Structures and dynamics of peptide and peptidomimetic inhibitors bound to the NS2B-NS3 protease of the ZIKA virus

References

• Agumadu, V. C., & Ramphul, K. (2018). Zika Virus: a review of literature. Cureus, 10, e3025. https://doi.org/10.7759/cureus.3025
   PubMed Web of Science ®Google Scholar
• Antoniou, E., Orovou, E., Sarella, A., Iliadou, M., Rigas, N., Palaska, E., Iatrakis, G., & Dagla, M. (2020). Zika virus and the risk of developing microcephaly in infants: A systematic review. International Journal of Environmental Research and Public Health, 17. https://doi.org/10.3390/ijerph17113806
   Google Scholar
• Bernatchez, J. A., Tran, L. T., Li, J., Luan, Y., Siqueira-Neto, J. L., & Li, R. (2020). Drugs for the treatment of Zika virus infection. Journal of Medicinal Chemistry, 63, 470–489. https://doi.org/10.1021/acs.jmedchem.9b00775
   PubMed Web of Science ®Google Scholar
• Besnard, M., Eyrolle-Guignot, D., Guillemette-Artur, P., Lastere, S., Bost-Bezeaud, F., Marcelis, L., Abadie, V., Garel, C., Moutard, M. L., Jouannic, J. M., Rozenberg, F., Leparc-Goffart, I., & Mallet, H. P. (2016). Congenital cerebral malformations and dysfunction in fetuses and newborns following the 2013 to 2014 Zika virus epidemic in French Polynesia. European Communicable Disease Bulletin [Euro Surveillance: bulletin Europeen Sur Les Maladies Transmissibles], 21(13). http://dx.doi.org/10.2807/1560-7917.ES.2016.21.13.30181
   Google Scholar
• Boldescu, V., Behnam, M. A. M., Vasilakis, N., & Klein, C. D. (2017). Broad-spectrum agents for flaviviral infections: dengue, Zika and beyond. Nature Reviews. Drug Discovery, 16, 565–586. https://doi.org/10.1038/nrd.2017.33
   PubMed Web of Science ®Google Scholar
• Brecher, M., Zhang, J., & Li, H. (2013). The flavivirus protease as a target for drug discovery. Virologica Sinica, 28, 326–336. https://doi.org/10.1007/s12250-013-3390-x
   PubMedGoogle Scholar
• Chen, Q., Gouilly, J., Ferrat, Y. J., Espino, A., Glaziou, Q., Cartron, G., El Costa, H., Al-Daccak, R., & Jabrane-Ferrat, N. (2020). Metabolic reprogramming by Zika virus provokes inflammation in human placenta. Nature Communications, 11, 2967. https://doi.org/10.1038/s41467-020-16754-z
   PubMed Web of Science ®Google Scholar
• Chibueze, E. C., Tirado, V., Lopes, K. D., Balogun, O. O., Takemoto, Y., Swa, T., Dagvadorj, A., Nagata, C., Morisaki, N., Menendez, C., Ota, E., Mori, R., & Oladapo, O. T. (2017). Zika virus infection in pregnancy: a systematic review of disease course and complications. Reproductive Health, 14, 28. https://doi.org/10.1186/s12978-017-0285-6
   PubMed Web of Science ®Google Scholar
• Gulland, A. (2016). Zika virus is a global public health emergency, declares WHO. BMJ, 352, i657. https://doi.org/10.1136/bmj.i657
   PubMed Web of Science ®Google Scholar
• Hilgenfeld, R., Lei, J., & Zhang, L. (2018). The structure of the Zika virus protease, NS2B/NS3(pro). Advances in Experimental Medicine and Biology, 1062, 131–145.
   PubMed Web of Science ®Google Scholar
• Jena, N. R., Pant, S., & Srivastava, H. K. (2021). Artificially expanded genetic information systems (AEGISs) as potent inhibitors of the RNA-dependent RNA polymerase of the SARS-CoV-2. Journal of Biomolecular Structure & Dynamics, 1–17. https://doi.org/10.1080/07391102.2021.1883112
   Google Scholar
• Kang, C. B., Gayen, S., Wang, W., Severin, R., et. al. (2013). Exploring the binding of peptidic West Nile virus NS2B-NS3 protease inhibitors by NMR. Antiviral Res, 97, 137–144.
   PubMed Web of Science ®Google Scholar
• Kang, C., Keller, T. H., & Luo, D. (2017). Zika virus protease: an antiviral drug target. Trends in Microbiology, 25, 797–808. https://doi.org/10.1016/j.tim.2017.07.001
   PubMed Web of Science ®Google Scholar
• 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, 18132–18141. https://doi.org/10.1021/acsomega.8b01002
   PubMed Web of Science ®Google Scholar
• Lei, J., Hansen, G., Nitsche, C., Klein, C. D., Zhang, L., & Hilgenfeld, R. (2016). Crystal structure of Zika virus NS2B-NS3 protease in complex with a boronate inhibitor. Science, 353, 503–505. https://doi.org/10.1126/science.aag2419
   PubMed Web of Science ®Google Scholar
• Li, Y., Loh, Y. R., Hung, A. W., & Kang, C. B. (2018). Characterization of molecular interactions between Zika virus protease and peptides derived from the C-terminus of NS2B. Biochemical and Biophysical Research Communications, 503, 691–696. https://doi.org/10.1016/j.bbrc.2018.06.062
   PubMed Web of Science ®Google Scholar
• Li, Y., Zhang, Z., Phoo, W. W., Loh, Y. R., Li, R., Yang, H. Y., Jansson, A. E., Hill, J., Keller, T. H., Nacro, K., Luo, D., & Kang, C. (2018). Structural insights into the inhibition of Zika virus NS2B-NS3 protease by a small-molecule inhibitor. Structure, 26, 555–564. e3
   PubMed Web of Science ®Google Scholar
• Li, Y., Zhang, Z., Phoo, W. W., Loh, Y. R., Wang, W., Liu, S., Chen, M. W., Hung, A. W., Keller, T. H., Luo, D., & Kang, C. (2017). Structural dynamics of Zika virus NS2B-NS3 protease binding to dipeptide inhibitors. Structure, 25, 1242–1250 e3. https://doi.org/10.1016/j.str.2017.06.006
   PubMed Web of Science ®Google Scholar
• Lu, C., Wu, C., Ghoreishi, D., Chen, W., Wang, L., Damm, W., Ross, G. A., Dahlgren, M. K., Russell, E., Von Bargen, C. D., Abel, R., Friesner, R. A., & Harder, E. D. (2021). OPLS4: Improving force field accuracy on challenging regimes of chemical space. Journal of Chemical Theory and Computation, 17, 4291–4300. https://doi.org/10.1021/acs.jctc.1c00302
   PubMed Web of Science ®Google Scholar
• Martyna, G. J., Tobias, D. J., & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. The Journal of Chemical Physics, 101, 4177–4189. https://doi.org/10.1063/1.467468
   Web of Science ®Google Scholar
• Mecharles, S., Herrmann, C., Poullain, P., Tran, T. H., Deschamps, N., Mathon, G., Landais, A., Breurec, S., & Lannuzel, A. (2016). Acute myelitis due to Zika virus infection. Lancet, 387, 1481. https://doi.org/10.1016/S0140-6736(16)00644-9
   PubMed Web of Science ®Google Scholar
• Morabito, K. M., & Graham, B. S. (2017). Zika virus vaccine development. The Journal of Infectious Diseases, 216, S957–S963. https://doi.org/10.1093/infdis/jix464
   PubMed Web of Science ®Google Scholar
• Noble, C. G., Seh, C. C., Chao, A. T., & Shi, P. Y. (2012). Ligand-bound structures of the Dengue virus protease reveal the active conformation. Journal of Virology, 86, 438–446. https://doi.org/10.1128/JVI.06225-11
   PubMed Web of Science ®Google Scholar
• Pant, S., & Jena, N. R. (2021). Inhibition of the RNA-dependent RNA polymerase of the SARS-CoV-2 by short peptide inhibitors. European Journal of Pharmaceutical Sciences: official Journal of the European Federation for Pharmaceutical Sciences, 167, 106012. https://doi.org/10.1016/j.ejps.2021.106012
   PubMed Web of Science ®Google Scholar
• Parra, B., Lizarazo, J., Jiménez-Arango, J. A., Zea-Vera, A. F., González-Manrique, G., Vargas, J., Angarita, J. A., Zuñiga, G., Lopez-Gonzalez, R., Beltran, C. L., Rizcala, K. H., Morales, M. T., Pacheco, O., Ospina, M. L., Kumar, A., Cornblath, D. R., Muñoz, L. S., Osorio, L., Barreras, P., & Pardo, C. A. (2016). Guillain–Barré syndrome associated with Zika virus infection in Colombia. New England Journal of Medicine, 375, 1513–1523. https://doi.org/10.1056/NEJMoa1605564
   PubMed Web of Science ®Google Scholar
• Pathak, N., Kuo, Y. P., Chang, T. Y., Huang, C. T., Hung, H. C., Hsu, J. T., Yu, G. Y., & Yang, J. M. (2020). Zika Virus NS3 protease pharmacophore anchor model and drug discovery. Scientific Reports, 10, 8929. https://doi.org/10.1038/s41598-020-65489-w
   PubMed Web of Science ®Google Scholar
• Petersen, H. G. (1995). Accuracy and efficiency of the particle mesh Ewald method. The Journal of Chemical Physics, 103, 3668–3679. https://doi.org/10.1063/1.470043
   Web of Science ®Google Scholar
• Phoo, W. W., Li, Y., Zhang, Z., Lee, M. Y., Loh, Y. R., Tan, Y. B., Ng, E. Y., Lescar, J., Kang, C., & Luo, D. (2016). Structure of the NS2B-NS3 protease from Zika virus after self-cleavage. Nature Communications, 7, 13410. https://doi.org/10.1038/ncomms13410
   PubMed Web of Science ®Google Scholar
• Phoo, W. W., Zhang, Z., Wirawan, M., Chew, E. J. C., Chew, A. B. L., Kouretova, J., Steinmetzer, T., & Luo, D. (2018). Structures of Zika virus NS2B-NS3 protease in complex with peptidomimetic inhibitors. Antiviral Research, 160, 17–24. https://doi.org/10.1016/j.antiviral.2018.10.006
   PubMed Web of Science ®Google Scholar
• Posch, H. A., Hoover, W. G., & Vesely, F. J. (1986). Canonical dynamics of the Nose oscillator: Stability, order, and chaos. Physical Review. A, General Physics, 33, 4253–4265. https://doi.org/10.1103/physreva.33.4253
   PubMedGoogle Scholar
• Poulsen, A., Kang, C., & Keller, T. H. (2014). Drug design for flavivirus proteases: what are we missing? Current Pharmaceutical Design, 20, 3422–3427. https://doi.org/10.2174/13816128113199990633
   PubMed Web of Science ®Google Scholar
• Proceedings of the 2006 ACM/IEEE conference on Supercomputing (2006). Tampa, Florida, Association for Computing Machinery.
   Google Scholar
• Robin, G., Chappel, K., Stoermer, M. J., Hu, S.-H., Young, P. R., Fairlie, D. P., & Martin, J. L. (2009). Structure of West Nile virus NS3 protease: ligand stabilization of the catalytic conformation. Journal of Molecular Biology., 385, 1568–1577.
   PubMed Web of Science ®Google Scholar
• Saputro, D. R. S., & Widyaningsih, P. 2017. Limited memory Broyden-Fletcher-Goldfarb-Shanno (L-BFGS) method for the parameter estimation on geographically weighted ordinal logistic regression model (GWOLR). AIP Conference Proceedings 2017, 1868, 040009.
   Google Scholar
• Schrödinger Release. (2021). 2021-4: Desmond Molecular Dynamics System. D. E. Shaw Research. 2021. Maestro-Desmond Interoperability Tools, Schrödinger,
   Google Scholar
• Sejal, Z. Y., Patel, J., Wang, W.-L., et. al. (2006). Peptide inhibitors of Dengu virus NS3 protease. Part 1: Warheads. Bioorganic and Medicinal Chemistry Letters, 16, 36–39. https://doi.org/10.1016/j.bmcl.2005.09.062
   PubMed Web of Science ®Google Scholar
• Sharma, V., Sharma, M., Dhull, D., Sharma, Y., Kaushik, S., & Kaushik, S. (2020). Zika virus: an emerging challenge to public health worldwide. Canadian Journal of Microbiology, 66, 87–98. https://doi.org/10.1139/cjm-2019-0331
   PubMed Web of Science ®Google Scholar
• Sirohi, D., & Kuhn, R. J. (2017). Zika virus structure, maturation, and receptors. The Journal of Infectious Diseases, 216, S935–S944. https://doi.org/10.1093/infdis/jix515
   PubMed Web of Science ®Google Scholar
• Schrödinger, L. & DeLano, W. (2020). PyMOL, Available at: http://www.pymol.org/pymol.
   Google Scholar
• Voss, S., & Nitsche, C. (2020). Inhibitors of the Zika virus protease NS2B-NS3. Bioorganic & Medicinal Chemistry Letters, 30, 126965. https://doi.org/10.1016/j.bmcl.2020.126965
   PubMed Web of Science ®Google Scholar
• Wen, Z., Song, H., & Ming, G. L. (2017). How does Zika virus cause microcephaly? Genes & Development, 31, 849–861. https://doi.org/10.1101/gad.298216.117
   PubMed Web of Science ®Google Scholar
• Zielkiewicz, J. (2005). Structural properties of water: Comparison of the SPC, SPCE, TIP4P, and TIP5P models of water. The Journal of Chemical Physics, 123, 104501. https://doi.org/10.1063/1.2018637
   PubMed Web of Science ®Google Scholar