Transcription termination controls prophage maintenance in
            <i>Escherichia coli</i>
            genomes

Menouni, Rachid; Champ, Stéphanie; Espinosa, Léon; Boudvillain, Marc; Ansaldi, Mireille

doi:10.1073/pnas.1303400110

Cited by 43 publications

(50 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For example, in E. coli, the Rho-specific terminator t imm blocks induction of toxin genes from the rac prophage (Cardinale et al, 2008). Rho has been also shown to control the lysogenic state of E. coli prophage KplE1 by inhibiting the expression of the torI gene that mediates excisive recombination (Menouni et al, 2013). A second hypothesis implies that codon usage in foreign DNA could inhibit translation and thus expose rut sequences, which are Rho targets.…”

Section: Limitation Of Deleterious Foreign Dna Expressionmentioning

confidence: 99%

“…coli Rho is known to be involved in the control of a variety of important biological processes, including (i) enforcement of transcription-translation coupling and termination of transcription of untranslated mRNAs (well known also as a phenomenon of Rho-dependent transcriptional polarity) (reviewed by Ciampi, 2006;Peters et al, 2011); (ii) suppression of pervasive antisense transcription (Peters et al, 2012); (iii) assistance in preventing deleterious R-loops (Harinarayanan & Gowrishankar, 2003;Leela et al, 2013) and maintenance of genome integrity by prevention of conflicts between transcription and replication machineries (Dutta et al, 2011;Washburn & Gottesman, 2011); (iv) silencing of horizontally transferred DNA (Cardinale et al, 2008;Menouni et al, 2013); and (v) regulation of gene expression mediated by small regulatory RNAs (sRNA) and riboswitches (Bossi et al, 2012;Hollands et al, 2012;Proshkin et al, 2014). Thus, Rho-dependent transcription termination plays an important role in linking transcription to other vital cellular processes.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

et al. 2016

View full text Add to dashboard Cite

Factor-dependent termination of transcription in bacteria relies on the activity of a specific RNA helicase, the termination factor Rho. Rho is nearly ubiquitous in bacteria, but the extent to which its physiological functions are conserved throughout the different phyla remains unknown. Most of our current knowledge concerning the mechanism of Rho's activity and its physiological roles comes from the model micro-organism Escherichia coli, where Rho is essential and involved in the control of several important biological processes. However, the rather comprehensive knowledge about the general mechanisms of action and activities of Rho based on the E. coli paradigm cannot be directly extrapolated to other bacteria. Recent studies performed in different species favour the view that Rho-dependent termination plays a significant role even in bacteria where Rho is not essential. Here, we summarize the current state of the ever-increasing knowledge about the various aspects of the physiological functions of Rho, such as limitation of deleterious foreign DNA expression, control of gene expression, suppression of pervasive transcription, prevention of R-loops and maintenance of chromosome integrity, focusing on similarities and differences of the activities of Rho in various bacterial species. Introduction Transcription termination is a critical step in gene regulation in all living organisms. In bacteria, transcription termination is well known to be essential for the generation of different types of functional RNAs, the definition of the boundaries of the transcriptional units, the release of RNA polymerase (RNAP) and the regulation of gene expression via the mechanism known as transcription attenuation (Peters et al., 2011;Santangelo & Artsimovitch, 2011).However, recent studies have revealed new roles of transcriptional termination, e.g. those linked to the maintenance of genome integrity or degradation of untranslated mRNAs. Particular attention is now paid to transcription termination due to its crucial role in the control of pervasive transcription. This type of genome-wide transcription, not associated with annotated genome features such as protein-coding genes, is a universal phenomenon for all the three domains of life and viruses (Georg & Hess, 2011;Wade & Grainger, 2014). In eukaryotes, pervasive transcription arises mainly from bidirectional promoters that synthesize both mRNA and diverse non-coding RNAs, but this phenomenon is also controlled by selective transcriptional termination (Kapranov et al., 2007;Schulz et al., 2013). Recently, an essential role of transcription termination in the control of pervasive transcription was demonstrated for both Gram-positive and Gram-negative model micro-organisms Bacillus subtilis and Escherichia coli (Nicolas et al., 2012;Peters et al., 2012).In bacteria, transcription termination is achieved by two mechanisms: factor-independent (intrinsic) and factordependent termination. Intrinsic termination is strongly associated with sequence-specific signals characterized by ...

show abstract

Section: Limitation Of Deleterious Foreign Dna Expressionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

et al. 2016

View full text Add to dashboard Cite

show abstract

“…The best characterized physiological functions that are influenced by the Rho-dependent termination are as follows: (i) prophage gene silencing (6) and maintaining their lysogenic states (33), (ii) regulation of small RNA expression (34), and (iii) riboswitch formations (8). We probed the up-regulation status of the genes involved in these functions in both the NusA and Rho mutants.…”

Section: Nusa Binding To Nut Site(s) Delays the Loading Of Rho At Thementioning

confidence: 99%

Transcription Elongation Factor NusA Is a General Antagonist of Rho-dependent Termination in Escherichia coli

Qayyum

Dey

Sen

2016

Journal of Biological Chemistry

View full text Add to dashboard Cite

NusA is an essential protein that binds to RNA polymerase and also to the nascent RNA and influences transcription by inducing pausing and facilitating the process of transcription termination/antitermination. Its participation in Rho-dependent transcription termination has been perceived, but the molecular nature of this involvement is not known. We hypothesized that, because both Rho and NusA are RNA-binding proteins and have the potential to target the same RNA, the latter is likely to influence the global pattern of the Rho-dependent termination. Analyses of the nascent RNA binding properties and consequent effects on the Rho-dependent termination functions of specific NusA-RNA binding domain mutants revealed an existence of Rho-NusA direct competition for the overlapping nut (NusA-binding site) and rut (Rho-binding site) sites on the RNA. This leads to delayed entry of Rho at the rut site that inhibits the latter's RNA release process. High density tiling microarray profiles of these NusA mutants revealed that a significant number of genes, together with transcripts from intergenic regions, are up-regulated. Interestingly, the majority of these genes were also up-regulated when the Rho function was compromised. These results provide strong evidence for the existence of NusA-binding sites in different operons that are also the targets of Rho-dependent terminations. Our data strongly argue in favor of a direct competition between NusA and Rho for the access of specific sites on the nascent transcripts in different parts of the genome. We propose that this competition enables NusA to function as a global antagonist of the Rho function, which is unlike its role as a facilitator of hairpin-dependent termination.The bacterial transcription terminator, Rho, functions as a hexameric RNA-dependent ATPase that is capable of translocating along the RNA. It dislodges the elongating RNA polymerase (RNAP) 4 once it is loaded onto the nascent RNA (1, 2). Its termination function is facilitated upon interaction with the transcription elongation factor, NusG (3-5). Recent genomics studies have revealed that Rho-dependent termination occurs at more than one-third of the operons of a dividing Escherichia coli (6, 7). This mode of transcription termination is involved in many physiological processes, like control of translation (2), riboswitch formation (8), inhibition of unwanted antisense transcription, etc. (7). Rho is capable of loading onto unstructured stretches of RNA (the rut ([R]ho [ut]ilization) sites), and once it is bound to the RNA, it translocates in a processive manner along the 5Јto 3Ј direction, which may induce unwanted termination of transcription. Interestingly, in vivo negative regulation by cellular factors or any control switch of the Rho function has not been documented. In principle, any RNA-binding protein that has overlapping binding sites with the rut sites on the nascent RNA could influence the Rho activity by a direct competition for occupancy of the same sites.NusA, a ubiquitous transcription elo...

show abstract

“…Two well-studied transcription bacterial termination factors, Rho and Mfd (13,(146)(147)(148)(149)(150), lack clear homologues in archaeal genomes, but there are hints that analogous activities may be present in archaeal species. Rho is a homohexamer helicase that represses phage transcription and mediates polar repression of downstream genes when transcription and translation become uncoupled (142,(151)(152)(153). Archaea demonstrate polar repression of downstream genes in the absence of continued translation, and it is likely that a factor or factors mediate polarity in archaea (115).…”

Section: Identification Of Factor-dependent Terminationmentioning

confidence: 99%

Transcription Regulation in Archaea

2016

View full text Add to dashboard Cite

The known diversity of metabolic strategies and physiological adaptations of archaeal species to extreme environments is extraordinary. Accurate and responsive mechanisms to ensure that gene expression patterns match the needs of the cell necessitate regulatory strategies that control the activities and output of the archaeal transcription apparatus. Archaea are reliant on a single RNA polymerase for all transcription, and many of the known regulatory mechanisms employed for archaeal transcription mimic strategies also employed for eukaryotic and bacterial species. Novel mechanisms of transcription regulation have become apparent by increasingly sophisticated in vivo and in vitro investigations of archaeal species. This review emphasizes recent progress in understanding archaeal transcription regulatory mechanisms and highlights insights gained from studies of the influence of archaeal chromatin on transcription. RNA polymerase (RNAP) is a well-conserved, multisubunit essential enzyme that transcribes DNA to generate RNA in all cells. Although RNA synthesis is carried out by RNAP, the activities of RNAP during each phase of transcription are subject to basal and regulatory transcription factors. Substantial differences in transcription regulatory strategies exist in the three domains (Bacteria, Archaea, and Eukarya). Only a single transcription factor (NusG or Spt5) is universally conserved (1, 2), and the roles of many archaeon-encoded factors have not been evaluated using in vivo and in vitro techniques. Archaea are reliant on a transcription apparatus that is homologous to the eukaryotic transcription machinery; similarities include additional RNAP subunits that form a discrete subdomain of RNAP (3, 4) as well as basal transcription factors that direct transcription initiation and elongation (5-8).The shared homology of archaeal-eukaryotic transcription components aligns with the shared ancestry of Archaea and Eukarya, and this homology often is exclusive of Bacteria. Archaea are prokaryotic, but the transcription apparatus of Bacteria differs significantly from that of Archaea and Eukarya.The archaeal transcription apparatus is most commonly summarized as a simplified version of the eukaryotic machinery. In some respects this is true, as homologs of only a few eukaryotic transcription factors are encoded in archaeal genomes, and archaeal transcription in vitro can be supported by just a few transcription factors. However, much regulatory activity in eukaryotes is devoted to posttranslational modifications of chromatin, RNAP, and transcription factors, and this complexity seemingly does not transfer to the Archaea, where few posttranslational modifications or chromatin-imposed regulation events are currently known. The ostensible simplicity of archaeal transcription is under constant revision, as more detailed examinations of archaeon-encoded factors become possible through increasingly sophisticated in vivo and in vitro techniques. This review will highlight the current understanding of archaeal transcriptio...

show abstract

Transcription termination controls prophage maintenance in Escherichia coli genomes

Cited by 43 publications

References 48 publications

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

Transcription Elongation Factor NusA Is a General Antagonist of Rho-dependent Termination in Escherichia coli

Transcription Regulation in Archaea

Contact Info

Product

Resources

About