Ligand-based virtual screening, molecular dynamics, and biological evaluation of repurposed drugs as inhibitors of Trypanosoma cruzi proteasome

References

• Adams, J. (2003). The proteasome: Structure, function, and role in the cell, Cancer. Cancer Treatment Reviews, 29, 3–9. https://doi.org/10.1016/S0305-7372(03)00081-1
   PubMed Web of Science ®Google Scholar
• Agarwala, R., Barrett, T., Beck, J., Benson, D. A., Bollin, C., Bolton, E., … Zbicz, K. (2016). Database resources of the National Center for Biotechnology Information. Nucleic Acids Research., 44, D7–D19. https://doi.org/10.1093/nar/gkv1290
   PubMed Web of Science ®Google Scholar
• Bateman, A., Martin, M. J., Orchard, S., Magrane, M., Agivetova, R., … Teodoro, D., The UniProt Consortium. (2021). UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Research, 49(D1), D480–D489. https://doi.org/10.1093/nar/gkaa1100
   PubMed Web of Science ®Google Scholar
• BLAST (Basic Local Alignment Search Tool). (2022). https://blast.ncbi.nlm.nih.gov/Blast.cgi.
   Google Scholar
• Bowie, J. U., Lüthy, R., & Eisenberg, D. (1991). A method to identify protein sequences that fold into a known three-dimensional structure. Science (New York, N.Y.), 253(5016), 164–170. https://doi.org/10.1126/science.1853201
   PubMed Web of Science ®Google Scholar
• Cavasotto, C. N., & Phatak, S. S. (2009). Homology modeling in drug discovery: Current trends and applications. Drug Discovery Today, 14(13–14), 676–683. https://doi.org/10.1016/j.drudis.2009.04.006
   PubMed Web of Science ®Google Scholar
• Chávez Thielemann, H., Cardellini, A., Fasano, M., Bergamasco, L., Alberghini, M., Ciorra, G., Chiavazzo, E., & Asinari, P. (2019). From GROMACS to LAMMPS: GRO2LAM: A converter for molecular dynamics software. Journal of Molecular Modeling, 25(6), 1-12. https://doi.org/10.1007/s00894-019-4011-x
   PubMed Web of Science ®Google Scholar
• Chowdhury, B., & Garai, G. (2017). A review on multiple sequence alignment from the perspective of genetic algorithm. Genomics, 109(5–6), 419–431. https://doi.org/10.1016/j.ygeno.2017.06.007
   PubMed Web of Science ®Google Scholar
• Clustal Omega. (2022). https://www.ebi.ac.uk/Tools/msa/clustalo/.
   Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science: A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Douguet, D. (2018). Data sets representative of the structures and experimental properties of FDA-approved drugs. ACS Medicinal Chemistry Letters, 9(3), 204–209. https://doi.org/10.1021/acsmedchemlett.7b00462
   PubMed Web of Science ®Google Scholar
• Dugs for Neglected Diseases initiative - DNDi. (2017). https://dndi.org/press-releases/2017/fda-approves-benznidazole-chagas-children/.
   Google Scholar
• El-Sayed, N. M., Myler, P. J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., Caler, E., … Hall, N. (2005). Comparative genomics of trypanosomatid parasitic protozoa. Science (New York, N.Y.), 309(5733), 404–409. https://doi.org/10.1126/science.1112181
   PubMed Web of Science ®Google Scholar
• França, T. C. C. (2015). Homology modeling: An important tool for the drug discovery. Journal of Biomolecular Structure & Dynamics, 33(8), 1780–1793. https://doi.org/10.1080/07391102.2014.971429
   PubMed Web of Science ®Google Scholar
• Greene, N., Judson, P., Langowski, J., & Marchant, C. (1999). Knowledge-based expert systems for toxicity and metabolism prediction: DEREK, StAR and METEOR, SAR QSAR. SAR and QSAR in Environmental Research, 10(2–3), 299–314. https://doi.org/10.1080/10629369908039182
   PubMed Web of Science ®Google Scholar
• Hawkins, P. C. D., Skillman, A. G., Warren, G. L., Ellingson, B. A., & Stahl, M. T. (2010). Conformer generation with OMEGA: Algorithm and validation using high quality structures from the protein databank and Cambridge structural database. Journal of Chemical Information and Modeling, 50(4), 572–584. https://doi.org/10.1021/ci100031x
   PubMed Web of Science ®Google Scholar
• Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., De Groot, B. L., Grubmüller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73. https://doi.org/10.1038/nmeth.4067
   PubMed Web of Science ®Google Scholar
• Ibrahim Uba, A., & Yelekçi, K. (2019). Homology modeling of human histone deacetylase 10 and design of potential selective inhibitors. Journal of Biomolecular Structure & Dynamics, 37(14), 3627–3636. https://doi.org/10.1080/07391102.2018.1521747
   PubMed Web of Science ®Google Scholar
• Jackson, Y., Alirol, E., Getaz, L., Wolff, H., Combescure, C., & Chappuis, F. (2010). Tolerance and safety of nifurtimox in patients with chronic Chagas disease. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 51(10), e69–e75. https://doi.org/10.1086/656917
   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
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Keating, G. M. (2017). Sorafenib: A review in hepatocellular carcinoma. Targeted Oncology, 12(2), 243–253. https://doi.org/10.1007/s11523-017-0484-7
   PubMed Web of Science ®Google Scholar
• Khare, S., Nagle, A. S., Biggart, A., Lai, Y. H., Liang, F., Davis, L. C., Barnes, S. W., … Supek, F. (2016). Proteasome inhibition for treatment of leishmaniasis, Chagas disease and sleeping sickness. Nature, 537(7619), 229–233. https://doi.org/10.1038/nature19339
   PubMed Web of Science ®Google Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Kourbeli, V., Chontzopoulou, E., Moschovou, K., Pavlos, D., Mavromoustakos, T., & Papanastasiou, I. P. (2021). An overview on target-based drug design against kinetoplastid protozoan infections: Human African trypanosomiasis, Chagas disease and leishmaniases. Molecules, 26(15), 4629. https://doi.org/10.3390/molecules26154629
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A, Open Source Drug Discovery Consortium. (2014). G-MMPBSA -A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Lemkul, J. (2019). From proteins to perturbed Hamiltonians: A suite of tutorials for the GROMACS-2018 molecular simulation package [Article v1.0]. Living Journal of Computational Molecular Science, 1(1), 1–53. https://doi.org/10.33011/livecoms.1.1.5068
   Google Scholar
• Liu, X., Fan, K., & Wang, W. (2004). The number of protein folds and their distribution over families in nature. Proteins Struct Proteins, 54(3), 491–499. https://doi.org/10.1002/prot.10514
   PubMed Web of Science ®Google Scholar
• Liu, T., Lin, Y., Wen, X., Jorissen, R. N., & Gilson, M. K. (2007). BindingDB: A web-accessible database of experimentally determined protein-ligand binding affinities. Nucleic Acids Research., 35(Database), D198–D201. https://doi.org/10.1093/nar/gkl999
   PubMed Web of Science ®Google Scholar
• Lüthy, R., Bowie, J. U., & Eisenberg, D. (1992). With three-dimensional profiles. Nature, 356(6364), 83–85. https://doi.org/10.1038/356083a0
   PubMed Web of Science ®Google Scholar
• Madeira, F., Pearce, M., Tivey, A. R. N., Basutkar, P., Lee, J., Edbali, O., Madhusoodanan, N., Kolesnikov, A., & Lopez, R. (2022). Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Research, 50(W1), W276–W279. https://doi.org/10.1093/nar/gkac240
   PubMed Web of Science ®Google Scholar
• Madhavi Sastry, G., 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(3), 221–234. https://doi.org/10.1007/s10822-013-9644-8
   PubMed Web of Science ®Google Scholar
• Mysinger, M. M., Carchia, M., Irwin, J. J., & Shoichet, B. K. (2012). Directory of useful decoys, enhanced (DUD-E): Better ligands and decoys for better benchmarking. Journal of Medicinal Chemistry, 55(14), 6582–6594. https://doi.org/10.1021/jm300687e
   PubMed Web of Science ®Google Scholar
• Nagle, A., Biggart, A., Be, C., Srinivas, H., Hein, A., Caridha, D., Sciotti, R. J., … Molteni, V. (2020). Discovery and characterization of clinical candidate LXE408 as a kinetoplastid-selective proteasome inhibitor for the treatment of leishmaniases. Journal of Medicinal Chemistry, 63(19), 10773–10781. https://doi.org/10.1021/acs.jmedchem.0c00499
   PubMed Web of Science ®Google Scholar
• O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). De novodesign of molecular wires with optimal properties for solar energy conversion. Journal of Cheminformatics, 3(S1), 14. https://jcheminf.biomedcentral.com/track/pdf/10.1186/1758-2946-3-33.
   PubMedGoogle Scholar
• OpenEye Scientific Software. (2020). www.eyesopen.com.
   Google Scholar
• OpenEye Scientific Software. OMEGA 4.0.0.4. (2020). www.eyesopen.com.
   Google Scholar
• Patterson, S., & Wyllie, S. (2014). Nitro drugs for the treatment of trypanosomatid diseases: Past, present, and future prospects. Trends in Parasitology, 30(6), 289–298. https://doi.org/10.1016/j.pt.2014.04.003
   PubMed Web of Science ®Google Scholar
• Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. https://doi.org/10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Sliwoski, G., Kothiwale, S., Meiler, J., & Lowe, E. W. (2014). Computational methods in drug discovery. Pharmacological Reviews, 66(1), 334–395. https://doi.org/10.1124/pr.112.007336
   PubMed Web of Science ®Google Scholar
• Sterling, T., & Irwin, J. J. (2015). ZINC 15 – Ligand discovery for everyone. Journal of Chemical Information and Modeling, 55(11), 2324–2337. https://doi.org/10.1021/acs.jcim.5b00559
   PubMed Web of Science ®Google Scholar
• Tanaka, K. (2009). The proteasome: Overview of structure and functions. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences, 85(1), 12–36. https://doi.org/10.2183/pjab.85.12
   PubMed Web of Science ®Google Scholar
• Uba, A. I., & Yelekçi, K. (2020). Crystallographic structure versus homology model: A case study of molecular dynamics simulation of human and zebrafish histone deacetylase 10. Journal of Biomolecular Structure & Dynamics, 38(15), 4397–4406. https://doi.org/10.1080/07391102.2019.1691658
   PubMed Web of Science ®Google Scholar
• UCLA-DOE Institute. (2019). http://servicesn.mbi.ucla.edu/SAVES.
   Google Scholar
• UCLA-DOE LAB — SAVES v6.0. (2022). https://www.doe-mbi.ucla.edu/saves/.
   Google Scholar
• Vanommeslaeghe, K., & MacKerell, A. D. (2012). Automation of the CHARMM general force field (CGenFF) I: Bond perception and atom typing. Journal of Chemical Information and Modeling, 52(12), 3144–3154. https://doi.org/10.1021/ci300363c
   PubMed Web of Science ®Google Scholar
• Verdonk, M. L., Cole, J. C., Hartshorn, M. J., Murray, C. W., & Taylor, R. D. (2003). Improved protein-ligand docking using GOLD. Proteins Struct Proteins, 52(4), 609–623. https://doi.org/10.1002/prot.10465
   PubMed Web of Science ®Google Scholar
• Vriend, G. (1990). WHAT IF: a molecular modeling and drug design program. Journal of Molecular Graphics, 8(1), 52–56, 29. https://doi.org/10.1016/0263-7855(90)80070-v 2268628
   PubMedGoogle Scholar
• Vriend, G., & Sander, C. (1993). Quality control of protein models: Directional atomic contact analysis the method fragment types. Journal of Applied Crystallography, 26(1), 47–60. https://doi.org/10.1107/S0021889892008240
   Web of Science ®Google Scholar
• Vyas, V. K., Ukawala, R. D., Ghate, M., & Chintha, C. (2012). Homology modeling a fast tool for drug discovery: Current perspectives. Indian Journal of Pharmaceutical Sciences, 74(1), 1–17. https://doi.org/10.4103/0250-474X.102537
   PubMed Web of Science ®Google Scholar
• Wishart, D. S., Knox, C., Guo, A. C., Shrivastava, S., Hassanali, M., Stothard, P., Chang, Z., & Woolsey, J. (2006). DrugBank: A comprehensive resource for in silico drug discovery and exploration. Nucleic Acids Research., 34(90001), D668–D672. https://doi.org/10.1093/nar/gkj067
   PubMedGoogle Scholar
• World Health Organization. (2022). https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis).
   Google Scholar
• Wyllie, S., Brand, S., Thomas, M., De Rycker, M., Wa Chung, C., Pena, I., … Wyatt, P. G. (2019). Preclinical candidate for the treatment of visceral leishmaniasis that acts through proteasome inhibition. Proceedings of the National Academy of Sciences of the United States of America, 116(19), 9318–9323. https://doi.org/10.1073/pnas.1820175116
   PubMed Web of Science ®Google Scholar
• Xiang, Z. (2006). Advances in homology protein structure modeling. Current Protein & Peptide Science, 7(3), 217–227. https://doi.org/10.2174/138920306777452312
   PubMed Web of Science ®Google Scholar