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RNA Degradation in Staphylococcus aureus: Diversity of Ribonucleases and Their Impact.

Bonnin RA, Bouloc P - Int J Genomics (2015)

Bottom Line: Based on identified RNases in these two models, putative orthologs have been identified in S. aureus.The main staphylococcal RNases involved in the processing and degradation of the bulk RNA are (i) endonucleases RNase III and RNase Y and (ii) exonucleases RNase J1/J2 and PNPase, having 5' to 3' and 3' to 5' activities, respectively.The diversity and potential roles of each RNase and of Hfq and RppH are discussed in the context of recent studies, some of which are based on next-generation sequencing technology.

View Article: PubMed Central - PubMed

Affiliation: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, 91400 Orsay, France.

ABSTRACT
The regulation of RNA decay is now widely recognized as having a central role in bacterial adaption to environmental stress. Here we present an overview on the diversity of ribonucleases (RNases) and their impact at the posttranscriptional level in the human pathogen Staphylococcus aureus. RNases in prokaryotes have been mainly studied in the two model organisms Escherichia coli and Bacillus subtilis. Based on identified RNases in these two models, putative orthologs have been identified in S. aureus. The main staphylococcal RNases involved in the processing and degradation of the bulk RNA are (i) endonucleases RNase III and RNase Y and (ii) exonucleases RNase J1/J2 and PNPase, having 5' to 3' and 3' to 5' activities, respectively. The diversity and potential roles of each RNase and of Hfq and RppH are discussed in the context of recent studies, some of which are based on next-generation sequencing technology.

No MeSH data available.


Related in: MedlinePlus

Examples of RNase III functions (a) Schematic view of S. aureus RNAIII structure. RNAIII is involved in the regulation of virulence genes by base-pairing with specific mRNAs [57]. (b) The region of coa mRNA (encoding coagulase) close to its Shine-Dalgarno sequence base-pairs with the RNAIII helix H13 and is stabilized by a second interaction involving the RNAIII helixH7. RNase III degrades the coa mRNA-RNAIII duplex, both in the SD region and within the loop-loop interaction region. (c) RNase III degrades ds-RNAs including sense-antisense RNA duplexes as exemplified by type I toxin-antitoxin systems [16]. (d) Cleavage inside a stem-loop can give rise to a more stable mRNA, as demonstrated for the cold shock protein A cspA mRNA. Cleavage of the stem-loop releases the translation start codon and a new stem-loop protects the 5′ end from RNase J-mediated degradation [24].
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fig2: Examples of RNase III functions (a) Schematic view of S. aureus RNAIII structure. RNAIII is involved in the regulation of virulence genes by base-pairing with specific mRNAs [57]. (b) The region of coa mRNA (encoding coagulase) close to its Shine-Dalgarno sequence base-pairs with the RNAIII helix H13 and is stabilized by a second interaction involving the RNAIII helixH7. RNase III degrades the coa mRNA-RNAIII duplex, both in the SD region and within the loop-loop interaction region. (c) RNase III degrades ds-RNAs including sense-antisense RNA duplexes as exemplified by type I toxin-antitoxin systems [16]. (d) Cleavage inside a stem-loop can give rise to a more stable mRNA, as demonstrated for the cold shock protein A cspA mRNA. Cleavage of the stem-loop releases the translation start codon and a new stem-loop protects the 5′ end from RNase J-mediated degradation [24].

Mentions: RNase III is the most studied S. aureus RNase; its role was mainly determined through the characterization of virulence genes regulated by the agr system [17–20]. RNAIII, a 514 nucleotide regulatory RNA which base-pairs with numerous targets, is the agr system effector (Figure 2(a)) [20, 21]. The staphylococcal protein A, encoded by the spa gene, inhibits phagocytic engulfment; its mRNA is RNAIII targets. The regulation of spa involves the formation of an RNAIII-spa mRNA duplex that is then degraded by RNase III [18]. Duplex formation is sufficient to prevent translation of spa mRNA; spa mRNA degradation by RNase III contributes to the irreversibility of the process. Other examples where mRNA-RNAIII duplex formation leads to a translational arrest and consequent mRNA degradation include (i) rot mRNA (encoding a regulator of toxins) through imperfect base pairings involving two loop-loop interactions and of (ii) coa mRNA (encoding the staphylococcal coagulase) via the binding of two distant regions of coa mRNA (Figure 2(b)) [17, 22]. Toeprinting and RNase cleavage assays demonstrated that RNase III cleaves at the bottom of a stem loop and also inside loop-loop interactions (Figure 2(b)).


RNA Degradation in Staphylococcus aureus: Diversity of Ribonucleases and Their Impact.

Bonnin RA, Bouloc P - Int J Genomics (2015)

Examples of RNase III functions (a) Schematic view of S. aureus RNAIII structure. RNAIII is involved in the regulation of virulence genes by base-pairing with specific mRNAs [57]. (b) The region of coa mRNA (encoding coagulase) close to its Shine-Dalgarno sequence base-pairs with the RNAIII helix H13 and is stabilized by a second interaction involving the RNAIII helixH7. RNase III degrades the coa mRNA-RNAIII duplex, both in the SD region and within the loop-loop interaction region. (c) RNase III degrades ds-RNAs including sense-antisense RNA duplexes as exemplified by type I toxin-antitoxin systems [16]. (d) Cleavage inside a stem-loop can give rise to a more stable mRNA, as demonstrated for the cold shock protein A cspA mRNA. Cleavage of the stem-loop releases the translation start codon and a new stem-loop protects the 5′ end from RNase J-mediated degradation [24].
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4419217&req=5

fig2: Examples of RNase III functions (a) Schematic view of S. aureus RNAIII structure. RNAIII is involved in the regulation of virulence genes by base-pairing with specific mRNAs [57]. (b) The region of coa mRNA (encoding coagulase) close to its Shine-Dalgarno sequence base-pairs with the RNAIII helix H13 and is stabilized by a second interaction involving the RNAIII helixH7. RNase III degrades the coa mRNA-RNAIII duplex, both in the SD region and within the loop-loop interaction region. (c) RNase III degrades ds-RNAs including sense-antisense RNA duplexes as exemplified by type I toxin-antitoxin systems [16]. (d) Cleavage inside a stem-loop can give rise to a more stable mRNA, as demonstrated for the cold shock protein A cspA mRNA. Cleavage of the stem-loop releases the translation start codon and a new stem-loop protects the 5′ end from RNase J-mediated degradation [24].
Mentions: RNase III is the most studied S. aureus RNase; its role was mainly determined through the characterization of virulence genes regulated by the agr system [17–20]. RNAIII, a 514 nucleotide regulatory RNA which base-pairs with numerous targets, is the agr system effector (Figure 2(a)) [20, 21]. The staphylococcal protein A, encoded by the spa gene, inhibits phagocytic engulfment; its mRNA is RNAIII targets. The regulation of spa involves the formation of an RNAIII-spa mRNA duplex that is then degraded by RNase III [18]. Duplex formation is sufficient to prevent translation of spa mRNA; spa mRNA degradation by RNase III contributes to the irreversibility of the process. Other examples where mRNA-RNAIII duplex formation leads to a translational arrest and consequent mRNA degradation include (i) rot mRNA (encoding a regulator of toxins) through imperfect base pairings involving two loop-loop interactions and of (ii) coa mRNA (encoding the staphylococcal coagulase) via the binding of two distant regions of coa mRNA (Figure 2(b)) [17, 22]. Toeprinting and RNase cleavage assays demonstrated that RNase III cleaves at the bottom of a stem loop and also inside loop-loop interactions (Figure 2(b)).

Bottom Line: Based on identified RNases in these two models, putative orthologs have been identified in S. aureus.The main staphylococcal RNases involved in the processing and degradation of the bulk RNA are (i) endonucleases RNase III and RNase Y and (ii) exonucleases RNase J1/J2 and PNPase, having 5' to 3' and 3' to 5' activities, respectively.The diversity and potential roles of each RNase and of Hfq and RppH are discussed in the context of recent studies, some of which are based on next-generation sequencing technology.

View Article: PubMed Central - PubMed

Affiliation: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, 91400 Orsay, France.

ABSTRACT
The regulation of RNA decay is now widely recognized as having a central role in bacterial adaption to environmental stress. Here we present an overview on the diversity of ribonucleases (RNases) and their impact at the posttranscriptional level in the human pathogen Staphylococcus aureus. RNases in prokaryotes have been mainly studied in the two model organisms Escherichia coli and Bacillus subtilis. Based on identified RNases in these two models, putative orthologs have been identified in S. aureus. The main staphylococcal RNases involved in the processing and degradation of the bulk RNA are (i) endonucleases RNase III and RNase Y and (ii) exonucleases RNase J1/J2 and PNPase, having 5' to 3' and 3' to 5' activities, respectively. The diversity and potential roles of each RNase and of Hfq and RppH are discussed in the context of recent studies, some of which are based on next-generation sequencing technology.

No MeSH data available.


Related in: MedlinePlus