Nucleoid-associated protein HU controls three regulons that coordinate virulence, response to stress and general physiology in Salmonella enterica serovar Typhimurium

Microbiology

Volumn 157, Issue 4, 2011, Pages 1075-1087

  Mangan, Michael W ^a   Lucchini, Sacha ^b   Cróinín, Tadhg Ó ^a   Fitzgerald, Stephen ^a   Hinton, Jay C D ^a,b   Dorman, Charles J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HU PROTEIN; INTEGRATION HOST FACTOR; PROTEIN HUPA; PROTEIN HUPB; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; BETA SHEET; CELL INVASION; CHEMOTAXIS; CONTROLLED STUDY; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATOR GENE; REGULON; SALMONELLA TYPHIMURIUM; SEROTYPE; STRESS; STRUCTURAL GENE; TEMPERATURE; TRANSCRIPTOMICS; UPREGULATION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CRICETINAE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENOMIC ISLANDS; LOCOMOTION; MACROPHAGES; MICE; MICROBIAL VIABILITY; PROTEIN SUBUNITS; REGULON; SALMONELLA TYPHIMURIUM; STRESS, PHYSIOLOGICAL; TEMPERATURE; TIME FACTORS; VIRULENCE;

SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 79953701342     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.046359-0     Document Type: Article

References (76)

1. Azam, T. A. & Ishihama, A. (1999). Twelve species of the nucleoidassociated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274, 33105-33113.
2. Balandina, A., Claret, L., Hengge-Aronis, R. & Rouvière-Yaniv, J. (2001). The Escherichia coli histone-like protein HU regulates rpoS translation. Mol Microbiol 39, 1069-1079.
3. 12-dependent 1, 2-propanediol degradation. J Bacteriol 181, 5967-5975.
4. 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.
5. Brown, J. D., Saini, S., Aldridge, C., Herbert, J., Rao, C. V. & Aldridge, P. D. (2008). The rate of protein secretion dictates the temporal dynamics of flagellar gene expression. Mol Microbiol 70, 924-937.
6. Champion, K. & Higgins, N. P. (2007). Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J Bacteriol 189, 5839-5849.
7. Cheng, S. & Bobik, T. A. (2010). Characterization of the PduS cobalamin reductase of Salmonella enterica and its role in the Pdu microcompartment. J Bacteriol 192, 5071-5080.
8. Cirillo, D. M., Valdivia, R. H., Monack, D. M. & Falkow, S. (1998). Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30, 175-188.
9. Claret, L. & Rouvière-Yaniv, J. (1997). Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J Mol Biol 273, 93-104.
10. Clarke, T. A., Mills, P. C., Poock, S. R., Butt, J. N., Cheesman, M. R., Cole, J. A., Hinton, J. C., Hemmings, A. M., Kemp, G. & other authors (2008). Escherichia coli cytochrome c nitrite reductase NrfA. Methods Enzymol 437, 63-77.
11. Datsenko, K. A. & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
12. Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. (2008). Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72, 317-364.
13. Dillon, S. C. & Dorman, C. J. (2010). Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8, 185-195.
14. Dillon, S. C., Cameron, A. D. S., Hokamp, K., Lucchini, S., Hinton, J. C. D. & Dorman, C. J. (2010). Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 76, 1250-1265.
15. Dorman, C. J. (2007). H-NS, the genome sentinel. Nat Rev Microbiol 5, 157-161.
16. Dorman, C. J. & Deighan, P. (2003). Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev 13, 179-184.
17. Doyle, M., Fookes, M., Ivens, A., Mangan, M. W., Wain, J. & Dorman, C. J. (2007). An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315, 251-252.
18. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. (2003). Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47, 103-118.
19. Fahlen, T. F., Mathur, N. & Jones, B. D. (2000). Identification and characterization of mutants with increased expression of hilA, the invasion gene transcriptional activator of Salmonella typhimurium. FEMS Immunol Med Microbiol 28, 25-35.
20. Finlay, B. B. & Brumell, J. H. (2000). Salmonella interactions with host cells: in vitro to in vivo. Philos Trans R Soc Lond B Biol Sci 355, 623-631.
21. Galán, J. E. (2001). Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17, 53-86.
22. Grifantini, R., Sebastian, S., Frigimelica, E., Draghi, M., Bartolini, E., Muzzi, A., Rappuoli, R., Grandi, G. & Genco, C. A. (2003). Identification of iron-activated and-repressed Fur-dependent genes by transcriptome analysis of Neisseria meningitidis group B. Proc Natl Acad Sci U S A 100, 9542-9547.
23. Groisman, E. A. & Mouslim, C. (2000). Molecular mechanisms of Salmonella pathogenesis. Curr Opin Infect Dis 13, 519-522.
24. Groisman, E. A. & Ochman, H. (1997). How Salmonella became a pathogen. Trends Microbiol 5, 343-349.
25. Guo, F. & Adhya, S. (2007). Spiral structure of Escherichia coli HUab provides foundation for DNA supercoiling. Proc Natl Acad Sci U S A 104, 4309-4314.
26. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galán, J. E. (1998). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826.
27. Harrison, J. A., Pickard, D., Higgins, C. F., Khan, A., Chatfield, S. N., Ali, T., Dorman, C. J., Hormaeche, C. E. & Dougan, G. (1994). Role of hns in the virulence phenotype of pathogenic salmonellae. Mol Microbiol 13, 133-140.
28. Hautefort, I., Thompson, A., Eriksson-Ygberg, S., Parker, M. L., Lucchini, S., Danino, V., Bongaerts, R. J., Ahmad, N., Rhen, M. & Hinton, J. C. (2008). During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10, 958-984.
29. Hensel, M. (2000). Salmonella pathogenicity island 2. Mol Microbiol 36, 1015-1023.
30. Hensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E. & Holden, D. W. (1995). Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400-403.
31. Higgins, C. F., Dorman, C. J., Stirling, D. A., Waddell, L., Booth, I. R., May, G. & Bremer, E. (1988). A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52, 569-584.
32. Hinton, J. C. D., Hautefort, I., Eriksson, S., Thompson, A. & Rhen, M. (2004). Benefits and pitfalls of using microarrays to monitor bacterial gene expression during infection. Curr Opin Microbiol 7, 277-282.
33. Hoiseth, S. K. & Stocker, B. A. (1981). Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238-239.
34. Holden, D. W. (2002). Trafficking of the Salmonella vacuole in macrophages. Traffic 3, 161-169.
35. Huisman, O., Faelen, M., Girard, D., Jaffé, A., Toussaint, A. & Rouvière-Yaniv, J. (1989). Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol 171, 3704-3712.
36. Kamashev, D., Balandina, A. & Rouvière-Yaniv, J. (1999). The binding motif recognized by HU on both nicked and cruciform DNA. EMBO J 18, 5434-5444.
37. Kamashev, D., Balandina, A., Mazur, A. K., Arimondo, P. B. & Rouvière-Yaniv, J. (2008). HU binds and folds single-stranded DNA. Nucleic Acids Res 36, 1026-1036.
38. Kar, S., Edgar, R. & Adhya, S. (2005). Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc Natl Acad Sci U S A 102, 16397-16402.
39. Kelly, A., Goldberg, M. D., Carroll, R. K., Danino, V., Hinton, J. C. D. & Dorman, C. J. (2004). A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150, 2037-2053.
40. S-dependent genes and identification of their promoter sequences. J Bacteriol 186, 7186-7195.
41. Lawhon, S. D., Frye, J. G., Suyemoto, M., Porwollik, S., McClelland, M. & Altier, C. (2003). Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48, 1633-1645.
42. Lewis, D. E., Geanacopoulos, M. & Adhya, S. (1999). Role of HU and DNA supercoiling in transcription repression: specialized nucleoprotein repression complex at gal promoters in Escherichia coli. Mol Microbiol 31, 451-461.
43. Lewis, D. E. A., Lee, S. J. & Adhya, S. (2010). Role of HU in regulation of gal promoters. In Bacterial Chromatin, pp. 395-417. Edited by R. T. Dame & C. J. Dorman. Heidelberg: Springer.
44. Li, S. & Waters, R. (1998). Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J Bacteriol 180, 3750-3756.
45. Lucchini, S., Rowley, G., Goldberg, M. D., Hurd, D., Harrison, M. & Hinton, J. C. D. (2006). H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog 2, e81.
46. 38) regulon during exponential growth of Salmonella Typhimurium. Mol Microbiol 74, 1169-1186.
47. Macnab, R. M. (1986). Proton-driven bacterial flagellar motor. Methods Enzymol 125, 563-581.
48. Macnab, R. M. (2003). How bacteria assemble flagella. Annu Rev Microbiol 57, 77-100.
49. Mahan, M. J., Slauch, J. M. & Mekalanos, J. J. (1993). Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259, 686-688.
50. Mangan, M. W., Lucchini, S., Danino, V., Ócróinín, T., Hinton, J. C. D. & Dorman, C. J. (2006). The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 59, 1831-1847.
51. Marshall, D. G., Sheehan, B. J. & Dorman, C. J. (1999). A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. Mol Microbiol 34, 134-145.
52. Marshall, D. G., Bowe, F., Hale, C., Dougan, G. & Dorman, C. J. (2000). DNA topology and adaptation of Salmonella typhimurium to an intracellular environment. Philos Trans R Soc Lond B Biol Sci 355, 565-574.
53. Merickel, S. K. & Johnson, R. C. (2004). Topological analysis of Hincatalysed DNA recombination in vivo and in vitro. Mol Microbiol 51, 1143-1154.
54. Mills, D. M., Bajaj, V. & Lee, C. A. (1995). A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15, 749-759.
55. Navarre, W. W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S. J. & Fang, F. C. (2006). Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313, 236-238.
56. O'Byrne, C. P. & Dorman, C. J. (1994a). The spv virulence operon of Salmonella typhimurium LT2 is regulated negatively by the cyclic AMP (cAMP)-cAMP receptor protein system. J Bacteriol 176, 905-912.
57. O'Byrne, C. P. & Dorman, C. J. (1994b). Transcription of the Salmonella typhimurium spv virulence locus is regulated negatively by the nucleoid-associated protein H-NS. FEMS Microbiol Lett 121, 99-105.
58. Oberto, J., Nabti, S., Jooste, V., Mignot, H. & Rouvière-Yaniv, J. (2009). The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS ONE 4, e4367.
59. Patten, C. L., Kirchhof, M. G., Schertzberg, M. R., Morton, R. A. & Schellhorn, H. E. (2004). Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272, 580-591.
60. Perni, S., Andrew, P. W. & Shama, G. (2005). Estimating the maximum growth rate from microbial growth curves: definition is everything. Food Microbiol 22, 491-495.
61. Pontiggia, A., Negri, A., Beltrame, M. & Bianchi, M. E. (1993). Protein HU binds specifically to kinked DNA. Mol Microbiol 7, 343-350.
62. Rhen, M. & Dorman, C. J. (2005). Hierarchical gene regulators adapt Salmonella enterica to its host milieus. Int J Med Microbiol 294, 487-502.
63. Ryan, V. T., Grimwade, J. E., Nievera, C. J. & Leonard, A. C. (2002). IHF and HU stimulate assembly of pre-replication complexes at Escherichia coli oriC by two different mechanisms. Mol Microbiol 46, 113-124.
64. Sambrook, J. & Russell, D. (2001). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
65. Schechter, L. M., Jain, S., Akbar, S. & Lee, C. A. (2003). The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. Infect Immun 71, 5432-5435.
66. Semsey, S., Tolstorukov, M. Y., Virnik, K., Zhurkin, V. B. & Adhya, S. (2004). DNA trajectory in the Gal repressosome. Genes Dev 18, 1898-1907.
67. Shanado, Y., Kato, J. & Ikeda, H. (1998). Escherichia coli HU protein suppresses DNA-gyrase-mediated illegitimate recombination and SOS induction. Genes Cells 3, 511-520.
68. Signon, L. & Kleckner, N. (1995). Negative and positive regulation of Tn10/IS10-promoted recombination by IHF: two distinguishable processes inhibit transposition off of multicopy plasmid replicons and activate chromosomal events that favor evolution of new transposons. Genes Dev 9, 1123-1136.
69. Sternberg, N. L. & Maurer, R. (1991). Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol 204, 18-43.
70. Swinger, K. K. & Rice, P. A. (2004). IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 14, 28-35.
71. Uzzau, S., Figueroa-Bossi, N., Rubino, S. & Bossi, L. (2001). Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98, 15264-15269.
72. Valdivia, R. H. & Falkow, S. (1997). Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277, 2007-2011.
73. Waterman, S. R. & Holden, D. W. (2003). Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5, 501-511.
74. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. (2005). Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187, 1591-1603.
75. Wood, M. W., Rosqvist, R., Mullan, P. B., Edwards, M. H. & Galyov, E. E. (1996). SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22, 327-338.
76. Yanisch-Perron, C., Vieira, J. & Messing, J. (1985). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.