Conformer and pharmacophore based identification of peptidomimetic inhibitors of chikungunya virus nsP2 protease

References

• ACD/structure elucidator, version 12. (2013). Toronto, ON: Advanced Chemistry Development. www.acdlabs.com.
   Google Scholar
• Aggarwal, M., Dhindwal, S., Kumar, P., Kuhn, R. J., & Tomar, S. (2014). Trans-protease activity and structural insights into the active form of the alphavirus capsid protease. Journal of Virology, 88, 12242–12253.10.1128/JVI.01692-14
   PubMed Web of Science ®Google Scholar
• Aggarwal, M., Dhindwal, S., Pratap, S., Kuhn, R. J., Kumar, P., & Tomar, S. (2011). Crystallization, high-resolution data collection and preliminary crystallographic analysis of Aura virus capsid protease and its complex with dioxane. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 67, 1394–1398.
   PubMedGoogle Scholar
• Aggarwal, M., Sharma, R., Kumar, P., Parida, M., & Tomar, S. (2015). Kinetic characterization of trans-proteolytic activity of Chikungunya virus capsid protease and development of a FRET-based HTS assay. Scientific Reports, 5, 14753.10.1038/srep14753
   PubMed Web of Science ®Google Scholar
• Aggarwal, M., Tapas, S., Preeti, S. A., Kumar, P., Kuhn, R. J., & Tomar, S. (2012). Crystal structure of aura virus capsid protease and its complex with dioxane: New insights into capsid-glycoprotein molecular contacts. PLoS ONE, 7, e51288.10.1371/journal.pone.0051288
   PubMed Web of Science ®Google Scholar
• Akhrymuk, I., Kulemzin, S. V., & Frolova, E. I. (2012). Evasion of the innate immune response: The old world alphavirus nsP2 protein induces rapid degradation of Rpb1, a catalytic subunit of RNA polymerase II. Journal of Virology, 86, 7180–7191.10.1128/JVI.00541-12
   PubMed Web of Science ®Google Scholar
• Avan, I., Hall, C. D., & Katritzky, A. R. (2014). Peptidomimetics via modifications of amino acids and peptide bonds. Chemical Society Reviews, 43, 3575–3594.10.1039/c3cs60384a
   PubMed Web of Science ®Google Scholar
• Case, D. A., Darden, T. A., Cheatham, T. E., Simmerling, C. L., Wang, J., Duke, R. E., … Merz, K. M. (2010). Amber 11. San Francisco, CA: University of California.
   Google Scholar
• DeLano, W. L. (2002). The PyMOL molecular graphics system, DeLano Scientific, Palo Alto, CA.
   Google Scholar
• Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U., & Ball, L. A. (2005). Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses. London: Academic Press.
   Google Scholar
• Floris, M., Masciocchi, J., Fanton, M., & Moro, S. (2011). Swimming into peptidomimetic chemical space using pepMMsMIMIC. Nucleic Acids Research, 39, W261–W269.10.1093/nar/gkr287
   PubMed Web of Science ®Google Scholar
• Freidinger, R. M. (2003). Design and synthesis of novel bioactive peptides and peptidomimetics. Journal of Medicinal Chemistry, 46, 5553–5566.10.1021/jm030484k
   PubMed Web of Science ®Google Scholar
• Freidinger, R. M., Perlow, D. S., & Veber, D. F. (1982). Protected lactam-bridged dipeptides for use as conformational constraints in peptides. The Journal of Organic Chemistry, 47, 104–109.10.1021/jo00340a023
   Web of Science ®Google Scholar
• Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., … Perry, J. K. (2004). Glide: A new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. Journal of Medicinal Chemistry, 47, 1739–1749.10.1021/jm0306430
   PubMed Web of Science ®Google Scholar
• Fros, J. J., Liu, W. J., Prow, N. A., Geertsema, C., Ligtenberg, M., Vanlandingham, D. L., … Pijlman, G. P. (2010). Chikungunya virus nonstructural protein 2 inhibits type I/II interferon-stimulated JAK-STAT signaling. Journal of Virology, 84, 10877–10887.10.1128/JVI.00949-10
   PubMed Web of Science ®Google Scholar
• Gante, J. (1994). Peptidomimetics-tailored enzyme inhibitors. Angewandte Chemie International Edition in English, 33, 1699–1720.10.1002/(ISSN)1521-3773
   Web of Science ®Google Scholar
• Goede, A., Michalsky, E., Schmidt, U., & Preissner, R. (2006). SuperMimic – Fitting peptide mimetics into protein structures. BMC Bioinformatics, 7, 11–15.10.1186/1471-2105-7-11
   PubMed Web of Science ®Google Scholar
• Gomis-Rüth, F. X., Meyer, E. F., Kress, L. F., & Politi, V. (1998). Structures of adamalysin II with peptidic inhibitors. Implications for the design of tumor necrosis factor alpha convertase inhibitors. Protein Science, 7, 283–292.
   PubMed Web of Science ®Google Scholar
• Hardy, W. R., & Strauss, J. H. (1989). Processing the nonstructural polyproteins of sindbis virus: Nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and in trans. Journal of Virology, 63, 4653–4664.
   PubMed Web of Science ®Google Scholar
• Hruby, V. J. (1997). Prospects for peptidomimetic drug design. Drug Discovery Today, 2, 165–167.10.1016/S1359-6446(96)20009-1
   Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38.10.1016/0263-7855(96)00018-5
   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. The Journal of Chemical Physics, 79, 926–935.10.1063/1.445869
   Web of Science ®Google Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., … Wang, W. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33, 889–897.10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Loughlin, W. A., Tyndall, J. D., Glenn, M. P., Hill, T. A., & Fairlie, D. P. (2010). Update 1 of: Beta-strand mimetics. Chemical Reviews, 110, PR32–PR69.
   PubMed Web of Science ®Google Scholar
• Lulla, A., Lulla, V., Tints, K., Ahola, T., & Merits, A. (2006). Molecular determinants of substrate specificity for semliki forest virus nonstructural protease. Journal of Virology, 80, 5413–5422.10.1128/JVI.00229-06
   PubMed Web of Science ®Google Scholar
• Luthman, K., & Hacksell, U. (2002). Peptides and peptidomimetics. In P. Krogsgaard-Larsen, T. Liljefors, & U. Madsen (Eds.), Textbook of Drug Design and Discovery (3rd Edition) (pp. 459–485). London: Taylor & Francis.
   Google Scholar
• Merits, A., Vasiljeva, L., Ahola, T., Kääriäinen, L., & Auvinen, P. (2001). Proteolytic processing of Semliki Forest virus-specific non-structural polyprotein by nsP2 protease. Journal of General Virology, 82, 765–773.10.1099/0022-1317-82-4-765
   PubMed Web of Science ®Google Scholar
• Ogbu, C. O., Qabar, M. N., Boatman, P. D., Urban, J., Meara, J. P., Ferguson, M. D., … Kahn, M. (1998). Highly efficient and versatile synthesis of libraries of constrained beta-strand mimetics. Bioorganic & Medicinal Chemistry Letters, 8, 2321–2326.10.1016/S0960-894X(98)00420-X
   PubMed Web of Science ®Google Scholar
• Olboyle, 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, 33–47.10.1186/1758-2946-3-33
   PubMed Web of Science ®Google Scholar
• Pardigon, N. (2009). The biology of Chikungunya: A brief review of what we still do not know. Pathologie Biologie, 57, 127–132.10.1016/j.patbio.2008.02.016
   PubMed Web of Science ®Google Scholar
• Pastorino, B. A. M., Peyrefitte, C. N., Almeras, L., Grandadam, M., Rolland, D., Tolou, H. J., & Bessaud, M. I. (2008). Expression and biochemical characterization of nsP2 cysteine protease of Chikungunya virus. Virus Research, 131, 293–298.10.1016/j.virusres.2007.09.009
   PubMed Web of Science ®Google Scholar
• Polgar, L. (1974). Mercaptide-imidazolium ion-pair: The reactive nucleophile in papain catalysis. FEBS Letters, 47, 15–18.10.1016/0014-5793(74)80415-1
   PubMed Web of Science ®Google Scholar
• Powers, A. M., & Logue, C. H. (2007). Changing patterns of chikungunya virus: Re-emergence of a zoonotic arbovirus. Journal of General Virology, 88, 2363–2377.10.1099/vir.0.82858-0
   PubMed Web of Science ®Google Scholar
• Qabar, M., Urban, J., Sia, C., Klein, M., & Kahn, M. (1996). Pharmaceutical applications of peptidomimetics. Letters in Peptide Science, 3, 25–30.10.1007/BF00131082
   Google Scholar
• Queyriaux, B., Simon, F., Grandadam, M., Michel, R., Tolou, H., & Boutin, J.-P. (2008). Clinical burden of chikungunya virus infection. The Lancet Infectious Diseases, 8, 2–3.10.1016/S1473-3099(07)70294-3
   PubMed Web of Science ®Google Scholar
• Randolph, J. T., & DeGoey, D. A. (2004). Peptidomimetic inhibitors of HIV protease. Current Topics in Medicinal Chemistry, 4, 1079–1095.10.2174/1568026043388330
   PubMed Web of Science ®Google Scholar
• Ravi, V. (2006). Re-emergence of Chikungunya virus in India. Indian Journal of Medical Microbiology, 24, 83–84.10.4103/0255-0857.25175
   PubMedGoogle Scholar
• Renault, P., Solet, J. L., Sissoko, D., Balleydier, E., Larrieu, S., Filleul, L., … Pierre, V. (2007). A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. The American Journal of Tropical Medicine and Hygiene, 77, 727–731.
   PubMed Web of Science ®Google Scholar
• Rigau-Pérez, J. G., Clark, G. G., Gubler, D. J., Reiter, P., Sanders, E. J., & Vance Vorndam, A. (1998). Dengue and dengue haemorrhagic fever. The Lancet, 352, 971–977.10.1016/S0140-6736(97)12483-7
   PubMed Web of Science ®Google Scholar
• Russo, A. T., Malmstrom, R. D., White, M. A., & Watowich, S. J. (2010). Structural basis for substrate specificity of alphavirus nsP2 proteases. Journal of Molecular Graphics and Modelling, 29, 46–53.10.1016/j.jmgm.2010.04.005
   PubMed Web of Science ®Google Scholar
• Russo, A. T., White, M. A., & Watowich, S. J. (2006). The crystal structure of the venezuelan equine encephalitis alphavirus nsP2 protease. Structure, 14, 1449–1458.10.1016/j.str.2006.07.010
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. Journal of Computational Physics, 23, 327–341.10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Sanderson, P. E., Lyle, T. A., Cutrona, K. J., Dyer, D. L., Dorsey, B. D., McDonough, C. M., … Vacca, J. P. (1998). Efficacious, orally bioavailable thrombin inhibitors based on 3-aminopyridinone or 3-aminopyrazinone acetamide peptidomimetic templates. Journal of Medicinal Chemistry, 41, 4466–4474.10.1021/jm980368v
   PubMed Web of Science ®Google Scholar
• 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, 221–234.10.1007/s10822-013-9644-8
   PubMed Web of Science ®Google Scholar
• Semple, J. E., Levy, O. E., Minami, N. K., Owens, T. D., & Siev, D. V. (1998). Novel, potent and selective chimeric FXa inhibitors featuring hydrophobic P-1-ketoamide moieties. Bioorganic & Medicinal Chemistry Letters, 10, 2305–2309.
   Web of Science ®Google Scholar
• Shah, K. V., Gibbs, Jr., C. J., & Banerjee, G. (1964). Virological investigation of the epidemic of haemorrhagic fever in Calcutta: Isolation of three strains of Chikungunya virus. Indian Journal of Medical Research, 52, 676–683.
   PubMed Web of Science ®Google Scholar
• Sharma, R., Fatma, B., Saha, A., Bajpai, S., Sistla, S., Dash, P. K., … Tomar, S. (2016). Inhibition of chikungunya virus by picolinate that targets viral capsid protein. Virology, 498, 265–276.10.1016/j.virol.2016.08.029
   PubMed Web of Science ®Google Scholar
• Shin, G., Yost, S. A., Miller, M. T., Elrod, E. J., Grakoui, A., & Marcotrigiano, J. (2012). Structural and functional insights into alphavirus polyprotein processing and pathogenesis. Proceedings of the National Academy of Sciences, 109, 16534–16539.10.1073/pnas.1210418109
   PubMed Web of Science ®Google Scholar
• Simizu, B., Yamamoto, K., Hashimoto, K., & Ogata, T. (1984). Structural proteins of Chikungunya virus. Journal of Virology, 51, 254–258.
   PubMed Web of Science ®Google Scholar
• Smith, 3rd, A. B., Hirschmann, R., Pasternak, A., Akaishi, R., Guzman, M. C., Jones, D. R., … Schleif, W. A. (1994). Design and synthesis of peptidomimetic inhibitors of HIV-1 protease and renin. Evidence for improved transport. Journal of Medicinal Chemistry, 37, 215–218.10.1021/jm00028a001
   PubMed Web of Science ®Google Scholar
• St Charles, R., Matthews, J. H., Zhang, E., & Tulinksy, A. (1999). Bound structures of novel P3–P1’ beta-strand mimetic inhibitors of thrombin. Journal of Medicinal Chemistry, 42, 1376–1383.10.1021/jm980052n
   PubMed Web of Science ®Google Scholar
• Staples, J. E., Breiman, R. F., & Powers, A. M. (2009). Chikungunya fever: An epidemiological review of a re-emerging infectious disease. Clinical Infectious Diseases, 49, 942–948.10.1086/599189
   PubMed Web of Science ®Google Scholar
• Strauss, E. G., De Groot, R. J., Levinson, R., & Strauss, J. H. (1992). Identification of the active site residues in the nsP2 proteinase of sindbis virus. Virology, 191, 932–940.10.1016/0042-6822(92)90268-T
   PubMed Web of Science ®Google Scholar
• Strauss, J. H., & Strauss, E. G. (1994). The alphaviruses: Gene expression, replication, and evolution. Microbiology and Molecular Biology Reviews, 58, 491–562.
   Google Scholar
• Tamura, S. Y., Semple, J. E., Reiner, J. E., Goldman, E. A., Brunck, T. K., Lim-Wilby, M. S., … Ripka, W. C. (1997). Design and synthesis of a novel class of thrombin inhibitors incorporating heterocyclic dipeptide surrogates. Bioorganic & Medicinal Chemistry Letters, 7, 1543–1548.10.1016/S0960-894X(97)00258-8
   Web of Science ®Google Scholar
• Taubitz, W., Cramer, J. P., Kapaun, A., Pfeffer, M., Drosten, C., Dobler, G., … Löscher, T. (2007). Chikungunya fever in travelers: Clinical presentation and course. Clinical Infectious Diseases, 45, e1–e4.10.1086/518701
   PubMed Web of Science ®Google Scholar
• Tomar, S., Hardy, R. W., Smith, J. L., & Kuhn, R. J. (2006). Catalytic core of alphavirus nonstructural protein nsP4 possesses terminal adenylyltransferase activity. Journal of Virology, 80, 9962–9969.10.1128/JVI.01067-06
   PubMed Web of Science ®Google Scholar
• Tomar, S., Narwal, M., Harms, E., Smith, J. L., & Kuhn, R. J. (2011). Heterologous production, purification and characterization of enzymatically active Sindbis virus nonstructural protein nsP1. Protein Expression and Purification, 79, 277–284.10.1016/j.pep.2011.05.022
   PubMed Web of Science ®Google Scholar
• Turner, P. J. (2005). XMGRACE, version 5.1. 19. Beaverton, OR: Center for Coastal and Land-Margin Research, Oregon Graduate Institute of Science and Technology.
   Google Scholar
• Vagner, J., Qu, H., & Hruby, V. J. (2008). Peptidomimetics, a synthetic tool of drug discovery. Current Opinion in Chemical Biology, 12, 292–296.10.1016/j.cbpa.2008.03.009
   PubMed Web of Science ®Google Scholar
• Vasiljeva, L., Valmu, L., Kaariainen, L., & Merits, A. (2001). Site-specific protease activity of the carboxyl-terminal domain of Semliki Forest virus replicase protein nsP2. Journal of Biological Chemistry, 276, 30786–30793.10.1074/jbc.M104786200
   PubMed Web of Science ®Google Scholar
• Wang, J., Wang, W., Kollman, P. A., & Case, D. A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics and Modelling, 25, 247–260.10.1016/j.jmgm.2005.12.005
   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, 1157–1174.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Weber, P. J., Bader, J. E., Folkers, G., & Beck-Sickinger, A. G. (1998). A fast and inexpensive method for N-terminal fluorescein-labeling of peptides. Bioorganic & Medicinal Chemistry Letters, 8, 597–600.10.1016/S0960-894X(98)00084-5
   PubMed Web of Science ®Google Scholar