Literature DB >> 24056837

A novel CsrA titration mechanism regulates fimbrial gene expression in Salmonella typhimurium.

Torsten Sterzenbach1, Kim T Nguyen, Sean-Paul Nuccio, Maria G Winter, Christopher A Vakulskas, Steven Clegg, Tony Romeo, Andreas J Bäumler.   

Abstract

A hierarchical control of fimbrial gene expression limits laboratory grown cultures of Salmonella enterica serovar typhimurium (S. typhimurium) to the production of type I fimbriae encoded by the fimAICDHF operon. Here we show that an unlikely culprit, namely the 5'-untranslated region (5'-UTR) of a messenger (m)RNA, coordinated the regulation. Binding of CsrA to the 5'-UTR of the pefACDEF transcript was required for expression of plasmid-encoded fimbriae. The 5'-UTR of the fimAICDHF transcript cooperated with two small untranslated RNAs, termed CsrB and CsrC, in antagonizing the activity of the RNA binding protein CsrA. Through this post-transcriptional mechanism, the 5'-UTR of the fimAICDHF transcript prevented production of PefA, the major structural subunit of plasmid-encoded fimbriae. This regulatory mechanism limits the costly expression of plasmid-encoded fimbriae to host environments in a mouse model. Collectively, our data suggest that the 5'-UTR of an mRNA coordinates a hierarchical control of fimbrial gene expression in S. typhimurium.

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Year:  2013        PMID: 24056837      PMCID: PMC3817462          DOI: 10.1038/emboj.2013.206

Source DB:  PubMed          Journal:  EMBO J        ISSN: 0261-4189            Impact factor:   11.598


  59 in total

Review 1.  Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek.

Authors:  Sean-Paul Nuccio; Andreas J Bäumler
Journal:  Microbiol Mol Biol Rev       Date:  2007-12       Impact factor: 11.056

Review 2.  Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease.

Authors:  T Proft; E N Baker
Journal:  Cell Mol Life Sci       Date:  2009-02       Impact factor: 9.261

3.  The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli.

Authors:  Shantanu Bhatt; Adrianne Nehrling Edwards; Hang Thi Thu Nguyen; Didier Merlin; Tony Romeo; Daniel Kalman
Journal:  Infect Immun       Date:  2009-07-06       Impact factor: 3.441

4.  Regulating the regulator: an RNA decoy acts as an OFF switch for the regulation of an sRNA.

Authors:  Pierre Mandin; Susan Gottesman
Journal:  Genes Dev       Date:  2009-09-01       Impact factor: 11.361

5.  Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression.

Authors:  Jeffrey Mercante; Adrianne N Edwards; Ashok K Dubey; Paul Babitzke; Tony Romeo
Journal:  J Mol Biol       Date:  2009-07-17       Impact factor: 5.469

6.  Binding specificity of Salmonella plasmid-encoded fimbriae assessed by glycomics.

Authors:  Daniela Chessa; Caleb W Dorsey; Maria Winter; Andreas J Baümler
Journal:  J Biol Chem       Date:  2008-01-22       Impact factor: 5.157

7.  Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target.

Authors:  Nara Figueroa-Bossi; Martina Valentini; Laurette Malleret; Francesca Fiorini; Lionello Bossi
Journal:  Genes Dev       Date:  2009-07-28       Impact factor: 11.361

Review 8.  Structural biology of the chaperone-usher pathway of pilus biogenesis.

Authors:  Gabriel Waksman; Scott J Hultgren
Journal:  Nat Rev Microbiol       Date:  2009-10-12       Impact factor: 60.633

9.  The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins.

Authors:  Kristina Jonas; Adrianne N Edwards; Roger Simm; Tony Romeo; Ute Römling; Ojar Melefors
Journal:  Mol Microbiol       Date:  2008-08-18       Impact factor: 3.501

10.  Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella Typhimurium.

Authors:  Kristina Jonas; Adrianne N Edwards; Irfan Ahmad; Tony Romeo; Ute Römling; Ojar Melefors
Journal:  Environ Microbiol       Date:  2009-11-17       Impact factor: 5.491

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  30 in total

1.  Identification and regulation of a novel Citrobacter rodentium gut colonization fimbria (Gcf).

Authors:  Gustavo G Caballero-Flores; Matthew A Croxen; Verónica I Martínez-Santos; B Brett Finlay; José L Puente
Journal:  J Bacteriol       Date:  2015-02-09       Impact factor: 3.490

Review 2.  Regulation of bacterial virulence by Csr (Rsm) systems.

Authors:  Christopher A Vakulskas; Anastasia H Potts; Paul Babitzke; Brian M M Ahmer; Tony Romeo
Journal:  Microbiol Mol Biol Rev       Date:  2015-06       Impact factor: 11.056

Review 3.  RNA-based mechanisms of virulence control in Enterobacteriaceae.

Authors:  Ann Kathrin Heroven; Aaron M Nuss; Petra Dersch
Journal:  RNA Biol       Date:  2016-07-21       Impact factor: 4.652

Review 4.  Competing endogenous RNAs: a target-centric view of small RNA regulation in bacteria.

Authors:  Lionello Bossi; Nara Figueroa-Bossi
Journal:  Nat Rev Microbiol       Date:  2016-09-19       Impact factor: 60.633

Review 5.  Global Regulation by CsrA and Its RNA Antagonists.

Authors:  Tony Romeo; Paul Babitzke
Journal:  Microbiol Spectr       Date:  2018-03

6.  Factors Required for Adhesion of Salmonella enterica Serovar Typhimurium to Corn Salad (Valerianella locusta).

Authors:  Laura Elpers; Juliane Kretzschmar; Sean-Paul Nuccio; Andreas J Bäumler; Michael Hensel
Journal:  Appl Environ Microbiol       Date:  2020-04-01       Impact factor: 4.792

7.  RsmV, a Small Noncoding Regulatory RNA in Pseudomonas aeruginosa That Sequesters RsmA and RsmF from Target mRNAs.

Authors:  Kayley H Janssen; Manisha R Diaz; Cindy J Gode; Matthew C Wolfgang; Timothy L Yahr
Journal:  J Bacteriol       Date:  2018-07-25       Impact factor: 3.490

8.  FliW antagonizes CsrA RNA binding by a noncompetitive allosteric mechanism.

Authors:  Sampriti Mukherjee; Reid T Oshiro; Helen Yakhnin; Paul Babitzke; Daniel B Kearns
Journal:  Proc Natl Acad Sci U S A       Date:  2016-08-11       Impact factor: 11.205

9.  The AlgZR two-component system recalibrates the RsmAYZ posttranscriptional regulatory system to inhibit expression of the Pseudomonas aeruginosa type III secretion system.

Authors:  Peter J Intile; Manisha R Diaz; Mark L Urbanowski; Matthew C Wolfgang; Timothy L Yahr
Journal:  J Bacteriol       Date:  2013-11-01       Impact factor: 3.490

Review 10.  Trans-Acting Small RNAs and Their Effects on Gene Expression in Escherichia coli and Salmonella enterica.

Authors:  Jens Hör; Gianluca Matera; Jörg Vogel; Susan Gottesman; Gisela Storz
Journal:  EcoSal Plus       Date:  2020-03
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