1887

Abstract

Group B streptococci (GBS) are pathogens of both neonates and adults, with serotype III strains in particular being associated with invasive disease and meningitis. In this study, a novel GBS surface antigen, , was found to be co-expressed with the previously reported antigen on an identical subset of serotype III GBS. Expression of / on the surface of serotype III GBS was shown to distinguish the restriction digest pattern (RDP) III-3 and multilocus sequence typing (ST)-17 lineage. -Specific antibodies were reactive with a unique, high-molecular-mass, serine-rich repeat protein (Srr-2) found exclusively in RDP III-3 strains. The gene encoding Srr-2 was located within a putative accessory secretory locus that included and homologues and had a genetic organization similar to that of the / locus of staphylococci. In contrast, serotype III /-negative strains and strains representative of serotypes Ia, Ib, Ic and II shared a common Srr-encoding gene, , and an organization of the / locus similar to that of previously reported serotype Ic, /-negative serotype III and serotype V GBS strains. Representative serotype III /-positive strains had LD values 3–4 logs less than those of serotype III /-negative strains in a neonatal mouse model of infection. These results indicate that the RDP III-3/ST-17 lineage expresses Srr-2 and is highly virulent in an model of neonatal sepsis.

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2006-04-01
2019-10-14
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References

  1. Adderson, E. E., Takahashi, S., Wang, Y., Armstrong, J., Miller, D. V. & Bohnsack, J. F. ( 2003; ). Subtractive hybridization identifies a novel predicted protein mediating epithelial cell invasion by virulent serotype III group B Streptococcus agalactiae. Infect Immun 71, 6857–6863.[CrossRef]
    [Google Scholar]
  2. Areschoug, T., Stalhammar-Carlemalm, M., Karlsson, I. & Lindahl, G. ( 2002; ). Streptococcal beta protein has separate binding sites for human factor H and IgA-Fc. J Biol Chem 277, 12642–12648.[CrossRef]
    [Google Scholar]
  3. Auperin, T. C., Bolduc, G. R., Baron, M. J., Heroux, A., Filman, D. J., Madoff, L. C. & Hogle, J. M. ( 2005; ). Crystal structure of the N-terminal domain of the group B Streptococcus alpha C protein. J Biol Chem 280, 18245–18252.[CrossRef]
    [Google Scholar]
  4. Baker, C. J. & Edwards, M. S. ( 2001; ). Group B streptococcal infections. In Infectious Diseases of the Fetus and Newborn Infant, pp. 1091–1156. Edited by J. S. Remington & J. O. Klein. Philadelphia, PA: W. B. Saunders.
  5. 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.[CrossRef]
    [Google Scholar]
  6. Bensing, B. A., Lopez, J. A. & Sullam, P. M. ( 2004; ). The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ibalpha. Infect Immun 72, 6528–6537.[CrossRef]
    [Google Scholar]
  7. Bevanger, L. ( 1985; ). The Ibc proteins of group B streptococci: isolation of the alpha and beta antigens by immunosorbent chromatography and test for human serum antibodies against the two antigens. Acta Pathol Microbiol Immunol Scand Sect B Microbiol 93, 113–119.
    [Google Scholar]
  8. Bisharat, N., Crook, D. W., Leigh, J., Harding, R. M., Ward, P. N., Coffey, T. J., Maiden, M. C., Peto, T. & Jones, N. ( 2004; ). Hyperinvasive neonatal group B streptococcus has arisen from a bovine ancestor. J Clin Microbiol 42, 2161–2167.[CrossRef]
    [Google Scholar]
  9. Bohnsack, J. F., Takahashi, S., Detrick, S. R., Pelinka, L. R., Hammitt, L. L., Aly, A. A., Whiting, A. A. & Adderson, E. E. ( 2001; ). Phylogenetic classification of serotype III group B streptococci on the basis of hylB gene analysis and DNA sequences specific to restriction digest pattern type III-3. J Infect Dis 183, 1694–1697.[CrossRef]
    [Google Scholar]
  10. Bohnsack, J. F., Whiting, A. A., Bradford, R. D., Van Frank, B. K., Takahashi, S. & Adderson, E. E. ( 2002; ). Long-range mapping of the Streptococcus agalactiae phylogenetic lineage restriction digest pattern type III-3 reveals clustering of virulence genes. Infect Immun 70, 134–139.[CrossRef]
    [Google Scholar]
  11. Boyer, K. M., Gadzala, C. A., Kelly, P. D., Burd, L. I. & Gotoff, S. P. ( 1983; ). Selective intrapartum chemoprophylaxis of neonatal group B streptococcal early-onset disease. II. Predictive value of prenatal cultures. J Infect Dis 148, 802–809.[CrossRef]
    [Google Scholar]
  12. Brady, L. J., Daphtary, U. D., Ayoub, E. M. & Boyle, M. D. ( 1988; ). Two novel antigens associated with group B streptococci identified by a rapid two-stage radioimmunoassay. J Infect Dis 158, 965–972.[CrossRef]
    [Google Scholar]
  13. Brady, L. J., Hofig, A., Addison, M. N. & Lim, D. V. ( 1996; ). Association of two antigens, delta and epsilon, with pathogenic serotype III group B streptococci. Proceedings of the 96th General Meeting of the American Society for Microbiology, abstract no. B-350. Washington, DC: American Society for Microbiology.
  14. Chen, Q., Wu, H. & Fives-Taylor, P. M. ( 2002; ). Construction of a novel transposon mutagenesis system useful in the isolation of Streptococcus parasanguis mutants defective in Fap1 glycosylation. Infect Immun 70, 6534–6540.[CrossRef]
    [Google Scholar]
  15. Chun, C. S., Brady, L. J., Boyle, M. D., Dillon, H. C. & Ayoub, E. M. ( 1991; ). Group B streptococcal C protein-associated antigens: association with neonatal sepsis. J Infect Dis 163, 786–791.[CrossRef]
    [Google Scholar]
  16. Cleat, P. H. & Timmis, K. N. ( 1987; ). Cloning and expression in Escherichia coli of the Ibc protein genes of group B streptococci: binding of human immunoglobulin A to the beta antigen. Infect Immun 55, 1151–1155.
    [Google Scholar]
  17. Davies, H. D., Jones, N., Whittam, T. S., Elsayed, S., Bisharat, N. & Baker, C. J. ( 2004; ). Multilocus sequence typing of serotype III streptococcus and correlation with pathogenic potential. J Infect Dis 189, 1097–1102.[CrossRef]
    [Google Scholar]
  18. Farley, M. M. ( 2001; ). Group B streptococcal disease in nonpregnant adults. Clin Infect Dis 33, 556–561.[CrossRef]
    [Google Scholar]
  19. Ferrieri, P. ( 1985; ). GBS infections in the newborn infant: diagnosis and treatment. Antibiot Chemother 35, 211–224.
    [Google Scholar]
  20. 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]
  21. Fleming, K. E., Bohnsack, J. F., Palacios, G. C., Takahashi, S. & Adderson, E. E. ( 2004; ). Equivalence of high-virulence clonotypes of serotype III group B Streptococcus agalactiae (GBS). J Med Microbiol 53, 505–508.[CrossRef]
    [Google Scholar]
  22. Glaser, P., Rusniok, C., Buchrieser, C. & 9 other authors ( 2002; ). Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45, 1499–1513.[CrossRef]
    [Google Scholar]
  23. Gravekamp, C., Horensky, D. S., Michel, J. L. & Madoff, L. C. ( 1996; ). Variation in repeat number within the alpha C protein of group B streptococci alters antigenicity and protective epitopes. Infect Immun 64, 3576–3583.
    [Google Scholar]
  24. Handley, P. S., Correia, F. F., Russell, K., Rosan, B. & DiRienzo, J. M. ( 2005; ). Association of a novel high molecular weight, serine-rich protein (SrpA) with fibril-mediated adhesion of the oral biofilm bacterium Streptococcus cristatus. Oral Microbiol Immunol 20, 131–140.[CrossRef]
    [Google Scholar]
  25. Héry-Arnaud, G., Bruant, G., Lanotte, P., Brun, S., Rosenau, A., van der Mee-Marquet, N., Quentin, R. & Mereghetti, L. ( 2005; ). Acquisition of insertion sequences and the GBSi1 intron by Streptococcus agalactiae isolates correlates with the evolution of the species. J Bacteriol 187, 6248–6252.[CrossRef]
    [Google Scholar]
  26. Johnson, D. R. & Ferrieri, P. ( 1984; ). Group B streptococcal Ibc protein antigen: distribution of two determinants in wild-type strains of common serotypes. J Clin Microbiol 19, 506–510.
    [Google Scholar]
  27. Jones, N., Bohnsack, J. F., Takahashi, S. & 9 other authors ( 2003; ). Multilocus sequence typing for group B streptococcus. J Clin Microbiol 41, 2530–2536.[CrossRef]
    [Google Scholar]
  28. Kremer, B. H., van der Kraan, M., Crowley, P. J., Hamilton, I. R., Brady, L. J. & Bleiweis, A. S. ( 2001; ). Characterization of the sat operon in Streptococcus mutans: evidence for a role of Ffh in acid tolerance. J Bacteriol 183, 2543–2552.[CrossRef]
    [Google Scholar]
  29. Law, M. R., Palomaki, G., Alfirevic, Z., Gilbert, R., Heath, P., McCartney, C., Reid, T. & Schrag, S. ( 2005; ). The prevention of neonatal group B streptococcal disease: a report by a working group of the Medical Screening Society. J Med Screen 12, 60–68.[CrossRef]
    [Google Scholar]
  30. Lindahl, G., Stalhammar-Carlemalm, M. & Areschoug, T. ( 2005; ). Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin Microbiol Rev 18, 102–127.[CrossRef]
    [Google Scholar]
  31. Luan, S. L., Granlund, M., Sellin, M., Lagergard, T., Spratt, B. G. & Norgren, M. ( 2005; ). Multilocus sequence typing of Swedish invasive group B streptococcus isolates indicates a neonatally associated genetic lineage and capsule switching. J Clin Microbiol 43, 3727–3733.[CrossRef]
    [Google Scholar]
  32. Maeland, J. A., Brakstad, O. G., Bevanger, L. & Kvam, A. I. ( 1997; ). Streptococcus agalactiae beta gene and gene product variations. J Med Microbiol 46, 999–1005.[CrossRef]
    [Google Scholar]
  33. Maione, D., Margarit, I., Rinaudo, C. D. & 24 other authors ( 2005; ). Identification of a universal Group B Streptococcus vaccine by multiple genome screen. Science 309, 148–150.[CrossRef]
    [Google Scholar]
  34. Martin, T. R., Rubens, C. E. & Wilson, C. B. ( 1988; ). Lung antibacterial defense mechanisms in infant and adult rats: implications for the pathogenesis of group B streptococcal infections in the neonatal lung. J Infect Dis 157, 91–100.[CrossRef]
    [Google Scholar]
  35. Michel, J. L., Madoff, L. C., Kling, D. E., Kasper, D. L. & Ausubel, F. M. ( 1991; ). Cloned alpha and beta C-protein antigens of group B streptococci elicit protective immunity. Infect Immun 59, 2023–2028.
    [Google Scholar]
  36. Michon, F., Brisson, J. R., Dell, A., Kasper, D. L. & Jennings, H. J. ( 1988; ). Multiantennary group-specific polysaccharide of group B Streptococcus. Biochemistry 27, 5341–5351.[CrossRef]
    [Google Scholar]
  37. Musser, J. M., Mattingly, S. J., Quentin, R., Goudeau, A. & Selander, R. K. ( 1989; ). Identification of a high-virulence clone of type III Streptococcus agalactiae (group B Streptococcus) causing invasive neonatal disease. Proc Natl Acad Sci U S A 86, 4731–4735.[CrossRef]
    [Google Scholar]
  38. Nagano, Y., Nagano, N., Takahashi, S., Murono, K., Fujita, K., Taguchi, F. & Okuwaki, Y. ( 1991; ). Restriction endonuclease digest patterns of chromosomal DNA from group B beta-haemolytic streptococci. J Med Microbiol 35, 297–303.[CrossRef]
    [Google Scholar]
  39. Puopolo, K. M., Madoff, L. C. & Eichenwald, E. C. ( 2005; ). Early-onset group B streptococcal disease in the era of maternal screening. Pediatrics 115, 1240–1246.[CrossRef]
    [Google Scholar]
  40. Reed, L. J. & Muench, M. H. ( 1938; ). A simple method of estimating fifty per cent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  41. Rodewald, A. K., Onderdonk, A. B., Warren, H. B. & Kasper, D. L. ( 1992; ). Neonatal mouse model of group B streptococcal infection. J Infect Dis 166, 635–639.[CrossRef]
    [Google Scholar]
  42. Rubens, C. E. & Heggen, L. ( 1988; ). Tn916ΔE: a Tn916 derivative expressing erythromycin resistance. Plasmid 20, 137–142.[CrossRef]
    [Google Scholar]
  43. 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 Med 160, 1476–1484.[CrossRef]
    [Google Scholar]
  44. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  45. Schrag, S. J., Zywicki, S., Farley, M. M. & 7 other authors ( 2000; ). Group B streptococcal disease in the era of intrapartum antibiotic prophylaxis. N Engl J Med 342, 15–20.[CrossRef]
    [Google Scholar]
  46. Seifert, K. N., McArthur, W. P., Bleiweis, A. S. & Brady, L. J. ( 2003; ). Characterization of group B streptococcal glyceraldehyde-3-phosphate dehydrogenase: surface localization, enzymatic activity, and protein-protein interactions. Can J Microbiol 49, 350–356.[CrossRef]
    [Google Scholar]
  47. Siboo, I. R., Chambers, H. F. & Sullam, P. M. ( 2005; ). Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 73, 2273–2280.[CrossRef]
    [Google Scholar]
  48. Staden, R. ( 1996; ). The Staden sequence analysis package. Mol Biotechnol 5, 233–241.[CrossRef]
    [Google Scholar]
  49. Stalhammar-Carlemalm, M., Stenberg, L. & Lindahl, G. ( 1993; ). Protein rib: a novel group B streptococcal cell surface protein that confers protective immunity and is expressed by most strains causing invasive infections. J Exp Med 177, 1593–1603.[CrossRef]
    [Google Scholar]
  50. Stephenson, A. E., Wu, H., Novak, J., Tomana, M., Mintz, K. & Fives-Taylor, P. ( 2002; ). The Fap1 fimbrial adhesin is a glycoprotein: antibodies specific for the glycan moiety block the adhesion of Streptococcus parasanguis in an in vitro tooth model. Mol Microbiol 43, 147–157.[CrossRef]
    [Google Scholar]
  51. Takahashi, S., Adderson, E. E., Nagano, Y., Nagano, N., Briesacher, M. R. & Bohnsack, J. F. ( 1998; ). Identification of a highly encapsulated, genetically related group of invasive type III group B streptococci. J Infect Dis 177, 1116–1119.[CrossRef]
    [Google Scholar]
  52. Takahashi, Y., Konishi, K., Cisar, J. O. & Yoshikawa, M. ( 2002; ). Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun 70, 1209–1218.[CrossRef]
    [Google Scholar]
  53. Takahashi, Y., Yajima, A., Cisar, J. O. & Konishi, K. ( 2004; ). Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect Immun 72, 3876–3882.[CrossRef]
    [Google Scholar]
  54. Takamatsu, D., Bensing, B. A. & Sullam, P. M. ( 2004a; ). Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J Bacteriol 186, 7100–7111.[CrossRef]
    [Google Scholar]
  55. Takamatsu, D., Bensing, B. A. & Sullam, P. M. ( 2004b; ). Genes in the accessory sec locus of Streptococcus gordonii have three functionally distinct effects on the expression of the platelet-binding protein GspB. Mol Microbiol 52, 189–203.[CrossRef]
    [Google Scholar]
  56. Tettelin, H., Masignani, V., Cieslewicz, M. J. & 40 other authors ( 2002; ). Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci U S A 99, 12391–12396.[CrossRef]
    [Google Scholar]
  57. Tettelin, H., Masignani, V., Cieslewicz, M. J. & 43 other authors ( 2005; ). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102, 13950–13955.[CrossRef]
    [Google Scholar]
  58. Tyrrell, G. J., Senzilet, L. D., Spika, J. S., Kertesz, D. A., Alagaratnam, M., Lovgren, M. & Talbot, J. A. ( 2000; ). Invasive disease due to group B streptococcal infection in adults: results from a Canadian, population-based, active laboratory surveillance study –1996. Sentinel Health Unit Surveillance System Site Coordinators. J Infect Dis 182, 168–173.[CrossRef]
    [Google Scholar]
  59. Ustinovitch, I., Vlasov, G., Totolyan, A. & Suvorov, A. ( 1999; ). Cloning and expression of gene fragment IgA-binding protein of group B streptococci. Folia Microbiol (Praha) 44, 726–728.[CrossRef]
    [Google Scholar]
  60. Wilkinson, H. W. & Eagon, R. G. ( 1971; ). Type-specific antigens of group B type Ic streptococci. Infect Immun 4, 596–604.
    [Google Scholar]
  61. Wu, H. & Fives-Taylor, P. M. ( 1999; ). Identification of dipeptide repeats and a cell wall sorting signal in the fimbriae-associated adhesin, Fap1, of Streptococcus parasanguis. Mol Microbiol 34, 1070–1081.[CrossRef]
    [Google Scholar]
  62. Wu, H., Mintz, K. P., Ladha, M. & Fives-Taylor, P. M. ( 1998; ). Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol Microbiol 28, 487–500.[CrossRef]
    [Google Scholar]
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