protease inhibitors. Journal of Biomolecular Structure and Dynamics, 1–14. https://doi.org/10.1080/07391102.2020.1848634
   Google Scholar
• Khater, S., Kumar, P., Dasgupta, N., Das, G., Ray, S., & Prakash, A. (2021). Combining SARS-CoV-2 proofreading exonuclease and RNA-dependent RNA polymerase inhibitors as a strategy to combat COVID-19: A high-throughput in silico screening. Frontiers in Microbiology, 12, 1934–1944. https://doi.org/10.3389/fmicb.2021.647693
   Google Scholar
• Kim, S., Thiessen, P. A., Bolton, E. E., Chen, J., Fu, G., Gindulyte, A., Han, L., He, J., He, S., Shoemaker, B. A., Wang, J., Yu, B., Zhang, J., & Bryant, S. H. (2016). PubChem substance and compound databases. Nucleic Acids Research, 44(D1), D1202–D1213. https://doi.org/10.1093/nar/gkv951
   PubMed Web of Science ®Google Scholar
• Li, S.-Y., Chen, C., Zhang, H.-Q., Guo, H.-Y., Wang, H., Wang, L., Zhang, X., Hua, S.-N., Yu, J., Xiao, P.-G., Li, R.-S., & Tan, X. (2005). Identification of natural compounds with antiviral activities against SARS-associated coronavirus. Antiviral Research, 67(1), 18–23. https://doi.org/10.1016/j.antiviral.2005.02.007
   PubMed Web of Science ®Google Scholar
• Lin, J.-C. (2003). Mechanism of action of glycyrrhizic acid in inhibition of Epstein-Barr virus replication in vitro. Antiviral Research, 59(1), 41–47. https://doi.org/10.1016/S0166-3542(03)00030-5
   PubMed Web of Science ®Google Scholar
• Luo, P., Liu, D., & Li, J. (2020). Pharmacological perspective: glycyrrhizin may be an efficacious therapeutic agent for COVID-19. International Journal of Antimicrobial Agents, 55(6), 105995. https://doi.org/10.1016/j.ijantimicag.2020.105995
   PubMed Web of Science ®Google Scholar
• Makhaeva, G. F., Elkina, N. A., Shchegolkov, E. V., Boltneva, N. P., Lushchekina, S. V., Serebryakova, O. G., Rudakova, E. V., Kovaleva, N. V., Radchenko, E. V., Palyulin, V. A., Burgart, Y. V., Saloutin, V. I., Bachurin, S. O., & Richardson, R. J. (2019). Synthesis, molecular docking, and biological evaluation of 3-oxo-2-tolylhydrazinylidene-4,4,4-trifluorobutanoates bearing higher and natural alcohol moieties as new selective carboxylesterase inhibitors . Bioorganic Chemistry, 91, 103097. https://doi.org/10.1016/j.bioorg.2019.103097
   PubMed Web of Science ®Google Scholar
• Mittal, L., Kumari, A., Srivastava, M., Singh, M., & Asthana, S. (2020). Identification of potential molecules against COVID-19 main protease through structure-guided virtual screening approach. Journal of Biomolecular Structure and Dynamics, 39(10), 3662–3680. https://doi.org/10.1080/07391102.2020.1768151
   PubMed Web of Science ®Google Scholar
• Murck, H. (2020). Symptomatic protective action of glycyrrhizin (licorice) in COVID-19 infection? Frontiers in Immunology, 11, 1239. https://doi.org/10.3389/fimmu.2020.01239
   PubMed Web of Science ®Google Scholar
• Pang, X., Zhang, B., Mu, G., Xia, J., Xiang, Q., Zhao, X., Liu, A., Du, G., & Cui, Y. (2018). Screening of cytochrome P450 3A4 inhibitors via in silico and in vitro approaches. RSC Advances, 8(61), 34783–34792. https://doi.org/10.1039/C8RA06311G
   PubMed Web of Science ®Google Scholar
• Parvez, M. S. A., Karim, M. A., Hasan, M., Jaman, J., Karim, Z., Tahsin, T., Hasan, M. N., & Hosen, M. J. (2020). Prediction of potential inhibitors for RNA-dependent RNA polymerase of SARS-CoV-2 using comprehensive drug repurposing and molecular docking approach. Int J Biol Macromol, 163, 1787–1797. https://doi.org/10.1016/j.ijbiomac.2020.09.098
   PubMed Web of Science ®Google Scholar
• Pastorino, G., Cornara, L., Soares, S., Rodrigues, F., & Oliveira, M. B. P. (2018). Liquorice (Glycyrrhiza glabra): A phytochemical and pharmacological review. Phytotherapy Research : PTR, 32(12), 2323–2339. https://doi.org/10.1002/ptr.6178
   PubMedGoogle Scholar
• Petric, D. (n.d.). Glycyrrhizin and COVID-19.
   Google Scholar
• R. Schrödinger. (2020). 2020-1, Prime., Schrödinger, LLC.
   Google Scholar
• Rashid, M. (2020). Design, synthesis and ADMET prediction of bis-benzimidazole as anticancer agent. Bioorganic Chemistry, 96, 103576. https://doi.org/10.1016/j.bioorg.2020.103576
   PubMed Web of Science ®Google Scholar
• S. Release. (2020). Desmond molecular dynamics system. DE Shaw Research, Maestro-Desmond Interoperability Tools, Schrödinger.
   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 25873628
   PubMed Web of Science ®Google Scholar
• Sasaki, K., Yonebayashi, S., Yoshida, M., Shimizu, K., Aotsuka, T., & Takayama, K. (2003). Improvement in the bioavailability of poorly absorbed glycyrrhizin via various non-vascular administration routes in rats. International Journal of Pharmaceutics, 265(1-2), 95–102. https://doi.org/10.1016/S0378-5173(03)00407-1
   PubMed Web of Science ®Google Scholar
• Schrödinger LLC. (2020). Schrödinger-Release-2020-3, Maestro, Schrödinger, LLC.
   Google Scholar
• Shannon, A., Le, N. T.-T., Selisko, B., Eydoux, C., Alvarez, K., Guillemot, J.-C., Decroly, E., Peersen, O., Ferron, F., & Canard, B. (2020). Remdesivir and SARS-CoV-2: Structural requirements at both nsp12 RdRp and nsp14 Exonuclease active-sites. Antiviral Research, 178, 104793. https://doi.org/10.1016/j.antiviral.2020.104793
   PubMed Web of Science ®Google Scholar
• Shivakumar, D., Williams, J., Wu, Y., Damm, W., Shelley, J., & Sherman, W. (2010). Prediction of absolute solvation free energies using molecular dynamics free energy perturbation and the OPLS force field. Journal of Chemical Theory and Computation, 6(5), 1509–1519. https://doi.org/10.1021/ct900587b
   PubMed Web of Science ®Google Scholar
• Showers, W. M., Leach, S. M., Kechris, K., & Strong, M. (2021). Analysis of SARS-CoV-2 mutations over time reveals increasing prevalence of variants in the spike protein and RNA-dependent RNA polymerase. bioRxiv, Preprint. https://doi.org/10.1101/2021.03.05.433666.
   Google Scholar
• Sinha, S. K., Prasad, S. K., Islam, M. A., Gurav, S. S., Patil, R. B., AlFaris, N. A., Aldayel, T. S., AlKehayez, N. M., Wabaidur, S. M., & Shakya, A. (2021). Identification of bioactive compounds from Glycyrrhiza glabra as possible inhibitor of SARS-CoV-2 spike glycoprotein and non-structural protein-15: a pharmacoinformatics study. Journal of Biomolecular Structure & Dynamics , 39(13), 4615–4686. https://doi.org/10.1080/07391102.2020.1779132
   Web of Science ®Google Scholar
• Smith, Q. R., Fisher, C., & Allen, D. D. (2001). The role of plasma protein binding in drug delivery to brain. In Blood—Brain barrier (pp. 311–321). Springer
   Google Scholar
• Su, S., Wong, G., Shi, W., Liu, J., Lai, A. C., Zhou, J., Liu, W., Bi, Y., & Gao, G. F. (2016). Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends in Microbiology, 24(6), 490–502. https://doi.org/10.1016/j.tim.2016.03.003
   PubMed Web of Science ®Google Scholar
• Ton, A. T., Gentile, F., Hsing, M., Ban, F., & Cherkasov, A. (2020). Rapid identification of potential inhibitors of SARS‐CoV‐2 main protease by deep docking of 1.3 billion compounds. Molecular Informatics, 39(8), 2000028. https://doi.org/10.1002/minf.202000028
   PubMed Web of Science ®Google Scholar
• van de Sand, L., Bormann, M., Alt, M., Schipper, L., Heilingloh, C. S., Steinmann, E., Todt, D., Dittmer, U., Elsner, C., Witzke, O., & Krawczyk, A. (2021). Glycyrrhizin effectively inhibits SARS-CoV-2 replication by inhibiting the viral main protease. Viruses, 13(4), 609. https://doi.org/10.3390/v13040609
   PubMed Web of Science ®Google Scholar
• Wang, L., Yang, R., Yuan, B., Liu, Y., & Liu, C. (2015). The antiviral and antimicrobial activities of licorice, a widely-used Chinese herb. Acta Pharmaceutica Sinica. B, 5(4), 310–315. https://doi.org/10.1016/j.apsb.2015.05.005
   PubMed Web of Science ®Google Scholar
• Weiss, S. R., & Leibowitz, J. L. (2011). Coronavirus pathogenesis. In Advances in Virus Research (pp. 85–164). Elsevier.
   Google Scholar
• WHO. (2020). Novel Coronavirus-China. https://www.who.int/csr/don/12-january-2020-novel-coronavirus-china/en/. Accessed 1 Feb 2020,
   Google Scholar
• Xie, Y., Ruan, B., Chen, Y., Wu, N., Hu, M., & Zhu, B. (2011). Kaposi's sarcoma‐associated herpesvirus infection in Chinese patients with chronic hepatitis B. Journal of Medical Virology, 83(5), 879–883. https://doi.org/10.1002/jmv.22001
   PubMed Web of Science ®Google Scholar
• Yamamura, Y., Santa, T., Kotaki, H., Uchino, K., Sawada, Y., & Iga, T. (1995). Administration-route dependency of absorption of glycyrrhizin in rats: intraperitoneal administration dramatically enhanced bioavailability. Biological & Pharmaceutical Bulletin, 18(2), 337–341. https://doi.org/10.1248/bpb.18.337
   PubMed Web of Science ®Google Scholar
• Yin, W., Mao, C., Luan, X., Shen, D.-D., Shen, Q., Su, H., Wang, X., Zhou, F., Zhao, W., Gao, M., Chang, S., Xie, Y.-C., Tian, G., Jiang, H.-W., Tao, S.-C., Shen, J., Jiang, Y., Jiang, H., Xu, Y., … Xu, H. E. (2020). Structural basis for inhibition of the RNA-dependent RNA polymerase from SARS-CoV-2 by remdesivir. Science (New York, N.Y.), 368(6498), 1499–1504. https://doi.org/10.1126/science.abc1560
   PubMed Web of Science ®Google Scholar
• Zaki, A. M., Van Boheemen, S., Bestebroer, T. M., Osterhaus, A. D., & Fouchier, R. A. (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
   PubMed Web of Science ®Google Scholar
• Zhang, L., & Zhou, R. (2020). Binding mechanism of remdesivir to SARS-CoV-2 RNA dependent RNA polymerase.
   Google Scholar
• Zhao, J., Guo, SSai., Yi, D., Li, Q., Ma, L., Zhang, Y., Wang, J., Li, X., Guo, F., Lin, R., Liang, C., Liu, Z., & Cen, S. (2021). A cell-based assay to discover inhibitors of SARS-CoV-2 RNA dependent RNA polymerase. Antiviral Research, 190, 105078. https://doi.org/10.1016/j.antiviral.2021.105078
   PubMed Web of Science ®Google Scholar
• Zhong, N. S., Zheng, B. J., Li, Y. M., Poon, L. L. M., Xie, Z. H., Chan, K. H., Li, P. H., Tan, S. Y., Chang, Q., Xie, J. P., Liu, X. Q., Xu, J., Li, D. X., Yuen, K. Y., Peiris, J. S. M., & Guan, Y. (2003). Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. The Lancet, 362(9393), 1353–1358. https://doi.org/10.1016/S0140-6736(03)14630-2
   PubMed Web of Science ®Google Scholar
• Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., & Tan, W. (2020). A novel coronavirus from patients with pneumonia in China, 2019. New England Journal of Medicine, 382(8), 727–733. https://doi.org/10.1056/NEJMoa2001017
   PubMed Web of Science ®Google Scholar