The DegU orphan response regulator of Listeria monocytogenes autorepresses its own synthesis and is required for bacterial motility, virulence and biofilm formation

Microbiology

Volumn 154, Issue 8, 2008, Pages 2251-2264

  Gueriri, Ibtissem ^a   Cyncynatus, Camille ^a,d   Dubrac, Sarah ^a   Arana, Alejandro Toledo ^b   Dussurget, Olivier ^c   Msadek, Tarek ^a  

^a INSTITUT PASTEUR   (France)

^b PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^c INSERM   (France)

^d AbAg   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PLASTIC; PROTEIN DEGU; PROTEIN GMAR; REPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CONTROLLED STUDY; DNA FOOTPRINTING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HIGH TEMPERATURE; IN VITRO STUDY; LD 50; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN SYNTHESIS;

BACTERIAL PROTEINS; BIOFILMS; CHEMOTAXIS; DOWN-REGULATION; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; LISTERIA MONOCYTOGENES; PROMOTER REGIONS (GENETICS); VIRULENCE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MURINAE; OCTODON DEGUS; POSIBACTERIA;

EID: 51149089685     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2008/017590-0     Document Type: Article

References (63)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generatibn of protein database search programs. Nucleic Acids Res 25, 3389-3402.
2. Amati, G., Bisicchia, P. & Galizzi, A. (2004). DegU-P represses expression of the motility fla-che operon in Bacillus subtilis. J Bacteriol 186, 6003-6014.
3. Amrein, K. E., Takacs, B., Stieger, M., Molnos, J., Flint, N. A. & Bum, P. (1995). Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc Natl Acad Sci U S A 92, 1048-1052.
4. Arnaud, M., Chastanet A. & Debarbouille, M. (2004). New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70, 6887-6891.
5. Bigot A., Pagniez, H., Botton, E., Frehel, C., Dubail, L., Jacquet C., Charbit A. & Raynaud, C. (2005). Role of FliF and FliI of Listeria monocytogenes in flagellar assembly and pathogenicity. Infect Immun 73, 5530-5539.
6. Borezée, E., Msadek, T., Durant L. & Berche, P. (2000). Identification in Listeria monocytogenes of MecA, a homologue of the Bacillus subtilis competence regulatory protein. J Bacteriol 182, 5931-5934.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
8. Brands, S. S., Gonzalez-Pastor, J. E., Ben-Yehuda, S., Losick R. & Kolter, R. (2001). Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98, 11621-11626.
9. Burkholder, P. R. & Giles, N. H., Jr (1947). Induced biochemical mutations in Bacillus subtilis. Am J Bot 34, 345-348.
10. Chastanet A., Prudhomme, M., Claverys, J. P. & Msadek, T. (2001). Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J Bacteriol 183, 7295-7307.
11. Chastanet A., Fart J. & Msadek, T. (2003). Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol Microbiol 47, 1061-1073.
12. Cossart, P. & Portnoy, D. A. (2000). The cell biology of invasion and intracellular growth by Listeria monocytogenes. In Gram-Positive Pathogens, pp. 507-515. Edited by V. A. Fischetti, R. P. Novick, J. J. Feretti, D. A. Portnoy & J. I. Rood. Washington, DC: American Society for Microbiology.
13. Cotter, P. D., Guinane, C. M. & Hill, C. (2002). The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. Antimicrob Agents Chemother 46, 2784-2790.
14. Dahl, M. K., Msadek T., Kunst F. & Rapoport, G. (1992). The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis. J Biol Chem 267, 14509-14514.
15. Derré, I., Rapoport G. & Msadek, T. (1999). CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in Gram-positive bacteria. Mol Microbiol 31, 117-132.
16. Dons, L., Eriksson, E., Jin, Y., Rottenberg, M. E., Kristensson, K., Larsen, C. N., Bresciani, J. & Olsen, J. E. (2004). Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72, 3237-3244.
17. Dubrac, S. & Msadek, T. (2004). Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J Bacteriol 186, 1175-1181.
18. Dubrac, S., Boneca, I. G., Poupel, O. & Msadek, T. (2007). New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189, 8257-8269.
19. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., Berche, P., Bloecker, H., Brandt, P. & other authors (2001). Comparative genomics of Listeria species. Science 294, 849-852.
20. Glatron, M. F. & Rapoport, G. (1972). Biosynthesis of the parasporal inclusion of Bacillus thuringiensis: half-life of its corresponding messenger RNA. Biochimie 54, 1291-1301.
21. Grundling, A., Burrack, L. S., Bouwer, H. G. & Higgins, D. E. (2004). Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc Natl Acad Sci U S A 101, 12318-12323.
22. Hamoen, L. W., Van Werkhoven, A. F., Bijlsma, J. J., Dubnau, D. & Venema, G. (1998). The competence transcription factor of Bacillus subtilis recognizes short A/T-rich sequences arranged in a unique, flexible pattern along the DNA helix. Genes Dev 12, 1539-1550.
23. Hamoen, L. W., Van Werkhoven, A. F., Venema, G. & Dubnau, D. (2000). The pleiotropic response regulator DegU functions as a priming protein in competence development in Bacillus subtilis. Proc Natl Acad Sci U S A 97, 9246-9251.
24. Helmann, J. D. (1991). Alternative sigma factors and the regulation of flagellar gene expression. Mol Microbiol 5, 2875-2882.
25. Henner, D. J., Yang, M. & Ferrari, E. (1988). Localization of Bacillus subtilis sacU(Hy) mutations to two linked genes with similarities to the conserved procaryotic family of two-component signalling systems. J Bacteriol 170, 5102-5109.
26. Hoch, J. A. & Silhavy, T. J. (1995). Two-Component Signal Transduction. Washington, DC: American Society for Microbiology.
27. Kallipolitis, B. H., Ingmer, H., Gahan, C. G., Hill, C. & Sogaard-Andersen, L. (2003). CesRK, a two-component signal transduction system in Listeria monocytogenes, responds to the presence of cell wall-acting antibiotics and affects β-lactam resistance. Antimicrob Agents Chemother 47, 3421-3429.
28. Karatzas, K. A., Wouters, J. A., Gahan, C. G., Hill, C., Abee, T. & Bennik, M. H. (2003). The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence. Mol Microbiol 49, 1227-1238.
29. Kathariou, S., Kanenaka, R., Allen, R. D., Fok, A. K. & Mizumoto, C. (1995). Repression of motility and flagellin production at 37 degrees C is stronger in Listeria monocytogenes than in the nonpathogenic species Listeria innocua. Can J Microbiol 41, 572-577.
30. Knudsen, G. M., Olsen, J. E. & Dons, L. (2004). Characterization of DegU, a response regulator in Listeria monocytogenes, involved in regulation of motility and contributes to virulence. FEMS Microbiol Lett 240, 171-179.
31. Kobayashi, K. (2007a). Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 66, 395-409.
32. Kobayashi, K (2007b). Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 189, 4920-4931.
33. Kunst, F., Debarbouille, M., Msadek, T., Young, M., Mauel, C., Karamata, D., Klier, A., Rapoport, G. & Dedonder, R. (1988). Deduced polypeptides encoded by the Bacillus subtilis sacU locus share homology with two-component sensor-regulator systems. J Bacteriol 170, 5093-5101.
34. Lemon, K. P., Higgins, D. E. & Kolter, R. (2007). Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189, 4418-4424.
35. Mandin, P., Fsihi, H., Dussurget, O., Vergassola, M., Milohanic, E., Toledo-Arana, A., Lasa, I., Johansson, J. & Cossart, P. (2005). VirR, a response regulator critical for Listeria monocytogenes virulence. Mol Microbiol 57, 1367-1380.
36. Michel, E., Mengaud, J., Galsworthy, S. & Cossart, P. (1998). Characterization of a large motility gene cluster containing the cheR, motAB genes of Listeria monocytogenes and evidence that PrfA downregulates motility genes. FEMS Microbiol Lett 169, 341-347.
37. Moszer, I., Jones, L. M., Moreira, S., Fabry, C. & Danchin, A. (2002). SubtiList: the reference database for the Bacillus subtilis genome. Nucleic Acids Res 30, 62-65.
38. MsadeK T. (1999). When the going gets tough: survival strategies and environmental signaling networks in Bacillus subtilis. Trends Microbiol 7, 201-207.
39. Msadek T., Kunst, F., Henner, D., Klier, A., Rapoport, G. & Dedonder, R. (1990). Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol 172, 824-834.
40. Msadek T., Kunst F. & Rapoport, G. (1993). Two-component regulatory systems. In Bacillus subtilis and other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics, pp. 729-745. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
41. Msadek T., Kunst, F. & Rapoport G. (1995). A signal transduction network in Bacillus subtilis includes the DegS/DegU and ComP/ComA two-component systems. In Two-Component Signal Transduction, pp. 447-471. Edited by J. A. Hoch & T. J. Silhavy. Washington, DC: American Society for Microbiology.
42. Msadek T., Dartois, V., Kunst F., Herbaud, M. L., Denizot, F. & Rapoport G. (1998). ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 27, 899-914.
43. Nair, S., Derre, I., Msadek, T., Gaillot, O. & Berche, P. (2000). CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol Microbiol 35, 800-811.
44. O'Neil, H. S. & Marquis, H. (2006). Listeria monocytogenes flagella are used for motility, not as adhesins, to increase host cell invasion. Infect Immun 74, 6675-6681.
45. Peel, M., Donachie, W. & Shaw, A. (1988). Temperature-dependent expression of flagella of Listeria monocytogenes studied by electron microscopy, SDS-PAGE and Western blotting. J Gen Microbiol 134, 2171-2178.
46. Premaratne, R. J., Lin, W. J. & Johnsoh, E. A. (1991). Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57, 3046-3048.
47. Sambrook J, Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
48. Sanchez-Campillo, M., Dramsi, S., Gomez-Gomez, J. M., Michel, E., Dehoux, P., Cossart, P., Baquero, F. & Perez-Diaz, J. C. (1995). Modulation of DNA topology by flaR, a new gene from Listeria monocytogenes. Mol Microbiol 18, 801-811.
49. Schmittgen, T. D. & Zakrajsek B. A. (2000). Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46, 69-81.
50. Shen, A. & Higgins, D. E. (2006). The MogR transcriptional repressor regulates nonhierarchal expression of flagellar motility genes and virulence in Listeria monocytogenes. PLoS Pathog 2, e30.
51. Shen, A., Kamp, H. D., Grundling, A. & Higgins, D. E. (2006). A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev 20, 3283-3295.
52. Smits, W. K., Eschevins, C. C., Susanna, K. A., Bron, S., Kuipers, O. P. & Hamoen, L. W. (2005). Stripping Bacillus: ComK auto-stimulation is responsible for the bistable response in competence development. Mol Microbiol 56, 604-614.
53. Smits, W. K., Hoa, T. T., Hamoen, L. W., Kuipers, O. P. & Dubnau, D. (2007). Antirepression as a second mechanism of transcriptional activation by a minor groove binding protein. Mol Microbiol 64, 368-381.
54. Stanley, N. R. & Lazazzera, B. A. (2005). Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-DL-glutamic acid production and biofilm formation. Mol Microbiol 57, 1143-1158.
55. Stock J. B., Ninfa, A. J. & Stock A. M. (1989). Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 53, 450-490.
56. Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113-130.
57. Sullivan, M. A., Yasbin, R. E. & Young, F. E. (1984). New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 29, 21-26.
58. Tokunaga, T., Rashid, M. H., Kuroda, A. & Sekiguchi, J. (1994). Effect of degS-degU mutations on the expression of sigD, encoding an alternative sigma factor, and autolysin operon of Bacillus subtilis. J Bacteriol 176, 5177-5180.
59. Tresse, O., Lebret, V., Benezech, T. & Faille, C. (2006). Comparative evaluation of adhesion, surface properties, and surface protein composition of Listeria monocytogenes strains after cultivation at constant pH of 5 and 7. J Appl Microbiol 101, 53-62.
60. Verhamme, D. T., Kiley, T. B. & Stanley-Wall, N. R. (2007). DegU coordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65, 554-568.
61. Way, S. S., Thompson, L. J., Lopes, J. E., Hajjar, A. M., Kollmann, T. R., Freitag, N. E. & Wilson, C. B. (2004). Characterization of flagellin expression and its role in Listeria monocytogenes infection and immunity. Cell Microbiol 6, 235-242.
62. Williams, T., Bauer, S., Beier, D. & Kuhn, M. (2005a). Construction and characterization of Listeria monocytogenes mutants with in-frame deletions in the response regulator genes identified in the genome sequence. Infect Immun 73, 3152-3159.
63. Williams, T., Joseph, B., Beier, D., Goebel, W. & Kuhn, M. (2005b). Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 252, 287-298.