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      Posttranscription Initiation Control of Gene Expression Mediated by Bacterial RNA-Binding Proteins

      1 , 2 , 1 , 2

      Annual Review of Microbiology

      Annual Reviews

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          Abstract

          RNA-binding proteins play vital roles in regulating gene expression and cellular physiology in all organisms. Bacterial RNA-binding proteins can regulate transcription termination via attenuation or antitermination mechanisms, while others can repress or activate translation initiation by affecting ribosome binding. The RNA targets for these proteins include short repeated sequences, longer single-stranded sequences, RNA secondary or tertiary structure, and a combination of these features. The activity of these proteins can be influenced by binding of metabolites, small RNAs, or other proteins, as well as by phosphorylation events. Some of these proteins regulate specific genes, while others function as global regulators. As the regulatory mechanisms, components, targets, and signaling circuitry surrounding RNA-binding proteins have become better understood, in part through rapid advances provided by systems approaches, a sense of the true nature of biological complexity is becoming apparent, which we attempt to capture for the reader of this review.

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          Most cited references 140

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          Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems.

          Originally described as a repressor of gene expression in the stationary phase of growth, CsrA (RsmA) regulates primary and secondary metabolic pathways, biofilm formation, motility, virulence circuitry of pathogens, quorum sensing and stress response systems by binding to conserved sequences in its target mRNAs and altering their translation and/or turnover. While the binding of CsrA to RNA is understood at an atomic level, new mechanisms of gene activation and repression by this protein are still emerging. In the γ-proteobacteria, small non-coding RNAs (sRNAs) use molecular mimicry to sequester multiple CsrA dimers away from mRNA. In contrast, the FliW protein of Bacillus subtilis inhibits CsrA activity by binding to this protein, thereby establishing a checkpoint in flagellum morphogenesis. Turnover of CsrB and CsrC sRNAs in Escherichia coli requires a specificity protein of the GGDEF-EAL domain superfamily, CsrD, in addition to the housekeeping nucleases RNase E and PNPase. The Csr system of E. coli contains extensive autoregulatory circuitry, which governs the expression and activity of CsrA. Interaction of the Csr system with transcriptional regulatory networks results in a variety of complex response patterns. This minireview will highlight basic principles and new insights into the workings of these complex eubacterial regulatory systems. © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd.
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            The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs.

            We report here the results of an analysis of the regulatory range of the GacS/GacA two-component system in Pseudomonas aeruginosa. Using microarrays, we identified a large number of genes that are regulated by the system, and detected a near complete overlap of these genes with those regulated by two small RNAs (sRNAs), RsmY and RsmZ, suggesting that the expression of all GacA-regulated genes is RsmY/Z-dependent. Using genome-wide DNA-protein interaction analyses, we identified only two genomic regions that associated specifically with GacA, located upstream of the rsmY and rsmZ genes. These results demonstrate that in P. aeruginosa, the GacS/GacA system transduces the regulatory signals to downstream genes exclusively by directly controlling the expression of only two genes rsmY and rsmZ. These two sRNAs serve as intermediates between the input signals and the output at the level of mRNA stability, although additional regulatory inputs can influence the levels of these two riboregulators. We show that the A+T-rich DNA segment upstream of rsmZ is bound and silenced by MvaT and MvaU, the global gene regulators of the H-NS family. This work highlights the importance of post-transcriptional mechanisms involving sRNAs in controlling gene expression during bacterial adaptation to different environments.
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              CsrB sRNA family: sequestration of RNA-binding regulatory proteins.

              Noncoding regulatory RNA molecules, also known as small RNAs, participate in several bacterial regulatory networks. The central component of the carbon storage regulator (Csr) and the homologous repressor of secondary metabolites (Rsm) systems is an RNA binding protein (CsrA or RsmA) that regulates gene expression post-transcriptionally by affecting ribosome binding and/or mRNA stability. Members of the CsrB family of noncoding regulatory RNA molecules contain multiple CsrA binding sites and function as CsrA antagonists by sequestering this protein. Depending on the particular organism, the Csr (or Rsm) system participates in global regulatory circuits that control central carbon flux, the production of extracellular products, cell motility, biofilm formation, quorum sensing and/or pathogenesis.
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                Author and article information

                Journal
                Annual Review of Microbiology
                Annu. Rev. Microbiol.
                Annual Reviews
                0066-4227
                1545-3251
                September 08 2019
                September 08 2019
                : 73
                : 1
                : 43-67
                Affiliations
                [1 ]Department of Biochemistry and Molecular Biology, Center for RNA Molecular Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA;,
                [2 ]Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, Florida 32611, USA;,
                Article
                10.1146/annurev-micro-020518-115907
                © 2019

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