In silico and structural investigation of sulfonamides targeting VraSR two component system in methicillin-resistant Staphylococcus aureus

References

• Altoparlak, U., Kadanali, A., & Celebi, S. (2004). Slime factor positivity in coagulase negative staphylococci isolated from nasal samples of hemodialysis patients. International Journal of Clinical Practice, 58(12), 1112–1114. https://doi.org/10.1111/j.1742-1241.2004.00211.x
   PubMed Web of Science ®Google Scholar
• Amadei, A., Linssen, A. B., & Berendsen, H. J. (1993). Essential dynamics of proteins. Proteins, 17(4), 412–425. https://doi.org/10.1002/prot.340170408
   PubMed Web of Science ®Google Scholar
• Basu, P. (2010). Gasification theory and modeling of gasifiers. Biomass Gasification Design Handbook. 117–165. (Academic Press.).
   Google Scholar
• Belcheva, A., & Golemi-Kotra, D. (2008). A close-up view of the VraSR two-component system: A mediator of Staphylococcus aureus response to cell wall damage. The Journal of Biological Chemistry, 283(18), 12354–12364. https://doi.org/10.1074/jbc.M710010200
   PubMed Web of Science ®Google Scholar
• Belcheva, A., Verma, V., & Golemi-Kotra, D. (2009). DNA-binding activity of the vancomycin resistance associated regulator protein VraR and the role of phosphorylation in transcriptional regulation of the vraSR operon. Biochemistry, 48(24), 5592–5601. https://doi.org/10.1021/bi900478b
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, IN., & Bourne, P. E. (2000). The Protein Data Bank. Nucleic Acids Research, 28(1), 235–242. https://doi.org/10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Boucher, H. W., & Corey, G. R. (2008). Epidemiology of methicillin-resistant Staphylococcus aureus. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 46 Suppl 5(S5), S344–S349. https://doi.org/10.1086/533590
   PubMedGoogle Scholar
• Boucher, H. W., Talbot, G. H., Bradley, J. S., Edwards, J. E., Gilbert, D., Rice, L. B., Scheld, M., Spellberg, B., & Bartlett, J. (2009). Bad bugs, no drugs: No ESKAPE! An update from the Infectious Diseases Society of America. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 48(1), 1–12. https://doi.org/10.1086/595011
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Da Re, S., Schumacher, J., Rousseau, P., Fourment, J., Ebel, C., & Kahn, D. (1999). Phosphorylation‐induced dimerization of the FixJ receiver domain. Molecular Microbiology, 34(3), 504–511. https://doi.org/10.1046/j.1365-2958.1999.01614.x
   PubMed Web of Science ®Google Scholar
• Dai, Y., Chang, W., Zhao, C., Peng, J., Xu, L., Lu, H., Zhou, S., & Ma, X. (2017). VraR binding to the promoter region of AGR inhibits its function in vancomycin-intermediate Staphylococcus aureus (VISA) and heterogeneous VISA. Antimicrobial Agents and Chemotherapy, 61(5), 10–1128. https://doi.org/10.1128/aac.02740-16
   Web of Science ®Google Scholar
• Davies, J. (2007). Microbes have the last word: A drastic re‐evaluation of antimicrobial treatment is needed to overcome the threat of antibiotic‐resistant bacteria. EMBO Reports, 8(7), 616–621. https://doi.org/10.1038/sj.embor.7401022
   PubMedGoogle Scholar
• Diekema, D. J., Pfaller, M. A., Schmitz, F. J., Smayevsky, J., Bell, J., Jones, R. N., … & Beach, M, SENTRY Participants Group. (2001). Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 32(s2), S114–S132. https://doi.org/10.1086/320184
   PubMedGoogle Scholar
• Domínguez, J. N., León, C., Rodrigues, J., Gamboa de Domínguez, N., Gut, J., & Rosenthal, P. J. (2005). Synthesis and antimalarial activity of sulfonamide chalcone derivatives. Farmaco (Societa Chimica Italiana: 1989), 60(4), 307–311. https://doi.org/10.1016/j.farmac.2005.01.005
   PubMedGoogle Scholar
• Emori, T. G., & Gaynes, R. P. (1993). An overview of nosocomial infections, including the role of the microbiology laboratory. Clinical Microbiology Reviews, 6(4), 428–442. https://doi.org/10.1128/cmr.6.4.428
   PubMed Web of Science ®Google Scholar
• Galperin, M. Y. (2010). Diversity of structure and function of response regulator output domains. Current Opinion in Microbiology, 13(2), 150–159. https://doi.org/10.1016/j.mib.2010.01.005
   PubMed Web of Science ®Google Scholar
• Gardete, S., Wu, S. W., Gill, S., & Tomasz, A. (2006). Role of VraSR in antibiotic resistance and antibiotic-induced stress response in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 50(10), 3424–3434. https://doi.org/10.1128/aac.00356-06
   PubMed Web of Science ®Google Scholar
• Hanaki, H., Kuwahara-Arai, K., Boyle-Vavra, S., Daum, R. S., Labischinski, H., & Hiramatsu, K. (1998). Activated cell-wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. The Journal of Antimicrobial Chemotherapy, 42(2), 199–209. https://doi.org/10.1093/jac/42.2.199
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12%3C1463::AID-JCC4%3E3.0.CO;2-H
   Web of Science ®Google Scholar
• Hiramatsu, K. (2001). Vancomycin-resistant Staphylococcus aureus: A new model of antibiotic resistance. The Lancet. Infectious Diseases, 1(3), 147–155. https://doi.org/10.1016/S1473-3099(01)00091-3
   PubMedGoogle Scholar
• Hoang, T. X., Trovato, A., Seno, F., Banavar, J. R., & Maritan, A. (2004). Geometry and symmetry presculpt the free-energy landscape of proteins. Proceedings of the National Academy of Sciences of the United States of America, 101(21), 7960–7964. https://doi.org/10.1073/pnas.0402525101
   PubMed Web of Science ®Google Scholar
• Jencks, W. P. (1981). On the attribution and additivity of binding energies. Proceedings of the National Academy of Sciences of the United States of America, 78(7), 4046–4050. https://doi.org/10.1073/pnas.78.7.4046
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Maxwell, D. S., & Tirado-Rives, J. (1996). Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society, 118(45), 11225–11236. https://doi.org/10.1021/ja9621760
   Web of Science ®Google Scholar
• Joshi, S., & Khosla, N. (2003). Nov 3 QSAR study on antibacterial activity of sulphonamides and derived Mannich bases. Bioorganic & Medicinal Chemistry Letters, 13(21), 3747–3751. https://doi.org/10.1016/j.bmcl.2003.08.017
   PubMed Web of Science ®Google Scholar
• Klein, E., Smith, D. L., & Laxminarayan, R. (2007). Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999–2005. Emerging Infectious Diseases, 13(12), 1840–1846. https://doi.org/10.3201/eid1312.070629
   PubMed Web of Science ®Google Scholar
• Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., Harrison, L. H., Lynfield, R., Dumyati, G., Townes, J. M., Craig, A. S., Zell, E. R., Fosheim, G. E., McDougal, L. K., Carey, R. B., … & Fridkin, S. K, Active Bacterial Core surveillance (ABCs) MRSA Investigators. (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA, 298(15), 1763–1771. https://doi.org/10.1001/jama.298.15.1763
   PubMed Web of Science ®Google Scholar
• Krissinel, E. (2010). Crystal contacts as nature’s docking solutions. Journal of Computational Chemistry, 31(1), 133–143. https://doi.org/10.1002/jcc.21303
   PubMed Web of Science ®Google Scholar
• Kumar, J. V., Tseng, T.-S., Lou, Y.-C., Wei, S.-Y., Wu, T.-H., Tang, H.-C., Chiu, Y.-C., Hsu, C.-H., & Chen, C. (2022). Structural insights into DNA binding domain of vancomycin‐resistance‐associated response regulator in complex with its promoter DNA from Staphylococcus aureus. Protein Science: A Publication of the Protein Society, 31(5), e4286. https://doi.org/10.1002/pro.4286
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A, Open Source Drug Discovery Consortium. (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
   PubMed Web of Science ®Google Scholar
• Kuroda, M., Kuroda, H., Oshima, T., Takeuchi, F., Mori, H., & Hiramatsu, K. (2003). Two‐component system VraSR positively modulates the regulation of cell‐wall biosynthesis pathway in Staphylococcus aureus. Molecular Microbiology, 49(3), 807–821. https://doi.org/10.1046/j.1365-2958.2003.03599.x
   PubMed Web of Science ®Google Scholar
• Kuroda, M., Kuwahara-Arai, K., & Hiramatsu, K. (2000). Identification of the up-and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochemical and Biophysical Research Communications, 269(2), 485–490. https://doi.org/10.1006/bbrc.2000.2277
   PubMed Web of Science ®Google Scholar
• Li, B., & Webster, T. J. (2018). Bacteria antibiotic resistance: New challenges and opportunities for implant‐associated orthopedic infections. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society, 36(1), 22–32. https://doi.org/10.1002/jor.23656
   PubMed Web of Science ®Google Scholar
• LigPrep Schrödinger, LLC, New York, NY, USA. Available online: https://www.schrodinger.com/products/ligprep (accessed on 10 November 2022).
   Google Scholar
• Liu, C., Sun, D., Zhu, J., & Liu, W. (2018). Two-component signal transduction systems: A major strategy for connecting input stimuli to biofilm formation. Frontiers in Microbiology, 9, 3279. https://doi.org/10.3389/fmicb.2018.03279
   PubMed Web of Science ®Google Scholar
• MacroModel Schrödinger, LLC, New York, NY, USA. Available online: https://www.schrodinger.com/products/macromodel (accessed on 10 November 2022).
   Google Scholar
• McCallum, N., Meier, P. S., Heusser, R., & Berger-Bächi, B. (2011). Mutational analyses of open reading frames within the vraSR operon and their roles in the cell wall stress response of Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 55(4), 1391–1402. https://doi.org/10.1128/aac.01213-10
   PubMed Web of Science ®Google Scholar
• Mengelers, M. J., Hougee, P. E., Janssen, L. H., & Van Miert, A. S. (1997). Structure-activity relationship between antibacterial activities and physicochemical properties of sulfonamides. Journal of Veterinary Pharmacology and Therapeutics, 20(4), 276–283. https://doi.org/10.1046/j.1365-2885.1997.00063.x
   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. https://doi.org/10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Oostenbrink, C., Villa, A., Mark, A. E., & Van Gunsteren, W. F. (2004). A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force‐field parameter sets 53A5 and 53A6. Journal of Computational Chemistry, 25(13), 1656–1676. https://doi.org/10.1002/jcc.20090
   PubMed Web of Science ®Google Scholar
• Ovung, A., & Bhattacharyya, J. (2021). Mar 29 Sulfonamide drugs: Structure, antibacterial property, toxicity, and biophysical interactions. Biophysical Reviews, 13(2), 259–272. https://doi.org/10.1007/s12551-021-00795-9
   PubMedGoogle Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• RCSB Protein Data Bank (RCSB.org). (2023). Delivery of experimentally-determined PDB structures alongside one million computed structure models of proteins from artificial intelligence/machine learning. Nucleic Acids Research, 51, D488–D508. https://doi.org/10.1093/nar/gkac1077
   PubMed Web of Science ®Google Scholar
• Rice, L. B. (2008). Federal funding for the study of antimicrobial resistance in nosocomial pathogens: No ESKAPE. The Journal of Infectious Diseases, 197(8), 1079–1081. https://doi.org/10.1086/533452
   PubMed Web of Science ®Google Scholar
• Schüttelkopf, A. W., & Van Aalten, D. M. (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
   PubMedGoogle Scholar
• Srivastava, S. K., Rajasree, K., Fasim, A., Arakere, G., & Gopal, B. (2014). Influence of the AgrC-AgrA complex on the response time of Staphylococcus aureus quorum sensing. Journal of Bacteriology, 196(15), 2876–2888. https://doi.org/10.1128/jb.01530-14
   PubMed Web of Science ®Google Scholar
• Stock, A. M., Robinson, V. L., & Goudreau, P. N. (2000). Two-component signal transduction. Annual Review of Biochemistry, 69(1), 183–215. https://doi.org/10.1146/annurev.biochem.69.1.183
   PubMedGoogle Scholar
• Swartz, M. N. (1997). Use of antimicrobial agents and drug resistance. The New England Journal of Medicine, 337(7), 491–492. https://doi.org/10.1056/NEJM199708143370709
   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. https://doi.org/10.1002/jcc.21334
   PubMed Web of Science ®Google Scholar
• Utaida, S., Dunman, P. M., Macapagal, D., Murphy, E., Projan, S. J., Singh, V. K., Jayaswal, R. K., & Wilkinson, B. J. (2003). Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology (Reading, England), 149(Pt 10), 2719–2732. https://doi.org/10.1099/mic.0.26426-0
   PubMedGoogle Scholar
• Vangone, A., Schaarschmidt, J., Koukos, P., Geng, C., Citro, N., Trellet, M. E., Xue, L. C., & Bonvin, A. M. J. J. (2019). Large-scale prediction of binding affinity in protein–small ligand complexes: The PRODIGY-LIG web server. Bioinformatics (Oxford, England), 35(9), 1585–1587. https://doi.org/10.1093/bioinformatics/bty816
   PubMed Web of Science ®Google Scholar
• Verma, A. K., Dubey, S., & Srivastava, S. K. (2023). Identification of alkaloid compounds as potent inhibitors of Mycobacterium tuberculosis NadD using computational strategies. Computers in Biology and Medicine, 158, 106863. May https://doi.org/10.1016/j.compbiomed.2023.106863
   PubMed Web of Science ®Google Scholar
• Verma, A. K., Jaiswal, G., Sultana, K. N., & Srivastava, S. K. (2023). Computational studies on coumestrol-ArlR interaction to target ArlRS signaling cascade involved in MRSA virulence. Journal of Biomolecular Structure & Dynamics, 1–19. https://doi.org/10.1080/07391102.2023.2220028
   Web of Science ®Google Scholar
• Weng, G., Wang, E., Wang, Z., Liu, H., Zhu, F., Li, D., & Hou, T. (2019). HawkDock: A web server to predict and analyze the protein–protein complex based on computational docking and MM/GBSA. Nucleic Acids Research, 47(W1), W322–W330. https://doi.org/10.1093/nar/gkz397
   PubMed Web of Science ®Google Scholar
• West, A. H., & Stock, A. M. (2001). Histidine kinases and response regulator proteins in two-component signaling systems. Trends in Biochemical Sciences, 26(6), 369–376. https://doi.org/10.1016/S0968-0004(01)01852-7
   PubMed Web of Science ®Google Scholar
• Zani, F., & Vicini, P. (1999). Antimicrobial activity of some 1,2-Benzisothiazoles having a Benzenesulfonamide Moiety. Archiv Der Pharmazie, 331(6), 219–223.
   Web of Science ®Google Scholar
• Zídek, L., Novotny, M. V., & Stone, M. J. (1999). Increased protein backbone conformational entropy upon hydrophobic ligand binding. Nature Structural Biology, 6(12), 1118–1121. https://doi.org/10.1038/70057
   PubMedGoogle Scholar