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Chapter 1 : RNase E and the High-Fidelity Orchestration of RNA Metabolism

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Abstract:

It may seem surprising that in almost all known life-forms, information-encoding transcripts are actively annihilated. Although at first glance this seems to be a potential waste of resources and loss of information, the anticipated advantages of restricting transcript lifetimes include fast response rates and a capacity to rapidly redirect gene expression pathways. In this way, destroying individual transcripts in a modulated manner might effectively enhance the collective information capacity of the living system. has proven to be a useful model system to study such processes, and nearly 45 years ago, a hypothetical endoribonuclease was proposed by Apirion as the key missing factor that might account for the observed degradation patterns of mRNA in that bacterium. At the time this hypothesis was formulated, transcript decay in was best described as a series of endonucleolytic cleavages and subsequent fragment scavenging by 3′ exonucleases ( ). A few years later, Apirion and colleagues reported the discovery of the endoribonuclease RNase E and showed it to be involved in processing of rRNA precursors ( ), and the enzyme was subsequently discovered to also cleave an mRNA from T4 phage into a stable intermediate ( ). Thus, RNase E seemed to be an ideal candidate for the proposed endonuclease factor to initiate RNA decay in bacteria. What made these findings surprising was that it had previously been thought that RNases might be specialized, with one set presumed responsible for mRNA decay and another set dedicated to stable RNA processing, whereas RNase E could perform both of these distinct tasks ( ). This broad functionality has been found to be a recurrent feature of other RNases in and evolutionarily distant bacteria ( ).

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0008-2017
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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.

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. 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 ( ).

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0008-2017
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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).

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0008-2017
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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 . (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.

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. 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

Citation: Bandyra K, Luisi B. 2019. RNase E and the High-Fidelity Orchestration of RNA Metabolism, p 3-18. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0008-2017

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