Analysis of the peptidoglycan hydrolase complement of lactobacillus casei and characterization of the major γ-D-Glutamyl-L-Lysyl-endopeptidase

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Regulski, Krzysztof ^a   Courtin, Pascal ^a   Meyrand, Mickael ^a   Claes, Ingmar J J ^b   Lebeer, Sarah ^b,d   Vanderleyden, Jos ^b   Hols, Pascal ^c   Guillot, Alain ^a   Chapot Chartier, Marie Pierre ^a  

^a UMR1319 MICALIS   (France)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; DISACCHARIDE; GAMMA DEXTRO GLUTAMYL LYSYL ENDOPEPTIDASE; MONOMER; OLIGOMER; PEPTIDOGLYCAN; PEPTIDOGLYCAN HYDROLASE; PROTEIN P75; PROTEINASE; TETRAPEPTIDE; TRIPEPTIDE; UNCLASSIFIED DRUG; COMPLEMENT; GAMMA D GLUTAMYL L LYSYL ENDOPEPTIDASE, LACTOBACILLUS CASEI; GAMMA-D-GLUTAMYL-L-LYSYL-ENDOPEPTIDASE, LACTOBACILLUS CASEI; LYSYL ENDOPEPTIDASE; N ACETYLMURAMOYLALANINE AMIDASE; PEPTIDE; SERINE PROTEINASE;

AMINO ACID SEQUENCE; ARTICLE; CELL GROWTH; CELL SEPARATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; COMPUTER MODEL; CONTROLLED STUDY; DAUGHTER CELL; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME SYNTHESIS; GENE SEQUENCE; GENETIC TRANSCRIPTION; HYDROLYSIS; INTESTINE EPITHELIUM; LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; LIQUID CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; ZYMOGRAPHY; BACTERIAL GENOME; BIOLOGICAL MODEL; BIOLOGY; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; METHODOLOGY; MUTATION; PHENOTYPE; PROTEOMICS;

BACTERIA (MICROORGANISMS); LACTOBACILLUS CASEI; LACTOBACILLUS RHAMNOSUS; POSIBACTERIA;

CHROMATOGRAPHY, LIQUID; COMPLEMENT SYSTEM PROTEINS; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; GENETIC COMPLEMENTATION TEST; GENOME, BACTERIAL; HYDROLYSIS; LACTOBACILLUS CASEI; MODELS, BIOLOGICAL; MUTATION; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PEPTIDES; PHENOTYPE; PROTEOMICS; SERINE ENDOPEPTIDASES; TANDEM MASS SPECTROMETRY; TRANSCRIPTION, GENETIC;

EID: 84857572926     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032301     Document Type: Article

References (41)

1. Vollmer W, Blanot D, de Pedro MA, (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32: 149-167.
2. Vollmer W, Joris B, Charlier P, Foster S, (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32: 259-286.
3. Chapot-Chartier M-P, (2010) Bacterial autolysins. In: König H, Claus H, Varna A, editors. Prokaryotic Cell Wall Compounds Berlin, Heidelberg, Germany Springer Verlag pp. 383-406 editor.
4. Corthesy B, Gaskins HR, Mercenier A, (2007) Cross-talk between probiotic bacteria and the host immune system. J Nutr 137: 781S-790S.
5. Lebeer S, Vanderleyden J, De Keersmaecker SC, (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8: 171-184.
6. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, et al. (2007) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13: 236-243.
7. Rochat T, Bermudez-Humaran L, Gratadoux JJ, Fourage C, Hoebler C, et al. (2007) Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb Cell Fact 6: 22.
8. Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M, (2009) Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology 128: e858-869.
9. Macho-Fernandez E, Valenti V, Rockel C, Hermann C, Pot B, et al. (2011) Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60: 1050-1059.
10. Maze A, Boel G, Zuniga M, Bourand A, Loux V, et al. (2010) Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J Bacteriol 192: 2647-2648.
11. Steen A, Buist G, Leenhouts KJ, El Khattabi M, Grijpstra F, et al. (2003) Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J Biol Chem 278: 23874-23881.
12. Whisstock JC, Lesk AM, (1999) SH3 domains in prokaryotes. Trends Biochem Sci 24: 132-133.
13. Rappsilber J, Ryder U, Lamond AI, Mann M, (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231-1245.
14. Seth A, Yan F, Polk DB, Rao RK, (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294: G1060-1069.
15. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, et al. (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575.
16. Bauerl C, Perez-Martinez G, Yan F, Polk DB, Monedero V, (2010) Functional analysis of the p40 and p75 proteins from Lactobacillus casei BL23. J Mol Microbiol Biotechnol 19: 231-241.
17. Lambert JM, Bongers RS, Kleerebezem M, (2007) Cre-lox-Based System for Multiple Gene Deletions and Selectable-Marker Removal in Lactobacillus plantarum. Appl Environ Microbiol 73: 1126-1135.
18. Bernard E, Rolain T, Courtin P, Guillot A, Langella P, et al. (2011) Characterization of O-acetylation of N-acetylglucosamine: a novel structural variation of bacterial peptidoglycan. J Biol Chem 286: 23950-23958.
19. Nagaoka M, Muto M, Nomoto K, Matuzaki T, Watanabe T, et al. (1990) Structure of polysaccharide-peptidoglycan complex from the cell wall of Lactobacillus casei YIT9018. J Biochem 108: 568-571.
20. Claes I, Schoofs G, Regulski K, Courtin P, Chapot-Chartier M-P, et al. (2012) Genetic and biochemical characterization of the cell wall hydrolase activity of the major secreted protein of Lactobacillus rhamnosus GG. Plos One doi:10.1371/journal.pone.0031588.
21. Layec S, Decaris B, Leblond-Bourget N, (2008) Diversity of Firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation. Res Microbiol 159: 507-515.
22. Asong J, Wolfert MA, Maiti KK, Miller D, Boons GJ, (2009) Binding and Cellular Activation Studies Reveal That Toll-like Receptor 2 Can Differentially Recognize Peptidoglycan from Gram-positive and Gram-negative Bacteria. J Biol Chem 284: 8643-8653.
23. Girardin SE, Travassos LH, Herve M, Blanot D, Boneca IG, et al. (2003) Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 278: 41702-41708.
24. Humann J, Lenz LL, (2009) Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J Innate Immun 1: 88-97.
25. Chaput C, Ecobichon C, Cayet N, Girardin SE, Werts C, et al. (2006) Role of AmiA in the morphological transition of Helicobacter pylori and in immune escape. PLoS Pathog 2: e97.
26. Humann J, Bjordahl R, Andreasen K, Lenz LL, (2007) Expression of the p60 autolysin enhances NK cell activation and is required for Listeria monocytogenes expansion in IFN-gamma-responsive mice. J Immunol 178: 2407-2414.
27. Beganovic J, Guillot A, van de Guchte M, Jouan A, Gitton C, et al. (2010) Characterization of the insoluble proteome of Lactococcus lactis by SDS-PAGE LC-MS/MS leads to the identification of new markers of adaptation of the bacteria to the mouse digestive tract. J Proteome Res 9: 677-688.
28. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272.
29. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning: a laboratory manual, 2nd ed Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
30. Dower WJ, Miller JF, Ragsdale CW, (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16: 6127-6145.
31. Aukrust TW, Brurberg MB, Nes IF, (1995) Transformation of Lactobacillus by electroporation. Methods Mol Biol 47: 201-208.
32. Sperandio B, Polard P, Ehrlich DS, Renault P, Guedon E, (2005) Sulfur amino acid metabolism and its control in Lactococcus lactis IL1403. J Bacteriol 187: 3762-3778.
33. Fontaine L, Dandoy D, Boutry C, Delplace B, de Frahan MH, et al. (2010) Development of a versatile procedure based on natural transformation for marker-free targeted genetic modification in Streptococcus thermophilus. Appl Environ Microbiol 76: 7870-7877.
34. Bryan EM, Bae T, Kleerebezem M, Dunny GM, (2000) Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44: 183-190.
35. de Ruyter PG, Kuipers OP, de Vos WM, (1996) Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62: 3662-3667.
36. Huard C, Miranda G, Wessner F, Bolotin A, Hansen J, et al. (2003) Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology 149: 695-705.
37. Courtin P, Miranda G, Guillot A, Wessner F, Mezange C, et al. (2006) Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an L,D-carboxypeptidase involved in peptidoglycan maturation. J Bacteriol 188: 5293-5298.
38. Meyrand M, Boughammoura A, Courtin P, Mezange C, Guillot A, et al. (2007) Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 153: 3275-3285.
39. Veiga P, Piquet S, Maisons A, Furlan S, Courtin P, et al. (2006) Identification of an essential gene responsible for D-Asp incorporation in the Lactococcus lactis peptidoglycan crossbridge. Mol Microbiol 62: 1713-1724.
40. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
41. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.