ResDE-dependent regulation of enterotoxin gene expression in Bacillus cereus: Evidence for multiple modes of binding for ResD and interaction with Fnr

Journal of Bacteriology

Volumn 191, Issue 13, 2009, Pages 4419-4426

  Esbelin, Julia ^a   Armengaud, Jean ^b   Zigha, Assia ^a,c   Duport, Catherine ^a  

^a UNIVERSITY OF AVIGNON   (France)

^b DIF   (France)

^c Metabolic Explorer   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENTEROTOXIN; PROTEIN FNR; PROTEIN RESD; PROTEIN RESE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL VIRULENCE; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATOR GENE; FAR WESTERN BLOTTING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; PHOSPHORYLATION; PHYSIOLOGY; PROMOTER REGION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; WESTERN BLOTTING;

BACILLUS CEREUS;

BACILLUS CEREUS; BACTERIAL PROTEINS; BLOTTING, FAR-WESTERN; BLOTTING, WESTERN; CLONING, MOLECULAR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

EID: 67649397593     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00321-09     Document Type: Article

References (39)

1. Agaisse, H., M. Gominet, O. A. Okstad, A. B. Kolsto, and D. Lereclus. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32:1043-1053.
2. Allen, M. P., K. B. Zumbrennen, and W. R. McCleary. 2001. Genetic evidence that the α5 helix of the receiver domain of PhoB is involved in interdomain interactions. J. Bacteriol. 183:2204-2211.
3. Brillard, J., K. Susanna, C. Michaud, C. Dargaignaratz, M. Gohar, C. Nielsen-Leroux, N. Ramarao, A. B. Kolsto, C. Nguyen-The, D. Lereclus, and V. Broussolle. 2008. The YvfTU two-component system is involved in plcR expression in Bacillus cereus. BMC Microbiol. 8:183.
4. de Been, M., M. J. Bart, T. Abee, R. J. Siezen, and C. Francke. 2008. The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives. Environ. Microbiol. 10:2796-2809.
5. de Been, M., C. Francke, R. Moezelaar, T. Abee, and R. J. Siezen. 2006. Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis. Microbiology 152:3035-3048.
6. de Groot, A., R. Dulermo, P. Ortet, L. Blanchard, P. Guérin, B. Fernandez, B. Vacherie, C. Dossat, E. Jolivet, P. Siguier, M. Chandler, M. Barakat, A. Dedieu, V. Barbe, T. Heulin, S. Sommer, W. Achouak, and J. Armengaud. 2009. Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet. 5:e1000434.
7. Duport, C., S. Thomassin, G. Bourel, and P. Schmitt. 2004. Anaerobiosis and low specific growth rates enhance hemolysin BL production by Bacillus cereus F4430/73. Arch. Microbiol. 182:90-95.
8. Duport, C., A. Zigha, E. Rosenfeld, and P. Schmitt. 2006. Control of enterotoxin gene expression in Bacillus cereus F4430/73 involves the redox-sensitive ResDE signal transduction system. J. Bacteriol. 188:6640-6651.
9. Esbelin, J., Y. Jouanneau, J. Armengaud, and C. Duport. 2008. ApoFnr binds as a monomer to promoters regulating the expression of enterotoxin genes of Bacillus cereus. J. Bacteriol. 190:4242-4251.
10. Galperin, M. Y. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188:4169-4182.
11. Gao, R., Y. Tao, and A. M. Stock. 2008. System-level mapping of Escherichia coli response regulator dimerization with FRET hybrids. Mol. Microbiol. 69:1358-1372.
12. Geng, H., Y. Zhu, K. Mullen, C. S. Zuber, and M. M. Nakano. 2007. Characterization of ResDE-dependent fnr transcription in Bacillus subtilis. J. Bacteriol. 189:1745-1755.
13. Geng, H., P. Zuber, and M. M. Nakano. 2007. Regulation of respiratory genes by ResD-ResE signal transduction system in Bacillus subtilis. Methods Enzymol. 422:448-464.
14. Gohar, M., K. Faegri, S. Perchat, S. Ravnum, O. A. Okstad, M. Gominet, A. B. Kolsto, and D. Lereclus. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3:e2793.
15. Gueriri, I., S. Bay, S. Dubrac, C. Cyncynatus, and T. Msadek. 2008. The Pta-AckA pathway controlling acetyl phosphate levels and the phosphorylation state of the DegU orphan response regulator both play a role in regulating Listeria monocytogenes motility and chemotaxis. Mol. Microbiol. 70:1342-1357.
16. Guinebretiere, M. H., and C. Nguyen-The. 2003. Sources of Bacillus cereus contamination in a pasteurized zucchini purée processing line, differentiated by two PCR-based methods. FEMS Microbiol. Ecol. 43:207-215.
17. Guyton, A. C. 1977. Basic human physiology: normal function and mechanisms of disease, 2nd ed. Elsevier Health Sciences, Philadelphia, PA.
18. Hoch, J. A. 2000. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 3:165-170.
19. Igoshin, O. A., R. Alves, and M. A. Savageau. 2008. Hysteretic and graded responses in bacterial two-component signal transduction. Mol. Microbiol. 68:1196-1215.
20. Ivanova, N., A. Sorokin, I. Anderson, N. Galleron, B. Candelon, V. Kapatral, A. Bhattacharyya, G. Reznik, N. Mikhailova, A. Lapidus, L. Chu, M. Mazur, E. Goltsman, N. Larsen, M. D'Souza, T. Walunas, Y. Grechkin, G. Pusch, R. Haselkorn, M. Fonstein, S. D. Ehrlich, R. Overbeek, and N. Kyrpides. 2003. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87-91.
21. Kenney, L. J. 2002. Structure/function relationships in OmpR and other winged-helix transcription factors. Curr. Opin. Microbiol. 5:135-141.
22. Khorchid, A., and M. Ikura. 2006. Bacterial histidine kinase as signal sensor and transducer. Int. J. Biochem. Cell Biol. 38:307-312.
23. Laemmli, U. K.. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Mascher, T., J. D. Helmann, and G. Unden. 2006. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70:910-938.
25. McCleary, W. R., and J. B. Stock. 1994. Acetyl phosphate and the activation of two-component response regulators. J. Biol. Chem. 269:31567-31572.
26. Miller, A. A., N. C. Engleberg, and V. J. DiRita. 2001. Repression of virulence genes by phosphorylation-dependent oligomerization of CsrR at target promoters in S. pyogenes. Mol. Microbiol. 40:976-990.
27. Moriarty-Craige, S. E., and D. P. Jones. 2004. Extracellular thiols and thiol/disulfide redox in metabolism. Annu. Rev. Nutr. 24:481-509.
28. Rhee, J. E., W. Sheng, L. K. Morgan, R. Nolet, X. Liao, and L. J. Kenney. 2008. Amino acids important for DNA recognition by the response regulator OmpR. J. Biol. Chem. 283:8664-8677.
29. Ruiz, D., P. Salinas, M. L. Lopez-Redondo, M. L. Cayuela, A. Marina, and A. Contreras. 2008. Phosphorylation-independent activation of the atypical response regulator NblR. Microbiology 154:3002-3015.
30. Skinner, F. A., and J. G. Carr. 1995. The normal microbial flora of man. Academic, London, United Kingdom.
31. Spira, W. M., and J. M. Goepfert. 1975. Biological characteristics of an enterotoxin produced by Bacillus cereus. Can. J. Microbiol. 21:1236-1246.
32. Steinberg, T. H., B. J. Agnew, K. R. Gee, W. Y. Leung, T. Goodman, B. Schulenberg, J. Hendrickson, J. M. Beechem, R. P. Haugland, and W. F. Patton. 2003. Global quantitative phosphoprotein analysis using multiplexed proteomics technology. Proteomics 3:1128-1144.
33. Stenfors Arnesen, L. P., A. Fagerlund, and P. E. Granum. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32:579-606.
34. Stock, J., and S. Da Re. 2000. Signal transduction: response regulators on and off. Curr. Biol. 10:420-424.
35. Vetter, S. M., and P. M. Schlievert. 2007. The two-component system Bacillus respiratory response A and B (BrrA-BrrB) is a virulence factor regulator in Bacillus anthracis. Biochemistry 46:7343-7352.
36. Wilson, A. C., J. A. Hoch, and M. Perego. 2008. Virulence gene expression is independent of ResDE-regulated respiration control in Bacillus anthracis. J. Bacteriol. 190:5522-5525.
37. Wittig, I., H. P. Braun, and H. Schagger. 2006. Blue native PAGE. Nat. Protoc. 1:418-428.
38. Zhang, X., and F. M. Hulett. 2000. ResD signal transduction regulator of aerobic respiration in Bacillus subtilis: ctaA promoter regulation. Mol. Microbiol. 37:1208-1219.
39. Zigha, A., E. Rosenfeld, P. Schmitt, and C. Duport. 2007. The redox regulator Fnr is required for fermentative growth and enterotoxin synthesis in Bacillus cereus F4430/73. J. Bacteriol. 189:2813- 2824.