Identification and prioritization of promising lead molecules from Syzygium aromaticum against Sortase C from Streptococcus pyogenes: an in silico investigation

References

• Adasme, M. F., Linnemann, K. L., Bolz, S. N., Kaiser, F., Salentin, S., Haupt, V. J., & Schroeder, M. (2021, July 2). PLIP 2021: Expanding the scope of the protein-ligand interaction profiler to DNA and RNA. Nucleic Acids Research, 49(W1), W530–W534. https://doi.org/10.1093/nar/gkab294
   PubMed Web of Science ®Google Scholar
• Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389
   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, January 1). 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
• Bowie, J. U., Lüthy, R., & Eisenberg, D. (1991, July 12). A method to identify protein sequences that fold into a known three-dimensional structure. Science (New York, N.Y.), 253(5016), 164–170. https://doi.org/10.1126/science.1853201
   PubMed Web of Science ®Google Scholar
• Bradshaw, W. J., Davies, A. H., Chambers, C. J., Roberts, A. K., Shone, C. C., & Acharya, K. R. (2015, June). Molecular features of the sortase enzyme family. The FEBS Journal, 282(11), 2097–2114. https://doi.org/10.1111/febs.13288
   PubMed Web of Science ®Google Scholar
• Caliot, É., Dramsi, S., Chapot-Chartier, M. P., Courtin, P., Kulakauskas, S., Péchoux, C., Trieu-Cuot, P., & Mistou, M. Y. (2012). Role of the Group B antigen of Streptococcus agalactiae: A peptidoglycan-anchored polysaccharide involved in cell wall biogenesis. PLoS Pathogens, 8(6), e1002756. https://doi.org/10.1371/journal.ppat.1002756
   PubMed Web of Science ®Google Scholar
• Camara, M., Dieng, A., & Boye, C. S. (2013, October 29). Antibiotic susceptibility of streptococcus pyogenes isolated from respiratory tract infections in Dakar, Senegal. Microbiology Insights, 6, 71–75. https://doi.org/10.4137/MBI.S12996
   PubMedGoogle Scholar
• Chan, A. H., Yi, S. W., Weiner, E. M., Amer, B. R., Sue, C. K., Wereszczynski, J., Dillen, C. A., Senese, S., Torres, J. Z., McCammon, J. A., Miller, L. S., Jung, M. E., & Clubb, R. T. (2017, September). NMR structure-based optimization of Staphylococcus aureus sortase A pyridazinone inhibitors. Chemical Biology & Drug Design, 90(3), 327–344. https://doi.org/10.1111/cbdd.12962
   PubMed Web of Science ®Google Scholar
• Chenna, B. C., Shinkre, B. A., King, J. R., Lucius, A. L., Narayana, S. V., & Velu, S. E. (2008, January 1). Identification of novel inhibitors of bacterial surface enzyme Staphylococcus aureus Sortase A. Bioorganic & Medicinal Chemistry Letters, 18(1), 380–385. https://doi.org/10.1016/j.bmcl.2007.10.051
   PubMed Web of Science ®Google Scholar
• Colovos, C., & Yeates, T. O. (1993, September). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science : A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
   PubMed Web of Science ®Google Scholar
• Condò, C., Anacarso, I., Sabia, C., Iseppi, R., Anfelli, I., Forti, L., de Niederhäusern, S., Bondi, M., & Messi, P. (2020, February). Antimicrobial activity of spices essential oils and its effectiveness on mature biofilms of human pathogens. Natural Product Research, 34(4), 567–574. https://doi.org/10.1080/14786419.2018.1490904
   PubMed Web of Science ®Google Scholar
• Cunningham, M. W. (2008). Pathogenesis of group A streptococcal infections and their sequelae. Advances in Experimental Medicine and Biology, 609, 29–42. https://doi.org/10.1007/978-0-387-73960-1_3
   PubMed Web of Science ®Google Scholar
• Das, S., Kumar, H. S. V., Pal, S. K., Srivastava, V. K., Jyoti, A., Kumar, S., & Kaushik, S. (2020). Prospecting potential inhibitors of sortase A from Enterococcus faecalis: A multidrug resistant bacteria, through in-silico and in-vitro approaches. Protein and Peptide Letters, 27(7), 582–592. https://doi.org/10.2174/0929866527666191227143048
   PubMed Web of Science ®Google Scholar
• Das, S., Srivastava, V. K., Parray, Z. A., Jyoti, A., Islam, A., & Kaushik, S. (2018, December). Identification of potential inhibitors of sortase A: Binding studies, in-silico docking and protein-protein interaction studies of sortase A from Enterococcus faecalis. International Journal of Biological Macromolecules, 120(Pt B), 1906–1916. https://doi.org/10.1016/j.ijbiomac.2018.09.174
   PubMedGoogle Scholar
• DeLano, W. (2002). The PyMOL molecular graphics system. DeLano Scientific.
   Google Scholar
• Deléage, G. (2017, December 15). ALIGNSEC: Viewing protein secondary structure predictions within large multiple sequence alignments. Bioinformatics (Oxford, England), 33(24), 3991–3992. https://doi.org/10.1093/bioinformatics/btx521
   PubMed Web of Science ®Google Scholar
• Delfani, S., Mohammadrezaei Khorramabadi, R., Abbaszadeh, S., Naghdi, N., & Shahsavari, S. (2017). Phytotherapy for Streptococcus pyogenes. Journal of Pharmaceutical Sciences and Research, 9, 513–526.
   Google Scholar
• Donahue, E. H., Dawson, L. F., Valiente, E., Firth-Clark, S., Major, M. R., Littler, E., Perrior, T. R., & Wren, B. W. (2014, August 31). Clostridium difficile has a single sortase, SrtB, that can be inhibited by small-molecule inhibitors. BMC Microbiology, 14, 219. https://doi.org/10.1186/s12866-014-0219-1
   PubMed Web of Science ®Google Scholar
• Dramsi, S., Trieu-Cuot, P., & Bierne, H. (2005, April). 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
   PubMed Web of Science ®Google Scholar
• El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., Qureshi, M., Richardson, L. J., Salazar, G. A., Smart, A., Sonnhammer, E. L. L., Hirsh, L., Paladin, L., Piovesan, D., Tosatto, S. C. E., & Finn, R. D. (2019, January 8). The Pfam protein families database in 2019. Nucleic Acids Research, 47(D1), D427–D432. https://doi.org/10.1093/nar/gky995
   PubMed Web of Science ®Google Scholar
• Faujdar, S. S., Bisht, D., & Sharma, A. (2020, January 28). Antibacterial activity of Syzygium aromaticum (clove) against uropathogens producing ESBL, MBL, and AmpC beta-lactamase: Are we close to getting a new antibacterial agent? Journal of Family Medicine and Primary Care, 9(1), 180–186. https://doi.org/10.4103/jfmpc.jfmpc_908_19
   PubMedGoogle Scholar
• Forli, S., Huey, R., Pique, M. E., Sanner, M. F., Goodsell, D. S., & Olson, A. J. (2016, May). Computational protein-ligand docking and virtual drug screening with the AutoDock suite. Nature Protocols, 11(5), 905–919. https://doi.org/10.1038/nprot.2016.051
   PubMed Web of Science ®Google Scholar
• Gao, C., Uzelac, I., Gottfries, J., & Eriksson, L. A. (2016, February 5). Exploration of multiple Sortase A protein conformations in virtual screening. Scientific Reports, 6, 20413. https://doi.org/10.1038/srep20413
   PubMed Web of Science ®Google Scholar
• Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In J. M. Walker (Ed.), The proteomics protocols handbook (pp. 571–607). Humana Press.
   Google Scholar
• Gupta, A., Deshpande, A., Amburi, J. K., Sabarinathan, R., Senthilkumar, R., & Sekar, K. (2009). CSSP (Consensus Secondary Structure Prediction): A web-based server for structural biologists. Journal of Applied Crystallography, 42(2), 336–338. https://doi.org/10.1107/S0021889808043847
   Google Scholar
• He, W., Zhang, Y., Bao, J., Deng, X., Batara, J., Casey, S., Guo, Q., Jiang, F., & Fu, L. (2017, February 15). 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
   PubMed Web of Science ®Google Scholar
• Helal, Z. M., Rizk, D. E., Adel El-Sokkary, M. M., & Hassan, R. (2020). Prevalence and characterization of Streptococcus pyogenes clinical isolates from different hospitals and clinics in mansoura. International Journal of Microbiology, 2020, 1–11. https://doi.org/10.1155/2020/5814945
   Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983, December). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Kanwal, S., & Vaitla, P. (2021, January). Streptococcus Pyogenes. In StatPearls [Internet]. StatPearls Publishing.
   Google Scholar
• Kappel, K., Wereszczynski, J., Clubb, R. T., & McCammon, J. A. (2012, December). The binding mechanism, multiple binding modes, and allosteric regulation of Staphylococcus aureus Sortase A probed by molecular dynamics simulations. Protein Science : A Publication of the Protein Society, 21(12), 1858–1871. https://doi.org/10.1002/pro.2168
   PubMed Web of Science ®Google Scholar
• Ko, J., Park, H., Heo, L., & Seok, C. (2012, July). GalaxyWEB server for protein structure prediction and refinement. Nucleic Acids Research, 40(W1), W294–W297. https://doi.org/10.1093/nar/gks493
   PubMed Web of Science ®Google Scholar
• Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., Tyka, M., Baker, D., & Karplus, K. (2009). Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins, 77(Suppl 9), 114–122. https://doi.org/10.1002/prot.22570
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A. (2014, July 28). 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
• Land, H., & Humble, M. S. (2018). YASARA: A tool to obtain structural guidance in biocatalytic investigations. Methods in Molecular Biology (Clifton, N.J.), 1685, 43–67. https://doi.org/10.1007/978-1-4939-7366-8_4
   PubMedGoogle Scholar
• Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., & Thornton, J. M. (1996, December). AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. Journal of Biomolecular NMR, 8(4), 477–486. https://doi.org/10.1007/BF00228148
   PubMed Web of Science ®Google Scholar
• Letunic, I., Khedkar, S., & Bork, P. (2021, January 8). SMART: Recent updates, new developments and status in 2020. Nucleic Acids Research, 49(D1), D458–D460. https://doi.org/10.1093/nar/gkaa937
   PubMed Web of Science ®Google Scholar
• Luo, H., Liang, D. F., Bao, M. Y., Sun, R., Li, Y. Y., Li, J. Z., Wang, X., Lu, K. M., & Bao, J. K. (2017, March). In silico identification of potential inhibitors targeting Streptococcus mutans sortase A. International Journal of Oral Science, 9(1), 53–62. https://doi.org/10.1038/ijos.2016.58
   PubMed Web of Science ®Google Scholar
• Marraffini, L. A., Dedent, A. C., & Schneewind, O. (2006, March). Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiology and Molecular Biology Reviews : MMBR, 70(1), 192–221. https://doi.org/10.1128/MMBR.70.1.192-221.2006
   PubMed Web of Science ®Google Scholar
• Mbaveng, A. T. (2017). Medicinal spices and vegetables from Africa ǁ Syzygium aromaticum (pp. 611–625). Academic Press. https://doi.org/10.1016/B978-0-12-809286-6.00029-7
   Google Scholar
• Mohanraj, K., Karthikeyan, B. S., Vivek-Ananth, R. P., Chand, R. P. B., Aparna, S. R., Mangalapandi, P., & Samal, A. (2018, March 12). IMPPAT: A curated database of Indian medicinal plants, phytochemistry and therapeutics. Scientific Reports, 8(1), 4329. https://doi.org/10.1038/s41598-018-22631-z PMID: 29531263; PMCID: PMC5847565.
   PubMed Web of Science ®Google Scholar
• Neiers, F., Madhurantakam, C., Fälker, S., Manzano, C., Dessen, A., Normark, S., Henriques-Normark, B., & Achour, A. (2009, October 30). Two crystal structures of pneumococcal pilus sortase C provide novel insights into catalysis and substrate specificity. Journal of Molecular Biology, 393(3), 704–716. https://doi.org/10.1016/j.jmb.2009.08.058
   PubMed Web of Science ®Google Scholar
• Nitulescu, G., Nicorescu, I. M., Olaru, O. T., Ungurianu, A., Mihai, D. P., Zanfirescu, A., Nitulescu, G. M., & Margina, D. (2017, October 23). 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
   PubMed Web of Science ®Google Scholar
• Oniga, S., Araniciu, C., Palage, M., Popa, M., Chifiriuc, M.-C., Marc, G., Pirnau, A., Stoica, C., Lagoudis, I., Dragoumis, T., & Oniga, O. (2017, October 27). New 2-phenylthiazoles as potential Sortase A inhibitors: Synthesis, biological evaluation and molecular docking. Molecules, 22(11), 1827. https://doi.org/10.3390/molecules22111827
   PubMed Web of Science ®Google Scholar
• Rashidieh, B., Madani, Z., Azam, M. K., Maklavani, S. K., Akbari, N. R., Tavakoli, S., & Rigi, G. (2015, November 30). Molecular docking based virtual screening of compounds for inhibiting sortase A in L.monocytogenes. Bioinformation, 11(11), 501–505. https://doi.org/10.6026/97320630011501
   PubMedGoogle Scholar
• Saha, S., & Raghava, G. P. (2006). VICMpred: An SVM-based method for the prediction of functional proteins of gram-negative bacteria using amino acid patterns and composition. Genomics, Proteomics & Bioinformatics, 4(1), 42–47. Feb https://doi.org/10.1016/S1672-0229(06)60015-6
   PubMedGoogle Scholar
• Schüttelkopf, A. W., & van Aalten, D. M. (2004, August). 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
• Shrivastava, K., Sahu, S., Mishra, S., & De, K. (2014). In vitro antimicrobial activity and phytochemical screening of Syzygium aromaticum. Asian Journal of Research in Pharmaceutical Science, 4(1), 12–15.
   Google Scholar
• Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539. Oct 11https://doi.org/10.1038/msb.2011.75
   PubMed Web of Science ®Google Scholar
• Spellerberg, B., & Brandt, C. (2016, February 10). Laboratory diagnosis of Streptococcus pyogenes (group A streptococci). In J. J. Ferretti, D. L. Stevens, & V. A. Fischetti (Eds.), Streptococcus pyogenes: Basic biology to clinical manifestations [Internet]. University of Oklahoma Health Sciences Center.
   Google Scholar
• Thappeta, K. R. V., Zhao, L. N., Nge, C. E., Crasta, S., Leong, C. Y., Ng, V., Kanagasundaram, Y., Fan, H., & Ng, S. B. (2020, November 14). In-silico identified new natural Sortase A inhibitors disrupt S. aureus biofilm formation. International Journal of Molecular Sciences, 21(22), 8601. https://doi.org/10.3390/ijms21228601
   PubMed Web of Science ®Google Scholar
• Tian, W., Chen, C., Lei, X., Zhao, J., & Liang, J. (2018, July 2). CASTp 3.0: Computed atlas of surface topography of proteins. Nucleic Acids Research, 46(W1), W363–W367. https://doi.org/10.1093/nar/gky473
   PubMed Web of Science ®Google Scholar
• Trott, O., & Olson, A. J. (2010, January 30). 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
• Tsirigos, K. D., Peters, C., Shu, N., Käll, L., & Elofsson, A. (2015, July 1). The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Research, 43(W1), W401–7. https://doi.org/10.1093/nar/gkv485
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005, December). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Volynets, G., Vyshniakova, H., Nitulescu, G., Nitulescu, G. M., Ungurianu, A., Margina, D., Moshynets, O., Bdzhola, V., Koleiev, I., Iungin, O., Tarnavskiy, S., & Yarmoluk, S. (2021, November 24). Identification of novel antistaphylococcal hit compounds targeting Sortase A. Molecules, 26(23), 7095. https://doi.org/10.3390/molecules26237095
   PubMed Web of Science ®Google Scholar
• Walker, M. J., Barnett, T. C., McArthur, J. D., Cole, J. N., Gillen, C. M., Henningham, A., Sriprakash, K. S., Sanderson-Smith, M. L., & Nizet, V. (2014). Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clinical Microbiology Reviews, 27(2), 264–301. Aprhttps://doi.org/10.1128/CMR.00101-13
   PubMed Web of Science ®Google Scholar
• Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018, July 2). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427
   PubMed Web of Science ®Google Scholar
• Yu, N. Y., Wagner, J. R., Laird, M. R., Melli, G., Rey, S., Lo, R., Dao, P., Sahinalp, S. C., Ester, M., Foster, L. J., & Brinkman, F. S. (2010, July 1). PSORTb 3.0: Improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics (Oxford, England), 26(13), 1608–1615. https://doi.org/10.1093/bioinformatics/btq249 Epub 2010 May 13.
   PubMed Web of Science ®Google Scholar