1887

Abstract

is the causative agent in a wide range of diseases of humans of varying severity. During a study scanning the genome sequence of a serotype M1 invasive isolate SF370 for novel surface proteins, an ORF, designated , was identified. The putative protein encoded by contains both a signal peptide and classic Gram-positive wall-associated sequences. Comparison of the sequences of this ORF with those from a number of unrelated isolates demonstrated that encodes a putative surface protein with a variable N-terminal sequence followed by a variable length tract of collagen-like GXY repeats. A further feature of is the presence of CAAAA repeat tracts immediately downstream of the putative start codon. The number of these pentameric repeats varies from 4 to 15 between strains and variation in repeat number results in the predicted SclB protein being either in or out of frame relative to the start codon. These observations suggest that expression of this protein may be regulated at the translational level as a result of gain or loss of CAAAA repeats. While the function of SclB remains to be elucidated, an -specific transcript was detected by RT-PCR during culture. Finally, it is shown that a second gene, , potentially encoding a protein with a similar extensive collagen-like structure and variable N-terminal sequence, is present in all isolates of tested to date. Thus harbours a novel family of structurally related and surface-exposed proteins of potential importance in the pathogenic process.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-2-419
2001-02-01
2022-01-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/2/1470419a.html?itemId=/content/journal/micro/10.1099/00221287-147-2-419&mimeType=html&fmt=ahah

References

  1. Beall B., Facklam R., Thompson T. 1996; Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol 34:953–958
    [Google Scholar]
  2. Beck K., Brodsky B. 1998; Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil. J Structural Biol 122:17–29 [CrossRef]
    [Google Scholar]
  3. van Belkum A., Scherer S., van Alphen L., Verbrugh H. 1998; Short-sequence DNA repeats in prokaryotic genomes. Microbiol Mol Biol Rev 62:275–293
    [Google Scholar]
  4. van Belkum A., van Leeuwen W., Scherer S., Verbrugh H. 1999; Occurrence and structure–function relationship of pentameric short sequence repeats in microbial genomes. Res Microbiol 150:617–626 [CrossRef]
    [Google Scholar]
  5. Charalambous B. M., Keen J. N., McPherson M. J. 1988; Collagen-like sequences stabilize homotrimers of a bacterial hydrolase. EMBO J 7:2903–2909
    [Google Scholar]
  6. Chen C. C., Cleary P. P. 1990; Complete nucleotide sequence of the streptococcal C5a peptidase gene of Streptococcus pyogenes. J Biol Chem 265:3161–3167
    [Google Scholar]
  7. Chou P. Y., Fasman G. D. 1978; Prediction of secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol 47:45–148
    [Google Scholar]
  8. Courtney H. S., Hasty D. L., Li Y., Chiang H. C., Thacker J. L., Dale J. B. 1999; Serum opacity factor is a major fibronectin-binding protein and a virulence determinant of M type 2 Streptococcus pyogenes. Mol Microbiol 32:89–98 [CrossRef]
    [Google Scholar]
  9. Cunningham M. W. 2000; Pathogenesis of Group A streptococcal infections. Clin Microbiol Rev 13:470–511 [CrossRef]
    [Google Scholar]
  10. Dev I. K., Ray P. H. 1990; Signal peptidases and signal peptide hydrolases. J Bioenerg Biomembr 22:271–290 [CrossRef]
    [Google Scholar]
  11. Engvall E., Ruoslahti E., Miller J. M. 1978; Affinity of fibronectin to collagen of different genetic types and to fibrinogen. J Exp Med 147:1584–1595 [CrossRef]
    [Google Scholar]
  12. Erickson P. R., Herzberg M. C. 1993; The Streptococcus sanguis platelet aggregation-associated protein. Identification and characterization of the minimal platelet-interactive domain. J Biol Chem 268:1646–1649
    [Google Scholar]
  13. Fischetti V. A., Pancholi V., Schneewind O. 1990; Conservation of a hexapeptide sequence in the anchor region of surface proteins from Gram-positive cocci. Mol Microbiol 4:1603–1605 [CrossRef]
    [Google Scholar]
  14. Frick I. M., Crossin K. L., Edelman G. M., Björck L. 1995; Protein H – a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains. EMBO J 14:1674–1679
    [Google Scholar]
  15. Garnier J., Osguthorpe D. J., Robson B. 1978; Analysis of the accuracy and implications of a simple method for predicting the secondary structure of globular proteins. J Mol Biol 120:97–120 [CrossRef]
    [Google Scholar]
  16. Goodfellow A. M., Hibble M., Talay S. R., Kreikemeyer B., Currie B. J., Sriprakash K. S., Chhatwal G. S. 2000; Distribution and antigenicity of fibronectin binding proteins (SfbI and SfbII) of Streptococcus pyogenes clinical isolates from the Northern Territory, Australia. J Clin Microbiol 38:389–392
    [Google Scholar]
  17. Harbaugh M. P., Podbielski A., Hügl S., Cleary P. P. 1993; Nucleotide substitutions and small-scale insertion produce size and antigenic variation in Group A streptococcal M1 protein. Mol Microbiol 8:981–991 [CrossRef]
    [Google Scholar]
  18. von Heijne G. 1990; The signal peptide. J Membr Biol 115:195–201 [CrossRef]
    [Google Scholar]
  19. Henderson I. R., Owen P., Nataro J. P. 1999; Molecular switches – the ON and OFF of bacterial phase variation. Mol Microbiol 33:919–932 [CrossRef]
    [Google Scholar]
  20. Hollingshead S. K., Fischetti V. A., Scott J. R. 1987; Size variation in group A streptococcal M protein is generated by homologous recombination between intragenic repeats. Mol Gen Genetics 207:196–203 [CrossRef]
    [Google Scholar]
  21. Hynes W. L., Hancock L., Ferretti J. J. 1995; Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immun 63:3015–3020
    [Google Scholar]
  22. Jenkinson H. F., Lamont R. J. 1997; Streptococcal adhesion and colonization. Crit Rev Oral Biol Med 8:175–200 [CrossRef]
    [Google Scholar]
  23. Joh D., Wann E. R., Kreikemeyer B., Speziale P., Höök M. 1999; Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol 18:211–223 [CrossRef]
    [Google Scholar]
  24. Johnsson E., Berggard K., Kotarsky H., Hellwage J., Zipfel P. F., Sjobring U., Lindahl G. 1998; Role of the hypervariable region in streptococcal M proteins: binding of a human complement inhibitor. J Immunol 161:4894–4901
    [Google Scholar]
  25. Jones D. T. 1999; Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292:195–202 [CrossRef]
    [Google Scholar]
  26. Jones K. F., Hollingshead S. K., Scott J. R., Fischetti V. A. 1988; Spontaneous M6 protein size mutants of group A streptococci display variation in antigenic and opsonogenic epitopes. Proc Natl Acad Sci USA 85:8271–8275 [CrossRef]
    [Google Scholar]
  27. Kehoe M. A. 1994; Cell-wall-associated proteins in Gram-positive bacteria. In Bacterial Cell Wall pp. 217–261Edited by Ghuysen J.-M., Hakenbeck R. Amsterdam: Elsevier Science;
    [Google Scholar]
  28. Kreikemeyer B., Talay S. R., Chhatwal G. S. 1995; Characterisation of a novel fibronectin-binding surface protein in group A streptococci. Mol Microbiol 17:137–145 [CrossRef]
    [Google Scholar]
  29. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132 [CrossRef]
    [Google Scholar]
  30. Lindmark H., Guss B. 1999; SFS, a novel fibronectin-binding protein from Streptococcus equi, inhibits the binding between fibronectin and collagen. Infect Immun 67:2383–2388
    [Google Scholar]
  31. Madoff L. C., Michel J. L., Gond 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 USA 93:4131–4136 [CrossRef]
    [Google Scholar]
  32. 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]
  33. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6 [CrossRef]
    [Google Scholar]
  34. Podbielski A., Hawlitzky J., Pack T. D., Flosdorff A., Boyle M. D. 1994; A group A streptococcal Enn protein potentially resulting from intergenomic recombination exhibits atypical immunoglobulin binding characteristics. Mol Microbiol 12:725–736 [CrossRef]
    [Google Scholar]
  35. Rakonjac J. V., Robbins J. C., Fischetti V. A. 1995; DNA sequence of the serum opacity factor of group A streptococci: identification of a fibronectin-binding repeat domain. Infect Immun 63:622–631
    [Google Scholar]
  36. Reichardt W., Gubbe K., Schmidt K. H. 1995; M3 protein with close sequence homology to M12 protein binds fibrinogen, albumin, fibronectin but not to any subclass of IgG – localisation of binding regions. Dev Biol Stand 85:179–182
    [Google Scholar]
  37. Roe B. A., Linn S. P., Song L., Yuan X., Clifton S., McLaughlin R. E., McShan M., Ferretti J. 1999; Streptococcal Genome Sequencing Project. http://wwwgenomeouedu/strephtml
  38. Saunders N. J., Peden J. F., Hood D. W., Moxon E. R. 1998; Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27:1091–1098 [CrossRef]
    [Google Scholar]
  39. Saunders N. J., Jeffries A. C., Peden J. F., Hood D. W., Tettelin H., Rappuoli R., Moxon E. R. 2000; Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37:207–215 [CrossRef]
    [Google Scholar]
  40. Schneewind O., Jones K. F., Fischetti V. A. 1990; Sequence and structural characteristics of the trypsin-resistant T6 surface protein of group A streptococci. J Bacteriol 172:3310–3317
    [Google Scholar]
  41. Sela S., Aviv A., Tovi A., Burstein I., Caparon M. G., Hanski E. 1993; Protein F: an adhesin of Streptococcus pyogenes bindings fibronectin via two distinct domains. Mol Microbiol 10:1049–1055 [CrossRef]
    [Google Scholar]
  42. Smith N. H., Maynard Smith J., Spratt B. G. 1995; Sequence evolution of the porB gene of Neisseria gonorrhoeae and Neisseria meningitidis; evidence of positive Darwinian selection. Mol Biol Evol 12:363–370
    [Google Scholar]
  43. Stern A., Brown M., Nickel P., Meyer T. 1986; Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61–71 [CrossRef]
    [Google Scholar]
  44. Stibitz S., Aaronson W., Monack D., Falkow S. 1989; Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338:266–269 [CrossRef]
    [Google Scholar]
  45. Talay S. R., Valentin-Weigand P., Timmis K. N., Chhatwal G. S. 1994; Domain structure and conserved epitopes of Sfb protein, the fibronectin binding adhesin of Streptococcus pyogenes. Mol Microbiol 13:531–539 [CrossRef]
    [Google Scholar]
  46. Whatmore A. M., Kehoe M. A. 1994; Horizontal gene transfer in the evolution of group A streptococcal emm-like genes: gene mosaics and variation in the Vir regulon. Mol Microbiol 11:363–374 [CrossRef]
    [Google Scholar]
  47. Whatmore A. M., Kapur V., Sullivan D. J., Musser J. M., Kehoe M. A. 1994; Noncongruent relationships between variation in emm gene sequences and the population genetic structure of group A streptococci. Mol Microbiol 14:619–631 [CrossRef]
    [Google Scholar]
  48. Whatmore A. M., Kapur V., Musser J. M., Kehoe M. A. 1995; Molecular population genetic analysis of the enn subdivision of group A streptococcal emm-like genes: horizontal gene transfer and restricted variation among enn genes. Mol Microbiol 15:1039–1048 [CrossRef]
    [Google Scholar]
  49. Yother J., Briles D. E. 1992; Structural properties and evolutionary relationships of PspA, a surface protein of Streptococcus pneumoniae as revealed by sequence analysis. J Bacteriol 174:601–609
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-2-419
Loading
/content/journal/micro/10.1099/00221287-147-2-419
Loading

Data & Media loading...

Most cited this month 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