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RNase E: at the interface of bacterial RNA processing and decay

Key Points

  • RNase E is an essential endoribonuclease involved in most aspects of RNA processing and degradation in many bacteria. It is active as a tetramer within the context of a membrane-bound RNA degradosome complex, which contains other enzymes involved in RNA and cellular metabolism in addition to RNase E.

  • RNase E is a central player in both stable-RNA processing and mRNA decay. It initiates the processing of about two-thirds of all pre-tRNAs and the decay of most mRNAs. It also participates in the maturation of 16S and 5S rRNAs.

  • RNase E has two modes of substrate recognition. The first relies on the substrate containing a 5′ monophosphate terminus, which is recognized by the 5′ sensor (the phosphate-sensing pocket of the enzyme); binding of such RNAs results in strong enhancement in their rate of cleavage. Alternatively, RNase E can bind other RNA substrates directly, independent of their 5′ termini. In either case, the subsequent cleavage of susceptible single-stranded sites is hydrolytic.

  • RNase E is capable of autoregulation whereby the rne mRNA (encoding the Rne monomers that constitute the RNase E tetramer) serves as a sensor for total cellular RNase E activity and thus limits RNase E activity in response to the availability of substrates and changes in growth rate. RNase E-binding proteins might regulate RNase E recognition of, and affinity for, subsets of RNAs.

  • On the basis of recent observations, a new model for the spatial regulation of RNA metabolism in the bacterial cell is proposed: the localization of the RNA degradosome on the inner cytoplasmic membrane spatially separates transcription from RNA processing and decay. Moreover, this model posits that rRNA and tRNA precursors must cycle past the inner membrane before their maturation.

Abstract

RNase E is an essential endonuclease that is abundant in many bacteria and plays an important part in all aspects of RNA metabolism. It functions as part of a large macromolecular complex known as the RNA degradosome. Recent evidence suggests that this complex associates with the inner membrane of bacteria, an observation that challenges traditional models in which soluble RNases are proposed to randomly interact with RNAs in the cytosol. In this Review, I summarize the major roles of RNase E in RNA processing and decay and discuss the various mechanisms that regulate its activity. I also propose a new model to rationalize the mechanism of RNase E action in the context of its localization in the bacterial cell.

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Figure 1: The architecture of RNase E.
Figure 2: Pathways of mRNA decay in Escherichia coli.
Figure 3: The maturation of rRNA in Escherichia coli.
Figure 4: Model of RNA processing and decay on the inner membrane.

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Acknowledgements

Work from the Mackie laboratory has been supported by the Canadian Institutes for Health Research and their predecessor, the Medical Research Council of Canada. The author thanks G. H. Jones for helpful feedback and apologizes to the many authors whose work could not be cited directly owing to space constraints.

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Glossary

Scissile bond

In the context of this Review: in an RNA substrate, the particular phosphodiester linkage that is hydrolysed by RNase E.

RISC

(RNA-induced silencing complex). A eukaryotic complex that accepts one strand of the short (22–23 nucleotide) duplex RNAs created by Dicer-mediated cleavage of double-stranded RNA. Following loading into the RISC complex, which contains an enzyme of the Argonaute family, this single strand of the RNA duplex guides the RISC complex to complementary sequences in target mRNAs, which may be subsequently cleaved or translationally silenced.

Transition state

A transient molecular structure lying between the initial substrate and the final product; in this state, no covalent bonds have yet been broken. Enzymes typically lower the energy barrier to forming a transition state intermediate between substrate and product (or products).

K d

The concentration at which 50% of a complex dissociates into its component parts. This value is an inverse measure of the strength of the interaction: the smaller the value (expressed as a Molar concentration), the stronger the interaction between the components of the complex.

Surface plasmon resonance

A way of measuring the interaction of macromolecules at a surface through changes in the refractive index. Valence electrons of molecules at a metal–liquid interface oscillate in response to incident light. When one ligand is immobilized on a metal surface (for example, using a hexahistidine tag) and a second ligand is passed across the surface, the association and dissociation of the two ligands result in a change of refractive index, which can be measured.

Electrophoretic mobility shift assays

Assays that use an empirical method of visualizing the formation of nucleic acid–protein complexes by electrophoretic separation in 'native' conditions. The binding of a protein frequently reduces the rate of nucleic acid migration through a polyacrylamide or agarose gel. By varying the ratio of protein to RNA as a function of increasing protein concentration, the affinity of the protein for the nucleic acid ligand can be estimated (as a Kd value).

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Mackie, G. RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11, 45–57 (2013). https://doi.org/10.1038/nrmicro2930

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