Catabolite repression of the SirA regulatory cascade in Salmonella enterica

International Journal of Medical Microbiology

Volumn 296, Issue 7, 2006, Pages 449-466

  Teplitski, Max ^a   Goodier, Robert I ^b   Ahmer, Brian M M ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Carbon storage regulator; gacA; gacS; Small regulatory RNA

Indexed keywords

PROTEIN SIRA; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; CATABOLITE REPRESSION; DNA SEQUENCE; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; REGULON; SALMONELLA ENTERICA; TRANSCRIPTION REGULATION;

EID: 33750027773     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2006.06.001     Document Type: Article

References (87)

1. Ahmer B.M., van Reeuwijk J., Timmers C.D., Valentine P.J., and Heffron F. Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J. Bacteriol. 180 (1998) 1185-1193
2. Ahmer B.M., Tran M., and Heffron F. The virulence plasmid of Salmonella typhimurium is self-transmissible. J. Bacteriol. 181 (1999) 1364-1368
3. Ahmer B.M., van Reeuwijk J., Watson P.R., Wallis T.S., and Heffron F. Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol. Microbiol. 31 (1999) 971-982
4. Ailion M., Bobik T.A., and Roth J.R. Two global regulatory systems (CRP and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium. J. Bacteriol. 175 (1993) 7200-7208
5. Altier C., Suyemoto M., and Lawhon S.D. Regulation of Salmonella enterica serovar Typhimurium invasion genes by csrA. Infect. Immun. 68 (2000) 6790-6797
6. Altier C., Suyemoto M., Ruiz A.I., Burnham K.D., and Maurer R. Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol. Microbiol. 35 (2000) 635-646
7. Bajaj V., Lucas R.L., Hwang C., and Lee C.A. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22 (1996) 703-714
8. Baker C.H., Tomlinson S.R., Garcia A.E., and Harman J.G. Amino acid substitution at position 99 affects the rate of CRP subunit exchange. Biochemistry 40 (2001) 12329-12338
9. Baxter M.A., Fahlen T.F., Wilson R.L., and Jones B.D. HilE interacts with HilD and negatively regulates hilA transcription and expression of the Salmonella enterica serovar Typhimurium invasive phenotype. Infect. Immun. 71 (2003) 1295-1305
10. Blondelet-Rouault M.H., Weiser J., Lebrihi A., Branny P., and Pernodet J.L. Antibiotic resistance gene cassettes derived from the omega interposon for use in E. coli and Streptomyces. Gene 190 (1997) 315-317
11. Blumer C., Heeb S., Pessi G., and Haas D. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc. Natl. Acad. Sci. USA 96 (1999) 14073-14078
12. Boichenko, M.N., Vorob'ev, A.A., Tymchuk, S.N., 1995. Prospects of obtaining Salmonella cya and crp mutants to be used as vaccine strains. Vestn. Ross. Akad. Med. Nauk. 37-39 (in Russian).
13. Brown C.T., and Callan Jr. C.G. Evolutionary comparisons suggest many novel cAMP response protein binding sites in E. coli. Proc. Natl. Acad. Sci. USA 101 (2004) 2404-2409
14. Chan K., Kim C.C., and Falkow S. Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect. Immun. 73 (2005) 5438-5449
15. Chatterjee A., Cui Y., and Chatterjee A.K. RsmA and the quorum-sensing signal, N-[3-oxohexanoyl]-l-homoserine lactone, control the levels of rsmB RNA in Erwinia carotovora subsp. carotovora by affecting its stability. J. Bacteriol. 184 (2002) 4089-4095
16. Clark M.A., and Barrett E.L. Catabolite repression of thiosulfate reduction by Salmonella typhimurium. Curr. Microbiol. 16 (1987) 27-31
17. Cui Y., Chatterjee A., and Chatterjee A.K. Effects of the two-component system comprising GacA and GacS of Erwinia carotovora subsp. carotovora on the production of global regulatory rsmB RNA, extracellular enzymes, and harpinEcc. Mol. Plant Microbe Interact. 14 (2001) 516-526
18. Curtiss III R., and Kelly S.M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect. Immun. 55 (1987) 3035-3043
19. de Crombrugghe B., Busby S., and Buc H. Cyclic AMP receptor protein: role in transcription activation. Science 224 (1984) 831-838
20. Ellermeier C.D., Janakiraman A., and Slauch J.M. Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290 (2002) 153-161
21. Eriksson A.R., Andersson R.A., Pirhonen M., and Palva E.T. Two-component regulators involved in the global control of virulence in Erwinia carotovora subsp. carotovora. Mol. Plant Microbe Interact. 11 (1998) 743-752
22. Fahlen T.F., Wilson R.L., Boddicker J.D., and Jones B.D. Hha is a negative modulator of transcription of hilA, the Salmonella enterica serovar Typhimurium invasion gene transcriptional activator. J. Bacteriol. 183 (2001) 6620-6629
23. Fandl J.P., Thorner L.K., and Artz S.W. Mutations that affect transcription and cyclic AMP-CRP regulation of the adenylate cyclase gene (cya) of Salmonella typhimurium. Genetics 125 (1990) 719-727
24. Fortune D.R., Suyemoto M., and Altier C. Identification of csrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect. Immun. 74 (2006) 331-339
25. Gavigan S.A., Nguyen T., Nguyen N., and Senear D.F. Role of multiple CytR binding sites on cooperativity, competition, and induction at the E. coli udp promoter. J. Biol. Chem. 274 (1999) 16010-16019
26. Goodier R.I., and Ahmer B.M. SirA orthologs affect both motility and virulence. J. Bacteriol. 183 (2001) 2249-2258
27. Gosset G., Zhang Z., Nayyar S., Cuevas W.A., and Saier Jr. M.H. Transcriptome analysis of CRP-dependent catabolite control of gene expression in E. coli. J. Bacteriol. 186 (2004) 3516-3524
28. Guzman L.M., Belin D., Carson M.J., and Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177 (1995) 4121-4130
29. Hammer B.K., Tateda E.S., and Swanson M.S. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 44 (2002) 107-118
30. Harman J.G. Allosteric regulation of the cAMP receptor protein. Biochim. Biophys. Acta 1547 (2001) 1-17
31. Heeb S., and Haas D. Regulatory roles of the GacS/GacA two-component system in plant-associated and other Gram-negative bacteria. Mol. Plant Microbe Interact. 14 (2001) 1351-1363
32. Heeb S., Blumer C., and Haas D. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J. Bacteriol. 184 (2002) 1046-1056
33. Heinzinger N.K., Fujimoto S.Y., Clark M.A., Moreno M.S., and Barrett E.L. Sequence analysis of the phs operon in Salmonella typhimurium and the contribution of thiosulfate reduction to anaerobic energy metabolism. J. Bacteriol. 177 (1995) 2813-2820
34. Hensel M. Salmonella pathogenicity island 2. Mol. Microbiol. 36 (2000) 1015-1023
35. Johnston C., Pegues D.A., Hueck C.J., Lee A., and Miller S.I. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol. Microbiol. 22 (1996) 715-727
36. Jones B.D., Ghori N., and Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J. Exp. Med. 180 (1994) 15-23
37. Kalogeraki V.S., and Winans S.C. Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188 (1997) 69-75
38. Kennedy M.J., Yancey Jr. R.J., Sanchez M.S., Rzepkowski R.A., Kelly S.M., and Curtiss III R. Attenuation and immunogenicity of Δcya Δcrp derivatives of Salmonella choleraesuis in pigs. Infect. Immun. 67 (1999) 4628-4636
39. Kutsukake K. Autogenous and global control of the flagellar master operon, flhD, in Salmonella typhimurium. Mol. Gen. Genet. 254 (1997) 440-448
40. Lawhon S.D., Maurer R., Suyemoto M., and Altier C. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46 (2002) 1451-1464
41. Lawhon S.D., Frye J.G., Suyemoto M., Porwollik S., McClelland M., and Altier C. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48 (2003) 1633-1645
42. Liu M.Y., and Romeo T. The global regulator CsrA of E. coli is a specific mRNA-binding protein. J. Bacteriol. 179 (1997) 4639-4642
43. Lostroh C.P., and Lee C.A. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 3 (2001) 1281-1291
44. Lucas R.L., and Lee C.A. Roles of hilC and hilD in regulation of hilA expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 183 (2001) 2733-2745
45. Lucas R.L., Lostroh C.P., DiRusso C.C., Spector M.P., Wanner B.L., and Lee C.A. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182 (2000) 1872-1882
46. Maloy S.R., Stewart V.J., and Taylor R.K. Genetic Analysis of Pathogenic Bacteria: a Laboratory Manual (1996), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
47. McClelland M., Sanderson K.E., Spieth J., Clifton S.W., Latreille P., Courtney L., Porwollik S., Ali J., Dante M., Du F., Hou S., Layman D., Leonard S., Nguyen C., Scott K., Holmes A., Grewal N., Mulvaney E., Ryan E., Sun H., Florea L., Miller W., Stoneking T., Nhan M., Waterston R., and Wilson R.K. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 (2001) 852-856
48. Metcalf W.W., Jiang W., Daniels L.L., Kim S.K., Haldimann A., and Wanner B.L. Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35 (1996) 1-13
49. Michael B., Smith J.N., Swift S., Heffron F., and Ahmer B.M. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183 (2001) 5733-5742
50. Miller J.H. Experiments in Molecular Genetics (1972), Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
51. Miller V.L., and Mekalanos J.J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170 (1988) 2575-2583
52. Nagasawa S., Tokishita S., Aiba H., and Mizuno T. A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in E. coli. Mol. Microbiol. 6 (1992) 799-807
53. O'Byrne C.P., and Dorman C.J. The spv virulence operon of Salmonella typhimurium LT2 is regulated negatively by the cyclic AMP (cAMP)-cAMP receptor protein system. J. Bacteriol. 176 (1994) 905-912
54. Olekhnovich I.N., and Kadner R.J. DNA-binding activities of the HilC and HilD virulence regulatory proteins of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184 (2002) 4148-4160
55. Olekhnovich I.N., and Kadner R.J. Crucial roles of both flanking sequences in silencing of the hilA promoter in Salmonella enterica. J. Mol. Biol. 357 (2006) 373-386
56. Parry C.M., Hien T.T., Dougan G., White N.J., and Farrar J.J. Typhoid fever. N. Engl. J. Med. 347 (2002) 1770-1782
57. Pernestig A.K., Melefors O., and Georgellis D. Identification of UvrY as the cognate response regulator for the BarA sensor kinase in E. coli. J. Biol. Chem. 276 (2001) 225-231
58. Petersen S., and Young G.M. Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect. Immun. 70 (2002) 3665-3672
59. Porter S.B., Tinge S.A., and Curtiss Jr. R. Virulence of Salmonella typhimurium mutants for White Leghorn chicks. Avian Dis. 37 (1993) 265-273
60. Rahme L.G., Stevens E.J., Wolfort S.F., Shao J., Tompkins R.G., and Ausubel F.M. Common virulence factors for bacterial pathogenicity in plants and animals. Science 268 (1995) 1899-1902
61. Rakeman J.L., Bonifield H.R., and Miller S.I. A HilA-independent pathway to Salmonella typhimurium invasion gene transcription. J. Bacteriol. 181 (1999) 3096-3104
62. Rappleye C.A., and Roth J.R. A Tn10 derivative (T-POP) for isolation of insertions with conditional (tetracycline-dependent) phenotypes. J. Bacteriol. 179 (1997) 5827-5834
63. Reverchon S., Expert D., Robert-Baudouy J., and Nasser W. The cyclic AMP receptor protein is the main activator of pectinolysis genes in Erwinia chrysanthemi. J. Bacteriol. 179 (1997) 3500-3508
64. Romeo T. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule csrB. Mol. Microbiol. 29 (1998) 1321-1330
65. Romeo T., Gong M., Liu M.Y., and Brun-Zinkernagel A.M. Identification and molecular characterization of csrA, a pleiotropic gene from E. coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol. 175 (1993) 4744-4755
66. Roof D.M., and Roth J.R. Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J. Bacteriol. 174 (1992) 6634-6643
67. Saier Jr. M.H., Chauvaux S., Cook G.M., Deutscher J., Paulsen I.T., Reizer J., and Ye J.J. Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142 (1996) 217-230
68. Schechter L.M., and Lee C.A. AraC/XylS family members, HilC and HilD, directly bind and derepress the Salmonella typhimurium hilA promoter. Mol. Microbiol. 40 (2001) 1289-1299
69. Schechter L.M., Jain S., Akbar S., and Lee C.A. The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium. Infect. Immun. 71 (2003) 5432-5435
70. Skorupski K., and Taylor R.K. Positive selection vectors for allelic exchange. Gene 169 (1996) 47-52
71. Skorupski K., and Taylor R.K. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 94 (1997) 265-270
72. Sutherland E.W. Studies on the mechanism of hormone action. Science 177 (1972) 401-408
73. Suzuki K., Wang X., Weilbacher T., Pernestig A.K., Melefors O., Georgellis D., Babitzke P., and Romeo T. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of E. coli. J. Bacteriol. 184 (2002) 5130-5140
74. Takeuchi A. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50 (1967) 109-136
75. Tan M.W. Identification of host and pathogen factors involved in virulence using Caenorhabditis elegans. Methods Enzymol 358 (2002) 13-29
76. Teplitski M., Goodier R.I., and Ahmer B.M. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J. Bacteriol. 185 (2003) 7257-7265
77. Trewavas A.J., Rodrigues C., Rato C., and Malho R. Cyclic nucleotides: the current dilemma!. Curr. Opin. Plant Biol. 5 (2002) 425-429
78. Valverde C., Heeb S., Keel C., and Haas D. RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol. Microbiol. 50 (2003) 1361-1379
79. Wang R.F., and Kushner S.R. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in E. coli. Gene 100 (1991) 195-199
80. Wang J.Y., Clegg D.O., and Koshland Jr. D.E. Molecular cloning and amplification of the adenylate cyclase gene. Proc. Natl. Acad. Sci. USA 78 (1981) 4684-4688
81. Wei B., Shin S., LaPorte D., Wolfe A.J., and Romeo T. Global regulatory mutations in csrA and rpoS cause severe central carbon stress in E. coli in the presence of acetate. J. Bacteriol. 182 (2000) 1632-1640
82. Weilbacher T., Suzuki K., Dubey A.K., Wang X., Gudapaty S., Morozov I., Baker C.S., Georgellis D., Babitzke P., and Romeo T. A novel sRNA component of the carbon storage regulatory system of E. coli. Mol. Microbiol. 48 (2003) 657-670
83. Wilson R.L., Libby S.J., Freet A.M., Boddicker J.D., Fahlen T.F., and Jones B.D. Fis, a DNA nucleoid-associated protein, is involved in Salmonella typhimurium SPI-1 invasion gene expression. Mol. Microbiol. 39 (2001) 79-88
84. Winson M.K., Swift S., Fish L., Throup J.P., Jorgensen F., Chhabra S.R., Bycroft B.W., Williams P., and Stewart G.S. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163 (1998) 185-192
85. Yanagihara S., Iyoda S., Ohnishi K., Iino T., and Kutsukake K. Structure and transcriptional control of the flagellar master operon of Salmonella typhimurium. Genes Genet. Syst. 74 (1999) 105-111
86. Yokota T., and Gots J.S. Requirement of adenosine 3',5'-cyclic phosphate for flagella formation in E. coli and Salmonella typhimurium. J. Bacteriol. 103 (1970) 513-516
87. Zhang S., Kingsley R.A., Santos R.L., Andrews-Polymenis H., Raffatellu M., Figueiredo J., Nunes J., Tsolis R.M., Adams L.G., and Baumler A.J. Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea. Infect. Immun. 71 (2003) 1-12