A proteomic investigation of Streptococcus agalactiae grown under conditions associated with neonatal exposure reveals the upregulation of the putative virulence factor C protein β antigen

International Journal of Medical Microbiology

Volumn 300, Issue 5, 2010, Pages 331-337

  Yang, Qian ^a   Zhang, Meng ^a   Harrington, Dean J ^b   Black, Gary W ^a   Sutcliffe, Iain C ^a  

^a NORTHUMBRIA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

Author keywords

C protein Beta antigen; Colonisation; Group B Streptococcus; Proteomics; Virulence factors

Indexed keywords

UNCLASSIFIED DRUG; VIRULENCE FACTOR; VIRULENCE FACTOR C PROTEIN BETA ANTIGEN;

ADAPTATION; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CULTURE MEDIUM; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEOMICS; STREPTOCOCCUS AGALACTIAE; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; AEROBIOSIS; ANTIGENS, BACTERIAL; CULTURE MEDIA; GENE EXPRESSION PROFILING; PROTEOME; STREPTOCOCCUS AGALACTIAE; UP-REGULATION; VIRULENCE FACTORS;

EID: 77952237522     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2010.01.001     Document Type: Article

References (56)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes. Nucl. Acids Res. 25 (1997) 3389-3402
2. Areschoug T., Linse S., Stålhammar-Carlemalm M., Hedén L.-O., and Lindahl G. A proline-rich region with a highly periodic sequence in streptococcal ß protein adopts the polyproline II structure and is exposed on the bacterial surface. J. Bacteriol. 184 (2002) 6376-6383
3. Ayala-Castro C., Saini A., and Outten F.W. Fe-S cluster assembly pathways in bacteria. Microbiol. Mol. Biol. Rev. 72 (2008) 110-125
4. Barcaite E., Bartusevicius A., Tameliene R., Kliucinskas M., Maleckiene L., and Nadisauskiene R. Prevalence of maternal Group B streptococcal colonisation in European countries. Acta Obstet. Gynecol. Scand. 87 (2008) 260-271
5. Brady L.J., and Boyle M.D.P. Identification of non-immunoglobulin A-Fc-binding forms low-molecular-weight secreted forms of the Group B streptococcal β antigen. Infect. Immun. 57 (1989) 1573-1581
6. Bray B.A., Sutcliffe I.C., and Harrington D.J. Impact of lgt mutation on lipoprotein biosynthesis and in vitro phenotypes of Streptococcus agalactiae. Microbiology 155 (2009) 1451-1458
7. Brenot A., King K.Y., and Caparon M.G. The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol. Microbiol. 55 (2005) 221-234
8. Caspi R., Foerster H., Fulcher C.A., Kaipa P., Krummenacker M., Latendresse M., Paley S.M., Rhee S.Y., Shearer A., Tissier C., Walk T.C., Zhang P., and Karp P.D. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome databases. Nucl. Acids Res. 36 (2008) D623-631
9. Chastanet A., Prudhomme M., Claverys J.-P., and Msadek T. Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J. Bacteriol. 183 (2001) 7295-7307
10. Colbourn T., and Gilbert R. An overview of the natural history of early onset Group B streptococcal disease in the UK. Early Human Dev. 83 (2007) 149-156
11. Dmitriev A., Yang Y.H., Shen A.D., and Totolian A. Adjacent location of the bac gene and two-component regulatory system genes within the putative Streptococcus agalactiae pathogenicity island. Folia Microbiol. 51 (2006) 229-235
12. Doran K.S., and Nizet V. Molecular pathogenesis of neonatal Group B streptococcal infection: no longer in its infancy. Mol. Microbiol. 54 (2004) 23-31
13. Dunwell J.M., Purvis A., and Khuri S. Cupins: the most functionally diverse protein superfamily?. Phytochemistry 65 (2004) 7-17
14. Eidelman A.I., Nevet A., Rudensky B., Rabinowitz R., Hammermanm C., Raveh D., and Schimmel M.S. The effect of meconium staining of amniotic fluid on the growth of Escherichia coli and Group B Streptococcus. J. Perinatol. 22 (2002) 467-471
15. Fernández M., Kleerebezem M., Kuipers O.P., Siezen R.J., and van Kranenburg R. Regulation of the metC-cysK operon, involved in sulfur metabolism in Lactococcus lactis. J. Bacteriol. 184 (2002) 82-90
16. Fernandez A., Ogawa J., Penaud S., Boudebbouze S., Ehrlich D., van de Guchte M., and Maguin E. Rerouting of pyruvate metabolism during acid adaptation in Lactobacillus bulgaricus. Proteomics 8 (2008) 3154-3163
17. Frees D., Vogensen F.K., and Ingmer H. Identification of proteins induced at low pH in Lactococcus lactis. Int. J. Food. Microbiol. 87 (2003) 293-300
18. Gaillot O., Poyart C., Berche B., and Trieu-Cuot P. Molecular characterisation and expression analysis of the superoxide dismutase gene from Streptococcus agalactiae. Gene 204 (1997) 213-218
19. Håkansson S., Axemo P., Bremme K., Bryngelsson A.-L., Wallin M.C., Ekström C.-M., Granlund M., Jacobsson B., Källén E., Tessin I., and Swedish Working Group for the Prevention of Perinatal Group B Streptococcal Infections. Group B streptococcal carriage in Sweden: a national study on risk factors for mother and infant colonisation. Acta Obstet. Gynecol. Scand. 87 (2008) 50-58
20. Hansen T., Schlichting B., Felgendreher M., and Schönheit P. Cupin-tvpe phosphoglucose isomerases (Cupin-PGls) constitute a novel metal-dependent PGI family representing a convergent line of PGI evolution. J. Bacteriol. 187 (2005) 1621-1631
21. Heath P.T., Balfour G., Weisner A.M., Efstratiou A., Lamagni T.L., Tighe H., O'Connell L.A., Cafferkey M., Verlander N.Q., Nicoll A., McCartney A.C., PHLS Group B, and Streptococcus Working Group. Group B streptococcal disease in UK and Irish infants younger than 90 days. Lancet 363 (2004) 292-294
22. Hemming V.G., Nagarajan K., Hess L.W., Fischer G.W., Wilson S.R., and Thomas L.S. Rapid in vitro replication of Group B Streptococcus in term human amniotic fluid. Gynecol. Obstet. Invest. 19 (1985) 124-129
23. Hughes M.J.G., Moore J.C., Lane J.D., Wilson R., Pribul P.K., Younes Z.N., Dobson R.J., Everest P., Reason A.J., Redfern J.M., Greer F.M., Paxton T., Panico M., Morris H.R., Feldman R.G., and Santangelo J.D. Identification of major outer surface proteins of Streptococcus agalactiae. Infect. Immun. 70 (2002) 1254-1259
24. Jiang S.-M., Ishmael N., Hotopp J.D., Puliti M., Tissi L., Kumar N., Cieslewicz M.J., Tettelin H., and Wessels M.R. Variation in the Group B Streptococcus CsrRS regulon and effects on pathogenicity. J. Bacteriol. 190 (2008) 1956-1965
25. Johri A.K., Margarit I., Broenstrup M., Brettoni C., Hua L., Gygi S.P., Telford J.L., Grandi G., and Paoletti L.C. Transcriptional and proteomic profiles of Group B Streptococcus type V reveal potential adherence proteins associated with high-level invasion. Infect. Immun. 75 (2007) 1473-1483
26. Jones N., Oliver K., Jones Y., Haines A., and Crook D. Carriage of Group B Streptococcus in pregnant women from Oxford, UK. J. Clin. Pathol. 59 (2006) 363-366
27. Kong F., Gidding H.F., Berner R., and Gilbert G.L. Streptococcus agalactiae Cβ protein gene (bac) sequence types, based on the repeated region of the cell-wall-spanning domain: relationship to virulence and a proposed standardized nomenclature. J. Med. Microbiol. 55 (2006) 829-837
28. La Carbona S., Sauvageot N., Giard J.-C., Benachour A., Posteraro B., Auffray Y., Sanguinetti M., and Hartke A. Comparative study of the physiological roles of three peroxidases (NADH peroxidase, Alkyl hydroperoxide reductase and Thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol. Microbiol. 66 (2007) 1148-1163
29. Lemos J.A.C., Chen Y.-Y.M., and Burne R.A. Genetic and physiologic analysis of the groE operon and role of the HrcA repressor in stress gene regulation and acid tolerance in Streptococcus mutans. J. Bacteriol. 183 (2001) 6074-6084
30. Lindahl G.A., Stålhammar-Carlemalm M., and Areschoug T. Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin. Microbiol. Rev. 18 (2005) 102-157
31. Madureira P., Baptista M., Vieira M., Magalhães V., Camelo A., Oliveira L., Ribeiro A., Tavares D., Trieu-Cuot P., Vilanova M., and Ferreira P. Streptococcus agalactiae GAPDH is a virulence-associated immunomodulatory protein. J. Immunol. 178 (2007) 1379-1387
32. Magalhães V., Veiga-Malta I., Almeida M.R., Baptista M., Ribeiro A., Trieu-Cuot P., and Ferreira P. Interaction with human plasminogen system turns on proteolytic activity in Streptococcus agalactiae and enhances its virulence in a mouse model. Microb. Infect. 9 (2007) 1276-1284
33. Manning S.D., Ki M., Marrs C.F., Kugeler K.J., Borchardt S.M., Baker C.J., and Foxman B. The frequency of genes encoding three putative Group B streptococcal virulence factors among invasive and colonizing isolates. BMC Infect. Dis. 6 (2006) 116
34. Mereghetti L., Sitkiewicz I., Green N.M., and Musser J.M. Remodeling of the Streptococcus agalactiae transcriptome in response to growth temperature. PLOS One 3 (2008) e2785
35. Mereghetti L., Sitkiewicz I., Green N.M., and Musser J.M. Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (Group B Streptococcus) in response to incubation with human blood. PLOS One 3 (2008) e3143
36. Nagano N., Nagano Y., Nakano R., Okamoto R., and Inoue M. Genetic diversity of the C protein β-antigen gene and its upstream regions within clonally related groups of type Ia and Ib Group B streptococci. Microbiology 152 (2006) 771-778
37. Nagano N., Nagano Y., and Taguchi F. High expression of the C protein β antigen gene among invasive strains from certain clonally related groups of type Ia and Ib Group B streptococci. Infect. Immun. 70 (2002) 4643-4649
38. Rajagopal L. Understanding the regulation of Group B Streptococcal virulence factors. Future Microbiol. 4 (2009) 201-221
39. Rajagopal L., Vo A., Silvestroni A., and Rubens C.E. Regulation of purine biosynthesis by a eukaryotic-type kinase in Streptococcus agalactiae. Mol. Microbiol. 56 (2005) 1329-1346
40. Riboldi G.P., Verli H., and Frazzon J. Structural studies of the Enterococcus faecalis SufU [Fe-S] cluster protein. BMC Biochem. 10 (2009) 3
41. Ross R.A., Madoff L.C., and Paoletti L.C. Regulation of cell component production by growth rate in the Group B Streptococcus. J. Bacteriol. 181 (1999) 5389-5394
42. Santi I., Grifantini R., Jiang S.M., Brettoni C., Grandi G., Wessels M.R., and Soriani M. CsrRS Regulates Group B Streptococcus virulence gene expression in response to environmental pH: a new perspective on vaccine development. J. Bacteriol. 191 (2009) 5387-5397
43. Serrano L.M., Molenaar D., Wels M., Teusink B., Bron P.A., de Vos W.M., and Smid E.J. Thioredoxin reductase is a key factor in the oxidative stress response of Lactobacillus plantarum WCFS1. Microb. Cell Fact. 6 (2007) 29
44. Shet A., and Ferrieri P. Neonatal and maternal Group B streptococcal infections: a comprehensive review. Ind. J. Med. Res. 120 (2004) 141-150
45. Silvestroni A., Jewell K.A., Lin W.-J., Connelly J.E., Ivancic M.M., Tao W.A., and Rajagopal L. Identification of serine/threonine kinase substrates in the human pathogen Group B Streptococcus. J. Proteome Res. 8 (2009) 2563-2574
46. Sitkiewicz I., Green N.M., Guo N., Bongiovanni A.M., Witkin S.S., and Musser J.M. Transcriptome adaptation of Group B Streptococcus to growth in human amniotic fluid. PLOS One 4 (2009) e6614
47. Sitkiewicz I., and Musser J.M. Analysis of growth-phase regulated genes in Streptococcus agalactiae by global transcript profiling. BMC Microbiol. 9 (2009) 32
48. Slotved H.-C., Kong F., Lambertsen L., Sauer S., and Gilbert G.L. Serotype IX, a proposed new Streptococcus agalactiae serotype. J. Clin. Microbiol. 45 (2007) 2929-2936
49. Sutcliffe I.C., Black G.W., and Harrington D.J. Bioinformatic insights into the biosynthesis of the Group B carbohydrate in Streptococcus agalactiae. Microbiology 154 (2008) 1354-1363
50. Tettelin H., Masignani V., Cieslewicz M.J., Donati C., Medini D., Ward N.L., Angiuoli S.V., Crabtree J., Jones A.L., Durkin A.S., DeBoy R.T., Davidsen T.M., Mora M., Scarselli M., Ros I.M.Y., Peterson J.D., Hauser C.R., Sundaram J.P., Nelson W.C., Madupu R., Brinkac L.M., Dodson R.J., Rosovitz M.J., Sullivan S.A., Daugherty S.C., Haft D.H., Selengut J., Gwinn M.L., Zhou L.W., Zafar N., Khouri H., Radune D., Dimitrov G., Watkins K., O'Connor K.J.B., Smith S., Utterback T.R., White O., Rubens C.E., Grandi G., Madoff L.C., Kasper D.L., Telford J.L., Wessels M.R., Rappuoli R., and Fraser C.M. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. USA 102 (2005) 13950-13955
51. UniProt Consortium. The Universal Protein Resource (UniProt) 2009. Nucl. Acids Res. 37 (2009) D169-D174
52. Vido K., Diemer H., Van Dorsselaer A., Leize E., Juillard V., Gruss A., and Gaudu P. Roles of thioredoxin reductase during the aerobic life of Lactococcus lactis. J. Bacteriol. 187 (2005) 601-610
53. Woodbury R., and Haldenwang W.G. HrcA is a negative regulator of the dnaK and groESL operons of Streptococcus pyogenes. Biochem. Biophys. Res. Commun. 302 (2003) 722-727
54. Yang H.-H., Madoff L.C., Guttormsen H.-K., Liu Y.-D., and Paoletti L.C. Recombinant Group B Streptococcus beta C protein and a variant with the deletion of its immunoglobulin A-binding site are protective mouse maternal vaccines and effective carriers in conjugate vaccines. Infect. Immun. 75 (2007) 3455-3461
55. Yamamoto Y., Poyart C., Trieu-Cuot P., Lamberet G., Gruss A., and Gaudu P. Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence. Mol. Microbiol. 56 (2005) 525-534
56. Zhang M., McDonald F.M., Sturrock S.S., Charnock S.J., Humphery-Smith I., and Black G.W. Group A Streptococcus cell-associated pathogenic proteins as revealed by growth in hyaluronic acid-enriched media. Proteomics 7 (2007) 1379-1390