280
Views
16
CrossRef citations to date
0
Altmetric
Research Articles

Computational analysis of BACE1-ligand complex crystal structures and linear discriminant analysis for identification of BACE1 inhibitors with anti P-glycoprotein binding property

ORCID Icon, &
Pages 262-276 | Received 20 Jun 2016, Accepted 16 Dec 2016, Published online: 12 Jan 2017

References

  • Ajmani, S., Janardhan, S., & Viswanadhan, V. N. (2013). Toward a general predictive QSAR model for gamma-secretase inhibitors. Molecular Diversity, 17, 421–434. doi:10.1007/s11030-013-9441-2
  • Alzheimer, A. (1987). About a peculiar disease of the cerebral cortex. By Alois Alzheimer, 1907 (Translated by L. Jarvik and H. Greenson). Alzheimer Disease and Associated Disorders, 1, 3–8. Retrieved from http://journals.lww.com/alzheimerjournal/Pages/default.aspx
  • Ashwood, V. A., Field, M. J., Horwell, D. C., Julien-Larose, C., Lewthwaite, R. A., McCleary, S., … Singh, L. (2001). Utilization of an intramolecular hydrogen bond to increase the CNS penetration of an NK 1 receptor antagonist. Journal of Medicinal Chemistry, 44, 2276–2285. doi:10.1021/jm010825z
  • Babor, M., Sobolev, V., & Edelman, M. (2002). Conserved positions for ribose recognition: importance of water bridging interactions among ATP, ADP and FAD-protein complexes. Journal of Molecular Biology, 323, 523–532. doi:10.1016/S0022-2836(02)00975-0
  • Barillari, C., Taylor, J., Viner, R., & Essex, J. W. (2007). Classification of water molecules in protein binding sites. Journal of the American Chemical Society, 129, 2577–2587. doi:10.1021/ja066980q
  • Bhat, T. N., Bentley, G. A., Boulot, G., Greene, M. I., Tello, D., Dall’Acqua, W., … Poljak, R. J. (1994). Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proceedings of the National Academy of Sciences, 91, 1089–1093. doi:10.1073/pnas.91.3.1089
  • Bissantz, C., Kuhn, B., & Stahl, M. (2010). A medicinal chemist’s guide to molecular interactions. Journal of Medicinal Chemistry, 53, 5061–5084. doi:10.1021/jm100112j
  • Brandl, M., Weiss, M. S., Jabs, A., Sühnel, J., & Hilgenfeld, R. (2001). C–H pi-interactions in proteins. Journal of Molecular Biology, 307, 357–377.10.1006/jmbi.2000.4473
  • Broccatelli, F., Larregieu, C. A., Cruciani, G., Oprea, T. I., & Benet, L. Z. (2012). Improving the prediction of the brain disposition for orally administered drugs using BDDCS. Advanced Drug Delivery Reviews, 64, 95–109. doi:10.1016/j.addr.2011.12.008
  • Charrier, N., Clarke, B., Cutler, L., Demont, E., Dingwall, C., Dunsdon, R., … Wayne, G. (2009). Second generation of BACE-1 inhibitors part 3: Towards non hydroxyethylamine transition state mimetics. Bioorganic & Medicinal Chemistry Letters, 19, 3674–3678. doi:10.1016/j.bmcl.2009.03.149
  • Coburn, C. A., Stachel, S. J., Li, Y. M., Rush, D. M., Steele, T. G., Chen-Dodson, E., … Wang, T. (2004). Identification of a small molecule nonpeptide active site β-secretase inhibitor that displays a nontraditional binding mode for aspartyl proteases. Journal of Medicinal Chemistry, 47, 6117–6119. doi:10.1021/jm049388p
  • Desai, P. V., Raub, T. J., & Blanco, M. J. (2012). How hydrogen bonds impact P-glycoprotein transport and permeability. Bioorganic & Medicinal Chemistry Letters, 22, 6540–6548. doi:10.1016/j.bmcl.2012.08.059
  • Di, L., Rong, H., & Feng, B. (2013). Demystifying brain penetration in central nervous system drug discovery. Journal of Medicinal Chemistry, 56, 2–12. doi:10.1021/jm301297f
  • Fridén, M., Winiwarter, S., Jerndal, G., Bengtsson, O., Wan, H., Bredberg, U., … Antonsson, M. (2009). Structure−brain exposure relationships in rat and human using a novel data set of unbound drug concentrations in brain interstitial and cerebrospinal fluids. Journal of Medicinal Chemistry, 52, 6233–6243. doi:10.1021/jm901036q
  • Ghosh, A. K., & Osswald, H. L. (2014). BACE1 (β-secretase) inhibitors for the treatment of Alzheimer’s disease. Chemical Society Reviews, 43, 6768–6813. doi:10.1039/c3cs60460h
  • Gleeson, M. P. (2008). Generation of a set of simple, interpretable ADMET rules of thumb. Journal of Medicinal Chemistry, 51, 817–834. doi:10.1021/jm701122q
  • Gueto-Tettay, C., Drosos, J. C., & Vivas-Reyes, R. (2011). Quantum mechanics study of the hydroxyethylamines-BACE-1 active site interaction energies. Journal of Computer-Aided Molecular Design, 25, 583–597. doi:10.1007/s10822-011-9443-z
  • Hamada, Y., & Kiso, Y. (2009). Recent progress in the drug discovery of non-peptidic BACE1 inhibitors. Expert Opinion on Drug Discovery, 4, 391–416. doi:10.1517/17460440902806377
  • Hilpert, H., Guba, W., Woltering, T. J., Wostl, W., Pinard, E., Mauser, H., … Narquizian, R. (2013). β-secretase (BACE1) inhibitors with high in vivo efficacy suitable for clinical evaluation in Alzheimer’s disease. Journal of Medicinal Chemistry, 56, 3980–3995. doi:10.1021/jm400225m
  • Hitchcock, S. A. (2012). Structural modifications that alter the P-glycoprotein efflux properties of compounds. Journal of Medicinal Chemistry, 55, 4877–4895. doi:10.1021/jm201136z
  • Hitchcock, S. A., & Pennington, L. D. (2006). Structure−brain exposure relationships. Journal of Medicinal Chemistry, 49, 7559–7583. doi:10.1021/jm060642i
  • Huang, D., Lüthi, U., Kolb, P., Cecchini, M., Barberis, A., & Caflisch, A. (2006). In silico discovery of β-secretase inhibitors. Journal of the American Chemical Society, 128, 5436–5443. doi:10.1021/ja0573108
  • Huang, D., Lüthi, U., Kolb, P., Edler, K., Cecchini, M., Audetat, S., … Caflisch, A. (2005). Discovery of cell-permeable non-peptide inhibitors of beta-secretase by high-throughput docking and continuum electrostatics calculations. Journal of Medicinal Chemistry, 48, 5108–5111. doi:10.1021/jm050499d
  • Huang, N., & Shoichet, B. K. (2008). Exploiting ordered waters in molecular docking. Journal of Medicinal Chemistry, 51, 4862–4865. doi:10.1021/jm8006239
  • Huberty, C. J., & Olejnik, S. (2006). Applied MANOVA and discriminant analysis (2nd ed., p. 488). Hoboken, NJ: Hohn Wiley and Sons.
  • Kandalepas, P. C., & Vassar, R. (2012). Identification and biology of β-secretase. Journal of Neurochemistry, 120, 55–61. doi:10.1111/j.1471-4159.2011.07512.x
  • Klaholz, B. P., & Moras, D. (2002). C–H·O hydrogen bonds in the nuclear receptor RARγ—a potential tool for drug selectivity. Structure, 10, 1197–1204. doi:10.1016/S0969-2126(02)00828-6
  • Kolb, P., & Caflisch, A. (2006). Automatic and efficient decomposition of two-dimensional structures of small molecules for fragment-based high-throughput docking. Journal of Medicinal Chemistry, 49, 7384–7392. doi:10.1021/jm060838i
  • Kuglstatter, A., Stahl, M., Peters, J. U., Huber, W., Stihle, M., Schlatter, D., … Hennig, M. (2008). Tyramine fragment binding to BACE-1. Bioorganic & Medicinal Chemistry Letters, 18, 1304–1307. doi:10.1016/j.bmcl.2008.01.032
  • Kuhn, B., Mohr, P., & Stahl, M. (2010). Intramolecular hydrogen bonding in medicinal chemistry. Journal of Medicinal Chemistry, 53, 2601–2611. doi:10.1021/jm100087s
  • Ladbury, J. E. (1996). Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design. Chemistry & Biology, 3, 973–980. doi:10.1016/S1074-5521(96)90164-7
  • Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: Multiple ligand–protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51, 2778–2786. doi:10.1021/ci200227u
  • Li, Z., & Lazaridis, T. (2003). Thermodynamic contributions of the ordered water molecule in HIV-1 protease. Journal of the American Chemical Society, 125, 6636–6637. doi:10.1021/ja0299203
  • Lu, Y., Yang, C. Y., & Wang, S. (2006). Binding free energy contributions of interfacial waters in HIV-1 protease/inhibitor complexes. Journal of the American Chemical Society, 128, 11830–11839. doi:10.1021/ja058042g
  • Mahar Doan, K. M., Humphreys, J. E., Webster, L. O., Wring, S. A., Shampine, L. J., Serabjit-Singh, C. J., … Polli, J. W. (2002). Passive permeability and P-glycoprotein-mediated efflux differentiate central nervous system (CNS) and non-CNS marketed drugs. Journal of Pharmacology and Experimental Therapeutics, 303, 1029–1037. doi:10.1124/jpet.102.039255
  • Manoharan, P., Chennoju, K., & Ghoshal, N. (2015). Target specific proteochemometric model development for BACE1 - protein flexibility and structural water are critical in virtual screening. Molecular BioSystems, 11, 1955–1972. doi:10.1039/c5mb00088b
  • Manoharan, P., & Ghoshal, N. (2010). Protein-bound fragment based virtual screening (PFVS) approach to identify potential lead fragments as BACE1 inhibitors. Neuroscience Research, 68S, e447–e456. doi:10.1016/j.neures.2010.07.1995
  • Manoharan, P., & Ghoshal, N. (2012). Rationalizing lead optimization by consensus 2D-CoMFA CoMSIA GRIND (3D) QSAR guided fragment hopping in search of γ-secretase inhibitors. Molecular Diversity, 16, 563–577. doi:10.1007/s11030-012-9388-8
  • Manoharan, P., Vijayan, R. S., & Ghoshal, N. (2010). Rationalizing fragment based drug discovery for BACE1: insights from FB-QSAR, FB-QSSR, multi objective (MO-QSPR) and MIF studies. Journal of Computer-Aided Molecular Design, 24, 843–864. doi:10.1007/s10822-010-9378-9
  • Meyer, E. A., Castellano, R. K., & Diederich, F. (2003). Interactions with aromatic rings in chemical and biological recognition. Angewandte Chemie International Edition, 42, 1210–1250. doi:10.1002/anie.200390319
  • Mok, N. Y., Chadwick, J., Kellett, K. A., Casas-Arce, E., Hooper, N. M., Johnson, A. P., & Fishwick, C. W. (2013). Discovery of biphenylacetamide-derived inhibitors of BACE1 using de novo structure-based molecular design. Journal of Medicinal Chemistry, 56, 1843–1852. doi:10.1021/jm301127x
  • Molecular Operating Environment. 2012.10. Chemical Computing Group Inc., 1010 Sherbooke St. West, Suite #910. Montreal, QC, Canada, H3A 2R7, 2012.
  • Nastase, A. F., & Boyd, D. B. (2012). Simple structure-based approach for predicting the activity of inhibitors of beta-secretase (BACE1) associated with Alzheimer’s disease. Journal of Chemical Information and Modeling, 52, 3302–3307. doi:10.1021/ci300331d
  • O’Brien, R. J., & Wong, P. C. (2011). Amyloid precursor protein processing and Alzheimer's disease. Annual Review of Neuroscience, 34, 185–204. doi:10.1146/annurev-neuro-061010-113613
  • Panigrahi, S. K., & Desiraju, G. R. (2007). Strong and weak hydrogen bonds in the protein-ligand interface. Proteins: Structure, Function, and Bioinformatics, 67, 128–141. doi:10.1002/prot.21253
  • Patel, H., Gruning, B. A., Gunther, S., & Merfort, I. (2014). PyWATER: A PyMOL plug-in to find conserved water molecules in proteins by clustering. Bioinformatics, 30, 2978–2980. doi:10.1093/bioinformatics/btu424
  • Polgár, T., Magyar, C., Simon, I., & Keserü, G. M. (2007). Impact of ligand protonation on virtual screening against β-secretase (BACE1). Journal of Chemical Information and Modeling, 47, 2366–2373. doi:10.1021/ci700223p
  • Quiocho, F. A., Wilson, D. K., & Vyas, N. K. (1989). Substrate specificity and affinity of a protein modulated by bound water molecules. Nature, 340, 404–407. doi:10.1038/340404a0
  • RCSB PDB. (2015). As of November, 02, 2015, there are 326 BACE1 X-ray structures using the key word Human BACE1. Retrieved from http://www.rcsb.org/pdb
  • Roos, K., Viklund, J., Meuller, J., Kaspersson, K., & Svensson, M. (2014). Potency prediction of β-secretase (BACE-1) inhibitors using density functional methods. Journal of Chemical Information and Modeling, 54, 818–825. doi:10.1021/ci400374z
  • Salentin, S., Schreiber, S., Haupt, V. J., Adasme, M. F., & Schroeder, M. (2015). PLIP: Fully automated protein-ligand interaction profiler. Nucleic Acids Research, 43, W443–W447. doi:10.1093/nar/gkv315
  • Sarkel, S., & Desiraju, G. R. (2004). N–H...O, O–H...O, and C–H...O hydrogen bonds in protein-ligand complexes: strong and weak interactions in molecular recognition. Proteins: Structure, Function, and Bioinformatics, 54, 247–259. doi:10.1002/prot.10567
  • Scheiner, S., Kar, T., & Pattanayak, J. (2002). Comparison of various types of hydrogen bonds involving aromatic amino acids. Journal of the American Chemical Society, 124, 13257–13264. doi:10.1021/ja027200q
  • SPSS Version 15.0. (2008). SPSS Inc. Chicago, IL.
  • Steiner, T. (2002). Hydrogen bonds from water molecules to aromatic acceptors in very high-resolution protein crystal structures. Biophysical Chemistry, 95, 195–201. doi:10.1016/S0301-4622(01)00256-3
  • Steiner, T., & Koellner, G. (2001). Hydrogen bonds with pi-acceptors in proteins: frequencies and role in stabilizing local 3D structures. Journal of Molecular Biology, 305, 535–557. doi:10.1006/jmbi.2000.4301
  • Tame, J. R., Sleigh, S. H., Wilkinson, A. J., & Ladbury, J. E. (1996). The role of water in sequence-independent ligand binding by an oligopeptide transporter protein. Nature Structural Biology, 3, 998–1001. doi:10.1038/nsb1296-998
  • Tiwari, A., & Panigrahi, S. K. (2007). HBAT: A complete package for analysing strong and weak hydrogen bonds in macromolecular crystal structures. Silico Biology, 7, 651–661. Retrieved from http://www.iospress.nl/journal/in-silico-biology
  • Toth, G., Bowers, S. G., Truong, A. P., & Probst, G. (2007). The role and significance of unconventional hydrogen bonds in small molecule recognition by biological receptors of pharmaceutical relevance. Current Pharmaceutical Design, 13, 3476–3493.10.2174/138161207782794284
  • Vassar, R. (2014). BACE1 inhibitor drugs in clinical trials for Alzheimer’s disease. Alzheimer’s Research & Therapy, 6, 89. doi:10.2174/138161207782794284
  • Vijayan, R. S., Prabu, M., Mascarenhas, N. M., & Ghoshal, N. (2009). Hybrid structure-based virtual screening protocol for the identification of novel BACE1 inhibitors. Journal of Chemical Information and Modeling, 49, 647–657. doi:10.1021/ci800386v
  • Yuan, J., Venkatraman, S., Zheng, Y., McKeever, B. M., Dillard, L. W., & Singh, S. B. (2013). Structure-based design of β-site app cleaving enzyme 1 (BACE1) inhibitors for the treatment of Alzheimer’s disease. Journal of Medicinal Chemistry, 56, 4156–4180. doi:10.1021/jm301659n

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.