242
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Phenotypic and in silico studies for a series of synthetic thiosemicarbazones as New Delhi metallo-beta-lactamase carbapenemase inhibitors

, , , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 14223-14235 | Received 04 Oct 2021, Accepted 28 Oct 2021, Published online: 12 Nov 2021

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, 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
  • Barberino, M. G., Cruvinel, S., de, A., Faria, C., Salvino, M. A., & Silva, M. d. O. (2018). Isolation of blaNDM-producing Enterobacteriaceae in a public hospital in Salvador, Bahia, Brazil. The Brazilian Journal of Infectious Diseases, 22(1), 47–50. https://doi.org/10.1016/j.bjid.2017.10.002
  • Barcelos, R. P., de Lima Portella, R., Lugokenski, T. H., da Rosa, E. J. F., Amaral, G. P., Garcia, L. F. M., Bresolin, L., Carratu, V., Soares, F. A. A., & de Vargas Barbosa, N. B. (2012). Isatin-3-N4-benzilthiosemicarbazone, a non-toxic thiosemicarbazone derivative, protects and reactivates rat and human cholinesterases inhibited by methamidophos in vitro and in silico. Toxicology In Vitro, 26(6), 1030–1039. https://doi.org/10.1016/j.tiv.2012.04.008
  • Bauer, D. J. (1965). Chemoprophylaxis of smallpox and treatment of vaccinia gangrenosa with 1-methylisatin 3-thiosemicarbazone. Antimicrobial Agents and Chemotherapy, 5, 544–547. https://doi.org/10.1128/aac.5.5.544
  • Berendsen, H. J. C., Grigera, J. R., & Straatsma, T. P. (1987). The missing term in effective pair potentials. The Journal of Physical Chemistry, 91(24), 6269–6271. https://doi.org/10.1021/j100308a038
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular-dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). Gromacs - A message-passing parallel molecular-dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Brem, J., Van Berkel, S. S., Aik, W., Rydzik, A. M., Avison, M. B., Pettinati, I., Umland, K. D., Kawamura, A., Spencer, J., Claridge, T. D. W. W., McDonough, M. A., & Schofield, C. J. (2014). Rhodanine hydrolysis leads to potent thioenolate mediated metallo-β-lactamase inhibition . Nature Chemistry, 6(12), 1084–1090. https://doi.org/10.1038/nchem.2110
  • 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
  • Büttner, D., Kramer, J. S., Klingler, F. M., Wittmann, S. K., Hartmann, M. R., Kurz, C. G., Kohnhäuser, D., Weizel, L., Brüggerhoff, A., Frank, D., Steinhilber, D., Wichelhaus, T. A., Pogoryelov, D., & Proschak, E. (2018). Challenges in the development of a thiol-based broad-spectrum inhibitor for metallo-β-lactamases. ACS Infectious Diseases, 4(3), 360–372. https://doi.org/10.1021/acsinfecdis.7b00129
  • Cassiano, D. S. A., Reis, I. M. A., Estrela, I., de, O., de Freitas, H. F., Pita, S. S., da, R., David, J. M., & Branco, A. (2019). Acetylcholinesterase inhibitory activities and bioguided fractionation of the Ocotea percoriacea extracts: HPLC-DAD-MS/MS characterization and molecular modeling of their alkaloids in the active fraction. Computational Biology and Chemistry, 83, 107129. https://doi.org/10.1016/j.compbiolchem.2019.107129
  • Cecchini, M., Langer, J., & Slawomirski, L. (2015). Resistance in G7 countries and beyond: Economic issues, policies. OECD. Retrieved December 15, 2020, from https://www.oecd.org/els/health-systems/Antimicrobial-Resistance-in-G7-Countries-and-Beyond.pdf
  • Celenza, G., Vicario, M., Bellio, P., Linciano, P., Perilli, M., Oliver, A., Blazquez, J., Cendron, L., & Tondi, D. (2018). Phenylboronic acid derivatives as validated leads active in clinical strains overexpressing KPC-2: A step against bacterial resistance. ChemMedChem, 13(7), 713–724. https://doi.org/10.1002/cmdc.201700788
  • ChemAxon. (2019). Marvin Sketch (Version 6.0.1). https://chemaxon.com
  • Clark, M., Cramer, R. D., Opdenbosch, N. V., & Van Opdenbosch, N. (1989). Validation of the general purpose tripos 5.2 force field. Journal of Computational Chemistry, 10(8), 982–1012. https://doi.org/10.1002/jcc.540100804
  • CLSI. (1999). Methods for determining bactericidal activity of antimicrobial agents; approved guideline. CLSI document M26-A. Clinical and Laboratory Standards Institute.
  • CLSI. (2018). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically (11th ed., Issue i). Clinical and Laboratory Standards Institute. https://clsi.org/standards/products/microbiology/documents/m07/
  • Cunha, S., & Silva, T. L. d. (2009). One-pot and catalyst-free synthesis of thiosemicarbazones via multicomponent coupling reactions. Tetrahedron Letters, 50(18), 2090–2093. https://doi.org/10.1016/j.tetlet.2009.02.134
  • 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
  • Gasteiger, J., & Marsili, M. (1980). Iterative partial equalization of orbital electronegativity—A rapid access to atomic charges. Tetrahedron, 36(22), 3219–3228. https://doi.org/10.1016/0040-4020(80)80168-2
  • Gomes, D. E., Da Silva, A. W., Lins, R. D., Pascutti, P. G., & Soares, T. A. (2009). Hbmap2grace. Retrieved December 15, 2020, fromhttp://lmdm.biof.ufrj.br/software/hbmap2grace/index.html
  • Halat, D. H., & Moubareck, C. A. (2020). The current burden of carbapenemases: Review of significant properties and dissemination among gram-negative bacteria. In Antibiotics (Vol. 9, Issue 4). MDPI AG. https://doi.org/10.3390/antibiotics9040186
  • Heffeter, P., Pape, V. F. S., Enyedy, É. A., Keppler, B. K., Szakacs, G., & Kowol, C. R. (2019). Anticancer thiosemicarbazones: Chemical properties, interaction with iron metabolism, and resistance development. Antioxidants and Redox Signaling, 30(8), 1062–1082. https://doi.org/10.1089/ars.2017.7487
  • Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 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
  • Hutchings, M., Truman, A., & Wilkinson, B. (2019). Antibiotics: Past, present and future. In Current opinion in microbiology (Vol. 51, pp. 72–80). Elsevier Ltd. https://doi.org/10.1016/j.mib.2019.10.008
  • IACG. (2019). No time to wait: Securing the future from drug-resistant infections report to the secretary-general of the United Nations. World Health Organisation. https://www.who.int/antimicrobial-resistance/interagency-coordination-group/IACG_final_report_EN.pdf?ua=1
  • Jackson, A. C., Pinter, T. B. J., Talley, D. C., Baker-Agha, A., Patel, D., Smith, P. J., & Franz, K. J. (2021). Benzimidazole and benzoxazole zinc chelators as inhibitors of metallo-β-lactamase NDM-1. ChemMedChem, 16(4), 654–661. https://doi.org/10.1002/cmdc.202000607
  • Jonas, O. B., Irwin, A., Berthe, F. C. J., Le Gall, F. G., & Marquez, P. V. (2017). Drug-resistant infections: A threat to our economic future (Vol. 2, p. 114679). Final Report. http://documents.worldbank.org/curated/en/323311493396993758/final-report
  • Jones, G., Willett, P., Glen, R. C., Leach, A. R., & Taylor, R. (1997). Development and validation of a genetic algorithm for flexible docking. Journal of Molecular Biology, 267(3), 727–748. https://doi.org/10.1006/jmbi.1996.0897
  • Khan, A. U., Ali, A., Danishuddin, D., Srivastava, G., & Sharma, A. (2017). Potential inhibitors designed against NDM-1 type metallo-β-lactamases: An attempt to enhance efficacies of antibiotics against multi-drug-resistant bacteria. Scientific Reports, 7(1), 9207. https://doi.org/10.1038/s41598-017-09588-1
  • Khan, A. U., Maryam, L., & Zarrilli, R. (2017). Structure, genetics and worldwide spread of New Delhi metallo-β-lactamase (NDM): A threat to public health. BMC Microbiology, 17(1), 101, 1-12. https://doi.org/10.1186/s12866-017-1012-8
  • King, A. M., Reid-Yu, S. A., Wang, W., King, D. T., De Pascale, G., Strynadka, N. C., Walsh, T. R., Coombes, B. K., & Wright, G. D. (2014). Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature, 510(7506), 503–506. https://doi.org/10.1038/nature13445
  • King, D., & Strynadka, N. (2011). Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance. Protein Science, 20(9), 1484–1491. https://doi.org/10.1002/pro.697
  • Kohli, E., Arora, R., & Kakkar, R. (2014). Theoretical study of the stability of tautomers and conformers of isatin-3-thiosemicarbazone (IBT). Canadian Chemical Transactions, 2(3), 327–342.   https://doi.org/10.13179/canchemtrans.2014.02.03.0112
  • 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. https://doi.org/10.1021/ci800298z
  • Kowol, C. R., Trondl, R., Heffeter, P., Arion, V. B., Jakupec, M. A., Roller, A., Galanski, M., Berger, W., & Keppler, B. K. (2009). Impact of metal coordination on cytotoxicity of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (triapine) and novel insights into terminal dimethylation. Journal of Medicinal Chemistry, 52(16), 5032–5043. https://doi.org/10.1021/jm900528d
  • Koziara, K. B., Stroet, M., Malde, A. K., & Mark, A. E. (2014). Testing and validation of the automated topology builder (ATB) version 2.0: Prediction of hydration free enthalpies. Journal of Computer-Aided Molecular Design, 28(3), 221–233. https://doi.org/10.1007/s10822-014-9713-7
  • Kumar, S. N., Siji, J. V., Nambisan, B., & Mohandas, C. (2012). Activity and synergistic interactions of stilbenes and antibiotic combinations against bacteria in vitro. World Journal of Microbiology and Biotechnology, 28(11), 3143–3150. https://doi.org/10.1007/s11274-012-1124-0
  • Kumar, A., & Zhang, K. Y. J. (2018). A cross docking pipeline for improving pose prediction and virtual screening performance. Journal of Computer-Aided Molecular Design, 32(1), 163–173. https://doi.org/10.1007/s10822-017-0048-z
  • Li, J. Q., Sun, L. Y., Jiang, Z., Chen, C., Gao, H., Chigan, J. Z., Ding, H. H., & Yang, K. W. (2021). Diaryl-substituted thiosemicarbazone: A potent scaffold for the development of New Delhi metallo-β-lactamase-1 inhibitors. Bioorganic Chemistry, 107, 104576. https://doi.org/10.1016/j.bioorg.2020.104576
  • Liebeschuetz, J. W., Cole, J. C., & Korb, O. (2012). Pose prediction and virtual screening performance of GOLD scoring functions in a standardized test. Journal of Computer-Aided Molecular Design, 26(6), 737–748. https://doi.org/10.1007/s10822-012-9551-4
  • Linciano, P., Cendron, L., Gianquinto, E., Spyrakis, F., & Tondi, D. (2019). Ten years with New Delhi metallo-β-lactamase-1 (NDM-1): From structural insights to inhibitor design. ACS Infectious Diseases, 5(1), 9–34. https://doi.org/10.1021/acsinfecdis.8b00247
  • Lobanov, M. Y., Bogatyreva, N. S., & Galzitskaya, O. V. (2008). Radius of gyration as an indicator of protein structure compactness. Molecular Biology, 42(4), 623–628. https://doi.org/10.1134/S0026893308040195
  • Lomovskaya, O., Tsivkovski, R., Nelson, K., Rubio-Aparicio, D., Sun, D., Totrov, M., & Dudley, M. N. (2020). Spectrum of beta-lactamase inhibition by the cyclic boronate QPX7728, an ultrabroad-spectrum beta-lactamase inhibitor of serine and metallo-beta-lactamases: Enhancement of activity of multiple antibiotics against isogenic strains expressing single beta-lactamases. Antimicrobial Agents and Chemotherapy, 64(6), e00212-20. https://doi.org/10.1128/AAC.00212-20
  • Malde, A. K., Zuo, L., Breeze, M., Stroet, M., Poger, D., Nair, P. C., Oostenbrink, C., & Mark, A. E. (2011). An automated force field topology builder (ATB) and repository: Version 1.0. Journal of Chemical Theory and Computation, 7(12), 4026–4037. https://doi.org/10.1021/ct200196m
  • Mendelson, M., & Matsoso, M. P. (2015). The world health organization global action plan for antimicrobial resistance. South African Medical Journal, 105(5), 325. https://doi.org/10.7196/SAMJ.9644
  • Miyamoto, S., & Kollman, P. A. (1992). Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. Journal of Computational Chemistry, 13(8), 952–962. https://doi.org/10.1002/jcc.540130805
  • Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., & Olson, A. J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Journal of Computational Chemistry, 19(14), 1639–1662. https://doi.org/10.1002/(Sici)1096-987x(19981115)19:14 < 1639::Aid-Jcc10 > 3.0.Co;2-B
  • Mulani, M. S., Kamble, E. E., Kumkar, S. N., Tawre, M. S., & Pardesi, K. R. (2019). Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: A review. Frontiers in Microbiology, 10, 539. https://doi.org/10.3389/fmicb.2019.00539
  • Nishida, C. R., & Ortiz De Montellano, P. R. (2011). Bioactivation of antituberculosis thioamide and thiourea prodrugs by bacterial and mammalian flavin monooxygenases. Chemico-Biological Interactions, 192(1–2), 21–25. https://doi.org/10.1016/j.cbi.2010.09.015
  • Odds, F. C. (2003). Synergy, antagonism, and what the chequerboard puts between them. Journal of Antimicrobial Chemotherapy, 52(1), 1. https://doi.org/10.1093/jac/dkg301
  • Olsson, M. H. M., SØndergaard, C. R., Rostkowski, M., & Jensen, J. H. (2011). PROPKA3: Consistent treatment of internal and surface residues in empirical pKa Predictions. Journal of Chemical Theory and Computation, 7(2), 525–537. https://doi.org/10.1021/ct100578z
  • Omar, A., ‐Mohsen, M. E., Eshba, N. H., & Salama, H. M. (1984). Syntheses of Some Substituted isatin-beta-thiosemicarbazones and isatin-beta-hydrazonothiazoline derivatives as potential antiviral and antimicrobial agents. Archiv Der Pharmazie, 317(8), 701–709. https://doi.org/10.1002/ardp.19843170810
  • World Health Organization. (2019). New report calls for urgent action to avert antimicrobial resistance crisis. In Joint News Release (Vol. 29). https://www.who.int/news/item/29-04-2019-new-report-calls-for-urgent-action-to-avert-antimicrobial-resistance-crisis
  • Pape, V. F. S., Tóth, S., Füredi, A., Szebényi, K., Lovrics, A., Szabó, P., Wiese, M., & Szakács, G. (2016). Design, synthesis and biological evaluation of thiosemicarbazones, hydrazinobenzothiazoles and arylhydrazones as anticancer agents with a potential to overcome multidrug resistance. European Journal of Medicinal Chemistry, 117, 335–354. https://doi.org/10.1016/j.ejmech.2016.03.078
  • Parkova, A., Lucic, A., Krajnc, A., Brem, J., Calvopiña, K., Langley, G. W., McDonough, M. A., Trapencieris, P., & Schofield, C. J. (2020). Broad spectrum β-lactamase inhibition by a thioether substituted bicyclic boronate. ACS Infectious Diseases, 6(6), 1398–1404. https://doi.org/10.1021/acsinfecdis.9b00330
  • Pillai, S. K., & Moellering, R. C., Jr. (2005). Antimicrobial combinations. In V. Lorian (Ed.), Antibiotics in laboratory medicine (5th ed., pp. 365–440). Lippincott Williams & Wilkins.
  • Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., Van Der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/bioinformatics/btt055
  • Rostkowski, M., Olsson, M. H. M., Søndergaard, C. R., & Jensen, J. H. (2011). Graphical analysis of pH-dependent properties of proteins predicted using PROPKA. BMC Structural Biology, 11(1), 6. https://doi.org/10.1186/1472-6807-11-6
  • Salentin, S., Schreiber, S., Haupt, V. J., Adasme, M. F., & Schroeder, M. (2015). PLIP: Fully automated protein-ligand interaction profiler. Nucleic Acids Research, 43(W1), W443–W447. https://doi.org/10.1093/nar/gkv315
  • Santucci, M., Spyrakis, F., Cross, S., Quotadamo, A., Farina, D., Tondi, D., De Luca, F., Docquier, J. D., Prieto, A. I., Ibacache, C., Blázquez, J., Venturelli, A., Cruciani, G., & Costi, M. P. (2017). Computational and biological profile of boronic acids for the detection of bacterial serine- and metallo-β-lactamases. Scientific Reports, 7(1), 1-15. https://doi.org/10.1038/s41598-017-17399-7
  • Sargsyan, K., Grauffel, C., & Lim, C. (2017). How molecular size impacts RMSD applications in molecular dynamics simulations. Journal of Chemical Theory and Computation, 13(4), 1518–1524. https://doi.org/10.1021/acs.jctc.7b00028
  • Šarkanj, B., Molnar, M., Čačić, M., & Gille, L. (2013). 4-Methyl-7-hydroxycoumarin antifungal and antioxidant activity enhancement by substitution with thiosemicarbazide and thiazolidinone moieties. Food Chemistry, 139(1–4), 488–495. https://doi.org/10.1016/j.foodchem.2013.01.027
  • Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., & van Gunsteren, W. F. (2011). Definition and testing of the GROMOS force-field versions 54A7 and 54B7. European Biophysics Journal, 40(7), 843–856. https://doi.org/10.1007/s00249-011-0700-9
  • Schrödinger L. L. C. (2009). The PyMOL molecular graphics system, version 1.3.
  • Sharma, S., Sharma, S., Singh, P. P., & Khan, I. A. (2020). Potential inhibitors against NDM-1 type metallo-β-lactamases: An overview. Microbial Drug Resistance (Larchmont, N.Y.), 26(12), 1568–1588. https://doi.org/10.1089/mdr.2019.0315
  • Soldatović, T. (2020). Correlation between HSAB principle and substitution reactions in bioinorganic reactions. In Photochemistry and photophysics - recent advances [Working Title]. IntechOpen. https://doi.org/10.5772/intechopen.91682
  • Søndergaard, C. R., Olsson, M. H. M. M., Rostkowski, M., & Jensen, J. H. (2011). Improved treatment of ligands and coupling effects in empirical calculation and rationalization of pKa values. Journal of Chemical Theory and Computation, 7(7), 2284–2295. https://doi.org/10.1021/ct200133y
  • Song, G. Q., Wang, W. M., Li, Z. S., Wang, Y., & Wang, J. G. (2018). First identification of isatin-β-thiosemicarbazones as novel inhibitors of New Delhi metallo-β-lactamase-1: Chemical synthesis, biological evaluation and molecular simulation. Chinese Chemical Letters, 29(6), 899–902. https://doi.org/10.1016/j.cclet.2017.09.035
  • Spyrakis, F., Santucci, M., Maso, L., Cross, S., Gianquinto, E., Sannio, F., Verdirosa, F., De Luca, F., Docquier, J. D., Cendron, L., Tondi, D., Venturelli, A., Cruciani, G., & Costi, M. P. (2020). Virtual screening identifies broad-spectrum β-lactamase inhibitors with activity on clinically relevant serine- and metallo-carbapenemases. Scientific Reports, 10(1). https://doi.org/10.1038/s41598-020-69431-y
  • Stroet, M., Caron, B., Visscher, K. M., Geerke, D. P., Malde, A. K., & Mark, A. E. (2018). Automated topology builder version 3.0: Prediction of solvation free enthalpies in water and hexane. Journal of Chemical Theory and Computation, 14(11), 5834–5845. https://doi.org/10.1021/acs.jctc.8b00768
  • Summers, K. L. (2019). A structural chemistry perspective on the antimalarial properties of thiosemicarbazone metal complexes. Mini-Reviews in Medicinal Chemistry, 19(7), 569–590. https://doi.org/10.2174/1389557518666181015152657
  • Sun, L.-Y., Chen, C., Su, J., Li, J.-Q., Jiang, Z., Gao, H., Chigan, J.-Z., Ding, H.-H., Zhai, L., & Yang, K.-W. (2021). Ebsulfur and Ebselen as highly potent scaffolds for the development of potential SARS-CoV-2 antivirals. Bioorganic Chemistry, 112, 104889. https://doi.org/10.1016/j.bioorg.2021.104889
  • Sun, Z., Hu, L., Sankaran, B., Prasad, B. V. V., & Palzkill, T. (2018). Differential active site requirements for NDM-1 β-lactamase hydrolysis of carbapenem versus penicillin and cephalosporin antibiotics. Nature Communications, 9(1), 1–14. https://doi.org/10.1038/s41467-018-06839-1
  • Talebi Bezmin Abadi, A., Rizvanov, A. A., Haertlé, T., & Blatt, N. L. (2019). World Health Organization Report: Current crisis of antibiotic resistance. BioNanoScience, 9(4), 778–788. Springer New York LLC. https://doi.org/10.1007/s12668-019-00658-4
  • Tripos Associates, I. (2012). Sybyl-X molecular modeling software packages. Version 2.1. 1.
  • van den Akker, F., & Bonomo, R. A. (2018). Exploring additional dimensions of complexity in inhibitor design for serine β-lactamases: Mechanistic and intra- and inter-molecular chemistry approaches. Frontiers in Microbiology, 9, 622. https://doi.org/10.3389/fmicb.2018.00622
  • Van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
  • Verdonk, M. L., Cole, J. C., Hartshorn, M. J., Murray, C. W., & Taylor, R. D. (2003). Improved protein-ligand docking using GOLD. Proteins, 52(4), 609–623. https://doi.org/10.1002/prot.10465
  • Verli, H. (2014). Bioinformática da Biologia à Flexibilidade Molecular. In H. Verli (Ed.), Universidade Federal do Rio Grande do Sul (1st ed., Vol. 53(9)). Sociedade Brasileira de Bioquímica e Biologia Molecular. https://www.lume.ufrgs.br/bitstream/handle/10183/166105/001012172.pdf?sequence=1&isAllowed=y
  • Westermaier, Y., Barril, X., & Scapozza, L. (2015). Virtual screening: An in silico tool for interlacing the chemical universe with the proteome. Methods (San Diego, Calif.), 71(C), 44–57. https://doi.org/10.1016/j.ymeth.2014.08.001
  • Wolff, N., Hendling, M., Schroeder, F., Schönthaler, S., Geiss, A. F., Bedenic, B., & Barišić, I. (2021). Full pathogen characterisation: Species identification including the detection of virulence factors and antibiotic resistance genes via multiplex DNA-assays. Scientific Reports, 11(1), 6001. https://doi.org/10.1038/s41598-021-85438-5
  • Wu, W., Feng, Y., Tang, G., Qiao, F., McNally, A., & Zong, Z. (2019). NDM metallo-β-lactamases and their bacterial producers in health care settings. Clinical Microbiology Reviews. American Society for Microbiology, 32(2), e00115-18. https://doi.org/10.1128/CMR.00115-18
  • Xiang, Y., Chen, C., Wang, W. M., Xu, L. W., Yang, K. W., Oelschlaeger, P., & He, Y. (2018). Rhodanine as a potent scaffold for the development of broad-spectrum metallo-β-lactamase inhibitors. ACS Medicinal Chemistry Letters, 9(4), 359–364. https://doi.org/10.1021/acsmedchemlett.7b00548
  • Xu, L., Sun, H., Li, Y., Wang, J., & Hou, T. (2013). Assessing the performance of MM/PBSA and MM/GBSA methods. 3. The impact of force fields and ligand charge models. The Journal of Physical Chemistry B, 117(28), 8408–8421. https://doi.org/10.1021/jp404160y
  • Yoshizumi, A., Ishii, Y., Livermore, D. M., Woodford, N., Kimura, S., Saga, T., Harada, S., Yamaguchi, K., & Tateda, K. (2013). Efficacies of calcium-EDTA in combination with imipenem in a murine model of sepsis caused by Escherichia coli with NDM-1 β-lactamase. Journal of Infection and Chemotherapy, 19(5), 992–995. https://doi.org/10.1007/s10156-012-0528-y
  • Yu, Y., Kalinowski, D. S., Kovacevic, Z., Siafakas, A. R., Jansson, P. J., Stefani, C., Lovejoy, D. B., Sharpe, P. C., Bernhardt, P. V., & Richardson, D. R. (2009). Thiosemicarbazones from the old to new: Iron chelators that are more than just ribonucleotide reductase inhibitors. Journal of Medicinal Chemistry, 52(17), 5271–5294. https://doi.org/10.1021/jm900552r
  • Zhang, D., Markoulides, M. S., Stepanovs, D., Rydzik, A. M., El-Hussein, A., Bon, C., Kamps, J. J. A. G., Umland, K. D., Collins, P. M., Cahill, S. T., Wang, D. Y., von Delft, F., Brem, J., McDonough, M. A., & Schofield, C. J. (2018). Structure activity relationship studies on rhodanines and derived enethiol inhibitors of metallo-β-lactamases. Bioorganic & Medicinal Chemistry, 26(11), 2928–2936. https://doi.org/10.1016/j.bmc.2018.02.043
  • Zhang, H. M., & Hao, Q. (2011). Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism. FASEB Journal, 25(8), 2574–2582. https://doi.org/10.1096/fj.11-184036
  • Zhao, B., Zhang, X., Yu, T., Liu, Y., Zhang, X., Yao, Y., Feng, X., Liu, H., Yu, D., Ma, L., & Qin, S. (2021). Discovery of thiosemicarbazone derivatives as effective New Delhi metallo-β-lactamase-1 (NDM-1) inhibitors against NDM-1 producing clinical isolates. Acta Pharmaceutica Sinica B, 11(1), 203–221. https://doi.org/10.1016/j.apsb.2020.07.005

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.