The RNA-Binding Protein Hfq of Listeria monocytogenes: Role in Stress Tolerance and Virulence

ABSTRACT In gram-negative bacteria, the RNA-binding protein Hfq has emerged as an important regulatory factor in a variety of physiological processes, including stress resistance and virulence. In Escherichia coli, Hfq modulates the stability or the translation of mRNAs and interacts with numerous small regulatory RNAs. Here, we studied the role of Hfq in the stress tolerance and virulence of the gram-positive food-borne human pathogen Listeria monocytogenes. We present evidence that Hfq is involved in the ability of L. monocytogenes to tolerate osmotic and ethanol stress and contributes to long-term survival under amino acid-limiting conditions. However, Hfq is not required for resistance to acid and oxidative stress. Transcription of hfq is induced under various stress conditions, including osmotic and ethanol stress and at the entry into the stationary growth phase, thus supporting the view that Hfq is important for the growth and survival of L. monocytogenes in harsh environments. The stress-inducible transcription of hfq depends on the alternative sigma factor σB, which controls the expression of numerous stress- and virulence-associated genes in L. monocytogenes. Infection studies showed that Hfq contributes to pathogenesis in mice, yet plays no role in the infection of cultured cell lines. This study provides, for the first time, information on the role of Hfq in the stress tolerance and virulence of a gram-positive pathogen.

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SpoVG Is a Conserved RNA-Binding Protein That RegulatesListeria monocytogenesLysozyme Resistance, Virulence, and Swarming Motility

mBio ◽

10.1128/mbio.00240-16 ◽

2016 ◽

Vol 7 (2) ◽

Cited By ~ 18

Author(s):

Thomas P. Burke ◽

Daniel A. Portnoy

Keyword(s):

Listeria Monocytogenes ◽

Noncoding Rna ◽

Rna Binding ◽

Methicillin Resistance ◽

Binding Protein ◽

Rna Binding Protein ◽

Gram Positive ◽

Swarming Motility ◽

Bacterial Physiology ◽

Gram Positive Bacteria

ABSTRACTIn this study, we sought to characterize the targets of the abundantListeria monocytogenesnoncoding RNA Rli31, which is required forL. monocytogeneslysozyme resistance and pathogenesis. Whole-genome sequencing of lysozyme-resistant suppressor strains identified loss-of-expression mutations in the promoter ofspoVG, and deletion ofspoVGrescued lysozyme sensitivity and attenuationin vivoof therli31mutant. SpoVG was demonstrated to be an RNA-binding protein that interacted with Rli31in vitro.The relationship between Rli31 and SpoVG is multifaceted, as both thespoVG-encoded protein and thespoVG5′-untranslated region interacted with Rli31. In addition, we observed thatspoVG-deficient bacteria were nonmotile in soft agar and suppressor mutations that restored swarming motility were identified in the gene encoding a major RNase in Gram-positive bacteria, RNase J1. Collectively, these findings suggest that SpoVG is similar to global posttranscriptional regulators, a class of RNA-binding proteins that interact with noncoding RNA, regulate genes in concert with RNases, and control pleiotropic aspects of bacterial physiology.IMPORTANCEspoVGis widely conserved among bacteria; however, the function of this gene has remained unclear since its initial characterization in 1977. Mutation ofspoVGimpacts various phenotypes in Gram-positive bacteria, including methicillin resistance, capsule formation, and enzyme secretion inStaphylococcus aureusand also asymmetric cell division, hemolysin production, and sporulation inBacillus subtilis. Here, we demonstrate thatspoVGmutant strains ofListeria monocytogenesare hyper-lysozyme resistant, hypervirulent, nonmotile, and misregulate genes controlling carbon metabolism. Furthermore, we demonstrate that SpoVG is an RNA-binding protein. These findings suggest that SpoVG has a role inL. monocytogenes, and perhaps in other bacteria, as a global gene regulator. Posttranscriptional gene regulators help bacteria adapt to various environments and coordinate differing aspects of bacterial physiology. SpoVG may help the organism coordinate environmental growth and virulence to survive as a facultative pathogen.

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Critical role of tristetraprolin and AU‐rich element RNA‐binding protein 1 in the suppression of cancer cell growth by globular adiponectin

FEBS Open Bio ◽

10.1002/2211-5463.12541 ◽

2018 ◽

Vol 8 (12) ◽

pp. 1964-1976 ◽

Cited By ~ 1

Author(s):

Nirmala Tilija Pun ◽

Amrita Khakurel ◽

Aastha Shrestha ◽

Sang‐Hyun Kim ◽

Pil‐Hoon Park

Keyword(s):

Cell Growth ◽

Cancer Cell ◽

Rna Binding ◽

Binding Protein ◽

Critical Role ◽

Rna Binding Protein ◽

Cancer Cell Growth ◽

Globular Adiponectin

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The control of inflammation via the phosphorylation and dephosphorylation of tristetraprolin: a tale of two phosphatases

Biochemical Society Transactions ◽

10.1042/bst20160166 ◽

2016 ◽

Vol 44 (5) ◽

pp. 1321-1337 ◽

Cited By ~ 39

Author(s):

Andrew R. Clark ◽

Jonathan L.E. Dean

Keyword(s):

Inflammatory Mediators ◽

Knockout Mouse ◽

Rna Binding ◽

Binding Protein ◽

Rna Binding Protein ◽

Human Orthologue ◽

And Function ◽

Detailed Picture ◽

Lines Of Evidence

Twenty years ago, the first description of a tristetraprolin (TTP) knockout mouse highlighted the fundamental role of TTP in the restraint of inflammation. Since then, work from several groups has generated a detailed picture of the expression and function of TTP. It is a sequence-specific RNA-binding protein that orchestrates the deadenylation and degradation of several mRNAs encoding inflammatory mediators. It is very extensively post-translationally modified, with more than 30 phosphorylations that are supported by at least two independent lines of evidence. The phosphorylation of two particular residues, serines 52 and 178 of mouse TTP (serines 60 and 186 of the human orthologue), has profound effects on the expression, function and localisation of TTP. Here, we discuss the control of TTP biology via its phosphorylation and dephosphorylation, with a particular focus on recent advances and on questions that remain unanswered.

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Role of RNA‐binding protein HuR and CUGBP1 in LPS‐induced Interleukin‐6 Expression in Macrophages

The FASEB Journal ◽

10.1096/fasebj.24.1_supplement.494.7 ◽

2010 ◽

Vol 24 (S1) ◽

Author(s):

Weibin Zha ◽

Guangji Wang ◽

Beth S. Pecora ◽

Elaine Studer ◽

Phillip B Hylemon ◽

...

Keyword(s):

Interleukin 6 ◽

Rna Binding ◽

Binding Protein ◽

Rna Binding Protein

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The role of the RNA-binding protein Sam68 in mammary tumourigenesis

The Journal of Pathology ◽

10.1002/path.2753 ◽

2010 ◽

Vol 222 (3) ◽

pp. 223-226 ◽

Cited By ~ 12

Author(s):

David J Elliott ◽

Prabhakar Rajan

Keyword(s):

Rna Binding ◽

Binding Protein ◽

Rna Binding Protein

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Role of transcription factor Sp1 and RNA binding protein HuR in the downregulation of Dr+Escherichia colireceptor protein decay accelerating factor (DAF or CD55) by nitric oxide

FEBS Journal ◽

10.1111/febs.12073 ◽

2012 ◽

pp. n/a-n/a

Author(s):

Manu Banadakoppa ◽

Daniel Liebenthal ◽

David E. Nowak ◽

Petri Urvil ◽

Uma Yallampalli ◽

...

Keyword(s):

Nitric Oxide ◽

Transcription Factor ◽

Rna Binding ◽

Binding Protein ◽

Rna Binding Protein ◽

Decay Accelerating Factor ◽

Transcription Factor Sp1

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Chitin binding protein as a possible RNA binding protein in Leishmania parasites

Pathogens and Disease ◽

10.1093/femspd/ftaa007 ◽

2020 ◽

Vol 78 (1) ◽

Author(s):

Sajad Rashidi ◽

Kurosh Kalantar ◽

Celia Fernandez-Rubio ◽

Enayat Anvari ◽

Paul Nguewa ◽

...

Keyword(s):

Rna Binding ◽

Binding Protein ◽

Rna Binding Protein ◽

Novel Proteins ◽

Transcriptional Gene Regulation ◽

Chitin Binding Protein ◽

Effective Drugs ◽

Genus Leishmania ◽

Leishmania Parasites

ABSTRACT Leishmaniasis includes a broad spectrum of pathological outcomes in humans caused by protozoan parasites from the genus Leishmania. In recent years, proteomic techniques have introduced novel proteins with critical functions in Leishmania parasites. Based on our report of a Chitin binding protein (CBP) in our previous immunoproteomic study, this article suggests that CBP might be an RNA binding protein (RBP) in Leishmania parasites. RBPs, as key regulatory factors, have a role in post-transcriptional gene regulation. The presence of RBPs in Leishmania parasites has not been considered so far; however, this study aims to open a new venue regarding RBPs in Leishmania parasites. Confirming CBP as an RBP in Leishmania parasites, exploring other RBPs and their functions might lead to interesting issues in leishmaniasis. In fact, due to the regulatory role of RBPs in different diseases including cancers and their further classification as therapeutic targets, the emerging evaluation of CBP and RBPs from Leishmania parasites may allow the discovery of novel and effective drugs against leishmaniasis.

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