1887

Abstract

C protein antigen (Bac), a surface protein of group B streptococci (GBS), is known to concurrently bind the Fc portion of IgA and factor H (FH). The authors' previous work has demonstrated that mRNA expression levels show diversity among clonally related strains containing genes () encoding Bac, with high expression noted in invasive strains. In this study, the gene and upstream regions containing putative promoters, three ORFs and an IS insertion sequence were characterized. Three invasive strains showed high expression levels and did not show any notable mutations except one strain producing Bac that was able to bind FH but not IgA. A deletion of 51 amino acid residues, including part of the Bac IgA-binding region, was identified and hypothesized to contribute to the loss of the IgA-binding ability of this strain. A vaginal strain that showed somewhat higher expression levels and produced Bac lacking immunoreactivity contained an 11 bp deletion, which generated a premature termination codon, in the region preceding the IgA-binding region. In another vaginal strain that did not express , disruption of the upstream ORFs of the sensor histidine kinase and DNA-binding response regulator, due to frameshift mutations, was noted although it is not known whether these proteins directly affect expression levels. An IS insertion into the promoter region was found in another vaginal strain that showed low expression levels and produced Bac with a significantly larger proline-rich repeat region. These results demonstrate considerable genetic diversity of the and upstream regions of invasive and noninvasive GBS, which may contribute to the variability of expression levels among those strains.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28535-0
2006-03-01
2020-08-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/3/771.html?itemId=/content/journal/micro/10.1099/mic.0.28535-0&mimeType=html&fmt=ahah

References

  1. Areschoug T, Linse S, Stålhammar-Carlemalm M, Hedén L.-O, Lindahl G. 2002a; A proline-rich region with a highly periodic sequence in streptococcal β protein adopts the polyproline II structure and is exposed on the bacterial surface. J Bacteriol184:6376–6383[CrossRef]
    [Google Scholar]
  2. Areschoug T, Stålhammar-Carlemalm M, Karlsson I, Lindahl G. 2002b; Streptococcal β protein has separate binding sites for human factor H and IgA-Fc. J Biol Chem277:12642–12648[CrossRef]
    [Google Scholar]
  3. Baron M. J, Bolduc G. R, Goldberg M. B, Auperin T. C, Madoff L. C. 2004; Alpha C protein of group B Streptococcus binds host cell surface glycosaminoglycan and enters cells by an actin-dependent mechanism. J Biol Chem279:24714–24723[CrossRef]
    [Google Scholar]
  4. Beckmann C, Waggoner J. D, Harris T. O, Tamura G. S, Rubens C. E. 2002; Identification of novel adhesins from group B streptococci by use of phage display reveals that C5a peptidase mediates fibronectin binding. Infect Immun70:2869–2876[CrossRef]
    [Google Scholar]
  5. Berner R, Ruess M, Bereswill S, Brandis M. 2002; Polymorphisms in the cell wall-spanning domain of the C protein β -antigen in clinical Streptococcus agalactiae isolates are caused by genetic instability of repeating DNA sequences. Pediatr Res51:106–111[CrossRef]
    [Google Scholar]
  6. Blackmore T. K, Fischetti V. A, Higgs N. H, Sadlon T. A, Ward H. M, Gordon D. L. 1998; M protein of the group A streptococcus binds to the seventh short consensus repeat of human complement factor H. Infect Immun66:1427–1431
    [Google Scholar]
  7. Bohnsack J. F, Mollison K. W, Buko A. M, Ashworth J. C, Hill H. R. 1991; Group B streptococci inactivate complement component C5a by enzymic cleavage at the C-terminus. Biochem J273:635–640
    [Google Scholar]
  8. Dmitriev A, Yang M, Shakleina E, Tkacikova L, Suvorov A, Mikula I, Yang Y. H. 2003; The presence of insertion elements IS 1548 and IS 861 in group B streptococci. Folia Microbiol48:105–110[CrossRef]
    [Google Scholar]
  9. Ferrieri P, Burke B, Nelson J. 1980; Production of bacteremia and meningitis in infant rats with group B streptococcal serotypes. Infect Immun27:1023–1032
    [Google Scholar]
  10. Galas D. J, Chandler M. 1989; Bacterial insertion sequences. In Mobile DNA pp 109–162 Edited by Berg D. E., How M. M.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  11. Granlund M, Oberg L, Sellin M, Norgren M. 1998; Identification of a novel insertion element, IS 1548 , in group B streptococci, predominantly in strains causing endocarditis. J Infect Dis177:967–976[CrossRef]
    [Google Scholar]
  12. Granlund M, Michel F, Norgren M. 2001; Mutually exclusive distribution of IS 1548 and GBSi1, an active group II intron identified in human isolates of group B streptococci. J Bacteriol183:2560–2569[CrossRef]
    [Google Scholar]
  13. Harries L. W, Hattersley A. T, Ellard S. 2004; Messenger RNA transcripts of the hepatocyte nuclear factor-1alpha gene containing premature termination codons are subject to nonsense-mediated decay. Diabetes53:500–504[CrossRef]
    [Google Scholar]
  14. Hedén L.-O, Frithz E, Lindahl G. 1991; Molecular characterization of an IgA receptor from group B streptococci: sequence of the gene, identification of a proline-rich region with unique structure and isolation of N-terminal fragments with IgA-binding capacity. Eur J Immunol21:1481–1490[CrossRef]
    [Google Scholar]
  15. Jarva H, Janulczyk R, Hellwage J, Zipfel P. F, Bjorck J, Meri S. 2002; Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hic protein that binds to short consensus repeats 8–11 of factor H. J Immunol168:1886–1894[CrossRef]
    [Google Scholar]
  16. Jerlström P. G, Chhatwal G. S, Timmis K. N. 1991; The IgA-binding β antigen of the c protein complex of group B streptococci: sequence determination of its gene and detection of two binding regions. Mol Microbiol5:843–849[CrossRef]
    [Google Scholar]
  17. Jerlström P. G, Talay S. R, Valentin-Weigand P, Timmis K. N, Chhatwal G. S. 1996; Identification of an immunoglobulin A binding motif located in the β -antigen of the c protein complex of group B streptococci. Infect Immun64:2787–2793
    [Google Scholar]
  18. Kerr M. A. 1990; The structure and function of human IgA. Biochem J271:285–296
    [Google Scholar]
  19. Kong F, Gowan S, Martin D, James G, Gilbert G. L. 2002; Molecular profiles of group B streptococcal surface protein antigen genes: relationship to molecular serotypes. J Clin Microbiol40:620–626[CrossRef]
    [Google Scholar]
  20. Lindahl G, Sjöbring U, Johnsson E. 2000; Human complement regulators: a major target for pathogenic microorganisms. Curr Opin Immunol12:44–51[CrossRef]
    [Google Scholar]
  21. Lindahl G, Stålhammar-Carlemalm M, Areschoug T. 2005; Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin Microbiol Rev18:102–127[CrossRef]
    [Google Scholar]
  22. Mahillon J, Chandler M. 1998; Insertion sequences. Microbiol Mol Biol Rev62:725–774
    [Google Scholar]
  23. Maquat L. E. 1995; When cells stop making sense: effects of nonsense codons on RNA-metabolism in vertebrate cells. RNA 1:453–465
    [Google Scholar]
  24. Naess A. I, Bevanger L, Iversen O.-J, Maeland J. A. 1991; Evaluation of monoclonal antibodies in serovar classification of group B streptococci (GBS). Acta Pathol Microbiol Immunol Scand103:731–736
    [Google Scholar]
  25. Nagano N, Nagano Y, Taguchi F. 2002; High expression of a C protein β antigen gene among invasive strains from certain clonally related groups of type Ia and Ib group B streptococci. Infect Immun70:4643–4649[CrossRef]
    [Google Scholar]
  26. Pandiripally V, Wei L, Skerka C, Zipfel P. F, Cue D. 2003; Recruitment of complement factor H-like protein 1 promotes intracellular invasion by group A streptococci. Infect Immun71:7119–7128[CrossRef]
    [Google Scholar]
  27. Pangburn M. K, Schreiber R. D, Muller-Eberhard H. J. 1977; Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein beta 1H for cleavage of C3b and C4b in solution. J Exp Med146:257–270[CrossRef]
    [Google Scholar]
  28. Peltz S. W, He F, Welch E, Jacobson A. 1994; Nonsense-mediated messenger-RNA decay in yeast. Prog Nucleic Acid Res Mol Biol47:271–298
    [Google Scholar]
  29. Pleass R. J, Areschoug T, Lindahl G, Woof J. M. 2001; Streptococcal IgA-binding proteins bind in the C α 2-C α 3 interdomain region and inhibit binding of IgA to human CD89. J Biol Chem276:8197–8204[CrossRef]
    [Google Scholar]
  30. Podglajen I, Breuil J, Casin I, Collatz E. 1995; Genotypic identification of two groups within the species Bacteroides fragilis by ribotyping and by analysis of PCR-generated fragment patterns and insertion sequence content. J Bacteriol177:5270–5275
    [Google Scholar]
  31. Ram S, McQuillen D. P, Gulati S, Elkins C, Pangburn M. K, Rice P. A. 1998a; Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae . J Exp Med188:671–680[CrossRef]
    [Google Scholar]
  32. Ram S, Sharma A. K, Simpson S. D, Gulati S, McQuillen D. P, Pangburn M. K, Rice P. A. 1998b; A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae . J Exp Med187:743–752[CrossRef]
    [Google Scholar]
  33. Rubens C. E, Heggen L. M, Kuypers J. M. 1989; IS 861 , a group B streptococcal insertion sequence related to IS 150 and IS 3 of Escherichia coli . J Bacteriol171:5531–5535
    [Google Scholar]
  34. Ruizechevarria M. J, Czaplinski K, Peltz S. W. 1996; Making sense of nonsense in yeast. Trends Biochem Sci21:433–438[CrossRef]
    [Google Scholar]
  35. Russell-Jones G. J, Gotschlich E. C. 1984; Identification of protein antigens of group B streptococci, with special reference to the Ibc antigens. J Exp Med160:1476–1484[CrossRef]
    [Google Scholar]
  36. Sanchez-Beato A. R, Garcia E, Lopez R, Garcia J. L. 1997; Identification and characterization of IS 1381 , a new insertion sequence in Streptococcus pneumoniae . J Bacteriol179:2459–2463
    [Google Scholar]
  37. Sandhya D, Carmicle S, Hammerschmidt S, Pangburn M. K, McDaniel L. S. 2004; Dual roles of PspC, a surface protein of Streptococcus pneumoniae , in binding human secretory IgA and factor H1. J Immunol173:471–477[CrossRef]
    [Google Scholar]
  38. Schubert A, Zakikhany K, Schreiner M, Frank R, Spellerberg B, Eikmanns B. J, Reinscheid D. J. 2002; A fibrinogen receptor from group B Streptococcus interacts with fibrinogen by repetitive units with novel ligand binding sites. Mol Microbiol46:557–569[CrossRef]
    [Google Scholar]
  39. Spellerberg B, Rozdzinski E, Martin S, Weber-Heynemann J, Schnitzler N, Lütticken R, Podbielski A. 1999; Lmb, a protein with similarities to the LraI adhesin family, mediates attachment of Streptococcus agalactiae to human laminin. Infect Immun67:871–878
    [Google Scholar]
  40. Spellerberg B, Martin S, Franken C, Berner C, Lutticken R. 2000; Identification of a novel insertion sequence element in Streptococcus agalactiae . Gene241:51–56[CrossRef]
    [Google Scholar]
  41. Tamura G. S, Herndon M, Prezekwas J, Rubens C. E, Ferrieri P, Hillier S. L. 2000; Analysis of restriction fragment length polymorphisms of the insertion sequence IS 1381 in group B streptococci. J Infect Dis181:364–368[CrossRef]
    [Google Scholar]
  42. van Egmond M, van Garderen E, van Spriel A. B, Damen C. A, van Amersfoort E. S, van Zandbergen G, van Hattum J, Kuiper J, van de Winkel J. G. 2000; FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat Med6:680–685[CrossRef]
    [Google Scholar]
  43. Weiler J. M, Daha M. R, Austen K. F, Fearon D. T. 1976; Control of the amplification convertase of complement by the plasma protein beta 1H. Proc Natl Acad Sci U S A73:3268–3272[CrossRef]
    [Google Scholar]
  44. Whaley K, Ruddy S. 1976; Modulation of the alternative complement pathway by beta 1H globulin. J Exp Med144:1147–1163[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28535-0
Loading
/content/journal/micro/10.1099/mic.0.28535-0
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