Combining molecular docking and molecular dynamics studies for modelling Staphylococcus aureus MurD inhibitory activity

References

• World Health Organization. Antimicrobial resistance: Global report on surveillance. (2014), http://apps.who.int/iris/bitstream/10665/112647/1/WHO_HSE_PED_AIP_2014.2_eng.pdf?ua=1
   Google Scholar
• S. Nambiar, K. Laessig, J. Toerner, J. Farley, and E. Cox, Antibacterial drug development: Challenges, recent developments, and future considerations, Clin. Pharmacol. Ther. 96 (2014), pp. 147–149.
   Google Scholar
• X. Duval, F. Delahaye, F. Alla, P. Tattevin, J.F. Obadia, V. Le Moing, T. Doco-Lecompte, M. Celard, C. Poyart, C. Strady, C. Chirouze, M. Bes, E. Cambau, B. Iung, C. Selton-Suty, and B. Hoen, Temporal trends in infective endocarditis in the context of prophylaxis guideline modifications: Three successive population-based surveys, J. Am. Coll. Cardiol. 59 (2012), pp. 1968–1976.
   PubMed Web of Science ®Google Scholar
• U. Fedeli, E. Schievano, D. Buonfrate, G. Pellizzer, and P. Spolaore, Increasing incidence and mortality of infective endocarditis: A population-based study through a record-linkage system, BMC Infect. Dis. 11 (2011), p. 48.
   PubMed Web of Science ®Google Scholar
• H. Barreteau, A. Kovac, A. Boniface, M. Sova, S. Gobec, and D. Blanot, Cytoplasmic steps of peptidoglycan biosynthesis, FEMS Microbiol. Rev. 32 (2008), pp. 168–207.
   PubMed Web of Science ®Google Scholar
• A. Bouhss, S. Dementin, J. van Heijenoort, C. Parquet, and D. Blanot, MurC and MurD synthetases of peptidoglycan biosynthesis: Borohydride trapping of acylphosphate intermediates, Methods Enzymol. 354 (2002), pp. 189–196.
   PubMed Web of Science ®Google Scholar
• S.S. Eveland, D.L. Pompliano, and M.S. Anderson, Conditionally lethal Escherichia coli murein mutants contain point defects that map to regions conserved among murein and folyl poly-g-glutamate ligases: Identification of a ligase superfamily, Biochemistry 36 (1997), pp. 6223–6229.
   PubMed Web of Science ®Google Scholar
• A. Bouhss, S. Dementin, C. Parquet, D. Mengin-Lecreulx, J.A. Bertrand, D. Le Beller, O. Dideberg, J. van Heijenoort, and D. Blanot, Role of the ortholog and paralog amino acid invariants in the active site of the UDP-MurNAc-l-alanine: D-glutamateligase (MurD), Biochemistry 38 (1999), pp. 12240–12247.
   PubMed Web of Science ®Google Scholar
• J. van Heijenoort, Recent advances in the formation of the bacterial peptidoglycan monomer unit, Nat. Prod. Rep. 18 (2001), pp. 503–519.
   PubMed Web of Science ®Google Scholar
• V. Skedelj, T. Tomasic, L.P. Masic, and A. Zega, ATP‐binding site of bacterial enzymes as a target for antibacterial drug design, J. Med. Chem. 54 (2011), pp. 915–929.
   PubMed Web of Science ®Google Scholar
• A.W. Walsh, P.J. Falk, J. Thanassi, L. Discotto, M.J. Pucci, and H.T. Ho, Comparison of the D-glutamate-adding enzymes from selected gram-positive and gram-negative bacteria, J. Bacteriol. 181 (1999), pp. 5395–5401.
   PubMed Web of Science ®Google Scholar
• A. El Zoeiby, F. Sanschagrin, and R.C. Levesque, Structure and function of the Mur enzymes: Development of novel inhibitors, Mol. Microbiol. 47 (2003), pp. 1–12.
   PubMed Web of Science ®Google Scholar
• A. Perdih, M. Kotnik, M. Hodoscek, and T. Solmajer, Targeted molecular dynamics simulation studies of binding and conformational changes in E. coli MurD, Proteins 68 (2007), pp. 243–254.
   PubMed Web of Science ®Google Scholar
• A. Bouhss, D. Mengin-Lecreulx, D. Blanot, J. van Heijenoort and C. Parquet, Invariant amino acids in the Mur peptide synthetases of bacterial peptidoglycan synthesis and their modification by site-directed mutagenesis in the UDP-MurNAc: L-alanineligase from Escherichia coli, Biochemistry 36 (1997), pp. 11556–11563.
   PubMed Web of Science ®Google Scholar
• H. Barreteau, I. Sosic, S. Turk, J. Humljan, T. Tomasic, N. Zidar, M. Herve, A. Boniface, L. Peterlin-Masic, D. Kikelj, D. Mengin-Lecreulx, S. Gobec, and D. Blanot, MurD enzymes from different bacteria: Evaluation of inhibitors, Biochem. Pharmacol. 84 (2012), pp. 625–632.
   PubMed Web of Science ®Google Scholar
• J.A. Bertrand, G. Auger, L. Martin, E. Fanchon, D. Blanot, D. Le Beller, J. van Heijenoort, and O. Dideberg, Determination of the MurD mechanism through crystallographic analysis of enzyme complexes, J. Mol. Biol. 289 (1999), pp. 579–590.
   PubMed Web of Science ®Google Scholar
• E. Gordon, B. Flouret, L. Chantalat, J. van Heijenoort, D. Mengin-Lecreulx, and O. Dideberg, Crystal structure of UDP-N-acetylmuramoyl-L-alanyl-D-glutamate: Meso-diaminopimelate ligase from Escherichia coli, J. Biol. Chem. 276 (2001), pp. 10999–11006.
   PubMed Web of Science ®Google Scholar
• Y. Yan, S. Munshi, B. Leiting, M.S. Anderson, J. Chrzas, and Z. Chen, Crystal structure of Escherichia coli UDPMurNAc-tripeptide d-alanyl-d-alanine-adding enzyme (MurF) at 2.3 A resolution, J. Mol. Biol. 304 (2000), pp. 435–445.
   PubMed Web of Science ®Google Scholar
• C.A. Smith, Structure, function and dynamics in the mur family of bacterial cell wall ligases, J. Mol. Biol. 362 (2006), pp. 640–655.
   PubMed Web of Science ®Google Scholar
• L.D. Gegnas, S.T. Waddell, R.M. Chabin, S. Reddy, and K.K. Wong, Inhibitors of the bacterial cell wall biosynthesis enzyme MurD, Bioorg. Med. Chem. Lett. 8 (1998), pp. 1643–1648.
   PubMed Web of Science ®Google Scholar
• S. Gobec, U. Urleb, G. Auger, and D. Blanot, Synthesis and biochemical evaluation of some novel N-acyl phosphono- and phosphinoalanine derivatives as potential inhibitors of the D-glutamic acid-adding enzyme, Die Pharmazie 56 (2001), pp. 295–297.
   PubMed Web of Science ®Google Scholar
• K. Strancar, D. Blanot, and S. Gobec, Design, synthesis and structure–activity relationships of new phosphinate inhibitors of MurD, Bioorg. Med. Chem. Lett. 16 (2006), pp. 343–348.
   PubMedGoogle Scholar
• G. Auger, J. van Heijenoort, and D. Blanot, Synthesis of N-Acetylmuramic acid derivatives as potential inhibitors of the D-glutamic acid-adding enzyme, J. Prakt. Chem. 337 (1995), pp. 351–357.
   Google Scholar
• M. Kotnik, J. Humljan, C. Contreras-Martel, M. Oblak, K. Kristan, M. Herve, D. Blanot, U. Urleb, S. Gobec, A. Dessen, and T. Solmajer, Structural and functional characterization of enantiomeric glutamic acid derivatives as potential transition state analogue inhibitors of MurD ligase, J. Mol. Biol. 370 (2007), pp. 107–115.
   PubMed Web of Science ®Google Scholar
• J. Humljan, M. Kotnik, C. Contreras-Martel, D. Blanot, U. Urleb, A. Dessen, T. Solmajer, and S. Gobec, Novel naphthalene-N-sulfonyl-D-glutamic acid derivatives as inhibitors of MurD, a key peptidoglycan biosynthesis enzyme, J. Med. Chem. 51 (2008), pp. 7486–7494.
   PubMed Web of Science ®Google Scholar
• F. Pratviel-Sosa, F. Acher, F. Trigalo, D. Blanot, R. Azerad, and J. van Heijenoort, Effect of various analogues of D-glutamic acid on the D-glutamate-adding enzyme from Escherichia coli, FEMS Microbiol. Lett. 115 (1994), pp. 223–228.
   PubMed Web of Science ®Google Scholar
• A. Perdih, U. Bren, and T. Solmajer, Binding free energy calculations of N-sulphonyl-glutamic acid inhibitors of MurD ligase, Mol. Model. 15 (2009), pp. 983–996.
   PubMed Web of Science ®Google Scholar
• M. Sova, A. Kovac, S. Turk, M. Hrast, D. Blanot, and S. Gobec, Phosphorylated hydroxyethylamines as novel inhibitors of the bacterial cell wall biosynthesis enzymes MurC to MurF, Bioorg. Chem. 37 (2009), pp. 217–222.
   PubMed Web of Science ®Google Scholar
• N. Zidar, T. Tomasic, R. Sink, V. Rupnik, A. Kovac, S. Turk, D. Patin, D. Blanot, C. Contreras Martel, A. Dessen, M. Muller Premru, A. Zega, S. Gobec, L. Masic and D. Kikelj, Discovery of novel 5-benzylidenerhodanine and 5-benzylidenethiazolidine-2,4-dione inhibitors of MurD ligase, J. Med. Chem. 53 (2010), pp. 6584–6594.
   PubMed Web of Science ®Google Scholar
• N. Zidar, T. Tomasic, R. Sink, A. Kovac, D. Patin, D. Blanot, C. Contreras-Martel, A. Dessen, M.M. Premru, A. Zega, S. Gobec, L.P. Masic, and D. Kikelj, New 5-benzylidenethiazolidin-4-one inhibitors of bacterial MurD ligase: Design, synthesis, crystal structures, and biological evaluation, Eur. J. Med. Chem. 46 (2011), pp. 5512–5523.
   PubMed Web of Science ®Google Scholar
• I. Sosic, H. Barreteau, M. Simcic, R. Sink, J. Cesar, A. Zega, S.G. Grdadolnik, C. Contreras-Martel, A. Dessen, A. Amoroso, B. Joris, D. Blanot, and S. Gobec, Second-generation sulfonamide inhibitors of D-glutamic acid-adding enzyme: Activity optimisation with conformationally rigid analogues of D-glutamic acid, Eur. J. Med. Chem. 46 (2011), pp. 2880–2894.
   PubMed Web of Science ®Google Scholar
• A. Perdih, M. Hrast, H. Barreteau, S. Gobec, G. Wolber, and T. Solmajer, Benzene-1,3-dicarboxylic acid 2,5-dimethylpyrrole derivatives as multiple inhibitors of bacterial Mur ligases (MurC-MurF), Bioorg. Med. Chem. 22 (2014), pp. 4124–4134.
   PubMed Web of Science ®Google Scholar
• A. Perdih, A. Kovac, G. Wolber, D. Blanot, S. Gobec, and T. Solmajer, Discovery of novel benzene 1,3-dicarboxylic acid inhibitors of bacterial MurD and MurE ligases by structure-based virtual screening approach, Bioorg. Med. Chem. Lett. 19 (2009), pp. 2668–2673.
   PubMed Web of Science ®Google Scholar
• S. Turk, A. Kovac, A. Boniface, J.M. Bostock, I. Chopra, D. Blanot, and S. Gobec, Discovery of new inhibitors of the bacterial peptidoglycan biosynthesis enzymes MurD and MurF by structure-based virtual screening, Bioorg. Med. Chem. 17 (2009), pp. 1884–1889.
   PubMed Web of Science ®Google Scholar
• M. Kotnik, P.S. Anderluh, and A. Prezelj, Development of novel inhibitors targeting intracellular steps of peptidoglycan biosynthesis, Curr. Pharm. Des. 13 (2007), pp. 2283–2309.
   PubMed Web of Science ®Google Scholar
• T. Tomasic, R. Sink, N. Zidar, A. Fic, C. Contreras-Martel, A. Dessen, D. Patin, D. Blanot, M. Muller-Premru, S. Gobec, A. Zega, D. Kikelj, and L.P. Masic, Dual inhibitor of MurD and MurE ligases from Escherichia coli and Staphylococcus aureus, ACS Med. Chem. Lett. 3 (2012), pp. 626–630.
   PubMed Web of Science ®Google Scholar
• M.P. Jacobson, D.L. Pincus, C.S. Rapp, T.J.F. Day, B. Honig, D.E. Shaw, and R.A. Friesner, A hierarchical approach to all-atom protein loop prediction, Proteins: Struct. Funct. Bioinf. 55 (2004), pp. 351–367.
   PubMed Web of Science ®Google Scholar
• E. Harder, W. Damm, J. Maple, C. Wu, M. Reboul, J.Y. Xiang, L. Wang, D. Lupyan, M.K. Dahlgren, J.L. Knight, J.W. Kaus, D.S. Cerutti, G. Krilov, W.L. Jorgensen, R. Abel, and R.A. Friesner, OPLS3: A force field providing broad coverage of drug-like small molecules and proteins, J. Chem. Theory. Comput. 12 (2016), pp. 281–296.
   PubMed Web of Science ®Google Scholar
• Z. Guo, U. Mohanty, J. Noehre, T.K. Sawyer, W. Sherman, and G. Krilov, Probing the α-helical structural stability of stapled p53 peptides: Molecular dynamics simulations and analysis, Chem. Biol. Drug Des. 75 (2010), pp. 348–359.
   PubMed Web of Science ®Google Scholar
• W.L. Jorgensen and J.D. Madura, Temperature and size dependence for Monte Carlo simulations of TIP4P water, Mol. Phys. 56 (1985), pp. 1381–1392.
   Web of Science ®Google Scholar
• C.P. Lawrence and J.L. Skinner, Flexible TIP4P model for molecular dynamics simulation of liquid water, Chem. Phys. Lett. 372 (2003), pp. 842–847.
   Web of Science ®Google Scholar
• G.J. Martyna, M.L. Klein, and M. Tuckerman, Nose-Hoover chains: The canonical ensemble via continuous dynamics, J. Chem. Phys. 97 (1992), pp. 2635–2643.
   Web of Science ®Google Scholar
• G.J. Martyna, D.J. Tobias, and M.L. Klein, Constant-pressure molecular dynamics algorithms, J. Chem. Phys. 101 (1994), pp. 4177–4189.
   Web of Science ®Google Scholar
• U. Essmann, L. Perera, M.L. Berkowit, T. Darden, H. Lee, and L.G. Pedersen, A smooth particle mesh Ewald method, J. Chem. Phys. 103 (1995), pp. 8577–8593.
   Web of Science ®Google Scholar
• G.M. Sastry, M. Adzhigirey, T. Day, R. Annabhimoju, and W. Sherman, Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments, J. Comput. Aided Mol. Des. 27 (2013), pp. 221–234.
   PubMed Web of Science ®Google Scholar
• J. Li, R. Abel, K. Zhu, Y. Cao, S. Zhao, and R.A. Friesner, The VSGB 2.0 Model: A next generation energy model for high resolution protein structure modelling, Proteins 79 (2011), pp. 2794–2812.
   PubMed Web of Science ®Google Scholar
• R. Sanchez and A. Sali, Advances in comparative protein-structure modelling, Curr. Opin. Struct. Biol. 7 (1997), pp. 206–214.
   PubMed Web of Science ®Google Scholar
• G.N. Ramachandran, C. Ramakrishnan, and V. Sasisekharan, Stereochemistry of polypeptide chain configurations, J. Mol. Biol. 7 (1963), pp. 95–99.
   PubMed Web of Science ®Google Scholar
• J.A. Bertrand, G. Auger, E. Fanchon, L. Martin, D. Blanot, J. van Heijenoort, and O. Dideberg, Crystal structure of UDP-N-acetylmuramoyl-L-alanine: D-glutamateligase from Escherichia coli, EMBO J. 16 (1997), pp. 3416–3425.
   PubMed Web of Science ®Google Scholar
• T. Tomasic, N. Zidar, R. Sink, A. Kovac, D. Blanot, C. Contreras-Martel, A. Dessen, M. Muller-Premru, A. Zega, S. Gobec, D. Kikelj, and L.P. Masic, Structure-based design of a new series of D-glutamic acid based inhibitors of bacterial UDP-N-acetylmuramoyl-L-alanine: D-glutamateligase (MurD), J. Med. Chem. 54 (2011), pp. 4600–4610.
   PubMed Web of Science ®Google Scholar
• T. Tomasic, A. Kovac, M. Simcic, D. Blanot, S.G. Grdadolnik, S. Gobec, D. Kikelj, and L. Peterlin Masic, Novel 2-thioxothiazolidin-4-one inhibitors of bacterial MurD ligase targeting D-Glu- and diphosphate-binding sites, Eur. J. Med. Chem. 46 (2011), pp. 3964–3975.
   PubMed Web of Science ®Google Scholar
• J. Aqvist, C. Medina, and J.E. Samuelsson, A new method for predicting binding affinity in computer-aided drug design, Protein Eng. 7 (1994), pp. 385–391.
   PubMedGoogle Scholar