186
Views
2
CrossRef citations to date
0
Altmetric
Research Article

Structure-based virtual screening and molecular dynamics approaches to identify new inhibitors of Staphylococcus aureus sortase A

, , &
Pages 1157-1169 | Received 27 Dec 2022, Accepted 28 Mar 2023, Published online: 15 May 2023

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindah, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
  • Adcock, S. A., & McCammon, J. A. (2006). Molecular dynamics: Survey of methods for simulating the activity of proteins. Chemical Reviews, 106(5), 1589–1615. https://doi.org/10.1021/cr040426m
  • Allouche, A. (2011). Software news and updates gabedit—A graphical user interface for computational chemistry softwares. Journal of Computational Chemistry, 32(1), 174–182. https://doi.org/10.1002/jcc
  • Bassoum, O., Ba-Diallo, A., Sougou, N. M., Lèye, M. M. M., Diongue, M., Cissé, N. F., Faye, A., Seck, I., Fall, D., & Tal-Dia, A. (2019). Community pharmacists’ knowledge, practices and perceptions on antibiotic use and resistance: A cross-sectional, self-administered questionnaire survey, in Guediawaye and Pikine, Senegal. Open Journal of Epidemiology, 09(04), 289–308. https://doi.org/10.4236/ojepi.2019.94021
  • Bentley, M. L., Lamb, E. C., & McCafferty, D. G. (2008). Mutagenesis studies of substrate recognition and catalysis in the sortase A transpeptidase from Staphylococcus aureus. The Journal of Biological Chemistry, 283(21), 14762–14771. https://doi.org/10.1074/jbc.M800974200
  • Bhardwaj, V. K., & Purohit, R. (2021). Targeting the protein-protein interface pocket of Aurora-A-TPX2 complex: Rational drug design and validation. Journal of Biomolecular Structure & Dynamics, 39(11), 3882–3891. https://doi.org/10.1080/07391102.2020.1772109
  • Cada, D. J., & Baker, D. E. (2014). Oritavancin diphosphate. Hospital Pharmacy, 49(11), 1049–1060. https://doi.org/10.1310/hpj4911-1049
  • Candel, F. J., & Peñuelas, M. (2017). Delafloxacin: Design, development and potential place in therapy. Drug Design, Development and Therapy, 11, 881–891. https://doi.org/10.2147/DDDT.S106071
  • Cascioferro, S., Totsika, M., & Schillaci, D. (2014). Sortase A: An ideal target for anti-virulence drug development. Microbial Pathogenesis, 77, 105–112. https://doi.org/10.1016/j.micpath.10.007
  • Chan, A. H., Yi, S. W., Weiner, E. M., Amer, B. R., Sue, C. K., Wereszczynski, J., … Robert, T. (2018). NMR structure-based optimization of Staphylococcus aureus sortase A pyridazinone inhibitors. HHS Public Access, 90(3), 327–344. https://doi.org/10.1111/cbdd.12962.NMR
  • Clancy, K. W., Melvin, J. A., & McCafferty, D. G. (2010). Sortase transpeptidases: Insights into mechanism, substrate specificity, and inhibition. Biopolymers, 94(4), 385–396. https://doi.org/10.1002/bip.21472
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
  • Dramsi, S., Trieu-Cuot, P., & Bierne, H. (2005). Sorting sortases: A nomenclature proposal for the various sortases of Gram-positive bacteria. Research in Microbiology, 156(3), 289–297. https://doi.org/10.1016/j.resmic.2004.10.011
  • Hall, J. W., Lima, B. P., Herbomel, G. G., Gopinath, T., McDonald, L., Shyne, M. T., Lee, J. K., Kreth, J., Ross, K. F., Veglia, G., & Herzberg, M. C. (2019). An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins. Science Signaling, 12(580):eaas9941. https://doi.org/10.1126/scisignal.aas9941
  • He, W., Zhang, Y., Bao, J., Deng, X., Batara, J., Casey, S., Guo, Q., Jiang, F., & Fu, L. (2017). Synthesis, biological evaluation and molecular docking analysis of 2-phenyl-benzofuran-3-carboxamide derivatives as potential inhibitors of Staphylococcus aureus Sortase A. Bioorganic & Medicinal Chemistry, 25(4), 1341–1351. https://doi.org/10.1016/j.bmc.2016.12.030
  • Hess, B., Kutzner, C., Van Der Spoel, D., & Lindahl, E. (2008). GRGMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. https://doi.org/10.1021/ct700301q
  • Jacobitz, A. W., Kattke, M. D., Wereszczynski, J., & Clubb, R. T. (2017). Sortase transpeptidases: Structural biology and catalytic mechanism. Advances in Protein Chemistry and Structural Biology, 109, 223–264. https://doi.org/10.1016/bs.apcsb.2017.04.008
  • Jaudzems, K., Kurbatska, V., Je Kabsons, A., Bobrovs, R., Rudevica, Z., & Leonchiks, A. (2020). Targeting bacterial sortase A with covalent inhibitors: 27 new starting points for structure-based hit-to-lead optimization. ACS Infectious Diseases, 6(2), 186–194. https://doi.org/10.2210/pdb6R1V/pdb
  • Kappel, K., Wereszczynski, J., Clubb, R. T., & McCammon, J. A. (2012). The binding mechanism, multiple binding modes, and allosteric regulation of Staphylococcus aureus sortase A probed by molecular dynamics simulations. Protein Science, 21(12), 1858–1871. https://doi.org/10.1002/pro.2168
  • Kumari, R., Kumar, R., Open Source Drug Discovery Consortium, & Lynn, A. (2014). g_mmpbsa—A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
  • Kwiecinski, J. M., & Horswill, A. R. (2020). Staphylococcus aureus bloodstream infections: Pathogenesis and regulatory mechanisms. Current Opinion in Microbiology, 53, 51–60. https://doi.org/10.1016/j.mib.2020.02.005
  • Lee, C. R., Cho, I. H., Jeong, B. C., & Lee, S. H. (2013). Strategies to minimize antibiotic resistance. International Journal of Environmental Research and Public Health, 10(9), 4274–4305. https://doi.org/10.3390/ijerph10094274
  • Lee, G. (2013). Ciprofloxacin resistance in Enterococcus faecalis strains isolated from male patients with complicated urinary tract infection. Korean Journal of Urology, 54(6), 388–393. https://doi.org/10.4111/kju.2013.54.6.388
  • Leuthner, K. D., Yuen, A., Mao, Y., & Rahbar, A. (2015). Dalbavancin (BI-387) for the treatment of complicated skin and skin structure infection. Expert Review of anti-Infective Therapy, 13(2), 149–159. https://doi.org/10.1586/14787210.2015.995633
  • Marraffini, L. A., DeDent, A. C., & Schneewind, O. (2006). Sortases and the Art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiology and Molecular Biology Reviews, 70(1), 192–221. https://doi.org/10.1128/MMBR.70.1.192-221.2006
  • Matthews, M. (2015). The high cost of inventing new drugs—And of not inventing them.
  • Mazmanian, S. K., Liu, G., Jensen, E. R., Lenoy, E., & Schneewind, O. (2000). Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proceedings of the National Academy of Sciences of the United States of America, 97(10), 5510–5515. https://doi.org/10.1073/pnas.080520697
  • Nitulescu, G., Nicorescu, I., Olaru, O., Ungurianu, A., Mihai, D., Zanfirescu, A., Nitulescu, G., & Margina, D. (2017). Molecular docking and screening studies of new natural sortase A inhibitors. International Journal of Molecular Sciences, 18(10), 2217. https://doi.org/10.3390/ijms18102217
  • Ong, K. C., & Khoo, H. E. (1997). Biological effects of myricetin. General Pharmacology, 29(2), 121–126. https://doi.org/10.1016/S0306-3623(96)00421-1
  • Parrino, B., Diana, P., Cirrincione, G., & Cascioferro, S. (2018). Bacterial biofilm inhibition in the development of effective anti-virulence strategy. Open Medicinal Chemistry Journal, 12, 84–87. https://doi.org/10.2174/1874104501812010084
  • Pasetto, S., Pardi, V., & Murata, R. M. (2014). Anti-HIV-1 activity of flavonoid myricetin on HIV-1 infection in a dual-chamber in vitro model. PLOS One, 9(12), e115323. https://doi.org/10.1371/journal.pone.0115323
  • Paterson, G. K., & Mitchell, T. J. (2004). The biology of gram-positive sortase enzymes. Trends in Microbiology, 12(2), 89–95. https://doi.org/10.1016/j.tim.2003.12.007
  • Phillips, P. A., Sangwan, V., Borja-Cacho, D., Dudeja, V., Vickers, S. M., & Saluja, A. K. (2011). Myricetin induces pancreatic cancer cell death via the induction of apoptosis and inhibition of the phosphatidylinositol 3-kinase (PI3K) signaling pathway. Cancer Letters, 308(2), 181–188. https://doi.org/10.1016/j.canlet.2011.05.002
  • Rajendran, V., Gopalakrishnan, C., & Sethumadhavan, R. (2018). Pathological role of a point mutation (T315I) in BCR-ABL1 protein - A computational insight. Journal of Cellular Biochemistry, 119(1), 918–925. https://doi.org/10.1002/jcb.26257
  • Ramírez, D., & Caballero, J. (2018). Is it reliable to take the molecular docking top scoring position as the best solution without considering available structural data? Molecules, 23(5), 1038. https://doi.org/10.3390/molecules23051038
  • Rasko, D. A., & Sperandio, V. (2010). Anti-virulence strategies to combat bacteria-mediated disease. Nature Reviews. Drug Discovery, 9(2), 117–128. https://doi.org/10.1038/nrd3013
  • Sapra, R., Rajora, A. K., Kumar, P., Maurya, G. P., Pant, N., & Haridas, V. (2021). Chemical biology of sortase A inhibition: A gateway to anti-infective therapeutic agents. Journal of Medicinal Chemistry, 64(18), 13097–13130. https://doi.org/10.1021/acs.jmedchem.1c00386
  • Sato, M., Murakami, K., Uno, M., Nakagawa, Y., Katayama, S., Akagi, K.-i., Masuda, Y., Takegoshi, K., & Irie, K. (2013). Site-specific inhibitory mechanism for amyloid β42 aggregation by catechol-type flavonoids targeting the lys residues. The Journal of Biological Chemistry, 288(32), 23212–23224. https://doi.org/10.1074/jbc.M113.464222
  • Schüttelkopf, A. W., & Van Aalten, D. M. F. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica, Section D, Biological Crystallography, 60(Pt 8), 1355–1363. https://doi.org/10.1107/S0907444904011679
  • Semwal, D. K., Semwal, R. B., Combrinck, S., & Viljoen, A. (2016). Myricetin: A dietary molecule with diverse biological activities. Nutrients, 8(2), 90. https://doi.org/10.3390/nu8020090
  • Shakour, N., Hadizadeh, F., Kesharwani, P., & Sahebkar, A. (2021). 3D-QSAR studies of 1,2,4-oxadiazole derivatives as sortase A inhibitors. BioMed Research International, 2021, 6380336. https://doi.org/10.1155/2021/6380336
  • Shorr, A. F., Lodise, T. P., Corey, G. R., De Anda, C., Fang, E., Das, A. F., & Prokocimer, P. (2015). Analysis of the phase 3 ESTABLISH trials of tedizolid versus linezolid in acute bacterial skin and skin structure infections. Antimicrobial Agents and Chemotherapy, 59(2), 864–871. https://doi.org/10.1128/AAC.03688-14
  • Si, L., Li, P., Liu, X., & Luo, L. (2016). Chinese herb medicine against Sortase A catalyzed transformations, a key role in gram-positive bacterial infection progress. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(sup1), 184–196. https://doi.org/10.1080/14756366.2016.1178639
  • Singh, R., Bhardwaj, V., & Purohit, R. (2021). Identification of a novel binding mechanism of Quinoline based molecules with lactate dehydrogenase of Plasmodium falciparum. Journal of Biomolecular Structure and Dynamics, 39(1), 348–356. https://doi.org/10.1080/07391102.2020.1711809
  • Tam, K., & Torres, V. J. (2019). Staphylococcus aureus secreted toxins and extracellular enzymes. Microbiology Spectrum, 7(2), 2–7. https://doi.org/10.1128/microbiolspec.GPP3-0039-2018
  • Uba, A. I., & Yelekçi, K. (2018). Carboxylic acid derivatives display potential selectivity for human histone deacetylase 6: Structure-based virtual screening, molecular docking and dynamics simulation studies. Computational Biology and Chemistry, 75, 131–142. https://doi.org/10.1016/j.compbiolchem.2018.05.004
  • Veve, M. P., & Wagner, J. L. (2018). Lefamulin: Review of a promising novel pleuromutilin antibiotic. Pharmacotherapy, 38(9), 935–946. https://doi.org/10.1002/phar.2166
  • Villano, S., Steenbergen, J., & Loh, E. (2016). Omadacycline: Development of a novel aminomethylcycline antibiotic for treating drug-resistant bacterial infections. Future Microbiology, 11(11), 1421–1434. https://doi.org/10.2217/fmb-2016-0100
  • Wang, S.-J., Tong, Y., Lu, S., Yang, R., Liao, X., Xu, Y.-F., & Li, X. (2010). Anti-inflammatory activity of myricetin isolated from Myrica rubra Sieb. et Zucc. leaves. Planta Medica, 76(14), 1492–1496. https://doi.org/10.1055/s-0030-1249780
  • Weako, J., Uba, A. I., Keskin, Ö., Gürsoy, A., & Yelekçi, K. (2020). Identification of potential inhibitors of human methionine aminopeptidase (type II) for cancer therapy: Structure-based virtual screening, ADMET prediction and molecular dynamics studies. Computational Biology and Chemistry, 86(February), 107244. https://doi.org/10.1016/j.compbiolchem.2020.107244
  • Xu, H. X., & Lee, S. F. (2001). Activity of plant flavonoids against antibiotic-resistant bacteria. Phytotherapy Research, 15(1), 39–43. https://doi.org/10.1002/1099-1573(200102)15:1<39::AID-PTR684>3.0.CO;2-R
  • Xu, H., Ziegelin, G., Schröder, W., Frank, J., Ayora, S., Alonso, J. C., Lanka, E., & Saenger, W. (2001). Flavones inhibit the hexameric replicative helicase RepA. Nucleic Acids Research, 29(24), 5058–5066. https://doi.org/10.1093/nar/29.24.5058
  • Yamaguchi, M., Terao, Y., Ogawa, T., Takahashi, T., Hamada, S., & Kawabata, S. (2006). Role of Streptococcus sanguinis sortase A in bacterial colonization. Microbes and Infection, 8(12–13), 2791–2796. https://doi.org/10.1016/j.micinf.2006.08.010

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.