Identification of promising anti-DNA gyrase antibacterial compounds using de novo design, molecular docking and molecular dynamics studies

References

• Ali, A., Danishuddin, Maryam, L., Srivastava, G., Sharma, A., & Khan, A. U. (2018). Designing of inhibitors against CTX-M-15 type beta-lactamase: Potential drug candidate against beta-lactamases-producing multi-drug-resistant bacteria. Journal of Biomolecular Structure and Dynamics, 36(7), 1806–1821. doi: 10.1080/07391102.2017.1335434
   PubMed Web of Science ®Google Scholar
• Ali, A., Gupta, D., Srivastava, G., Sharma, A., & Khan, A. U. (2019). Molecular and computational approaches to understand resistance of New Delhi Metallo beta- lactamase variants (NDM-1, NDM-4, NDM-5, NDM-6, NDM-7)-producing strains against carbapenems. Journal of Biomolecular Structure and Dynamics, 37(8), 2061–2071. doi: 10.1080/07391102.2018.1475261
   Web of Science ®Google Scholar
• Aqvist, J., Medina, C., & Samuelsson, J. E. (1994). A new method for predicting binding affinity in computer-aided drug design. Protein Engineering, Design and Selection, 7(3), 385–391. doi: 10.1093/protein/7.3.385
   Web of Science ®Google Scholar
• Barancokova, M., Kikelj, D., & Ilas, J. (2018). Recent progress in the discovery and development of DNA gyrase B inhibitors. Future Medicinal Chemistry, 10(10), 1207–1227. doi: 10.4155/fmc-2017-0257
   PubMed Web of Science ®Google Scholar
• Behmard, E., Najafi, A., & Ahmadi, A. (2019). Understanding the resistance mechanism of penicillin binding protein 1a mutant against cefotaxime using molecular dynamic simulation. Journal of Biomolecular Structure and Dynamics, 37(3), 741–749. doi: 10.1080/07391102.2018.1439404
   PubMed Web of Science ®Google Scholar
• Beveridge, D. L., & DiCapua, F. M. (1989). Free energy via molecular simulation: Applications to chemical and biomolecular systems. Annual Review of Biophysics and Biophysical Chemistry, 18(1), 431–492. doi: 10.1146/annurev.bb.18.060189.002243
   PubMedGoogle Scholar
• Brown, E. D., & Wright, G. D. (2016). Antibacterial drug discovery in the resistance era. Nature, 529(7586), 336–343. doi: 10.1038/nature17042
   PubMed Web of Science ®Google Scholar
• Case, D. A., Babin, V., Berryman, J. T., Betz, R. M., Cai, Q., Cerutti, D. S., … Kollman, P. A. (2014). AMBER 14. San Francisco, CA: University of California.
   Google Scholar
• Champoux, J. J. (2001). DNA topoisomerases: structure, function, and mechanism. Annual Review of Biochemistry, 70(1), 369–413. doi: 10.1146/annurev.biochem.70.1.369
   PubMedGoogle Scholar
• Chikhale, R. V., Barmade, M. A., Murumkar, P. R., & Yadav, M. R. (2018). Overview of the development of DprE1 inhibitors for combating the menace of tuberculosis. Journal of Medicinal Chemistry, 61(19), 8563–8593. doi: 10.1021/acs.jmedchem.8b00281
   PubMed Web of Science ®Google Scholar
• Collin, F., Karkare, S., & Maxwell, A. (2011). Exploiting bacterial DNA gyrase as a drug target: Current state and perspectives. Applied Microbiology and Biotechnology, 92(3), 479–497. doi: 10.1007/s00253-011-3557-z
   PubMed Web of Science ®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, 42717. doi: 10.1038/srep42717
   PubMed Web of Science ®Google Scholar
• Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417–433. doi: 10.1128/MMBR.00016-10
   PubMed Web of Science ®Google Scholar
• Douguet, D. (2010). e-LEA3D: a computational-aided drug design web server. Nucleic Acids Research, 38(Web Server), W615–W621. doi: 10.1093/nar/gkq322
   PubMedGoogle Scholar
• Douguet, D., Munier-Lehmann, H., Labesse, G., & Pochet, S. (2005). LEA3D: A computer-aided ligand design for structure-based drug design. Journal of Medicinal Chemistry, 48(7), 2457–2468. doi: 10.1021/jm0492296
   PubMed Web of Science ®Google Scholar
• Durcik, M., Lovison, D., Skok, Ž., Durante Cruz, C., Tammela, P., Tomašič, T., … Zidar, N. (2018a). New N-phenylpyrrolamide DNA gyrase B inhibitors: optimization of efficacy and antibacterial activity. European Journal of Medicinal Chemistry, 154, 117–132. doi: 10.1016/j.ejmech.2018.05.011
   PubMed Web of Science ®Google Scholar
• Durcik, M., Tammela, P., Barancokova, M., Tomasic, T., Ilas, J., Kikelj, D., & Zidar, N. (2018b). Synthesis and evaluation of n-phenylpyrrolamides as DNA gyrase B inhibitors. ChemMedChem, 13(2), 186–198. doi: 10.1002/cmdc.201700549
   PubMed Web of Science ®Google Scholar
• East, S. P., & Silver, L. L. (2013). Multitarget ligands in antibacterial research: Progress and opportunities. Expert Opinion on Drug Discovery, 8(2), 143–156. doi: 10.1517/17460441.2013.743991
   PubMed Web of Science ®Google Scholar
• Gellert, M., Mizuuchi, K., O'Dea, M. H., & Nash, H. A. (1976). DNA gyrase: An enzyme that introduces superhelical turns into DNA. Proceedings of the National Academy of Sciences of the United States of America, 73(11), 3872–3876. doi: 10.1073/pnas.73.11.3872
   PubMed Web of Science ®Google Scholar
• Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. doi: 10.1517/17460441.2015.1032936
   PubMed Web of Science ®Google Scholar
• Gjorgjieva, M., Tomašič, T., Barančokova, M., Katsamakas, S., Ilaš, J., Tammela, P., … Kikelj, D. (2016). Discovery of benzothiazole scaffold-based DNA gyrase B inhibitors. Journal of Medicinal Chemistry, 59(19), 8941–8954. doi: 10.1021/acs.jmedchem.6b00864
   PubMed Web of Science ®Google Scholar
• Hopkins, A. L., Groom, C. R., & Alex, A. (2004). Ligand efficiency: A useful metric for lead selection. Drug Discovery Today, 9(10), 430–431. doi: 10.1016/S1359-6446(04)03069-7
   PubMed Web of Science ®Google Scholar
• Hughes, J. P., Rees, S., Kalindjian, S. B., & Philpott, K. L. (2011). Principles of early drug discovery. British Journal of Pharmacology, 162(6), 1239–1249. doi: 10.1111/j.1476-5381.2010.01127.x
   PubMed Web of Science ®Google Scholar
• Islam, M. A., & Pillay, T. S. (2016). Structural requirements for potential HIV-integrase inhibitors identified using pharmacophore-based virtual screening and molecular dynamics studies. Molecular Biosystems, 12(3), 982–993. doi: 10.1039/C5MB00767D
   PubMedGoogle Scholar
• Jeankumar, V. U., Renuka, J., Santosh, P., Soni, V., Sridevi, J. P., Suryadevara, P., … Sriram, D. (2013). Thiazole-aminopiperidine hybrid analogues: design and synthesis of novel Mycobacterium tuberculosis GyrB inhibitors. European Journal of Medicinal Chemistry, 70, 143–153. doi: 10.1016/j.ejmech.2013.09.025
   PubMed Web of Science ®Google Scholar
• Jedrzejas, M. J., Singh, S., Brouillette, W. J., Air, G. M., & Luo, M. (1995). A strategy for theoretical binding constant, Ki, calculations for neuraminidase aromatic inhibitors designed on the basis of the active site structure of influenza virus neuraminidase. Proteins: Structure, Function, and Genetics, 23(2), 264–277. doi: 10.1002/prot.340230215
   PubMed Web of Science ®Google Scholar
• Kaur, P., Agarwal, S., & Datta, S. (2009). Delineating bacteriostatic and bactericidal targets in mycobacteria using IPTG inducible antisense expression. PLoS One, 4(6), e5923. doi: 10.1371/journal.pone.0005923
   PubMed Web of Science ®Google Scholar
• Keseru, G. M., & Makara, G. M. (2009). The influence of lead discovery strategies on the properties of drug candidates. Nature Reviews Drug Discovery, 8(3), 203–212. doi: 10.1038/nrd2796
   PubMed Web of Science ®Google Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., … Cheatham, T. E. 3rd. (2000). Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. doi: 10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Korb, O., StüTzle, T., & Exner, T. E. (2009). Empirical scoring functions for advanced protein-ligand docking with PLANTS. Journal of Chemical Information and Modeling, 49(1), 84–96. doi: 10.1021/ci800298z
   PubMed Web of Science ®Google Scholar
• Kozhikkadan Davis, C., Nasla, K., Anjana, A. K., & Rajanikant, G. K. (2018). Taxifolin as dual inhibitor of Mtb DNA gyrase and isoleucyl-tRNA synthetase: In silico molecular docking, dynamics simulation and in vitro assays. In Silico Pharmacology, 6(1), 8. doi: 10.1007/s40203-018-0045-5
   PubMedGoogle 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(2), 283–291. doi:citeulike-article-id:1720734 doi: 10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Mbaye, M. N., Gilis, D., & Rooman, M. (2019). Rational antibiotic design: in silico structural comparison of the functional cavities of penicillin-binding proteins and ss-lactamases. Journal of Biomolecular Structure and Dynamics, 37(1), 65–74. doi: 10.1080/07391102.2017.1418678
   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(16), 2785–2791. doi: 10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Oblak, M., Kotnik, M., & Solmajer, T. (2007). Discovery and development of ATPase inhibitors of DNA gyrase as antibacterial agents. Current Medicinal Chemistry, 14(19), 2033–2047. doi: 10.2174/092986707781368414
   PubMed Web of Science ®Google Scholar
• Parasuraman, S. (2012). Protein data bank. Journal of Pharmacology and Pharmacotherapeutics, 3(4), 351–352. doi: 10.4103/0976-500X.103704
   PubMedGoogle Scholar
• Reynolds, C. H., Bembenek, S. D., & Tounge, B. A. (2007). The role of molecular size in ligand efficiency. Bioorganic and Medicinal Chemistry Letters, 17(15), 4258–4261. doi: 10.1016/j.bmcl.2007.05.038
   PubMed Web of Science ®Google Scholar
• Reynolds, C. H., & Reynolds, R. C. (2017). Group Additivity in ligand binding affinity: An alternative approach to ligand efficiency. Journal of Chemical Information and Modeling, 57(12), 3086–3093. doi: 10.1021/acs.jcim.7b00381
   PubMed Web of Science ®Google Scholar
• Savage, V. J., Charrier, C., Salisbury, A.-M., Moyo, E., Forward, H., Chaffer-Malam, N., … Stokes, N. R. (2016). Biological profiling of novel tricyclic inhibitors of bacterial DNA gyrase and topoisomerase IV. Journal of Antimicrobial Chemotherapy, 71(7), 1905–1913. doi: 10.1093/jac/dkw061
   PubMed Web of Science ®Google Scholar
• Schrodinger, L. (2015). The PyMOL Molecular Graphics System, Version 1.8.
   Google Scholar
• Schultes, S., de Graaf, C., Haaksma, E. E. J., de Esch, I. J. P., Leurs, R., & KräMer, O. (2010). Ligand efficiency as a guide in fragment hit selection and optimization. Drug Discovery Today Technologies, 7(3), e147–202. doi: 10.1016/j.ddtec.2010.11.003
   Google Scholar
• Shi, C., Zhang, Y., Wang, T., Lu, W., Zhang, S., Guo, B., … Yang, Y. (2019). Design, synthesis, and biological evaluation of novel DNA gyrase-inhibiting spiropyrimidinetriones as potent antibiotics for treatment of infections caused by multidrug-resistant gram-positive bacteria. Journal of Medicinal Chemistry, 62(6), 2950–2973. doi: 10.1021/acs.jmedchem.8b01750
   Google Scholar
• Shityakov, S., & Forster, C. (2013). Multidrug resistance protein P-gp interaction with nanoparticles (fullerenes and carbon nanotube) to assess their drug delivery potential: A theoretical molecular docking study. International Journal of Computational Biology and Drug Design, 6(4), 343–357. doi: 10.1504/IJCBDD.2013.056801
   PubMedGoogle Scholar
• Silver, L. L. (2011). Challenges of antibacterial discovery. Clinical Microbiology Reviews, 24(1), 71–109. doi: 10.1128/CMR.00030-10
   PubMed Web of Science ®Google Scholar
• Sulaiman, K. O., Kolapo, T. U., Onawole, A. T., Islam, A., Adegoke, R. O., & Badmus, S. O. (2018). Molecular dynamics and combined docking studies for the identification of Zaire Ebola Virus inhibitors. Journal of Biomolecular Structure and Dynamics, 1–31. doi: 10.1080/07391102.2018.1506362
   PubMedGoogle Scholar
• Tiz, D. B., Skok, Ž., Durcik, M., Tomašič, T., Mašič, L. P., Ilaš, J., … Zidar, N. (2019). An optimised series of substituted N-phenylpyrrolamides as DNA gyrase B inhibitors. European Journal of Medicinal Chemistry, 167, 269–290. doi: 10.1016/j.ejmech.2019.02.004
   PubMed Web of Science ®Google Scholar
• Tomasic, T., & Masic, L. P. (2014). Prospects for developing new antibacterials targeting bacterial type IIA topoisomerases. Current Topics in Medicinal Chemistry, 14(1), 130–151. doi: 10.2174/1568026613666131113153251
   PubMed Web of Science ®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(2), 455–461. doi: 10.1002/jcc.21334
   PubMed Web of Science ®Google Scholar
• Verma, P., Maurya, P., Tiwari, M., & Tiwari, V. (2019). In-silico interaction studies suggest RND efflux pump mediates polymyxin resistance in Acinetobacter baumannii. Journal of Biomolecular Structure and Dynamics, 37(1), 95–103. doi: 10.1080/07391102.2017.1418680
   PubMed Web of Science ®Google Scholar
• Walsh, C. T., & Wencewicz, T. A. (2014). Prospects for new antibiotics: A molecule-centered perspective. The Journal of Antibiotics, 67(1), 7–22. doi: 10.1038/ja.2013.49
   PubMed Web of Science ®Google Scholar
• Wang, J. M., Hou, T. J., & Xu, X. J. (2006). Recent advances in free energy calculations with a combination of molecular mechanics and continuum models. Current Computer Aided-Drug Design, 2(3), 287–306. doi: 10.2174/157340906778226454
   Web of Science ®Google Scholar
• Wang, W., Donini, O., Reyes, C. M., & Kollman, P. A. (2001). Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annual Review of Biophysics and Biomolecular Structure, 30(1), 211–243. doi: 10.1146/annurev.biophys.30.1.211
   PubMedGoogle Scholar
• Wigley, D. B., Davies, G. J., Dodson, E. J., Maxwell, A., & Dodson, G. (1991). Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature, 351(6328), 624–629. doi: 10.1038/351624a0
   PubMed Web of Science ®Google Scholar