The prolipoprotein diacylglyceryl transferase (Lgt) of Enterococcus faecalis contributes to virulence

Microbiology

Volumn 158, Issue 3, 2012, Pages 816-825

  Reffuveille, Fany ^a   Serror, Pascale ^b   Chevalier, Sylvie ^c   Budin Verneuil, Aurélie ^a   Ladjouzi, Rabia ^a   Bernay, Benoit ^d   Auffray, Yanick ^a   Rincé, Alain ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b UMR1319 MICALIS   (France)

^c UNIVERSITÉ DE ROUEN   (France)

^d UNIVERSITÉ DE CAEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LIPOPROTEIN; MANGANESE; PROLIPOPROTEIN DIACYLGLYCERYL TRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL MEMBRANE; ENTEROCOCCUS FAECALIS; GENE INACTIVATION; HOSPITAL INFECTION; IN VITRO STUDY; LGT GENE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STRESS;

ANIMALS; DISEASE MODELS, ANIMAL; ENTEROCOCCUS FAECALIS; GENE DELETION; GENETIC COMPLEMENTATION TEST; GRAM-POSITIVE BACTERIAL INFECTIONS; LARVA; LEPIDOPTERA; MANGANESE; SURVIVAL ANALYSIS; TRANSFERASES; VIRULENCE; VIRULENCE FACTORS;

ENTEROCOCCUS FAECALIS; POSIBACTERIA;

EID: 84857711626     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.055319-0     Document Type: Article

References (48)

1. Baumgärtner, M., Kärst, U., Gerstel, B., Loessner, M., Wehland, J. & Jänsch, L. (2007). Inactivation of Lgt allows systematic characterization of lipoproteins from Listeria monocytogenes. J Bacteriol 189, 313-324.
2. Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44, 276-287.
3. Bizzini, A., Zhao, C., Budin-Verneuil, A., Sauvageot, N., Giard, J.-C., Auffray, Y. & Hartke, A. (2010). Glycerol is metabolized in a complex and strain-dependent manner in Enterococcus faecalis. J Bacteriol 192, 779-785.
4. Bradford, M. M. (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.
5. Bray, B. A., Sutcliffe, I. C. & Harrington, D. J. (2009). Impact of lgt mutation on lipoprotein biosynthesis and in vitro phenotypes of Streptococcus agalactiae. Microbiology 155, 1451-1458.
6. Bubeck Wardenburg, J., Williams, W. A. & Missiakas, D. (2006). Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A 103, 13831-13836.
7. Clewell, D. B., An, F. Y., Flannagan, S. E., Antiporta, M. & Dunny, G. M. (2000). Enterococcal sex pheromone precursors are part of signal sequences for surface lipoproteins. Mol Microbiol 35, 246-247.
8. Cron, L. E., Bootsma, H. J., Noske, N., Burghout, P., Hammerschmidt, S. & Hermans, P. W. (2009). Surface-associated lipoprotein PpmA of Streptococcus pneumoniae is involved in colonization in a strain-specific manner. Microbiology 155, 2401-2410.
9. Hamilton, A., Robinson, C., Sutcliffe, I. C., Slater, J., Maskell, D. J., Davis-Poynter, N., Smith, K., Waller, A. & Harrington, D. J. (2006). Mutation of the maturase lipoprotein attenuates the virulence of Streptococcus equi to a greater extent than does loss of general lipoprotein lipidation. Infect Immun 74, 6907-6919.
10. Hancock, L. E. & Gilmore, M. S. (2002). The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc Natl Acad Sci U S A 99, 1574-1579.
11. Henneke, P., Dramsi, S., Mancuso, G., Chraibi, K., Pellegrini, E., Theilacker, C., Hübner, J., Santos-Sierra, S., Teti, G. & other authors (2008). Lipoproteins are critical TLR2 activating toxins in group B streptococcal sepsis. J Immunol 180, 6149-6158.
12. Hermans, P. W. M., Adrian, P. V., Albert, C., Estevã o, S., Hoogenboezem, T., Luijendijk, I. H. T., Kamphausen, T. & Hammerschmidt, S. (2006). The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J Biol Chem 281, 968-976.
13. Hutchings, M. I., Palmer, T., Harrington, D. J. & Sutcliffe, I. C. (2009). Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends Microbiol 17, 13-21.
14. Kontinen, V. P. & Sarvas, M. (1993). The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol Microbiol 8, 727-737.
15. Kovacs-Simon, A., Titball, R. W. & Michell, S. L. (2011). Lipoproteins of bacterial pathogens. Infect Immun 79, 548-561.
16. Kurokawa, K., Lee, H., Roh, K. B., Asanuma, M., Kim, Y. S., Nakayama, H., Shiratsuchi, A., Choi, Y., Takeuchi, O. & other authors (2009). The triacylated ATP binding cluster transporter substrate-binding lipoprotein of Staphylococcus aureus functions as a native ligand for the Toll-like receptor 2. J Biol Chem 284, 8406-8411.
17. La Carbona, S., Sauvageot, N., Giard, J.-C., Benachour, A., Posteraro, B., Auffray, Y., Sanguinetti, M. & Hartke, A. (2007). Comparative study of the physiological roles of three peroxidases (NADH peroxidase, alkyl hydroperoxide reductase and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 66, 1148-1163.
18. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
19. Lebreton, F., Riboulet-Bisson, E., Serror, P., Sanguinetti, M., Posteraro, B., Torelli, R., Hartke, A., Auffray, Y. & Giard, J.-C. (2009). ace, which encodes an adhesin in Enterococcus faecalis, is regulated by Ers and is involved in virulence. Infect Immun 77, 2832-2839.
20. Leskelä, S., Wahlström, E., Kontinen, V. P. & Sarvas, M. (1999). Lipid modification of prelipoproteins is dispensable for growth but essential for efficient protein secretion in Bacillus subtilis: characterization of the lgt gene. Mol Microbiol 31, 1075-1085.
21. Low, Y. L., Jakubovics, N. S., Flatman, J. C., Jenkinson, H. F. & Smith, A. W. (2003). Manganese-dependent regulation of the endocarditisassociated virulence factor EfaA of Enterococcus faecalis. J Med Microbiol 52, 113-119.
22. Machata, S., Tchatalbachev, S., Mohamed, W., Jänsch, L., Hain, T. & Chakraborty, T. G. (2008). Lipoproteins of Listeria monocytogenes are critical for virulence and TLR2-mediated immune activation. J Immunol 181, 2028-2035.
23. Maguin, E., Duwat, P., Hege, T., Ehrlich, D. & Gruss, A. (1992). New thermosensitive plasmid for Gram-positive bacteria. J Bacteriol 174, 5633-5638.
24. Meijerink, J., Mandigers, C., van de Locht, L., Tönnissen, E., Goodsaid, F. & Raemaekers, J. (2001). A novel method to compensate for different amplification efficiencies between patient DNA samples in quantitative real-time PCR. J Mol Diagn 3, 55-61.
25. Morsczeck, C., Prokhorova, T., Sigh, J., Pfeiffer, M., Bille-Nielsen, M., Petersen, J., Boysen, A., Kofoed, T., Frimodt-Møller, N. & other authors (2008). Streptococcus pneumoniae: proteomics of surface proteins for vaccine development. Clin Microbiol Infect 14, 74-81.
26. Muller, C., Le Breton, Y., Morin, T., Benachour, A., Auffray, Y. & Rincé, A. (2006). The response regulator CroR modulates expression of the secreted stress-induced SalB protein in Enterococcus faecalis. J Bacteriol 188, 2636-2645.
27. Murray, B. E. (1990). The life and times of the Enterococcus. Clin Microbiol Rev 3, 46-65.
28. Nguyen, H. T., Wolff, K. A., Cartabuke, R. H., Ogwang, S. & Nguyen, L. (2010). A lipoprotein modulates activity of the MtrAB twocomponent system to provide intrinsic multidrug resistance, cytokinetic control and cell wall homeostasis in Mycobacterium. Mol Microbiol 76, 348-364.
29. Paulsen, I. T., Banerjei, L., Myers, G. S., Nelson, K. E., Seshadri, R., Read, T. D., Fouts, D. E., Eisen, J. A., Gill, S. R. & other authors (2003). Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299, 2071-2074.
30. Petit, C. M., Brown, J. R., Ingraham, K., Bryant, A. P. & Holmes, D. J. (2001). Lipid modification of prelipoproteins is dispensable for growth in vitro but essential for virulence in Streptococcus pneumoniae. FEMS Microbiol Lett 200, 229-233.
31. Prousek, J. (2007). Fenton chemistry in biology and medicine. Pure Appl Chem 79, 2325-2338.
32. Qin, X., Singh, K. V., Weinstock, G. M. & Murray, B. E. (2000). Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68, 2579-2586.
33. Reffuveille, F., Leneveu, C., Chevalier, S., Auffray, Y. & Rincé, A. (2011). Lipoproteins of Enterococcus faecalis: bioinformatic identification, expression analysis and relation to virulence. Microbiology 157, 3001-3013.
34. Riboulet-Bisson, E., Sanguinetti, M., Budin-Verneuil, A., Auffray, Y., Hartke, A. & Giard, J.-C. (2008). Characterization of the Ers regulon of Enterococcus faecalis. Infect Immun 76, 3064-3074.
35. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
36. Sava, I. G., Heikens, E. & Huebner, J. (2010). Pathogenesis and immunity in enterococcal infections. Clin Microbiol Infect 16, 533-540.
37. Schmaler, M., Jann, N. J., Ferracin, F., Landolt, L. Z., Biswas, L., Götz, F. & Landmann, R. (2009). Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J Immunol 182, 7110-7118.
38. Shin, H. S., Xu, F., Bagchi, A., Herrup, E., Prakash, A., Valentine, C., Kulkarni, H., Wilhelmsen, K., Warren, S. & Hellman, J. (2011). Bacterial lipoprotein TLR2 agonists broadly modulate endothelial function and coagulation pathways in vitro and in vivo. J Immunol 186, 1119-1130.
39. Singh, K. V., Coque, T. M., Weinstock, G. M. & Murray, B. E. (1998). In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21, 323-331.
40. Stoll, H., Dengjel, J., Nerz, C. & Götz, F. (2005). Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect Immun 73, 2411-2423.
41. Sutcliffe, I. C. & Harrington, D. J. (2002). Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes. Microbiology 148, 2065-2077.
42. Sutcliffe, I. C. & Harrington, D. J. (2004). Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol Rev 28, 645-659.
43. Tendolkar, P. M., Baghdayan, A. S. & Shankar, N. (2003). Pathogenic enterococci: new developments in the 21st century. Cell Mol Life Sci 60, 2622-2636.
44. Terzaghi, B. E. & Sandine, W. E. (1975). Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 29, 807-813.
45. Thompson, B. J., Widdick, D. A., Hicks, M. G., Chandra, G., Sutcliffe, I. C., Palmer, T. & Hutchings, M. I. (2010). Investigating lipoprotein biogenesis and function in the model Gram-positive bacterium Streptomyces coelicolor. Mol Microbiol 77, 943-957.
46. Verneuil, N., Mazé, A., Sanguinetti, M., Laplace, J.-M., Benachour, A., Auffray, Y., Giard, J.-C. & Hartke, A. (2006). Implication of (Mn)superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages. Microbiology 152, 2579-2589.
47. Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P. & Edmond, M. B. (2004). Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39, 309-317.
48. Zhao, C., Hartke, A., La Sorda, M., Posteraro, B., Laplace, J.-M., Auffray, Y. & Sanguinetti, M. (2010). Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect Immun 78, 3889-3897.