Cellular RNA Targets of Cold Shock Proteins CspC and CspE and Their Importance for Serum Resistance in Septicemic Escherichia coli

Yair, Yael; Michaux, Charlotte; Biran, Dvora; Bernhard, Jörg; Vogel, Jörg; Barquist, Lars; Ron, Eliora Z.

doi:10.1128/msystems.00086-22

Cited by 13 publications

(13 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In total, 717 transcripts are bound by at least one CSP, with 430 CspC peaks directly overlapping with a CspE peak ( Fig. 3 B ) supporting the previously reported partial redundancy between these proteins ( 11 ) and similar observations in E. coli ( 44 ). We saw especially dense clusters of CspC/E peaks in transcripts encoding genes involved in the TCA cycle, flagellar proteins, and proteins involved in host invasion associated with the Salmonella pathogenicity island 1 (SPI-1) type three secretion system ( Fig.…”

Section: Resultssupporting

confidence: 85%

Improved RNA stability estimation through Bayesian modeling reveals most Salmonella transcripts have subminute half-lives

Jenniches,

Michaux,

Popella

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

RNA decay is a crucial mechanism for regulating gene expression in response to environmental stresses. In bacteria, RNA-binding proteins (RBPs) are known to be involved in posttranscriptional regulation, but their global impact on RNA half-lives has not been extensively studied. To shed light on the role of the major RBPs ProQ and CspC/E in maintaining RNA stability, we performed RNA sequencing of Salmonella enterica over a time course following treatment with the transcription initiation inhibitor rifampicin (RIF-seq) in the presence and absence of these RBPs. We developed a hierarchical Bayesian model that corrects for confounding factors in rifampicin RNA stability assays and enables us to identify differentially decaying transcripts transcriptome-wide. Our analysis revealed that the median RNA half-life in Salmonella in early stationary phase is less than 1 min, a third of previous estimates. We found that over half of the 500 most long-lived transcripts are bound by at least one major RBP, suggesting a general role for RBPs in shaping the transcriptome. Integrating differential stability estimates with cross-linking and immunoprecipitation followed by RNA sequencing (CLIP-seq) revealed that approximately 30% of transcripts with ProQ binding sites and more than 40% with CspC/E binding sites in coding or 3′ untranslated regions decay differentially in the absence of the respective RBP. Analysis of differentially destabilized transcripts identified a role for ProQ in the oxidative stress response. Our findings provide insights into posttranscriptional regulation by ProQ and CspC/E, and the importance of RBPs in regulating gene expression.

show abstract

Section: Resultssupporting

confidence: 85%

Improved RNA stability estimation through Bayesian modeling reveals most Salmonella transcripts have subminute half-lives

Jenniches,

Michaux,

Popella

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

show abstract

“…Another example of indirect effects on serum resistance is the cold shock proteins (CSPs) CspC and CspE. Both of them play an important role in serum resistance of Septicemic E. coli [ 45 ]. The stability of many transcripts.…”

Section: Discussionmentioning

confidence: 99%

“…including serum survival genes tdcA and clpX , were controlled by CspC and CspE. Interestingly, the transcription of RyhB and Fur were related to both CspC and CspE [ 45 ]. Fur is also a major regulator of ExPEC response to serum [ 46 ].…”

Section: Discussionmentioning

confidence: 99%

RyhB in Avian Pathogenic Escherichia coli Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model

Meng

Chen

Wang

et al. 2022

IJMS

View full text Add to dashboard Cite

Avian pathogenic Escherichia coli (APEC) is an important member of extraintestinal pathogenic Escherichia coli (ExPEC). It shares similar pathogenic strategies with neonatal meningitis E. coli (NMEC) and may threaten human health due to its potential zoonosis. RyhB is a small non-coding RNA that regulates iron homeostasis in E. coli. However, it is unclear whether RyhB regulates meningitis occurrence. To investigate the function of RyhB in the development of meningitis, we constructed the deletion mutant APEC XM∆ryhB and the complemented mutant APEC XM∆ryhB/pryhB, established a mouse meningitis model and evaluated the role of RyhB in virulence of APEC. The results showed that the deletion of ryhB decreased biofilm formation, adhesion to the brain microvascular endothelial cell line bEnd.3 and serum resistance. RNA-seq data showed that the expression of multiple virulence-related genes changed in the ryhB deletion mutant in the presence of duck serum. Deletion of ryhB reduced the clinical symptoms of mice, such as opisthotonus, diarrhea and neurological signs, when challenged with APEC. Compared with the mice infected with the wild-type APEC, fewer histopathological lesions were observed in the brain of mice infected with the ryhB deletion mutant APEC XM∆ryhB. The bacterial loads in the tissues and the relative expression of cytokines (IL-1β, IL-6, and TNF-α) in the brain significantly decreased when challenged with the APEC XM∆ryhB. The expressions of tight junction proteins (claudin-5, occludin and ZO-1) were not reduced in the brain of mice infected with APEC XM∆ryhB; that is, the blood-brain barrier permeability of mice was not significantly damaged. In conclusion, RyhB contributes to the pathogenicity of APEC XM in the meningitis-causing process by promoting biofilm formation, adhesion to endothelial cells, serum resistance and virulence-related genes expression.

show abstract

“…The appearance of the GO term 'response to cold' might be a result of the lack of cold stress in our compendium of stressors. Additionally, it should be noted that genes associated to this GO term include cold shock proteins which may have broader roles in survival of stress conditions, 122,123 as well as several prophage genes and ribosome biogenesis factors. We found that mild acid stress turns on nodes which correspond to gene sets associated with nucleotide and ribosome biosynthesis, including the GO terms 'ribosome large subunit assembly', ribosome small subunit assembly' and 'de novo IMP biosynthetic process', while severe acid stress turns them off (Fig.…”

Section: Differentiation Of the Acid Stress And General Stress Respon...mentioning

confidence: 99%

Ribosome profiling reveals the fine-tuned response ofEscherichia colito mild and severe acid stress

Schumacher

Gelhausen

Kion-Crosby

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

The ability to respond to acidic environments is crucial for neutralophilic bacteria. Escherichia coli has a well-characterized regulatory network that triggers a multitude of defense mechanisms to counteract excess of protons. Nevertheless, systemic studies of the transcriptional and translational reprogramming of E. coli to different degrees of acid stress have not yet been performed. Here, we used ribosome profiling and RNA sequencing to compare the response of E. coli (pH 7.6) to sudden mild (pH 5.8) and severe near-lethal acid stress (pH 4.4) conditions that mimic passage through the gastrointestinal tract. We uncovered new differentially regulated genes and pathways, key transcriptional regulators, and 18 novel acid-induced candidate sORFs. By using machine learning leveraging large compendia of publicly available E. coli expression data, we were able to distinguish between the response to acid stress and general stress. These results expand the acid resistance network and provide new insights into the fine-tuned response of E. coli to mild and severe acid stress.

show abstract

Cellular RNA Targets of Cold Shock Proteins CspC and CspE and Their Importance for Serum Resistance in Septicemic Escherichia coli

Cited by 13 publications

References 57 publications

Improved RNA stability estimation through Bayesian modeling reveals most Salmonella transcripts have subminute half-lives

Improved RNA stability estimation through Bayesian modeling reveals most Salmonella transcripts have subminute half-lives

RyhB in Avian Pathogenic Escherichia coli Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model

Ribosome profiling reveals the fine-tuned response ofEscherichia colito mild and severe acid stress

Contact Info

Product

Resources

About