Multiple ways to regulate translation initiation in bacteria: Mechanisms, regulatory circuits, dynamics

Duval, Manuel; Simonetti, Angelita; Caldelari, Isabelle; Marzi, Stefano

doi:10.1016/j.biochi.2015.03.007

Cited by 56 publications

(58 citation statements)

References 188 publications

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“…Many bacterial translational regulatory mechanisms have been characterized, some global in action and others narrowly targeted (33)(34)(35). The cases shown in Figs.…”

Section: Discussionmentioning

confidence: 99%

Dynamic translation regulation in Caulobacter cell cycle control

Schrader

Childers

et al. 2016

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

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Progression of the Caulobacter cell cycle requires temporal and spatial control of gene expression, culminating in an asymmetric cell division yielding distinct daughter cells. To explore the contribution of translational control, RNA-seq and ribosome profiling were used to assay global transcription and translation levels of individual genes at six times over the cell cycle. Translational efficiency (TE) was used as a metric for the relative rate of protein production from each mRNA. TE profiles with similar cell cycle patterns were found across multiple clusters of genes, including those in operons or in subsets of operons. Collections of genes associated with central cell cycle functional modules (e.g., biosynthesis of stalk, flagellum, or chemotaxis machinery) have consistent but different TE temporal patterns, independent of their operon organization. Differential translation of operon-encoded genes facilitates precise cell cycle-timing for the dynamic assembly of multiprotein complexes, such as the flagellum and the stalk and the correct positioning of regulatory proteins to specific cell poles. The cell cycleregulatory pathways that produce specific temporal TE patterns are separate from-but highly coordinated with-the transcriptional cell cycle circuitry, suggesting that the scheduling of translational regulation is organized by the same cyclical regulatory circuit that directs the transcriptional control of the Caulobacter cell cycle.T he Caulobacter crescentus cell cycle produces two daughter cell types at each cell division: a nonreplicative motile swarmer cell, and a replication-competent sessile stalked cell. At the time of the asymmetric cell division, each daughter cell activates a different genetic program. Caulobacter has a cyclical genetic circuit that controls the varying temporal and spatial expression of multiple functional modules (Fig. 1) that implement biogenesis of polar organelles, replication and segregation of the chromosome, and cytokinesis (1-4). The circular 4-Mb genome has 3,885 ORFs and 199 noncoding RNAs (5, 6). mRNA profiling by microarrays or RNA-seq (7-10) and global promoter activity profiles from 5′ Global RACE experiments (11) have shown that several hundred Caulobacter mRNAs have significant temporal transcriptional variation over the cell cycle. The expression of cell cycle-controlled mRNAs largely correlates with the times they are required for the functional modules that implement progression of the cell cycle (8). The transcriptional activity of most of the Caulobacter cell cycle-regulated promoters is controlled by a genetic circuit comprised of four transcriptional master regulators, a DNA methyltransferase (2), and a dynamic set of polar-localized phospho-signaling proteins that control asymmetric cell division (12-15). Because regulation of translation has an immediate impact on protein production, a major cellular energy drain, tight regulation of translation is essential for rapid cell adaptation to changing circumstances. In eukaryotic cells translational contr...

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“…Many bacterial translational regulatory mechanisms have been characterized, some global in action and others narrowly targeted (33)(34)(35). The cases shown in Figs.…”

Section: Discussionmentioning

confidence: 99%

Dynamic translation regulation in Caulobacter cell cycle control

Schrader

Childers

et al. 2016

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

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“…In case of sRNA- trans , a single mRNA can be regulated by more than one sRNA (Bardill and Hammer, 2012; Duval et al, 2014; Chang et al, 2015). This type of sRNA has been more widely studied and is the most abundant type of sRNA discovered to date.…”

Section: Classification Of Srnasmentioning

confidence: 99%

“…In this case, Hfq binds with both sRNA- trans and its corresponding mRNA target mediates the interaction (Fröhlich and Vogel, 2009; Feng et al, 2015). This can decrease the constant of apparent dissociation between the sRNA and its target mRNA and stabilize the sRNAs, protecting them from degradation by the RNase E (Bardill and Hammer, 2012; Duval et al, 2014). …”

Section: Classification Of Srnasmentioning

confidence: 99%

Role of Non-coding Regulatory RNA in the Virulence of Human Pathogenic Vibrios

et al. 2017

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In recent decades, the identification of small non-coding RNAs in bacteria has revealed an important regulatory mechanism of gene expression involved in the response to environmental signals and to the control of virulence. In the family Vibrionaceae, which includes several human and animal pathogens, small non-coding RNAs (sRNAs) are closely related to important processes including metabolism, quorum sensing, virulence, and fitness. Studies conducted in silico and experiments using microarrays and high-throughput RNA sequencing have led to the discovery of an unexpected number of sRNAs in Vibrios. The present review discusses the most relevant reports regarding the mechanisms of action of sRNAs and their implications in the virulence of the main human pathogens in the family Vibrionaceae: Vibrio parahaemolyticus, V. vulnificus and V. cholerae.

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“…Developing a precise and predictive understanding of these interactions has become essential to controlling protein expression levels for a wide variety of biotechnological applications (12), including biosensor development (13–15), metabolic pathway engineering (16–24) and genetic circuit engineering (25–27). Within this sequence-function relationship, different portions of the mRNA play distinct roles, though most studies have largely focused on how the bacterial ribosome binding site sequence affects the mRNA's translation rate (2,14,28). Beyond the ribosome binding site, it has been established that a mRNA's protein coding sequence can greatly affect its translation initiation rate (3,7,29), though the biophysical rules that govern the extent of its control remains unpredictable and poorly quantified.…”

Section: Introductionmentioning

confidence: 99%

“…Translation initiation is a rate-limiting step in gene expression whereby the 30S ribosomal subunit binds to a mRNA's standby site, hybridizes to its Shine-Dalgarno sequence (SD), and inserts the coding region into its entry channel to form a 30S initiation complex (30SIC), together with tRNA fMet and initiation factors (2,30,31). Afterward, the 50S ribosomal subunit is recruited to form a 70SIC, GTP is hydrolyzed, and translation elongation begins (32).…”

Section: Introductionmentioning

confidence: 99%

Precise quantification of translation inhibition by mRNA structures that overlap with the ribosomal footprint in N-terminal coding sequences

Borujeni

Cetnar

Farasat

et al. 2017

Nucleic Acids Research

130

138

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A mRNA's translation rate is controlled by several sequence determinants, including the presence of RNA structures within the N-terminal regions of its coding sequences. However, the physical rules that govern when such mRNA structures will inhibit translation remain unclear. Here, we introduced systematically designed RNA hairpins into the N-terminal coding region of a reporter protein with steadily increasing distances from the start codon, followed by characterization of their mRNA and expression levels in Escherichia coli. We found that the mRNAs’ translation rates were repressed, by up to 530-fold, when mRNA structures overlapped with the ribosome's footprint. In contrast, when the mRNA structure was located outside the ribosome's footprint, translation was repressed by <2-fold. By combining our measurements with biophysical modeling, we determined that the ribosomal footprint extends 13 nucleotides into the N-terminal coding region and, when a mRNA structure overlaps or partially overlaps with the ribosomal footprint, the free energy to unfold only the overlapping structure controlled the extent of translation repression. Overall, our results provide precise quantification of the rules governing translation initiation at N-terminal coding regions, improving the predictive design of post-transcriptional regulatory elements that regulate translation rate.

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Multiple ways to regulate translation initiation in bacteria: Mechanisms, regulatory circuits, dynamics

Cited by 56 publications

References 188 publications

Dynamic translation regulation in Caulobacter cell cycle control

Dynamic translation regulation in Caulobacter cell cycle control

Role of Non-coding Regulatory RNA in the Virulence of Human Pathogenic Vibrios

Precise quantification of translation inhibition by mRNA structures that overlap with the ribosomal footprint in N-terminal coding sequences

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