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Pervasive transcription: detecting functional RNAs in bacteria.

Lybecker M, Bilusic I, Raghavan R - Transcription (2014)

Bottom Line: Pervasive, or genome-wide, transcription has been reported in all domains of life.Initially considered to be non-functional transcriptional noise, pervasive transcription is increasingly being recognized as important in regulating gene expression.The function of pervasive transcription is an extensively debated question in the field of transcriptomics and regulatory RNA biology.

View Article: PubMed Central - PubMed

Affiliation: a Department of Biochemistry and Cell Biology ; Max F Perutz Laboratories; University of Vienna ; Vienna, Austria.

ABSTRACT
Pervasive, or genome-wide, transcription has been reported in all domains of life. In bacteria, most pervasive transcription occurs antisense to protein-coding transcripts, although recently a new class of pervasive RNAs was identified that originates from within annotated genes. Initially considered to be non-functional transcriptional noise, pervasive transcription is increasingly being recognized as important in regulating gene expression. The function of pervasive transcription is an extensively debated question in the field of transcriptomics and regulatory RNA biology. Here, we highlight the most recent contributions addressing the purpose of pervasive transcription in bacteria and discuss their implications.

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Mechanisms of dsRNA-mediated gene regulation. (A) dsRNA-mediated translation inhibition. An asRNA that overlaps the RBS of its cognate mRNA could prevent the ribosome from binding the RBS and inhibit translation; the dsRNA would then be degraded by RNase III, but the translational regulation would not be dependent on RNase III. (B) dsRNA-mediated translation stimulation. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. (C) dsRNA-mediated transcription attenuation. dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III.
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f0001: Mechanisms of dsRNA-mediated gene regulation. (A) dsRNA-mediated translation inhibition. An asRNA that overlaps the RBS of its cognate mRNA could prevent the ribosome from binding the RBS and inhibit translation; the dsRNA would then be degraded by RNase III, but the translational regulation would not be dependent on RNase III. (B) dsRNA-mediated translation stimulation. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. (C) dsRNA-mediated transcription attenuation. dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III.

Mentions: All known mechanisms of asRNA-mediated regulation, except transcription interference, require that an asRNA interacts with the complementary sense RNA (forming double-stranded RNA). Most asRNA-mediated gene regulation mechanisms requiring an RNA/RNA interaction affect the stability and/or translation efficiency or attenuate transcription of the mRNA. RNase III can cleave dsRNA resulting in either the destabilization or stabilization of one or both transcripts. In this mechanism, RNase III plays a direct role in the regulation of gene expression via dsRNAs, as proposed for several Gram-positive bacteria.20,24 Alternatively, the formation of the dsRNA itself may regulate gene expression and the dsRNA (subsequently degraded by RNase III) would be a byproduct of the regulation. In this mechanism, gene regulation is independent of RNase III, but the resulting dsRNA levels are RNase III-dependent (Fig. 1). Specifically, an asRNA that overlaps the ribosome-binding site (RBS) of its cognate mRNA could prevent the ribosome from binding and inhibit translation; subsequently the dsRNA would be degraded by RNase III, but the translational regulation would not be RNase III-dependent. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. Finally, dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III. The dsRNA-mediated gene regulation mechanism is supported by the observation in E. coli that the regions of RNAs that are double-stranded are the most stable fragments.21 There are many factors that may influence the pairing of 2 transcripts, including transcript abundance, RNA structure, and the presence of ribosomes or proteins on the transcripts. An RNA chaperone likely aids in the restructuring and annealing of the complementary RNAs. One candidate is the RNA chaperone Hfq. Notably, forty-eight of the transcripts found in dsRNA duplexes were also co-immunoprecipitated with Hfq.7,21 These data suggest that Hfq may play a role in the annealing of antisense and sense RNAs in the cell.Figure 1.


Pervasive transcription: detecting functional RNAs in bacteria.

Lybecker M, Bilusic I, Raghavan R - Transcription (2014)

Mechanisms of dsRNA-mediated gene regulation. (A) dsRNA-mediated translation inhibition. An asRNA that overlaps the RBS of its cognate mRNA could prevent the ribosome from binding the RBS and inhibit translation; the dsRNA would then be degraded by RNase III, but the translational regulation would not be dependent on RNase III. (B) dsRNA-mediated translation stimulation. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. (C) dsRNA-mediated transcription attenuation. dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581347&req=5

f0001: Mechanisms of dsRNA-mediated gene regulation. (A) dsRNA-mediated translation inhibition. An asRNA that overlaps the RBS of its cognate mRNA could prevent the ribosome from binding the RBS and inhibit translation; the dsRNA would then be degraded by RNase III, but the translational regulation would not be dependent on RNase III. (B) dsRNA-mediated translation stimulation. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. (C) dsRNA-mediated transcription attenuation. dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III.
Mentions: All known mechanisms of asRNA-mediated regulation, except transcription interference, require that an asRNA interacts with the complementary sense RNA (forming double-stranded RNA). Most asRNA-mediated gene regulation mechanisms requiring an RNA/RNA interaction affect the stability and/or translation efficiency or attenuate transcription of the mRNA. RNase III can cleave dsRNA resulting in either the destabilization or stabilization of one or both transcripts. In this mechanism, RNase III plays a direct role in the regulation of gene expression via dsRNAs, as proposed for several Gram-positive bacteria.20,24 Alternatively, the formation of the dsRNA itself may regulate gene expression and the dsRNA (subsequently degraded by RNase III) would be a byproduct of the regulation. In this mechanism, gene regulation is independent of RNase III, but the resulting dsRNA levels are RNase III-dependent (Fig. 1). Specifically, an asRNA that overlaps the ribosome-binding site (RBS) of its cognate mRNA could prevent the ribosome from binding and inhibit translation; subsequently the dsRNA would be degraded by RNase III, but the translational regulation would not be RNase III-dependent. Translation could also be stimulated by dsRNA formation by releasing the RBS for ribosome binding. Finally, dsRNA formation could cause transcriptional attenuation and termination, also resulting in a dsRNA byproduct, which would be degraded by RNase III. The dsRNA-mediated gene regulation mechanism is supported by the observation in E. coli that the regions of RNAs that are double-stranded are the most stable fragments.21 There are many factors that may influence the pairing of 2 transcripts, including transcript abundance, RNA structure, and the presence of ribosomes or proteins on the transcripts. An RNA chaperone likely aids in the restructuring and annealing of the complementary RNAs. One candidate is the RNA chaperone Hfq. Notably, forty-eight of the transcripts found in dsRNA duplexes were also co-immunoprecipitated with Hfq.7,21 These data suggest that Hfq may play a role in the annealing of antisense and sense RNAs in the cell.Figure 1.

Bottom Line: Pervasive, or genome-wide, transcription has been reported in all domains of life.Initially considered to be non-functional transcriptional noise, pervasive transcription is increasingly being recognized as important in regulating gene expression.The function of pervasive transcription is an extensively debated question in the field of transcriptomics and regulatory RNA biology.

View Article: PubMed Central - PubMed

Affiliation: a Department of Biochemistry and Cell Biology ; Max F Perutz Laboratories; University of Vienna ; Vienna, Austria.

ABSTRACT
Pervasive, or genome-wide, transcription has been reported in all domains of life. In bacteria, most pervasive transcription occurs antisense to protein-coding transcripts, although recently a new class of pervasive RNAs was identified that originates from within annotated genes. Initially considered to be non-functional transcriptional noise, pervasive transcription is increasingly being recognized as important in regulating gene expression. The function of pervasive transcription is an extensively debated question in the field of transcriptomics and regulatory RNA biology. Here, we highlight the most recent contributions addressing the purpose of pervasive transcription in bacteria and discuss their implications.

Show MeSH