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Research Articles

Identification of a C2-symmetric diol based human immunodeficiency virus protease inhibitor targeting Zika virus NS2B-NS3 protease

, , , ORCID Icon, , & show all
Pages 5526-5536 | Received 01 Nov 2019, Accepted 06 Dec 2019, Published online: 27 Dec 2019

References

  • Akaberi, D., Bergfors, A., Kjellin, M., Kameli, N., Lidemalm, L., Kolli, B., … Lennerstrand, J. (2018). Baseline dasabuvir resistance in Hepatitis C virus from the genotypes 1, 2 and 3 and modeling of the NS5B-dasabuvir complex by the in silico approach. Infection Ecology & Epidemiology, 8(1). doi:10.1080/20008686.2018.1528117
  • Almlöf, M., Carlsson, J., & Åqvist, J. (2007). Improving the accuracy of the linear interaction energy method for solvation free energies. Journal of Chemical Theory and Computation, 3(6), 2162–2175. doi:10.1021/ct700106b
  • Bauer, P., Barrozo, A., Purg, M., Amrein, B. A., Esguerra, M., Wilson, P. B., … Kamerlin, S. C. L. (2018). Q6: A comprehensive toolkit for empirical valence bond and related free energy calculations. SoftwareX, 7, 388–395. doi:10.1016/j.softx.2017.12.001
  • Behnam, M. A. M., Graf, D., Bartenschlager, R., Zlotos, D. P., & Klein, C. D. (2015). Discovery of nanomolar Dengue and West Nile virus protease inhibitors containing a 4-benzyloxyphenylglycine residue. Journal of Medicinal Chemistry, 58(23), 9354–9370. doi:10.1021/acs.jmedchem.5b01441
  • Cao-Lormeau, V.-M., Roche, C., Teissier, A., Robin, E., Berry, A.-L., Mallet, H.-P., … Musso, D. (2014). Zika Virus, French Polynesia, South Pacific, 2013. Emerging Infectious Diseases, 20(6), 1084–1086. doi:10.3201/eid2006.140138
  • Chambers, T. J., Hahn, C. S., Galler, R., & Rice, C. M. (1990). Flavivirus genome organization, expression, and replication. Annual Review of Microbiology, 44(1), 649–688. doi:10.1146/annurev.mi.44.100190.003245
  • Chan, J. F.-W., Chik, K. K.-H., Yuan, S., Yip, C. C.-Y., Zhu, Z., Tee, K.-M., … Yuen, K.-Y. (2017). Novel antiviral activity and mechanism of bromocriptine as a Zika virus NS2B-NS3 protease inhibitor. Antiviral Research, 141, 29–37. doi:10.1016/j.antiviral.2017.02.002
  • Chappell, K. J., Stoermer, M. J., Fairlie, D. P., & Young, P. R. (2006). Insights to substrate binding and processing by West Nile Virus NS3 protease through combined modeling, protease mutagenesis, and kinetic studies. Journal of Biological Chemistry, 281(50), 38448–38458. doi:10.1074/jbc.M607641200
  • Cheng, Y., & Prusoff, W. H. (1973). Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochemical Pharmacology, 22(23), 3099–3108. doi:10.1016/0006-2952(73)90196-2
  • Dodda, L. S., Cabeza de Vaca, I., Tirado-Rives, J., & Jorgensen, W. L. (2017). LigParGen web server: An automatic OPLS-AA parameter generator for organic ligands. Nucleic Acids Research, 45(W1), W331–W336. doi:10.1093/nar/gkx312
  • D’Ortenzio, E., Matheron, S., Yazdanpanah, Y., de Lamballerie, X., Hubert, B., Piorkowski, G., … Leparc-Goffart, I. (2016). Evidence of sexual transmission of Zika virus. New England Journal of Medicine, 374(22), 2195–2198. doi:10.1056/NEJMc1604449
  • Driggers, R. W., Ho, C.-Y., Korhonen, E. M., Kuivanen, S., Jääskeläinen, A. J., Smura, T., … Vapalahti, O. (2016). Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. New England Journal of Medicine, 374(22), 2142–2151. doi:10.1056/NEJMoa1601824
  • Duffy, M. R., Chen, T.-H., Hancock, W. T., Powers, A. M., Kool, J. L., Lanciotti, R. S., … Hayes, E. B. (2009). Zika virus outbreak on Yap Island, Federated States of Micronesia. New England Journal of Medicine, 360(24), 2536–2543. doi:10.1056/NEJMoa0805715
  • Halgren, T. A. (1996). Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. Journal of Computational Chemistry, 17(5-6), 490–519. doi:10.1002/(SICI)1096-987X(199604)17:5/6<490::AID-JCC1>3.0.CO;2-P
  • Hansson, T., Marelius, J., & Åqvist, J. (1998). Ligand binding affinity prediction by linear interaction energy methods. Journal of Computer-Aided Molecular Design, 12(1), 27–35. doi:10.1023/A:1007930623000
  • Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. doi:10.1021/ct700301q
  • Hsu, K.-C., Chen, Y.-F., Lin, S.-R., & Yang, J.-M. (2011). iGEMDOCK: A graphical environment of enhancing GEMDOCK using pharmacological interactions and post-screening analysis. BMC Bioinformatics, 12(Suppl 1), S33. doi:10.1186/1471-2105-12-S1-S33
  • Jorgensen, W. L., Maxwell, D. S., & Tirado-Rives, J. (1996). Development and testing of the OPLS All-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society, 118(45), 11225–11236. doi:10.1021/ja9621760
  • Kim, S., Thiessen, P. A., Bolton, E. E., Chen, J., Fu, G., Gindulyte, A., … Bryant, S. H. (2016). PubChem substance and compound databases. Nucleic Acids Research, 44(D1), D1202–1213. doi:10.1093/nar/gkv951
  • Kuiper, B. D., Slater, K., Spellmon, N., Holcomb, J., Medapureddy, P., Muzzarelli, K. M., … Kovari, L. C. (2017). Increased activity of unlinked Zika virus NS2B/NS3 protease compared to linked Zika virus protease. Biochemical and Biophysical Research Communications, 492(4), 668–673. doi:10.1016/j.bbrc.2017.03.108
  • Kuno, G., & Chang, G.-J. J. (2007). Full-length sequencing and genomic characterization of Bagaza, Kedougou, and Zika viruses. Archives of Virology, 152(4), 687–696. doi:10.1007/s00705-006-0903-z
  • Lee, H., Ren, J., Nocadello, S., Rice, A. J., Ojeda, I., Light, S., … Johnson, M. E. (2017). Identification of novel small molecule inhibitors against NS2B/NS3 serine protease from Zika virus. Antiviral Research, 139, 49–58. doi:10.1016/j.antiviral.2016.12.016
  • 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(6298), 503–505. doi:10.1126/science.aag2419
  • Leung, D., Abbenante, G., & Fairlie, D. P. (2000). Protease inhibitors: Current status and future prospects. Journal of Medicinal Chemistry, 43(3), 305–341. doi:10.1021/jm990412m
  • Leuw, P. D., & Stephan, C. (2018). Protease inhibitor therapy for hepatitis C virus-infection. Expert Opinion on Pharmacotherapy, 19(6), 577–587. doi:10.1080/14656566.2018.1454428
  • Li, Y., Zhang, Z., Phoo, W. W., Loh, Y. R., Wang, W., Liu, S., … Kang, C. (2017). Structural dynamics of Zika virus NS2B-NS3 protease binding to dipeptide inhibitors. Structure, 25(8), 1242–1250.e3. doi:10.1016/j.str.2017.06.006
  • Lim, H., Nguyen, T. T. H., Kim, N. M., Park, J.-S., Jang, T.-S., & Kim, D. (2017). Inhibitory effect of flavonoids against NS2B-NS3 protease of ZIKA virus and their structure activity relationship. Biotechnology Letters, 39(3), 415–421. doi:10.1007/s10529-016-2261-6
  • Lv, Z., Chu, Y., & Wang, Y. (2015). HIV protease inhibitors: A review of molecular selectivity and toxicity. HIV/AIDS - Research and Palliative Care, 7, 95–104. 10.2147/HIV.S79956.
  • MacNamara, F. N. (1954). Zika virus: A report on three cases of human infection during an epidemic of jaundice in Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 48(2), 139–145. doi:10.1016/0035-9203(54)90006-1
  • Nitsche, C., Zhang, L., Weigel, L. F., Schilz, J., Graf, D., Bartenschlager, R., … Klein, C. D. (2017). Peptide-boronic acid inhibitors of flaviviral proteases: Medicinal chemistry and structural biology. Journal of Medicinal Chemistry, 60(1), 511–516. doi:10.1021/acs.jmedchem.6b01021
  • O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: An open chemical toolbox. Journal of Cheminformatics, 3, 33. doi:10.1186/1758-2946-3-33
  • Oehler, E., Watrin, L., Larre, P., Leparc-Goffart, I., Lastere, S., Valour, F., … Ghawche, F. (2014). Zika virus infection complicated by Guillain-Barre syndrome–case report, French Polynesia, December 2013. Eurosurveillance, 19(9). 10.2807/1560-7917.es2014.19.9.20720.
  • Palanisamy, N., Akaberi, D., & Lennerstrand, J. (2017). Protein backbone flexibility pattern is evolutionarily conserved in the Flaviviridae family: A case of NS3 protease in Flavivirus and Hepacivirus. Molecular Phylogenetics and Evolution, 118, 58–63. doi:10.1016/j.ympev.2017.09.015
  • Phoo, W. W., Li, Y., Zhang, Z., Lee, M. Y., Loh, Y. R., Tan, Y. B., … Luo, D. (2016). Structure of the NS2B-NS3 protease from Zika virus after self-cleavage. Nature Communications, 7(1), 13410. doi:10.1038/ncomms13410
  • Pyring, D., Lindberg, J., Rosenquist, Å., Zuccarello, G., Kvarnström, I., Zhang, H., … Samuelsson, B. (2001). Design and synthesis of potent C2-symmetric diol-based HIV-1 protease inhibitors: Effects of fluoro substitution. Journal of Medicinal Chemistry, 44(19), 3083–3091. doi:10.1021/jm001134q
  • Rawlings, N. D., Barrett, A. J., & Finn, R. (2016). Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Research, 44(D1), D343–D350. doi:10.1093/nar/gkv1118
  • Roth, A., Mercier, A., Lepers, C., Hoy, D., Duituturaga, S., Benyon, E., … Souarès, Y. (2014). Concurrent outbreaks of dengue, chikungunya and Zika virus infections – an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012–2014. Eurosurveillance, 19(41), 20929. doi:10.2807/1560-7917.ES2014.19.41.20929
  • Sandeep, G., Nagasree, K. P., Hanisha, M., & Kumar, M. M. K. (2011). AUDocker LE: A GUI for virtual screening with AUTODOCK Vina. BMC Research Notes, 4 (1), 445. doi:10.1186/1756-0500-4-445
  • Simmonds, P., Becher, P., Collett, M. S., Gould, E. A., Heinz, F. X., Meyers, G., … Bukh, J. (2011). Family Flaviviridae. In Virus taxonomy, classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses (1st ed., pp. 1004–1010). The Netherlands: Elsevier.
  • Sirohi, D., Chen, Z., Sun, L., Klose, T., Pierson, T. C., Rossmann, M. G., & Kuhn, R. J. (2016). The 3.8 Å resolution cryo-EM structure of Zika virus. Science, 352(6284), 467–470. doi:10.1126/science.aaf5316
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. Journal of Computational Chemistry, 31(2), 455–461. doi:10.1002/jcc.21334
  • World Health Organization. (2016). Zika situation report: Zika virus, microcephaly and Guillain Barré syndrome. Retrieved from https://apps.who.int/iris/bitstream/handle/10665/204491/zikasitrep_26Feb2016_eng.pdf;jsessionid=0AD32F347339C536879C0EC1777A779A?sequence=1
  • Yuan, S., Chan, J. F.-W., den-Haan, H., Chik, K. K.-H., Zhang, A. J., Chan, C. C.-S., … Yuen, K.-Y. (2017). Structure-based discovery of clinically approved drugs as Zika virus NS2B-NS3 protease inhibitors that potently inhibit Zika virus infection in vitro and in vivo. Antiviral Research, 145, 33–43. doi:10.1016/j.antiviral.2017.07.007
  • Zhang, Z., Li, Y., Loh, Y. R., Phoo, W. W., Hung, A. W., Kang, C., & Luo, D. (2016). Crystal structure of unlinked NS2B-NS3 protease from Zika virus. Science, 354(6319), 1597–1600. doi:10.1126/science.aai9309