827
Views
16
CrossRef citations to date
0
Altmetric
Research Articles

Virtual screening of small molecules databases for discovery of novel PARP-1 inhibitors: combination of in silico and in vitro studies

, , , , &
Pages 1899-1915 | Received 25 Apr 2016, Accepted 02 Jun 2016, Published online: 17 Jul 2016

References

  • Antolin, A. A., Carotti, A., Nuti, R., Hakkaya, A., Camaioni, E., Mestres, J., … Macchiarulo, A. (2013). Exploring the effect of PARP-1 flexibility in docking studies. Journal of Molecular Graphics and Modelling, 45, 192–201. doi:10.1016/j.jmgm.2013.08.006
  • Bas, D. C., Rogers, D. M., & Jensen, J. H. (2008). Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins: Structure, Function and Genetics, 73, 765–783. doi:10.1002/prot.22102
  • Bellocchi, D., Macchiarulo, A., Costantino, G., & Pellicciari, R. (2005). Docking studies on PARP-1 inhibitors: Insights into the role of a binding pocket water molecule. Bioorganic and Medicinal Chemistry, 13, 1151–1157. doi:10.1016/j.bmc.2004.11.024
  • Bowers, K., Chow, E., Xu, H., Dror, R., Eastwood, M., Gregersen, B., … Shaw, D. (2006). Scalable algorithms for molecular dynamics simulations on commodity clusters. In ACM/IEEE SC 2006 Conference (SC’06) (pp. 43–43). New York, NY. doi:10.1109/SC.2006.54
  • Bryant, H. E., Schultz, N., Thomas, H. D., Parker, K. M., Flower, D., Lopez, E., … Helleday, T. (2005). Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913–917. doi:10.1038/nature03443
  • Case, D. A., Cheatham, T. E., & Darden, T. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26, 1668–1688. doi:10.1002/jcc.20290
  • Cho, A. E., Guallar, V., Berne, B., & Friesner, R. A. (2005). Importance of accurate charges in molecular docking: Quantum Mechanical/Molecular Mechanical (QM/MM) approach. Journal of Computational Chemistry, 26, 915–931. doi:10.1002/jcc.20222. Retrieved from http://www3.interscience.wiley.com/cgi-bin/abstract/110472845/ABSTRACT
  • Costantino, G., Macchiarulo, A., Camaioni, E., & Pellicciari, R. (2001). Modeling of poly(ADP-ribose)polymerase (PARP) inhibitors. Docking of ligands and quantitative structure-activity relationship analysis. Journal of Medicinal Chemistry, 44, 3786–3794. doi:10.1021/jm010116l
  • Damm, W., Frontera, A., Tirado-Rives, J., & Jorgensen, W. L. (1997). OPLS all-atom force field for carbohydrates. Journal of Computational Chemistry, 18, 1955–1970. doi:10.1002/(sici)1096-987x(199712)18:16<1955:aid-jcc1>3.0.co;2-l
  • De Murcia, G., Schreiber, V., Molinete, M., Saulier, B., Poch, O., Masson, M., … De Murcia, J. M. (1994). Structure and function of poly(ADP-ribose) polymerase. Molecular and Cellular Biochemistry., 3, 209–214. doi:10.1007/BF00928438
  • Desmond Molecular Dynamics System, version 3.6. (2013). D. E. Shaw Research. New York, NY.
  • Durdagi, S., Randall, T., Duff, H. J., Chamberlin, A., & Noskov, S. Y. (2014). Rehabilitating drug-induced long-QT promoters: In-silico design of hERG-neutral cisapride analogues with retained pharmacological activity. BMC Pharmacology and Toxicology, 15, 14. doi:10.1186/2050-6511-15-14
  • Durdagi, S., Salmas, R. E., Stein, M., Yurtsever, M., & Seeman, P. (2016). Binding interactions of dopamine and apomorphine in D2High and D2Low states of human Dopamine D2 Receptor (D2R) using computational and experimental techniques. ACS Chemistry Neuroscience, 7, 185–195. doi:10.1021/acschemneuro.5b00271
  • Ekhteiari Salmas, R., Mestanoglu, M., Durdagi, S., Senturk, M., Kaya, A. A., & Kaya, E. C. (2015). Kinetic and in silico studies of hydroxy-based inhibitors of carbonic anhydrase isoforms I and II. Journal of Enzyme Inhibition and Medicinal Chemistry, 31, 31–37. doi:10.3109/14756366.2014.1003216
  • Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. J Chem Phys, 103, 8577–8593. doi:10.1063/1.470117
  • Ferraris, D. V. (2010). Evolution of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors from concept to clinic. Journal of Medicinal Chemistry., 53, 4561–4584. doi:10.1021/jm100012m
  • Ferraris, D., Ko, Y. Sen, Pahutski, T., Ficco, R. P., Serdyuk, L., Alemu, C., … Kalish, V. (2003). Design and synthesis of poly ADP-ribose polymerase-1 inhibitors. 2. Biological evaluation of aza-5[H]-phenanthridin-6-ones as potent, aqueous-soluble compounds for the treatment of ischemic injuries. Journal of Medicinal Chemistry, 46, 3138–3151. doi:10.1021/jm030109s
  • Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., … 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, 6177–6196. Retrieved from http://dx.doi.org/10.1021/jm051256o. doi: 10.1021/jm051256o
  • Griffin, R. J., Curtin, N. J., Newell, D. R., Golding, B. T., Durkacz, B. W., & Calvert, A. H. (1995). The role of inhibitors of poly(ADP-ribose) polymerase as resistance-modifying agents in cancer therapy. Biochimie, 77, 408–422. doi:10.1016/0300-9084(96)88154-5
  • Ha, H. C., & Snyder, S. H. (2000). Poly(ADP-ribose) polymerase-1 in the nervous system. Neurobiology of Disease, 7, 225–239. doi:10.1006/nbdi.2000.0324
  • Halder, A. K., Saha, A., Saha, K. D., & Jha, T. (2015). Stepwise development of structure–activity relationship of diverse PARP-1 inhibitors through comparative and validated in silico modeling techniques and molecular dynamics simulation. Journal of Biomolecular Structure and Dynamics, 33, 1756–1779. doi:10.1080/07391102.2014.969772
  • Halgren, T. A., Murphy, R. B., Friesner, R. A., Beard, H. S., Frye, L. L., Pollard, W. T., & Banks, J. L. (2004). Glide: A new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. Journal of Medicinal Chemistry, 47, 1750–1759. doi:10.1021/jm030644s
  • Hannigan, K., Kulkarni, S. S., Bdzhola, V. G., Golub, A. G., Yarmoluk, S. M., & Talele, T. T. (2013). Identification of novel PARP-1 inhibitors by structure-based virtual screening. Bioorganic and Medicinal Chemistry Letters, 23, 5790–5794. doi:10.1016/j.bmcl.2013.09.007
  • Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review A, 31, 1695–1697. doi:10.1103/PhysRevA.31.1695
  • Huang, H., Cao, Y., Wei, W., Liu, W., Lu, S. Y., Chen, Y. B., … Wu, Y. L. (2013). Targeting poly (ADP-Ribose) polymerase partially contributes to bufalin-induced cell death in multiple myeloma cells. PLoS ONE, 8, e66130. doi:10.1371/journal.pone.0066130
  • Huber, A., Bai, P., De Murcia, J. M., & Murcia, G. De (2004). PARP-1, PARP-2 and ATM in the DNA damage response: Functional synergy in mouse development. DNA Repair, 3, 1103–1108. doi:10.1016/j.dnarep.2004.06.002
  • Irwin, J. J., Sterling, T., Mysinger, M. M., Bolstad, E. S., & Coleman, R. G. (2012). ZINC: A free tool to discover chemistry for biology. Journal of Chemical Information and Modeling. 23, 52, 1757–1768 doi:10.1021/ci3001277
  • Jones, P., Altamura, S., Boueres, J., Ferrigno, F., Fonsi, M., Giomini, C., … Rowley, M. (2009). Discovery of 2-{4-[(3S)-piperidin-3-yl]phenyl}-2H-indazole-7-carboxamide (MK-4827): A novel oral poly(ADP-ribose)polymerase (PARP) inhibitor efficacious in BRCA-1 and -2 mutant tumors. Journal of Medicinal Chemistry, 52, 7170–7185. doi:10.1021/jm901188v
  • Jones, P., Wilcoxen, K., Rowley, M., & Toniatti, C. (2015). Niraparib: A Poly(ADP-ribose) polymerase (PARP) inhibitor for the treatment of tumors with defective homologous recombination. Journal of Medicinal Chemistry, 58, 3302–3314. doi:10.1021/jm5018237
  • Kulkarni, S. S., Singh, S., Shah, J. R., Low, W. K., & Talele, T. T. (2012). Synthesis and SAR optimization of quinazolin-4(3H)-ones as poly(ADP-ribose)polymerase-1 inhibitors. European Journal of Medicinal Chemistry, 50, 264–273. doi:10.1016/j.ejmech.2012.02.001
  • Leonis, G., Avramopoulos, A., Salmas, R. E., Durdagi, S., Yurtsever, M., & Papadopoulos, M. G. (2014). Elucidation of conformational states, dynamics, and mechanism of binding in human kappa-opioid receptor complexes. Journal of Chemical Information and Modeling, 54, 2294–2308. doi:10.1021/ci5002873
  • Li, J. H., Serdyuk, L., Ferraris, D. V., Xiao, G., Tays, K. L., Kletzly, P. W., … Kalish, V. J. (2001). Synthesis of substituted 5[H]phenanthridin-6-ones as potent poly(ADP-ribose)polymerase-1 (PARP1) inhibitors. Bioorganic and Medicinal Chemistry Letters, 11, 1687–1690. doi:10.1016/S0960-894X(01)00281-5
  • Liu, X., Shi, Y., Guan, R., Donawho, C., Luo, Y., & Palma, J. (2008). Potentiation of temozolomide cytotoxicity by poly(ADP)ribose polymerase inhibitor ABT-888 requires a conversion of single-stranded DNA damages to double-stranded DNA breaks. Molecular Cancer, 6, 1621–1629. doi:10.1158/1541-7786.MCR-08-0240
  • Maciag, A. E., Holland, R. J., Kim, Y., Kumari, V., Luthers, C. E., Sehareen, W. S., … Keefer, L. K. (2014). Nitric oxide (NO) releasing poly ADP-ribose polymerase 1 (PARP-1) inhibitors targeted to glutathione S-transferase P1-overexpressing cancer cells. Journal of Medicinal Chemistry, 57, 2292–2302. doi:10.1021/jm401550d
  • Madhavi Sastry, G., Adzhigirey, M., Day, T., Annabhimoju, R., & Sherman, W. (2013). Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments. Journal of Computer-Aided Molecular Design, 27, 221–234. doi:10.1007/s10822-013-9644-8
  • Martyna, G. J., Tobias, D. J., & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. The Journal of Chemical Physics, 101, 4177. doi:10.1063/1.467468
  • 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, 3314–3321. doi:10.1021/ct300418h
  • Mirza, S. B., Salmas, R. E., Fatmi, M. Q., & Durdagi, S. (2016). Virtual screening of eighteen million compounds against Dengue Virus: Combined molecular docking and molecular dynamics simulations study. Journal of Molecular Graphics and Modelling, 66, 99–107. doi:10.1016/j.jmgm.2016.03.008
  • Penning, T. D., Zhu, G. D., Gong, J., Thomas, S., Gandhi, V. B., Liu, X., … Giranda, V. L. (2010). Optimization of phenyl-substituted benzimidazole carboxamide poly(ADP-ribose) polymerase inhibitors: Identification of (S)-2-(2-fluoro-4- (pyrrolidin-2-yl)phenyl)-1 H -benzimidazole-4-carboxamide (A-966492), a highly potent and efficacious inhibitor. Journal of Medicinal Chemistry, 53, 3142–3153. doi:10.1021/jm901775y
  • Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., … Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry, 26, 1781–1802. doi:10.1002/jcc.20289
  • Rigakos, G., & Razis, E. (2012). BRCAness: Finding the Achilles heel in ovarian cancer. The Oncologist, 17, 956–962. doi:10.1634/theoncologist.2012-0028
  • Salmas, R. E., Mestanoglu, M., Yurtsever, M., Noskov, S. Y., & Durdagi, S. (2015). Molecular simulations of solved co-crystallized X-ray structures identify action mechanisms of PDEδ inhibitors. Biophysical Journal, 109, 1163–1166. doi:10.1016/j.bpj.2015.08.001
  • Salmas, R. E., Senturk, M., Yurtsever, M., & Durdagi, S. (2015). Discovering novel carbonic anhydrase type IX (CA IX) inhibitors from seven million compounds using virtual screening and in vitro analysis. Journal of Enzyme Inhibition and Medicinal Chemistry, 6366, 1–9. doi:10.3109/14756366.2015.1036049
  • Salmas, R. E., Unlu, A., Yurtsever, M., Noskov, S. Y., & Durdagi, S. (2015). In silico investigation of PARP-1 catalytic domains in holo and apo states for the design of high-affinity PARP-1 inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry, 6366, 1–9. doi:10.3109/14756366.2015.1005011
  • Salmas, R. E., Yurtsever, M., & Durdagi, S. (2015). Investigation of inhibition mechanism of chemokine receptor CCR5 by micro-second molecular dynamics simulations. Scientific Reports, 5, 13180. doi: 10.1038/srep13180
  • Salmas, R. E., Mestanoglu, M., Unlu, A., Yurtsever, M., & Durdagi, S. (in press). Mutated form (G52E) of inactive Diphtheria Toxin CRM197: Molecular simulations clearly display effect of the mutation to NAD binding. Journal of Biomolecular Structure and Dynamics, in press. doi:10.1080/07391102.2015.1119060
  • Salmas, R. E., Yurtsever, M, & Durdagi, S. (in press). Atomistic molecular dynamics simulations of typical and atypical antipsychotic drugs at the dopamine D2 receptor (D2R) elucidates their inhibition mechanism. Journal of Biomolecular Structure and Dynamics. doi:10.1080/07391102.2016.1159986
  • Schrödinger Release 2014-1: LigPrep. (2014). ( Version 2.9). New York, NY: Schrödinger, LLC.
  • Schrödinger Release 2015-1: QikProp. (2015). ( version 3.4). New York, NY: Schrödinger, LLC.
  • Schrödinger Release 2015-2: Canvas. (2015). ( version 2.4). New York, NY: Schrödinger, LLC.
  • Schrödinger Release 2015-4: Maestro. (2015). ( version 10.4). New York, NY: Schrödinger, LLC.
  • Sherman, W., Beard, H. S., & Farid, R. (2006). Use of an induced fit receptor structure in virtual screening. Chemical Biology and Drug Design, 8, 83–84. doi:10.1111/j.1747-0285.2005.00327.x
  • Steffen, J. D., Brody, J. R., Armen, R. S., & Pascal, J. M. (2013). Structural implications for selective targeting of PARPs. Front Oncol, 3, 301. doi:10.3389/fonc.2013.00301
  • Subbotina, J., Yarov-Yarovoy, V., Lees-Miller, J., Durdagi, S., Guo, J., Duff, H. J., & Noskov, S. Y. (2010). Structural refinement of the hERG1 pore and voltage-sensing domains with ROSETTA-membrane and molecular dynamics simulations. Proteins: Structure Function and Bioinformatics, 78, 2922–2934. doi:10.1002/prot.22815
  • Tikhe, J. G., Webber, S. E., Hostomsky, Z., Maegley, K. a, Ekkers, A., Li, J., … Newell, D. R. (2004). Design, synthesis, and evaluation of 3,4-dihydro-2H-[1,4]diazepino[6,7,1-hi]indol-1-ones as inhibitors of poly(ADP-ribose) polymerase. Journal of Medicinal Chemistry, 47, 5467–5481. doi:10.1021/jm030513r
  • Weiser, J. J., Shenkin, P. S., & Still, W. C. (1999). Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO). Journal of Computational Chemistry, 20, 217–230. doi:10.1002/(SICI)1096-987X(19990130)20:2<217:AID-JCC4>3.0.CO;2-A
  • White, A. W., Almassy, R., Calvert, A. H., Curtin, N. J., Griffin, R. J., Hostomsky, Z., … Golding, B. T. (2000). Resistance-modifying agents. 9.Synthesis and biological properties of benzimidazole inhibitors of the DNA repair enzyme poly(ADP-ribose) polymerase. Journal of Medicinal Chemistry, 43, 4084–4097. doi:10.1021/jm000950v
  • Xie, Z., Zhou, Y., Zhao, W., Jiao, H., Chen, Y., Yang, Y., & Li, Z. (2015). Identification of novel PARP-1 inhibitors: Drug design, synthesis and biological evaluation. Bioorganic & Medicinal Chemistry Letters, 25, 4557–4561. doi:10.1016/j.bmcl.2015.08.060
  • Ye, N., Chen, C. H., Chen, T., Song, Z., He, J. X., Huan, X. J., … Zhang, A. (2013). Design, synthesis, and biological evaluation of a series of benzo[de ][1,7]naphthyridin-7(8 H)-ones bearing a functionalized longer chain appendage as novel PARP1 inhibitors. Journal of Medicinal Chemistry, 56, 2885–2903. doi:10.1021/jm301825t

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.