145
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Discovery of novel natural products as rhodesain inhibitors for human African trypanosomiasis using in silico techniques

, , , , , & ORCID Icon show all
Pages 5672-5684 | Received 25 Jan 2022, Accepted 17 Jun 2022, Published online: 24 Jun 2022

References

  • Alsford, S., Currier, R. B., Guerra-Assunção, J. A., Clark, T. G., & Horn, D. (2014). Cathepsin-L can resist lysis by human serum in Trypanosoma brucei brucei. PLoS Pathogens, 10(5), e1004130. https://doi.org/10.1371/journal.ppat.1004130
  • Alzain, A. A., & Elbadwi, F. A. (2021). Identification of novel TMPRSS2 inhibitors for COVID-19 using e-pharmacophore modelling, molecular docking, molecular dynamics and quantum mechanics studies. Informatics in Medicine Unlocked, 26, 100758. https://doi.org/10.1016/j.imu.2021.100758
  • Amnerkar, N. D., & Bhusari, K. P. (2010). Synthesis, anticonvulsant activity and 3D-QSAR study of some prop-2-eneamido and 1-acetyl-pyrazolin derivatives of aminobenzothiazole. European Journal of Medicinal Chemistry, 45(1), 149–159. https://doi.org/10.1016/j.ejmech.2009.09.037
  • Baker, C. H., & Welburn, S. C. (2018). The long wait for a new drug for human African Trypanosomiasis. Trends in Parasitology, 34(10), 818–827. https://doi.org/10.1016/j.pt.2018.08.006
  • Banerjee, H., & Rachubinski, R. A. (2017). Involvement of SNARE protein Ykt6 in glycosome biogenesis in Trypanosoma brucei. Molecular and Biochemical Parasitology, 218, 28–37. https://doi.org/10.1016/j.molbiopara.2017.10.003
  • Banik, A., Ghosh, K., Patil, U. K., & Gayen, S. (2021). Identification of molecular fingerprints of natural products for the inhibition of breast cancer resistance protein (BCRP). Phytomedicine: international Journal of Phytotherapy and Phytopharmacology, 85, 153523. https://doi.org/10.1016/j.phymed.2021.153523
  • Beteck, R. M., Legoabe, L. J., Isaacs, M., Khanye, S. D., Laming, D., & Hoppe, H. C. (2019). Anti-trypanosomal and antimalarial properties of tetralone derivatives and structurally related benzocycloalkanones. Med, 55(5), 206–211. https://doi.org/10.3390/medicina55050206
  • Bhadoriya, K. S., Kumawat, N. K., Bhavthankar, S. V., Avchar, M. H., Dhumal, D. M., Patil, S. D., & Jain, S. V. (2016). Exploring 2D and 3D QSARs of benzimidazole derivatives as transient receptor potential melastatin 8 (TRPM8) antagonists using MLR and kNN-MFA methodology. J. Saudi Chem. Soc, 20, S256–S270. https://doi.org/10.1016/j.jscs.2012.11.001
  • Bhadoriya, K. S., Sharma, M. C., Sharma, S., Jain, S. V., & Avchar, M. H. (2014). An approach to design potent anti-Alzheimer’s agents by 3D-QSAR studies on fused 5,6-bicyclic heterocycles as γ-secretase modulators using kNN-MFA methodology. Arab. J. Chem, 7(6), 924–935. https://doi.org/10.1016/j.arabjc.2013.02.002
  • Bindseil, K. U., Jakupovic, J., Wolf, D., Lavayre, J., Leboul, J., & Van Der Pyl, D. (2001). Pure compound libraries; a new perspective for natural product based drug discovery. Drug Discovery Today, 6(16), 840–847. https://doi.org/10.1016/S1359-6446(01)01856-6
  • Blum, A., Mudji, J., Grize, L., Burri, C., Zellweger, M. J., & Blum, J. (2020). Sleeping hearts: 12 years after a follow up study on cardiac findings due to sleeping sickness. One Health (Amsterdam, Netherlands), 11, 100182. https://doi.org/10.1016/j.onehlt.2020.100182
  • Brun, R., Blum, J., Chappuis, F., & Burri, C. (2010). Human African trypanosomiasis. Lancet (London, England), 375(9709), 148–159. https://doi.org/10.1016/S0140-6736(09)60829-1
  • Büscher, P., Cecchi, G., Jamonneau, V., & Priotto, G. (2017). Human African trypanosomiasis. Lancet (London, England), 390(10110), 2397–2409. https://doi.org/10.1016/S0140-6736(17)31510-6
  • Chtita, S., Ghamali, M., Ousaa, A., Aouidate, A., Belhassan, A., Taourati, A. I., Masand, V. H., Bouachrine, M., & Lakhlifi, T. (2019). QSAR study of anti-Human African Trypanosomiasis activity for 2-phenylimidazopyridines derivatives using DFT and Lipinski’s descriptors. Heliyon, 5(3), e01304. https://doi.org/10.1016/j.heliyon.2019.e01304
  • Correia, M. M. G., Barboza, J. V. M., & Espíndola, A. L. (2021). Sleeping sickness: An agent-based model approach. Physica A: Statistical Mechanics and its Applications, 582, 126282. https://doi.org/10.1016/j.physa.2021.126282
  • Elbadwi, F. A., Khairy, E. A., Alsamani, F. O., Mahadi, M. A., Abdalrahman, S. E., Ahmed, Z. A. M., Elsayed, I., Ibraheem, W., & Alzain, A. A. (2021). Identification of novel transmembrane Protease Serine Type 2 drug candidates for COVID-19 using computational studies. Informatics in Medicine Unlocked, 26, 100725. https://doi.org/10.1016/j.imu.2021.100725
  • Enanga, B., Burchmore, R. J. S., Stewart, M. L., & Barrett, M. P. (2002). Sleeping sickness and the brain. Cellular and Molecular Life Sciences: CMLS, 59(5), 845–858. https://doi.org/10.1007/s00018-002-8472-0
  • Franco, J., Scarone, L., & Comini, M. A. (2020). Novel distamycin analogues that block the cell cycle of African trypanosomes with high selectivity and potency. Eur. J. Med. Chem, 189, 112043. https://doi.org/10.1016/j.ejmech.2020.112043
  • Frier, B. M. (2014). Hypoglycaemia in diabetes mellitus: Epidemiology and clinical implications. Nature Reviews. Endocrinology, 10(12), 711–722. https://doi.org/10.1038/nrendo.2014.170
  • Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., & Mainz, D. T. (2006). Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. Journal of Medicinal Chemistry, 49(21), 6177–6196. https://doi.org/10.1021/jm051256o
  • Galiano, V., Garcia-Valtanen, P., Micol, V., & Encinar, J. A. (2016). Looking for inhibitors of the dengue virus NS5 RNA-dependent RNA-polymerase using a molecular docking approach. Drug Design, Development and Therapy, ume 10, 3163–3181. https://doi.org/10.2147/DDDT.S117369
  • Gao, J. M., Qian, Z. Y., Hide, G., Lai, D. H., Lun, Z. R., & Wu, Z. D. (2020). Human African trypanosomiasis: The current situation in endemic regions and the risks for non-endemic regions from imported cases. Parasitology, 147(9), 922–931. https://doi.org/10.1017/S0031182020000645
  • Giroud, M., Dietzel, U., Anselm, L., Banner, D., Kuglstatter, A., Benz, J., Blanc, J., Gaufreteau, D., Liu, H., Lin, X., Stich, A., Kuhn, B., Schuler, F., Kaiser, M., Brun, R., Schirmeister, T., & Kisker, C. (2018). Repurposing a library of human Cathepsin L Ligands: Identification of macrocyclic lactams as potent rhodesain and trypanosoma brucei inhibitors, https://doi.org/10.1021/acs.jmedchem.7b01869
  • Greenwood, J. R., Calkins, D., Sullivan, A. P., & Shelley, J. C. (2010). Towards the comprehensive, rapid, and accurate prediction of the favorable tautomeric states of drug-like molecules in aqueous solution. Journal of Computer-Aided Molecular Design, 24(6-7), 591–604. https://doi.org/10.1007/s10822-010-9349-1
  • Hassan, M. D., Castanha, R. C. G., & Wolfram, D. (2020). Scientometric analysis of global trypanosomiasis research: 1988–2017. Journal of Infection and Public Health, 13(4), 514–520. https://doi.org/10.1016/j.jiph.2019.10.006
  • Helikumi, M., Lolika, P. O., & Mushayabasa, S. (2021). Implications of seasonal variations, host and vector migration on spatial spread of sleeping sickness: Insights from a mathematical model. Informatics Med. Unlocked, 24, 100570. https://doi.org/10.1016/j.imu.2021.100570
  • Jacobson, M. P., Friesner, R. A., Xiang, Z., & Honig, B. (2002). On the role of the crystal environment in determining protein side-chain conformations. Journal of Molecular Biology, 320(3), 597–608. https://doi.org/10.1016/S0022-2836(02)00470-9
  • Janežič, M., Valjavec, K., Loboda, K. B., Herlah, B., Ogris, I., Kozorog, M., Podobnik, M., Grdadolnik, S. G., Wolber, G., & Perdih, A. (2021). Dynophore-based approach in virtual screening: A case of human DNA topoisomerase IIα. International Journal of Molecular Sciences, 22(24), 13474. https://doi.org/10.3390/ijms222413474
  • Johé, P., Jaenicke, E., Neuweiler, H., Schirmeister, T., Kersten, C., & Hellmich, U. A. (2021). Structure, interdomain dynamics, and pH-dependent autoactivation of pro-rhodesain, the main lysosomal cysteine protease from African trypanosomes. The Journal of Biological Chemistry, 296, 100565. https://doi.org/10.1016/j.jbc.2021.100565
  • Kato, C. D., Nanteza, A., Mugasa, C., Edyelu, A., Matovu, E., & Alibu, V. P. (2015). Clinical profiles, disease outcome and co- Morbidities among T.b. rhodesiense sleeping sickness patients in uganda. PLoS One, 10(2), e0118370–13. https://doi.org/10.1371/journal.pone.0118370
  • KB, S., Kumari, A., Shetty, D., Fernandes, E., DV, C., Jays, J., & Murahari, M. (2020). Structure based pharmacophore modelling approach for the design of azaindole derivatives as DprE1 inhibitors for tuberculosis. Journal of Molecular Graphics & Modelling, 101, 107718. https://doi.org/10.1016/j.jmgm.2020.107718
  • Kennedy, P. G. E. (2008). The continuing problem of human African trypanosomiasis (sleeping sickness). Annals of Neurology, 64(2), 116–126. https://doi.org/10.1002/ana.21429
  • Kennedy, P. G. E. (2013). Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). The Lancet. Neurology, 12(2), 186–194. https://doi.org/10.1016/S1474-4422(12)70296-X
  • Kennedy, P. G. E., & Rodgers, J. (2019). Clinical and neuropathogenetic aspects of human African trypanosomiasis. Frontiers in Immunology, 10, 39–11. https://doi.org/10.3389/fimmu.2019.00039
  • Kerr, I. D., Lee, J. H., Farady, C. J., Marion, R., Rickert, M., Sajid, M., Pandey, K. C., Caffrey, C. R., Legac, J., Hansell, E., Mckerrow, J. H., Craik, C. S., Rosenthal, P. J., & Brinen, L. S. (2009). Vinyl sulfones as antiparasitic agents and a structural basis for drug design. The Journal of Biological Chemistry, 284(38), 25697–25703. https://doi.org/10.1074/jbc.M109.014340
  • Kerr, I. D., Wu, P., Marion-tsukamaki, R., Mackey, Z. B., & Brinen, L. S. (2010). Crystal Structures of TbCatB and Rhodesain. Potential Chemotherapeutic Targets and Major Cysteine Proteases of Trypanosoma brucei, 4, 1–10. https://doi.org/10.1371/journal.pntd.0000701
  • Lascano, S., Lopez, M., & Arimondo, P. B. (2018). Natural products and chemical biology tools: Alternatives to target epigenetic mechanisms in cancers. Chemical Record (New York, N.Y.), 18(12), 1854–1876. https://doi.org/10.1002/tcr.201800133
  • MacroModel. (2020). Schrödinger, LLC.
  • Matetovici, I., De Vooght, L., & Van Den Abbeele, J. (2019). Innate immunity in the tsetse fly (Glossina), vector of African trypanosomes. Developmental and Comparative Immunology, 98, 181–188. https://doi.org/10.1016/j.dci.2019.05.003
  • Meisner, J., Barnabas, R. V., & Rabinowitz, P. M. (2019). A mathematical model for evaluating the role of trypanocide treatment of cattle in the epidemiology and control of Trypanosoma brucei rhodesiense and T. b. gambiense sleeping sickness in Uganda, Parasite Epidemiol. Parasite Epidemiology and Control, 5, e00106. https://doi.org/10.1016/j.parepi.2019.e00106
  • Mesu, V., Kalonji, W. M., Bardonneau, C., Mordt, O. V., Blesson, S., Simon, F., Delhomme, S., Bernhard, S., Kuziena, W., Lubaki, J. P. F., Vuvu, S. L., Ngima, P. N., Mbembo, H. M., Ilunga, M., Bonama, A. K., Heradi, J. A., Solomo, J. L. L., Mandula, G., Badibabi, L. K., … Tarral, A. (2018). Oral fexinidazole for late-stage African Trypanosoma brucei gambiense trypanosomiasis: A pivotal multicentre, randomised, non-inferiority trial. Lancet (London, England), 391(10116), 144–154. https://doi.org/10.1016/S0140-6736(17)32758-7
  • Nasution, M. A. F., Toepak, E. P., Alkaff, A. H., & Tambunan, U. S. F. (2018). Flexible docking-based molecular dynamics simulation of natural product compounds and Ebola virus Nucleocapsid (EBOV NP): A computational approach to discover new drug for combating Ebola. BMC Bioinformatics, 19(S14) . https://doi.org/10.1186/s12859-018-2387-8
  • Obi, C. F., Nzeakor, T. A., Okpala, M. I., Ezeh, I. O., Nwobi, L. G., Omeje, M. O., & Ezeokonkwo, R. C. (2019). Evaluation of antitrypanosomal activity of Pterocarpus santalinoides L’H’erit ex DC hydroethanol leaf extract in rats experimentally infected with Trypanosoma brucei. J. Ethnopharmacol, 243, 112085. https://doi.org/10.1016/j.jep.2019.112085
  • Palmer, J. T., Rasnick, D., Klaus, J. L., & Brömme, D. (1995). Vinyl Sulfones as Mechanism-Based Cysteine Protease Inhibitors. Journal of Medicinal Chemistry, 38(17), 3193–3196. https://doi.org/10.1021/jm00017a002
  • Pamer, E. G., Davis, C. E., & So, M. (1991). Expression and deletion analysis of the Trypanosoma brucei rhodesiense cysteine protease in Escherichia coli. Infection and Immunity, 59(3), 1074–1078. https://doi.org/10.1128/iai.59.3.1074-1078.1991
  • Pays, E., & Nolan, D. P. (2021). Genetic and immunological basis of human African trypanosomiasis. Current Opinion in Immunology, 72, 13–20. https://doi.org/10.1016/j.coi.2021.02.007
  • Perdih, A., Hrast, M., Pureber, K., Barreteau, H., Grdadolnik, S. G., Kocjan, D., Gobec, S., Solmajer, T., & Wolber, G. (2015). Furan-based benzene mono- and dicarboxylic acid derivatives as multiple inhibitors of the bacterial Mur ligases (MurC-MurF): Experimental and computational characterization. Journal of Computer-Aided Molecular Design, 29(6), 541–560. https://doi.org/10.1007/s10822-015-9843-6
  • Pereira, G. A. N., da Silva, E. B., Braga, S. F. P., Leite, P. G., Martins, L. C., Vieira, R. P., Soh, W. T., Villela, F. S., Costa, F. M. R., Ray, D., de Andrade, S. F., Brandstetter, H., Oliveira, R. B., Caffrey, C. R., Machado, F. S., & Ferreira, R. S. (2019). Discovery and characterization of trypanocidal cysteine protease inhibitors from the ‘malaria box. European Journal of Medicinal Chemistry, 179, 765–778. https://doi.org/10.1016/j.ejmech.2019.06.062
  • Pogorelčnik, B., Brvar, M., Žegura, B., Filipič, M., Solmajer, T., & Perdih, A. (2015). Discovery of mono- and disubstituted 1H-pyrazolo[3,4]pyrimidines and 9H-purines as catalytic inhibitors of human DNA topoisomerase IIα. ChemMedChem, 10(2), 345–359. https://doi.org/10.1002/cmdc.201402459
  • QikProp. (2020). Schrödinger, LLC.
  • Ramachandran, R., & Piramanyagam, S. (2017). Pharmacophore modeling, atom based 3D-QSAR and molecular docking approaches to screen C-X-C chemokine receptor type 4 antagonists as microbicides for human immunodeficiency virus-1. VirusDisease, 28(3), 272–280. https://doi.org/10.1007/s13337-017-0397-1
  • Riyaphan, J., Jhong, C. H., Lin, S. R., Chang, C. H., Tsai, M. J., Lee, D. N., Sung, P. J., Leong, M. K., & Weng, C. F. (2018). Hypoglycemic efficacy of docking selected natural compounds against α-glucosidase and α-amylase. Molecules, 23(9), 2260. https://doi.org/10.3390/molecules23092260
  • Rodgers, J., Steiner, I., & Kennedy, P. G. E. (2019). Generation of neuroinflammation in human African trypanosomiasis. Neurol. Neuroimmunol. Neuroinflammation, 6 https://doi.org/10.1212/NXI.0000000000000610.
  • Ruiz-Torres, V., Losada-Echeberría, M., Herranz-López, M., Barrajón-Catalán, E., Galiano, V., Micol, V., & Encinar, J. A. (2018). New mammalian target of rapamycin (mTOR) modulators derived from natural product databases and marine extracts by using molecular docking techniques. Mar. Drugs, 16(10), 385–324. https://doi.org/10.3390/md16100385
  • Salam, N. K., Nuti, R., & Sherman, W. (2009). Novel method for generating structure-based pharmacophores using energetic analysis. Journal of Chemical Information and Modeling, 49(10), 2356–2368. https://doi.org/10.1021/ci900212v
  • Schirmeister, T., Kesselring, J., Jung, S., Schneider, T. H., Weickert, A., Becker, J., Lee, W., Bamberger, D., Wich, P. R., Distler, U., Tenzer, S., Johé, P., Hellmich, U. A., & Engels, B. (2016). Quantum chemical-based protocol for the rational design of covalent inhibitors. Journal of the American Chemical Society, 138(27), 8332–8335. https://doi.org/10.1021/jacs.6b03052
  • Schirmeister, T., Schmitz, J., Jung, S., Schmenger, T., Krauth-Siegel, R. L., & Gütschow, M. (2017). Evaluation of dipeptide nitriles as inhibitors of rhodesain, a major cysteine protease of Trypanosoma brucei. Bioorganic & Medicinal Chemistry Letters, 27(1), 45–50. https://doi.org/10.1016/j.bmcl.2016.11.036
  • Scotti, L., Bezerra Mendonca, F. J., Ribeiro, F. F., Tavares, J. F., da Silva, M. S., Barbosa Filho, J. M., & Scotti, M. T. (2017). Natural product inhibitors of topoisomerases: Review and docking study, curr. Current Protein & Peptide Science, 19, 275–291. https://doi.org/10.2174/1389203718666170111114442
  • Seidel, T., Ibis, G., Bendix, F., & Wolber, G. (2010). Strategies for 3D pharmacophore-based virtual screening. Drug Discovery Today: Technologies, 7. https://doi.org/10.1016/j.ddtec.2010.11.004.
  • Simarro, P. P., Cecchi, G., Franco, J. R., Paone, M., Diarra, A., Ruiz-Postigo, J. A., Fèvre, E. M., Mattioli, R. C., & Jannin, J. G. (2012). Estimating and Mapping the Population at Risk of Sleeping Sickness. PLoS Negl. Trop. Dis, 6. https://doi.org/10.1371/journal.pntd.0001859.
  • Singh, J., Meshram, V., & Gupta, M. (2020). Bioactive natural products in drug discovery, Bioact. Nat. Prod. Drug Discov, 1–733. https://doi.org/10.1007/978-981-15-1394-7
  • Subramaniyan, V., Mathiyalagan, S., Praveenkumar, A., Srinivasan, P., Palani, M., Ravichandran, V., & Nallasamy, P. (2018). Molecular docking and ADME properties of bioactive molecules against human acid-beta-glucosidase enzyme, cause of Gaucher’s disease. In Silico Pharmacology, 6(1), 3–11. https://doi.org/10.1007/s40203-018-0039-3.
  • TA, H. (2009). Identifying and characterizing binding sites and assessing druggability. J. Chem. Inf. Model, 49, 377–389.
  • Thompson, A. M., Marshall, A. J., Maes, L., Yarlett, N., Bacchi, C. J., Gaukel, E., Wring, S. A., Launay, D., Braillard, S., Chatelain, E., Mowbray, C. E., & Denny, W. A. (2018). Assessment of a pretomanid analogue library for African trypanosomiasis: Hit-to-lead studies on 6-substituted 2-nitro-6,7-dihydro-5H-imidazo. Bioorganic & Medicinal Chemistry Letters, 28(2), 207–213. https://doi.org/10.1016/j.bmcl.2017.10.067
  • Wall, R. J., Rico, E., Lukac, I., Zuccotto, F., Elg, S., Gilbert, I. H., Freund, Y., & Alley, M. R. K. (2018). Clinical and Veterinary Trypanocidal Benzoxaboroles Target CPSF3. https://doi.org/10.1073/pnas.1807915115
  • Xu, Y., Wang, F., Guo, H., Wang, S., Ni, S., Zhou, Y., Wang, Z., Bao, H., & Wang, Y. (2019). Antitussive and anti-inflammatory dual-active agents developed from natural product lead compound 1-methylhydantoin. Molecules, 24(13), 2355–2312. https://doi.org/10.3390/molecules24132355

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.