Elucidation of the inhibitory activity of ivermectin with host nuclear importin α and several SARS-CoV-2 targets

References

• Borkotoky, S., & Banerjee, M. (2020). A computational prediction of SARS-CoV-2 structural protein inhibitors from Azadirachta indica (Neem). Journal of Biomolecular Structure and Dynamics, 1–11.
   PubMed Web of Science ®Google Scholar
• Azam, F., Taban, I. M., Eid, E. E., Iqbal, M., Alam, O., Khan, S., Mahmood, D., Anwar, M. J., Khalilullah, H., & Khan, M. U. (2020). An in-silico analysis of ivermectin interaction with potential SARS-CoV-2 targets and host nuclear importin α. Journal of Biomolecular Structure and Dynamics, 1–14.
   PubMed Web of Science ®Google Scholar
• Bello, M. (2020, December). Prediction of potential inhibitors of the dimeric SARS-CoV2 main proteinase through the MM/GBSA approach. Journal of Molecular Graphics & Modelling, 101, 107762. https://doi.org/10.1016/j.jmgm.2020.107762
   PubMed Web of Science ®Google Scholar
• Bello, M., & García‐Hernández, E. (2014). Ligand entry into the calyx of β-lactoglobulin. Biopolymers, 101(7), 744–757. https://doi.org/10.1002/bip.22454
   PubMed Web of Science ®Google Scholar
• Bello, M., Martínez-Muñoz, A., & Balbuena-Rebolledo, I. (2020). Identification of saquinavir as a potent inhibitor of dimeric SARS-CoV2 main protease through MM/GBSA. Journal of Molecular Modeling, 26(12), 1–11. https://doi.org/10.1007/s00894-020-04600-4
   Web of Science ®Google Scholar
• 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. Journal of Chemical Physics, 81(8), 3684–3690.
   Web of Science ®Google Scholar
• Brinks, V., & Ibert, O. (2020, July). From corona virus to corona crisis: The value of an analytical and geographical understanding of crisis. Tijdschrift Voor Economische en Sociale Geografie, 111(3), 275–287. https://doi.org/10.1111/tesg.12428
   PubMed Web of Science ®Google Scholar
• Caly, L., Druce, J. D., Catton, M. G., Jans, D. A., & Wagstaff, K. M. (2020). The FDA-approved drug ivermectin inhibits the replication of SARS-CoV-2 in vitro. Antiviral Research, 178, 104787. https://doi.org/10.1016/j.antiviral.2020.104787
   PubMed Web of Science ®Google Scholar
• Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., & Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. https://doi.org/10.1002/jcc.20290
   PubMed Web of Science ®Google Scholar
• Chen, Y. L. Q., & Guo, D. (2020). Emerging coronaviruses: Genome structure, replication, parthenogenesis. Journal of Virology, 92, 418423.
   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
• de Oliveira, O. V., Rocha, G. B., Paluch, A. S., & Costa, L. T. (2020). Repurposing approved drugs as inhibitors of SARS-CoV-2S-protein from molecular modeling and virtual screening. Journal of Biomolecular Structure and Dynamics, 1–10.
   PubMedGoogle Scholar
• Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J., & Kollman, P. (2003). A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. Journal of Computational Chemistry, 24(16), 1999–2012. https://doi.org/10.1002/jcc.10349
   PubMed Web of Science ®Google Scholar
• Fraser, J. E., Watanabe, S., Wang, C., Chan, W. K. K., Maher, B., Lopez- Denman, A., Hick, C., Wagstaff, K. M., Mackenzie, J. M., Sexton, P. M., Vasudevan, S. G., & Jans, D. A. (2014). A nuclear transport inhibitor that modulates the unfolded protein response and provides in vivo protection against lethal dengue virus infection. The Journal of Infectious Diseases, 210(11), 1780–1791. https://doi.org/10.1093/infdis/jiu319
   PubMed Web of Science ®Google Scholar
• Frisch, M. J. T., G. W., Schlegel, H. B., & Scuseria, G. E. (2009). Gaussian 09, Revision D.01. Gaussian Gaussian Inc.
   Google Scholar
• Gohlke, H., & Case, D. A. (2004). Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf . Journal of Computational Chemistry, 25(2), 238–250. https://doi.org/10.1002/jcc.10379
   PubMed Web of Science ®Google Scholar
• Gordon, D. E., Jang, G. M., Bouhaddou, M., Xu, J., Obernier, K., White, K. M., O'Meara, M. J., Rezelj, V. V., Guo, J. Z., Swaney, D. L., Tummino, T. A., Hüttenhain, R., Kaake, R. M., Richards, A. L., Tutuncuoglu, B., Foussard, H., Batra, J., Haas, K., Modak, M., … Krogan, N. J. (2020). A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature, 583(7816), 459–468. https://doi.org/10.1038/s41586-020-2286-9
   PubMed Web of Science ®Google Scholar
• Gorlich, D., Henklein, P., Laskey, R. A., & Hartmann, E. (1996). A 41 amino acid motif in importin-alpha confers binding to importin-beta and hence transit into the nucleus. The EMBO Journal, 15(8), 1810–1817. https://doi.org/10.1002/j.1460-2075.1996.tb00530.x
   PubMed Web of Science ®Google Scholar
• Guan, W.-J., Ni, Z.-Y., Hu, Y., Liang, W.-H., Ou, C.-Q., He, J.-X., Liu, L., Shan, H., Lei, C.-L., Hui, D. S. C., Du, B., Li, L.-J., Zeng, G., Yuen, K.-Y., Chen, R.-C., Tang, C.-L., Wang, T., Chen, P.-Y., Xiang, J., … Zhong, N.-S. (2020, April). Clinical characteristics of coronavirus disease 2019 in China. New England Journal of Medicine, 382(18), 1708–1720. https://doi.org/10.1056/NEJMoa2002032
   PubMed Web of Science ®Google Scholar
• Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., Zhang, L., Fan, G., Xu, J., Gu, X., Cheng, Z., Yu, T., Xia, J., Wei, Y., Wu, W., Xie, X., Yin, W., Li, H., Liu, M., … Cao, B. (2020, February). Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet (London, England), 395(10223), 497–506. https://doi.org/10.1016/S0140-6736(20)30183-5
   PubMed Web of Science ®Google Scholar
• Jia, Z., Yan, L., Ren, Z., Wu, L., Wang, J., Guo, J., Zheng, L., Ming, Z., Zhang, L., Lou, Z., & Rao, Z. (2019). Delicate structural coordination of the severe acute respiratory syndrome coronavirus Nsp13 upon ATP hydrolysis. Nucleic Acids Research, 47(12), 6538–6550. https://doi.org/10.1093/nar/gkz409
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., Klein, M. L., (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kanchan, A., John, Z., Parvesh, W., Jeroen, R. M., & Rolf, H. (2003). Coronavirus main proteinase (3CLpro) structure: Basis for design of anti-SARS drugs. Science, 300, 1763–1767.
   PubMed Web of Science ®Google Scholar
• Khan, M. T., Ali, A., Wang, Q., Irfan, M., Khan, A., Zeb, M. T., Zhang, Y.-J., Chinnasamy, S., & Wei, D.-Q. (2020). Marine natural compounds as potents inhibitors against the main protease of SARS-CoV-2—a molecular dynamic study. Journal of Biomolecular Structure and Dynamics, 1–11.
   Google Scholar
• Kobe, B. (1999). Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nature Structural Biology, 6(4), 388–397. https://doi.org/10.1038/7625
   PubMedGoogle Scholar
• Kong, R., Yang, G., Xue, R., Liu, M., Wang, F., Hu, J., Guo, X., & Chang, S. (2020). COVID-19 Docking Server: A meta server for docking small molecules, peptides and antibodies against potential targets of COVID-19. Bioinformatics (Oxford, England), 36(20), 5109–5111. https://doi.org/10.1093/bioinformatics/btaa645
   PubMed Web of Science ®Google Scholar
• Kwong, J. C., Schwartz, K. L., Campitelli, M. A., Chung, H., Crowcroft, N. S., Karnauchow, T., Katz, K., Ko, D. T., McGeer, A. J., McNally, D., Richardson, D. C., Rosella, L. C., Simor, A., Smieja, M., Zahariadis, G., & Gubbay, J. B. (2018). Acute myocardial infarction after laboratory-confirmed influenza infection. New England Journal of Medicine, 378(4), 345–353. https://doi.org/10.1056/NEJMoa1702090
   PubMed Web of Science ®Google Scholar
• Littler, D. R., Gully, B. S., Colson, R. N., & Rossjohn, J. (2020). Crystal Structure of the SARS-CoV-2 Non-structural Protein 9, Nsp9. iScience, 23(7), 101258. https://doi.org/10.1016/j.isci.2020.101258
   PubMed Web of Science ®Google Scholar
• Li, Z. (2020). Caution on kidney dysfunctions of COVID-19 patients. SSRN Electronic Journal, 2020.02.08.20021212. Mar. https://doi.org/10.1101/2020.02.08.20021212
   Google Scholar
• Luvira, V., Watthanakulpanich, D., & Pittisuttithum, P. (2014). Management of Strongyloides stercoralis: A puzzling parasite. International Health, 6(4), 273–281. https://doi.org/10.1093/inthealth/ihu058
   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
• Morris, G. M., Huey, R., 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
   PubMed Web of Science ®Google Scholar
• Nguyen, J. L., Yang, W., Ito, K., Matte, T. D., Shaman, J., & Kinney, P. L. (2016). Seasonal influenza infections and cardiovascular disease mortality. JAMA Cardiology, 1(3), 274–281. https://doi.org/10.1001/jamacardio.2016.0433
   PubMed Web of Science ®Google Scholar
• Onufriev, A., Bashford, D., & Case, D. A. (2004). Exploring protein native states and large‐scale conformational changes with a modified generalized born model. Proteins: Structure, Function, and Bioinformatics, 55(2), 383–394. https://doi.org/10.1002/prot.20033
   PubMed Web of Science ®Google Scholar
• Pumroy, R. A., & Cingolani, G. (2015). Diversification of importin-a isoforms in cellular trafficking and disease states. Biochemical Journal, 466(1), 13–28. https://doi.org/10.1042/BJ20141186
   PubMedGoogle Scholar
• Qiu, Y., & Xu, K. (2020). Functional studies of the coronavirus nonstructural proteins. STEMedicine, 1(2), e39–e39. https://doi.org/10.37175/stemedicine.v1i2.39
   Google Scholar
• Schrödinger, LLC. (2016). Maestro, version 10.5. 2016–1.
   Google Scholar
• Sen Gupta, P. S., Biswal, S., Panda, S. K., Ray, A. K., & Rana, M. K. (2020). Binding mechanism and structural insights into the identified protein target of COVID-19 and importin-α with in-vitro effective drug ivermectin. Journal of Biomolecular Structure and Dynamics, 1–10.
   Web of Science ®Google Scholar
• Shu, B., & Gong, P. (2016). Structural basis of viral RNA-dependent RNA polymerase catalysis and translocation. Proceedings of the National Academy of Sciences, 113(28), E4005–E4014.
   PubMed Web of Science ®Google Scholar
• Sutton, G., Fry, E., Carter, L., Sainsbury, S., Walter, T., Nettleship, J., Berrow, N., Owens, R., Gilbert, R., Davidson, A., Siddell, S., Poon, L. L. M., Diprose, J., Alderton, D., Walsh, M., Grimes, J. M., & Stuart, D. I. (2004). The nsp9 Replicase Protein of SARS-coronavirus, structure and functional insights. Structure (London, England : 1993), 12(2), 341–353. https://doi.org/10.1016/j.str.2004.01.016
   PubMed Web of Science ®Google Scholar
• Tay, M. Y. F., Smith, K., Ng, I. H. W., Chan, K. W. K., Zhao, Y., Ooi, E. E., Lescar, J., Luo, D., Jans, D. A., Forwood, J. K., & Vasudevan, S. G. (2016). The C-terminal 18 amino acid region of dengue virus NS5 regulates its subcellular localization and contains a conserved arginine residue essential for infectious virus production. PLoS Pathogens, 12(9), e1005886. https://doi.org/10.1371/journal.ppat.1005886
   PubMed Web of Science ®Google Scholar
• Van Gunsteren, W. F., & Berendsen, H. J. C. (1977). Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics, 34(5), 1311–1327. ehttps://doi.org/10.1080/00268977700102571
   Web of Science ®Google Scholar
• Wagstaff, K. M., Sivakumaran, H., Heaton, S. M., Harrich, D., & Jans, D. A. (2012). Ivermectin is a specific inhibitor of importin a/b-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus. Biochemical Journal, 443(3), 851–856. https://doi.org/10.1042/BJ20120150
   PubMed Web of Science ®Google Scholar
• Walls, A. C., Park, Y. J., Tortorici, M. A., Wall, A., McGuire, A. T., Veesler, D., & Alexandra, C. W. (2020). Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell, 181(2), 281–292. https://doi.org/10.1016/j.cell.2020.02.058
   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
• Woo, P. C., Huang, Y., Lau, S. K., & Yuen, K. Y. (2010). Coronavirus genomics and bioinformatics analysis. Viruses, 2(8), 1804–1820. https://doi.org/10.3390/v2081803
   PubMed Web of Science ®Google Scholar
• Wu, C., Liu, Y., Yang, Y., Zhang, P., Zhong, W., Wang, Y., Wang, Q., Xu, Y., Li, M., Li, X., Zheng, M., Chen, L., & Li, H. (2020). Analysis of therapeutic targets for SARS-CoV-2 and discovery of potential drugs by computational methods. Acta Pharmaceutica Sinica B, 10(5), 766–788. https://doi.org/10.1016/j.apsb.2020.02.008
   PubMed Web of Science ®Google Scholar
• Yamasmith, E. (2018). Efficacy and safety of ivermectin against dengue infection: A phase III, randomized, double-blind, placebo-controlled trial [Paper presentation]. 34th Annual Meeting the Royal College of Physicians of Thailand. Internal Medicine and One Health.
   Google Scholar
• Yang, S. N. Y., Atkinson, S. C., Fraser, J. E., Wang, C., Maher, B., Roman, N., Forwood, J. K., Wagstaff, K. M., Borg, N. A., & Jans, D. A. (2019). Novel flavivirus antiviral that targets the host nuclear transport importin a/b1 heterodimer. Cells, 8(3), 281. https://doi.org/10.3390/cells8030281
   PubMed Web of Science ®Google Scholar
• Zhang, L., Lin, D., Sun, X., Curth, U., Drosten, C., Sauerhering, L., Becker, S., Rox, K., & Hilgenfeld, R. (2020). Crystal structure of SARS-CoV-2 main protease provides a basis for design of improved α-ketoamide inhibitors. Science, 368(6489), 409–412. https://doi.org/10.1126/science.abb3405
   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