Exonuclease requirements for mammalian ribosomal RNA biogenesis and surveillance

Pirouz, Mehdi; Munafò, Marzia; Ebrahimi, Aref G.; Choe, Joong-Seon; Gregory, Richard I.

doi:10.1038/s41594-019-0234-x

Cited by 28 publications

(26 citation statements)

References 56 publications

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“…Misprocessed rRNAs are usually detected and degraded by surveillance machinery during ribosome biogenesis [13,14,23,32]. Previously, our lab identified a class of risiRNAs that downregulate pre-rRNAs through the nuclear RNAi pathway to suppress the accumulation of erroneous rRNAs.…”

Section: Discussionmentioning

confidence: 99%

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CDE-1 suppresses the production of risiRNA by coupling polyuridylation and degradation of rRNA

et al. 2020

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Background: Modification of RNAs, particularly at the terminals, is critical for various essential cell processes; for example, uridylation is implicated in tumorigenesis, proliferation, stem cell maintenance, and immune defense against viruses and retrotransposons. Ribosomal RNAs can be regulated by antisense ribosomal siRNAs (risiRNAs), which downregulate pre-rRNAs through the nuclear RNAi pathway in Caenorhabditis elegans. However, the biogenesis and regulation of risiRNAs remain obscure. Previously, we showed that 26S rRNAs are uridylated at the 3′-ends by an unknown terminal polyuridylation polymerase before the rRNAs are degraded by a 3′ to 5′ exoribonuclease SUSI-1(ceDIS3L2). Results: Here, we found that CDE-1, one of the three C.elegans polyuridylation polymerases (PUPs), is specifically involved in suppressing risiRNA production. CDE-1 localizes to perinuclear granules in the germline and uridylates Argonaute-associated 22G-RNAs, 26S, and 5.8S rRNAs at the 3′-ends. Immunoprecipitation followed by mass spectrometry (IP-MS) revealed that CDE-1 interacts with SUSI-1(ceDIS3L2). Consistent with these results, both CDE-1 and SUSI-1(ceDIS3L2) are required for the inheritance of RNAi. Conclusions: This work identified a rRNA surveillance machinery of rRNAs that couples terminal polyuridylation and degradation.

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Section: Discussionmentioning

confidence: 99%

“…Aberrant RNAs are degraded by exosomes in a 3′-5′ exonucleolytic decay manner [16][17][18]. The exosome-independent exoribonuclease DIS3L2 plays a pivotal role in the 3′-5′ degradation of oligouridylated RNA fragments [19][20][21][22][23].…”

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confidence: 99%

CDE-1 suppresses the production of risiRNA by coupling polyuridylation and degradation of rRNA

et al. 2020

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“…Multiple surveillance machineries, including the nuclear-localized RNA exosome complex and the cytoplasmic exoribonuclease SUSI-1(ceDIS3L2), degrade defective rRNAs [3,22,42,43]. Surveillance machinery deficiencies result in the accumulation of erroneous rRNAs.…”

Section: Discussionmentioning

confidence: 99%

Co-surveillance of ribosomal RNA by the exosome complex and nucleolar RNAi inC. elegans

Liao

Chen

et al. 2020

Preprint

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Eukaryotic cells express a wide variety of endogenous small regulatory RNAs that function in the nucleus. We previously found that erroneous rRNAs induce the generation of antisense ribosomal siRNAs (risiRNAs) which silence the expression of rRNAs via the nuclear RNAi defective (Nrde) pathway. To further understand the biological roles and mechanisms of this class of small regulatory RNAs, we conducted forward genetic screening to identify factors involved in risiRNA generation in Caenorhabditis elegans. We found that risiRNAs accumulated in the RNA exosome mutants. risiRNAs directed a NRDE-dependent silencing of pre-rRNAs in the nucleolus. In the presence of risiRNA, NRDE-2 accumulated in the nucleolus and colocalized with RNA polymerase I. risiRNA inhibited the transcription elongation of RNA polymerase I by decreasing RNAP I occupancy downstream of the site of RNAi. Meanwhile, exosome mislocalized from the nucleolus to nucleoplasm in suppressor of siRNA (susi) mutants, in which erroneous rRNAs accumulated. These results establish a novel model of rRNA surveillance by combining ribonuclease-mediated RNA degradation with small RNA-directed nucleolar RNAi system.

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“…The newly generated 30S pre-rRNA is further processed directly to 21S pre-rRNA through cutting at the A0 and 1 sites, or via an intermediate form called 26S pre-rRNA, where the cleavage at these sites is uncoupled ( Figure 2 ) [ 96 , 98 , 99 , 100 ]. Intriguingly, a role for the exosome and DIS3L2/ERI1 in the 5.8S maturation steps via the formation of a cytoplasmic precursor, named 7SB, was recently demonstrated [ 101 ].…”

Section: Rrna Processing and Maturationmentioning

confidence: 99%

RNA Metabolism Guided by RNA Modifications: The Role of SMUG1 in rRNA Quality Control

et al. 2021

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RNA modifications are essential for proper RNA processing, quality control, and maturation steps. In the last decade, some eukaryotic DNA repair enzymes have been shown to have an ability to recognize and process modified RNA substrates and thereby contribute to RNA surveillance. Single-strand-selective monofunctional uracil-DNA glycosylase 1 (SMUG1) is a base excision repair enzyme that not only recognizes and removes uracil and oxidized pyrimidines from DNA but is also able to process modified RNA substrates. SMUG1 interacts with the pseudouridine synthase dyskerin (DKC1), an enzyme essential for the correct assembly of small nucleolar ribonucleoproteins (snRNPs) and ribosomal RNA (rRNA) processing. Here, we review rRNA modifications and RNA quality control mechanisms in general and discuss the specific function of SMUG1 in rRNA metabolism. Cells lacking SMUG1 have elevated levels of immature rRNA molecules and accumulation of 5-hydroxymethyluridine (5hmU) in mature rRNA. SMUG1 may be required for post-transcriptional regulation and quality control of rRNAs, partly by regulating rRNA and stability.

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Exonuclease requirements for mammalian ribosomal RNA biogenesis and surveillance

Cited by 28 publications

References 56 publications

CDE-1 suppresses the production of risiRNA by coupling polyuridylation and degradation of rRNA

CDE-1 suppresses the production of risiRNA by coupling polyuridylation and degradation of rRNA

Co-surveillance of ribosomal RNA by the exosome complex and nucleolar RNAi inC. elegans

RNA Metabolism Guided by RNA Modifications: The Role of SMUG1 in rRNA Quality Control

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