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RNase E and the High-Fidelity Orchestration of RNA Metabolism

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  • Authors: Katarzyna J. Bandyra1, Ben F. Luisi2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biochemistry, University of Cambridge, Cambridge CB2 1GA, United Kingdom; 2: Department of Biochemistry, University of Cambridge, Cambridge CB2 1GA, United Kingdom; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017
  • Received 01 November 2017 Accepted 22 January 2018 Published 20 April 2018
  • Ben F. Luisi, [email protected]
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  • Abstract:

    The bacterial endoribonuclease RNase E occupies a pivotal position in the control of gene expression, as its actions either commit transcripts to an irreversible fate of rapid destruction or unveil their hidden functions through specific processing. Moreover, the enzyme contributes to quality control of rRNAs. The activity of RNase E can be directed and modulated by signals provided through regulatory RNAs that guide the enzyme to specific transcripts that are to be silenced. Early in its evolutionary history, RNase E acquired a natively unfolded appendage that recruits accessory proteins and RNA. These accessory factors facilitate the activity of RNase E and include helicases that remodel RNA and RNA-protein complexes, and polynucleotide phosphorylase, a relative of the archaeal and eukaryotic exosomes. RNase E also associates with enzymes from central metabolism, such as enolase and aconitase. RNase E-based complexes are diverse in composition, but generally bear mechanistic parallels with eukaryotic machinery involved in RNA-induced gene regulation and transcript quality control. That these similar processes arose independently underscores the universality of RNA-based regulation in life. Here we provide a synopsis and perspective of the contributions made by RNase E to sustain robust gene regulation with speed and accuracy.

  • Citation: Bandyra K, Luisi B. 2018. RNase E and the High-Fidelity Orchestration of RNA Metabolism. Microbiol Spectrum 6(2):RWR-0008-2017. doi:10.1128/microbiolspec.RWR-0008-2017.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0008-2017
2018-04-20
2019-08-25

Abstract:

The bacterial endoribonuclease RNase E occupies a pivotal position in the control of gene expression, as its actions either commit transcripts to an irreversible fate of rapid destruction or unveil their hidden functions through specific processing. Moreover, the enzyme contributes to quality control of rRNAs. The activity of RNase E can be directed and modulated by signals provided through regulatory RNAs that guide the enzyme to specific transcripts that are to be silenced. Early in its evolutionary history, RNase E acquired a natively unfolded appendage that recruits accessory proteins and RNA. These accessory factors facilitate the activity of RNase E and include helicases that remodel RNA and RNA-protein complexes, and polynucleotide phosphorylase, a relative of the archaeal and eukaryotic exosomes. RNase E also associates with enzymes from central metabolism, such as enolase and aconitase. RNase E-based complexes are diverse in composition, but generally bear mechanistic parallels with eukaryotic machinery involved in RNA-induced gene regulation and transcript quality control. That these similar processes arose independently underscores the universality of RNA-based regulation in life. Here we provide a synopsis and perspective of the contributions made by RNase E to sustain robust gene regulation with speed and accuracy.

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Figures

Image of FIGURE 1
FIGURE 1

RNase-dependent processes in bacteria. RNases play crucial roles in efficient removal of defective or unnecessary RNAs, regulation of gene expression by sRNAs, and processing of various types of RNAs. (Left) RNA degradation is initiated by endoribonucleolytic cleavage, which can be preceded by pyrophosphate removal from the primary transcript. The majority of degradation initiation events are RNase E dependent. The initial cleavage generates monophosphorylated RNA fragments that can either boost subsequent RNase E cleavage or become substrates for cellular exoribonucleases. Fragments resulting from exoribonucleolytic degradation are further converted to nucleotides by oligoribonuclease. (Middle) When RNA degradation is mediated by sRNA, sRNA-chaperone complexes (such as sRNA-Hfq) can recognize a complementary sequence near the translation initiation region and prevent ribosome association on the transcript (left branch). Naked mRNA is rapidly scavenged by endo- and exoribonucleases. The sRNA-Hfq complex can also bind within the coding region of mRNA, recruiting RNase E and promoting transcript decay (right branch). (Right) In the case of substrates for processing, the order of RNA processing can be defined by the structure of precursors and the specificity of the RNases. The processing can form a cascade of interdependent events where some target sites are being revealed only upon specific initial cleavage. RNA, dark blue; endoribonucleases, purple; exoribonucleases, light blue; sRNA, red; ribosomes, gray ovals; Hfq, orange.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017
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Image of FIGURE 2
FIGURE 2

RNase E catalytic domain and a model of the organization of the RNA degradosome. (Top) RNase E is a tetramer (purple, with a single protomer highlighted in dark purple), and the quaternary organization is secured through zinc coordination (black spot) linking NTDs. The CTD is predicted to be predominantly unstructured and provides binding sites for the other degradosome components: RhlB (green), enolase (yellow), and PNPase (blue). The C terminus also harbors two RNA-binding sites (red) and a membrane anchor (dark gray). (Bottom) Structure of the RNase E catalytic domain, with the subdomains of one protomer color-coded. Close view of the phosphate binding pocket (left) and the active site (right), with the main amino acids of functional importance labeled ( 47 ).

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017
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Image of FIGURE 3
FIGURE 3

RNase E and interactions with RNA substrates. (A) RNase E activation by 5′-monophosphorylated substrate binding (5′P depicted as a yellow star). Only the principle dimer of the RNase E tetramer (purple) is shown for clarity. The S1 domain together with 5′ sensor (red bar) is capturing the substrate (dark blue) and aligning it in the active site by structural changes induced by RNA binding. (B) Substrate (dark blue) channeling by the ATP helicase (green) to the active site of PNPase (blue). Its action may thread substrate down the channel into the active site, as occurs for the exosome and the mitochondrial exoribonuclease-helicase complex of yeast. The helicase is also likely to provide the same threading function for RNase E (purple).

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017
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Image of FIGURE 4
FIGURE 4

Model of the degradosome interaction with polysomes and the cellular membrane. (A) Speculative model of degradosome interaction with the polysome. RNase E can gain access to translated transcripts (dark blue) upon sRNA action (top), when an sRNA (red) in complex with Hfq (orange) targets the translation initiation region (TIR, black) and by inhibiting assembly of ribosomes provides access for RNase E. The enzyme can also gain access to translated mRNA on its own (bottom). Adapted from reference 140 . (B) Association with the inner membrane (gray) is mediated by an amphipathic helix (dark gray) localized in the CTD of RNase E. RNase E, purple; RhlB, green; enolase, yellow; PNPase, blue.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017
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Tables

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TABLE 1

Components of the bacterial RNA degradosome and analogous or homologous assemblies from archaea and eukaryotes

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0008-2017

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