Identification and characterization of the metal ion-dependent l-alanoyl-d-glutamate peptidase encoded by bacteriophage T5

FEBS Journal

Volumn 276, Issue 24, 2009, Pages 7329-7342

  Mikoulinskaia, Galina V ^a   Odinokova, Irina V ^b   Zimin, Andrei A ^c   Lysanskaya, Valentina Ya ^c   Feofanov, Sergei A ^a   Stepnaya, Olga A ^c  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^c SKRYABIN INSTITUTE OF BIOCHEMISTRY AND PHYSIOLOGY OF MICROORGANISMS   (Russian Federation)

Author keywords

Bacteriophage T5; Endolysin; Gram negative; Holin; L alanoyl d glutamate peptidase

Indexed keywords

ALANOYL DEXTRO GLUTAMATE PEPTIDASE; BUFFER; CALCIUM CHLORIDE; EDETIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; HYDROLASE; MANGANESE CHLORIDE; METAL ION; PEPTIDASE; PEPTIDOGLYCAN; UNCLASSIFIED DRUG; VIRUS ENZYME; ZINC;

ARTICLE; BACTERIAL CELL; BACTERIOPHAGE T5; COLIPHAGE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ELECTROPHORESIS; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME REACTIVATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PECTOBACTERIUM CAROTOVORUM; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEUS MIRABILIS; PROTEUS VULGARIS; PSEUDOMONAS PUTIDA; VIRUS GENE; VIRUS INFECTION; VIRUS VIRULENCE;

AMINO ACID SEQUENCE; BACTERIOLYSIS; CALCIUM CHLORIDE; CHLORIDES; CLONING, MOLECULAR; EDETIC ACID; EGTAZIC ACID; ENDOPEPTIDASES; MANGANESE COMPOUNDS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; PEPTIDOGLYCAN; PROTEASE INHIBITORS; SEQUENCE ALIGNMENT; SIPHOVIRIDAE; SUBSTRATE SPECIFICITY; VIRAL PROTEINS;

ESCHERICHIA COLI; NEGIBACTERIA; PECTOBACTERIUM CAROTOVORUM; PROTEUS MIRABILIS; PROTEUS VULGARIS; PSEUDOMONAS PUTIDA;

EID: 71949115542     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07443.x     Document Type: Article

References (54)

1. Young R (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56, 430 481.
2. Bernhardt TG, Wang IN, Struck DK Young R (2002) Breaking free: 'protein antibiotics' and phage lysis. Res Microbiol 153, 493 501.
3. Xu M, Struck DK, Deaton J, Wang IN Young R (2004) A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci USA 101, 6415 6420.
4. Borysowski J, Weber-Dabrowska B Górski A (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med (Maywood) 231, 366 377.
5. Loessner MJ (2005) Bacteriophage endolysins - current state of research and applications. Curr Opin Microbiol 8, 480 487.
6. Pritchard DG, Dong S, Baker JR Engler JA (2004) The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. Microbiology 150, 2079 2087.
7. Düring K, Porsch P, Mahn A, Brinkmann O Gieffers W (1999) The non-enzymatic microbicidal activity of lysozymes. FEBS Lett 449, 93 100.
8. Deutsch SM, Guezenec S, Piot M, Foster S Lortal S (2004) Mur-LH, the broad-spectrum endolysin of Lactobacillus helveticus temperate bacteriophage phi-0303. Appl Environ Microbiol 70, 96 103.
9. Zimmer M, Vukov N, Scherer S Loessner MJ (2002) The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol 68, 5311 5317.
10. Nelson D, Loomis L Fischetti VA (2001) Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc Natl Acad Sci USA 98, 4107 4112.
11. Schuch R, Nelson D Fischetti VA (2002) A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418, 884 889.
12. Djurkovic S, Loeffler JM Fischetti VA (2005) Synergistic killing of Streptococcus pneumoniae with the bacteriophage lytic enzyme Cpl-1 and penicillin or gentamicin depends on the level of penicillin resistance. Antimicrob Agents Chemother 49, 1225 1228.
13. de Ahrenholtz I, Harms K, de Vries J Wackernagel W (2000) Increased killing of Bacillus subtilis on the hair roots of transgenic T4 lysozyme-producing potatoes. Appl Environ Microbiol 66, 1862 1865.
14. Mikoulinskaia GV, Zimin AA, Feofanov SA Miroshnikov AI (2004) Identification, cloning, and expression of bacteriophage T5 dnk gene encoding a broad specificity deoxyribonucleoside monophosphate kinase (EC 2.7.4.13). Protein Expr Purif 33, 166 175.
15. Caldentey J Bamford DH (1992) The lytic enzyme of the Pseudomonas phage phi 6. Purification and biochemical characterization. Biochim Biophys Acta 1159, 44 50.
16. Aballay A, Sarrouf MN, Colombo MI, Stahl PD Mayorga LS (1995) Zn2+ depletion blocks endosome fusion. Biochem J 312, 919 923.
17. Britigan BE, Rasmussen GT Cox CD (1998) Binding of iron and inhibition of iron-dependent oxidative cell injury by the 'calcium chelator' 1,2-bis(2-aminophenoxy)ethane n,n,n′,n′-tetraacetic acid (BAPTA). Biochem Pharmacol 55, 287 295.
18. Auld DS (1988) Use of chelating agents to inhibit enzymes. Methods Enzymol 158, 110 114.
19. Auld DS (1995) Removal and replacement of metal ions in metallopeptidases. Methods Enzymol 248, 228 242.
20. Schleifer KH Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36, 407 477.
21. Quintela JC, Caparrós M de Pedro MA (1995) Variability of peptidoglycan structural parameters in gram-negative bacteria. FEMS Microbiol Lett 125, 95 100.
22. Bonhivers M Letellier L (1995) Calcium controls phage T5 infection at the level of the Escherichia coli cytoplasmic membrane. FEBS Lett 374, 169 173.
23. Moyer RW Buchanan JM (1970) Effect of calcium ions on synthesis of T5-specific ribonucleic acid. J Biol Chem 245, 5904 5913.
24. Moyer RW Buchanan JM (1970) Effect of calcium ions on synthesis of T5-specific proteins. J Biol Chem 245, 5897 5903.
25. Danielsen EM, Noren O, Sjostrom H, Ingram J Kenny AJ (1980) Aspartate aminopeptidase: purification by immunoadsorbent chromatography and properties of the detergent- and proteinase-solubilized forms. Biochem J 189, 591 603.
26. Goto Y, Hattori A, Mizutani S Tsujimoto M (2007) Aspartic acid 221 is critical in the calcium-induced modulation of the enzymatic activity of human aminopeptidase A. J Biol Chem 282, 37074 37081.
27. Claperon C, Rozenfeld R, Iturrioz X, Inguimbert N, Okada M, Roques B, Maigret B Llorens-Cortes C (2008) Asp218 participates with Asp213 to bind a Ca2+ atom into the S1 subsite of aminopeptidase A: a key element for substrate specificity. Biochem J 416, 37 46.
28. Korndörfer IP, Kanitz A, Danzer J, Zimmer M, Loessner MJ Skerra A (2008) Structural analysis of the l-alanoyl-d-glutamate endopeptidase domain of Listeria bacteriophage endolysin Ply500 reveals a new member of the LAS peptidase family. Acta Crystallogr 64, 644 650.
29. Loessner MJ, Wendlinger G Scherer S (1995) Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol Microbiol 16, 1231 1241.
30. Fukushima T, Yao Y, Kitajima T, Yamamoto H Sekiguchi J (2007) Characterization of new L,D-endopeptidase gene product CwlK (previous YcdD) that hydrolyzes peptidoglycan in Bacillus subtilis. Mol Genet Genomics 278, 371 383.
31. Loessner MJ, Kramer K, Ebel F Scherer S (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44, 335 349.
32. Rawlings ND Barrett AJ (1995) Evolutionary families of metallopeptidases. Methods Enzymol 248, 183 228.
33. Wang J Cooper MD (1993) Histidine residue in the zinc-binding motif of aminopeptidase A is critical for enzymatic activity. Proc Natl Acad Sci USA 90, 1222 1226.
34. Larsen KS Auld DS (1989) Carboxypeptidase A: mechanism of zinc inhibition. Biochemistry 28, 9620 9625.
35. Martín AC, López R García P (1998) Functional analysis of the two-gene lysis system of the pneumococcal phage Cp-1 in homologous and heterologous host cells. J Bacteriol 180, 210 217.
36. Summer EJ, Berry J, Tran TA, Niu L, Struck DK Young R (2007) Rz/Rz1 lysis gene equivalents in phages of Gram-negative hosts. J Mol Biol 373, 1098 1112.
37. Brunel F, Thi VH, Pilaete MF Davison J (1983) Transcription regulatory elements in the late region of bacteriophage T5 DNA. Nucleic Acids Res 11, 7649 7658.
38. Wang J, Jiang Y, Vincent M, Sun Y, Yu H, Wang J, Bao Q, Kong H Hu S (2005) Complete genome sequence of bacteriophage T5. Virol 332, 45 65.
39. McPheeters DS, Christensen A, Young ET, Stormo G Gold L (1986) Translational regulation of expression of the bacteriophage T4 lysozyme gene. Nucleic Acids Res 14, 5813 5826.
40. Fiedler F (1988) Biochemistry of the cell surface of Listeria strains: a locating general view. Infection 16, 592 597.
41. Ananou S, Gálvez A, Martínez-Bueno M, Maqueda M Valdivia E (2005) Synergistic effect of enterocin AS-48 in combination with outer membrane permeabilizing treatments against Escherichia coli O157:H7. J App. Microbiol 99, 1364 1372.
42. Rapoport N, Smirnov AI, Timoshin A, Pratt AM Pitt WG (1997) Factors affecting the permeability of Pseudomonas aeruginosa cell walls toward lipophilic compounds: effects of ultrasound and cell age. Arch Biochem Biophys 344, 114 124.
43. Besson F, Peypoux F, Quentin MJ Michel G (1984) Action of antifungal peptidolipids from Bacillus subtilis on the cell membrane of Saccharomyces cerevisiae. J Antibiot(Tokyo) 37, 172 177.
44. Begunova EA, Stepnaia OA, Tsfasman IM Kulaev IS (2004) The effect of the extracellular bacteriolytic enzymes of Lysobacter sp. on gram-negative bacteria. Microbiology (Russia) 73, 320 325.
45. Streshinskaia GM, Naumova IB Panina LI (1979) Chemical composition of the cell wall of Streptomyces chrysomallus which produces the antibiotic aurantin. Microbiology (Russia) 48, 814 819.
46. Riordan JF Vallee BL (1967) Acetylation. Methods Enzymol 11, 565 570.
47. Ward JB (1973) The chain length of the glycans in bacterial cell walls. Biochem J 133, 395 398.
48. Park KT Johnson MJ (1949) A submicrodetermination of glucose. J Biol Chem 181, 149 151.
49. Ghuysen JM, Tipper DJ Strominger JL (1966) Enzymes that degrade bacterial cell walls. Methods Enzymol 8, 685 711.
50. 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.
51. Laemmli UK (1968) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 170, 5259 5268.
52. Jeanmougin F, Thompson JD, Gouy M, Higgins DG Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23, 403 405.
53. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389 3402.
54. Tamura K, Dudley J, Nei M Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596 1599.