Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase

Journal of Bacteriology

Volumn 192, Issue 2, 2010, Pages 446-455

  Albert Weissenberger, Christiane ^a,b   Sahr, Tobias ^a   Sismeiro, Odile ^c   Hacker, Jörg ^b,d   Heuner, Klaus ^b,d   Buchrieser, Carmen ^a  

^a CNRS   (France)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INSTITUT PASTEUR   (France)

^d ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FLEQ PROTEIN; FLER PROTEIN; FLIA PROTEIN; PROTEIN; SIGMA FACTOR RPON; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLAGELLUM; GENE CONTROL; GENE EXPRESSION; KINETOSOME; LEGIONELLA PNEUMOPHILA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA;

EID: 73649119529     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00610-09     Document Type: Article

References (52)

1. Albert-Weissenberger, C., C. Cazalet, and C. Buchrieser. 2007. Legionella pneumophila-a human pathogen that co-evolved with fresh water protozoa. Cell. Mol. Life Sci. 64:432-448.
2. 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.
3. Brüggemann, H., A. Hagman, M. Jules, O. Sismeiro, M. Dillies, C. Gouyette, F. Kunst, M. Steinert, K. Heuner, J. Coppée, and C. Buchrieser. 2006. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8:1228-1240.
4. Byrne, B., and M. S. Swanson. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
5. Cazalet, C., C. Rusniok, H. Bruggemann, N. Zidane, A. Magnier, L. Ma, M. Tichit, S. Jarraud, C. Bouchier, F. Vandenesch, F. Kunst, J. Etienne, P. Glaser, and C. Buchrieser. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-1173.
6. Chien, M., I. Morozova, S. Shi, H. Sheng, J. Chen, S. M. Gomez, G. Asamani, K. Hill, J. Nuara, M. Feder, J. Rineer, J. J. Greenberg, V. Steshenko, S. H. Park, B. Zhao, E. Teplitskaya, J. R. Edwards, S. Pampou, A. Georghiou, I. C. Chou, W. Iannuccilli, M. E. Ulz, D. H. Kim, A. Geringer-Sameth, C. Goldsberry, P. Morozov, S. G. Fischer, G. Segal, X. Qu, A. Rzhetsky, P. Zhang, E. Cayanis, P. J. De Jong, J. Ju, S. Kalachikov, H. A. Shuman, and J. J. Russo. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
7. Cullen, P. J., W. C. Bowman, D. F. Hartnett, S. C. Reilly, and R. G. Kranz. 1998. Translational activation by an NtrC enhancer-binding protein. J. Mol. Biol. 278:903-914.
8. Cullen, P. J., W. C. Bowman, and R. G. Kranz. 1996. In vitro reconstitution and characterization of the Rhodobacter capsulatus NtrB and NtrC twocomponent system. J. Biol. Chem. 271:6530-6536.
9. Dalebroux, Z. D., R. L. Edwards, and M. S. Swanson. 2009. SpoT governs Legionella pneumophila differentiation in host macrophages. Mol. Microbiol. 71:640-658.
10. Dasgupta, N., E. P. Ferrell, K. J. Kanack, S. E. West, and R. Ramphal. 2002. fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is sigma70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J. Bacteriol. 184:5240-5250.
11. Dasgupta, N., and R. Ramphal. 2001. Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 183:6636-6644.
12. Dasgupta, N., M. C. Wolfgang, A. L. Goodman, S. K. Arora, J. Jyot, S. Lory, and R. Ramphal. 2003. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 50:809-824.
13. Delmar, P., S. Robin, and J. J. Daudin. 2005. VarMixt: efficient variance modelling for the differential analysis of replicated gene expression data. Bioinformatics 21:502-508.
14. Dietrich, C., K. Heuner, B. C. Brand, J. Hacker, and M. Steinert. 2001. Flagellum of Legionella pneumophila positively affects the early phase of infection of eukaryotic host cells. Infect. Immun. 69:2116-2122.
15. Edwards, R. L., Z. D. Dalebroux, and M. S. Swanson. 2009. Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol. Microbiol. 71:1190-1204.
16. Fettes, P. S., V. Forsbach-Birk, D. Lynch, and R. Marre. 2001. Overexpresssion of a Legionella pneumophila homologue of the E. coli regulator csrA affects cell size, flagellation, and pigmentation. Int. J. Med. Microbiol. 291:353-360.
17. Foster-Hartnett, D., P. J. Cullen, E. M. Monika, and R. G. Kranz. 1994. A new type of NtrC transcriptional activator. J. Bacteriol. 176:6175-6187.
18. Gal-Mor, O., and G. Segal. 2003. The Legionella pneumophila GacA homolog (LetA) is involved in the regulation of icm virulence genes and is required for intracellular multiplication in Acanthamoeba castellanii. Microb. Pathog. 34:187-194.
19. Glöckner, G., C. Albert-Weissenberger, E. Weinmann, S. Jacobi, E. Schunder, M. Steinert, J. Hacker, and K. Heuner. 2007. Identification and characterization of a new conjugation/type IVA secretion system (trb/tra) of Legionella pneumophila Corby localized on a mobile genomic island. Int. J. Med. Microbiol. 298:411-428.
20. Hammer, B. K., and M. S. Swanson. 1999. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33:721-731.
21. Hammer, B. K., E. S. Tateda, and M. S. Swanson. 2002. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 44:107-118.
22. Heuner, K., L. Bender-Beck, B. C. Brand, P. C. Luck, K. H. Mann, R. Marre, M. Ott, and J. Hacker. 1995. Cloning and genetic characterization of the flagellum subunit gene (flaA) of Legionella pneumophila serogroup 1. Infect. Immun. 63:2499-2507.
23. Heuner, K., B. C. Brand, and J. Hacker. 1999. The expression of the flagellum of Legionella pneumophila is modulated by different environmental factors. FEMS Microbiol. Lett. 175:69-77.
24. Heuner, K., C. Dietrich, C. Skriwan, M. Steinert, and J. Hacker. 2002. Influence of the alternative sigma(28) factor on virulence and flagellum expression of Legionella pneumophila. Infect. Immun. 70:1604-1608.
25. Heuner, K., and M. Steinert. 2003. The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int. J. Med. Microbiol. 293:133-143.
26. Hickman, J. W., and C. S. Harwood. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69:376-389.
27. Horwitz, M. A. 1983. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158:1319-1331.
28. Horwitz, M. A., and F. R. Maxfield. 1984. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J. Cell Biol. 99:1936-1943.
29. Horwitz, M. A., and S. C. Silverstein. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiplies intracellularly in human monocytes. J. Clin. Invest. 66:441-450.
30. Jacobi, S., R. Schade, and K. Heuner. 2004. Characterization of the alternative sigma factor sigma54 and the transcriptional regulator FleQ of Legionella pneumophila, which are both involved in the regulation cascade of flagellar gene expression. J. Bacteriol. 186:2540-2547.
31. Jepras, R. I., R. B. Fitzgeorge, and A. Baskerville. 1985. A comparison of virulence of two strains of Legionella pneumophila based on experimental aerosol infection of guinea pigs. J. Hyg. (London) 95:29-38.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
33. Lynch, D., N. Fieser, K. Gloggler, V. Forsbach-Birk, and R. Marre. 2003. The response regulator LetA regulates the stationary-phase stress response in Legionella pneumophila and is required for efficient infection of Acanthamoeba castellanii. FEMS Microbiol. Lett. 219:241-248.
34. McCarter, L. L. 2006. Regulation of flagella. Curr. Opin. Microbiol. 9:180-186.
35. Milohanic, E., P. Glaser, J. Y. Coppee, L. Frangeul, Y. Vega, J. A. Vazquez-Boland, F. Kunst, P. Cossart, and C. Buchrieser. 2003. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47:1613-1625.
36. Molofsky, A. B., B. G. Byrne, N. N. Whitfield, C. A. Madigan, E. T. Fuse, K. Tateda, and M. S. Swanson. 2006. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 17:1093-1104.
37. Molofsky, A. B., and M. S. Swanson. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40.
38. Molofsky, A. B., and M. S. Swanson. 2003. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50:445-461.
39. Nyström, T. 2004. Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol. Microbiol. 54:855-862.
40. Reiner, A., D. Yekutieli, and Y. Benjamini. 2003. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368-375.
41. Ren, T., D. S. Zamboni, C. R. Roy, W. F. Dietrich, and R. E. Vance. 2006. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2:e18.
42. Rowbotham, T. J. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33:1179-1183.
43. Sahr, T., H. Bruggemann, M. Jules, M. Lomma, C. Albert-Weissenberger, C. Cazalet, and C. Buchrieser. 2009. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol. Microbiol. 72:741-762.
44. Sauer, J. D., M. A. Bachman, and M. S. Swanson. 2005. The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc. Natl. Acad. Sci. U. S. A. 102:9924-9929.
45. Sturgill-Koszycki, S., and M. S. Swanson. 2000. Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J. Exp. Med. 192:1261-1272.
46. Swanson, M. S., and E. Fernandez-Moreira. 2002. A microbial strategy to multiply in macrophages: the pregnant pause. Traffic 3:170-177.
47. Swanson, M. S., and B. K. Hammer. 2000. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54:567-613.
48. Tiaden, A., T. Spirig, S. S. Weber, H. Brüggemann, R. Bosshard, C. Buchrieser, and H. Hilbi. 2007. The Legionella pneumophila response regulator LqsR promotes virulence as an element of the regulatory network controlled by RpoS and LetA. Cell. Microbiol. 9:2903-2920.
49. Wigneshweraraj, S., D. Bose, P. C. Burrows, N. Joly, J. Schumacher, M. Rappas, T. Pape, X. Zhang, P. Stockley, K. Severinov, and M. Buck. 2008. Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol. Microbiol. 68:538-546.
50. Wolfe, A. J., and K. L. Visick. 2008. Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. J. Bacteriol. 190:463-475.
51. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15.
52. Zusman, T., O. Gal-Mor, and G. Segal. 2002. Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J. Bacteriol. 184:67-75.