Exploration of new drug-like inhibitors for serine/threonine protein phosphatase 5 of Plasmodium falciparum: a docking and simulation study

References

• Aguiar, A. C. C., Rocha, E. M., Souza, N. B., França, T. C., & Krettli, A. U. (2012). New approaches in antimalarial drug discovery and development: a review. Memórias do Instituto Oswaldo Cruz, 107, 831–845.10.1590/S0074-02762012000700001
   PubMed Web of Science ®Google Scholar
• Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.10.1093/nar/25.17.3389
   PubMed Web of Science ®Google Scholar
• Baba, Y., Hirukawa, N., Tanohira, N., & Sodeoka, M. (2003). Structure-based design of a highly selective catalytic site-directed inhibitor of Ser/Thr protein phosphatase 2B (calcineurin). Journal of the American Chemical Society, 125, 9740–9749.10.1021/ja034694y
   PubMed Web of Science ®Google Scholar
• Bajsa, J., Duke, S. O., & Tekwani, B. L. (2008). Plasmodium falciparum serine/threonine phoshoprotein phosphatases (PPP): From housekeeper to the ‘holy grail’. Current Drug Targets, 9, 997–1012.10.2174/138945008786786055
   PubMed Web of Science ®Google Scholar
• Bajsa, J., McCluskey, A., Gordon, C. P., Stewart, S. G., Hill, T. A., Sahu, R., … Tekwani, B. L. (2010). The antiplasmodial activity of norcantharidin analogs NOVA. The University of Newcastle's Digital Repository. Bioorganic & Medicinal Chemistry Letters, 20, 6688–6695.
   PubMed Web of Science ®Google Scholar
• Barford, D., Das, A. K., & Egloff, M. P. (1998). The structure and mechanism of protein phosphatases: Insights into catalysis and regulation. Annual Review of Biophysics and Biomolecular Structure, 27, 133–164.10.1146/annurev.biophys.27.1.133
   PubMedGoogle Scholar
• Berendsen, H. J., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91, 43–56.10.1016/0010-4655(95)00042-E
   Web of Science ®Google Scholar
• Bertini, I., Calderone, V., Fragai, M., Luchinat, C., & Talluri, E. (2009). Structural basis of serine/threonine phosphatase inhibition by the archetypal small molecules cantharidin and norcantharidin. Journal of Medicinal Chemistry, 52, 4838–4843.10.1021/jm900610k
   PubMed Web of Science ®Google Scholar
• Bowie, J. U., Luthy, R., & Eisenberg, D. (1991). A method to identify protein sequences that fold into a known three-dimensional structure. Science, 253, 164–170.10.1126/science.1853201
   PubMed Web of Science ®Google Scholar
• Breman, J. G., Alilio, M. S., & Mills, A. (2004). Conquering the intolerable burden of malaria: What’s new, what’s needed: A summary. The American Journal of Tropical Medicine and Hygiene, 71(Suppl. 2), 1–15.
   PubMed Web of Science ®Google Scholar
• Chen, D., Menche, G., Power, T. D., Sower, L., Peterson, J. W., & Schein, C. H. (2007). Accounting for ligand-bound metal ions in docking small molecules on adenylyl cyclase toxins. Proteins: Structure, Function, and Bioinformatics, 67, 593–605.10.1002/prot.21249
   PubMed Web of Science ®Google Scholar
• Chen, X. E., Liu, J., & Zhang, Y. (2014). Cantharidin impedes the activity of protein serine/threonine phosphatase in Plutella xylostella. Molecular BioSystems, 10, 240–250.10.1039/C3MB70410F
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science, 2, 1511–1519.10.1002/pro.v2:9
   PubMed Web of Science ®Google Scholar
• Cosconati, S., Forli, S., Perryman, A. L., Harris, R., Goodsell, D. S., & Olson, A. J. (2010). Virtual screening with AutoDock: Theory and practice. Expert Opinion on Drug Discovery, 5, 597–607.10.1517/17460441.2010.484460
   PubMed Web of Science ®Google Scholar
• Cowman, A. F., Berry, D., & Baum, J. (2012). The cell biology of disease: The cellular and molecular basis for malaria parasite invasion of the human red blood cell. The Journal of Cell Biology, 198, 961–971.10.1083/jcb.201206112
   PubMed Web of Science ®Google Scholar
• Daneshvar, C., Davis, T. M., Cox-Singh, J., Rafa’ee, M. Z., Zakaria, S. K., Divis, P. C., & Singh, B. (2009). Clinical and laboratory features of human Plasmodium knowlesi infection. Clinical Infectious Diseases, 49, 852–860.10.1086/599189
   PubMed Web of Science ®Google Scholar
• Dobson, S., Kar, B., Kumar, R., Adams, B., & Barik, S. (2001). A novel tetratricopeptide repeat (TPR) containing PP5 serine/threonine protein phosphatase in the malaria parasite, Plasmodium falciparum. BMC Microbiology, 1, 31.10.1186/1471-2180-1-31
   PubMedGoogle Scholar
• Dondorp, A. M., Pongponratn, E., & White, N. J. (2004). Reduced microcirculatory flow in severe falciparum malaria: Pathophysiology and electron-microscopic pathology. Acta Tropica, 89, 309–317.10.1016/j.actatropica.2003.10.004
   PubMed Web of Science ®Google Scholar
• Dorin-Semblat, D., Bottrill, A. R., Solyakov, L., Tobin, A., & Doerig, C. (2013). Experimental tools for the study of protein phosphorylation in Plasmodium. In Robert Ménard (Ed.), Malaria (pp. 241–257). Paris: Humana Press.
   Google Scholar
• Dundas, J., Ouyang, Z., Tseng, J., Binkowski, A., Turpaz, Y., & Liang, J. (2006). CASTp: Computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Research, 34(Web Server), W116–W118. Retrieved from http://sts.bioe.uic.edu/castp/10.1093/nar/gkl282
   PubMed Web of Science ®Google Scholar
• Eswar, N., Webb, B., Marti‐Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., … Sali, A. (2006). Comparative protein structure modeling using Modeller. Current Protocols in Bioinformatics, 5–6. doi:10.1002/0471250953.bi0506s15
   Google Scholar
• Gaedt, K., & Höltje, H. D. (1998). Consistent valence force-field parameterization of bond lengths and angles with quantum chemicalab initio methods applied to some heterocyclic dopamine D3-receptor agonists. Journal of Computational Chemistry, 19, 935–946.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Gahoi, S., Mandal, R. S., Ivanisenko, N., Shrivastava, P., Jain, S., Singh, A. K., … Raghunandanan, M. V. (2013). Computational screening for new inhibitors of M. tuberculosis mycolyltransferases antigen 85 group of proteins as potential drug targets. Journal of Biomolecular Structure and Dynamics, 31, 30–43.10.1080/07391102.2012.691343
   PubMed Web of Science ®Google Scholar
• Gaulton, A., Bellis, L. J., Bento, A. P., Chambers, J., Davies, M., Hersey, A., … Light, Y. (2012). ChEMBL: A large-scale bioactivity database for drug discovery. Nucleic Acids Research, 40, D1100–D1107.10.1093/nar/gkr777
   PubMed Web of Science ®Google Scholar
• Gauss, C. M., Sheppeck, II, J. E., Nairn, A. C., & Chamberlin, R. (1997). A molecular modeling analysis of the binding interactions between the okadaic acid class of natural product inhibitors and the Ser–Thr phosphatases, PP1 and PP2A. Bioorganic & Medicinal Chemistry, 5, 1751–1773.
   PubMed Web of Science ®Google Scholar
• Goodsell, D. S., Morris, G. M., & Olson, A. J. (1996). Automated docking of flexible ligands: Applications of autodock. Journal of Molecular Recognition, 9(1), 1–5.10.1002/(ISSN)1099-1352
   PubMed Web of Science ®Google Scholar
• Grosberg, A. Y., & Khokhlov, A. R. (1994). Statistical physics of macromolecules. (pp. 1–144). New York, NY: American Institute of Physics.
   Google Scholar
• Haslbeck, V., Helmuth, M., Alte, F., Popowicz, G., Schmidt, W., Weiwad, M., … Richter, K. (in press). Selective targeting of the autoinhibition of PP5 reduces tau phosphorylation in mouse. doi:10.2210/pdb4ja7/pdb
   Google Scholar
• Honkanan, R. E., Codispoti, B. A., Tse, K., & Boynton, A. L. (1994). Characterization of natural toxins with inhibitory activity against serine/threonine protein phosphatases. Toxicon, 32, 339–350.10.1016/0041-0101(94)90086-8
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A. (2014). g_mmpbsa – A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54, 1951–1962.10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., … Valentin, F. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.10.1093/bioinformatics/btm404
   PubMed Web of Science ®Google Scholar
• 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, 283–291.10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Laskowski, R. A., Watson, J. D., & Thornton, J. M. (2005). ProFunc: A server for predicting protein function from 3D structure. Nucleic Acids Research, 33(Web Server), W89–W93. Retrieved from https://www.ebi.ac.uk/thornton-srv/databases/profunc/10.1093/nar/gki414
   PubMedGoogle Scholar
• Lindenthal, C., & Klinkert, M. Q. (2002). Identification and biochemical characterisation of a protein phosphatase 5 homologue from Plasmodium falciparum. Molecular and Biochemical Parasitology, 120, 257–268.10.1016/S0166-6851(02)00007-5
   PubMed Web of Science ®Google Scholar
• Lipinski, C. A. (2000). Drug-like properties and the causes of poor solubility and poor permeability. Journal of Pharmacological and Toxicological Methods, 44, 235–249.10.1016/S1056-8719(00)00107-6
   PubMed Web of Science ®Google Scholar
• Luo, R., David, L., & Gilson, M. K. (2002). Accelerated Poisson–Boltzmann calculations for static and dynamic systems. Journal of Computational Chemistry, 23, 1244–1253.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Lüthy, R., Bowie, J. U., & Eisenberg, D. (1992). Assessment of protein models with three-dimensional profiles. Nature, 356, 83–85.10.1038/356083a0
   PubMed Web of Science ®Google Scholar
• McCluskey, A., Sim, A. T., & Sakoff, J. A. (2002). Serine–threonine protein phosphatase inhibitors: Development of potential therapeutic strategies. Journal of Medicinal Chemistry, 45, 1151–1175.10.1021/jm010066k
   PubMed Web of Science ®Google Scholar
• McConnell, J. L., & Wadzinski, B. E. (2009). Targeting protein serine/threonine phosphatases for drug development. Molecular Pharmacology, 75, 1249–1261.10.1124/mol.108.053140
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30, 2785–2791.10.1002/jcc.v30:16
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera – A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605–1612.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Prasad, C. V. S. S., Gupta, S., Gaponenko, A., & Dhar, M. (2012). In-silico comparative study of inhibitory mechanism of plant serine proteinase inhibitors. Bioinformation, 8, 673.10.6026/bioinformation
   PubMedGoogle Scholar
• Prasad, C. V. S., Gupta, S., Gaponenko, A., & Tiwari, M. (2013). Molecular dynamic and docking interaction study of Heterodera glycines serine proteinase with Vigna mungo proteinase inhibitor. Applied Biochemistry and Biotechnology, 170, 1996–2008. doi:10.1007/s12010-013-0342-8
   PubMed Web of Science ®Google Scholar
• Prasad, C. S., Gupta, S., Kumar, H., & Tiwari, M. (2013). Evolutionary and functional analysis of fructose bisphosphate aldolase of plant parasitic nematodes. Bioinformation, 9(1), 1–8. doi:10.6026/97320630009001 10.6026/bioinformation
   PubMedGoogle Scholar
• Price, R. N., Douglas, N. M., & Anstey, N. M. (2009). New developments in Plasmodium vivax malaria: Severe disease and the rise of chloroquine resistance. Current Opinion in Infectious Diseases, 22, 430–435.10.1097/QCO.0b013e32832f14c1
   PubMed Web of Science ®Google Scholar
• Rappe, A. K., Casewit, C. J., Colwell, K. S., Goddard, W. A., & Skiff, W. M. (1992). UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations. Journal of the American Chemical Society, 114, 10024–10035.10.1021/ja00051a040
   Web of Science ®Google Scholar
• Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234, 779–815.
   PubMed Web of Science ®Google Scholar
• Sander, T. (2001). OSIRIS property explorer. Allschwil: Actelion Pharmaceuticals Ltd.
   Google Scholar
• Seiler, K. P., George, G. A., Happ, M. P., Bodycombe, N. E., Carrinski, H. A., Norton, S., … Clemons, P. A. (2008). ChemBank: A small-molecule screening and cheminformatics resource database. Nucleic Acids Research, 36(Suppl. 1), D351–D359.
   PubMed Web of Science ®Google Scholar
• Sinclair, C., Borchers, C., Parker, C., Tomer, K., Charbonneau, H., & Rossie, S. (1999). The tetratricopeptide repeat domain and a C-terminal region control the activity of Ser/Thr protein phosphatase 5. Journal of Biological Chemistry, 274, 23666–23672.10.1074/jbc.274.33.23666
   PubMed Web of Science ®Google Scholar
• Sippl, M. J. (1993). Recognition of errors in three-dimensional structures of proteins. Proteins: Structure, Function, and Genetics, 17, 355–362.10.1002/(ISSN)1097-0134
   PubMed Web of Science ®Google Scholar
• Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y., & Hay, S. I. (2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature, 434, 214–217.10.1038/nature03342
   PubMed Web of Science ®Google Scholar
• Swingle, M. R., Honkanen, R. E., & Ciszak, E. M. (2004). Structural basis for the catalytic activity of human serine/threonine protein phosphatase-5. Journal of Biological Chemistry, 279, 33992–33999.10.1074/jbc.M402855200
   PubMed Web of Science ®Google Scholar
• Swingle, M., Ni, L., & Honkanen, R. E. (2007). Small-molecule inhibitors of Ser/Thr protein phosphatases. In Protein Phosphatase Protocols (pp. 23–38). New York, NY: Springer.
   Google Scholar
• Thomsen, R., & Christensen, M. H. (2006). MolDock: A new technique for high-accuracy molecular docking. Journal of Medicinal Chemistry, 49, 3315–3321.10.1021/jm051197e
   PubMed Web of Science ®Google Scholar
• Totrov, M., & Abagyan, R. (1997). Flexible protein–ligand docking by global energy optimization in internal coordinates. Proteins Structure Function and Genetics, 29S1(Suppl. 1), 215–220.10.1002/(ISSN)1097-0134
   Google Scholar
• Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31, 455–461.
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26, 1701–1718.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Vriend, G. (1990). WHAT IF: A molecular modeling and drug design program. Journal of Molecular Graphics, 8, 52–56.10.1016/0263-7855(90)80070-V
   PubMedGoogle Scholar
• Wang, Y., Xiao, J., Suzek, T. O., Zhang, J., Wang, J., & Bryant, S. H. (2009). PubChem: A public information system for analyzing bioactivities of small molecules. Nucleic Acids Research, 37(Web Server), W623–W633. Retrieved from https://pubchem.ncbi.nlm.nih.gov/10.1093/nar/gkp456
   PubMedGoogle Scholar
• World malaria report. 2013. WHO Library Cataloguing-in-Publication Data. Retrieved from http://www.who.int/malaria/media/world_malaria_report_2013/en/
   Google Scholar
• Yang, J., Roe, S. M., Cliff, M. J., Williams, M. A., Ladbury, J. E., Cohen, P. T., & Barford, D. (2005). Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. The EMBO Journal, 24(1), 1–10.10.1038/sj.emboj.7600496
   PubMed Web of Science ®Google Scholar