Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae

Journal of Bacteriology

Volumn 187, Issue 24, 2005, Pages 8340-8349

  Iyer, Ramkumar ^b   Baliga, Nitin S ^c   Camilli, Andrew ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSIDASE; ALPHA GLUCOSIDASE; BACTERIAL PROTEIN; BETA GALACTOSIDASE; BETA GLUCOSIDASE; CARBON; CATABOLITE CONTROL PROTEIN A; GENOMIC DNA; GLUCOSE; LACTOSE; MANNITOL; MESSENGER RNA; N ACETYLGLUCOSAMINE; RAFFINOSE; RIBONUCLEASE; SUCROSE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BIOSYNTHESIS; CARBOHYDRATE METABOLISM; ENZYME ASSAY; ESCHERICHIA COLI; LUNG; METABOLIC REGULATION; NASOPHARYNX; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; RESPIRATORY TRACT INFECTION; STREPTOCOCCUS PNEUMONIAE; TANDEM MASS SPECTROMETRY;

ALPHA-GALACTOSIDASE; ALPHA-GLUCOSIDASES; ANIMALS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; BETA-GLUCOSIDASE; CARBOHYDRATE METABOLISM; CARRIER STATE; CELL WALL; COLONY COUNT, MICROBIAL; DNA-BINDING PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; LACTOSE; MICE; MUTAGENESIS, INSERTIONAL; NASOPHARYNX; PNEUMOCOCCAL INFECTIONS; PNEUMONIA, PNEUMOCOCCAL; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, MESSENGER; STREPTOCOCCUS PNEUMONIAE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; POSIBACTERIA; STREPTOCOCCUS PNEUMONIAE;

EID: 28844482813     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.24.8340-8349.2005     Document Type: Article

References (82)

1. Asanuma, N., T. Yoshii, and T. Hino. 2004. Molecular characterization of CcpA and involvement of this protein in transcriptional regulation of lactate dehydrogenase and pyruvate formate-lyase in the ruminai bacterium Streplococcus bovis. Appl. Environ. Microbiol. 70:5244-5251.
2. Aslanidis, C., K. Schmid, and R. Schmitt. 1989. Nucleotide sequences and operon structure of plasmid-borne genes mediating uptake and utilization of raffinose in Escherichia coll. J. Bacteriol. 171:6753-6763.
3. Barletta, R. G., and R. Curtiss, 3rd. 1989. Impairment of melibiose utilization in Streptococcus mulans serotype c gtfA mutants. Infect. Immun. 57:992-995.
4. Belitsky, B. R., H. J. Kim, and A. L. Sonenshein. 2004. CcpA-dependent regulation of Bacillus subtilis glutamate dehydrogenase gene expression. J. Bacteriol. 186:3392-3398.
5. Bender, M. H., R. T. Cartee, and J. Yother. 2003. Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J. Bacteriol. 185:6057-6066.
6. Bergmann, S., M. Rohde, G. S. Chhatwal, and S. Hammerschmidt. 2001. α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40:1273-1287.
7. Bricker, A. L., and A. Camilli. 1999. Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol. Lett. 172:131-135.
8. Brochu, D., and C. Vadeboncoeur. 1999. The HPr(Ser) kinase of Streptococcus salivarius: purification, properties, and cloning of the hprK gene. J. Bacteriol. 181:709-717.
9. Chasin, L. A., and B. Magasanik. 1968. Induction and repression of the histidine-degrading enzymes of Bacillus subtilis. J. Biol. Chem. 243:5165-5178.
10. Chauvaux, S. 1996. CcpA and HPr(ser-P): mediators of catabolite repression in Bacillus subtilis. Res. Microbiol. 147:518-522.
11. Chauvaux, S., I. T. Paulsen, and M. H. Saier, Jr. 1998. CcpB, a novel transcription factor implicated in catabolite repression in Bacillus subtilis. J. Bacteriol. 180:491-197.
12. Darbon, E., P. Servant, S. Poncet, and J. Deutscher. 2002. Antitermination by GlpP, catabolite repression via CcpA and inducer exclusion triggered by P-GlpK dephosphorylation control Bacillus subtilis glpFK expression. Mol. Microbiol. 43:1039-1052.
13. Deutscher, J., E. Kuster, U. Bergstedt, V. Charrier, and W. Hillen. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol. Microbiol. 15:1049-1053.
14. Deutscher, J., J. Reizer, C. Fischer, A. Galinier, M. H. Saier, Jr., and M. Steinmetz. 1994. Loss of protein kinase-catalyzed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J. Bacteriol. 176:3336-3344.
15. de Vos, W. M., I. Boerrigter, R. J. van Rooyen, B. Reiche, and W. Hengstenberg. 1990. Characterization of the lactose-specific enzymes of the phosphotransferase system in Lactococcus lactis. J. Biol. Chem. 265:22554-22560.
16. Doan, T., and S. Aymerich. 2003. Regulation of the central glycolytic genes in Bacillus subtilis: binding of the represser CggR to its single DNA target sequence is modulated by fructose-l,6-bisphosphate. Mol. Microbiol. 47:1709-1721.
17. 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.
18. Dubreuil, J. D., M. Jacques, D. Brochu, M. Frenette, and C. Vadeboncoeur. 1996. Surface location of HPr, a phosphocarrier of the phosphoenolpyruvate: sugar phosphotransferase system in Streptococcus suis. Microbiology 142(Pt. 4):837-843.
19. Egeter, O., and R. Bruckner. 1996. Catabolite repression mediated by the catabolite control protein CcpA in Staphylococcus xylosus. Mol. Microbiol. 21:739-749.
20. Ehinger, S., W. D. Schubert, S. Bergmann, S. Hammerschmidt, and D. W. Heinz. 2004. Plasmin(ogen)-binding α-enolase from Streptococcus pneumoniae: crystal structure and evaluation of plasmin(ogen)-binding sites. J. Mol. Biol. 343:997-1005.
21. Frey, N., S. Nessler, S. Fieulaine, K. Vaillancourt, M. Frenette, and C. Vadeboncoeur. 2003. The HPr(Ser) kinase of Streptococcus salivarius: a hexameric bifunctional enzyme controlled by glycolytic intermediates and inorganic phosphate. FEMS Microbiol. Lett. 224:67-72.
22. Giammarinaro, P., and J. C. Paton. 2002. Role of RegM, a homologue of the catabolite represser protein CcpA, in the virulence of Streptococcus pneumoniae. Infect. Immun. 70:5454-5461.
23. Gilbreth, S. E., A. K. Benson, and R. W. Hutkins. 2004. Catabolite repression and virulence gene expression in Listeria monocytogenes. Curr. Microbiol. 49:95-98.
24. Crunch, F. J., A. J. Turinsky, and T. M. Henkin. 1994. Catabolite regulation of Bacillus subtilis acetate and acetoin utilization genes by CcpA. J. Bacteriol. 176:4527-4533.
25. Crunch, F. J., D. A. Waters, T. Y. Takova, and T. M. Henkin. 1993. Identification of genes involved in utilization of acetate and acetoin in Bacillus subtilis. Mol. Microbiol. 10:259-271.
26. Guffanti, A. A., and W. A. Corpe. 1975. Maltose metabolism of Pseudomonas fluorescens. J. Bacteriol. 124:262-268.
27. Hava, D. L., and A. Camilli. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45:1389-1406.
28. Hava, D. L., C. J. Hemsley, and A. Camilli. 2003. Transcriptional regulation in the Sirepiococcuspneumoniae rlrA pathogenicity islet by RlrA. J. Bacteriol. 185:413-121.
29. Hemsley, C., E. Joyce, D. L. Hava, A. Kawale, and A. Camilli. 2003. MgrA, an orthologue of Mga, acts as a transcriptional repressor of the genes within the rlrA pathogenicity islet in Streptococcus pneumoniae. J. Bacteriol. 185:6640-6647.
30. Henkin, T. M. 1996. The role of CcpA transcriptional regulator in carbon metabolism in Bacillus subtilis. FEMS Microbiol. Lett. 135:9-15.
31. Henkin, T. M., F. J. Crunch, W. L. Nicholson, and G. H. Chambliss. 1991. Catabolite repression of α-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacl and galR repressers. Mol. Microbiol. 5:575-584.
32. Horten, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. BioTechniques 8:528-535.
33. Hueck, C. J., and W. Hillen. 1995. Catabolite repression in Bacillus subtilis: a global regulatory mechanism for the gram-positive bacteria? Mol. Microbiol. 15:395-401.
34. Jiresova, M., Z. Dobrova, J. Naprstek, P. Rysavy, and J. Janecek. 1983. Induction of β-D-glucosidase in Streptomyces granaticolor. Folia Microbiol. 28:379-385.
35. Jourlin-Castelli, C., N. Mani, M. M. Nakano, and A. L. Sonenshein. 2000. CcpC, a novel regulator of the LysR family required for glucose repression of the citB gene in Bacillus subtilis. J. Mol. Biol. 295:865-878.
36. Kim, H. J., A. Roux, and A. L. Sonenshein. 2002. Direct and indirect roles of CcpA in regulation of Bacillus subtilis Krebs cycle genes. Mol. Microbiol. 45:179-190.
37. 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.
38. Kraus, A., E. Kuster, A. Wagner, K. Hoffmann, and W. Hillen. 1998. Identification of a co-repressor binding site in catabolite control protein CcpA. Mol. Microbiol. 30:955-963.
39. Lacks, S. 1966. Integration efficiency and genetic recombination in pneumococcal transformation. Genetics 53:207-235.
40. Ling, E., G. Feldman, M. Portnoi, R. Dagan, K. Overweg, F. Mulholland, V. Chalifa-Caspi, J. Wells, and Y. Mizrachi-Nebenzahl. 2004. Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin. Exp. Immunol. 138:290-298.
41. Ludwig, H., C. Meinken, A. Matin, and J. Stulke. 2002. Insufficient expression of the ilv-leu operon encoding enzymes of branched-chain amino acid biosynthesis limits growth of a Bacillus subtilis ccpA mutant. J. Bacteriol. 184:5174-5178.
42. Mahr, K., W. Hillen, and F. Titgemeyer. 2000. Carbon catabolite repression in Lactobacillus pentosus: analysis of the ccpA region. Appl. Environ. Microbiol. 66:277-283.
43. Marasco, R., C. T. Lago, and M. De Felice. 1995. Utilization of cellobiose and other β-D-glucosides in Agrobacterium tumefaciens. Res. Microbiol. 146:485-192.
44. Marra. A., J. Asundi, M. Bartilson, S. Lawson, F. Fang, J. Christine, C. Wiesner, D. Brigham, W. P. Schneider, and A. E. Hromockyj. 2002. Differential fluorescence induction analysis of Streptococcus pneumoniae identifies genes involved in pathogenesis. Infect. Immun. 70:1422-1433.
45. Martin, B., M. Prudhomme, G. Alloing, C. Granadel, and J. P. Claverys. 2000. Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol. Microbiol. 38:867-878.
46. Milenbachs, A. A., D. P. Brown, M. Moors, and P. Youngman. 1997. Carbon-source regulation of virulence gene expression in Listeria monocytogenes. Mol. Microbiol. 23:1075-1085.
47. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
48. Miwa, Y., K. Nagura, S. Eguchi, H. Fukuda, J. Deutscher, and Y. Fujita. 1997. Catabolite repression of the Bacillus subtilis gnt operon exerted by two catabolite-responsive elements. Mol. Microbiol. 23:1203-1213.
49. Monedero, V, O. P. Kuipers, E. Jamet, and J. Deutscher. 2001. Regulatory functions of serine-46-phosphorylated HPr in Lactococcus lactis. J. Bacteriol. 183:3391-3398.
50. Nieto, C., M. Espinosa, and A. Puyet. 1997. The maltose/maltodextrin regulon of Streptococcus pneumoniae. Differential promoter regulation by the transcriptional represser MalR. J. Biol. Chem. 272:30860-30865.
51. Orihuela, C. J., J. N. Radin, J. E. Sublett, G. Gao, D. Kaushal, and E. I. Tuomanen. 2004. Microarray analysis of pneumococcal gene expression during invasive disease. Infect. Immun. 72:5582-5596.
52. Paton, J. C., and P. Giammarinaro. 2001. Genome-based analysis of pneumococcal virulence factors: the quest for novel vaccine antigens and drug targets. Trends Microbiol. 9:515-518.
53. Pericone, C. D., S. Park, J. A. Imlay, and J. N. Weiser. 2003. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J. Bacteriol. 185:6815-6825.
54. Poncet, S., I. Mijakovic, S. Nessler, V. Gueguen-Chaignon, V. Chaptal, A. Galinier, G. Boel, A. Maze, and J. Deutscher. 2004. HPr kinase/phosphorylase, a Walker motif A-containing bifunctional sensor enzyme controlling catabolite repression in gram-positive bacteria. Biochim. Biophys. Acta 1697:123-135.
55. Postma, P. W., and J. W. Lengeler. 1985. Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol. Rev. 49:232-269.
56. Ramseier, T. M, J. Reizer, E. Kuster, W. Hillen, and M. H. Saier. 1995. In vitro binding of the CcpA protein of Bacillus megaterium to cis-acting catabolite responsive elements (CREs) of gram-positive bacteria. FEMS Microbiol. Lett. 129:207-213.
57. Reizer, J., S. Bachem, A. Reizer, M. Arnaud, M. H. Saier, Jr., and J. Stulke. 1999. Novel phosphotransferase system genes revealed by genome analysis-the complete complement of PTS proteins encoded within the genome of Bacillus subtilis. Microbiology 145(Pt. 12):3419-3429.
58. Reizer, J., C. Heischen, F. Titgemeyer, C. Rivolta, R. Rabus, J. Stulke, D. Karamata, M. H. Saier, Jr., and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:1157-1169.
59. Rogers, J. D., and F. A. Scannapieco. 2001. RegG, a CcpA homolog, participates in regulation of amylase-binding protein A gene (abpA) expression in Streptococcus gordonii. J. Bacteriol. 183:3521-3525.
60. Rosenow, C., M. Maniar, and J. Trias. 1999. Regulation of the α-galactosidase activity in Streptococcus pneumoniae: characterization of the raffinose utilization system. Genome Res. 9:1189-1197.
61. Rowland, P., O. Bjornberg, F. S. Nielsen, K. F. Jensen, and S. Larsen. 1998. The crystal structure of Lactococcus lactis dihydroorotate dehydrogenase A complexed with the enzyme reaction product throws light on its enzymatic function. Protein Sci. 7:1269-1279.
62. Schonert, S., T. Buder, and M. K. Dahl. 1998. Identification and enzymatic characterization of the maltose-inducible α-glucosidase MalL (sucrase-isomaltase-maltase) of Bacillus subtilis. J. Bacteriol. 180:2574-2578.
63. 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.
64. Seki, M., K. Iida, M. Saito, H. Nakayama, and S. Yoshida. 2004. Hydrogen peroxide production in Streptococcus pyogenes: involvement of lactate oxidase and coupling with aerobic utilization of lactate. J. Bacteriol. 186:2046-2051.
65. Servant, P., D. Le Coq, and S. Aymerich. 2005. CcpN (YqzB), a novel regulator for CcpA-independent catabolite repression of Bacillus subtilis gluconeogenic genes. Mol. Microbiol. 55:1435-1451.
66. Shaw, G. C., H. S. Kao, and C. Y. Chiou. 1998. Cloning, expression, and catabolite repression of a gene encoding β-galactosidase of Bacillus megaterium ATCC 14581. J. Bacteriol. 180:4734-4738.
67. Simpson, C. L., and R. R. Russell. 1998. Identification of a homolog of CcpA catabolite repressor protein in Streptococcus mutons. Infect. Immun. 66:2085-2092.
68. Smith, A. W., H. Roche, M. C. Trombe, D. E. Briles, and A. Hakansson. 2002. Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol. Microbiol. 44:431-448.
69. Stulke, J., and W. Hillen. 1999. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2:195-201.
70. Stulke, J., and W. Hillen. 1998. Coupling physiology and gene regulation in bacteria: the phosphotransferase sugar uptake system delivers the signals. Naturwissenschaften 85:583-592.
71. Stulke, J., and W. Hillen. 2000. Regulation of carbon catabolism in Bacillus species. Annu. Rev. Microbiol. 54:849-880.
72. 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.
73. Thevenot, T., D. Brochu, C. Vadeboncoeur, and I. R. Hamilton. 1995. Regulation of ATP-dependent P-(Ser)-HPr formation in Streptococcus mutans and Streptococcus salivarius. J. Bacteriol. 177:2751-2759.
74. Titgemeyer, F., and W. Hillen. 2002. Global control of sugar metabolism: a gram-positive solution. Antonie Van Leeuwenhoek 82:59-71.
75. Tobisch, S., D. Zuhlke, J. Bernhardt, J. Stulke, and M. Hecker. 1999. Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis. J. Bacteriol. 181:6996-7004.
76. Tuomanen, E. 1999. Molecular and cellular biology of pneumococcal infection. Curr. Opin. Microbiol. 2:35-39.
77. van den Bogaard, P. T., M. Kleerebezem, O. P. Kuipers, and W. M. de Vos. 2000. Control of lactose transport, β-galactosidase activity, and glycolysis by CcpA in Streptococcus thermophilus: evidence for carbon catabolite repression by a non-phosphoenolpyruvate-dependent phosphotransferase system sugar. J. Bacteriol. 182:5982-5989.
78. 2+-citrate transporter CitM of Bacillus subtilis. J. Bacteriol. 182:6099-6105.
79. Warner, J. B., and J. S. Lolkema. 2003. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
80. Wen, Z. T., and R. A. Burne. 2002. Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl. Environ. Microbiol. 68:1196-1203.
81. Whiting, G. C., J. T. Evans, S. Patel, and S. H. Gillespie. 2002. Purification of native α-enolase from Streptococcus pneumoniae that binds plasminogen and is immunogenic. J. Med. Microbiol. 51:837-843.
82. Zahner, D., and R. Hakenbeck. 2000. The Streptococcus pneumoniae β-galactosidase is a surface protein. J. Bacteriol. 182:5919-5921.