1887

Abstract

The role of lipoprotein diacylglyceryl transferase (Lgt) and lipoprotein signal peptidase (Lsp) responsible for processing lipoproteins was investigated in , a common cause of bovine mastitis. In the absence of Lgt, three lipoproteins [MtuA (SUB0473), Hap (SUB1625) and an extracellular solute-binding protein (SUB0365)] were detected in extracellular locations. All were shown by Edman degradation analysis to be cleaved on the carboxy side of the LXXC lipobox. Detection of MtuA, a lipoprotein shown previously to be essential for infectivity and virulence, was used as a surrogate lipoprotein marker to locate and assess processing of lipoproteins. The absence of Lgt did not prevent location of MtuA to the cell membrane, its location in the wild-type strain but, in contrast to the situation with wild-type, did result in a widespread location of this protein. In the absence of both Lgt and Lsp, MtuA was similarly released from the bacterial cell. In such strains, however, the cell-associated MtuA represented the full-length gene product, indicating that Lsp was able to cleave non-lipidated (lipo)proteins but was not responsible for their release from this bacterium.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022061-0
2009-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/1/134.html?itemId=/content/journal/micro/10.1099/mic.0.022061-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Meyers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Antelmann H., Tjalsma H., Voigt B., Ohlmeier S., Bron S., van Dijl J. M., Hecker M. 2001; A proteomic view on genome-based signal peptide predictions. Genome Res 11:1484–1502
    [Google Scholar]
  3. Baumgartner M., Karst U., Gerstel B., Loessner M., Wehland J., Jansch L. 2007; Inactivation of Lgt allows systematic characterization of lipoproteins from Listeria monocytogenes . J Bacteriol 189:313–324
    [Google Scholar]
  4. Braun V., Hantke K. 1975; Characterization of the free form of murein-lipoprotein from the outer membrane of Escherichia coli B/r. FEBS Lett 60:26–28
    [Google Scholar]
  5. 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
    [Google Scholar]
  6. Chattopadhyay P. K., Wu H. C. 1977; Biosynthesis of the covalently linked diglyceride in murein lipoprotein of Escherichia coli . Proc Natl Acad Sci U S A 74:5318–5322
    [Google Scholar]
  7. Dartois V., Djavakhishvili T., Hoch J. A. 1997; KapB is a lipoprotein required for KinB signal transduction and activation of the phosphorelay to sporulation in Bacillus subtilis . Mol Microbiol 26:1097–1108
    [Google Scholar]
  8. Denham E. L., Ward P. N., Leigh J. A. 2008; Lipoprotein signal peptides are processed by Lsp and Eep of Streptococcus uberis . J Bacteriol 190:4641–4647
    [Google Scholar]
  9. Dev I. K., Ray P. H. 1984; Rapid assay and purification of a unique signal peptidase that processes the prolipoprotein from Escherichia coli B. J Biol Chem 259:11114–11120
    [Google Scholar]
  10. Gan K., Gupta S. D., Sankaran K., Schmid M. B., Wu H. C. 1993; Isolation and characterization of a temperature-sensitive mutant of Salmonella typhimurium defective in prolipoprotein modification. J Biol Chem 268:16544–16550
    [Google Scholar]
  11. 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
    [Google Scholar]
  12. Hantke K., Braun V. 1973; Covalent binding of lipid to protein. Diglyceride and amide-linked fatty acid at the N-terminal end of the murein-lipoprotein of the Escherichia coli outer membrane. Eur J Biochem 34:284–296
    [Google Scholar]
  13. Henneke P., Dramsi S., Mancuso G., Chraibi K., Pellegrini E., Theilacker C., Hubner 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
    [Google Scholar]
  14. Hill A. W., Leigh J. A. 1989; DNA fingerprinting of Streptococcus uberis: a useful tool for epidemiology of bovine mastitis. Epidemiol Infect 103:165–171
    [Google Scholar]
  15. Hulo N., Bairoch A., Bulliard V., Cerutti L., De Castro E., Langendijk-Genevaux P. S., Pagni M., Sigrist C. J. 2006; The PROSITE database. Nucleic Acids Res 34:D227–D230
    [Google Scholar]
  16. Hussain M., Ichihara S., Mizushima S. 1982; Mechanism of signal peptide cleavage in the biosynthesis of the major lipoprotein of the Escherichia coli outer membrane. J Biol Chem 257:5177–5182
    [Google Scholar]
  17. Innis M. A., Tokunaga M., Williams M. E., Loranger J. M., Chang S. Y., Chang S., Wu H. C. 1984; Nucleotide sequence of the Escherichia coli prolipoprotein signal peptidase ( lsp) gene. Proc Natl Acad Sci U S A 81:3708–3712
    [Google Scholar]
  18. Inukai M., Ghrayeb J., Nakamura K., Inouye M. 1984; Apolipoprotein, an intermediate in the processing of the major lipoprotein of the Escherichia coli outer membrane. J Biol Chem 259:757–760
    [Google Scholar]
  19. Janulczyk R., Ricci S., Bjorck L. 2003; MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes . Infect Immun 71:2656–2664
    [Google Scholar]
  20. Jones C. L., Monaghan P., Field T. R., Smith A. J., Ward P. N., Leigh J. A. 2004; Localization of MtuA, an LraI homologue in Streptococcus uberis . J Appl Microbiol 97:149–157
    [Google Scholar]
  21. Kontinen V. P., Saris P., Sarvas M. 1991; A gene ( prsA) of Bacillus subtilis involved in a novel, late stage of protein export. Mol Microbiol 5:1273–1283
    [Google Scholar]
  22. Lee N., Yamagata H., Inouye M. 1983; Inhibition of secretion of a mutant lipoprotein across the cytoplasmic membrane by the wild-type lipoprotein of the Escherichia coli outer membrane. J Bacteriol 155:407–411
    [Google Scholar]
  23. Leskela S., Wahlstrom 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
    [Google Scholar]
  24. Machata S., Tchatalbachev S., Mohamed W., Jansch L., Hain T., Chakraborty T. 2008; Lipoproteins of Listeria monocytogenes are critical for virulence and TLR2-mediated immune activation. J Immunol 181:2028–2035
    [Google Scholar]
  25. Maguin E., Prevost H., Ehrlich S. D., Gruss A. 1996; Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol 178:931–935
    [Google Scholar]
  26. 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
    [Google Scholar]
  27. Qi H. Y., Sankaran K., Gan K., Wu H. C. 1995; Structure-function relationship of bacterial prolipoprotein diacylglyceryl transferase: functionally significant conserved regions. J Bacteriol 177:6820–6824
    [Google Scholar]
  28. Reizer J., Hoischen C., Titgemeyer F., Rivolta C., Rabus R., Stulke J., Karamata D., Saier M. H. Jr, Hillen W. 1998; A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 27:1157–1169
    [Google Scholar]
  29. Sankaran K., Wu H. C. 1994; Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J Biol Chem 269:19701–19706
    [Google Scholar]
  30. Sibbald M. J., Ziebandt A. K., Engelmann S., Hecker M., de Jong A., Harmsen H. J., Raangs G. C., Stokroos I., Arends J. P. other authors 2006; Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70:755–788
    [Google Scholar]
  31. Smith A. J., Ward P. N., Field T. R., Jones C. L., Lincoln R. A., Leigh J. A. 2003; MtuA, a lipoprotein receptor antigen from Streptococcus uberis, is responsible for acquisition of manganese during growth in milk and is essential for infection of the lactating bovine mammary gland. Infect Immun 71:4842–4849
    [Google Scholar]
  32. Stoll H., Dengjel J., Nerz C., Gotz F. 2005; Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect Immun 73:2411–2423
    [Google Scholar]
  33. 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
    [Google Scholar]
  34. 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
    [Google Scholar]
  35. Sutcliffe I. C., Russell R. R. 1995; Lipoproteins of gram-positive bacteria. J Bacteriol 177:1123–1128
    [Google Scholar]
  36. Tjalsma H., Kontinen V. P., Pragai Z., Wu H., Meima R., Venema G., Bron S., Sarvas M., van Dijl J. M. 1999a; The role of lipoprotein processing by signal peptidase II in the Gram-positive eubacterium Bacillus subtilis. Signal peptidase II is required for the efficient secretion of alpha-amylase, a non-lipoprotein. J Biol Chem 274:1698–1707
    [Google Scholar]
  37. Tjalsma H., Zanen G., Venema G., Bron S., van Dijl J. M. 1999b; The potential active site of the lipoprotein-specific (type II) signal peptidase of Bacillus subtilis . J Biol Chem 274:28191–28197
    [Google Scholar]
  38. Tokunaga H., Wu H. C. 1984; Studies on the modification and processing of prolipoprotein in Escherichia coli. Effects of structural alterations in prolipoprotein on its maturation in wild type and lpp mutants. J Biol Chem 259:6098–6104
    [Google Scholar]
  39. Tokunaga M., Tokunaga H., Wu H. C. 1982; Post-translational modification and processing of Escherichia coli prolipoprotein in vitro. Proc Natl Acad Sci U S A 79:2255–2259
    [Google Scholar]
  40. Tokunaga M., Loranger J. M., Chang S. Y., Regue M., Chang S., Wu H. C. 1985; Identification of prolipoprotein signal peptidase and genomic organization of the lsp gene in Escherichia coli . J Biol Chem 260:5610–5615
    [Google Scholar]
  41. von Heijne G. 1989; The structure of signal peptides from bacterial lipoproteins. Protein Eng 2:531–534
    [Google Scholar]
  42. Wahlstrom E., Vitikainen M., Kontinen V. P., Sarvas M. 2003; The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis . Microbiology 149:569–577
    [Google Scholar]
  43. Ward P. N., Field T. R., Ditcham W. G., Maguin E., Leigh J. A. 2001; Identification and disruption of two discrete loci encoding hyaluronic acid capsule biosynthesis genes hasA, hasB, and hasC in Streptococcus uberis . Infect Immun 69:392–399
    [Google Scholar]
  44. Yamagata H. 1983; Temperature-sensitive prolipoprotein signal peptidase in an Escherichia coli mutant: use of the mutant for an efficient and convenient assay system. J Biochem 93:1509–1515
    [Google Scholar]
  45. Yamagata H., Ippolito C., Inukai M., Inouye M. 1982; Temperature-sensitive processing of outer membrane lipoprotein in an Escherichia coli mutant. J Bacteriol 152:1163–1168
    [Google Scholar]
  46. Yamaguchi K., Yu F., Inouye M. 1988; A single amino acid determinant of the membrane localization of lipoproteins in E. coli . Cell 53:423–432
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022061-0
Loading
/content/journal/micro/10.1099/mic.0.022061-0
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