Structural and Functional Characterization of Enantiomeric Glutamic Acid Derivatives as Potential Transition State Analogue Inhibitors of MurD Ligase

Journal of Molecular Biology

Volumn 370, Issue 1, 2007, Pages 107-115

  Kotnik, Miha ^a   Humljan, Jan ^a   Contreras Martel, Carlos ^b   Oblak, Marko ^a   Kristan, Katja ^a   Hervé, Mireille ^c   Blanot, Didier ^c   Urleb, Uroš ^a   Gobec, Stanislav ^d   Dessen, Andréa ^b   Solmajer, Tom ^a,e  

^a Lek dd   (Slovenia)

^b CEA GRENOBLE   (France)

^c IBBMC   (France)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

^e NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

crystal structure; drug design; inhibitor; kinetic study; Mur ligase

Indexed keywords

DEXTRO GLUTAMIC ACID; GLUTAMIC ACID DERIVATIVE; LIGASE; LIGASE INHIBITOR; MURD LIGASE; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; CRYSTAL STRUCTURE; ENANTIOMER; ENZYME INHIBITION; ENZYME INHIBITOR COMPLEX; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS);

EID: 34249703449     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.048     Document Type: Article

References (44)

1. van Heijenoort J. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nature Prod. Rep. 18 (2001) 503-519
2. Mol C.D., Brooun A., Dougan D.R., Hilgers M.T., Tari L.W., Wijnands R.A., et al. Crystal structures of active fully assembled substrate- and product-bound complexes of UDP-N-acetylmuramic acid:l-alanine ligase (MurC) from Haemophilus influenzae. J. Bacteriol. 185 (2003) 4152-4162
3. Spraggon G., Schwarzenbacher R., Kreusch A., Lee C.C., Abdubek P., Ambing E., et al. Crystal structure of an UDP-N-acetylmuramate-alanine ligase MurC (TM0231) from Thermotoga maritima at 2.3 Å resolution. Proteins: Struct. Funct. Bioinf. 55 (2004) 1078-1081
4. Bertrand J.A., Auger G., Fanchon E., Martin L., Blanot D., van Heijenoort J., and Dideberg O. Crystal structure of UDP-N-acetylmuramoyl-l-alanine:d-glutamate ligase from Escherichia coli. EMBO J. 16 (1997) 3416-3425
5. Bertrand J.A., Auger G., Martin L., Fanchon E., Blanot D., Le Beller D., et al. Determination of the MurD mechanism through crystallographic analysis of enzyme complexes. J. Mol. Biol. 289 (1999) 579-590
6. Bertrand J.A., Fanchon E., Martin L., Chantalat L., Auger G., Blanot D., et al. "Open" structures of MurD: domain movements and structural similarities with folylpolyglutamate synthetase. J. Mol. Biol. 301 (2000) 1257-1266
7. Gordon E., Flouret B., Chantalat L., van Heijenoort J., Mengin-Lecreulx D., and Dideberg O. Crystal structure of UDP-N-acetylmuramoyl-l-alanyl-d-glutamate: meso-diaminopimelate ligase from Escherichia coli. J. Biol. Chem. 276 (2001) 10999-11006
8. Yan Y., Munshi S., Leiting B., Anderson M.S., Chrzas J., and Chen Z. Crystal structure of Escherichia coli UDPMurNAc-tripeptide d-alanyl-d-alanine-adding enzyme (MurF) at 2.3 Å resolution. J. Mol. Biol. 304 (2000) 435-445
9. Longenecker K.L., Stamper G.F., Hajduk P.J., Fry E.H., Jakob C.G., Harlan J.E., et al. Structure of MurF from Streptococcus pneumoniae co-crystallized with a small molecule inhibitor exhibits interdomain closure. Protein Sci. 14 (2005) 3039-3047
10. Deva T., Baker E.N., Squire C.J., and Smith C.A. Structure of Escherichia coli UDP-N-acetylmuramoyl:l-alanine ligase (MurC). Acta Crystallog. sect. D 62 (2006) 1466-1474
11. Ikeda M., Wachi M., Jung H.K., Ishino F., and Matsunashi M. Homology among MurC, MurD, MurE and MurF proteins in Escherichia coli and that between Escherichia coli MurG and a possible MurG protein in Bacillus subtilis. J. Gen. Appl. Microbiol. 36 (1990) 179-187
12. Bouhss A., Dementin S., Parquet C., Mengin-Lecreulx D., Bertrand J.A., Le Beller D., et al. 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 (1999) 12240-12247
13. Eveland S.S., Pompliano D.L., and Anderson M.S. Conditionally lethal Escherichia coli murein mutants contain point defects that map to regions conserved among murein and folyl poly-γ-glutamate ligases: identification of a ligase superfamily. Biochemistry 36 (1997) 6223-6229
14. Vaganay S., Tanner M.E., van Heijenoort J., and Blanot D. Study of the reaction mechanism of the d-glutamic acid-adding enzyme from Escherichia coli. Microb. Drug Resist. 2 (1996) 51-54
15. Bouhss A., Dementin S., van Heijenoort J., Parquet C., and Blanot D. MurC and MurD synthetases of peptidoglycan biosynthesis: borohydride trapping of acyl-phosphate intermediates. Methods Enzymol. 354 (2002) 189-196
16. Liger D., Masson A., Blanot D., van Heijenoort J., and Parquet C. Study of the overproduced uridine-diphosphate-N-acetylmuramate:l-alanine ligase from Escherichia coli. Microb. Drug Resist. 2 (1996) 25-27
17. Falk P.J., Ervin K.M., Volk K.S., and Ho H.T. Biochemical evidence for the formation of a covalent acyl-phosphate linkage between UDP-N-acetylmuramate and ATP in the Escherichia coli UDP-N-acetylmuramate:l-alanine ligase-catalyzed reaction. Biochemistry 35 (1996) 1417-1422
18. Emanuele Jr. J.J., Jin H., Yanchunas Jr. J., and Villafranca J.J. Evaluation of the kinetic mechanism of Escherichia coli uridine diphosphate-N-acetylmuramate:l-alanine ligase. Biochemistry 36 (1997) 7264-7271
19. Anderson M.S., Eveland S.S., Onishi H.R., and Pompliano D.L. Kinetic mechanism of the Escherichia coli UDPMurNAc-tripeptide d-alanyl-d-alanine-adding enzyme: use of a glutathione S-transferase fusion. Biochemistry 35 (1996) 16264-16269
20. Perdih, A., Kotnik, M., Hodoscek, M. & Solmajer, T. (2007). Targeted molecular dynamics (TMD) simulation studies of binding and conformational changes in E. coli Mur D. Proteins: Struct. Funct. Bioinf. 68 [Electronic publication ahead of print].
21. Michaud C., Blanot D., Flouret B., and van Heijenoort J. Partial purification and specificity studies of the d-glutamate-adding and d-alanyl-d-alanine-adding enzymes from Escherichia coli K12. Eur. J. Biochem. 166 (1987) 631-637
22. Pratviel-Sosa F., Acher F., Trigalo F., Blanot D., Azerad R., and van Heijenoort J. Effect of various analogues of d-glutamic acid on the d-glutamate-adding enzyme from Escherichia coli. FEMS Microbiol. Letters 115 (1994) 223-228
23. Tanner M.E., Vaganay S., van Heijenoort J., and Blanot D. Phosphinate inhibitors of the d-glutamic acid-adding enzyme of peptidoglycan biosynthesis. J. Org. Chem. 61 (1996) 1756-1760
24. Gegnas L.D., Waddell S.T., Chabin R.M., Reddy S., and Wong K.K. Inhibitors of the bacterial cell wall biosynthesis enzyme MurD. Bioorg. Med. Chem. Letters 8 (1998) 1643-1648
25. Gobec S., Urleb U., Auger G., and Blanot D. Synthesis and biochemical evaluation of some novel N-acyl phosphono- and phosphinoalanine derivatives as potential inhibitors of the d-glutamic acid-adding enzyme. Pharmazie 56 (2001) 295-297
26. Štrancar K., Blanot D., and Gobec S. Design, synthesis and structure-activity relationships of new phosphinate inhibitors of MurD. Bioorg. Med. Chem. Letters 16 (2006) 343-348
27. Auger G., van Heijenoort J., Blanot D., and Deprun C. Synthesis of N-acetylmuramic acid derivatives as potential inhibitors of the d-glutamic acid adding enzyme. J. Prakt. Chem. 337 (1995) 351-357
28. Humljan J., Kotnik M., Boniface A., Solmajer T., Urleb U., Blanot D., and Gobec S. A new approach towards peptidosulfonamides: synthesis of potential inhibitors of bacterial peptidoglycan biosynthesis enzymes MurD and MurE. Tetrahedron 62 (2006) 10980-10988
29. Štrancar K., Boniface A., Blanot D., and Gobec S. Phosphinate inhibitors of UDP-N-acetylmuramoyl-l-alanyl-d-glutamate:l-lysine ligase (MurE). Arch. Pharm. Chem. Life Sci. 340 (2007) 127-134
30. Pratviel-Sosa F., Mengin-Lecreulx D., and van Heijenoort J. Over-production, purification and properties of the uridine diphosphate N-acetylmuramoyl-l-alanine:d-glutamate ligase from Escherichia coli. Eur. J. Biochem. 202 (1991) 1169-1176
31. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallog. sect. D 60 (2004) 432-438
32. Dementin S., Bouhss A., Auger G., Parquet C., Mengin-Lecreulx D., Dideberg O., et al. Evidence of a functional requirement for a carbamoylated lysine residue in MurD, MurE and MurF synthetases as established by chemical rescue experiments. Eur. J. Biochem. 268 (2001) 5800-5807
33. Walsh A.W., Falk P.J., Thanassi J., Discotto L., Pucci M.J., and Ho H.T. Comparison of the d-glutamate-adding enzymes from selected Gram-positive and Gram-negative bacteria. J. Bacteriol. 181 (1999) 5395-5401
34. Purdie J.E., Demayo R.E., Seely J.H., and Benoiton N. L. The trypsin-catalysed hydrolysis of d-lysine and d-arginine ethyl esters. Biochim. Biophys. Acta 268 (1972) 523-526
35. Sanborn B.M., and Hein G.E. The interaction of trypsin with neutral substrates and modifiers. Biochemistry 7 (1968) 3616-3624
36. Auger G., Martin L., Bertrand J., Ferrari P., Fanchon E., Vaganay S., et al. Large-scale preparation, purification, and crystallization of UDP-N-acetylmuramoyl-l-alanine: d-glutamate ligase from Escherichia coli. Protein Expr. Purif. 13 (1998) 23-29
37. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
38. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 26 (1993) 795-800
39. Emsley P., and Cowtan K. COOT: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
40. Murshudov G., Vagin A., and Dodson E. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
41. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
42. Cohen S.X., Morris R.J., Fernandez F.J., Ben Jelloul M., Kakaris M., Parthasarathy V., et al. Towards complete validated models in the next generation of ARP/wARP. Acta Crystallog. sect. D 60 (2004) 2222-2229
43. Laskowsky R., McArthur M., Moss D., and Thornton J. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-294
44. SYBYL 7.3, Tripos Inc., 1699 South Hanley Rd., St. Louis, Missouri, 63144, USA.