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  • Vogel, Jorg  (85)
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  • 1
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 25 August 2015, Vol.112(34), pp.E4772-81
    Description: Horizontal gene transfer via plasmid conjugation is a major driving force in microbial evolution but constitutes a complex process that requires synchronization with the physiological state of the host bacteria. Although several host transcription factors are known to regulate plasmid-borne transfer genes, RNA-based regulatory circuits for host-plasmid communication remain unknown. We describe a posttranscriptional mechanism whereby the Hfq-dependent small RNA, RprA, inhibits transfer of pSLT, the virulence plasmid of Salmonella enterica. RprA employs two separate seed-pairing domains to activate the mRNAs of both the sigma-factor σ(S) and the RicI protein, a previously uncharacterized membrane protein here shown to inhibit conjugation. Transcription of ricI requires σ(S) and, together, RprA and σ(S) orchestrate a coherent feedforward loop with AND-gate logic to tightly control the activation of RicI synthesis. RicI interacts with the conjugation apparatus protein TraV and limits plasmid transfer under membrane-damaging conditions. To our knowledge, this study reports the first small RNA-controlled feedforward loop relying on posttranscriptional activation of two independent targets and an unexpected role of the conserved RprA small RNA in controlling extrachromosomal DNA transfer.
    Keywords: Hfq ; Rpra ; Feedforward Control ; Plasmid Conjugation ; Srna ; Chromosomes, Bacterial ; DNA, Bacterial -- Genetics ; RNA, Bacterial -- Genetics ; Salmonella -- Genetics
    ISSN: 00278424
    E-ISSN: 1091-6490
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  • 2
    In: Nature, 2011, Vol.471(7340), p.602
    Description: CRISPR/Cas systems constitute a widespread class of immunity systems that protect bacteria and archaea against phages and plasmids, and commonly use repeat/spacer-derived short crRNAs to silence foreign nucleic acids in a sequence-specific manner. Although the maturation of crRNAs represents a key event in CRISPR activation, the responsible endoribonucleases (CasE, Cas6, Csy4) are missing in many CRISPR/Cas subtypes. Here, differential RNA sequencing of the human pathogen Streptococcus pyogenes uncovered tracrRNA, a trans -encoded small RNA with 24 nucleotide complementarity to the repeat regions of crRNA precursor transcripts. We show that tracrRNA directs the maturation of crRNAs by the activities of the widely conserved endogenous RNase III and the CRISPR-associated Csn1 protein; all these components are essential to protect S. pyogenes against prophage-derived DNA. Our study reveals a novel pathway of small guide RNA maturation and the first example of a host factor (RNase III) required for bacterial RNA-mediated immunity against invaders.
    Keywords: Article;
    ISSN: 0028-0836
    E-ISSN: 14764687
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  • 3
    In: Molecular Microbiology, April 2012, Vol.84(1), pp.1-5
    Description: The transcription factor CsgD governing the production of curli fimbriae and cellulose is a key player in the complex regulatory circuit that decides whether form biofilms. The gene itself is tightly controlled at the level of transcription by a large array of DNA‐binding proteins, but what happens after transcription is less understood. In this issue of , Jørgensen (2012), Mika (2012) and Thomason (2012) report on small RNAs (McaS, RprA and GcvB) that together with the RNA‐chaperone Hfq regulate the mRNAs of and other biofilm genes, and illustrate the burgeoning concept that the 5′ region of bacterial mRNA serves as a hub for sRNA‐mediated signal integration at the post‐transcriptional level.
    Keywords: Transcription (Genetics) ; Proteins ; Messenger Rna ; Genes ; Cellulose;
    ISSN: 0950-382X
    E-ISSN: 1365-2958
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  • 4
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 2012, Vol.109(12), pp.4621-4626
    Description: The conserved RNA-binding protein Hfq and its associated small regulatory RNAs (sRNAs) are increasingly recognized as the players of a large network of posttranscriptional control of gene expression in Gram-negative bacteria. The role of Hfq in this network is to facilitate base pairing between sRNAs and their trans-encoded target mRNAs. Although the number of known sRNA–mRNA interactions has grown steadily, cellular factors that influence Hfq, the mediator of these interactions, have remained unknown. We report that RelA, a protein long known as the central regulator of the bacterial-stringent response, acts on Hfq and thereby affects the physiological activity of RyhB sRNA as a regulator of iron homeostasis. RyhB requires RelA in vivo to arrest growth during iron depletion and to down-regulate a subset of its target mRNAs (fdoG, nuoA, and sodA), whereas the sodB and sdhC targets are barely affected by RelA. In vitro studies with recombinant proteins show that RelA enhances multimerization of Hfq monomers and stimulates Hfq binding of RyhB and other sRNAs. Hfq from polysomes extracted from wild-type cells binds RyhB in vitro, whereas Hfq from polysomes of a relA mutant strain shows no binding. We propose that, by increasing the level of the hexameric form of Hfq, RelA enables binding of RNAs whose affinity for Hfq is low. Our results suggest that, under specific conditions and/or environments, Hfq concentrations are limiting for RNA binding, which thereby provides an opportunity for cellular proteins such as RelA to impact sRNA-mediated responses by modulating the activity of Hfq. ; p. 4621-4626.
    Keywords: Polyribosomes ; In Vitro Studies ; Messenger Rna ; Gram-Negative Bacteria ; Gene Expression ; Recombinant Proteins
    ISSN: 0027-8424
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  • 5
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 27 June 2017, Vol.114(26), pp.6824-6829
    Description: The functions of many bacterial RNA-binding proteins remain obscure because of a lack of knowledge of their cellular ligands. Although well-studied cold-shock protein A (CspA) family members are induced and function at low temperature, others are highly expressed in infection-relevant conditions. Here, we have profiled transcripts bound in vivo by the CspA family members of serovar Typhimurium to link the constitutively expressed CspC and CspE proteins with virulence pathways. Phenotypic assays in vitro demonstrated a crucial role for these proteins in membrane stress, motility, and biofilm formation. Moreover, double deletion of and fully attenuates in systemic mouse infection. In other words, the RNA ligand-centric approach taken here overcomes a problematic molecular redundancy of CspC and CspE that likely explains why these proteins have evaded selection in previous virulence factor screens in animals. Our results highlight RNA-binding proteins as regulators of pathogenicity and potential targets of antimicrobial therapy. They also suggest that globally acting RNA-binding proteins are more common in bacteria than currently appreciated.
    Keywords: RNA-Binding Protein ; Salmonella ; Bacterial Pathogenesis ; Cold-Shock Protein ; Stress Response ; Bacterial Proteins ; Cold Shock Proteins and Peptides ; Heat-Shock Proteins ; RNA-Binding Proteins ; Salmonella Infections ; Salmonella Typhimurium ; Virulence Factors
    ISSN: 00278424
    E-ISSN: 1091-6490
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  • 6
    In: Molecular Microbiology, December 2010, Vol.78(6), pp.1327-1331
    Description: Although most bacterial small RNAs act to repress target mRNAs, some also activate messengers. The predominant mode of activation has been seen in ‘anti‐antisense’ regulation whereby a small RNA prevents the formation of an inhibitory 5′ mRNA structure that otherwise impairs translational initiation and protein synthesis. The translational activation might also stabilize the target yet this was considered a secondary effect in the examples known thus far. Two recent papers in investigate post‐transcriptional activation of collagenase mRNA by VR‐RNA, and streptokinase mRNA by FasX RNA, to suggest that small RNAs exert positive regulation of virulence genes primarily at the level of mRNA stabilization.
    Keywords: Protein Synthesis ; Messenger Rna;
    ISSN: 0950-382X
    E-ISSN: 1365-2958
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  • 7
    Language: English
    In: PLoS ONE, 2011, Vol.6(3), p.e17296
    Description: P-bodies are dynamic aggregates of RNA and proteins involved in several post-transcriptional regulation processes. P-bodies have been shown to play important roles in regulating viral infection, whereas their interplay with bacterial pathogens, specifically intracellular bacteria that extensively manipulate host cell pathways, remains unknown. Here, we report that Salmonella infection induces P-body disassembly in a cell type-specific manner, and independently of previously characterized pathways such as inhibition of host cell RNA synthesis or microRNA-mediated gene silencing. We show that the Salmonella -induced P-body disassembly depends on the activation of the SPI-2 encoded type 3 secretion system, and that the secreted effector protein SpvB plays a major role in this process. P-body disruption is also induced by the related pathogen, Shigella flexneri , arguing that this might be a new mechanism by which intracellular bacterial pathogens subvert host cell function.
    Keywords: Research Article ; Biology ; Medicine ; Infectious Diseases ; Microbiology ; Molecular Biology ; Cell Biology
    E-ISSN: 1932-6203
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  • 8
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 23 November 2010, Vol.107(47), pp.20435-40
    Description: The abundant class of bacterial Hfq-associated small regulatory RNAs (sRNAs) parallels animal microRNAs in their ability to control multiple genes at the posttranscriptional level by short and imperfect base pairing. In contrast to the universal length and seed pairing mechanism of microRNAs, the sRNAs are heterogeneous in size and structure, and how they regulate multiple targets is not well understood. This paper provides evidence that a 5' located sRNA domain is a critical element for the control of a large posttranscriptional regulon. We show that the conserved 5' end of RybB sRNA recognizes multiple mRNAs of Salmonella outer membrane proteins by ≥7-bp Watson-Crick pairing. When fused to an unrelated sRNA, the 5' domain is sufficient to guide target mRNA degradation and maintain σ(E)-dependent envelope homeostasis. RybB sites in mRNAs are often conserved and flanked by 3' adenosine. They are found in a wide sequence window ranging from the upstream untranslated region to the deep coding sequence, indicating that some targets might be repressed at the level of translation, whereas others are repressed primarily by mRNA destabilization. Autonomous 5' domains seem more common in sRNAs than appreciated and might improve the design of synthetic RNA regulators.
    Keywords: Bacterial Outer Membrane Proteins -- Metabolism ; Gene Expression Regulation, Bacterial -- Genetics ; RNA, Messenger -- Metabolism ; Regulatory Sequences, Ribonucleic Acid -- Genetics ; Regulon -- Genetics ; Salmonella -- Genetics
    ISSN: 00278424
    E-ISSN: 1091-6490
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  • 9
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 11 October 2016, Vol.113(41), pp.11591-11596
    Description: The functional annotation of transcriptomes and identification of noncoding RNA (ncRNA) classes has been greatly facilitated by the advent of next-generation RNA sequencing which, by reading the nucleotide order of transcripts, theoretically allows the rapid profiling of all transcripts in a cell. However, primary sequence per se is a poor predictor of function, as ncRNAs dramatically vary in length and structure and often lack identifiable motifs. Therefore, to visualize an informative RNA landscape of organisms with potentially new RNA biology that are emerging from microbiome and environmental studies requires the use of more functionally relevant criteria. One such criterion is the association of RNAs with functionally important cognate RNA-binding proteins. Here we analyze the full ensemble of cellular RNAs using gradient profiling by sequencing (Grad-seq) in the bacterial pathogen Salmonella enterica, partitioning its coding and noncoding transcripts based on their network of RNA-protein interactions. In addition to capturing established RNA classes based on their biochemical profiles, the Grad-seq approach enabled the discovery of an overlooked large collective of structured small RNAs that form stable complexes with the conserved protein ProQ. We show that ProQ is an abundant RNA-binding protein with a wide range of ligands and a global influence on Salmonella gene expression. Given its generic ability to chart a functional RNA landscape irrespective of transcript length and sequence diversity, Grad-seq promises to define functional RNA classes and major RNA-binding proteins in both model species and genetically intractable organisms.
    Keywords: Hfq ; Proq ; RNA–Protein Interaction ; Noncoding RNA ; Small RNA ; Bacterial Proteins -- Metabolism ; High-Throughput Nucleotide Sequencing -- Methods ; RNA, Bacterial -- Metabolism ; RNA-Binding Proteins -- Metabolism ; Salmonella Enterica -- Metabolism
    ISSN: 00278424
    E-ISSN: 1091-6490
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  • 10
    Language: English
    In: Proceedings of the National Academy of Sciences of the United States of America, 10 September 2013, Vol.110(37), pp.E3487-96
    Description: Small RNAs (sRNAs) constitute a large and heterogeneous class of bacterial gene expression regulators. Much like eukaryotic microRNAs, these sRNAs typically target multiple mRNAs through short seed pairing, thereby acting as global posttranscriptional regulators. In some bacteria, evidence for hundreds to possibly more than 1,000 different sRNAs has been obtained by transcriptome sequencing. However, the experimental identification of possible targets and, therefore, their confirmation as functional regulators of gene expression has remained laborious. Here, we present a strategy that integrates phylogenetic information to predict sRNA targets at the genomic scale and reconstructs regulatory networks upon functional enrichment and network analysis (CopraRNA, for Comparative Prediction Algorithm for sRNA Targets). Furthermore, CopraRNA precisely predicts the sRNA domains for target recognition and interaction. When applied to several model sRNAs, CopraRNA revealed additional targets and functions for the sRNAs CyaR, FnrS, RybB, RyhB, SgrS, and Spot42. Moreover, the mRNAs gdhA, lrp, marA, nagZ, ptsI, sdhA, and yobF-cspC were suggested as regulatory hubs targeted by up to seven different sRNAs. The verification of many previously undetected targets by CopraRNA, even for extensively investigated sRNAs, demonstrates its advantages and shows that CopraRNA-based analyses can compete with experimental target prediction approaches. A Web interface allows high-confidence target prediction and efficient classification of bacterial sRNAs.
    Keywords: E. Coli ; RNA–RNA Interaction ; Regulatory RNA ; RNA, Bacterial -- Genetics
    ISSN: 00278424
    E-ISSN: 1091-6490
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