Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes

Nielsen, Jørgen Feldbæk; Luo, Lei; Ebersbach, Tine; Olsen, Anders Steno; Klitgaard, Janne Kudsk; Valentin‐Hansen, Poul; Kallipolitis, Birgitte H.

doi:10.1093/nar/gkp1081

Cited by 125 publications

(164 citation statements)

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“…197 From the 150 putative regulatory RNAs reported thus far, three Hfqinteracting small RNAs (sRNAs) were identified, 198 and one functionally characterized. 199 Three other appear to be required for efficient bacterial growth in macrophages (see intracellular multiplication section) and at least two are involved in virulence in mice. 156,187 Several expression analyses showed an overlap among regulons of key regulatory proteins of L. monocytogenes.…”

Section: O N O T D I S T R I B U T Ementioning

confidence: 99%

The arsenal of virulence factors deployed byListeria monocytogenesto promote its cell infection cycle

et al. 2011

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Section: O N O T D I S T R I B U T Ementioning

confidence: 99%

The arsenal of virulence factors deployed byListeria monocytogenesto promote its cell infection cycle

et al. 2011

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“…An interesting correlation has been emphasized between the number of positively charged amino acids (arginines or lysines) at the rim and the function of Hfq from Gram-positive bacteria in sRNA regulation (Panja et al 2013). Indeed, among the Hfq proteins studied in Gram-positive bacteria, L. monocytogenes Hfq carries the RKEK rim motif and stabilizes at least one sRNA-mRNA complex (Nielsen et al 2010(Nielsen et al , 2011, while B. subtilis Hfq having a RKEN motif associated with numerous RNAs was not required for sRNA regulation (Heidrich et al 2007;Gaballa et al 2008;Dambach et al 2013). The function of S. aureus Hfq carrying the KANQ rim motif remains unclear (Bohn et al 2007).…”

Section: Similarities and Differences Of Ec-hfq And Cd-hfqmentioning

confidence: 99%

“…Although numerous sRNAs have been detected in many Gram-positive bacteria, it is not yet clear whether Hfq is implicated in sRNA network. In Listeria monocytogenes, Hfq has been shown to play a role in stress tolerance and virulence (Christiansen et al 2004) and its inactivation does not generally affect sRNAs abundance, only three sRNAs coimmunoprecipitated with Hfq (Christiansen et al 2006;Mandin et al 2007;ToledoArana et al 2009) with facilitation of LhrA binding to its targets (Nielsen et al 2010(Nielsen et al , 2011. In S. aureus, Hfq is neither required for RNAIII function nor for sRNA stabilization (Boisset et al 2007;Geissmann et al 2009).…”

Section: Introductionmentioning

confidence: 99%

Clostridium difficile Hfq can replace Escherichia coli Hfq for most of its function

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et al. 2014

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A gene for the Hfq protein is present in the majority of sequenced bacterial genomes. Its characteristic hexameric ring-like core structure is formed by the highly conserved N-terminal regions. In contrast, the C-terminal forms an extension, which varies in length, lacks homology, and is predicted to be unstructured. In Gram-negative bacteria, Hfq facilitates the pairing of sRNAs with their mRNA target and thus affects gene expression, either positively or negatively, and modulates sRNA degradation. In Gram-positive bacteria, its role is still poorly characterized. Numerous sRNAs have been detected in many Gram-positive bacteria, but it is not yet known whether these sRNAs act in association with Hfq. Compared with all other Hfqs, the C. difficile Hfq exhibits an unusual C-terminal sequence with 75% asparagine and glutamine residues, while the N-terminal core part is more conserved. To gain insight into the functionality of the C. difficile Hfq (Cd-Hfq) protein in processes regulated by sRNAs, we have tested the ability of Cd-Hfq to fulfill the functions of the E. coli Hfq (Ec-Hfq) by examining various functions associated with Hfq in both positive and negative controls of gene expression. We found that Cd-Hfq substitutes for most but not all of the tested functions of the Ec-Hfq protein. We also investigated the role of the C-terminal part of the Hfq proteins. We found that the C-terminal part of both Ec-Hfq and Cd-Hfq is not essential but contributes to some functions of both the E. coli and C. difficile chaperons.

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“…Cells (OD 600 0.35) were exposed to 4 mg cefuroxime ml 21 , 0.1 mg ampicillin ml 21 , 5 % ethanol, 0.08 % bile salts or 8 % sodium chloride, for 1 h. Unstressed cultures were used as controls. Total RNA was extracted as described previously (Nielsen et al, 2010). Superscript III reverse transcriptase (Invitrogen) was used to synthesize cDNA using DNase-treated total RNA.…”

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Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes

et al. 2012

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The Gram-positive bacterium Listeria monocytogenes is widely distributed in the environment and capable of causing food-borne infections in susceptible individuals. In this study, we investigated the cell envelope stress response in L. monocytogenes. Whole-genome transcriptional profiling was performed to investigate the response upon exposure to the cell wall antibiotic cefuroxime. Differential expression (at least twofold) of 558 genes was observed, corresponding to 20 % of the L. monocytogenes genome. The majority of genes that were strongly induced by cefuroxime exposure have cell-envelope-related functions, including the dlt operon and the gene encoding penicillin-binding protein PBPD2. A large overlap was observed between the cefuroxime stimulon and genes known to be induced in L. monocytogenes in blood and during intracellular infection, indicating that the cell envelope stress response is active at various stages of the infectious process. We analysed the roles of the two-component systems LisRK and CesRK in the cell envelope response, showing that activation of the most highly cefuroxime-induced genes was LisR-and CesR-dependent. In addition, multiple VirRS-and LiaSR-regulated genes were found to be induced in response to cefuroxime exposure. In total, 53 % of the genes upregulated at least fourfold by cefuroxime exposure are under positive control by one of the four two-component systems. Using genetic analyses, we showed that several genes of the cefuroxime stimulon contribute to the innate resistance of L. monocytogenes to cefuroxime and tolerance to other cellenvelope-perturbing conditions. Collectively, these findings demonstrate central roles for twocomponent systems in orchestrating the cell envelope stress response in L. monocytogenes. INTRODUCTIONListeria monocytogenes is a Gram-positive, food-borne intracellular pathogen, causing life-threatening infections in susceptible individuals (Vázquez-Boland et al., 2001). L. monocytogenes is able to survive and propagate within many different environments, including soil, food processing environments, the gastrointestinal tract and the cytosol of mammalian cells. In order to adapt and multiply within such diverse and changing surroundings, L. monocytogenes must continuously monitor and respond to environmental signals by means of complex gene regulatory networks that coordinate the expression of specific sets of genes supporting bacterial survival and growth. The genome of L. monocytogenes encodes 14 two-component signal transduction systems and a single orphan response regulator which are thought to contribute to the coordinated response to various 3Present address: Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, The Netherlands. The microarrays used in this study were generated and designed as described by van der Veen et al. (2010) (GEO Platform no. GPL14687) and the microarray data from this study have been deposited in the GEO database with accession...

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Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes

Cited by 125 publications

References 67 publications

The arsenal of virulence factors deployed byListeria monocytogenesto promote its cell infection cycle

The arsenal of virulence factors deployed byListeria monocytogenesto promote its cell infection cycle

Clostridium difficile Hfq can replace Escherichia coli Hfq for most of its function

Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes

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