Downregulation of GbpB, a component of the VicRK regulon, affects biofilm formation and cell surface characteristics of Streptococcus mutans

Infection and Immunity

Volumn 79, Issue 2, 2011, Pages 786-796

  Duque, Cristiane ^a   Stipp, Rafael N ^a   Wang, Bing ^b,d   Smith, Daniel J ^c   Höfling, José F ^a   Kuramitsu, Howard K ^b   Duncan, Margaret J ^c   Mattos Graner, Renata O ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY AT BUFFALO   (United States)

^c FORSYTH INSTITUTE   (United States)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GBPB PROTEIN; SUCROSE; TETRACYCLINE; UNCLASSIFIED DRUG;

ANTIBIOTIC SENSITIVITY; ARTICLE; AUTOLYSIS; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOFILM; CELL SHAPE; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; HYDROPHOBICITY; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; REGULON; STREPTOCOCCUS MUTANS;

BACTERIAL PROTEINS; BIOFILMS; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MUTATION; REGULON; RNA, BACTERIAL; STREPTOCOCCUS MUTANS; SUCROSE;

EID: 79251485283     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00725-10     Document Type: Article

References (55)

1. Ahn, S. J., and R. A. Burne. 2006. The atlA operon of Streptococcus mutans: role in autolysin maturation and cell surface biogenesis. J. Bacteriol. 188:6877-6888.
2. Ahn, S. J., and R. A. Burne. 2007. Effects of oxygen on biofilm formation and the AtlA autolysin of Streptococcus mutans. J. Bacteriol. 189:6293-6302.
3. Ahn, S. J., Z. T. Wen, and R. A. Burne. 2007. Effects of oxygen on virulence traits of Streptococcus mutans. J. Bacteriol. 189:8519-8527.
4. Banas, J. A., and M. M. Vickerman. 2003. Glucan-binding proteins of the oral streptococci. Crit. Rev. Oral Biol. Med. 14:89-99.
5. Barendt, S. M., et al. 2009. Influences of capsule on cell shape and chain formation of wild-type and pcsB mutants of serotype 2 Streptococcus pneumoniae. J. Bacteriol. 191:3024-3040.
6. Bateman, B. T., N. P. Donegan, T. M. Jarry, M. Palma, and A. L. Cheung. 2001. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69:7851-7857.
7. Biswas, I., L. Drake, D. Erkina, and S. Biswas. 2008. Involvement of sensor kinases in the stress tolerance response of Streptococcus mutans. J. Bacteriol. 190:68-77.
8. Biswas, S., and I. Biswas. 2005. Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans. Infect. Immun. 73:6923-6934.
9. Biswas, S., and I. Biswas. 2006. Regulation of the glucosyltransferase (gtfBC) operon by CovR in Streptococcus mutans. J. Bacteriol. 188:988-998.
10. Brown, T. A., Jr., et al. 2005. A hypothetical protein of Streptococcus mutans is critical for biofilm formation. Infect. Immun. 73:3147-3151.
11. Catt, D. M., and R. L. Gregory. 2005. Streptococcus mutans murein hydrolase. J. Bacteriol. 187:7863-7865.
12. Chia, J. S., et al. 2001. A 60-kilodalton immunodominant glycoprotein is essential for cell wall integrity and the maintenance of cell shape in Streptococcus mutans. Infect. Immun. 69:6987-6998.
13. Chia, J. S., Y. Y. Lee, P. T. Huang, and J. Y. Chen. 2001. Identification of stress-responsive genes in Streptococcus mutans by differential display reverse transcription-PCR. Infect. Immun. 69:2493-2501.
14. Deng, D. M., M. J. Liu, J. M. Ten Cate, and W. Crielaard. 2007. The VicRK system of Streptococcus mutans responds to oxidative stress. J. Dent. Res. 86:606-610.
15. Dubrac, S., P. Bisicchia, K. M. Devine, and T. Msadek. 2008. A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol. Microbiol. 70:1307-1322.
16. Dubrac, S., and T. Msadek. 2004. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J. Bacteriol. 186:1175-1181.
17. Fujita, K., M. Matsumoto-Nakano, S. Inagaki, and T. Ooshima. 2007. Biological functions of glucan-binding protein B of Streptococcus mutans. Oral Microbiol. Immunol. 22:289-292.
18. Fujiwara, T., et al. 1998. Molecular analyses of glucosyltransferase genes among strains of Streptococcus mutans. FEMS Microbiol. Lett. 161:331-336.
19. Gibbons, R. J., and I. Etherden. 1983. Comparative hydrophobicities of oral bacteria and their adherence to salivary pellicles. Infect. Immun. 41:1190-1196.
20. Higuchi, M., et al. 1999. Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. J. Bacteriol. 181:5940-5947. (Pubitemid 29459903)
21. Hughes, J. D., P. W. Estep, S. Tavazoie, and G. M. Church. 2000. Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J. Mol. Biol. 296: 1205-1214.
22. Lau, P. C., C. K. Sung, J. H. Lee, D. A. Morrison, and D. G. Cvitkovitch. 2002. PCR ligation mutagenesis in transformable streptococci: application and efficiency. J. Microbiol. Methods 49:193-205.
23. Layec, S., B. Decaris, and N. Leblond-Bourget. 2008. Characterization of proteins belonging to the CHAP-related superfamily within the Firmicutes. J. Mol. Microbiol. Biotechnol. 14:31-40.
24. Lynch, D. J., T. L. Fountain, J. E. Mazurkiewicz, and J. A. Banas. 2007. Glucan-binding proteins are essential for shaping Streptococcus mutans bio-film architecture. FEMS Microbiol. Lett. 268:158-165.
25. Lyon, W. R., and M. G. Caparon. 2004. Role for serine protease HtrA (DegP) of Streptococcus pyogenes in the biogenesis of virulence factors SpeB and the hemolysin streptolysin S. Infect. Immun. 72:1618-1625.
26. Macrina, F. L., J. A. Tobian, K. R. Jones, R. P. Evans, and D. B. Clewell. 1982. A cloning vector able to replicate in Escherichia coli and Streptococcus sanguis. Gene 19:345-353.
27. Matsumoto-Nakano, M., K. Fujita, and T. Ooshima. 2007. Comparison of glucan-binding proteins in cariogenicity of Streptococcus mutans. Oral Microbiol. Immunol. 22:30-35.
28. Mattos-Graner, R. O., et al. 2001. Cloning of the Streptococcus mutans gene encoding glucan binding protein B and analysis of genetic diversity and protein production in clinical isolates. Infect. Immun. 69:6931-6941.
29. Mattos-Graner, R. O., M. H. Napimoga, K. Fukushima, M. J. Duncan, and D. J. Smith. 2004. Comparative analysis of Gtf isozyme production and diversity in isolates of Streptococcus mutans with different biofilm growth phenotypes. J. Clin. Microbiol. 42:4586-4592.
30. Mattos-Graner, R. O., K. A. Porter, D. J. Smith, Y. Hosogi, and M. J. Duncan. 2006. Functional analysis of glucan binding protein B from Streptococcus mutans. J. Bacteriol. 188:3813-3825.
31. Ng, W. L., K. M. Kazmierczak, and M. E. Winkler. 2004. Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Mol. Microbiol. 53:1161-1175.
32. Ng, W. L., et al. 2003. Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol. Microbiol. 50:1647-1663.
33. Ng, W. L., H. C. Tsui, and M. E. Winkler. 2005. Regulation of the pspA virulence factor and essential pcsB murein biosynthetic genes by the phosphorylated VicR (YycF) response regulator in Streptococcus pneumoniae. J. Bacteriol. 187:7444-7459.
34. Nogueira, R. D., et al. 2007. Age-specific salivary immunoglobulin A response to Streptococcus mutans GbpB. Clin. Vaccine Immunol. 14:804-807.
35. Nogueira, R. D., A. C. Alves, M. H. Napimoga, D. J. Smith, and R. O. Mattos-Graner. 2005. Characterization of salivary immunoglobulin A responses in children heavily exposed to the oral bacterium Streptococcus mutans: influence of specific antigen recognition in infection. Infect. Immun. 73:5675-5684.
36. Perry, D., and H. K. Kuramitsu. 1981. Genetic transformation of Streptococcus mutans. Infect. Immun. 32:1295-1297.
37. Reinscheid, D. J., K. Ehlert, G. S. Chhatwal, and B. J. Eikmanns. 2003. Functional analysis of a PcsB-deficient mutant of group B streptococcus. FEMS Microbiol. Lett. 221:73-79.
38. Reinscheid, D. J., B. Gottschalk, A. Schubert, B. J. Eikmanns, and G. S. Chhatwal. 2001. Identification and molecular analysis of PcsB, a protein required for cell wall separation of group B streptococcus. J. Bacteriol. 183:1175-1183.
39. Rigoulay, C., et al. 2005. Comparative analysis of the roles of HtrA-like surface proteases in two virulent Staphylococcus aureus strains. Infect. Immun. 73:563-572.
40. Roth, F. P., J. D. Hughes, P. W. Estep, and G. M. Church. 1998. Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation. Nat. Biotechnol. 16:939-945.
41. Sato, Y., Y. Yamamoto, and H. Kizaki. 1997. Cloning and sequence analysis of the gbpC gene encoding a novel glucan-binding protein of Streptococcus mutans. Infect. Immun. 65:668-675.
42. Senadheera, D., et al. 2009. Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. J. Bacteriol. 191:6415-6424.
43. Senadheera, M. D., et al. 2005. A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J. Bacteriol. 187:4064-4076.
44. Senadheera, M. D., et al. 2007. The Streptococcus mutans vicX gene product modulates gtfB/C expression, biofilm formation, genetic competence, and oxidative stress tolerance. J. Bacteriol. 189:1451-1458.
45. Smith, D. J., H. Akita, W. F. King, and M. A. Taubman. 1994. Purification and antigenicity of a novel glucan-binding protein of Streptococcus mutans. Infect. Immun. 62:2545-2552.
46. Smith, D. J., W. F. King, H. Akita, and M. A. Taubman. 1998. Association of salivary immunoglobulin A antibody and initial mutans streptococcal infection. Oral Microbiol. Immunol. 13:278-285.
47. Smith, D. J., W. F. King, and M. A. Taubman. 1995. Synthesis, cellular distribution and immunogenicity of S. mutans glucan-binding protein (GbpB59). J. Dent. Res. 74:123.
48. Smith, D. J., and M. A. Taubman. 1996. Experimental immunization of rats with a Streptococcus mutans 59-kilodalton glucan-binding protein protects against dental caries. Infect. Immun. 64:3069-3073.
49. Stipp, R. N., R. B. Goncalves, J. F. Hofling, D. J. Smith, and R. O. Mattos-Graner. 2008. Transcriptional analysis of gtfB, gtfC, and gbpB and their putative response regulators in several isolates of Streptococcus mutans. Oral Microbiol. Immunol. 23:466-473.
50. Thompson, W., E. C. Rouchka, and C. E. Lawrence. 2003. Gibbs Recursive Sampler: finding transcription factor binding sites. Nucleic Acids Res. 31:3580-3585.
51. Vollmer, W., B. Joris, P. Charlier, and S. Foster. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259-286.
52. Vriesema, A. J., R. Brinkman, J. Kok, J. Dankert, and S. A. Zaat. 2000. Broad-host-range shuttle vectors for screening of regulated promoter activity in viridans group streptococci: isolation of a pH-regulated promoter. Appl. Environ. Microbiol. 66:535-542.
53. Wang, B., and H. K. Kuramitsu. 2005. Inducible antisense RNA expression in the characterization of gene functions in Streptococcus mutans. Infect. Immun. 73:3568-3576.
54. Welin, J., J. C. Wilkins, D. Beighton, and G. Svensater. 2004. Protein expression by Streptococcus mutans during initial stage of biofilm formation. Appl. Environ. Microbiol. 70:3736-3741.
55. Xiao, J., and H. Koo. 2010. Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms. J. Appl. Microbiol. 108:2103-2113.