Structure and function of the first full-length murein peptide ligase (Mpl) cell wall recycling protein

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Das, Debanu ^a,b   Hervé, Mireille ^c,d   Feuerhelm, Julie ^a,e   Farr, Carol L ^a,f   Chiu, Hsiu Ju ^a,b   Elsliger, Marc André ^a,f   Knuth, Mark W ^a,e   Klock, Heath E ^a,e   Miller, Mitchell D ^a,b   Godzik, Adam ^a,g,h   Lesley, Scott A ^a,e,f   Deacon, Ashley M ^a,b   Mengin Lecreulx, Dominique ^c,d   Wilson, Ian A ^a,f  

^a Joint Center for Structural Genomics (http://wwwjcsgorg)   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d CNRS   (France)

^e GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MAGNESIUM; MUREIN PEPTIDE LIGASE; PEPTIDOGLYCAN; TRIPEPTIDE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLMURAMIC ACID; PEPTIDE SYNTHASE; UDP N ACETYLMURAMOYLALANYL D GLUTAMATE 2,6 DIAMINOPIMELATE LIGASE; UDP-N-ACETYLMURAMOYLALANYL-D-GLUTAMATE-2,6-DIAMINOPIMELATE LIGASE;

ARTICLE; BACTERIAL CELL WALL; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME SUBSTRATE COMPLEX; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PH MEASUREMENT; PROTEIN FUNCTION; PSYCHROBACTER; PSYCHROBACTER ARCTICUS; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; TEMPERATURE SENSITIVITY; AMINO ACID SEQUENCE; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; VALIDATION STUDY; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSYCHROBACTER; PSYCHROBACTER ARCTICUS 273-4;

AMINO ACID SEQUENCE; CELL WALL; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE SYNTHASES; PROTEIN CONFORMATION; PSYCHROBACTER; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 79952783663     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017624     Document Type: Article

References (66)

1. Vollmer W, Blanot D, de Pedro MA, (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32: 149-167.
2. Schneider T, Sahl HG, (2010) An oldie but a goodie- cell wall biosynthesis as antibiotic target pathway. Int J Med Microbiol 300: 161-169.
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. Bouhss A, Trunkfield AE, Bugg TD, Mengin-Lecreulx D, (2008) The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32: 208-233.
5. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P, (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32: 234-258.
6. Mengin-Lecreulx D, van Heijenoort J, Park JT, (1996) 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 178: 5347-5352.
7. Eveland SS, Pompliano DL, Anderson MS, (1997) Conditionally lethal Escherichia coli murein mutants contain point defects that map to regions conserved among murein and folyl poly-gamma-glutamate ligases: identification of a ligase superfamily. Biochemistry 36: 6223-6229.
8. Bouhss A, Mengin-Lecreulx D, Blanot D, van Heijenoort J, Parquet C, (1997) 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 36: 11556-11563.
9. Bouhss A, Dementin S, van Heijenoort J, Parquet C, Blanot D, (2002) MurC and MurD synthetases of peptidoglycan biosynthesis: borohydride trapping of acyl-phosphate intermediates. Methods Enzymol 354: 189-196.
10. Smith CA, (2006) Structure, function and dynamics in the mur family of bacterial cell wall ligases. J Mol Biol 362: 640-655.
11. Park JT, Uehara T, (2008) How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 72: 211-227.
12. Vollmer W, Joris B, Charlier P, Foster S, (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32: 259-286.
13. Hervé M, Boniface A, Gobec S, Blanot D, Mengin-Lecreulx D, (2007) Biochemical characterization and physiological properties of Escherichia coli UDP-N-acetylmuramate:L-alanyl-gamma-D-glutamyl-meso-diaminopimelate ligase. J Bacteriol 189: 3987-3995.
14. Kotnik M, Anderluh PS, Prezelj A, (2007) Development of novel inhibitors targeting intracellular steps of peptidoglycan biosynthesis. Curr Pharm Des 13: 2283-2309.
15. Basavannacharya C, Robertson G, Munshi T, Keep NH, Bhakta S, (2010) ATP-dependent MurE ligase in Mycobacterium tuberculosis: biochemical and structural characterisation. Tuberculosis (Edinb) 90: 16-24.
16. Deva T, Baker EN, Squire CJ, Smith CA, (2006) Structure of Escherichia coli UDP-N-acetylmuramoyl:L-alanine ligase (MurC). Acta Crystallogr D Biol Crystallogr 62: 1466-1474.
17. Spraggon G, Schwarzenbacher R, Kreusch A, Lee CC, Abdubek P, et al. (2004) Crystal structure of an Udp-n-acetylmuramate-alanine ligase MurC (TM0231) from Thermotoga maritima at 2.3 Å resolution. Proteins 55: 1078-1081.
18. Mol CD, Brooun A, Dougan DR, Hilgers MT, Tari LW, et al. (2003) 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: 4152-4162.
19. Klock HE, Koesema EJ, Knuth MW, Lesley SA, (2008) Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts. Proteins 71: 982-994.
20. Van Duyne GD, Standaert RF, Karplus PA, Schreiber SL, Clardy J, (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229: 105-124.
21. Santarsiero BD, Yegian DT, Lee CC, Spraggon G, Gu J, et al. (2002) An approach to rapid protein crystallization using nanodroplets. J Appl Crystallogr 35: 278-281.
22. Lesley SA, Kuhn P, Godzik A, Deacon AM, Mathews I, et al. (2002) Structural genomics of the Thermotoga maritima proteome implemented in a high-throughput structure determination pipeline. Proc Natl Acad Sci U S A 99: 11664-11669.
23. Cohen AE, Ellis PJ, Miller MD, Deacon AM, Phizackerley RP, (2002) An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot. J Appl Crystallogr pp. 720-726.
24. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, et al. (2002) Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 9: 401-406.
25. Leslie AGW, (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4+ESF-EAMCB Newsletter on Protein Crystallography 26.
26. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
27. Sheldrick GM, (2008) A short history of SHELX. Acta Crystallogr A 64: 112-122.
28. Vonrhein C, Blanc E, Roversi P, Bricogne G, (2007) Automated structure solution with autoSHARP. Methods Mol Biol 364: 215-230.
29. Abrahams JP, Leslie AG, (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr D Biol Crystallogr 52: 30-42.
30. Langer G, Cohen SX, Lamzin VS, Perrakis A, (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3: 1171-1179.
31. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
32. Winn MD, Murshudov GN, Papiz MZ, (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 374: 300-321.
33. Cruickshank DW, (1999) Remarks about protein structure precision. Acta Crystallogr D Biol Crystallogr 55: 583-601.
34. Yang H, Guranovic V, Dutta S, Feng Z, Berman HM, et al. (2004) Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank. Acta Crystallogr D Biol Crystallogr 60: 1833-1839.
35. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
36. Vriend G, (1990) WHAT IF: a molecular modeling and drug design program. J Mol Graph 8: 52-56, 29.
37. Vaguine AA, Richelle J, Wodak SJ, (1999) SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D Biol Crystallogr 55: 191-205.
38. Terwilliger TC, (2000) Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
39. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
40. Kleywegt GJ, (2000) Validation of protein crystal structures. Acta Crystallogr D Biol Crystallogr 56: 249-265.
41. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
42. Laskowski RA, Chistyakov VV, Thornton JM, (2005) PDBsum more: new summaries and analyses of the known 3D structures of proteins and nucleic acids. Nucleic Acids Res 33: D266-268.
43. DeLano WL, (2008) The PyMOL Molecular Graphics System. USA DeLano Scientific LLC, Palo Alto, CA.
44. Babič A, Pečar S, (2007) An improved total synthesis of UDP-N-acetyl-muramic acid. Tetrahedron Lett 48: 4403-4405.
45. Babič A, Patin D, Boniface A, Hervé M, Mengin-Lecreulx D, et al. (2007) Chemoenzymatic synthesis of the nucleotide substrates of the Mur ligases. In: Kikelj D, editors. Bologna, Italy Medimond Srl pp. 1-4 5th Joint Meeting on Medicinal Chemistry, June 17-21, Portoroz, Slovenia.
46. Sachs H, Brand E, (1953) Optical rotation of peptides, VII. α-and γ-dipeptides of glutamic acid and alanine. J Am Chem Soc 75: 4608-4610.
47. Schmidt DM, Hubbard BK, Gerlt JA, (2001) Evolution of enzymatic activities in the enolase superfamily: functional assignment of unknown proteins in Bacillus subtilis and Escherichia coli as L-Ala-D/L-Glu epimerases. Biochemistry 40: 15707-15715.
48. Girardin SE, Travassos LH, Hervé M, Blanot D, Boneca IG, et al. (2003) Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 278: 41702-41708.
49. Blanot D, Kretsovali A, Abo-Ghalia M, Mengin-Lecreulx D, van Heijenoort J, (1983) Synthesis of analogues of precursors of bacterial peptidoglycan. Peptides 1982: 311-314.
50. Pennartz A, Genereux C, Parquet C, Mengin-Lecreulx D, Joris B, (2009) Substrate-induced inactivation of the Escherichia coli AmiD N-acetylmuramoyl-L-alanine amidase highlights a new strategy to inhibit this class of enzyme. Antimicrob Agents Chemother 53: 2991-2997.
51. Laemmli UK, Johnson RA, (1973) Maturation of the head of bacteriophage T4. II. Head-related, aberrant tau-particles. J Mol Biol 80: 601-611.
52. Bolanos-Garcia VM, Davies OR, (2006) Structural analysis and classification of native proteins from E. coli commonly co-purified by immobilised metal affinity chromatography. Biochim Biophys Acta 1760: 1304-1313.
53. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
54. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-288.
55. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
56. Gouet P, Robert X, Courcelle E, (2003) ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 31: 3320-3323.
57. Matthews BW, (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497.
58. 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.
59. Ye Y, Godzik A, (2005) Multiple flexible structure alignment using partial order graphs. Bioinformatics 21: 2362-2369.
60. Jin H, Emanuele JJ Jr, Fairman R, Robertson JG, Hail ME, et al. (1996) Structural studies of Escherichia coli UDP-N-acetylmuramate:L-alanine ligase. Biochemistry 35: 1423-1431.
61. Wallace AC, Laskowski RA, Thornton JM, (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127-134.
62. Bellamacina CR, (1996) The nicotinamide dinucleotide binding motif: a comparison of nucleotide binding proteins. Faseb J 10: 1257-1269.
63. Dementin S, Bouhss A, Auger G, Parquet C, Mengin-Lecreulx D, et al. (2001) 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: 5800-5807.
64. Gordon E, Flouret B, Chantalat L, van Heijenoort J, Mengin-Lecreulx D, et al. (2001) Crystal structure of UDP-N-acetylmuramoyl-L-alanyl-D-glutamate: meso-diaminopimelate ligase from Escherichia coli. J Biol Chem 276: 10999-11006.
65. Lugtenberg EJ, (1972) Studies on Escherichia coli enzymes involved in the synthesis of uridine diphosphate-N-acetyl-muramyl-pentapeptide. J Bacteriol 110: 26-34.
66. Gomez MJ, Neyfakh AA, (2006) Genes involved in intrinsic antibiotic resistance of Acinetobacter baylyi. Antimicrob Agents Chemother 50: 3562-3567.