The Binding Mode of Second-Generation Sulfonamide Inhibitors of MurD: Clues for Rational Design of Potent MurD Inhibitors

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Simčič, Mihael ^a,b   Sosič, Izidor ^c   Hodošček, Milan ^b   Barreteau, Hélène ^d   Blanot, Didier ^d,e   Gobec, Stanislav ^c   Grdadolnik, Simona Golič ^a,b  

^a EN FIST CENTRE OF EXCELLENCE   (Slovenia)

^b NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; CARBON 13; DEXTRO GLUTAMIC ACID; ENZYME; ENZYME INHIBITOR; ISOLEUCINE; LEUCINE; LIGAND; METHYL GROUP; N [6 [4 CYANO 2 FLUOROBENZYLOXY]NAPHATHALENE 2 SULFONAMIDO] DEXTRO GLUTAMIC ACID; NAPHTHALENE N SULFONIC DEXTRO GLUTAMIC ACID; NAPHTHALENE N SULFONYL DERIVATIVE; SULFONAMIDE; UNCLASSIFIED DRUG; URIDINE 5' DIPHOSPHATE N ACETYLMURAMOYL ALANINE DEXTRO GLUTAMATE LIGASE; URIDINE 5' DIPHOSPHATE N ACETYLMURAMOYL ALANINE DEXTRO GLUTAMATE LIGASE INHIBITOR; VALINE;

ARTICLE; BINDING AFFINITY; CONFORMATION; CONTROLLED STUDY; DRUG BINDING; DRUG BINDING SITE; DRUG DESIGN; DRUG POTENCY; DRUG STRUCTURE; HETERONUCLEAR MULTIPLE QUANTUM COHERENCE; ISOTOPE LABELING; LIGAND BINDING; MOLECULAR DYNAMICS; NUCLEAR OVERHAUSER EFFECT; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTON NUCLEAR MAGNETIC RESONANCE;

ANTI-BACTERIAL AGENTS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EPITOPE MAPPING; HYDROGEN BONDING; LIGANDS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PEPTIDE SYNTHASES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; SULFONAMIDES;

EID: 84871402820     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052817     Document Type: Article

References (42)

1. Chopra I, Schofield C, Everett M, O'Neill A, Miller K, et al. (2008) Treatment of health-care-associated infections caused by Gram-negative bacteria: a consensus statement. Lancet Infect Dis 8: 133-139.
2. Petek M, Baebler S, Kuzman D, Rotter A, Podlesek Z, et al. (2010) Revealing fosfomycin primary effect on Staphylococcus aureus transcriptome: modulation of cell envelope biosynthesis and phosphoenolpyruvate induced starvation. BMC Microbiol 10: 1-12.
3. Barreteau H, Kovač A, Boniface A, Sova M, Gobec S, et al. (2008) Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 32: 168-207.
4. Bertrand JA, Auger G, Fanchon E, Martin L, Blanot D, et al. (1997) Crystal structure of UDP-N-acetylmuramoyl-L-alanine:D-glutamate ligase from Escherichia coli. EMBO J 16: 3416-3425.
5. Bertrand JA, Auger G, Martin L, Fanchon E, Blanot D, et al. (1999) Determination of the MurD mechanism through crystallographic analysis of enzyme complexes. J Mol Biol 289: 579-590.
6. Bertrand JA, Fanchon E, Martin L, Chantalat L, Auger G, et al. (2000) "Open" structures of MurD: domain movements and structural similarities with folylpolyglutamate synthetase. J Mol Biol 301: 1257-1266.
7. Kotnik M, Humljan J, Contreras-Martel C, Oblak M, Kristan K, et al. (2007) Structural and functional characterization of enantiomeric glutamic acid derivatives as potential transition state analogue inhibitors of MurD ligase. J Mol Biol 370: 107-115.
8. Humljan J, Kotnik M, Contreras-Martel C, Blanot D, Urleb U, et al. (2008) Novel naphthalene-N-sulfonyl-D-glutamic acid derivatives as inhibitors of MurD, a key peptidoglycan biosynthesis enzyme. J Med Chem 51: 7486-7494.
9. Zidar N, Tomašić T, Šink R, Rupnik V, Kovač A, et al. (2010) Discovery of novel 5-benzylidenerhodanine and 5-benzylidenethiazolidine-2,4-dione inhibitors of MurD ligase. J Med Chem 53: 6584-6594.
10. Tomašić T, Zidar N, Šink R, Kovac A, Blanot D, et al. (2011) Structure-based design of a new series of D-glutamic acid-based inhibitors of bacterial UDP-N-acetylmuramoyl-L-alanine:D-glutamate ligase (MurD). J Med Chem 54: 4600-4610.
11. Sosič I, Barreteau H, Simčič M, Šink R, Cesar J, et al. (2011) 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: 2880-2894.
12. Tanner ME, Vaganay S, van Heijenoort J, Blanot D, (1996) Phosphinate inhibitors of the D-glutamic acid-adding enzyme of peptidoglycan biosynthesis. J Org Chem 61: 1756-1760.
13. Gegnas LD, Waddell ST, Chabin RM, Reddy S, Wong KK, (1998) Inhibitors of the bacterial cell wall biosynthesis enzyme Mur D. Bioorg Med Chem Lett. 8: 1643-1648.
14. Štrancar K, Blanot D, Gobec S, (2006) Design, synthesis and structure-activity relationships of new phosphinate inhibitors of MurD. Bioorg Med Chem Lett 16: 343-348.
15. El Zoeiby A, Sanschagrin F, Levesque RC, (2003) Structure and function of the Mur enzymes: development of novel inhibitors. Mol Microbiol 47: 1-12.
16. Pratviel-Sosa F, Acher F, Trigalo F, Blanot D, Azerad R, et al. (1994) Effect of various analogues of D-glutamic acid on the D-glutamate-adding enzyme from Escherichia coli. FEMS Microbiol Lett 115: 223-228.
17. Simčič M, Hodošček M, Humljan J, Kristan K, Urleb U, et al. (2009) NMR and molecular dynamics study of the binding mode of naphthalene-N-sulfonyl-D-glutamic acid derivatives: novel MurD ligase inhibitors. J Med Chem 52: 2899-2908.
18. Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton NJ (2007) Larger proteins and molecular interactions. In: Protein NMR spectroscopy: principles and practice, second edition. San Diego: Academic press. 725-780.
19. Tomašić T, Zidar N, Kovač A, Turk S, Simčič M, et al. (2010) 5-benzylidenethiazolidin-4-ones as multitarget inhibitors of bacterial Mur ligases. ChemMedChem 5: 286-295.
20. Xu XP, Case D, (2001) Automated prediction of 15N, 13Cα, 13Cβ and 13C chemical shifts in proteins using a density functional database. J Biomol NMR 21: 321-333.
21. Tugarinov V, Kanelis V, Kay LE, (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 1: 749-754.
22. Bouhss A, Dementin S, Parquet C, Mengin-Lecreulx D, Bertrand JA, et al. (1999) Role of the ortholog and paralog amino acid invariants in the active site of the UDP-MurNAc-L-alanine:D-glutamate ligase (MurD). Biochemistry 38: 12240-12247.
23. Lanzetta PA, Alvarez LJ, Reinach PS, Candia OA, (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100: 95-97.
24. Kristan K, Kotnik M, Oblak M, Urleb U, (2009) New high-throughput fluorimetric assay for discovering inhibitors of UDP-N-acetylmuramyl-L-alanine: D-glutamate (MurD) ligase. J Biomol Screen 14: 412-418.
25. Mayer M, Meyer B, (2001) Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J Am Chem Soc 123: 6108-6117.
26. Yan J, Kline AD, Mo H, Shapiro MJ, Zartler ER, (2003) The effect of relaxation on the epitope mapping by saturation transfer difference NMR. J Magn Reson 163: 270-276.
27. Hwang TL, Shaka AJ, (1995) Water suppresion that works. Excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J Magn Reson 112: 275-279.
28. Dalvit C, (1998) Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules. J Biomol NMR 11: 437-444.
29. McCullough C, Wang M, Rong L, Caffrey M, (2012) Characterization of influenza hemagglutinin interactions with receptor by NMR. PLoS ONE 7: e33958.
30. Clore GM, Gronenborn AM, (1982) Theory and applications of the transferred nuclear overhauser effect to the study of the conformations of small ligands bound to proteins. J Magn Reson 48: 402-417.
31. Clore GM, Gronenborn AM, (1983) Theory of the time dependent transferred nuclear Overhauser effect: Applications to structural analysis of ligand-protein complexes in solution. J Magn Reson 53: 423-442.
32. Thrippleton MJ, Keeler J, (2003) Elimination of zero-quantum interference in two-dimensional NMR spectra. Angew Chem Int Ed Engl 115: 4068-4071.
33. Kay L, Keifer P, Saarinen T, (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114: 10663-10665.
34. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
35. Goddard TD, Kneller DG (2008) SPARKY 3, University of California, San Francisco.
36. Borštnik U, Hodošček M, Janežič D, (2004) Improving the performance of molecular dynamics simulations on parallel clusters. J Chem Inf Comput Sci 44: 359-364.
37. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, et al. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4: 187-217.
38. MacKerell AD, Bashford D, Bellott, Dunbrack RL, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
39. Mackerell AD, Feig M, Brooks CL, (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25: 1400-1415.
40. Vanommeslaeghe K, Hatcher E, Acharya C, Kundu S, Zhong S, et al. (2009) CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 31: 671-690.
41. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 30: 2785-2791.
42. Humphrey W, Dalke A, Schulten K, (1996) VMD: Visual molecular dynamics. J Mol Graph 14: 33-38.