Regulation of Expression of Uropathogenic Escherichia Coli Nonfimbrial Adhesin TosA by PapB Homolog TosR in Conjunction with H-NS and Lrp

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 2016 Jan 13

PMID 26755158

Citations 12

Authors

Michael D Engstrom

Harry L T Mobley

Affiliations

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Abstract

Urinary tract infections (UTIs) are a major burden to human health. The overwhelming majority of UTIs are caused by uropathogenic Escherichia coli (UPEC) strains. Unlike some pathogens, UPEC strains do not have a fixed core set of virulence and fitness factors but do have a variety of adhesins and regulatory pathways. One such UPEC adhesin is the nonfimbrial adhesin TosA, which mediates adherence to the epithelium of the upper urinary tract. The tos operon is AT rich, resides on pathogenicity island aspV, and is not expressed under laboratory conditions. Because of this, we hypothesized that tosA expression is silenced by H-NS. Lrp, based on its prominent function in the regulation of other adhesins, is also hypothesized to contribute to tos operon regulation. Using a variety of in vitro techniques, we mapped both the tos operon promoter and TosR binding sites. We have now identified TosR as a dual regulator of the tos operon, which could control the tos operon in association with H-NS and Lrp. H-NS is a negative regulator of the tos operon, and Lrp positively regulates the tos operon. Exogenous leucine also inhibits Lrp-mediated tos operon positive regulation. In addition, TosR binds to the pap operon, which encodes another important UPEC adhesin, P fimbria. Induction of TosR synthesis reduces production of P fimbria. These studies advance our knowledge of regulation of adhesin expression associated with uropathogen colonization of a host.

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References

Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A . Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol. 1999; 181(20):6361-70. PMC: 103771. DOI: 10.1128/JB.181.20.6361-6370.1999. View

Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S, Danchin A . Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol. 1999; 181(24):7500-8. PMC: 94207. DOI: 10.1128/JB.181.24.7500-7508.1999. View

Ko M, Park C . H-NS-Dependent regulation of flagellar synthesis is mediated by a LysR family protein. J Bacteriol. 2000; 182(16):4670-2. PMC: 94646. DOI: 10.1128/JB.182.16.4670-4672.2000. View

Dame R, Wyman C, Goosen N . H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Res. 2000; 28(18):3504-10. PMC: 110753. DOI: 10.1093/nar/28.18.3504. View

Fullner K, Mekalanos J . In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J. 2000; 19(20):5315-23. PMC: 314022. DOI: 10.1093/emboj/19.20.5315. View

Villapakkam A, Ronaszeki K, Young S . H-NS controls pap and daa fimbrial transcription in Escherichia coli in response to multiple environmental cues. J Bacteriol. 2000; 182(22):6391-400. PMC: 94785. DOI: 10.1128/JB.182.22.6391-6400.2000. View

Khlebnikov A, Risa O, Skaug T, Carrier T, Keasling J . Regulatable arabinose-inducible gene expression system with consistent control in all cells of a culture. J Bacteriol. 2000; 182(24):7029-34. PMC: 94830. DOI: 10.1128/JB.182.24.7029-7034.2000. View

Weyand N, Braaten B, van der Woude M, Tucker J, Low D . The essential role of the promoter-proximal subunit of CAP in pap phase variation: Lrp- and helical phase-dependent activation of papBA transcription by CAP from -215. Mol Microbiol. 2001; 39(6):1504-22. DOI: 10.1046/j.1365-2958.2001.02338.x. View

Paul L, Blumenthal R, Matthews R . Activation from a distance: roles of Lrp and integration host factor in transcriptional activation of gltBDF. J Bacteriol. 2001; 183(13):3910-8. PMC: 95273. DOI: 10.1128/JB.183.13.3910-3918.2001. View

10.

Holden N, Uhlin B, Gally D . PapB paralogues and their effect on the phase variation of type 1 fimbriae in Escherichia coli. Mol Microbiol. 2001; 42(2):319-30. DOI: 10.1046/j.1365-2958.2001.02656.x. View

11.

Smolke C, Khlebnikov A, Keasling J . Effects of transcription induction homogeneity and transcript stability on expression of two genes in a constructed operon. Appl Microbiol Biotechnol. 2002; 57(5-6):689-96. DOI: 10.1007/s002530100812. View

12.

Rimsky S, Zuber F, Buckle M, Buc H . A molecular mechanism for the repression of transcription by the H-NS protein. Mol Microbiol. 2002; 42(5):1311-23. DOI: 10.1046/j.1365-2958.2001.02706.x. View

13.

Foxman B . Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med. 2002; 113 Suppl 1A:5S-13S. DOI: 10.1016/s0002-9343(02)01054-9. View

14.

Hernday A, Krabbe M, Braaten B, Low D . Self-perpetuating epigenetic pili switches in bacteria. Proc Natl Acad Sci U S A. 2002; 99 Suppl 4:16470-6. PMC: 139910. DOI: 10.1073/pnas.182427199. View

15.

Welch R, Burland V, Plunkett 3rd G, Redford P, Roesch P, Rasko D . Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 2002; 99(26):17020-4. PMC: 139262. DOI: 10.1073/pnas.252529799. View

16.

Braaten B, Platko J, van der Woude M, Simons B, de Graaf F, Calvo J . Leucine-responsive regulatory protein controls the expression of both the pap and fan pili operons in Escherichia coli. Proc Natl Acad Sci U S A. 1992; 89(10):4250-4. PMC: 49059. DOI: 10.1073/pnas.89.10.4250. View

17.

Jordi B, Dagberg B, de Haan L, Hamers A, van der Zeijst B, Gaastra W . The positive regulator CfaD overcomes the repression mediated by histone-like protein H-NS (H1) in the CFA/I fimbrial operon of Escherichia coli. EMBO J. 1992; 11(7):2627-32. PMC: 556738. DOI: 10.1002/j.1460-2075.1992.tb05328.x. View

18.

Forsman K, Sonden B, Goransson M, Uhlin B . Antirepression function in Escherichia coli for the cAMP-cAMP receptor protein transcriptional activator. Proc Natl Acad Sci U S A. 1992; 89(20):9880-4. PMC: 50237. DOI: 10.1073/pnas.89.20.9880. View

19.

Troutt A, McHeyzer-Williams M, Pulendran B, Nossal G . Ligation-anchored PCR: a simple amplification technique with single-sided specificity. Proc Natl Acad Sci U S A. 1992; 89(20):9823-5. PMC: 50225. DOI: 10.1073/pnas.89.20.9823. View

20.

Will W, Lu J, Frost L . The role of H-NS in silencing F transfer gene expression during entry into stationary phase. Mol Microbiol. 2004; 54(3):769-82. DOI: 10.1111/j.1365-2958.2004.04303.x. View