Identification of IbeR As a Stationary-phase Regulator in Meningitic Escherichia Coli K1 That Carries a Loss-of-function Mutation in RpoS

Overview

Journal J Biomed Biotechnol

Specialty Biology

Date 2009 Mar 21

PMID 19300523

Citations 12

Authors

Feng Chi

Ying Wang

Timothy K Gallaher

Chun-Hua Wu

Ambrose Jong

Sheng-He Huang

Affiliations

Soon will be listed here.

Abstract

IbeR is a regulator present in meningitic Escherichia coli strain E44 that carries a loss-of-function mutation in the stationary-phase (SP) regulatory gene rpoS. In order to determine whether IbeR is an SP regulator in E44, two-dimensional gel electrophoresis and LC-MS were used to compare the proteomes of a noninvasive ibeR deletion mutant BR2 and its parent strain E44 in the SP. Four up-regulated (TufB, GapA, OmpA, AhpC) and three down-regulated (LpdA, TnaA, OpmC) proteins in BR2 were identified when compared to E44. All these proteins contribute to energy metabolism or stress resistance, which is related to SP regulation. One of the down-regulated proteins, tryptophanase (TnaA), which is regulated by RpoS in other E. coli strains, is associated with SP regulation via production of a signal molecule indole. Our studies demonstrated that TnaA was required for E44 invasion, and that indole was able to restore the noninvasive phenotype of the tnaA mutant. The production of indole was significantly reduced in BR2, indicating that ibeR is required for the indole production via tnaA. Survival studies under different stress conditions indicated that IbeR contributed to bacteria stress resistance in the SP. Taken together, IbeR is a novel regulator contributing to the SP regulation.

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References

Rolhion N, Carvalho F, Darfeuille-Michaud A . OmpC and the sigma(E) regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol. 2007; 63(6):1684-700. DOI: 10.1111/j.1365-2958.2007.05638.x. View

Bachler C, Schneider P, Bahler P, Lustig A, Erni B . Escherichia coli dihydroxyacetone kinase controls gene expression by binding to transcription factor DhaR. EMBO J. 2004; 24(2):283-93. PMC: 545809. DOI: 10.1038/sj.emboj.7600517. View

Zou Y, He L, Huang S . Identification of a surface protein on human brain microvascular endothelial cells as vimentin interacting with Escherichia coli invasion protein IbeA. Biochem Biophys Res Commun. 2006; 351(3):625-30. DOI: 10.1016/j.bbrc.2006.10.091. View

Wang Y, Kim K . Effect of rpoS mutations on stress-resistance and invasion of brain microvascular endothelial cells in Escherichia coli K1. FEMS Microbiol Lett. 2000; 182(2):241-7. DOI: 10.1111/j.1574-6968.2000.tb08902.x. View

Alphen W, Lugtenberg B . Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol. 1977; 131(2):623-30. PMC: 235471. DOI: 10.1128/jb.131.2.623-630.1977. View

Wang Y . The function of OmpA in Escherichia coli. Biochem Biophys Res Commun. 2002; 292(2):396-401. DOI: 10.1006/bbrc.2002.6657. View

Nikaido H . Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003; 67(4):593-656. PMC: 309051. DOI: 10.1128/MMBR.67.4.593-656.2003. View

Donnenberg M, Kaper J . Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun. 1991; 59(12):4310-7. PMC: 259042. DOI: 10.1128/iai.59.12.4310-4317.1991. View

Smith A, Roche H, Trombe M, Briles D, Hakansson A . Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol Microbiol. 2002; 44(2):431-48. DOI: 10.1046/j.1365-2958.2002.02883.x. View

10.

Yang W, Ni L, SOMERVILLE R . A stationary-phase protein of Escherichia coli that affects the mode of association between the trp repressor protein and operator-bearing DNA. Proc Natl Acad Sci U S A. 1993; 90(12):5796-800. PMC: 46809. DOI: 10.1073/pnas.90.12.5796. View

11.

Donnenberg M, Calderwood S, Donohue-Rolfe A, Keusch G, Kaper J . Construction and analysis of TnphoA mutants of enteropathogenic Escherichia coli unable to invade HEp-2 cells. Infect Immun. 1990; 58(6):1565-71. PMC: 258676. DOI: 10.1128/iai.58.6.1565-1571.1990. View

12.

Huang S, Chen Y, Fu Q, Stins M, Wang Y, Wass C . Identification and characterization of an Escherichia coli invasion gene locus, ibeB, required for penetration of brain microvascular endothelial cells. Infect Immun. 1999; 67(5):2103-9. PMC: 115944. DOI: 10.1128/IAI.67.5.2103-2109.1999. View

13.

Zheng M, Wang X, Templeton L, Smulski D, LaRossa R, Storz G . DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol. 2001; 183(15):4562-70. PMC: 95351. DOI: 10.1128/JB.183.15.4562-4570.2001. View

14.

Badger J, Wass C, Weissman S, Kim K . Application of signature-tagged mutagenesis for identification of escherichia coli K1 genes that contribute to invasion of human brain microvascular endothelial cells. Infect Immun. 2000; 68(9):5056-61. PMC: 101737. DOI: 10.1128/IAI.68.9.5056-5061.2000. View

15.

. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell. 1993; 72(2):165-8. DOI: 10.1016/0092-8674(93)90655-a. View

16.

. Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol Microbiol. 1996; 21(5):887-93. DOI: 10.1046/j.1365-2958.1996.511405.x. View

17.

Wang D, Ding X, Rather P . Indole can act as an extracellular signal in Escherichia coli. J Bacteriol. 2001; 183(14):4210-6. PMC: 95310. DOI: 10.1128/JB.183.14.4210-4216.2001. View

18.

Loewen P . The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994; 48:53-80. DOI: 10.1146/annurev.mi.48.100194.000413. View

19.

Silver R, AARONSON W, Sutton A, Schneerson R . Comparative analysis of plasmids and some metabolic characteristics of Escherichia coli K1 from diseased and healthy individuals. Infect Immun. 1980; 29(1):200-6. PMC: 551096. DOI: 10.1128/iai.29.1.200-206.1980. View

20.

Udekwu K, Wagner E . Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res. 2007; 35(4):1279-88. PMC: 1851643. DOI: 10.1093/nar/gkl1154. View