A Novel RNA Phosphorylation State Enables 5′ End-Dependent Degradation in Escherichia coli

Luciano, Daniel; Vasilyev, Nikita; Richards, Jamie; Serganov, Alexander; Belasco, Joel G.

doi:10.1016/j.molcel.2017.05.035

Cited by 75 publications

(134 citation statements)

References 52 publications

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“…The next study explained some of these observations. This work confirmed that RppH can function on diphosphorylated RNAs in vitro (Luciano, Vasilyev, Richards, Serganov, & Belasco, ) and demonstrated that RppH activity was more than tenfold greater on diphosphorylated RNAs compared to their triphosphorylated counterparts. These data suggested that the diphosphorylated RNAs are the natural substrates of RppH in E. coli .…”

Section: Phosphorylation States Of the 5′‐end Of Bacterial Rnassupporting

confidence: 79%

“…This new method takes advantage of yeast mRNA guanylyltransferase which uses diphosphorylated RNA as a substrate for capping. A combination of PACO and PABLO (Celesnik, Deana, & Belasco, ) made it possible to precisely determine the phosphorylation state for representative E. coli mRNAs (Luciano et al, ). Surprisingly, the triphosphorylated primary transcripts were found to be much less abundant than their di‐ and monophosphorylated counterparts, while rppH knockout resulted in further increase of fraction of diphosphorylated RNAs.…”

Section: Phosphorylation States Of the 5′‐end Of Bacterial Rnasmentioning

confidence: 99%

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Noncanonical features and modifications on the 5′‐end of bacterial sRNAs and mRNAs

2018

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While many eukaryotic transcripts contain cap structures, it has been long thought that bacterial RNAs do not carry any special modifications on their 5′ ends. In bacteria, primary transcripts are produced by transcription initiated with a nucleoside triphosphate and are therefore triphosphorylated on 5′ ends. Some transcripts are then processed by nucleases that yield monophosphorylated RNAs for specific cellular activities. Many primary transcripts are also converted to monophosphorylated species by removal of the terminal pyrophosphate for 5′-end-dependent degradation. Recent studies surprisingly revealed an expanded repertoire of chemical groups on 5′-ends of bacterial RNAs. In addition to mono- and triphosphorylated moieties, some mRNAs and sRNAs contain cap-like structures and diphosphates on their 5′-ends. Although incorporation and removal of these groups have become better understood in recent years, the physiological significance of these modification remain obscure. This review highlights recent studies aimed at identification and elucidation of novel modifications on the 5′ ends of bacterial RNAs and discusses possible physiological applications of the modified RNAs.

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Section: Phosphorylation States Of the 5′‐end Of Bacterial Rnassupporting

confidence: 79%

Section: Phosphorylation States Of the 5′‐end Of Bacterial Rnasmentioning

confidence: 99%

Noncanonical features and modifications on the 5′‐end of bacterial sRNAs and mRNAs

2018

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“…Bacteria use transcript degradation extensively as a strategy for gene regulation [27][28][29][30][31][32][37][38][39]. Degradation helps to tightly couple transcription and translation, such that protein abundances closely match those of transcripts and bacteria can more quickly respond to changes in their environment.…”

Section: Discussionmentioning

confidence: 99%

“…Pinetree employs a directional model of transcript degradation modeled after observations from E. coli [27][28][29]. In E. coli, degradation occurs either from the 5'-end of a newly-synthesized transcript or from the 5'-end of a transcript recently cleaved by an RNase III ribnuclease [30].…”

Section: Degradation Can Produce Gene Expression Patterns Similar To mentioning

confidence: 99%

Transcript degradation and codon usage regulate gene expression in a lytic phage

Jack

Boutz

Paff

et al. 2019

Preprint

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Many viral genomes are small, containing only single-or double-digit numbers of genes and relatively few regulatory elements. Yet viruses successfully execute complex regulatory programs as they take over their host cells. Here, we propose that some viruses regulate gene expression via a carefully balanced interplay between transcription, translation, and transcript degradation. As our model system, we employ bacteriophage T7, whose genome of approximately 60 genes is well annotated and for which there is a long history of computational models of gene regulation. We expand upon prior modeling work by implementing a stochastic gene expression simulator that tracks individual transcripts, polymerases, ribosomes, and RNases participating in the transcription, translation, and transcript-degradation processes occurring during a T7 infection. By combining this detailed mechanistic modeling of a phage infection with high throughput gene expression measurements of several strains of bacteriophage T7, evolved and engineered, we can show that both the dynamic interplay between transcription and transcript degradation, and between these two processes and translation, appear to be critical components of T7 gene regulation. Our results point to a generic gene regulation strategy that may have evolved in many other viruses. Further, our results suggest that detailed mechanistic modeling may uncover the biological mechanisms at work in both evolved and engineered virus variants.

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“…Thus, RNase E processing is significantly enhanced by the removal of the pyrophosphate from the 5′ terminal triphosphate of many primary transcripts. While conversion of the 5′ triphosphate to a 5′ monophosphate was believed to be catalyzed by the RNA pyrophosphohydrolase (RppH) encoded by rppH (13), a recent report suggests that an unidentified enzyme converts the triphosphate to a diphosphate, which is the substrate of choice for the RppH protein (14). Although RNase E prefers to bind to substrates containing a 5′ monophosphate, a number of experiments have demonstrated that it can also cleave both mRNAs and tRNAs using a direct entry mechanism (15–19).…”

Section: General Messenger Rna Decaymentioning

confidence: 99%

Enzymes Involved in Posttranscriptional RNA Metabolism in Gram-Negative Bacteria

Mohanty¹,

Kushner

2018

Microbiol Spectr

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Gene expression in Gram-negative bacteria is regulated at many levels, including transcription initiation, RNA processing, RNA/RNA interactions, mRNA decay, and translational controls involving enzymes that alter translational efficiency. In this chapter we discuss the various enzymes that control transcription, translation and RNA stability through RNA processing and degradation. RNA processing is essential to generate functional RNAs, while degradation helps control the steady-state level of each individual transcript. For example, all the pre-tRNAs are transcribed with extra nucleotides at both their 5′ and 3′ termini, which are subsequently processed to produce mature tRNAs that can be aminoacylated. Similarly, rRNAs that are transcribed as part of a 30S polycistronic transcript, are matured to individual 16S, 23S and 5S rRNAs. Decay of mRNAs plays a key role in gene regulation through controlling the steady-state level of each transcript, which is essential for maintaining appropriate protein levels. In addition, degradation of both translated and non-translated RNAs recycles nucleotides to facilitate new RNA synthesis. To carry out all these reactions Gram-negative bacteria employ a large number of endonucleases, exonucleases, RNA helicases, and poly(A) polymerase as well as proteins that regulate the catalytic activity of particular ribonucleases. Under certain stress conditions an additional group of specialized endonucleases facilitate the cell’s ability to adapt and survive. Many of the enzymes, such as RNase E, RNase III, polynucleotide phosphorylase, RNase R, and poly(A) polymerase I participate in multiple RNA processing and decay pathways.

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A Novel RNA Phosphorylation State Enables 5′ End-Dependent Degradation in Escherichia coli

Cited by 75 publications

References 52 publications

Noncanonical features and modifications on the 5′‐end of bacterial sRNAs and mRNAs

Noncanonical features and modifications on the 5′‐end of bacterial sRNAs and mRNAs

Transcript degradation and codon usage regulate gene expression in a lytic phage

Enzymes Involved in Posttranscriptional RNA Metabolism in Gram-Negative Bacteria

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