Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP

Molecular Microbiology

Volumn 58, Issue 5, 2005, Pages 1354-1367

  Oglesby, Amanda G ^a   Murphy, Erin R ^a   Iyer, Vishwanath R ^a   Payne, Shelley M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; BACTERIAL PROTEIN; GLUTAMIC ACID; IRON; OXIDOREDUCTASE;

ARTICLE; BACTERIAL STRAIN; DEFENSE MECHANISM; DNA MICROARRAY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC CODE; HOMEOSTASIS; IRON TRANSPORT; NONHUMAN; PH MEASUREMENT; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SHIGELLA FLEXNERI; SURVIVAL; WILD TYPE;

BACTERIAL PROTEINS; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HYDROGEN-ION CONCENTRATION; IRON; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDOREDUCTASES; POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; SHIGELLA FLEXNERI; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); SHIGELLA FLEXNERI;

EID: 28244485425     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04920.x     Document Type: Article

References (63)

1. Bagg, A., and Neilands, J.B. (1987) Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26: 5471-5477.
2. Baichoo, N., and Helmann, J.D. (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184: 5826-5832.
3. Blattner, F.R., Plunkett, G., 3rd, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
4. Calderwood, S.B., and Mekalanos, J.J. (1987) Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J Bacteriol 169: 4759-4764.
5. Campoy, S., Jara, M., Busquets, N., de Rozas, A.M., Badiola, I., and Barbe, J. (2002) Intracellular cyclic AMP concentration is decreased in Salmonella typhimurium fur mutants. Microbiology 148: 1039-1048.
6. Carlioz, A., and Touati, D. (1986) Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5: 623-630.
7. Castanie-Cornet, M.P., and Foster, J.W. (2001) Escherichia coli acid resistance: cAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 147: 709-715.
8. Castanie-Cornet, M.P., Penfound, T.A., Smith, D., Elliott, J.F., and Foster, J.W. (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181: 3525-3535.
9. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
10. Daskaleros, P.A., and Payne, S.M. (1987) Congo red binding phenotype is associated with hemin binding and increased infectivity of Shigella flexneri in the HeLa cell model. Infect Immun 55: 1393-1398.
11. De Biase, D., Tramonti, A., Bossa, F., and Visca, P. (1999) The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol 32:1198-1211.
12. DuPont, H.L., Levine, M.M., Hornick, R.B., and Formal, S.B. (1989) Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 159: 1126-1128.
13. Escolar, L., Perez-Martin, J., and de Lorenzo, V. (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
14. Fischer, E., Gunter, K., and Braun, V. (1989) Involvement of ExbB and TonB in transport across the outer membrane of Escherichia coli: phenotypic complementation of exb mutants by overexpressed tonB and physical stabilization of TonB by ExbB. J Bacteriol 171: 5127-5134.
15. Foster, J.W. (1991) Salmonella acid shock proteins are required for the adaptive acid tolerance response. J Bacteriol 173: 6896-6902.
16. Foster, J.W., and Hall, H.K. (1991) Inducible pH homeostasis and the acid tolerance response of Salmonella typhimurium. J Bacteriol 173: 5129-5135.
17. Foster, J.W., and Hall, H.K. (1992) Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron- and pH-regulated protein synthesis. J Bacteriol 174: 4317-4323.
18. Gajiwala, K.S., and Burley, S.K. (2000) HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295: 605-612.
19. Gerhardt, P., Murray, R.G.E., Wood, W.A., and Krieg, N.R. (eds) (1994) Methods for General and Molecular Bacteriology. Washington, DC: American Society for Microbiology.
20. Gorden, J., and Small, P.L. (1993) Acid resistance in enteric bacteria. Infect Immun 61: 364-367.
21. Hall, H.K., and Foster, J.W. (1996) The role of fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol 178: 5683-5691.
22. Hantke, K. (1983) Identification of an iron uptake system specific for coprogen and rhodotorulic acid in Escherichia coli K12. Mol General Genet 191: 301-306.
23. Hantke, K. (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172-177.
24. Heimer, S.R., Welch, R.A., Perna, N.T., Posfai, G., Evans, P.S., Kaper, J.B., et al. (2002) Urease of enterohemorrhagic Escherichia coli: evidence for regulation by fur and a trans-acting factor. Infect Immun 70: 1027-1031.
25. Hersh, B.M., Farooq, FT., Barstad, D.N., Blankenhorn, D.L., and Slonczewski, J.L. (1996) A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178: 3978-3981.
26. Hershberg, R., Altuvia, S., and Margalit, H. (2003) A survey of small RNA-encoding genes in Escherichia coli. Nucl Acids Res 31: 1813-1820.
27. Hommais, F., Krin, E., Coppee, J.Y., Lacroix, C., Yeramian, E., Danchin, A., and Bertin, P. (2004) GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150: 61-72.
28. Jennison, A.V., and Verma, N.K. (2004) Shigella flexneri infection: pathogenesis and vaccine development. FEMS Microbiol Rev 28: 43-58.
29. Jin, Q., Yuan, Z., Xu, J., Wang, Y., Shen, Y., Lu, W., et al. (2002) Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucl Acids Res 30: 4432-4441.
30. Kammler, M., Schon, C., and Hantke, K. (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175: 6212-6219.
31. Lin, J., Lee, I., Frey, J., Slonczewski, J., and Foster, J. (1995) Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177: 4097-4104.
32. de Lorenzo, V., Wee, S., Herrero, M., and Neilands, J.B. (1987) Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (Fur) repressor. J Bacteriol 169: 2624-2630.
33. Ma, Z., Gong, S., Richard, H., Tucker, D.L., Conway, T., and Foster, J.W. (2003) GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol 49: 1309-1320.
34. Ma, Z., Masuda, N., and Foster, J.W. (2004) Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli. J Bacteriol 186: 7378-7389.
35. McHugh, J.P., Rodriguez-Quinones, F., Abdul-Tehrani, H., Svistunenko, D.A., Poole, R.K., Cooper, C.E., and Andrews, S.C. (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 278: 29478-29486.
36. Martinez, A., and Kolter, R. (1997) Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179: 5188-5194.
37. Masse, E., and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99: 4620-4625.
38. Masse, E., Escorcia, F.E., and Gottesman, S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383.
39. Masuda, N., and Church, G.M. (2002) Escherichia coli gene expression responsive to levels of the response regulator EvgA. J Bacteriol 184: 6225-6234.
40. Masuda, N., and Church, G.M. (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48: 699-712.
41. Matzanke, B.F., Anemuller, S., Schunemann, V., Trautwein, A.X., and Hantke, K. (2004) FhuF, part of a siderophore-reductase system. Biochemistry 43: 1386-1392.
42. Nishino, K., Inazumi, Y., and Yamaguchi, A. (2003) Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli. J Bacteriol 185: 2667-2672.
43. Outten, F.W., Djaman, O., and Storz, G. (2004) A sufoperon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol Microbiol 52: 861-872.
44. Park, Y.K., Bearson, B., Bang, S.H., Bang, I.S., and Foster, J.W. (1996) Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella typhimurium. Mol Microbiol 20: 605-611.
45. Payne, S.M., and Mey, A.R. (2004) Pathogenic Escherichia coli, Shigella, and Salmonella. In Iron Transport in Bacteria. Crosa, J.H., Mey, A.R., and Payne, S.M. (eds). Washington, DC: American Society for Microbiology Press, pp. 199-218.
46. Payne, S.M., Niesel, D.W., Peixotto, S.S., and Lawlor, K.M. (1983) Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol 155: 949-955.
47. Rogers, H.J. (1973) Iron-binding catechols and virulence in Escherichia coli. Infect Immun 7: 438-444.
48. Rossmann, R., Sawers, G., and Bock, A. (1991) Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol Microbiol 5: 2807-2814.
49. Runyen-Janecky, L.J., Reeves, S.A., Gonzales, E.G., and Payne, S.M. (2003) Contribution of the Shigella flexneri Sit, luc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71: 1919-1803.
50. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Sawers, G. (1994) The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 66: 57-88.
52. Schmitt, M.P. (1989) Genetics and regulation of the enterobactin genes in strains of Shigella flexneri. PhD Thesis Austin, TX: University of Texas at Austin.
53. Schmitt, M.P., and Payne, S.M. (1988) Genetics and regulation of enterobactin genes in Shigella flexneri. J Bacteriol 170: 5579-5587.
54. Stancik, L.M., Stancik, D.M., Schmidt, B., Barnhart, D.M., Yoncheva, Y.N., and Slonczewski, J.L. (2002) pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol 184: 4246-4258.
55. Taylor, R.K., Manoil, C., and Mekalanos, J.J. (1989) Broad-host-range vectors for delivery of TnphoA: use in genetic analysis of secreted virulence determinants of Vibrio cholerae. J Bacteriol 171: 1870-1878.
56. Touati, D., Jacques, M., Tardat, B., Bouchard, L., and Despied, S. (1995) Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177: 2305-2314.
57. Tucker, D.L., Tucker, N., and Conway, T. (2002) Gene expression profiling of the pH response in Escherichia coli. J Bacteriol 184: 6551-6558.
58. Vecerek, B., Moll, I., Afonyushkin, T., Kaberdin, V., and Blasi, U. (2003) Interaction of the RNA chaperone Hfq with mRNAs: direct and indirect roles of Hfq in iron metabolism of Escherichia coli. Mol Microbiol 50: 897-909.
59. Venkatesan, M.M., Goldberg, M.B., Rose, D.J., Grotbeck, E.J., Burland, V., and Blattner, F.R. (2001) Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect Immun 69: 3271-3285.
60. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
61. Waterman, S.R., and Small, P.L. (1996) Identification of sigma S-dependent genes associated with the stationary-phase acid-resistance phenotype of Shigella flexneri. Mol Microbiol 21: 925-940.
62. Wei, J., Goldberg, M.B., Burland, V., Venkatesan, M.M., Deng, W., Fournier, G., et al. (2003) Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 71: 2775-2786.
63. Zhu, C., Ngeleka, M., Potter, A.A., and Allan, B.J. (2002) Effect of fur mutation on acid-tolerance response and in vivo virulence of avian septicemic Escherichia coli. Can J Microbiol 48: 458-462.