Bioinformatic insights into the biosynthesis of the Group B carbohydrate in Streptococcus agalactiae

Microbiology

Volumn 154, Issue 5, 2008, Pages 1354-1363

  Sutcliffe, Iain C ^a   Black, Gary W ^a   Harrington, Dean J ^b  

^a NORTHUMBRIA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; CARBOHYDRATE GROUP B; LIPOTEICHOIC ACID; N ACETYLGLUCOSAMINE TRANSFERASE; TEICHOIC ACID; TRANSFERASE; BACTERIAL ANTIGEN; BACTERIAL DNA; LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENOME; BACTERIAL METABOLISM; BIOINFORMATICS; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYMOLOGY; GENE LOCUS; GENOME ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STREPTOCOCCUS AGALACTIAE; BACTERIAL GENE; BIOLOGY; BIOSYNTHESIS; CHEMICAL STRUCTURE; GENE ORDER; GENETICS; IMMUNOLOGY; METABOLISM; MULTIGENE FAMILY;

ANIMALIA; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS SP. 'GROUP B';

ANTIGENS, BACTERIAL; BIOSYNTHETIC PATHWAYS; CARBOHYDRATES; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; GENE ORDER; GENES, BACTERIAL; LIPOPOLYSACCHARIDES; MOLECULAR STRUCTURE; MULTIGENE FAMILY; STREPTOCOCCUS AGALACTIAE; TEICHOIC ACIDS;

EID: 46249105600     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2007/014522-0     Document Type: Article

References (70)

1. Alaimo, C., Catrein, I., Mort, L., Marolda, C. L., Callewaert N., Valvano, M. A., Feldman, M. F. & Aebi, M. (2006). Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J 125, 967-976.
2. Almeida, M. S., Herrmann, T., Peti, W., Wilson, I. A. & Wüthrich, K. (2005). NMR structure of the conserved hypothetical protein TM0487 from Thermotoga maritima: implications for 216 homologous DUF59 proteins. Protein Sci 14, 2880-2886.
3. Anthony, B. F., Concepcion, N. F. & Concepcion, K. F. (1985). Human-antibody to the group-specific polysaccharide of Group-B Streptococcus. J Infect Dis 151, 221-226.
4. Barabote, R. D. & Saler, M. H. (2005). Comparative genomic analysis of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69, 608-634.
5. Bentley, S. D., Aanensen, D. M., Mavroidi, A., Saunders, D., Rabbinowitsch, E., Collins, M., Donohoe, K., Harris, D., Murphy, L. & other authors (2006). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2, e31.
6. Bhavsar, A. P. & Brown, E. D. (2006). Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol Microbiol 60, 1077-1090.
7. Bourgoin, F., Pluvinet, A., Ginte, B., Decaris, B. & Guedon, G. (1999). Are horizontal transfers involved in the evolution of the Streptococcus thermophilus exopolysaccharide synthesis loci? Gene 233, 151-161.
8. Bradley, A. J. (2002). Bovine mastitis: an evolving disease. Vet J 164, 116-124.
9. Brooks, S., Apostol, M., Nadle, J., Wymore, K., Haubert, N., Burnite, S., Daniels, A., Hadler, J. L., Farley, M. M. & other authors (2006). Early-onset and late-onset neonatal Group B streptococcal disease - United States, 1996-2004. JAMA 295, 1371-1372.
10. Cieslewicz, M. J., Chaffin, D., Glusmann, G., Kasper, D., Madan, A., Rodrigues, S., Fahey, J., Wessels, M. R. & Rubens, C. E. (2005). Structural and genetic diversity of Group B Streptococcus capsular polysaccharides. Infect Immun 73, 3096-3103.
11. Coutinho, P. M. & Henrissat, B. (1999). Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering, pp. 3-12. Edited by H. J. Gilbert, G. Davies, B. Henrissat & B. Svensson. Cambridge: The Royal Society of Chemistry.
12. D'Elia, M. A., Millar, K. E., Beveridge, T. J. & Brown, E. D. (2006). Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188, 8313-8316.
13. Damjanovic, M., Kharat, A. S., Eberhardt, A., Tomasz, A. & Vollmer, W. (2007). The essential tacF gene is responsible for the choline-dependent growth phenotype of Streptococcus pneumoniae. J Bacteriol 189, 7105-7111.
14. Davies, S., Gear, J. E., Mason, C. M. & McIntyre, S. M. (2003). Streptococcus grouping latex kits: evaluation of five commercially available examples. Br J Biomed Sci 60, 136-140.
15. Deng, L. Y., Kasper, D. L., Krick, T. P. & Wessels, M. R. (2000). Characterization of the linkage between the type III capsular polysaccharide and the bacterial cell wall of Group B Streptococcus. J Biol Chem 275, 7497-7504.
16. Doran, K. S., Engelson, E. J., Khosravi, A., Maisey, H. C., Fedtke, I., Equils, O., Michelsen, K. S., Arditi, M., Peschel, A. & Nizet, V. (2005). Blood-brain barrier invasion by Group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115, 2499-2507.
17. Edwards, M. S. & Baker, C. J. (2005). Group B streptococcal infections in elderly adults. Clin Infect Dis 41, 839-847.
18. Erbing, B., Kenne, L., Lindberg, B., Helting, T. & Hammerschmid, F. (1986). structural studies of a teichoic acid from Streptococcus agalactiae Type III. Carbohydr Res 156, 145-155.
19. Finn, R. D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A. & other authors (2006). Pfam: clans, web tools and services. Nucleic Acids Res 34, D247-D25l.
20. Follens, A., Veiga-Da-Cunha, M., Merckx, R., Van Schaftingen, E. & Van Eldere, J. (1999). acs1 of Haemophilus influenzae type a capsulation locus region II encodes a bifunctional ribulose 5-phosphate reductase- CDP-ribitol pyrophosphorylase. J Bacteriol 181, 2001-2007.
21. Glaser, P., Rusniok C., Buchrieser, C., Chevalier, F., Frangeul, L., Msadek, T., Zouine, M., Couve, E., Lalioui, L. & other authors (2002). Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45, 1499-1513.
22. Goldschmidt, J. C. & Panos, C. (1984). Teichoic acids of Streptococcus agalactiae: chemistry, cytotoxicity, and effect on bacterial adherence to human cells in tissue culture. Infect Immun 43, 670-677.
23. Gray, K. J., Bennett, S. L., French, N., Phiri, A. J. & Graham, S. M. (2007). Invasive group B streptococcal infection in infants, Malawi. Emerg Infect Dis 13, 223-229.
24. Greenberg, D. N., Ascher, D. P., Yoder, B. A., Hensley, D. M., Heiman, H. S. & Keith, J. F. (1995). Sensitivity and specificity of rapid diagnostic tests for detection of Group B streptococcal antigen in bacteremic neonates. J Clin Microbiol 33, 193-198.
25. Gutekunst, H., Eikmanns, B. J. & Reinscheid, D. J. (2003). Analysis of RogB-controlled virulence mechanisms and gene expression in Streptococcus agalactiae. Infect Immun 71, 5056-5064.
26. Heath, P. T., Balfour, G., Weisner, A. M., Esfratiou, A., Lamagni, T. L., Tighe, H., O'Connell, L. A. F., Cafferkey, M., Verlander, N. O. & other authors (2004). Group B streptococcal disease in UK and Irish infants younger than 90 days. Lancet 363, 292-294.
27. Henneke, P. & Berner, R. (2006). Interaction of neonatal phagocytes with Group B Streptococcus: recognition and response. Infect Immun 74, 3085-3095.
28. Hofmann, K. & Stoffel, W. (1993). TMbase - a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 374, 166.
29. Johri, A. K, Paoletti, L. C., Glaser, P., Due, M., Sharma, P. K., Grandi, G. & Rappuoli, R. (2006). Group B Streptococcus: global incidence and vaccine development. Nat Rev Microbiol 4, 932-942.
30. Käll, L., Krogh, A. & Sonnhammer, E. L. L. (2004). A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338, 1027-1036.
31. Kogan, G., Uhrin, D., Brisson, J. R., Paoletti, L. C., Blodgett, A. E., Kasper, D. L. & Jennings, H. J. (1996). Structural and immunochemical characterization of the type VIII Group B Streptococcus capsular polysaccharide. J Biol Chem 271, 8786-8790.
32. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305, 567-580.
33. Lancefield, R. C. (1934). A serological differentiation of specific types of bovine hemolytic streptococci (Group B). J Exp Med 59, 441-458.
34. Lancefield, R. C., McCarty, M. & Everly, W. N. (1975). Multiple mouse-protective antibodies directed against group B streptococci. Special reference to antibodies effective against protein antigens. J Exp Med 142, 165.
35. Lehrer, J., Vigeant, K. A., Tatar, L. D. & Valvano, M. A. (2007). Functional characterization and membrane topology of Escherichia coli WecA, a sugar-phosphate transferase initiating the biosynthesis of enterobacterial common antigen and O-antigen lipopolysaccharide. J Bacteriol 189, 2618-2628.
36. 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.
37. Liu, D., Cole, R. A. & Reeves, P. R. (1996). An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol 178, 2102-2107.
38. Lysenko, E., Richards, J. C., Cox, A. D., Stewart, A., Martin, A., Kapoor, M. & Weiser, J. N. (2000). The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol Microbiol 35, 234-245.
39. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V. & other authors (2006). Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103, 15611-15616.
40. Marolda, C. L., Tatar, L. D., Alaimo, C., Aebi, M. & Valvano, M. A. (2006). Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J Bacteriol 188, 5124-5135.
41. Marques, M. B., Kasper, D. L., Schroff, A., Michon, F., Jennings, H. J. & Wessels, M. R. (1994). Functional activity of antibodies to the group B polysaccharide of Group B streptococci elicited by a polysaccharide-protein conjugate vaccine. Infect Immun 62, 1593-1599.
42. Mattingly, S. J. & Johnston, B. P. (1987). Comparative analysis of the localisation of lipotechoic add in Streptococcus agalactiae and Streptococcus pyogenes. Infect Immun 55, 2383-2386.
43. McGinnis, S. & Madden, T. L. (2004). BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32, W20-W25.
44. Michon, F., Katzenellenbogen, E., Kasper, D. L. & Jennings, H. J. (1987). Structure of the complex group-specific polysaccharide of group B Streptococcus. Biochemistry 26, 476-486.
45. 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.
46. Michon, F., Chalifour, R., Feldman, R., Wessels, M., Kasper, D. L., Gamian, A., Pozsgay, V. & Jennings, H.A. (1991). The α-L-(1→2)- trirhamnopyranoside epitope on the group-specific polysaccharide of Group B Streptococci. Infect Immun 59, 1690-1696.
47. Michon, F., Moore, S. L., Kim, J., Blake, M. S., Auzanneau, F. I., Johnston, B. D., Johnson, M. A. & Pinto, B. M. (2005). Doubly branched hexasaccharide epitope on the cell wall polysaccharide of group A streptococci recognized by human and rabbit antisera. Infect Immun 73, 6383-6389.
48. Neuhaus, F. C. & Baddiley, J. (2003). A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67, 686-723.
49. Pincus, S. H., Cole, R. L., Wessels, M. R., Corwin, M. D., Kamangasollo, E., Hayes, S. F., Cieplak, W. & Swanson, J. (1992). Group B Streptococcal opacity variants. J Bacteriol 174, 3739-3749.
50. Pincus, S. H., Cole, R. L., Kamangasollo, E. & Fischer, S. H. (1993). Interaction of Group B Streptococcal opacity variants with the host-defense system. Infect Immun 61, 3761-3768.
51. Poyart, C., Larny, M. C., Boumaila, C., Fiedler, F. & Trieu-Cuot P. (2001). Regulation of D-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J Bacteriol 183, 6324-6334.
52. Pritchard, D. G., Gray, B. M. & Dillon, H. C. (1984). Characterization of the group-specific polysaccharide of group B Streptococcus. Arch Biochem Biophys 235, 385-392.
53. Rosini, R., Rinaudo, C. D., Soriani, M., Lauer, P., Mora, M, Maione, D., Taddei, A., Santi, I., Ghezzo, C. & other authors (2006). Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol 61, 126-141.
54. Sabharwal, H., Michon, F., Nelson, D., Dong, W. L., Fuchs, K., Manjarrez, R. C., Sarkar, A., Uitz, C., Viteri-Jackson, A. & other authors (2006). Group A Streptococcus (GAS) carbohydrate as an immunogen for protection against GAS infection. J Infect Dis 193, 129-135.
55. Shibata, Y., Yamashita, Y., Ozaki, K., Nakano, Y. & Koga, T. (2002). Expression and characterization of streptococcal rgp genes required for rhamnan synthesis in Escherichia coli. Infect Immun 70, 2891-2898.
56. Soldo, B., Lazarevic, V. & Karamata, D. (2002). tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148, 2079-2087.
57. Sutcliffe, I. C. & Harrington, D. J. (2004). Putative lipoproteins of Streptococcus agalactiae identified by bioinformatic genome analysis. Antonie van Leeuwenhoek 85, 305-315.
58. Takamatsu, D., Bensing, B. A. & Sullam, P. M. (2004). 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.
59. Tettelin, H., Masignani, V., Cieslewicz, M. J., Eisen, J. A., Peterson, S., Wessels, M. R., Paulsen, I. T., Nelson, K. E., Margarit, I. & 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.
60. Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., Crabtree, J., Jones, A. L. & 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.
61. Trotman, H. & Bell, Y. (2006). Neonatal group B streptococcal infection at the University Hospital of the West Indies, Jamaica: a 10-year experience. Ann Trop Paediatr 26, 53-57.
62. Tsukioka, Y., Yamashita, Y., Nakano, Y., Oho, T. & Koga, T. (1997). Identification of a fourth gene involved in dTDP-rhamnose synthesis in Streptococcus mutans. J Bacteriol 179, 4411-4414.
63. UniProt Consortium (2007). The universal protein resource (UniProt). Nucleic Acids Res 35, D193-D197.
64. Vallejo, J. G., Baker, C. J. & Edwards, M. S. (1996). Role of the bacterial cell wall and capsule in induction of tumor necrosis factor alpha by Type III Group B streptococci. Infect Immun 64, 5042-5046.
65. Wegmann, U., O'Connell-Motherwy, M., Zomer, A., Bulst, G., Shearman, C., Canchaya, C., Ventura, M., Goesmann, A., Gasson, M. J. & other authors (2007). Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp cremoris MG1363. J Bacteriol 189, 3256-3270.
66. Whitfield, C. (2006). Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75, 39-68.
67. Yamashita, Y., Tsukioka, Y., Tomihisa, K., Nakano, Y. & Koga, T. (1998). Genes involved in cell wall localization and side chain formation of rhamnose-glucose polysaccharide in Streptococcus mutans. J Bacteriol 180, 5803-5807.
68. Yamashita, Y., Sibata, Y., Nakano, Y., Tsuda, H., Kido, N., Ohta, M. & Koga, T. (1999). A novel gene required for rhamnose-glucose polysaccharide synthesis in Streptococcus mutans. J Bacteriol 181, 6556-6559.
69. Yoshida, Y., Ganguly, S., Bush, C. A. & Cisar, J. O. (2006). Molecular basis of L-rhamnose branch formation in streptococcal coaggregation receptor polysaccharides. J Bacteriol 188, 4125-4130.
70. Zhang, J. R., Idanpaan-Heikkila, I., Fischer, W. & Tuomanen, E. I. (1999). Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol Microbiol 31, 1477-1488.