An in silico quest for next-generation antimalarial drugs by targeting Plasmodium falciparum hexose transporter protein: a multi-pronged approach

References

• Ali, F., Wali, H., Jan, S., Zia, A., Aslam, M., Ahmad, I., Afridi, S. G., Shams, S., & Khan, A. (2021). Analysing the essential proteins set of Plasmodium falciparum PF3D7 for novel drug targets identification against malaria. Malaria Journal, 20(1), 1–11. https://doi.org/10.1186/s12936-021-03865-1
   PubMedGoogle Scholar
• Balikagala, B., Fukuda, N., Ikeda, M., Katuro, O. T., Tachibana, S.-I., Yamauchi, M., Opio, W., Emoto, S., Anywar, D. A., Kimura, E., Palacpac, N. M., Odongo-Aginya, E. I., Ogwang, M., Horii, T., & Mita, T. (2021). Evidence of artemisinin-resistant malaria in Africa. New England Journal of Medicine, 385(13), 1163–1171. https://doi.org/10.1056/NEJMoa2101746
   PubMed Web of Science ®Google Scholar
• Benedict, M. I., White, R. B., Wulff, L. M., & Hall, B. J. (1990). Reported maltreatment in children with multiple disabilities. Child Abuse & Neglect, 14(2), 207–217. https://doi.org/10.1016/0145-2134(90)90031-N
   PubMed Web of Science ®Google Scholar
• Bhatt, S., Weiss, D. J., Cameron, E., Bisanzio, D., Mappin, B., Dalrymple, U., Battle, K., Moyes, C. L., Henry, A., Eckhoff, P. A., Wenger, E. A., Briët, O., Penny, M. A., Smith, T. A., Bennett, A., Yukich, J., Eisele, T. P., Griffin, J. T., Fergus, C. A., … Gething, P. W. (2015). The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature, 526(7572), 207–211.
   PubMed Web of Science ®Google Scholar
• Blume, M., Hliscs, M., Rodriguez-Contreras, D., Sanchez, M., Landfear, S., Lucius, R., Matuschewski, K., & Nishith, G. (2011). A constitutive pan-hexose permease for the Plasmodium life cycle and transgenic models for screening of antimalarial sugar analogs. The FASEB Journal, 25(4), 1218–1229. https://doi.org/10.1096/fj.10-173278
   PubMed Web of Science ®Google Scholar
• Case, D. A., Belfon, K., Ben-Shalom, I., Brozell, S. R., Cerutti, D., Cheatham, T., Cruzeiro, V. W. D., Darden, T., Duke, R. E., & Giambasu, G. (2020). Amber 2020.
   Google Scholar
• Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7(1), 1–13. https://doi.org/10.1038/srep42717
   PubMed Web of Science ®Google Scholar
• Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. In Chemical biology (pp. 243–250). Springer.
   Google Scholar
• Flannery, E. L., Chatterjee, A. K., & Winzeler, E. A. (2013). Antimalarial drug discovery—approaches and progress towards new medicines. Nature Reviews Microbiology, 11(12), 849–862. https://doi.org/10.1038/nrmicro3138
   PubMed Web of Science ®Google Scholar
• Gaulton, A., Hersey, A., Nowotka, M., Bento, A. P., Chambers, J., Mendez, D., Mutowo, P., Atkinson, F., Bellis, L. J., Cibrián-Uhalte, E., Davies, M., Dedman, N., Karlsson, A., Magariños, M. P., Overington, J. P., Papadatos, G., Smit, I., & Leach, A. R. (2017). The ChEMBL database in 2017. Nucleic Acids Research, 45(D1), D945–D954. https://doi.org/10.1093/nar/gkw1074
   PubMed Web of Science ®Google Scholar
• Genheden, S., Kuhn, O., Mikulskis, P., Hoffmann, D., & Ryde, U. (2012). The normal-mode entropy in the MM/GBSA method: Effect of system truncation, buffer region, and dielectric constant. Journal of Chemical Information and Modeling, 52(8), 2079–2088. https://doi.org/10.1021/ci3001919
   PubMed Web of Science ®Google Scholar
• Hawkes, M., Conroy, A. L., & Kain, K. C. (2014). Spread of artemisinin resistance in malaria. The New England Journal of Medicine, 371(20), 1944–1945.
   PubMed Web of Science ®Google Scholar
• Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the Performance of the MM_PBSA and MM_GBSA Methods. 1. The Accuracy.pdf. 69–82.
   Google Scholar
• Huang, J., Yuan, Y., Zhao, N., Pu, D., Tang, Q., Zhang, S., Luo, S., Yang, X., Wang, N., Xiao, Y., Zhang, T., Liu, Z., Sakata-Kato, T., Jiang, X., Kato, N., Yan, N., & Yin, H. (2021). Orthosteric–allosteric dual inhibitors of PfHT1 as selective antimalarial agents. Proceedings of the National Academy of Sciences of United States of America, 118(3), e2017749118. https://doi.org/10.1073/pnas.2017749118
   PubMed Web of Science ®Google Scholar
• Izaguirre, J. A., Catarello, D. P., Wozniak, J. M., & Skeel, R. D. (2001). Langevin stabilization of molecular dynamics. The Journal of Chemical Physics, 114(5), 2090–2098. https://doi.org/10.1063/1.1332996
   Web of Science ®Google Scholar
• Jagannathan, P., & Kakuru, A. (2022). Malaria in 2022: Increasing challenges, cautious optimism. Nature Communications, 13(1), 1–3. https://doi.org/10.1038/s41467-022-30133-w
   PubMed Web of Science ®Google Scholar
• Jiang, X., Yuan, Y., Huang, J., Zhang, S., Luo, S., Wang, N., Pu, D., Zhao, N., Tang, Q., Hirata, K., Yang, X., Jiao, Y., Sakata-Kato, T., Wu, J.-W., Yan, C., Kato, N., Yin, H., & Yan, N. (2020). Structural basis for blocking sugar uptake into the malaria parasite Plasmodium falciparum. Cell, 183(1), 258–268.e12. https://doi.org/10.1016/j.cell.2020.08.015
   PubMed Web of Science ®Google Scholar
• Joët, T., Eckstein-Ludwig, U., Morin, C., & Krishna, S. (2003). Validation of the hexose transporter of Plasmodium falciparum as a novel drug target. Proceedings of the National Academy of Sciences, 100(13), 7476–7479. https://doi.org/10.1073/pnas.1330865100
   PubMed Web of Science ®Google Scholar
• Kaliappan, S., & Bombay, I. I. T. (2018). UCSF Chimera-Overview.
   Google Scholar
• Kirk, K. (2001). Membrane transport in the malaria-infected erythrocyte. Physiological Reviews, 81(2), 495–537. https://doi.org/10.1152/physrev.2001.81.2.495
   PubMed Web of Science ®Google Scholar
• Kräutler, V., van Gunsteren, W. F., & Hünenberger, P. H. (2001). A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. Journal of Computational Chemistry, 22(5), 501–508. https://doi.org/10.1002/1096-987X(20010415)22:5<501::AID-JCC1021>3.0.CO;2-V
   Web of Science ®Google Scholar
• Kumar, S., Bhardwaj, T. R., Prasad, D. N., & Singh, R. K. (2018). Drug targets for resistant malaria: historic to future perspectives. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie, 104, 8–27. https://doi.org/10.1016/j.biopha.2018.05.009
   PubMed Web of Science ®Google Scholar
• Lipinski, C. A. (2004). Lead- and drug-like compounds: The rule-of-five revolution. Drug Discovery Today: Technologies, 1(4), 337–341. https://doi.org/10.1016/j.ddtec.2004.11.007
   PubMedGoogle Scholar
• Lyu, C., Chen, T., Qiang, B., Liu, N., Wang, H., Zhang, L., & Liu, Z. (2021). CMNPD: A comprehensive marine natural products database towards facilitating drug discovery from the ocean. Nucleic Acids Research, 49(D1), D509–D515. https://doi.org/10.1093/nar/gkaa763
   PubMed Web of Science ®Google Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K. E., & Simmerling, C. (2015). ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB. Journal of Chemical Theory and Computation, 11(8), 3696–3713. https://doi.org/10.1021/acs.jctc.5b00255
   PubMed Web of Science ®Google Scholar
• Meier, A., Erler, H., & Beitz, E. (2018). Targeting channels and transporters in protozoan parasite infections. Frontiers in Chemistry, 6, 88. https://doi.org/10.3389/fchem.2018.00088
   PubMed Web of Science ®Google Scholar
• Miller, B. R., McGee, T. D., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Monroe, A., Williams, N. A., Ogoma, S., Karema, C., & Okumu, F. (2022). Reflections on the 2021 World Malaria Report and the future of malaria control. Springer.
   Google Scholar
• Perkins, D. J., Were, T., Davenport, G. C., Kempaiah, P., Hittner, J. B., & Ong’echa, J. M. (2011). Severe malarial anemia: innate immunity and pathogenesis. International Journal of Biological Sciences, 7(9), 1427–1442. https://doi.org/10.7150/ijbs.7.1427
   PubMed Web of Science ®Google Scholar
• Pires, D. E. V., Blundell, T. L., & Ascher, D. B. (2015). pkCSM: Predicting small-molecule pharmacokinetic and toxicity properties using graph-based signatures. Journal of Medicinal Chemistry, 58(9), 4066–4072. https://doi.org/10.1021/acs.jmedchem.5b00104
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham III, T. E. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. https://doi.org/10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Sahayarayan, J. J., Rajan, K. S., Nachiappan, M., Prabhu, D., Rao, R. G. R., Jeyakanthan, J., Mahmoud, A. H., Mohammed, O. B., & Morgan, A. M. A. (2020). Identification of potential drug target in malarial disease using molecular docking analysis. Saudi Journal of Biological Sciences, 27(12), 3327–3333. https://doi.org/10.1016/j.sjbs.2020.10.019
   PubMed Web of Science ®Google Scholar
• Schafmeister, C., Ross, W. S., & Romanovski, V. (1995). The leap module of AMBER. University of California.
   Google Scholar
• Sprenger, K. G., Jaeger, V. W., & Pfaendtner, J. (2015). The general AMBER force field (GAFF) can accurately predict thermodynamic and transport properties of many ionic liquids. The Journal of Physical Chemistry B, 119(18), 5882–5895. https://doi.org/10.1021/acs.jpcb.5b00689
   PubMed Web of Science ®Google Scholar
• Talele, T. T., Khedkar, S. A., & Rigby, A. C. (2010). Successful applications of computer aided drug discovery: Moving drugs from concept to the clinic. Current Topics in Medicinal Chemistry, 10(1), 127–141. https://doi.org/10.2174/156802610790232251
   PubMed Web of Science ®Google Scholar
• The International Transporter Consortium. (2010). Membrane transporters in drug development. Nature Reviews Drug Discovery, 9(3), 215–236.
   PubMed Web of Science ®Google Scholar
• Tizifa, T. A., Kabaghe, A. N., McCann, R. S., van den Berg, H., Van Vugt, M., & Phiri, K. S. (2018). Prevention efforts for malaria. Current Tropical Medicine Reports, 5(1), 41–50. https://doi.org/10.1007/s40475-018-0133-y
   PubMedGoogle Scholar
• Turner, P. J. (2005). XMGRACE, Version 5.1. 19. Center for Coastal and Land-Margin Research, Oregon Graduate Institute of Science and Technology.
   Google Scholar
• Uwimana, A., Umulisa, N., Venkatesan, M., Svigel, S. S., Zhou, Z., Munyaneza, T., Habimana, R. M., Rucogoza, A., Moriarty, L. F., Sandford, R., Piercefield, E., Goldman, I., Ezema, B., Talundzic, E., Pacheco, M. A., Escalante, A. A., Ngamije, D., Mangala, J.-L N., Kabera, M., … Lucchi, N. W. (2021). Association of Plasmodium falciparum kelch13 R561H genotypes with delayed parasite clearance in Rwanda: An open-label, single-arm, multicentre, therapeutic efficacy study. The Lancet Infectious Diseases, 21(8), 1120–1128. https://doi.org/10.1016/S1473-3099(21)00142-0
   PubMed Web of Science ®Google Scholar
• Van De Waterbeemd, H., & Gifford, E. (2003). ADMET in silico modelling: Towards prediction paradise? Nature Reviews Drug Discovery, 2(3), 192–204. https://doi.org/10.1038/nrd1032
   PubMed Web of Science ®Google Scholar
• Wolber, G., & Langer, T. (2005). LigandScout: 3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. Journal of Chemical Information and Modeling, 45(1), 160–169. https://doi.org/10.1021/ci049885e
   PubMed Web of Science ®Google Scholar
• Woodrow, C. J., Burchmore, R. J., & Krishna, S. (2000). Hexose permeation pathways in Plasmodium falciparum-infected erythrocytes. Proceedings of the National Academy of Sciences, 97(18), 9931–9936. https://doi.org/10.1073/pnas.170153097
   PubMed Web of Science ®Google Scholar
• Woodrow, C. J., Penny, J. I., & Krishna, S. (1999). Intraerythrocytic Plasmodium falciparum expresses a high affinity facilitative hexose transporter. The Journal of Biological Chemistry, 274(11), 7272–7277.
   PubMed Web of Science ®Google Scholar
• Woods, C. J., Malaisree, M., Michel, J., Long, B., McIntosh-Smith, S., & Mulholland, A. J. (2014). Rapid decomposition and visualisation of protein-ligand binding free energies by residue and by water. Faraday Discuss, 169, 477–499. https://doi.org/10.1039/C3FD00125C
   PubMed Web of Science ®Google Scholar
• Yu, W., & MacKerell, A. D. (2017). Computer-aided drug design methods. In Antibiotics (pp. 85–106). Springer.
   Google Scholar