CcpA-dependent and -independent control of beta-galactosidase expression in Streptococcus pneumoniae occurs via regulation of an upstream phosphotransferase system-encoding operon

Journal of Bacteriology

Volumn 189, Issue 14, 2007, Pages 5183-5192

  Kaufman, Greer E ^a   Yother, Janet ^a,b  

^a University of Alabama at Birmingham   (United States)

^b BBRB 661/12 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; GLUCOSE; MEMBRANE PROTEIN; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASE; PROTEIN BGAA; PROTEIN CCPA; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BGAA GENE; CARBON METABOLISM; CRE GENE; CULTURE MEDIUM; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENETIC TRANSCRIPTION; NASOPHARYNX; NONHUMAN; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PTS GENE; REPRESSOR GENE; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; BETA-GALACTOSIDASE; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; MOLECULAR SEQUENCE DATA; MUTATION; OPERON; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; REPRESSOR PROTEINS; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION, GENETIC;

STREPTOCOCCUS PNEUMONIAE;

EID: 34447517615     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00449-07     Document Type: Article

References (49)

1. Advisory Committee on Immunization Practice. 1997. Prevention of pneumococcal disease. Morb. Mortal. Wkly. Rep. 46:1-24.
2. Alloing, G., C. Granadel, D. A. Morrison, and J. P. Claverys. 1996. Competence pheromone, oligopeptide permease, and induction of competence in Streptococcus pneumoniae. Mol. Microbiol. 21:471-478.
3. Alwine, J. C., D. J. Kemp, and G. R. Stark. 1977. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl- paper and hybridization with DNA probes. Proc. Natl. Acad. Sci. USA 74:5350-5354.
4. Austrian, R. 1986. Some aspects of the pneumococcal carrier state. J. Antimicrob. Chemother. 18(Suppl. A):35-45.
5. Avery, O. T., C. M. MacLeod, and M. McCarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a deoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158.
6. Baker, E. H., N. Clark, A. L. Brennan, D. A. Fisher, K. M. Gyi, M. E. Hodson, B. J. Philips, D. L. Baines, and D. M. Wood. 2007. Hyperglycaemia and cystic fibrosis alter respiratory fluid glucose concentrations estimated by breath condensate analysis. J. Appl. Physiol. 102:1969-1975.
7. Bentley, S. D., D. M. Aanensen, A. Mavroidi, D. Saunders, E. Rabbinowitsch, M. Collins, K. Donohoe, D. Harris, L. Murphy, M. A. Quail, G. Samuel, I. C. Skovsted, M. S. Kaltoft, B. Barrell, P. R. Reeves, J. Parkhill, and B. G. Spratt. 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet. 2:262-269.
8. Crain, M. J., W. D. Waltman II, J. S. Turner, J. Yother, D. F. Talkington, L. S. McDaniel, B. M. Gray, and D. E. Briles. 1990. Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae. Infect. Immun. 58:3293-3299.
9. Deutscher, J., C. Francke, and P. W. Postma. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol Rev. 70:939-1031.
10. Dong, Y., Y. Y. Chen, and R. A. Burne. 2004. Control of expression of the arginine deiminase operon of Streptococcus gordonii by CcpA and Flp. J. Bacteriol. 186:2511-2514.
11. Georgellis, D., S. Arvidson, and A. von Gabain. 1992. Decay of ompA mRNA and processing of 9S RNA are immediately affected by shifts in growth rate, but in opposite manners. J. Bacteriol. 174:5382-5390.
12. Giammarinaro, P., and J. C. Paton. 2002. Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae. Infect. Immun. 70:5454-5461.
13. Gosalbes, M. J., V. Monedero, C. A. Alpert, and G. Perez-Martinez. 1997. Establishing a model to study the regulation of the lactose operon in Lactobacillus casei. FEMS Microbiol. Lett. 148:83-89.
14. Hardy, G. G., M. J. Caimano, and J. Yother. 2000. Capsule biosynthesis and basic metabolism in Streptococcus pneumoniae are linked through the cellular phosphoglucomutase. J. Bacteriol. 182:1854-1863.
15. Hava, D. L., and A. Camilli. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45:1389-1406.
16. Hoskins, J., W. E. Alborn, Jr., J. Arnold, L. C. Blaszczak, S. Burgett, B. S. DeHoff, S. T. Estrem, L. Fritz, D. J. Fu, W. Fuller, C. Geringer, R. Gilmour, J. S. Glass, H. Khoja, A. R. Kraft, R. E. Lagace, D. J. LeBlanc, L. N. Lee, E. J. Lefkowitz, J. Lu, P. Matsushima, S. M. McAhren, M. McHenney, K. McLeaster, C. W. Mundy, T. I. Nicas, F. H. Norris, M. O'Gara, R. B. Peery, G. T. Robertson, P. Rockey, P. M. Sun, M. E. Winkler, Y. Yang, M. Young-Bellido, G. Zhao, C. A. Zook, R. H. Baltz, S. R. Jaskunas, P. R. Rosteck, Jr., P. L. Skatrud, and J. I. Glass. 2001. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183:5709-5717.
17. Iyer, R., N. S. Baliga, and A. Camilli. 2005. Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J. Bacteriol. 187:8340-8349.
18. Kamerling, J. P. 2000. Pneumococcal polysaccharides: a chemical view, p. 81-114. In A. Tomasz (cd.), Streptococcus pneumoniae: molecular biology and mechanisms of disease. Mary Ann. Liebert, Inc., Larchmont, NY.
19. Kim, J. H., and G. H. Chambliss. 1997. Contacts between Bacillus subtilis catabolite regulatory protein CcpA and amyO target site. Nucleic Acids Res. 25:3490-3496.
20. Kim, J. H., Z. T. Guvener, J. Y. Cho, K. C. Chung, and G. H. Chambliss. 1995. Specificity of DNA binding activity of the Bacillus subtilis catabolite control protein CcpA. J. Bacteriol. 177:5129- 5134.
21. Kim, J. H., Y. K. Yang, and G. H. Chambliss. 2005. Evidence that Bacillus catabolite control protein CcpA interacts with RNA polymerase to inhibit transcription. Mol. Microbiol. 56:155-162.
22. Kim, J. O., S. Romero-Steiner, U. B. Sorensen, J. Blom, M. Carvalho, S. Barnard, G. Carlone, and J. N. Weiser. 1999. Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect. Immun. 67:2327-2333.
23. Kim, J. O., and J. N. Weiser. 1998. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J. Infect. Dis. 177:368-377.
24. King, S. J., K. R. Hippe, J. M. Gould, D. Bae, S. Peterson, R. T. Cline, C. Fasching, E. N. Janoff, and J. N. Weiser. 2004. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol. Microbiol. 54:159-171.
25. King, S. J., K. R. Hippe, and J. N. Weiser. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol. Microbiol. 59:961-974.
26. Kojima, K., M. Iwamori, S. Takasaki, K. Kubushiro, S. Nozawa, R. Iizuka, and Y. Nagai. 1987. Diplococcal beta-galactosidase with a specificity reacting to beta 1-4 linkage but not to beta 1-3 linkage as a useful exoglycosidase for the structural elucidation of glycolipids. Anal. Biochem. 165:465-469.
27. Lanie, J. A., W. L. Ng, K. M. Kazmierczak, T. M. Andrzejewski, T. M. Davidsen, K. J. Wayne, H. Tettelin, J. I. Glass, and M. E. Winkler. 2007. Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189:38-51.
28. Martin, B., O. Humbert, M. Camara, E. Guenzi, J. Walker, T. Mitchell, P. Andrew, M. Prudhomme, G. Alloing, R. Hakenbeck, et al. 1992. A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res. 20:3479-3483.
29. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Miwa, Y., A. Nakata, A. Ogiwara, M. Yamamoto, and Y. Fujita. 2000. Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucleic Acids Res. 28:1206-1210.
31. Philips, B. J., J. X. Meguer, J. Redman, and E. H. Baker. 2003. Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intensive Care Med. 29:2204-2210.
32. Schumacher, M. A., G. S. Allen, M. Diel, G. Seidel, W. Hillen, and R. G. Brennan. 2004. Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P. Cell 118:731-741.
33. Shivers, R. P., S. S. Dineen, and A. L. Sonenshein. 2006. Positive regulation of Bacillus subtilis ackA by CodY and CcpA: establishing a potential hierarchy in carbon flow. Mol. Microbiol. 62:811-822.
34. Simpson, C. L., and R. R. Russell. 1998. Identification of a homolog of CcpA catabolite repressor protein in Streptococcus mutans. Infect. Immun. 66:2085-2092.
35. Sonenshein, A. L. 2005. CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8:203-207.
36. Spik, G., G. Strecker, B. Fournet, S. Bouquelet, J. Montreuil, L. Dorland, H. van Halbeek, and J. F. Vliegenthart. 1982. Primary structure of the glycans from human lactotransferrin. Eur. J. Biochem. 121:413-419.
37. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
38. Titgemeyer, F., and W. Hillen. 2002. Global control of sugar metabolism: a gram-positive solution. Antonie Leeuwenhoek 82:59-71.
39. Turinsky, A. J., F. J. Grundy, J. H. Kim, G. H. Chambliss, and T. M. Henkin. 1998. Transcriptional activation of the Bacillus subtilis ackA gene requires sequences upstream of the promoter. J. Bacteriol. 180:5961-5967.
40. Warner, J. B., and J. S. Lolkema. 2003. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
41. Weickert, M. J., and S. Adhya. 1992. A family of bacterial regulators homologous to Gal and Lac repressors. J. Biol. Chem. 267:15869-15874.
42. Weickert, M. J., and G. H. Chambliss. 1990. Site-directed mutagenesis of a catabolite repression operator sequence in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 87:6238-6242.
43. Weiser, J. N., D. Bae, H. Epino, S. B. Gordon, M. Kapoor, L. A. Zenewicz, and M. Shchepetov. 2001. Changes in availability of oxygen accentuate differences in capsular polysaccharide expression by phenotypic variants and clinical isolates of Streptococcus pneumoniae. Infect. Immun. 69:5430-5439.
44. West, A. H., and A. M. Stock. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369-376.
45. Xayarath, B., and J. Yother. 2007. Mutations blocking side chain assembly, polymerization, or transport of a Wzy-dependent Streptococcus pneumoniae capsule are lethal in the absence of suppressor mutations and can affect polymer transfer to the cell wall. J. Bacteriol. 189:3369-3381.
46. Yother, J., G. L. Handsome, and D. E. Briles. 1992. Truncated forms of PspA that arc secreted from Streptococcus pneumoniae and their use in functional studies and cloning of the pspA gene. J. Bacteriol. 174:610-618.
47. Zahner, D., and R. Hakenbeck. 2000. The Streptococcus pneumoniae beta-galactosidase is a surface protein. J. Bacteriol. 182:5919-5921.
48. Zeng, L., Y. Dong, and R. A. Burne. 2006. Characterization of cis-acting sites controlling arginine deiminase gene expression in Streptococcus gordonii. J. Bacteriol. 188:941-949.
49. Zysk, G., R. J. Bongaerts, E. ten Thoren, G. Bethe, R. Hakenbeck, and H. P. Heinz. 2000. Detection of 23 immunogenic pneumococcal proteins using convalescent-phase serum. Infect. Immun. 68:3740-3743.