Insight into the structural requirements of thiophene-3-carbonitriles-based MurF inhibitors by 3D-QSAR, molecular docking and molecular dynamics study

References

• Chellat MF, Raguž L, Riedl R. Targeting antibiotic resistance. Angew Chem Int Ed Engl. 2016;55:6600–6626.
   PubMed Web of Science ®Google Scholar
• Dumbre S, Derouaux A, Lescrinier E, et al. Synthesis of modified peptidoglycan precursor analogues for the inhibition of glycosyltransferase. J Am Chem Soc. 2012;134:9343–9351.
   PubMed Web of Science ®Google Scholar
• Anderson MS, Eveland SS, Onishi HR, et al. Kinetic mechanism of the Escherichia coli UDPMurNAc-tripeptide D-alanyl-D-alanine-adding enzyme: use of a glutathione S-transferase fusion. Biochemistry. 1996;35:16264–16269.
   PubMed Web of Science ®Google Scholar
• Bugg TD, Walsh CT. Intracellular steps of bacterial cell wall peptidoglycan biosynthesis: enzymology, antibiotics, and antibiotic resistance. Nat Prod Rep. 1992;9:199–215.
   PubMed Web of Science ®Google Scholar
• Mengin-Lecreulx D, van Heijenoort J, Park JT. Identification of the mpl gene encoding UDP-N-acetylmuramate: L-alanyl-gamma-D-glutamyl-meso-diaminopimelate ligase in Escherichia coli and its role in recycling of cell wall peptidoglycan. J Bacteriol. 1996;178:5347–5352.
   PubMed Web of Science ®Google Scholar
• Zoeiby AE, Sanschagrin F, Levesque RC. Structure and function of the Mur enzymes: development of novel inhibitors. Mol Microbiol. 2003;47:1–12.
   PubMed Web of Science ®Google Scholar
• Longenecker KL, Stamper GF, Hajduk PJ, et al. Structure of MurF from Streptococcus pneumoniae co-crystallized with a small molecule inhibitor exhibits interdomain closure. Protein Sci. 2005;14:3039–3047.
   PubMed Web of Science ®Google Scholar
• Bouhss A, Mengin-Lecreulx D, Blanot D, et al. Invariant amino acids in the Mur peptide synthetases of bacterial peptidoglycan synthesis and their modification by site-directed mutagenesis in the UDP-MurNAc:L-alanine ligase from Escherichia coli. Biochemistry. 1997;36:11556–11563.
   PubMed Web of Science ®Google Scholar
• Schulz GE. Binding of nucleotides by proteins. Curr Opin Struct Biol. 1992;2:61–67.
   Google Scholar
• Baum EZ, Crespo-Carbone SM, Abbanat D, et al. Utility of muropeptide ligase for identification of inhibitors of the cell wall biosynthesis enzyme MurF. Antimicrob Agents Chemother. 2006;50:230–236.
   PubMed Web of Science ®Google Scholar
• Yan Y, Munshi S, Leiting B, et al. Crystal structure of Escherichia coli UDPMurNAc-tripeptide d-alanyl-d-alanine-adding enzyme (MurF) at 2.3 A resolution. J Mol Biol. 2000;304:435–445.
   PubMed Web of Science ®Google Scholar
• Miller DJ, Hammond SM, Anderluzzi D, et al. Aminoalkylphosphinate inhibitors of D-Ala-D-Ala adding enzyme. J Chem Soc Perkin Trans. 1998;1:131–142.
   Google Scholar
• Gu YG, Florjancic AS, Clark RF, et al. Structure-activity relationships of novel potent MurF inhibitors. Bioorg Med Chem Lett. 2004;14:267–270.
   PubMed Web of Science ®Google Scholar
• Paradis-Bleau C, Lloyd A, Sanschagrin F, et al. Phage display-derived inhibitor of the essential cell wall biosynthesis enzyme MurF. BMC Biochem. 2008;9:33.
   PubMed Web of Science ®Google Scholar
• Murakami R, Muramatsu Y, Minami E, et al. A novel assay of bacterial peptidoglycan synthesis for natural product screening. J Antibiot (Tokyo). 2009;62:153–158.
   PubMed Web of Science ®Google Scholar
• Baum EZ, Crespo-Carbone SM, Foleno BD, et al. MurF inhibitors with antibacterial activity: effect on muropeptide levels. Antimicrob Agents Chemother. 2009;53:3240–3247.
   PubMed Web of Science ®Google Scholar
• Hrast M, Turk S, Sosič I, et al. Structure activity relationships of new cyanothiophene inhibitors of the essential peptidoglycan biosynthesis enzyme MurF. Eur J Med Chem. 2013;66:32–45.
   PubMed Web of Science ®Google Scholar
• Hrast M, Anderluh M, Knez D, et al. Design, synthesis and evaluation of second generation MurF inhibitors based on a cyanothiophene scaffold. Eur J Med Chem. 2014;73:83–96.
   PubMed Web of Science ®Google Scholar
• Khedkar SA, Malde AK, Coutinho EC. Design of inhibitors of the MurF enzyme of Streptococcus pneumoniae using docking, 3D-QSAR, and de novo design. J Chem Inf Model. 2007;47:1839–1846.
   PubMed Web of Science ®Google Scholar
• Taha MO, Atallah N, Al-Bakri AG, et al. Discovery of new MurF inhibitors via pharmacophore modeling and QSAR analysis followed by in-silico screening. Bioorg Med Chem. 2008;16:1218–1235.
   PubMed Web of Science ®Google Scholar
• Kovac A, Konc J, Vehar B, et al. Discovery of new inhibitors of D-alanine: D-alanine ligase by structure-based virtual screening. J Med Chem. 2008;51:7442–7448.
   PubMed Web of Science ®Google Scholar
• Turk S, Kovac A, Boniface A, et al. Discovery of new inhibitors of the bacterial peptidoglycan biosynthesis enzymes MurD and MurF by structure-based virtual screening. Bioorg Med Chem. 2009;17:1884–1889.
   PubMed Web of Science ®Google Scholar
• Shivakumar D, Williams J, Wu Y, et al. Prediction of absolute solvation free energies using molecular dynamics free energy perturbation and the OPLS force field. J Chem Theory Comput. 2010;6:1509–1519.
   PubMed Web of Science ®Google Scholar
• Dixon SL, Smondyrev AM, Knoll EH, et al. PHASE: a new engine for pharmacophore perception, 3D QSAR model development, and 3D database screening: 1. Methodology and preliminary results. J Comput Aided Mol Des. 2006;20:647–671.
   PubMed Web of Science ®Google Scholar
• Watts KS, Dalal P, Murphy RB, et al. ConfGen: a conformational search method for efficient generation of bioactive conformers. J Chem Inf Model. 2010;50:534–546.
   PubMed Web of Science ®Google Scholar
• Kirchmair J, Mark P, Distinto S, et al. Evaluation of the performance of 3D virtual screening protocols: RMSD comparisons, enrichment assessments and decoy selection what can we learn from earlier mistakes? J Comput Aided Mol Des. 2008;22:213–228.
   PubMed Web of Science ®Google Scholar
• Sheridan RP, Singh SB, Fluder EM, et al. Protocols for bridging the peptide to nonpeptide gap in topological similarity searches. J Chem Inf Comput Sci. 2001;41:1395–1406.
   PubMedGoogle Scholar
• Stamper GF, Longenecker KL, Fry EH, et al. Structure-based optimization of MurF inhibitors. Chem Biol Drug Design. 2006;67:58–65.
   PubMed Web of Science ®Google Scholar
• Perdih A, Hrast M, Pureber K, et al. Furan-based benzene mono- and dicarboxylic acid derivatives as multiple inhibitors of the bacterial Mur ligases (MurC-MurF): experimental and computational characterization. J Comput Aided Mol Des. 2015;29:541–560.
   PubMed Web of Science ®Google Scholar
• Comess KM, Schurdak ME, Voorbach MJ, et al. An ultraefficient affinity-based high-throughout screening process: application to bacterial cell wall biosynthesis enzyme MurF. J Biomol Screen. 2006;11:743–754.
   PubMed Web of Science ®Google Scholar
• Sastry GM, Adzhigirey M, Day T, et al. Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J Comput Aided Mol Des. 2013;27:221–234.
   PubMed Web of Science ®Google Scholar
• Jacobson MP, Pincus DL, Rapp CS, et al. A hierarchical approach to all-atom protein loop prediction. Proteins. 2004;55:351–367.
   PubMed Web of Science ®Google Scholar
• Friesner RA, Murphy RB, Repasky MP, et al. Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J Med Chem. 2006;49:6177–6196.
   PubMed Web of Science ®Google Scholar
• Li J, Abel R, Zhu K, et al. The VSGB 2.0 model: a next generation energy model for high resolution protein structure modeling. Proteins. 2011;79:2794–2812.
   PubMed Web of Science ®Google Scholar
• Guo Z, Mohanty U, Noehre J, et al. Probing the α-helical structural stability of stapled p53 peptides: molecular dynamics simulations and analysis. Chem Biol Drug Des. 2010;75:348–359.
   PubMed Web of Science ®Google Scholar
• Essmann U, Perera L, Berkowit ML, et al. A smooth particle mesh Ewald method. J Chem Phys. 1995;103:8577–8593.
   Web of Science ®Google Scholar
• Martyna GJ, Klein ML, Tuckerman M. Nose-Hoover chains – the canonical ensemble via continuous dynamics. J Chem Phys. 1992;97:2635–2643.
   Web of Science ®Google Scholar
• Martyna GJ, Tobias DJ, Klein ML. Constant-pressure molecular dynamics algorithms. J Chem Phys. 1994;01:4177–4189.
   Web of Science ®Google Scholar
• Golbraikh A, Tropsha A. Beware of q2! J Mol Graph Model. 2002;20:269–276.
   PubMed Web of Science ®Google Scholar
• Golbraikh A, Tropsha A. Predictive QSAR modeling based on diversity sampling of experimental datasets for the training and test set selection. J Comput Aided Mol Des. 2002;5:231–243.
   Google Scholar