The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal

@article{Deana2008TheBE,
  title={The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal},
  author={Atilio Deana and Helena {\vC}ele{\vs}nik and Joel G. Belasco},
  journal={Nature},
  year={2008},
  volume={451},
  pages={355-358}
}
The long-standing assumption that messenger RNA (mRNA) degradation in Escherichia coli begins with endonucleolytic cleavage has been challenged by the recent discovery that RNA decay can be triggered by a prior non-nucleolytic event that marks transcripts for rapid turnover: the rate-determining conversion of the 5′ terminus from a triphosphate to a monophosphate. This modification creates better substrates for the endonuclease RNase E, whose cleavage activity at internal sites is greatly… 
A Novel RNA Phosphorylation State Enables 5' End-Dependent Degradation in Escherichia coli.
TLDR
It is concluded that triphosphate-to-monophosphate conversion to induce 5' end-dependent RNA degradation is a two-step process in E. coli involving γ-phosphates removal by an unidentified enzyme to enable subsequent β-ph phosphate removal by RppH.
An RNA pyrophosphohydrolase triggers 5'-exonucleolytic degradation of mRNA in Bacillus subtilis.
TLDR
It is reported that the degradation of primary transcripts in B. subtilis can nevertheless be triggered by an analogous process to generate a short-lived, monophosphorylated intermediate.
Importance of a diphosphorylated intermediate for RppH-dependent RNA degradation
TLDR
It is determined that diphosphorylated mRNA decay intermediates are abundant in wild-type E. coli and that their fractional level increases to almost 100% for representative mRNAs in mutant cells lacking RppH.
Specificity of RppH-dependent RNA degradation in Bacillus subtilis
TLDR
It is reported that purified B. subtilis RppH requires at least two unpaired nucleotides at the 5′ end of its RNA substrates and prefers three or more, and a parallel pathway for 5′-end–dependent RNA degradation in that species appears to involve an alternative phosphate-removing enzyme that is relatively insensitive to sequence variation at the first three positions.
Influence of translation on RppH‐dependent mRNA degradation in Escherichia coli
TLDR
It is indicated that ribosome binding and translocation can have a major impact on 5′ end‐dependent mRNA degradation in E. coli and a possible sequence of events that follow pyrophosphate removal is suggested.
Structures of RNA Complexes with the Escherichia coli RNA Pyrophosphohydrolase RppH Unveil the Basis for Specific 5′-End-dependent mRNA Decay*
TLDR
These structures show distinct conformations of EcRppH·RNA complexes on the catalytic pathway and suggest a common catalytic mechanism for Nudix hydrolases, which have important implications for mRNA decay and the regulation of protein biosynthesis in bacteria.
Rapid cleavage of RNA by RNase E in the absence of 5′ monophosphate stimulation
TLDR
It is shown that RNase E can cleave certain RNAs rapidly without requiring a 5′‐monophosphorylated end, and the relative simplicity of the requirements identified here for direct entry suggests that this mode of cleavage could represent a major means by which mRNA degradation is initiated in E.’coli and other organisms that contain homologues ofRNase E.
5′ End-independent RNase J1 Endonuclease Cleavage of Bacillus subtilis Model RNA*
TLDR
In vivo and in vitro evidence is provided that RNase J1 accesses its internal target site on trp leader RNA in a 5′ end-independent manner, suggesting that lowering RNase Y concentration may affect RNA decay indirectly via an effect on RNaseJ1, which is thought to exist withRNase Y in a degradosome complex.
Multifaceted impact of a nucleoside monophosphate kinase on 5′-end-dependent mRNA degradation in bacteria
TLDR
The metabolic enzyme cytidylate kinase is identified as another protein that affects rates of 5-end-dependent mRNA degradation in E. coli by utilizing two distinct mechanisms to influence the 5′-terminal phosphorylation state of RNA.
Direct entry by RNase E is a major pathway for the degradation and processing of RNA in Escherichia coli
TLDR
It is shown that 5′-monophosphate-independent, ‘direct entry’ cleavage is a major pathway for degrading and processing RNA, and further evidence is presented that direct entry is facilitated by RNase E binding simultaneously to multiple unpaired regions.
...
1
2
3
4
5
...

References

SHOWING 1-10 OF 34 REFERENCES
Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal.
TLDR
The role of RNase E is redefined in RNA degradation and how unpaired 5'-terminal nucleotides can facilitate access to internal cleavage sites within primary transcripts is explained, revealing a striking parallel between the mechanisms of mRNA decay in prokaryotic and eukaryotic organisms.
Ribonuclease E is a 5′-end-dependent endonuclease
TLDR
Results show that RNase E has inherent vectorial properties, with its activity depending on the 5′ end of its substrates; this can account for the direction of mRNA decay in E. coli, the phenomenon of ‘all or none’ mRNA decay, and the stabilization provided by 5′ stem–loop structures.
Control of RNase E-mediated RNA degradation by 5′-terminal base pairing in E. coil
TLDR
It is reported here that RNase E has an unprecedented substrate specificity for an endoribonuclease, as it preferentially cleaves RNAs that have several unpaired nucleotides at the 5′ end, which may explain how determinants near the5′ end can control rates of mRNA decay in bacteria.
Regions of RNase E Important for 5′-End-Dependent RNA Cleavage and Autoregulated Synthesis
TLDR
Although it is dispensable for 5'-end-dependent RNA cleavage, the carboxy-terminal half of RNase E significantly enhances the ability of this ribonuclease to autoregulate its synthesis in E. coli.
Catalytic activation of multimeric RNase E and RNase G by 5'-monophosphorylated RNA.
  • Xunqing Jiang, J. Belasco
  • Biology, Medicine
    Proceedings of the National Academy of Sciences of the United States of America
  • 2004
TLDR
To investigate the mechanism by which 5'-terminal phosphorylation can influence distant cleavage events, fluorogenic RNA substrates are developed that allow the activity of RNase E and RNase G to be quantified much more accurately and easily than before.
Stabilization of Circular rpsT mRNA Demonstrates the 5′-End Dependence of RNase E Action in Vivo *
  • G. Mackie
  • Biology, Medicine
    The Journal of Biological Chemistry
  • 2000
TLDR
The results show unambiguously the importance of an accessible 5′-end in controlling mRNA stability in vivo and support a two-step (“looping”) model for RNase E action in which the first step is end recognition and the second is actual cleavage.
Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the product of the ams gene in vivo and in vitro
  • G. Mackie
  • Biology, Medicine
    Journal of bacteriology
  • 1991
TLDR
Taken together, the data show that the fractionated extract described here reproduces steps in the degradation of some mRNAs which occur in living cells.
Unpaired terminal nucleotides and 5' monophosphorylation govern 3' polyadenylation by Escherichia coli poly(A) polymerase I.
  • Y. Feng, S. Cohen
  • Biology, Medicine
    Proceedings of the National Academy of Sciences of the United States of America
  • 2000
TLDR
The results provide a mechanistic basis for the susceptibility of certain RNAs to 3' polyadenylation and suggest a model of "programmed" RNA decay in which endonucleolytically generated RNA fragments containing single-stranded monophosphorylated 5' termini are targeted for poly(A) addition and further degradation.
The CafA Protein Required for the 5′-Maturation of 16 S rRNA Is a 5′-End-dependent Ribonuclease That Has Context-dependent Broad Sequence Specificity*
TLDR
It is shown here that a highly purified preparation of CafA is sufficient in vitro for RNA cutting, and it is raised the possibility that the context dependence of cleavage by CafA may be due at least in part to the separation of a cleavable sequence from the 5′-end of an RNA.
Secondary structure of the mRNA for ribosomal protein S20. Implications for cleavage by ribonuclease E.
  • G. Mackie
  • Medicine, Biology
    The Journal of biological chemistry
  • 1992
TLDR
It is proposed that ribonuclease E is a single-strand-specific enzyme with few primary structural constraints but a preference for an AU dinucleotide 3' to the site of cleavage.
...
1
2
3
4
...