Glucose-dependent activation of Bacillus anthracis toxin gene expression and virulence requires the carbon catabolite protein CcpA

Journal of Bacteriology

Volumn 193, Issue 1, 2011, Pages 52-62

  Chiang, Christina ^a   Bongiorni, Cristina ^a,b   Perego, Marta ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b GENENCOR INTERNATIONAL INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTAXIN; BACTERIAL TOXIN; CATABOLITE CONTROL PROTEIN A; GLUCOSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACILLUS ANTHRACIS; CONTROLLED STUDY; GENE EXPRESSION; MOLECULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRULENCE;

ANIMALS; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; MICE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATORS; VIRULENCE;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 78650097558     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01656-09     Document Type: Article

References (79)

1. Abranches, J., M. M. Nascimento, L. Zeng, C. M. Browngardt, Z. T. Wen, M. F. Rivera, and R. A. Burne. 2008. CcpA regulates central metabolism and virulence gene expression in Streptococcus mutans. J. Bacteriol. 190:2340-2349.
2. Almengor, A. C., T. L. Kinkel, S. J. Day, and K. S. McIver. 2007. The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the group A streptococcus. J. Bacteriol. 189:8405-8416.
3. Arantes, O., and D. Lereclus. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119.
4. Barabote, R. D., and M. H. Saier, Jr. 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608-634.
5. Bartkus, J. M., and S. H. Leppla. 1989. Transcriptional regulation of the protective antigen gene of Bacillus anthracis. Infect. Immun. 57:2295-2300.
6. 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.
7. Bongiorni, C., T. Fukushima, A. C. Wilson, C. Chiang, M. C. Mansilla, J. A. Hoch, and M. Perego. 2008. Dual promoters control the expression of the Bacillus anthracis virulence factor AtxA. J. Bacteriol. 190:6483-6492.
8. Bongiorni, C., R. Stoessel, and M. Perego. 2007. Negative regulation of Bacillus anthracis sporulation by the Spo0E family of phosphatases. J. Bacteriol. 189:2637-2645.
9. Boyer, M., and F. Wisniewski-Dye. 2009. Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70:1-19.
10. Brunsing, R. L., C. La Clair, S. Tang, C. Chiang, L. E. Hancock, M. Perego, and J. A. Hoch. 2005. Characterization of sporulation histidine kinases of Bacillus anthracis. J. Bacteriol. 187:6972-6981.
11. Cataldi, A., A. Fouet, and M. Mock. 1992. Regulation of pag gene expression in Bacillus anthracis: use of a pag-lacZ transcriptional fusion. FEMS Microbiol. Lett. 77:89-93.
12. Chauvaux, S., I. T. Paulsen, and M. H. Saier. 1998. CcpB, a novel transcription factor implicated in catabolite repression in Bacillus subtilis. J. Bacteriol. 180:491-497.
13. 2/bicarbonate, affects AtxA synthesis. Infect. Immun. 65:2576-2582.
14. Dai, Z., J. C. Sirard, M. Mock, and T. M. Koehler. 1995. The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence. Mol. Microbiol. 16:1171-1181.
15. De Buck, E., E. Lammertyn, and J. Anne. 2008. The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol. 16:442-453.
16. 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.
17. Dossonnet, V., V. Monedero, M. Zagorec, A. Galinier, G. Perez-Martinez, and J. Deutscher. 2000. Phosphorylation of HPr by the bifunctional HPr Kinase/P-ser-HPr phosphatase from Lactobacillus casei controls catabolite repression and inducer exclusion but not inducer expulsion. J. Bacteriol. 182:2582-2590.
18. Drysdale, M., A. Bourgogne, S. G. Hilsenbeck, and T. M. Koehler. 2004. atxA controls Bacillus anthracis capsule synthesis via acpA and a newly discovered regulator, acpB. J. Bacteriol. 186:307-315.
19. Drysdale, M., A. Bourgogne, and T. M. Koehler. 2005. Transcriptional analysis of the Bacillus anthracis capsule regulators. J. Bacteriol. 187:5108-5114.
20. Eckart, R. A., S. Brantl, and A. Licht. 2009. Search for additional targets of the transcriptional regulator CcpN from Bacillus subtilis. FEMS Microbiol. Lett. 299:223-231.
21. Ellermeier, J. R., and J. M. Slauch. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10:24-29.
22. Fujita, Y. 2009. Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci. Biotechnol. Biochem. 73:245-259.
23. Galinier, A., J. Deutscher, and I. Martin-Verstraete. 1999. Phosphorylation of either Crh or HPr mediates binding of CcpA to the Bacillus subtilis xyn cre and catabolite repression of the xyn operon. J. Mol. Biol. 286:307-314. (Pubitemid 29090151)
24. 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.
25. Gosseringer, R., E. Kuster, A. Galinier, J. Deutscher, and W. Hillen. 1997. Cooperative and noncooperative DNA binding modes of catabolite control protein CcpA from Bacillus megaterium result from sensing two different signals. J. Mol. Biol. 266:665-676.
26. Grundy, F. J., D. A. Waters, S. H. G. Allen, and T. M. Henkin. 1993. Regulation of the Bacillus subtilis acetate kinase gene by CcpA. J. Bacteriol. 175:7348-7355.
27. Hogema, B. M., J. C. Arents, T. Inada, H. Aiba, K. van Dam, and P. W. Postma. 1997. Catabolite repression by glucose 6-phosphate, gluconate and lactose in Escherichia coli. Mol. Microbiol. 24:857-867.
28. 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.
29. Janes, B. K., and S. Stibitz. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect. Immun. 74:1949-1953.
30. Jones, B. E., V. Dossonnet, E. Küster, W. Hillen, J. Deutscher, and R. E. Klevitt. 1997. Binding of the catabolite repressor protein CcpA to its DNA target is regulated by phosphorylation of its corepressor HPr. J. Biol. Chem. 272:26530-26535.
31. 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.
32. Kietzman, C. C., and M. G. Caparon. 2010. CcpA and LacD.1 affect temporal regulation of S. pyogenes virulence genes. Infect. Immun. 78:241-252.
33. Kim, H. J., C. Jourlin-Castelli, S. I. Kim, and A. L. Sonenshein. 2002. Regulation of the Bacillus subtilis ccpC gene by ccpA and ccpC. Mol. Microbiol. 43:399-410.
34. 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.
35. Kinkel, T. L., and K. S. McIver. 2008. CcpA-mediated repression of streptolysin S expression and virulence in the group A streptococcus. Infect. Immun. 76:3451-3463.
36. 2 and a trans-acting element activate transcription from one of two promoters. J. Bacteriol. 176:586-595.
37. Kravanja, M., R. Engelmann, V. Dossonnet, M. Bluggel, H. E. Meyer, R. Frank, A. Galinier, J. Deutscher, N. Schnell, and W. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol. Microbiol. 31:59-66.
38. Li, C., F. Sun, H. Cho, V. Yelavarthi, C. Sohn, C. He, O. Schneewind, and T. Bae. 2010. CcpA mediates proline auxotrophy and is required for Staphylococcus aureus pathogenesis. J. Bacteriol. 192:3883-3892.
39. Lorca, G. L., Y. J. Chung, R. D. Barabote, W. Weyler, C. H. Schilling, and M. H. Saier, Jr. 2005. Catabolite repression and activation in Bacillus subtilis: dependency on CcpA, HPr, and HprK. J. Bacteriol. 187:7826-7839.
40. 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.
41. Ludwig, H., and J. Stulke. 2001. The Bacillus subtilis catabolite control protein CcpA exerts all its regulatory functions by DNA-binding. FEMS Microbiol. Lett. 203:125-129.
42. Marijuan, P. C., J. Navarro, and R. Del Moral. 2010. On prokaryotic intelligence: strategies for sensing the environment. Biosystems 99:94-103.
43. Martin-Verstraete, I., J. Deutscher, and A. Galinier. 1999. Phosphorylation of HPr and Crh by HprK, early steps in the catabolite repression signaling pathway for the Bacillus subtilis levanase operon. J. Bacteriol. 181:2966-2969.
44. Mereghetti, L., I. Sitkiewicz, N. M. Green, and J. M. Musser. 2008. Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (group B streptococcus) in response to incubation with human blood. PLoS One 3:e3143.
45. Miller, J. H. 1972. Experiments in molecular genetics, p. 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
46. 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.
47. Mock, M., and A. Fouet. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671.
48. Moir-Blais, T. R., F. J. Grundy, and T. M. Henkin. 2001. Transcriptional activation of the Bacillus subtilis ackA promoter requires sequences upstream of the CcpA binding site. J. Bacteriol. 183:2389-2393.
49. Moreno, M. S., B. L. Schneider, R. R. Maile, W. Weyler, and M. H. Saier, Jr. 2001. Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol. Microbiol. 39:1366-1381.
50. Nicholson, W. L., and P. Setlow. 1990. Sporulation, germination and outgrowth, p. 391-450. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley & Sons, Chichester, United Kingdom.
51. Okada, N., R. T. Geist, and M. G. Caparon. 1993. Positive transcriptional control of mry regulates virulence in the group A streptococcus. Mol. Microbiol. 7:893-903.
52. Perego, M., and J. A. Hoch. 2008. Commingling regulatory systems following acquisition of virulence plasmids by Bacillus anthracis. Trends Microbiol. 16:215-221.
53. Poncet, S., E. Milohanic, A. Maze, J. N. Abdallah, F. Ake, M. Larribe, A. E. Deghmane, M. K. Taha, M. Dozot, X. De Bolle, J. J. Letesson, and J. Deutscher. 2009. Correlations between carbon metabolism and virulence in bacteria. Contrib. Microbiol. 16:88-102.
54. Poyart, C., and P. Trieu-Cuot. 1997. A broad-host-range mobilizable shuttle vector for the construction of transcriptional fusions to β-galactosidase in Gram-positive bacteria. FEMS Microbiol. Lett. 156:193-198.
55. Puri-Taneja, A., S. Paul, Y. Chen, and F. M. Hulett. 2006. CcpA causes repression of the phoPR promoter through a novel transcription start site, P(A6). J. Bacteriol. 188:1266-1278.
56. Reizer, J., S. L. Sutrina, L. F. Wu, J. Deutscher, P. Reddy, and M. H. Saier, Jr. 1992. Functional interactions between proteins of the phosphoenolpyruvate: sugar phosphotransferase systems of Bacillus subtilis and Escherichia coli. J. Biol. Chem. 267:9158-9169.
57. Ristroph, J. D., and B. E. Ivins. 1983. Elaboration of Bacillus anthracis antigens in a new, defined culture medium. Infect. Immun. 39:483-486.
58. Roux, A., S. M. Payne, and M. S. Gilmore. 2009. Microbial telesensing: probing the environment for friends, foes, and food. Cell Host Microbe 6:115-124.
59. Saier, M. H., Jr. 1998. Multiple mechanisms controlling carbon metabolism in bacteria. Biotechnol. Bioeng. 58:170-174.
60. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74:5463-5467.
61. 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.
62. Schumacher, M. A., G. Seidel, W. Hillen, and R. G. Brennan. 2007. Structural mechanism for the fine-tuning of CcpA function by the small molecule effectors glucose 6-phosphate and fructose 1,6-bisphosphate. J. Mol. Biol. 368:1042-1050.
63. Seidl, K., M. Bischoff, and B. Berger-Bachi. 2008. CcpA mediates the catabolite repression of tst in Staphylococcus aureus. Infect. Immun. 76:5093-5099.
64. Seidl, K., C. Goerke, C. Wolz, D. Mack, B. Berger-Bachi, and M. Bischoff. 2008. Staphylococcus aureus CcpA affects biofilm formation. Infect. Immun. 76:2044-2050.
65. Seidl, K., S. Muller, P. Francois, C. Kriebitzsch, J. Schrenzel, S. Engelmann, M. Bischoff, and B. Berger-Bachi. 2009. Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol. 9:95.
66. Seidl, K., M. Stucki, M. Ruegg, C. Goerke, C. Wolz, L. Harris, B. Berger-Bachi, and M. Bischoff. 2006. Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance. Antimicrob. Agents Chemother. 50:1183-1194.
67. Shelburne, S. A., III, D. Keith, N. Horstmann, P. Sumby, M. T. Davenport, E. A. Graviss, R. G. Brennan, and J. M. Musser. 2008. A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc. Natl. Acad. Sci. U. S. A. 105:1698-1703.
68. Sterne, M. 1937. Variation in Bacillus anthracis. Onderstepoort J. Vet. Sci. Anim. Ind. 8:271-349.
69. Stoll, R., S. Mertins, B. Joseph, S. Muller-Altrock, and W. Goebel. 2008. Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. Microbiology 154:3856-3876.
70. Tsvetanova, B., A. C. Wilson, C. Bongiorni, C. Chiang, J. A. Hoch, and M. Perego. 2007. Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis. Mol. Microbiol. 63:644-655.
71. Vagner, V., E. Dervyn, and S. D. Ehrlich. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144(Pt 11):3097-3104.
72. van der Voort, M., O. P. Kuipers, G. Buist, W. M. de Vos, and T. Abee. 2008. Assessment of CcpA-mediated catabolite control of gene expression in Bacillus cereus ATCC 14579. BMC Microbiol. 8:62.
73. Varga, J., V. L. Stirewalt, and S. B. Melville. 2004. The CcpA protein is necessary for efficient sporulation and enterotoxin gene (cpe) regulation in Clostridium perfringens. J. Bacteriol. 186:5221-5229.
74. Varga, J. J., B. Therit, and S. B. Melville. 2008. Type IV pili and the CcpA protein are needed for maximal biofilm formation by the gram-positive anaerobic pathogen Clostridium perfringens. Infect. Immun. 76:4944-4951.
75. Warner, J. B., and J. S. Lolkema. 2003. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
76. Weickert, M. J., and G. H. Chambliss. 1990. Site-directed mutagenesis of a catabolite repression operator sequence in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 87:6238-6242.
77. Welkos, S. L., T. J. Keener, and P. H. Gibbs. 1986. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect. Immun. 51:795-800.
78. 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.
79. White-Ziegler, C. A., A. J. Malhowski, and S. Young. 2007. Human body temperature (37°C) increases the expression of iron, carbohydrate, and amino acid utilization genes in Escherichia coli K-12. J. Bacteriol. 189:5429-5440.