Crystal structure of <i>Escherichia coli</i> PNPase: Central channel residues are involved in processive RNA degradation

Shi, Zhonghao; Yang, Wei‐Zen; Lin‐Chao, Sue; Chak, Kin‐Fu; Yuan, Hanna S.

doi:10.1261/rna.1244308

Cited by 92 publications

(118 citation statements)

References 35 publications

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“…A conformational change in Rrp44 from the RNA-free to the RNA-bound state is stabilized when the RNA tail reaches Site2 (4). As the RNA substrate is shortened by the continuous degradation (5), the 5′ end of the RNA passes Site 1 and cannot hold Rrp44 in the RNA-bound state (6), thus resulting in the conformational recovery of the exosome for the next round of reaction (7). In the cartoon model, the exosome is divided into two parts, Exo9-Rrp44PIN (grey) and the RNase II-like domain (green).…”

Section: Discussionmentioning

confidence: 99%

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CryoEM structure of yeast cytoplasmic exosome complex

Liu

Niu

et al. 2016

Cell Res

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The eukaryotic multi-subunit RNA exosome complex plays crucial roles in 3′-to-5′ RNA processing and decay. Rrp6 and Ski7 are the major cofactors for the nuclear and cytoplasmic exosomes, respectively. In the cytoplasm, Ski7 helps the exosome to target mRNAs for degradation and turnover via a through-core pathway. However, the interaction between Ski7 and the exosome complex has remained unclear. The transaction of RNA substrates within the exosome is also elusive. In this work, we used single-particle cryo-electron microscopy to solve the structures of the Ski7-exosome complex in RNA-free and RNA-bound forms at resolutions of 4.2 Å and 5.8 Å, respectively. These structures reveal that the N-terminal domain of Ski7 adopts a structural arrangement and interacts with the exosome in a similar fashion to the C-terminal domain of nuclear Rrp6. Further structural analysis of exosomes with RNA substrates harboring 3′ overhangs of different length suggests a switch mechanism of RNA-induced exosome activation in the through-core pathway of RNA processing.

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Section: Discussionmentioning

confidence: 99%

“…The eukaryotic exosome complex shares a homologous 9-subunit core complex with the prokaryotic PNPase and the archaeal exosome complexes [6][7][8][9]. All have a barrel-shaped structure with a region at the top for RNA substrate recruitment and a central channel allowing single-stranded RNA substrate to access.…”

Section: Introductionmentioning

confidence: 99%

CryoEM structure of yeast cytoplasmic exosome complex

Liu

Niu

et al. 2016

Cell Res

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“…These differences probably reflect the long coevolution history of PNPase-RNase E interactions in different species. One remarkable feature for the PNPase binding sites identified in E. coli, C. crescentus, and Anabaena is that they all reside at the very C-terminal end of RNase E. Such an arrangement may save more space in RNase E for other components to be assembled into the complex using the noncatalytic domain as a scaffold, because PNPase as a homotrimer is relatively large in size (Shi et al 2008;Hardwick et al 2012).…”

Section: Discussionmentioning

confidence: 99%

RNase E forms a complex with polynucleotide phosphorylase in cyanobacteria via a cyanobacterial-specific nonapeptide in the noncatalytic region

Zhang

Deng

et al. 2014

RNA

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RNase E, a central component involved in bacterial RNA metabolism, usually has a highly conserved N-terminal catalytic domain but an extremely divergent C-terminal domain. While the C-terminal domain of RNase E in Escherichia coli recruits other components to form an RNA degradation complex, it is unknown if a similar function can be found for RNase E in other organisms due to the divergent feature of this domain. Here, we provide evidence showing that RNase E forms a complex with another essential ribonuclease-the polynucleotide phosphorylase (PNPase)-in cyanobacteria, a group of ecologically important and phylogenetically ancient organisms. Sequence alignment for all cyanobacterial RNase E proteins revealed several conserved and variable subregions in their noncatalytic domains. One such subregion, an extremely conserved nonapeptide (RRRRRRSSA) located near the very end of RNase E, serves as the PNPase recognition site in both the filamentous cyanobacterium Anabaena PCC7120 and the unicellular cyanobacterium Synechocystis PCC6803. These results indicate that RNase E and PNPase form a ribonuclease complex via a common mechanism in cyanobacteria. The PNPase-recognition motif in cyanobacterial RNase E is distinct from those previously identified in Proteobacteria, implying a mechanism of coevolution for PNPase and RNase E in different organisms.

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“…1). Interestingly, a third RNA-processing and -degradation complex known as polynucleotide phosphorylase (PNPase) forms a similar ring structure (Leszczyniecka et al, 2002;Littauer and Kornberg, 1957;Shi et al, 2008;Symmons et al, 2000). PNPase is present both in bacteria and in higher eukaryotes (Leszczyniecka et al, 2002), where it is located in the mitochondria (Piwowarski et al, 2003), suggesting that the eukaryotic enzyme might have been derived from bacteria through endosymbiosis.…”

Section: Structural Organisation Of the Exosome Corementioning

confidence: 99%

Origins and activities of the eukaryotic exosome

Lykke‐Andersen

Brodersen

Jensen

2009

Journal of Cell Science

157

131

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The exosome is a multi-subunit 3Ј-5Ј exonucleolytic complex that is conserved in structure and function in all eukaryotes studied to date. The complex is present in both the nucleus and cytoplasm, where it continuously works to ensure adequate quantities and quality of RNAs by facilitating normal RNA processing and turnover, as well as by participating in more complex RNA quality-control mechanisms. Recent progress in the field has convincingly shown that the nucleolytic activity of the exosome is maintained by only two exonuclease co-factors, one of which is also an endonuclease. The additional association of the exosome with RNA-helicase and poly(A) polymerase activities results in a flexible molecular machine that is capable of dealing with the multitude of cellular RNA substrates that are found in eukaryotic cells. Interestingly, the same basic set of enzymatic activities is found in prokaryotic cells, which might therefore illustrate the evolutionary origin of the eukaryotic system. In this Commentary, we compare the structural and functional characteristics of the eukaryotic and prokaryotic RNA-degradation systems, with an emphasis on some of the functional networks in which the RNA exosome participates in eukaryotes.Key words: Exosome function, Exosome structure, RNA exosome The existence of two similar ring-shaped RNA degradation complexes in bacteria (RNase PH and PNPase) suggests that one was derived from the other via gene duplication or lateral gene transfer. However, phylogenetic analysis shows that RNase PH is more closely related to the second catalytic domain of PNPase than the two domains of PNPase are to each other, suggesting that the proteins co-evolved from a common primordial single-domain enzyme (Leszczyniecka et al., 2004). That enzyme also evolved into two archaeal (Rrp41 and Rrp42) and six eukaryotic genes (Rrp41, Rrp42, Rrp45, Rrp46, Rrp43 and Mtr3). In fact, the eukaryotic genes can be organised into two groups based on their similarity to either archaeal Rrp41 (eukaryotic Rrp41, Rrp46 and Mtr3) or Rrp42 (eukaryotic Rrp42, Rrp43 and Rrp45) (Lorentzen et al., 2005). This indicates that the eukaryotic exosome evolved from a single RNase PH-type ancestor by several subsequent gene duplication events, the first of which produced Rrp41 and Rrp42, which later diversified into the six individual proteins. The finding that the cap proteins are present in both eukaryotes and archaea also indicates common ancestry. However, a strict requirement of the cap for stability of the exosome core seems to be a development that is specific to eukaryotes (Buttner et al., 2005;Liu et al., 2006;Lorentzen et al., 2005). The exosome core is catalytically inactive in yeast and humansThe homo-hexameric RNase PH has three phosphorolytic active sites on each side of the ring, whereas in PNPase, this is reduced to a single active site per subunit (three active sites per complex) (Ishii et al., 2003;Symmons et al., 2000) (Fig. 1). This is reminiscent of the archaeal exosome, where the Rrp41-Rrp42 heterodimers e...

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Crystal structure of Escherichia coli PNPase: Central channel residues are involved in processive RNA degradation

Cited by 92 publications

References 35 publications

CryoEM structure of yeast cytoplasmic exosome complex

CryoEM structure of yeast cytoplasmic exosome complex

RNase E forms a complex with polynucleotide phosphorylase in cyanobacteria via a cyanobacterial-specific nonapeptide in the noncatalytic region

Origins and activities of the eukaryotic exosome

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