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Research Articles

In silico validation of novel inhibitors of malarial aspartyl protease, plasmepsin V and antimalarial efficacy prediction

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Pages 8352-8364 | Received 30 Dec 2020, Accepted 26 Mar 2021, Published online: 19 Apr 2021

References

  • Aamir, M., Singh, V. K., Dubey, M. K., Meena, M., Kashyap, S. P., Katari, S. K., Upadhyay, R. S., Umamaheswari, A., & Singh, S. (2018). In silico prediction, characterization, molecular docking, and dynamic studies on fungal SDRs as novel targets for searching potential fungicides against Fusarium wilt in tomato. Frontiers in Pharmacology, 9, 1038. https://doi.org/10.3389/fphar.2018.01038
  • Aggarwal, M., Kaur, R., Saha, A., Mudgal, R., Yadav, R., Dash, P. K., Parida, M., Kumar, P., & Tomar, S. (2017). Evaluation of antiviral activity of piperazine against Chikungunya virus targeting hydrophobic pocket of alphavirus capsid protein. Antiviral Research, 146, 102–111. https://doi.org/10.1016/j.antiviral.2017.08.015
  • Agnello, S., Brand, M., Chellat, M. F., Gazzola, S., & Riedl, R. (2019). A structural view on medicinal chemistry strategies against drug resistance. Angewandte Chemie (International ed. in English), 58(11), 3300–3345. https://doi.org/10.1002/anie.201802416
  • Ahenkorah, S., Coertzen, D., Tong, J. X., Fridianto, K., Wittlin, S., Birkholtz, L.-M., Tan, K. S. W., Lam, Y., Go, M.-L., & Haynes, R. K. (2020). Antimalarial N1, N3-dialkyldioxonaphthoimidazoliums: Synthesis, biological activity, and structure–activity relationships. ACS Medicinal Chemistry Letters, 11(1), 49–55. https://doi.org/10.1021/acsmedchemlett.9b00457
  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
  • Andrey, V. P., Grishina Maria, A., & Vladimir, A. P. (2017). Grid-based continual analysis of molecular interior for drug discovery, QSAR and QSPR. Current Drug Discovery Technologies, 14(3), 181–205. https://doi.org/10.2174/1570163814666170207144018
  • Bartashevich, E. V., Potemkin, V. A., Grishina, M. A., & Belik, A. V. (2002). A method for multiconformational modeling of the three‐dimensional shape of a molecule. Journal of Structural Chemistry, 43(6), 1033–1039. https://doi.org/10.1023/A:1023611131068
  • Bedi, R. K., Patel, C., Mishra, V., Xiao, H., Yada, R. Y., & Bhaumik, P. (2016). Understanding the structural basis of substrate recognition by Plasmodium falciparum plasmepsin V to aid in the design of potent inhibitors. Scientific Reports, 6, 31420. https://doi.org/10.1038/srep31420
  • Boddey, J. A., Carvalho, T. G., Hodder, A. N., Sargeant, T. J., Sleebs, B. E., Marapana, D., Lopaticki, S., Nebl, T., & Cowman, A. F. (2013). Role of plasmepsin V in export of diverse protein families from the Plasmodium falciparum exportome. Traffic (Copenhagen, Denmark), 14(5), 532–550. https://doi.org/10.1111/tra.12053
  • Boddey, J. A., Hodder, A. N., Günther, S., Gilson, P. R., Patsiouras, H., Kapp, E. A., Pearce, J. A., de Koning-Ward, T. F., Simpson, R. J., Crabb, B. S., & Cowman, A. F. (2010). An aspartyl protease directs malaria effector proteins to the host cell. Nature, 463(7281), 627–631. https://doi.org/10.1038/nature08728
  • Boddey, J. A., Moritz, R. L., Simpson, R. J., & Cowman, A. F. (2009). Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic (Copenhagen, Denmark), 10(3), 285–299. https://doi.org/10.1111/j.1600-0854.2008.00864.x
  • Boonyalai, N., Collins, C. R., Hackett, F., Withers-Martinez, C., & Blackman, M. J. (2018). Essentiality of Plasmodium falciparum plasmepsin V. PLoS One, 13(12), e0207621. https://doi.org/10.1371/journal.pone.0207621
  • Chang, H. H., Falick, A. M., Carlton, P., Sedat, J. W., DeRisi, J. L., & Marletta, M. A. (2008). N-terminal processing of proteins exported by malaria parasites. Molecular and Biochemical Parasitology, 160(2), 107–115. https://doi.org/10.1016/j.molbiopara.2008.04.011
  • Cheuka, P. M., Dziwornu, G., Okombo, J., & Chibale, K. (2020). Plasmepsin inhibitors in antimalarial drug discovery: Medicinal chemistry and target validation (2000 to present). Journal of Medicinal Chemistry, 63(9), 4445–4467. https://doi.org/10.1021/acs.jmedchem.9b01622
  • Cibulskis, R. E., Alonso, P., Aponte, J., Aregawi, M., Barrette, A., Bergeron, L., Fergus, C. A., Knox, T., Lynch, M., Patouillard, E., Schwarte, S., Stewart, S., & Williams, R. (2016). Malaria: Global progress 2000 - 2015 and future challenges. Infectious Diseases of Poverty, 5(1), 61. https://doi.org/10.1186/s40249-016-0151-8
  • Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
  • The UniProt Consortium. (2018). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47(D1), D506–D515. https://doi.org/10.1093/nar/gky1049
  • Daina, A., Michielin, O., & Zoete, V. (2019). SwissTargetPrediction: Updated data and new features for efficient prediction of protein targets of small molecules. Nucleic Acids Research, 47(W1), W357–W364. https://doi.org/10.1093/nar/gkz382
  • Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. In Jonathan E. Hempel, Charles H. Williams, & Charles C. Hong (Eds.), Chemical biology: Methods and protocols (pp. 243–250). Springer New York.
  • Eisenberg, D., Roland, L., & Bowie, J. U. (1997). VERIFY3D: Assessment of protein models with three-dimensional profiles. In Method enzymol (pp. 396–404). Academic Press.
  • Elsliger, M. A., & Wilson, I. A. (2012). 1.8 structure validation and analysis. In Edward H. Egelman (Ed.), Comprehensive biophysics (pp. 116–135). Elsevier.
  • Gioia, D., Bertazzo, M., Recanatini, M., Masetti, M., & Cavalli, A. (2017). Dynamic docking: A paradigm shift in computational drug discovery. Molecules, 22(11), 2029. https://doi.org/10.3390/molecules22112029
  • Hamilton, W. L., Amato, R., van der Pluijm, R. W., Jacob, C. G., Quang, H. H., Thuy-Nhien, N. T., Hien, T. T., Hongvanthong, B., Chindavongsa, K., Mayxay, M., Huy, R., Leang, R., Huch, C., Dysoley, L., Amaratunga, C., Suon, S., Fairhurst, R. M., Tripura, R., Peto, T. J., … Miotto, O. (2019). Evolution and expansion of multidrug-resistant malaria in southeast Asia: A genomic epidemiology study. The Lancet Infectious Diseases, 19(9), 943–951. https://doi.org/10.1016/S1473-3099(19)30392-5
  • Hiller, N. L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estraño, C., & Haldar, K. (2004). A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science (New York, N.Y.), 306(5703), 1934–1937. https://doi.org/10.1126/science.1102737
  • Krohn, A., Redshaw, S., Ritchie, J. C., Graves, B. J., & Hatada, M. H. (1991). Novel binding mode of highly potent HIV-proteinase inhibitors incorporating the (R)-hydroxyethylamine isostere. Journal of Medicinal Chemistry, 34(11), 3340–3342. https://doi.org/10.1021/jm00115a028
  • Kumar, S., Upadhyay, C., Bansal, M., Grishina, M., Chhikara, B. S., Potemkin, V., Rathi, B., & Poonam. (2020). Experimental and computational studies of microwave-assisted, facile ring opening of epoxide with less reactive aromatic amines in nitromethane. ACS Omega, 5(30), 18746–18757. https://doi.org/10.1021/acsomega.0c01760
  • Kumar Singh, A., Rajendran, V., Singh, S., Kumar, P., Kumar, Y., Singh, A., & Miller, W. (2018). Antiplasmodial activity of hydroxyethylamine analogs: Synthesis, biological activity and structure activity relationship of plasmepsin inhibitors. Bioorganic & Medicinal Chemistry, 26(13), 3837–3844. https://doi.org/10.1016/j.bmc.2018.06.037
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
  • Liu, J., Gluzman, I. Y., Drew, M. E., & Goldberg, D. E. (2005). The role of Plasmodium falciparum food vacuole plasmepsins. The Journal of Biological Chemistry, 280(2), 1432–1437. https://doi.org/10.1074/jbc.M409740200
  • Liu, P. (2017). Plasmepsin: Function, characterization and targeted antimalarial drug development. In G. Benelli, H. Khater, & M. Govindarajan (Eds.), Natural Remedies in the Fight Against Parasites (183–218). IntechOpen.
  • Liu, Z., & Peng, R. (2010). Inorganic nanomaterials for tumor angiogenesis imaging. European Journal of Nuclear Medicine and Molecular Imaging, 37(Suppl 1), S147–S163. https://doi.org/10.1007/s00259-010-1452-y
  • Marapana, D. S., Dagley, L. F., Sandow, J. J., Nebl, T., Triglia, T., Pasternak, M., Dickerman, B. K., Crabb, B. S., Gilson, P. R., Webb, A. I., Boddey, J. A., & Cowman, A. F. (2018). Plasmepsin V cleaves malaria effector proteins in a distinct endoplasmic reticulum translocation interactome for export to the erythrocyte. Nature Microbiology, 3(9), 1010–1022. https://doi.org/10.1038/s41564-018-0219-2
  • Mark, P., & Nilsson, L. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. https://doi.org/10.1021/jp003020w
  • Marti, M., Good, R. T., Rug, M., Knuepfer, E., & Cowman, A. F. (2004). Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science (New York, N.Y.), 306(5703), 1930–1933. https://doi.org/10.1126/science.1102452
  • Meissner, K. A., Kronenberger, T., Maltarollo, V. G., Trossini, G. H. G., & Wrenger, C. (2019). Targeting the Plasmodium falciparum plasmepsin V by ligand-based virtual screening. Chemical Biology & Drug Design, 93(3), 300–312. https://doi.org/10.1111/cbdd.13416
  • Moult, J., Fidelis, K., Kryshtafovych, A., Schwede, T., & Tramontano, A. (2016). Critical assessment of methods of protein structure prediction: Progress and new directions in round XI. Proteins: Structure, Function, and Bioinformatics, 84(S1), 4–14. https://doi.org/10.1002/prot.25064
  • Msugupakulya, B. J., Kaindoa, E. W., Ngowo, H. S., Kihonda, J. M., Kahamba, N. F., Msaky, D. S., Matoke-Muhia, D., Tungu, P. K., & Okumu, F. O. (2020). Preferred resting surfaces of dominant malaria vectors inside different house types in rural south-eastern Tanzania. Malaria Journal, 19(1), 22. https://doi.org/10.1186/s12936-020-3108-0
  • Parkes, K. E. B., Bushnell, D. J., Crackett, P. H., Dunsdon, S. J., Freeman, A. C., Gunn, M. P., Hopkins, R. A., Lambert, R. W., & Martin, J. A. (1994). Studies toward the large-scale synthesis of the HIV proteinase inhibitor Ro 31-8959. The Journal of Organic Chemistry, 59(13), 3656–3664. https://doi.org/10.1021/jo00092a026
  • Polino, A. J., Nasamu, A. S., Niles, J. C., & Goldberg, D. E. (2020). Assessment of biological role and insight into druggability of the Plasmodium falciparum protease plasmepsin V. ACS Infectious Diseases, 6(4), 738–746. https://doi.org/10.1021/acsinfecdis.9b00460
  • Poonam, Y. G., Gupta, N., Singh, S., Wu, L., Singh Chhikara, B., Rawat, M., & Rathi, B. (2018). Multistage inhibitors of the malaria parasite: Emerging hope for chemoprotection and malaria eradication. Medicinal Research Reviews, 38(5), 1511–1535. https://doi.org/10.1002/med.21486
  • Raj, U., Kumar, H., & Varadwaj, P. K. (2017). Molecular docking and dynamics simulation study of flavonoids as BET bromodomain inhibitors. Journal of Biomolecular Structure & Dynamics, 35(11), 2351–2362. https://doi.org/10.1080/07391102.2016.1217276
  • Rathi, B., Sharma, P. P., & Singh, R. P. (2014). Tetrahedral hydroxyethylamine: A privileged scaffold in development of antimalarial agents. Chemical Biology Letters, 1(1), 3.
  • Rathi, B., Singh, A. K., Kishan, R., Singh, N., Latha, N., Srinivasan, S., Pandey, K. C., Tiwari, H. K., & Singh, B. K. (2013). Functionalized hydroxyethylamine based peptide nanostructures as potential inhibitors of falcipain-3, an essential proteases of Plasmodium falciparum. Bioorganic & Medicinal Chemistry, 21(17), 5503–5509. https://doi.org/10.1016/j.bmc.2013.05.052
  • Rosenblum, L. T., Kosaka, N., Mitsunaga, M., Choyke, P. L., & Kobayashi, H. (2010). In vivo molecular imaging using nanomaterials: General in vivo characteristics of nano-sized reagents and applications for cancer diagnosis. Molecular Membrane Biology, 27(7), 274–285. https://doi.org/10.3109/09687688.2010.481640
  • Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5(4), 725–738. https://doi.org/10.1038/nprot.2010.5
  • Russo, I., Babbitt, S., Muralidharan, V., Butler, T., Oksman, A., & Goldberg, D. E. (2010). Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. Nature, 463(7281), 632–636. https://doi.org/10.1038/nature08726
  • Ryckebusch, A., Rébecca, D.-P., Marie-Ange, D.-F., Richard, V., Elisabeth, M., Philippe, G., & Christian, S. (2003). Synthesis and antimalarial evaluation of new 1,4-bis(3-aminopropyl)piperazine derivatives. Bioorganic & Medicinal Chemistry Letters, 13(21), 3783–3787. https://doi.org/10.1016/j.bmcl.2003.07.008
  • Sachs, J., & Malaney, P. (2002). The economic and social burden of malaria. Nature, 415(6872), 680–685. https://doi.org/10.1038/415680a
  • Sangai, N. P., Patel, C. N., & Pandya, H. A. (2018). Ameliorative effects of quercetin against bisphenol A-caused oxidative stress in human erythrocytes: An in vitro and in silico study. Toxicology Research, 7(6), 1091–1099. https://doi.org/10.1039/c8tx00105g
  • Schrödinger Release 2020-1. (2020). Desmond Molecular Dynamics System, D. E. S. R. Maestro-Desmond Interoperability Tools. Schrödinger.
  • Schrödinger Release 2020-1. (2020). Epik, S., LLC.
  • Schrödinger Release 2020-1. (2020). Glide, S., LLC.
  • Schrödinger Release 2020-1. (2020). LigPrep, S., LLC.
  • Schrödinger Release 2020-1. (2020). Maestro, S., LLC.
  • Schrödinger Release 2020-1. (2020). Prime, S., LLC.
  • Schrödinger Release 2020-1. (2016). Protein preparation Wizard; Epik, S., LLC. Impact, Schrödinger, LLC. (2016). Prime, Schrödinger, LLC. (2020).
  • Schulze, J., Kwiatkowski, M., Borner, J., Schlüter, H., Bruchhaus, I., Burmester, T., Spielmann, T., & Pick, C. (2015). The Plasmodium falciparum exportome contains non-canonical PEXEL/HT proteins. Molecular Microbiology, 97(2), 301–314. https://doi.org/10.1111/mmi.13024
  • Shanmugam, G., Lee, S., & Jeon, J. (2018). Identification of potential nematicidal compounds against the pine wood nematode, Bursaphelenchus xylophilus through an in silico approach. Molecules, 23(7), 1828. https://doi.org/10.3390/molecules23071828
  • Singh, A. K., Rajendran, V., Pant, A., Ghosh, P. C., Singh, N., Latha, N., Garg, S., Pandey, K. C., Singh, B. K., & Rathi, B. (2015). Design, synthesis and biological evaluation of functionalized phthalimides: A new class of antimalarials and inhibitors of falcipain-2, a major hemoglobinase of malaria parasite. Bioorganic & Medicinal Chemistry, 23(8), 1817–1827. https://doi.org/10.1016/j.bmc.2015.02.029
  • Singh, A. K., Rathore, S., Tang, Y., Goldfarb, N. E., Dunn, B. M., Rajendran, V., Ghosh, P. C., Singh, N., Latha, N., Singh, B. K., Rawat, M., & Rathi, B. (2015). Hydroxyethylamine based phthalimides as new class of plasmepsin hits: Design, synthesis and antimalarial evaluation. PLoS One, 10(10), e0139347. https://doi.org/10.1371/journal.pone.0139347
  • Sippl, M. J. (1993). Recognition of errors in three-dimensional structures of proteins. Proteins, 17(4), 355–362. https://doi.org/10.1002/prot.340170404
  • Smith, C. (2003). Drug target validation: Hitting the target. Nature, 422(6929), 341. https://doi.org/10.1038/422341a
  • Souza, M. C., Padua, T. A., Torres, N. D., Costa, M. F. d S., Facchinetti, V., Gomes, C. R. B., Souza, M. V. N., & Henriques, M. d G. (2015). Study of the antimalarial properties of hydroxyethylamine derivatives using green fluorescent protein transformed Plasmodium berghei. Memórias do Instituto Oswaldo Cruz, 110(4), 560–565. https://doi.org/10.1590/0074-02760140466
  • Stefanidou, M., Herrera, C., Armanasco, N., & Shattock, R. J. (2012). Saquinavir inhibits early events associated with establishment of HIV-1 infection: Potential role for protease inhibitors in prevention. Antimicrobial Agents and Chemotherapy, 56(8), 4381–4390. https://doi.org/10.1128/AAC.00399-12
  • The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrödinger, LLC.
  • Vladimir, P., & Grishina, M. (2018). Grid-based technologies for in silico screening and drug design. Current Medicinal Chemistry, 25(29), 3526–3537. https://doi.org/10.2174/0929867325666180309112454
  • WHO. (2020). World Malaria Report 2020.
  • Wiederstein, M., & Sippl, M. J. (2007). ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research, 35, W407–W410. https://doi.org/10.1093/nar/gkm290
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER Suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8. https://doi.org/10.1038/nmeth.3213
  • Zhang, C., Freddolino, P. L., & Zhang, Y. (2017). COFACTOR: Improved protein function prediction by combining structure, sequence and protein-protein interaction information. Nucleic Acids Research, 45(W1), W291–W299. https://doi.org/10.1093/nar/gkx366
  • Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9(1), 40. https://doi.org/10.1186/1471-2105-9-40

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