1887

Abstract

is an opportunistic pathogen responsible for nosocomial infections. Lipoproteins in Gram-positive bacteria are translocated across the plasma membrane and anchored by the fatty acid group. They perform critical roles, with some described as virulence determinants. The aim of this study was to explore the roles of lipoproteins in the stress response and virulence. We constructed a mutant affected in the predicted prolipoprotein diacylglyceryl transferase gene , and examined the role of Lgt in membrane anchoring, growth, the stress response and virulence. Inactivation of enhanced growth in a high concentration of Mn or under oxidative stress , and significantly decreased virulence.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.055319-0
2012-03-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/3/816.html?itemId=/content/journal/micro/10.1099/mic.0.055319-0&mimeType=html&fmt=ahah

References

  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. [CrossRef] [PubMed]
    [Google Scholar]
  2. Beauchamp C. , Fridovich I. . ( 1971; ). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. . Anal Biochem 44:, 276–287. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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.[PubMed] [CrossRef]
    [Google Scholar]
  12. Hermans P. W. M. , Adrian P. V. , Albert C. , Estevão 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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  15. Kovacs-Simon A. , Titball R. W. , Michell S. L. . ( 2011; ). Lipoproteins of bacterial pathogens. . Infect Immun 79:, 548–561. [CrossRef] [PubMed]
    [Google Scholar]
  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.[PubMed] [CrossRef]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  18. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  21. Low Y. L. , Jakubovics N. S. , Flatman J. C. , Jenkinson H. F. , Smith A. W. . ( 2003; ). Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis . . J Med Microbiol 52:, 113–119. [CrossRef] [PubMed]
    [Google Scholar]
  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.[PubMed] [CrossRef]
    [Google Scholar]
  23. Maguin E. , Duwat P. , Hege T. , Ehrlich D. , Gruss A. . ( 1992; ). New thermosensitive plasmid for Gram-positive bacteria. . J Bacteriol 174:, 5633–5638.[PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  27. Murray B. E. . ( 1990; ). The life and times of the Enterococcus . . Clin Microbiol Rev 3:, 46–65.[PubMed]
    [Google Scholar]
  28. Nguyen H. T. , Wolff K. A. , Cartabuke R. H. , Ogwang S. , Nguyen L. . ( 2010; ). A lipoprotein modulates activity of the MtrAB two-component system to provide intrinsic multidrug resistance, cytokinetic control and cell wall homeostasis in Mycobacterium . . Mol Microbiol 76:, 348–364. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  31. Prousek J. . ( 2007; ). Fenton chemistry in biology and medicine. . Pure Appl Chem 79:, 2325–2338. [CrossRef]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  35. Sambrook J. , Fritsch E. F. , Maniatis T. . ( 1989; ). Molecular Cloning: a Laboratory Manual, , 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  36. Sava I. G. , Heikens E. , Huebner J. . ( 2010; ). Pathogenesis and immunity in enterococcal infections. . Clin Microbiol Infect 16:, 533–540. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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.[PubMed] [CrossRef]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  44. Terzaghi B. E. , Sandine W. E. . ( 1975; ). Improved medium for lactic streptococci and their bacteriophages. . Appl Microbiol 29:, 807–813.[PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
  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. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.055319-0
Loading
/content/journal/micro/10.1099/mic.0.055319-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error