1887

Microbiology Society logo

Volume 149, Issue 3

Characterization of novel LPXTG-containing proteins of identified from genome sequences Free

Abstract

Twenty-one genes encoding surface proteins belonging to the LPXTG family have been identified by analysis of six genome sequences. Eleven genes encode previously described proteins, while 10 have not yet been characterized. Of these, eight contain the cell-wall sorting signal LPXTG responsible for covalently anchoring proteins to the cell-wall peptidoglycan. The remaining two, SasF and SasD, harbour a single residue variation in the fourth position of the LPXTG motif (LPXAG). Western blotting of lysostaphin-solubilized . cell-wall proteins demonstrated the release of SasF in the cell-wall fraction, indicating that proteins carrying LPXAG are sorted normally. Analysis of primary sequences of the urface (Sas) proteins indicated that several share a similar structural organization and a common signal sequence with previously characterized LPXTG proteins of . and other Gram-positive cocci. Protein SasG has 128 residue B repeats that are almost identical at the DNA level. PCR analysis indicated that recombinants with repeat length variations are present in the bacterial population whereas they are not detectable in the B-repeat-encoding region of . The and genes are significantly associated with invasive disease isolates compared to nasal carriage isolates. Several IgG samples purified from patients recovering from . infections had higher titres against Sas proteins than control IgG, suggesting that expression occurred during infection in some patients.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): MLST, multilocus sequence typing and Sas, Staphylococcus aureus surface
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25996-0
2003-03-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/3/mic149643.html?itemId=/content/journal/micro/10.1099/mic.0.25996-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F, Madden T. L, Schaffer A. A, Zhang J, Zhang Z, Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
     [Google Scholar]
  2. Bensing B. A., Sullam P. M. 2002; An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44:1081–1094
     [Google Scholar]
  3. Casolini F, Visai L, Joh D, Conaldi P. G, Toniolo A, Höök M., Speziale P. 1998; Antibody response to fibronectin-binding adhesin FnbpA in patients with Staphylococcus aureus infections. Infect Immun 66:5433–5442
     [Google Scholar]
  4. Cucarella C, Solano C, Valle J, Amorena B, Lasa L., Penadés J. R. 2001; Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896
     [Google Scholar]
  5. Deivanayagam C. C, Wann E. R, Chen W, Carson M, Rajashankar K. R, Höök M., Narayana S. V. L. 2002; A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus : crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J 21:6660–6672
     [Google Scholar]
  6. Doolittle R. F. 1995; The multiplicity of domains in proteins. Annu Rev Biochem 64:287–314
     [Google Scholar]
  7. Edman M, Jarhede T, Sjöström M., Wieslander A. 1999; Different sequence patterns in signal peptides from mycoplasmas, other gram-positive bacteria, and Escherichia coli : a multivariate data analysis. Proteins 35:195–205
     [Google Scholar]
  8. Enright M. C, Day N. P. J, Davies C. E, Peacock S. J., Spratt B. J. 2000; Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus . J Clin Microbiol 38:1008–1015
     [Google Scholar]
  9. Enright M. C, Robinson D. A, Randle G, Feil E. J, Grundmann H., Spratt B. G. 2002; The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99:7687–7692
     [Google Scholar]
  10. Etz H, Minh D. B, Henics T. 15 other authors 2002; Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus . Proc Natl Acad Sci U S A 99:6573–6578
     [Google Scholar]
  11. Foster T. J., Höök M. 1998; Surface protein adhesins of Staphylococcus aureus . Trends Microbiol 6:484–488
     [Google Scholar]
  12. Hartford O, Francois P, Vaudaux P., Foster T. J. 1997; The dipeptide repeat region of the fibrinogen-binding protein (clumping factor) is required for functional expression of the fibrinogen-binding domain on the Staphylococcus aureus cell surface. Mol Microbiol 25:1065–1076
     [Google Scholar]
  13. House-Pompeo K, Xu Y, Joh D, Speziale P., Höök M. 1996; Conformational changes in the fibronectin binding MSCRAMMs are induced by ligand binding. J Biol Chem 271:1379–1384
     [Google Scholar]
  14. Janulczyk R., Rasmussen M. 2001; Improved pattern for genome-based screening identifies novel cell wall-attached proteins from Gram-positive bacteria. Infect Immun 69:4019–4016
     [Google Scholar]
  15. Josefsson E, McCrea K. W, Ní Eidhin D, O'Connell D, Cox J, Höök M., Foster T. J. 1998a; Three new members of the serine-aspartate repeat protein multigene family of Staphylococcus aureus . Microbiology 144:3387–3395
     [Google Scholar]
  16. Josefsson E, O'Connell D, Foster T. J, Durussel I., Cox J. A. 1998b; The binding of calcium to the B-repeat segment of SdrD, a cell surface protein of Staphylococcus aureus . J Biol Chem 273:31145–31152
     [Google Scholar]
  17. Josefsson E, Hartford O, O'Brien L, Patti J. M., Foster T. J. 2001; Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis 184:1572–1580
     [Google Scholar]
  18. Komatsuzawa H, Ohta K, Sugai M, Fujiwara T, Glanzmann P, Berger-Bachi B., Suginaka H. 2000; Tn 551 -mediated insertional inactivation of the fmtB gene encoding a cell wall-associated protein abolishes methicillin resistance in Staphylococcus aureus . J Antimicrob Chemother 45:421–431
     [Google Scholar]
  19. Kuroda M, Ohta T, Uchiyama I. 34 other authors 2001; Whole genome sequencing of methicillin-resistant Staphylococcus aureus . Lancet 357:1225–1240
     [Google Scholar]
  20. Madoff L. C, Michel J. L, Gong E. W, Kling D. E., Kasper D. L. 1996; Group B streptococci escape host immunity by deletion of tandem repeat elements of the alpha C protein. Proc Natl Acad Sci U S A 93:4131–4136
     [Google Scholar]
  21. Mazmanian S. K, Lui G, Jensen E. R, Lenoy E., Schneewind O. 2000; Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci U S A 97:5510–5515
     [Google Scholar]
  22. Mazmanian S. K, Ton-That H., Schneewind O. 2001; Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus . Mol Microbiol 40:1049–1057
     [Google Scholar]
  23. Mazmanian S. K, Ton-That H, Su K., Schneewind O. 2002; An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci U S A 99:2293–2298
     [Google Scholar]
  24. McAleese F. M, Walsh E. J, Sieprawska M, Potempa J., Foster T. J. 2001; Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J Biol Chem 276:29969–29978
     [Google Scholar]
  25. McDevitt D., Foster T. J. 1995; Variation in the size of the repeat region of the fibrinogen receptor (clumping factor) of Staphylococcus aureus strains. Microbiology 141:937–943
     [Google Scholar]
  26. McGavin M. J, Gurusiddappa S, Lingren P. E, Lindberg M, Raucci G., Höök M. 1993; Fibronectin receptors from Streptococcus dysgalactiae and Staphylococcus aureus : involvement of conserved residues in ligand binding. J Biol Chem 268:23946–23953
     [Google Scholar]
  27. Navarre W. W., Schneewind O. 1999; Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63:174–229
     [Google Scholar]
  28. Nilsson I. M, Patti J. M, Bremell T, Höök M., Tarkowski A. 1998; Vaccination with a recombinant fragment of the collagen adhesin provides protection against Staphylococcus aureus -mediated septic death. J Clin Invest 101:2640–2649
     [Google Scholar]
  29. Novick R. P. 1967; Properties of a cryptic high frequency transducing phage in Staphylococcus aureus . Virology 33:155–166
     [Google Scholar]
  30. O'Connell D, Nanavaty T, McDevitt D, Gurusiddappa S, Höök M., Foster T. J. 1998; The fibrinogen-binding MSCRAMM (clumping factor) of Staphylococcus aureus has a Ca2+-dependent inhibitory site. J Biol Chem 273:6821–6829
     [Google Scholar]
  31. Pallen M. J, Lam A. C, Antonio M., Dunbar K. 2001; An embarrassment of sortases – a richness of substrates?. Trends Microbiol 9:97–102
     [Google Scholar]
  32. Peacock S. J, Foster T. J, Cameron B. J., Berendt A. R. 1999; Bacterial fibronectin-binding proteins and endothelial cell surface fibronectin mediate adherence of Staphylococcus aureus to resting human endothelial cells. Microbiology 145:3477–3486
     [Google Scholar]
  33. Peacock S. J, Moore C. E, Justice A, Kantzanou M, Story L, Mackie K, O'Neill G., Day N. P. J. 2002; Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus . Infect Immun 70:4987–4996
     [Google Scholar]
  34. Perkins S, Walsh E. J, Deivanayagam C. C. S, Narayana S. V. L, Foster T. J., Höök M. 2001; Structural organization of the fibrinogen-binding region of the clumping factor B MSCRAMM of Staphylococcus aureus . J Biol Chem 276:44721–44728
     [Google Scholar]
  35. Savolainen K, Paulin L, Westerlund-Wikström B, Foster T. J, Korhonen T. K., Kuusela P. 2001; Expression of pls , a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus , prevents bacterial adhesion in vitro . Infect Immun 69:3013–3020
     [Google Scholar]
  36. Shields D. C, McDevitt D., Foster T. J. 1995; Evidence against concerted evolution in a tandem array in the clumping factor gene of Staphylococcus aureus . Mol Biol Evol 12:963–965
     [Google Scholar]
  37. Switalski L. M, Patti J. M, Butcher W, Gristina A. G, Speziale P., Höök M. 1993; A collagen receptor on Staphylococcus aureus strains isolated from patients with septic arthritis mediates adhesion to cartilage. Mol Microbiol 7:99–107
     [Google Scholar]
  38. Taylor J. M., Heinrichs D. E. 2002; Transferrin binding in Staphylococcus aureus : involvement of a cell wall-anchored protein. Mol Microbiol 43:1603–1614
     [Google Scholar]
  39. Tettelin H, Nelson K. E, Paulsen I. T. 39 other authors 2001; Complete genome sequence of a virulent isolate of Streptococcus pneumoniae . Science 293:498–506
     [Google Scholar]
  40. Thompson J. D, Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
     [Google Scholar]
  41. Ton-That H, Lui G, Mazmanian S. K, Faull K. F., Schneewind O. 1999; Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proc Natl Acad Sci U S A 96:12424–12429
     [Google Scholar]
  42. Visai L, Xu Y, Casolini F, Rindi S, Höök M., Speziale P. 2000; Monoclonal antibodies to CNA, a collagen-binding microbial surface component recognizing adhesive matrix molecules, detach Staphylococcus aureus from a collagen substrate. J Biol Chem 275:39837–39845
     [Google Scholar]
  43. Vytvytska O, Nagy E, Bluggel M, Meyer H. E, Kurzbauer R, Huber L. A., Klade C. S. 2002; Identification of vaccine candidate antigens of Staphylococcus aureus by serological proteome analysis. Proteomics 2:580–590
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25996-0
Loading
Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences
Microbiology 149, 643 (2003); https://doi.org/10.1099/mic.0.25996-0
/content/journal/micro/10.1099/mic.0.25996-0
/content/journal/micro/10.1099/mic.0.25996-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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